Skip to main content
Erschienen in: Clinical Reviews in Bone and Mineral Metabolism 2/2018

24.04.2018 | Review Paper

Skeletal Effects of Thyroid Hormones

verfasst von: Bence Bakos, Istvan Takacs, Paula H. Stern, Peter Lakatos

Erschienen in: Clinical & Translational Metabolism | Ausgabe 2/2018

Einloggen, um Zugang zu erhalten

Abstract

The importance of functional thyroid abnormalities can hardly be overstated as they affect over 5% of the population. Thyroid hormones exert a multitude of effects on the metabolism of both the developing and the adult skeleton. It is thus unsurprising that changes in thyroid function can have a variety of often severe skeletal consequences. In recent years, numerous advances were made in the understanding of this domain. These include for instance the mapping of different pathways mediating genomic and nongenomic actions of thyroid hormones in osteoblasts and osteoclasts, or the investigation of the direct role of thyrotropin in skeletal remodeling. New disease states such as RTHα were recently recognized, and the clinical significance of subclinical thyroid dysfunctions in bone pathology is also better understood. In this current paper, we review the influence of thyroid hormones and different forms of thyroid disorders on bone metabolism with a special focus on practical clinical considerations.
Literatur
1.
Zurück zum Zitat Germain P, Staels B, Dacquet C, Spedding M, Laudet V. Overview of nomenclature of nuclear receptors. Pharmacol Rev. 2006;58(4):685–704.PubMedCrossRef Germain P, Staels B, Dacquet C, Spedding M, Laudet V. Overview of nomenclature of nuclear receptors. Pharmacol Rev. 2006;58(4):685–704.PubMedCrossRef
2.
Zurück zum Zitat Williams GR, Bland R, Sheppard MC. Characterization of thyroid hormone (T3) receptors in three osteosarcoma cell lines of distinct osteoblast phenotype: interactions among T3, vitamin D3, and retinoid signaling. Endocrinology. 1994;135(6):2375–85.PubMedCrossRef Williams GR, Bland R, Sheppard MC. Characterization of thyroid hormone (T3) receptors in three osteosarcoma cell lines of distinct osteoblast phenotype: interactions among T3, vitamin D3, and retinoid signaling. Endocrinology. 1994;135(6):2375–85.PubMedCrossRef
3.
Zurück zum Zitat Williams GR, Bland R, Sheppard MC. Retinoids modify regulation of endogenous gene expression by vitamin D3 and thyroid hormone in three osteosarcoma cell lines. Endocrinology. 1995;136(10):4304–14.PubMedCrossRef Williams GR, Bland R, Sheppard MC. Retinoids modify regulation of endogenous gene expression by vitamin D3 and thyroid hormone in three osteosarcoma cell lines. Endocrinology. 1995;136(10):4304–14.PubMedCrossRef
4.
Zurück zum Zitat Chassande O, Fraichard A, Gauthier K, Flamant F, Legrand C, Savatier P, et al. Identification of transcripts initiated from an internal promoter in the c-erbA alpha locus that encode inhibitors of retinoic acid receptor-alpha and triiodothyronine receptor activities. Mol Endocrinol. 1997;11(9):1278–90.PubMed Chassande O, Fraichard A, Gauthier K, Flamant F, Legrand C, Savatier P, et al. Identification of transcripts initiated from an internal promoter in the c-erbA alpha locus that encode inhibitors of retinoic acid receptor-alpha and triiodothyronine receptor activities. Mol Endocrinol. 1997;11(9):1278–90.PubMed
5.
Zurück zum Zitat Izumo S, Mahdavi V. Thyroid hormone receptor alpha isoforms generated by alternative splicing differentially activate myosin HC gene transcription. Nature. 1988;334(6182):539–42.PubMedCrossRef Izumo S, Mahdavi V. Thyroid hormone receptor alpha isoforms generated by alternative splicing differentially activate myosin HC gene transcription. Nature. 1988;334(6182):539–42.PubMedCrossRef
6.
Zurück zum Zitat Plateroti M, Gauthier K, Domon-Dell C, Freund JN, Samarut J, Chassande O. Functional interference between thyroid hormone receptor alpha (TRalpha) and natural truncated TRDeltaalpha isoforms in the control of intestine development. Mol Cell Biol. 2001;21(14):4761–72.PubMedPubMedCentralCrossRef Plateroti M, Gauthier K, Domon-Dell C, Freund JN, Samarut J, Chassande O. Functional interference between thyroid hormone receptor alpha (TRalpha) and natural truncated TRDeltaalpha isoforms in the control of intestine development. Mol Cell Biol. 2001;21(14):4761–72.PubMedPubMedCentralCrossRef
8.
Zurück zum Zitat Allain TJ, Yen PM, Flanagan AM, McGregor AM. The isoform-specific expression of the tri-iodothyronine receptor in osteoblasts and osteoclasts. Eur J Clin Investig. 1996;26(5):418–25.CrossRef Allain TJ, Yen PM, Flanagan AM, McGregor AM. The isoform-specific expression of the tri-iodothyronine receptor in osteoblasts and osteoclasts. Eur J Clin Investig. 1996;26(5):418–25.CrossRef
9.
Zurück zum Zitat Abu EO, Bord S, Horner A, Chatterjee VK, Compston JE. The expression of thyroid hormone receptors in human bone. Bone. 1997;21(2):137–42.PubMedCrossRef Abu EO, Bord S, Horner A, Chatterjee VK, Compston JE. The expression of thyroid hormone receptors in human bone. Bone. 1997;21(2):137–42.PubMedCrossRef
10.
Zurück zum Zitat Milne M, Kang MI, Cardona G, Quail JM, Braverman LE, Chin WW, et al. Expression of multiple thyroid hormone receptor isoforms in rat femoral and vertebral bone and in bone marrow osteogenic cultures. J Cell Biochem. 1999;74(4):684–93.PubMedCrossRef Milne M, Kang MI, Cardona G, Quail JM, Braverman LE, Chin WW, et al. Expression of multiple thyroid hormone receptor isoforms in rat femoral and vertebral bone and in bone marrow osteogenic cultures. J Cell Biochem. 1999;74(4):684–93.PubMedCrossRef
11.
Zurück zum Zitat O'Shea PJ, Harvey CB, Suzuki H, Kaneshige M, Kaneshige K, Cheng SY, et al. A thyrotoxic skeletal phenotype of advanced bone formation in mice with resistance to thyroid hormone. Mol Endocrinol. 2003;17(7):1410–24.PubMedCrossRef O'Shea PJ, Harvey CB, Suzuki H, Kaneshige M, Kaneshige K, Cheng SY, et al. A thyrotoxic skeletal phenotype of advanced bone formation in mice with resistance to thyroid hormone. Mol Endocrinol. 2003;17(7):1410–24.PubMedCrossRef
12.
Zurück zum Zitat Monfoulet LE, Rabier B, Dacquin R, Anginot A, Photsavang J, Jurdic P, et al. Thyroid hormone receptor β mediates thyroid hormone effects on bone remodeling and bone mass. J Bone Miner Res. 2011;26(9):2036–44.PubMedCrossRef Monfoulet LE, Rabier B, Dacquin R, Anginot A, Photsavang J, Jurdic P, et al. Thyroid hormone receptor β mediates thyroid hormone effects on bone remodeling and bone mass. J Bone Miner Res. 2011;26(9):2036–44.PubMedCrossRef
13.
14.
Zurück zum Zitat Burch WM, Lebovitz HE. Triiodothyronine stimulation of in vitro growth and maturation of embryonic chick cartilage. Endocrinology. 1982;111(2):462–8.PubMedCrossRef Burch WM, Lebovitz HE. Triiodothyronine stimulation of in vitro growth and maturation of embryonic chick cartilage. Endocrinology. 1982;111(2):462–8.PubMedCrossRef
15.
Zurück zum Zitat Böhme K, Conscience-Egli M, Tschan T, Winterhalter KH, Bruckner P. Induction of proliferation or hypertrophy of chondrocytes in serum-free culture: the role of insulin-like growth factor-I, insulin, or thyroxine. J Cell Biol. 1992;116(4):1035–42.PubMedCrossRef Böhme K, Conscience-Egli M, Tschan T, Winterhalter KH, Bruckner P. Induction of proliferation or hypertrophy of chondrocytes in serum-free culture: the role of insulin-like growth factor-I, insulin, or thyroxine. J Cell Biol. 1992;116(4):1035–42.PubMedCrossRef
16.
Zurück zum Zitat Quarto R, Campanile G, Cancedda R, Dozin B. Thyroid hormone, insulin, and glucocorticoids are sufficient to support chondrocyte differentiation to hypertrophy: a serum-free analysis. J Cell Biol. 1992;119(4):989–95.PubMedCrossRef Quarto R, Campanile G, Cancedda R, Dozin B. Thyroid hormone, insulin, and glucocorticoids are sufficient to support chondrocyte differentiation to hypertrophy: a serum-free analysis. J Cell Biol. 1992;119(4):989–95.PubMedCrossRef
17.
Zurück zum Zitat Ballock RT, Reddi AH. Thyroxine is the serum factor that regulates morphogenesis of columnar cartilage from isolated chondrocytes in chemically defined medium. J Cell Biol. 1994;126(5):1311–8.PubMedCrossRef Ballock RT, Reddi AH. Thyroxine is the serum factor that regulates morphogenesis of columnar cartilage from isolated chondrocytes in chemically defined medium. J Cell Biol. 1994;126(5):1311–8.PubMedCrossRef
18.
Zurück zum Zitat Alini M, Kofsky Y, Wu W, Pidoux I, Poole AR. In serum-free culture thyroid hormones can induce full expression of chondrocyte hypertrophy leading to matrix calcification. J Bone Miner Res. 1996;11(1):105–13.PubMedCrossRef Alini M, Kofsky Y, Wu W, Pidoux I, Poole AR. In serum-free culture thyroid hormones can induce full expression of chondrocyte hypertrophy leading to matrix calcification. J Bone Miner Res. 1996;11(1):105–13.PubMedCrossRef
19.
Zurück zum Zitat Ishikawa Y, Genge BR, Wuthier RE, Wu LN. Thyroid hormone inhibits growth and stimulates terminal differentiation of epiphyseal growth plate chondrocytes. J Bone Miner Res. 1998;13(9):1398–411.PubMedCrossRef Ishikawa Y, Genge BR, Wuthier RE, Wu LN. Thyroid hormone inhibits growth and stimulates terminal differentiation of epiphyseal growth plate chondrocytes. J Bone Miner Res. 1998;13(9):1398–411.PubMedCrossRef
20.
Zurück zum Zitat Rosenthal AK, Henry LA. Thyroid hormones induce features of the hypertrophic phenotype and stimulate correlates of CPPD crystal formation in articular chondrocytes. J Rheumatol. 1999;26(2):395–401.PubMed Rosenthal AK, Henry LA. Thyroid hormones induce features of the hypertrophic phenotype and stimulate correlates of CPPD crystal formation in articular chondrocytes. J Rheumatol. 1999;26(2):395–401.PubMed
21.
Zurück zum Zitat Miura M, Tanaka K, Komatsu Y, Suda M, Yasoda A, Sakuma Y, et al. Thyroid hormones promote chondrocyte differentiation in mouse ATDC5 cells and stimulate endochondral ossification in fetal mouse tibias through iodothyronine deiodinases in the growth plate. J Bone Miner Res. 2002;17(3):443–54.PubMedCrossRef Miura M, Tanaka K, Komatsu Y, Suda M, Yasoda A, Sakuma Y, et al. Thyroid hormones promote chondrocyte differentiation in mouse ATDC5 cells and stimulate endochondral ossification in fetal mouse tibias through iodothyronine deiodinases in the growth plate. J Bone Miner Res. 2002;17(3):443–54.PubMedCrossRef
22.
Zurück zum Zitat Gouveia CHA, Miranda-Rodrigues M, Martins GM, Neofiti-Papi B. Thyroid hormone and skeletal development. Vitam Horm. 2018;106:383–472.PubMedCrossRef Gouveia CHA, Miranda-Rodrigues M, Martins GM, Neofiti-Papi B. Thyroid hormone and skeletal development. Vitam Horm. 2018;106:383–472.PubMedCrossRef
23.
Zurück zum Zitat A M, Chowdhury K, Gruss P. Follicular cells of the thyroid gland require Pax8 gene function. Nat Genet. 1998;19(1):87–90.CrossRef A M, Chowdhury K, Gruss P. Follicular cells of the thyroid gland require Pax8 gene function. Nat Genet. 1998;19(1):87–90.CrossRef
24.
Zurück zum Zitat Flamant F, Poguet AL, Plateroti M, Chassande O, Gauthier K, Streichenberger N, et al. Congenital hypothyroid Pax8(−/−) mutant mice can be rescued by inactivating the TRalpha gene. Mol Endocrinol. 2002;16(1):24–32.PubMed Flamant F, Poguet AL, Plateroti M, Chassande O, Gauthier K, Streichenberger N, et al. Congenital hypothyroid Pax8(−/−) mutant mice can be rescued by inactivating the TRalpha gene. Mol Endocrinol. 2002;16(1):24–32.PubMed
25.
Zurück zum Zitat Friedrichsen S, Christ S, Heuer H, Schäfer MK, Mansouri A, Bauer K, et al. Regulation of iodothyronine deiodinases in the Pax8−/− mouse model of congenital hypothyroidism. Endocrinology. 2003;144(3):777–84.PubMedCrossRef Friedrichsen S, Christ S, Heuer H, Schäfer MK, Mansouri A, Bauer K, et al. Regulation of iodothyronine deiodinases in the Pax8−/− mouse model of congenital hypothyroidism. Endocrinology. 2003;144(3):777–84.PubMedCrossRef
26.
Zurück zum Zitat Bassett JH, Bone WGR. Critical role of the hypothalamic-pituitary-thyroid axis in. Bone. 2008;43(3):418–26.PubMedCrossRef Bassett JH, Bone WGR. Critical role of the hypothalamic-pituitary-thyroid axis in. Bone. 2008;43(3):418–26.PubMedCrossRef
27.
Zurück zum Zitat Beamer WG, Cresswell LA. Defective thyroid ontogenesis in fetal hypothyroid (hyt/hyt) mice. Anat Rec. 1982;202(3):387–93.PubMedCrossRef Beamer WG, Cresswell LA. Defective thyroid ontogenesis in fetal hypothyroid (hyt/hyt) mice. Anat Rec. 1982;202(3):387–93.PubMedCrossRef
28.
Zurück zum Zitat Abe E, Marians RC, Yu W, Wu XB, Ando T, Li Y, et al. TSH is a negative regulator of skeletal remodeling. Cell. 2003;115(2):151–62.PubMedCrossRef Abe E, Marians RC, Yu W, Wu XB, Ando T, Li Y, et al. TSH is a negative regulator of skeletal remodeling. Cell. 2003;115(2):151–62.PubMedCrossRef
29.
Zurück zum Zitat Gu WX, Du GG, Kopp P, Rentoumis A, Albanese C, Kohn LD, et al. The thyrotropin (TSH) receptor transmembrane domain mutation (Pro556-Leu) in the hypothyroid hyt/hyt mouse results in plasma membrane targeting but defective TSH binding. Endocrinology. 1995;136(7):3146–53.PubMedCrossRef Gu WX, Du GG, Kopp P, Rentoumis A, Albanese C, Kohn LD, et al. The thyrotropin (TSH) receptor transmembrane domain mutation (Pro556-Leu) in the hypothyroid hyt/hyt mouse results in plasma membrane targeting but defective TSH binding. Endocrinology. 1995;136(7):3146–53.PubMedCrossRef
30.
Zurück zum Zitat Baliram R, Sun L, Cao J, Li J, Latif R, Huber AK, et al. Hyperthyroid-associated osteoporosis is exacerbated by the loss of TSH signaling. J Clin Invest. 2012;122(10):3737–41.PubMedPubMedCentralCrossRef Baliram R, Sun L, Cao J, Li J, Latif R, Huber AK, et al. Hyperthyroid-associated osteoporosis is exacerbated by the loss of TSH signaling. J Clin Invest. 2012;122(10):3737–41.PubMedPubMedCentralCrossRef
31.
Zurück zum Zitat Sun L, Zhu LL, Lu P, Yuen T, Li J, Ma R, et al. Genetic confirmation for a central role for TNFα in the direct action of thyroid stimulating hormone on the skeleton. Proc Natl Acad Sci U S A. 2013;110(24):9891–6.PubMedPubMedCentralCrossRef Sun L, Zhu LL, Lu P, Yuen T, Li J, Ma R, et al. Genetic confirmation for a central role for TNFα in the direct action of thyroid stimulating hormone on the skeleton. Proc Natl Acad Sci U S A. 2013;110(24):9891–6.PubMedPubMedCentralCrossRef
32.
Zurück zum Zitat Fraichard A, Chassande O, Plateroti M, Roux JP, Trouillas J, Dehay C, et al. The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J. 1997;16(14):4412–20.PubMedPubMedCentralCrossRef Fraichard A, Chassande O, Plateroti M, Roux JP, Trouillas J, Dehay C, et al. The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J. 1997;16(14):4412–20.PubMedPubMedCentralCrossRef
33.
Zurück zum Zitat Gauthier K, Chassande O, Plateroti M, Roux JP, Legrand C, Pain B, et al. Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. EMBO J. 1999;18(3):623–31.PubMedPubMedCentralCrossRef Gauthier K, Chassande O, Plateroti M, Roux JP, Legrand C, Pain B, et al. Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. EMBO J. 1999;18(3):623–31.PubMedPubMedCentralCrossRef
34.
Zurück zum Zitat Gauthier K, Plateroti M, Harvey CB, Williams GR, Weiss RE, Refetoff S, et al. Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus. Mol Cell Biol. 2001;21(14):4748–60.PubMedPubMedCentralCrossRef Gauthier K, Plateroti M, Harvey CB, Williams GR, Weiss RE, Refetoff S, et al. Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus. Mol Cell Biol. 2001;21(14):4748–60.PubMedPubMedCentralCrossRef
35.
Zurück zum Zitat Bassett JH, Swinhoe R, Chassande O, Samarut J, Williams GR. Thyroid hormone regulates heparan sulfate proteoglycan expression in the growth plate. Endocrinology. 2006;147(1):295–305.PubMedCrossRef Bassett JH, Swinhoe R, Chassande O, Samarut J, Williams GR. Thyroid hormone regulates heparan sulfate proteoglycan expression in the growth plate. Endocrinology. 2006;147(1):295–305.PubMedCrossRef
36.
Zurück zum Zitat Ernst M, Froesch ER. Triiodothyronine stimulates proliferation of osteoblast-like cells in serum-free culture. FEBS Lett. 1987;220(1):163–6.PubMedCrossRef Ernst M, Froesch ER. Triiodothyronine stimulates proliferation of osteoblast-like cells in serum-free culture. FEBS Lett. 1987;220(1):163–6.PubMedCrossRef
37.
Zurück zum Zitat LeBron BA, Pekary AE, Mirell C, Hahn TJ, Hershman JM. Thyroid hormone 5′-deiodinase activity, nuclear binding, and effects on mitogenesis in UMR-106 osteoblastic osteosarcoma cells. J Bone Miner Res. 1989;4(2):173–8.PubMedCrossRef LeBron BA, Pekary AE, Mirell C, Hahn TJ, Hershman JM. Thyroid hormone 5′-deiodinase activity, nuclear binding, and effects on mitogenesis in UMR-106 osteoblastic osteosarcoma cells. J Bone Miner Res. 1989;4(2):173–8.PubMedCrossRef
38.
Zurück zum Zitat Kassem M, Mosekilde L, Eriksen EF. Effects of triiodothyronine on DNA synthesis and differentiation markers of normal human osteoblast-like cells in vitro. Biochem Mol Biol Int. 1993;30(4):779–88.PubMed Kassem M, Mosekilde L, Eriksen EF. Effects of triiodothyronine on DNA synthesis and differentiation markers of normal human osteoblast-like cells in vitro. Biochem Mol Biol Int. 1993;30(4):779–88.PubMed
39.
Zurück zum Zitat Luegmayr E, Varga F, Frank T, Roschger P, Klaushofer K. Effects of triiodothyronine on morphology, growth behavior, and the actin cytoskeleton in mouse osteoblastic cells (MC3T3-E1). Bone. 1996;18(6):591–9.PubMedCrossRef Luegmayr E, Varga F, Frank T, Roschger P, Klaushofer K. Effects of triiodothyronine on morphology, growth behavior, and the actin cytoskeleton in mouse osteoblastic cells (MC3T3-E1). Bone. 1996;18(6):591–9.PubMedCrossRef
40.
Zurück zum Zitat Kasono K, Sato K, Han DC, Fujii Y, Tsushima T, Shizume K. Stimulation of alkaline phosphatase activity by thyroid hormone in mouse osteoblast-like cells (MC3T3-E1): a possible mechanism of hyperalkaline phosphatasia in hyperthyroidism. Bone Miner. 1988;4(4):355–63.PubMed Kasono K, Sato K, Han DC, Fujii Y, Tsushima T, Shizume K. Stimulation of alkaline phosphatase activity by thyroid hormone in mouse osteoblast-like cells (MC3T3-E1): a possible mechanism of hyperalkaline phosphatasia in hyperthyroidism. Bone Miner. 1988;4(4):355–63.PubMed
41.
Zurück zum Zitat Sato K, Han DC, Fujii Y, Tsushima T, Shizume K. Thyroid hormone stimulates alkaline phosphatase activity in cultured rat osteoblastic cells (ROS 17/2.8) through 3,5,3′-triiodo-L-thyronine nuclear receptors. Endocrinology. 1987;120(5):1873–81.PubMedCrossRef Sato K, Han DC, Fujii Y, Tsushima T, Shizume K. Thyroid hormone stimulates alkaline phosphatase activity in cultured rat osteoblastic cells (ROS 17/2.8) through 3,5,3′-triiodo-L-thyronine nuclear receptors. Endocrinology. 1987;120(5):1873–81.PubMedCrossRef
42.
Zurück zum Zitat Kawaguchi H, Pilbeam CC, Raisz LG. Anabolic effects of 3,3′,5-triiodothyronine and triiodothyroacetic acid in cultured neonatal mouse parietal bones. Endocrinology. 1994;135(3):971–6.PubMedCrossRef Kawaguchi H, Pilbeam CC, Raisz LG. Anabolic effects of 3,3′,5-triiodothyronine and triiodothyroacetic acid in cultured neonatal mouse parietal bones. Endocrinology. 1994;135(3):971–6.PubMedCrossRef
43.
Zurück zum Zitat Banovac K, Koren E. Triiodothyronine stimulates the release of membrane-bound alkaline phosphatase in osteoblastic cells. Calcif Tissue Int. 2000;67(6):460–5.PubMedCrossRef Banovac K, Koren E. Triiodothyronine stimulates the release of membrane-bound alkaline phosphatase in osteoblastic cells. Calcif Tissue Int. 2000;67(6):460–5.PubMedCrossRef
44.
Zurück zum Zitat Varga F, Spitzer S, Rumpler M, Klaushofer K. 1,25-Dihydroxyvitamin D3 inhibits thyroid hormone-induced osteocalcin expression in mouse osteoblast-like cells via a thyroid hormone response element. J Mol Endocrinol. 2003;30(1):49–57.PubMedCrossRef Varga F, Spitzer S, Rumpler M, Klaushofer K. 1,25-Dihydroxyvitamin D3 inhibits thyroid hormone-induced osteocalcin expression in mouse osteoblast-like cells via a thyroid hormone response element. J Mol Endocrinol. 2003;30(1):49–57.PubMedCrossRef
45.
Zurück zum Zitat Varga F, Spitzer S, Klaushofer K. Triiodothyronine (T3) and 1,25-dihydroxyvitamin D3 (1,25D3) inversely regulate OPG gene expression in dependence of the osteoblastic phenotype. Calcif Tissue Int. 2004;74(4):382–7.PubMedCrossRef Varga F, Spitzer S, Klaushofer K. Triiodothyronine (T3) and 1,25-dihydroxyvitamin D3 (1,25D3) inversely regulate OPG gene expression in dependence of the osteoblastic phenotype. Calcif Tissue Int. 2004;74(4):382–7.PubMedCrossRef
46.
Zurück zum Zitat Varga F, Rumpler M, Zoehrer R, Turecek C, Spitzer S, Thaler R, et al. T3 affects expression of collagen I and collagen cross-linking in bone cell cultures. Biochem Biophys Res Commun. 2010;402(2):180–5.PubMedPubMedCentralCrossRef Varga F, Rumpler M, Zoehrer R, Turecek C, Spitzer S, Thaler R, et al. T3 affects expression of collagen I and collagen cross-linking in bone cell cultures. Biochem Biophys Res Commun. 2010;402(2):180–5.PubMedPubMedCentralCrossRef
47.
Zurück zum Zitat Luegmayr E, Glantschnig H, Varga F, Klaushofer K. The organization of adherens junctions in mouse osteoblast-like cells (MC3T3-E1) and their modulation by triiodothyronine and 1,25-dihydroxyvitamin D3. Histochem Cell Biol. 2000;113(6):467–78.PubMed Luegmayr E, Glantschnig H, Varga F, Klaushofer K. The organization of adherens junctions in mouse osteoblast-like cells (MC3T3-E1) and their modulation by triiodothyronine and 1,25-dihydroxyvitamin D3. Histochem Cell Biol. 2000;113(6):467–78.PubMed
48.
Zurück zum Zitat Fratzl-Zelman N, Hörandner H, Luegmayr E, Varga F, Ellinger A, Erlee MP, et al. Effects of triiodothyronine on the morphology of cells and matrix, the localization of alkaline phosphatase, and the frequency of apoptosis in long-term cultures of MC3T3-E1 cells. Bone. 1997;20(3):225–36.PubMedCrossRef Fratzl-Zelman N, Hörandner H, Luegmayr E, Varga F, Ellinger A, Erlee MP, et al. Effects of triiodothyronine on the morphology of cells and matrix, the localization of alkaline phosphatase, and the frequency of apoptosis in long-term cultures of MC3T3-E1 cells. Bone. 1997;20(3):225–36.PubMedCrossRef
49.
Zurück zum Zitat Schmid C, Schläpfer I, Futo E, Waldvogel M, Schwander J, Zapf J, et al. Triiodothyronine (T3) stimulates insulin-like growth factor (IGF)-1 and IGF binding protein (IGFBP)-2 production by rat osteoblasts in vitro. Acta Endocrinol. 1992;126(5):467–73.PubMedCrossRef Schmid C, Schläpfer I, Futo E, Waldvogel M, Schwander J, Zapf J, et al. Triiodothyronine (T3) stimulates insulin-like growth factor (IGF)-1 and IGF binding protein (IGFBP)-2 production by rat osteoblasts in vitro. Acta Endocrinol. 1992;126(5):467–73.PubMedCrossRef
50.
Zurück zum Zitat Varga F, Rumpler M, Klaushofer K. Thyroid hormones increase insulin-like growth factor mRNA levels in the clonal osteoblastic cell line MC3T3-E1. FEBS Lett. 1994;345(1):67–70.PubMedCrossRef Varga F, Rumpler M, Klaushofer K. Thyroid hormones increase insulin-like growth factor mRNA levels in the clonal osteoblastic cell line MC3T3-E1. FEBS Lett. 1994;345(1):67–70.PubMedCrossRef
51.
Zurück zum Zitat Glantschnig H, Varga F, Klaushofer K. Thyroid hormone and retinoic acid induce the synthesis of insulin-like growth factor-binding protein-4 in mouse osteoblastic cells. Endocrinology. 1996;137(1):281–6.PubMedCrossRef Glantschnig H, Varga F, Klaushofer K. Thyroid hormone and retinoic acid induce the synthesis of insulin-like growth factor-binding protein-4 in mouse osteoblastic cells. Endocrinology. 1996;137(1):281–6.PubMedCrossRef
52.
Zurück zum Zitat Milne M, Kang MI, Quail JM, Baran DT. Thyroid hormone excess increases insulin-like growth factor I transcripts in bone marrow cell cultures: divergent effects on vertebral and femoral cell cultures. Endocrinology. 1998;139(5):2527–34.PubMedCrossRef Milne M, Kang MI, Quail JM, Baran DT. Thyroid hormone excess increases insulin-like growth factor I transcripts in bone marrow cell cultures: divergent effects on vertebral and femoral cell cultures. Endocrinology. 1998;139(5):2527–34.PubMedCrossRef
53.
Zurück zum Zitat Huang BK, Golden LA, Tarjan G, Madison LD, Stern PH. Insulin-like growth factor I production is essential for anabolic effects of thyroid hormone in osteoblasts. J Bone Miner Res. 2000;15(2):188–97.PubMedCrossRef Huang BK, Golden LA, Tarjan G, Madison LD, Stern PH. Insulin-like growth factor I production is essential for anabolic effects of thyroid hormone in osteoblasts. J Bone Miner Res. 2000;15(2):188–97.PubMedCrossRef
54.
Zurück zum Zitat Stevens DA, Harvey CB, Scott AJ, O'Shea PJ, Barnard JC, Williams AJ, et al. Thyroid hormone activates fibroblast growth factor receptor-1 in bone. Mol Endocrinol. 2003;17(9):1751–66.PubMedCrossRef Stevens DA, Harvey CB, Scott AJ, O'Shea PJ, Barnard JC, Williams AJ, et al. Thyroid hormone activates fibroblast growth factor receptor-1 in bone. Mol Endocrinol. 2003;17(9):1751–66.PubMedCrossRef
55.
Zurück zum Zitat Schmid C, Steiner T, Froesch ER. Triiodothyronine increases responsiveness of cultured rat bone cells to parathyroid hormone. Acta Endocrinol. 1986;111(2):213–6.PubMedCrossRef Schmid C, Steiner T, Froesch ER. Triiodothyronine increases responsiveness of cultured rat bone cells to parathyroid hormone. Acta Endocrinol. 1986;111(2):213–6.PubMedCrossRef
56.
Zurück zum Zitat Gu WX, Stern PH, Madison LD, Du GG. Mutual up-regulation of thyroid hormone and parathyroid hormone receptors in rat osteoblastic osteosarcoma 17/2.8 cells. Endocrinology. 2001;142(1):157–64.PubMedCrossRef Gu WX, Stern PH, Madison LD, Du GG. Mutual up-regulation of thyroid hormone and parathyroid hormone receptors in rat osteoblastic osteosarcoma 17/2.8 cells. Endocrinology. 2001;142(1):157–64.PubMedCrossRef
57.
Zurück zum Zitat Mundy GR, Shapiro JL, Bandelin JG, Canalis EM, Raisz LG. Direct stimulation of bone resorption by thyroid hormones. J Clin Invest. 1976;58(3):529–34.PubMedPubMedCentralCrossRef Mundy GR, Shapiro JL, Bandelin JG, Canalis EM, Raisz LG. Direct stimulation of bone resorption by thyroid hormones. J Clin Invest. 1976;58(3):529–34.PubMedPubMedCentralCrossRef
58.
Zurück zum Zitat Hoffmann O, Klaushofer K, Koller K, Peterlik M, Mavreas T, Stern P. Indomethacin inhibits thrombin-, but not thyroxin-stimulated resorption of fetal rat limb bones. Prostaglandins. 1986;31(4):601–8.PubMedCrossRef Hoffmann O, Klaushofer K, Koller K, Peterlik M, Mavreas T, Stern P. Indomethacin inhibits thrombin-, but not thyroxin-stimulated resorption of fetal rat limb bones. Prostaglandins. 1986;31(4):601–8.PubMedCrossRef
59.
Zurück zum Zitat Krieger NS, Stappenbeck TS, Stern PH. Characterization of specific thyroid hormone receptors in bone. J Bone Miner Res. 1988;3(4):473–8.PubMedCrossRef Krieger NS, Stappenbeck TS, Stern PH. Characterization of specific thyroid hormone receptors in bone. J Bone Miner Res. 1988;3(4):473–8.PubMedCrossRef
60.
Zurück zum Zitat Klaushofer K, Hoffmann O, Gleispach H, Leis HJ, Czerwenka E, Koller K, et al. Bone-resorbing activity of thyroid hormones is related to prostaglandin production in cultured neonatal mouse calvaria. J Bone Miner Res. 1989;4(3):305–12.PubMedCrossRef Klaushofer K, Hoffmann O, Gleispach H, Leis HJ, Czerwenka E, Koller K, et al. Bone-resorbing activity of thyroid hormones is related to prostaglandin production in cultured neonatal mouse calvaria. J Bone Miner Res. 1989;4(3):305–12.PubMedCrossRef
61.
Zurück zum Zitat Lakatos P, Stern PH. Effects of cyclosporins and transforming growth factor beta 1 on thyroid hormone action in cultured fetal rat limb bones. Calcif Tissue Int. 1992;50(2):123–8.PubMedCrossRef Lakatos P, Stern PH. Effects of cyclosporins and transforming growth factor beta 1 on thyroid hormone action in cultured fetal rat limb bones. Calcif Tissue Int. 1992;50(2):123–8.PubMedCrossRef
62.
Zurück zum Zitat Kawaguchi H, Pilbeam CC, Woodiel FN, Raisz LG. Comparison of the effects of 3,5,3′-triiodothyroacetic acid and triiodothyronine on bone resorption in cultured fetal rat long bones and neonatal mouse calvariae. J Bone Miner Res. 1994;9(2):247–53.PubMedCrossRef Kawaguchi H, Pilbeam CC, Woodiel FN, Raisz LG. Comparison of the effects of 3,5,3′-triiodothyroacetic acid and triiodothyronine on bone resorption in cultured fetal rat long bones and neonatal mouse calvariae. J Bone Miner Res. 1994;9(2):247–53.PubMedCrossRef
63.
Zurück zum Zitat Stracke H, Rossol S, Schatz H. Alkaline phosphatase and insulin-like growth factor in fetal rat bone under the influence of thyroid hormones. Horm Metab Res. 1986;18(11):794.PubMedCrossRef Stracke H, Rossol S, Schatz H. Alkaline phosphatase and insulin-like growth factor in fetal rat bone under the influence of thyroid hormones. Horm Metab Res. 1986;18(11):794.PubMedCrossRef
64.
Zurück zum Zitat Allain TJ, Chambers TJ, Flanagan AM, McGregor AM. Tri-iodothyronine stimulates rat osteoclastic bone resorption by an indirect effect. J Endocrinol. 1992;133(3):327–31.PubMedCrossRef Allain TJ, Chambers TJ, Flanagan AM, McGregor AM. Tri-iodothyronine stimulates rat osteoclastic bone resorption by an indirect effect. J Endocrinol. 1992;133(3):327–31.PubMedCrossRef
65.
Zurück zum Zitat Lakatos P, Caplice MD, Khanna V, Stern PH. Thyroid hormones increase insulin-like growth factor I content in the medium of rat bone tissue. J Bone Miner Res. 1993;8(12):1475–81.PubMedCrossRef Lakatos P, Caplice MD, Khanna V, Stern PH. Thyroid hormones increase insulin-like growth factor I content in the medium of rat bone tissue. J Bone Miner Res. 1993;8(12):1475–81.PubMedCrossRef
66.
Zurück zum Zitat Tarjan G, Stern PH. Triiodothyronine potentiates the stimulatory effects of interleukin-1 beta on bone resorption and medium interleukin-6 content in fetal rat limb bone cultures. J Bone Miner Res. 1995;10(9):1321–6.PubMedCrossRef Tarjan G, Stern PH. Triiodothyronine potentiates the stimulatory effects of interleukin-1 beta on bone resorption and medium interleukin-6 content in fetal rat limb bone cultures. J Bone Miner Res. 1995;10(9):1321–6.PubMedCrossRef
67.
Zurück zum Zitat Klaushofer K, Varga F, Glantschnig H, Fratzl-Zelman N, Czerwenka E, Leis HJ, et al. The regulatory role of thyroid hormones in bone cell growth and differentiation. J Nutr. 1995;125(7 Suppl):1996S–2003S.PubMedCrossRef Klaushofer K, Varga F, Glantschnig H, Fratzl-Zelman N, Czerwenka E, Leis HJ, et al. The regulatory role of thyroid hormones in bone cell growth and differentiation. J Nutr. 1995;125(7 Suppl):1996S–2003S.PubMedCrossRef
68.
Zurück zum Zitat Siddiqi A, Burrin JM, Wood DF, Monson JP. Tri-iodothyronine regulates the production of interleukin-6 and interleukin-8 in human bone marrow stromal and osteoblast-like cells. J Endocrinol. 1998;157(3):453–61.PubMedCrossRef Siddiqi A, Burrin JM, Wood DF, Monson JP. Tri-iodothyronine regulates the production of interleukin-6 and interleukin-8 in human bone marrow stromal and osteoblast-like cells. J Endocrinol. 1998;157(3):453–61.PubMedCrossRef
69.
Zurück zum Zitat Schiller C, Gruber R, Ho GM, Redlich K, Gober HJ, Katzgraber F, et al. Interaction of triiodothyronine with 1alpha,25-dihydroxyvitamin D3 on interleukin-6-dependent osteoclast-like cell formation in mouse bone marrow cell cultures. Bone. 1998;22(4):341–6.PubMedCrossRef Schiller C, Gruber R, Ho GM, Redlich K, Gober HJ, Katzgraber F, et al. Interaction of triiodothyronine with 1alpha,25-dihydroxyvitamin D3 on interleukin-6-dependent osteoclast-like cell formation in mouse bone marrow cell cultures. Bone. 1998;22(4):341–6.PubMedCrossRef
70.
Zurück zum Zitat Conaway HH, Ransjö M, Lerner UH. Prostaglandin-independent stimulation of bone resorption in mouse calvariae and in isolated rat osteoclasts by thyroid hormones (T4, and T3). Proc Soc Exp Biol Med. 1998;217(2):153–61.PubMedCrossRef Conaway HH, Ransjö M, Lerner UH. Prostaglandin-independent stimulation of bone resorption in mouse calvariae and in isolated rat osteoclasts by thyroid hormones (T4, and T3). Proc Soc Exp Biol Med. 1998;217(2):153–61.PubMedCrossRef
71.
Zurück zum Zitat Refetoff S, Weiss RE, Usala SJ. The syndromes of resistance to thyroid hormone. Endocr Rev. 1993;14(3):348–99.PubMed Refetoff S, Weiss RE, Usala SJ. The syndromes of resistance to thyroid hormone. Endocr Rev. 1993;14(3):348–99.PubMed
72.
Zurück zum Zitat Sakurai A, Miyamoto T, Refetoff S, DeGroot LJ. Dominant negative transcriptional regulation by a mutant thyroid hormone receptor-beta in a family with generalized resistance to thyroid hormone. Mol Endocrinol. 1990;4(12):1988–94.PubMedCrossRef Sakurai A, Miyamoto T, Refetoff S, DeGroot LJ. Dominant negative transcriptional regulation by a mutant thyroid hormone receptor-beta in a family with generalized resistance to thyroid hormone. Mol Endocrinol. 1990;4(12):1988–94.PubMedCrossRef
73.
Zurück zum Zitat Chatterjee VK, Nagaya T, Madison LD, Datta S, Rentoumis A, Jameson JL. Thyroid hormone resistance syndrome. Inhibition of normal receptor function by mutant thyroid hormone receptors. J Clin Invest. 1991;87(6):1977–84.PubMedPubMedCentralCrossRef Chatterjee VK, Nagaya T, Madison LD, Datta S, Rentoumis A, Jameson JL. Thyroid hormone resistance syndrome. Inhibition of normal receptor function by mutant thyroid hormone receptors. J Clin Invest. 1991;87(6):1977–84.PubMedPubMedCentralCrossRef
74.
Zurück zum Zitat Kopp P, Kitajima K, Jameson JL. Syndrome of resistance to thyroid hormone: insights into thyroid hormone action. Proc Soc Exp Biol Med. 1996;211(1):49–61.PubMedCrossRef Kopp P, Kitajima K, Jameson JL. Syndrome of resistance to thyroid hormone: insights into thyroid hormone action. Proc Soc Exp Biol Med. 1996;211(1):49–61.PubMedCrossRef
75.
Zurück zum Zitat Bochukova E, Schoenmakers N, Agostini M, Schoenmakers E, Rajanayagam O, Keogh JM, et al. A mutation in the thyroid hormone receptor alpha gene. N Engl J Med. 2012;366(3):243–9.PubMedCrossRef Bochukova E, Schoenmakers N, Agostini M, Schoenmakers E, Rajanayagam O, Keogh JM, et al. A mutation in the thyroid hormone receptor alpha gene. N Engl J Med. 2012;366(3):243–9.PubMedCrossRef
76.
Zurück zum Zitat van Mullem A, van Heerebeek R, Chrysis D, Visser E, Medici M, Andrikoula M, et al. Clinical phenotype and mutant TRα1. N Engl J Med. 2012;366(15):1451–3.PubMedCrossRef van Mullem A, van Heerebeek R, Chrysis D, Visser E, Medici M, Andrikoula M, et al. Clinical phenotype and mutant TRα1. N Engl J Med. 2012;366(15):1451–3.PubMedCrossRef
77.
Zurück zum Zitat Moran C, Schoenmakers N, Agostini M, Schoenmakers E, Offiah A, Kydd A, et al. An adult female with resistance to thyroid hormone mediated by defective thyroid hormone receptor α. J Clin Endocrinol Metab. 2013;98(11):4254–61.PubMedCrossRef Moran C, Schoenmakers N, Agostini M, Schoenmakers E, Offiah A, Kydd A, et al. An adult female with resistance to thyroid hormone mediated by defective thyroid hormone receptor α. J Clin Endocrinol Metab. 2013;98(11):4254–61.PubMedCrossRef
78.
Zurück zum Zitat Kaneshige M, Suzuki H, Kaneshige K, Cheng J, Wimbrow H, Barlow C, et al. A targeted dominant negative mutation of the thyroid hormone alpha 1 receptor causes increased mortality, infertility, and dwarfism in mice. Proc Natl Acad Sci U S A. 2001;98(26):15095–100.PubMedPubMedCentralCrossRef Kaneshige M, Suzuki H, Kaneshige K, Cheng J, Wimbrow H, Barlow C, et al. A targeted dominant negative mutation of the thyroid hormone alpha 1 receptor causes increased mortality, infertility, and dwarfism in mice. Proc Natl Acad Sci U S A. 2001;98(26):15095–100.PubMedPubMedCentralCrossRef
79.
Zurück zum Zitat O'Shea PJ, Bassett JH, Cheng SY, Williams GR. Characterization of skeletal phenotypes of TRalpha1 and TRbeta mutant mice: implications for tissue thyroid status and T3 target gene expression. Nucl Recept Signal. 2006;4:e011.PubMedPubMedCentralCrossRef O'Shea PJ, Bassett JH, Cheng SY, Williams GR. Characterization of skeletal phenotypes of TRalpha1 and TRbeta mutant mice: implications for tissue thyroid status and T3 target gene expression. Nucl Recept Signal. 2006;4:e011.PubMedPubMedCentralCrossRef
80.
Zurück zum Zitat Quignodon L, Vincent S, Winter H, Samarut J, Flamant F. A point mutation in the activation function 2 domain of thyroid hormone receptor alpha1 expressed after CRE-mediated recombination partially recapitulates hypothyroidism. Mol Endocrinol. 2007 Oct;21(10):2350–60.PubMedCrossRef Quignodon L, Vincent S, Winter H, Samarut J, Flamant F. A point mutation in the activation function 2 domain of thyroid hormone receptor alpha1 expressed after CRE-mediated recombination partially recapitulates hypothyroidism. Mol Endocrinol. 2007 Oct;21(10):2350–60.PubMedCrossRef
81.
Zurück zum Zitat Bassett JH, Boyde A, Zikmund T, Evans H, Croucher PI, Zhu X, et al. Thyroid hormone receptor α mutation causes a severe and thyroxine-resistant skeletal dysplasia in female mice. Endocrinology. 2014;155(9):3699–712.PubMedPubMedCentralCrossRef Bassett JH, Boyde A, Zikmund T, Evans H, Croucher PI, Zhu X, et al. Thyroid hormone receptor α mutation causes a severe and thyroxine-resistant skeletal dysplasia in female mice. Endocrinology. 2014;155(9):3699–712.PubMedPubMedCentralCrossRef
82.
Zurück zum Zitat Hase H, Ando T, Eldeiry L, Brebene A, Peng Y, Liu L, et al. TNFalpha mediates the skeletal effects of thyroid-stimulating hormone. Proc Natl Acad Sci U S A. 2006;103(34):12849–54.PubMedPubMedCentralCrossRef Hase H, Ando T, Eldeiry L, Brebene A, Peng Y, Liu L, et al. TNFalpha mediates the skeletal effects of thyroid-stimulating hormone. Proc Natl Acad Sci U S A. 2006;103(34):12849–54.PubMedPubMedCentralCrossRef
83.
Zurück zum Zitat Ma R, Morshed S, Latif R, Zaidi M, Davies TF. The influence of thyroid-stimulating hormone and thyroid-stimulating hormone receptor antibodies on osteoclastogenesis. Thyroid. 2011;21(8):897–906.PubMedPubMedCentralCrossRef Ma R, Morshed S, Latif R, Zaidi M, Davies TF. The influence of thyroid-stimulating hormone and thyroid-stimulating hormone receptor antibodies on osteoclastogenesis. Thyroid. 2011;21(8):897–906.PubMedPubMedCentralCrossRef
84.
Zurück zum Zitat Zhang W, Y Z, Y L, J W, L G, C Y, et al. Thyroid-stimulating hormone maintains bone mass and strength by suppressing osteoclast differentiation. J Biomech. 2014;47(6):1307–14.PubMedCrossRef Zhang W, Y Z, Y L, J W, L G, C Y, et al. Thyroid-stimulating hormone maintains bone mass and strength by suppressing osteoclast differentiation. J Biomech. 2014;47(6):1307–14.PubMedCrossRef
85.
Zurück zum Zitat Sampath TK, Simic P, Sendak R, Draca N, Bowe AE, O'Brien S, et al. Thyroid-stimulating hormone restores bone volume, microarchitecture, and strength in aged ovariectomized rats. J Bone Miner Res. 2007;22(6):849–59.PubMedCrossRef Sampath TK, Simic P, Sendak R, Draca N, Bowe AE, O'Brien S, et al. Thyroid-stimulating hormone restores bone volume, microarchitecture, and strength in aged ovariectomized rats. J Bone Miner Res. 2007;22(6):849–59.PubMedCrossRef
86.
87.
Zurück zum Zitat Baliram R, Latif R, Berkowitz J, Frid S, Colaianni G, Sun L, et al. Thyroid-stimulating hormone induces a Wnt-dependent, feed-forward loop for osteoblastogenesis in embryonic stem cell cultures. Proc Natl Acad Sci U S A. 2011;108(39):16277–82.PubMedPubMedCentralCrossRef Baliram R, Latif R, Berkowitz J, Frid S, Colaianni G, Sun L, et al. Thyroid-stimulating hormone induces a Wnt-dependent, feed-forward loop for osteoblastogenesis in embryonic stem cell cultures. Proc Natl Acad Sci U S A. 2011;108(39):16277–82.PubMedPubMedCentralCrossRef
88.
Zurück zum Zitat Tsai JA, Janson A, Bucht E, Kindmark H, Marcus C, Stark A, et al. Weak evidence of thyrotropin receptors in primary cultures of human osteoblast-like cells. Calcif Tissue Int. 2004;74(5):486–91.PubMedCrossRef Tsai JA, Janson A, Bucht E, Kindmark H, Marcus C, Stark A, et al. Weak evidence of thyrotropin receptors in primary cultures of human osteoblast-like cells. Calcif Tissue Int. 2004;74(5):486–91.PubMedCrossRef
89.
Zurück zum Zitat Williams AJ, Robson H, Kester MHA, van Leeuwen JPTM, Shalet SM, Visser TJ, et al. Iodothyronine deiodinase enzyme activities in bone. Bone. 2008;43(1):126–34.PubMedPubMedCentralCrossRef Williams AJ, Robson H, Kester MHA, van Leeuwen JPTM, Shalet SM, Visser TJ, et al. Iodothyronine deiodinase enzyme activities in bone. Bone. 2008;43(1):126–34.PubMedPubMedCentralCrossRef
90.
Zurück zum Zitat Bassett JH, Boyde A, Howell PG, Bassett RH, Galliford TM, Archanco M, et al. Optimal bone strength and mineralization requires the type 2 iodothyronine deiodinase in osteoblasts. Proc Natl Acad Sci U S A. 2010;107(16):7604–9.PubMedPubMedCentralCrossRef Bassett JH, Boyde A, Howell PG, Bassett RH, Galliford TM, Archanco M, et al. Optimal bone strength and mineralization requires the type 2 iodothyronine deiodinase in osteoblasts. Proc Natl Acad Sci U S A. 2010;107(16):7604–9.PubMedPubMedCentralCrossRef
91.
Zurück zum Zitat Capelo LP, Beber EH, Huang SA, Zorn TM, Bianco AC, Gouveia CH. Deiodinase-mediated thyroid hormone inactivation minimizes thyroid hormone signaling in the early development of fetal skeleton. Bone. 2008;43(5):921–30.PubMedPubMedCentralCrossRef Capelo LP, Beber EH, Huang SA, Zorn TM, Bianco AC, Gouveia CH. Deiodinase-mediated thyroid hormone inactivation minimizes thyroid hormone signaling in the early development of fetal skeleton. Bone. 2008;43(5):921–30.PubMedPubMedCentralCrossRef
92.
Zurück zum Zitat Liao XH, Di Cosmo C, Dumitrescu AM, Hernandez A, Van Sande J, St Germain DL, et al. Distinct roles of deiodinases on the phenotype of Mct8 defect: a comparison of eight different mouse genotypes. Endocrinology. 2011;152(3):1180–91.PubMedPubMedCentralCrossRef Liao XH, Di Cosmo C, Dumitrescu AM, Hernandez A, Van Sande J, St Germain DL, et al. Distinct roles of deiodinases on the phenotype of Mct8 defect: a comparison of eight different mouse genotypes. Endocrinology. 2011;152(3):1180–91.PubMedPubMedCentralCrossRef
93.
Zurück zum Zitat Hernandez A, Martinez ME, Fiering S, Galton VA, St Germain D. Type 3 deiodinase is critical for the maturation and function of the thyroid axis. J Clin Invest. 2006;116(2):476–84.PubMedPubMedCentralCrossRef Hernandez A, Martinez ME, Fiering S, Galton VA, St Germain D. Type 3 deiodinase is critical for the maturation and function of the thyroid axis. J Clin Invest. 2006;116(2):476–84.PubMedPubMedCentralCrossRef
94.
Zurück zum Zitat Hernandez A, Martinez ME, Liao XH, Van Sande J, Refetoff S, Galton VA, et al. Type 3 deiodinase deficiency results in functional abnormalities at multiple levels of the thyroid axis. Endocrinology. 2007;148(12):5680–7.PubMedCrossRef Hernandez A, Martinez ME, Liao XH, Van Sande J, Refetoff S, Galton VA, et al. Type 3 deiodinase deficiency results in functional abnormalities at multiple levels of the thyroid axis. Endocrinology. 2007;148(12):5680–7.PubMedCrossRef
95.
Zurück zum Zitat Capelo LP, Beber EH, Fonseca TL, Gouveia CH. The monocarboxylate transporter 8 and L-type amino acid transporters 1 and 2 are expressed in mouse skeletons and in osteoblastic MC3T3-E1 cells. Thyroid. 2009;19(2):171–80.PubMedCrossRef Capelo LP, Beber EH, Fonseca TL, Gouveia CH. The monocarboxylate transporter 8 and L-type amino acid transporters 1 and 2 are expressed in mouse skeletons and in osteoblastic MC3T3-E1 cells. Thyroid. 2009;19(2):171–80.PubMedCrossRef
96.
Zurück zum Zitat Davis PJ, Davis FB, Mousa SA, Luidens MK, Lin HY. Membrane receptor for thyroid hormone: physiologic and pharmacologic implications. Annu Rev Pharmacol Toxicol. 2011;51(1):99–115.PubMedCrossRef Davis PJ, Davis FB, Mousa SA, Luidens MK, Lin HY. Membrane receptor for thyroid hormone: physiologic and pharmacologic implications. Annu Rev Pharmacol Toxicol. 2011;51(1):99–115.PubMedCrossRef
97.
Zurück zum Zitat Davis PJ, Goglia F, Leonard JL. Nongenomic actions of thyroid hormone. Nat Rev Endocrinol. 2016;12(2):111–21.PubMedCrossRef Davis PJ, Goglia F, Leonard JL. Nongenomic actions of thyroid hormone. Nat Rev Endocrinol. 2016;12(2):111–21.PubMedCrossRef
98.
Zurück zum Zitat Davis PJ, Lin HY, Tang HY, Davis FB, Mousa SA. Adjunctive input to the nuclear thyroid hormone receptor from the cell surface receptor for the hormone. Thyroid. 2013;23(12):1503–9.PubMedCrossRef Davis PJ, Lin HY, Tang HY, Davis FB, Mousa SA. Adjunctive input to the nuclear thyroid hormone receptor from the cell surface receptor for the hormone. Thyroid. 2013;23(12):1503–9.PubMedCrossRef
99.
Zurück zum Zitat Kalyanaraman H, Schwappacher R, Joshua J, Zhuang S, Scott BT, Klos M, et al. Nongenomic thyroid hormone signaling occurs through a plasma membrane-localized receptor. Sci Signal. 2014;7(326):ra48.PubMedCrossRef Kalyanaraman H, Schwappacher R, Joshua J, Zhuang S, Scott BT, Klos M, et al. Nongenomic thyroid hormone signaling occurs through a plasma membrane-localized receptor. Sci Signal. 2014;7(326):ra48.PubMedCrossRef
100.
Zurück zum Zitat Scarlett A, Parsons MP, Hanson PL, Sidhu KK, Milligan TP, Burrin JM. Thyroid hormone stimulation of extracellular signal-regulated kinase and cell proliferation in human osteoblast-like cells is initiated at integrin alphaVbeta3. J Endocrinol. 2008;196(3):509–17.PubMedCrossRef Scarlett A, Parsons MP, Hanson PL, Sidhu KK, Milligan TP, Burrin JM. Thyroid hormone stimulation of extracellular signal-regulated kinase and cell proliferation in human osteoblast-like cells is initiated at integrin alphaVbeta3. J Endocrinol. 2008;196(3):509–17.PubMedCrossRef
101.
Zurück zum Zitat Hoffman SJ, Vasko-Moser J, Miller WH, Lark MW, Gowen M, Stroup G. Rapid inhibition of thyroxine-induced bone resorption in the rat by an orally active vitronectin receptor antagonist. J Pharmacol Exp Therap. 2002;302(1):205–11.CrossRef Hoffman SJ, Vasko-Moser J, Miller WH, Lark MW, Gowen M, Stroup G. Rapid inhibition of thyroxine-induced bone resorption in the rat by an orally active vitronectin receptor antagonist. J Pharmacol Exp Therap. 2002;302(1):205–11.CrossRef
102.
Zurück zum Zitat Lakatos P, Stern PH. Evidence for direct non-genomic effects of triiodothyronine on bone rudiments in rats: stimulation of the inositol phosphate second messenger system. Acta Endocrinol. 1991;125(5):603–8.PubMedCrossRef Lakatos P, Stern PH. Evidence for direct non-genomic effects of triiodothyronine on bone rudiments in rats: stimulation of the inositol phosphate second messenger system. Acta Endocrinol. 1991;125(5):603–8.PubMedCrossRef
103.
Zurück zum Zitat Fonseca TL, Teixeira MB, Miranda-Rodrigues M, Silva MV, Martins GM, Costa CC, et al. Thyroid hormone interacts with the sympathetic nervous system to modulate bone mass and structure in young adult mice. Am J Physiol Endocrinol Metab. 2014;307(4):E408–18.PubMedCrossRef Fonseca TL, Teixeira MB, Miranda-Rodrigues M, Silva MV, Martins GM, Costa CC, et al. Thyroid hormone interacts with the sympathetic nervous system to modulate bone mass and structure in young adult mice. Am J Physiol Endocrinol Metab. 2014;307(4):E408–18.PubMedCrossRef
104.
Zurück zum Zitat Cruz Grecco Teixeira MB, Martins GM, Miranda-Rodrigues M, De Araújo IF, Oliveira R, Brum PC, et al. Lack of α2C-adrenoceptor results in contrasting phenotypes of long bones and vertebra and prevents the thyrotoxicosis-induced osteopenia. PLoS One. 2016;11(1):e0146795.PubMedPubMedCentralCrossRef Cruz Grecco Teixeira MB, Martins GM, Miranda-Rodrigues M, De Araújo IF, Oliveira R, Brum PC, et al. Lack of α2C-adrenoceptor results in contrasting phenotypes of long bones and vertebra and prevents the thyrotoxicosis-induced osteopenia. PLoS One. 2016;11(1):e0146795.PubMedPubMedCentralCrossRef
105.
Zurück zum Zitat Mosekilde L, Melsen F. Morphometric and dynamic studies of bone changes in hypothyroidism. Acta Pathol Microbiol Scand A. 1978;86(1):56–62.PubMed Mosekilde L, Melsen F. Morphometric and dynamic studies of bone changes in hypothyroidism. Acta Pathol Microbiol Scand A. 1978;86(1):56–62.PubMed
106.
Zurück zum Zitat Heyerdahl S, Kase BF, Stake G. Skeletal maturation during thyroxine treatment in children with congenital hypothyroidism. Acta Paediatr. 1994;83(6):618–22.PubMedCrossRef Heyerdahl S, Kase BF, Stake G. Skeletal maturation during thyroxine treatment in children with congenital hypothyroidism. Acta Paediatr. 1994;83(6):618–22.PubMedCrossRef
108.
Zurück zum Zitat Ford G, LaFranchi SH. Screening for congenital hypothyroidism: a worldwide view of strategies. Best Pract Res Clin Endocrinol Metab. 2014;28(2):175–87.PubMedCrossRef Ford G, LaFranchi SH. Screening for congenital hypothyroidism: a worldwide view of strategies. Best Pract Res Clin Endocrinol Metab. 2014;28(2):175–87.PubMedCrossRef
109.
Zurück zum Zitat Alm J, Hagenfeldt L, Larsson A, Lundberg K. Incidence of congenital hypothyroidism: retrospective study of neonatal laboratory screening versus clinical symptoms as indicators leading to diagnosis. Br Med J (Clin Res Ed). 1984;289(6453):1171–5.CrossRef Alm J, Hagenfeldt L, Larsson A, Lundberg K. Incidence of congenital hypothyroidism: retrospective study of neonatal laboratory screening versus clinical symptoms as indicators leading to diagnosis. Br Med J (Clin Res Ed). 1984;289(6453):1171–5.CrossRef
110.
Zurück zum Zitat Hüffmeier U, Tietze HU, Rauch A. Severe skeletal dysplasia caused by undiagnosed hypothyroidism. Eur J Med Genet. 2007;50(3):209–15.PubMedCrossRef Hüffmeier U, Tietze HU, Rauch A. Severe skeletal dysplasia caused by undiagnosed hypothyroidism. Eur J Med Genet. 2007;50(3):209–15.PubMedCrossRef
111.
Zurück zum Zitat Salerno M, Micillo M, Di Maio S, Capalbo D, Ferri P, Lettiero T, et al. Longitudinal growth, sexual maturation and final height in patients with congenital hypothyroidism detected by neonatal screening. Eur J Endocrinol. 2001;145(4):377–83.PubMedCrossRef Salerno M, Micillo M, Di Maio S, Capalbo D, Ferri P, Lettiero T, et al. Longitudinal growth, sexual maturation and final height in patients with congenital hypothyroidism detected by neonatal screening. Eur J Endocrinol. 2001;145(4):377–83.PubMedCrossRef
112.
Zurück zum Zitat Salerno M, Lettiero T, Esposito-del Puente A, Esposito V, Capalbo D, Carpinelli A, et al. Effect of long-term L-thyroxine treatment on bone mineral density in young adults with congenital hypothyroidism. Eur J Endocrinol. 2004;151:689–94.PubMedCrossRef Salerno M, Lettiero T, Esposito-del Puente A, Esposito V, Capalbo D, Carpinelli A, et al. Effect of long-term L-thyroxine treatment on bone mineral density in young adults with congenital hypothyroidism. Eur J Endocrinol. 2004;151:689–94.PubMedCrossRef
113.
Zurück zum Zitat de Vries L, Bulvik S, Phillip M. Chronic autoimmune thyroiditis in children and adolescents: at presentation and during long-term follow-up. Arch Dis Child. 2009;94(1):33–7.PubMedCrossRef de Vries L, Bulvik S, Phillip M. Chronic autoimmune thyroiditis in children and adolescents: at presentation and during long-term follow-up. Arch Dis Child. 2009;94(1):33–7.PubMedCrossRef
114.
Zurück zum Zitat Kaplowitz PB. Subclinical hypothyroidism in children: normal variation or sign of a failing thyroid gland? Int J Pediatr Endocrinol. 2010;2010(1):281453.PubMedPubMedCentralCrossRef Kaplowitz PB. Subclinical hypothyroidism in children: normal variation or sign of a failing thyroid gland? Int J Pediatr Endocrinol. 2010;2010(1):281453.PubMedPubMedCentralCrossRef
115.
Zurück zum Zitat Aoki Y, Belin RM, Clickner R, Jeffries R, Phillips L, Mahaffey KR, et al. Total T4 in the United States population and their association with participant characteristics: National Health and Nutrition Examination Survey. Thyroid. 2007;17(12):1211–23.PubMedCrossRef Aoki Y, Belin RM, Clickner R, Jeffries R, Phillips L, Mahaffey KR, et al. Total T4 in the United States population and their association with participant characteristics: National Health and Nutrition Examination Survey. Thyroid. 2007;17(12):1211–23.PubMedCrossRef
116.
Zurück zum Zitat Nakamura H, Mori T, Genma R, Suzuki Y, Natsume H, Andoh S, et al. Urinary excretion of pyridinoline and deoxypyridinoline measured by immunoassay in hypothyroidism. Clin Endocrinol. 1996;44(4):447–51.CrossRef Nakamura H, Mori T, Genma R, Suzuki Y, Natsume H, Andoh S, et al. Urinary excretion of pyridinoline and deoxypyridinoline measured by immunoassay in hypothyroidism. Clin Endocrinol. 1996;44(4):447–51.CrossRef
117.
Zurück zum Zitat Sabuncu T, Aksoy N, Arikan E, Ugur B, Tasan E, Hatemi H. Early changes in parameters of bone and mineral metabolism during therapy for hyper- and hypothyroidism. Endocr Res. 2001;27(1–2):203–13.PubMedCrossRef Sabuncu T, Aksoy N, Arikan E, Ugur B, Tasan E, Hatemi H. Early changes in parameters of bone and mineral metabolism during therapy for hyper- and hypothyroidism. Endocr Res. 2001;27(1–2):203–13.PubMedCrossRef
118.
Zurück zum Zitat Stamato FJ, Amarante EC, Furlanetto RP. Effect of combined treatment with calcitonin on bone densitometry of patients with treated hypothyroidism. Rev Assoc Med Bras. 2000;46(2):177–81.PubMedCrossRef Stamato FJ, Amarante EC, Furlanetto RP. Effect of combined treatment with calcitonin on bone densitometry of patients with treated hypothyroidism. Rev Assoc Med Bras. 2000;46(2):177–81.PubMedCrossRef
119.
Zurück zum Zitat Vestergaard P, Mosekilde L. Fractures in patients with hyperthyroidism and hypothyroidism: a nationwide follow-up study in 16,249 patients. Thyroid. 2002;12(5):411–9.PubMedCrossRef Vestergaard P, Mosekilde L. Fractures in patients with hyperthyroidism and hypothyroidism: a nationwide follow-up study in 16,249 patients. Thyroid. 2002;12(5):411–9.PubMedCrossRef
120.
Zurück zum Zitat González-Rodríguez LA, Felici-Giovanini ME, Haddock L. Thyroid dysfunction in an adult female population: a population-based study of Latin American Vertebral Osteoporosis Study (LAVOS)—Puerto Rico site. P R Health Sci J. 2013;32(2):57–62.PubMedPubMedCentral González-Rodríguez LA, Felici-Giovanini ME, Haddock L. Thyroid dysfunction in an adult female population: a population-based study of Latin American Vertebral Osteoporosis Study (LAVOS)—Puerto Rico site. P R Health Sci J. 2013;32(2):57–62.PubMedPubMedCentral
121.
Zurück zum Zitat Vestergaard P, Weeke J, Hoeck HC, Nielsen HK, Rungby J, Rejnmark L, et al. Fractures in patients with primary idiopathic hypothyroidism. Thyroid. 2000;10(4):335–40.PubMedCrossRef Vestergaard P, Weeke J, Hoeck HC, Nielsen HK, Rungby J, Rejnmark L, et al. Fractures in patients with primary idiopathic hypothyroidism. Thyroid. 2000;10(4):335–40.PubMedCrossRef
122.
Zurück zum Zitat Vestergaard P, Rejnmark L, Mosekilde L. Influence of hyper- and hypothyroidism, and the effects of treatment with antithyroid drugs and levothyroxine on fracture risk. Calcif Tissue Int. 2005;77(3):139–44.PubMedCrossRef Vestergaard P, Rejnmark L, Mosekilde L. Influence of hyper- and hypothyroidism, and the effects of treatment with antithyroid drugs and levothyroxine on fracture risk. Calcif Tissue Int. 2005;77(3):139–44.PubMedCrossRef
123.
Zurück zum Zitat Lee JS, Buzková P, Fink HA, Vu J, Carbone L, Chen Z, et al. Subclinical thyroid dysfunction and incident hip fracture in older adults. Arch Intern Med. 2010;170(21):1876–83.PubMedPubMedCentralCrossRef Lee JS, Buzková P, Fink HA, Vu J, Carbone L, Chen Z, et al. Subclinical thyroid dysfunction and incident hip fracture in older adults. Arch Intern Med. 2010;170(21):1876–83.PubMedPubMedCentralCrossRef
124.
Zurück zum Zitat Waring AC, Harrison S, Fink HA, Samuels MH, Cawthon PM, Zmuda JM, et al. A prospective study of thyroid function, bone loss, and fractures in older men: the MrOS study. J Bone Miner Res. 2013;28(3):472–9.PubMedPubMedCentralCrossRef Waring AC, Harrison S, Fink HA, Samuels MH, Cawthon PM, Zmuda JM, et al. A prospective study of thyroid function, bone loss, and fractures in older men: the MrOS study. J Bone Miner Res. 2013;28(3):472–9.PubMedPubMedCentralCrossRef
125.
Zurück zum Zitat Blum MR, Bauer DC, Collet TH, Fink HA, Cappola AR, da Costa BR, et al. Subclinical thyroid dysfunction and fracture risk: a metaanalysis. JAMA. 2015;313:2055–65.PubMedPubMedCentralCrossRef Blum MR, Bauer DC, Collet TH, Fink HA, Cappola AR, da Costa BR, et al. Subclinical thyroid dysfunction and fracture risk: a metaanalysis. JAMA. 2015;313:2055–65.PubMedPubMedCentralCrossRef
126.
Zurück zum Zitat Eriksen EF. Normal and pathological remodeling of human trabecular bone: three dimensional reconstruction of the remodeling sequence in normals and in metabolic bone disease. Endocr Rev. 1986;7(4):379–408.PubMedCrossRef Eriksen EF. Normal and pathological remodeling of human trabecular bone: three dimensional reconstruction of the remodeling sequence in normals and in metabolic bone disease. Endocr Rev. 1986;7(4):379–408.PubMedCrossRef
127.
Zurück zum Zitat Polak M, Legac I, Vuillard E, Guibourdenche J, Castanet M, Luton D. Congenital hyperthyroidism: the fetus as a patient. Horm Res. 2006;65(5):235–42.PubMed Polak M, Legac I, Vuillard E, Guibourdenche J, Castanet M, Luton D. Congenital hyperthyroidism: the fetus as a patient. Horm Res. 2006;65(5):235–42.PubMed
128.
Zurück zum Zitat McLeod DS, Cooper DS, Ladenson PW, Whiteman DC, Jordan SJ. Race/ethnicity and the prevalence of thyrotoxicosis in young Americans. Thyroid. 2015;25(6):621–8.PubMedCrossRef McLeod DS, Cooper DS, Ladenson PW, Whiteman DC, Jordan SJ. Race/ethnicity and the prevalence of thyrotoxicosis in young Americans. Thyroid. 2015;25(6):621–8.PubMedCrossRef
129.
Zurück zum Zitat Nagasaka S, Sugimoto H, Nakamura T, Kusaka I, Fujisawa G, Sakum N, et al. Antithyroid therapy improves bony manifestations and bone metabolic markers in patients with Graves’ thyrotoxicosis. Clin Endocrinol. 1997;47(2):215–21.CrossRef Nagasaka S, Sugimoto H, Nakamura T, Kusaka I, Fujisawa G, Sakum N, et al. Antithyroid therapy improves bony manifestations and bone metabolic markers in patients with Graves’ thyrotoxicosis. Clin Endocrinol. 1997;47(2):215–21.CrossRef
130.
Zurück zum Zitat Pantazi H, Papapetrou PD. Changes in parameters of bone and mineral metabolism during therapy for hyperthyroidism. J Clin Endocrinol Metab. 2000;85(3):1099–106.PubMedCrossRef Pantazi H, Papapetrou PD. Changes in parameters of bone and mineral metabolism during therapy for hyperthyroidism. J Clin Endocrinol Metab. 2000;85(3):1099–106.PubMedCrossRef
131.
Zurück zum Zitat Garnero P, Vassy V, Bertholin A, Riou JP, Delmas PD. Markers of bone turnover in hyperthyroidism and the effects of treatment. J Clin Endocrinol Metab. 1994;78(4):955–9.PubMed Garnero P, Vassy V, Bertholin A, Riou JP, Delmas PD. Markers of bone turnover in hyperthyroidism and the effects of treatment. J Clin Endocrinol Metab. 1994;78(4):955–9.PubMed
132.
Zurück zum Zitat Miyakawa M, Tsushima T, Demura H. Carboxy-terminal propeptide of type 1 procollagen (P1CP) and carboxy-terminal telopeptide of type 1 collagen (1CTP) as sensitive markers of bone metabolism in thyroid disease. Endocr J. 1996;43(6):701–8.PubMedCrossRef Miyakawa M, Tsushima T, Demura H. Carboxy-terminal propeptide of type 1 procollagen (P1CP) and carboxy-terminal telopeptide of type 1 collagen (1CTP) as sensitive markers of bone metabolism in thyroid disease. Endocr J. 1996;43(6):701–8.PubMedCrossRef
133.
Zurück zum Zitat Krølner B, Jørgensen JV, Nielsen SP. Spinal bone mineral content in myxoedema and thyrotoxicosis. Effects of thyroid hormone(s) and antithyroid treatment. Clin Endocrinol. 1983;18(5):439–46.CrossRef Krølner B, Jørgensen JV, Nielsen SP. Spinal bone mineral content in myxoedema and thyrotoxicosis. Effects of thyroid hormone(s) and antithyroid treatment. Clin Endocrinol. 1983;18(5):439–46.CrossRef
134.
Zurück zum Zitat Toh SH, Claunch BC, Brown PH. Effect of hyperthyroidism and its treatment on bone mineral content. Arch Intern Med. 1985;145(5):883–6.PubMedCrossRef Toh SH, Claunch BC, Brown PH. Effect of hyperthyroidism and its treatment on bone mineral content. Arch Intern Med. 1985;145(5):883–6.PubMedCrossRef
135.
Zurück zum Zitat Vestergaard P, Mosekilde L. Hyperthyroidism, bone mineral, and fracture risk—a meta-analysis. Thyroid. 2003;13(6):585–93.PubMedCrossRef Vestergaard P, Mosekilde L. Hyperthyroidism, bone mineral, and fracture risk—a meta-analysis. Thyroid. 2003;13(6):585–93.PubMedCrossRef
136.
Zurück zum Zitat El Hadidy el HM, Ghonaim M, El Gawad SS, El Atta MA. Impact of severity, duration, and etiology of hyperthyroidism on bone turnover markers and bone mineral density in men. BMC Endocr Disord. 2011;11(1):15.PubMedPubMedCentralCrossRef El Hadidy el HM, Ghonaim M, El Gawad SS, El Atta MA. Impact of severity, duration, and etiology of hyperthyroidism on bone turnover markers and bone mineral density in men. BMC Endocr Disord. 2011;11(1):15.PubMedPubMedCentralCrossRef
137.
Zurück zum Zitat Bauer DC, Ettinger B, Nevitt MC, Stone KL, Group SoOFR. Risk for fracture in women with low serum levels of thyroid-stimulating hormone. Ann Intern Med. 2001;134(7):561–8.PubMedCrossRef Bauer DC, Ettinger B, Nevitt MC, Stone KL, Group SoOFR. Risk for fracture in women with low serum levels of thyroid-stimulating hormone. Ann Intern Med. 2001;134(7):561–8.PubMedCrossRef
138.
Zurück zum Zitat Numbenjapon N, Costin G, Pitukcheewanont P. Normalization of cortical bone density in children and adolescents with hyperthyroidism treated with antithyroid medication. Osteoporos Int. 2012;23(9):2277–82.PubMedCrossRef Numbenjapon N, Costin G, Pitukcheewanont P. Normalization of cortical bone density in children and adolescents with hyperthyroidism treated with antithyroid medication. Osteoporos Int. 2012;23(9):2277–82.PubMedCrossRef
139.
Zurück zum Zitat Olkawa M, Kushida K, Takahash M, Ohishi T, Hoshino H, Suzuk M, et al. Bone turnover and cortical bone mineral density in the distal radius in patients with hyperthyroidism being treated with antithyroid drugs for various periods of time. Clin Endocrinol. 1999;50(2):171–6.CrossRef Olkawa M, Kushida K, Takahash M, Ohishi T, Hoshino H, Suzuk M, et al. Bone turnover and cortical bone mineral density in the distal radius in patients with hyperthyroidism being treated with antithyroid drugs for various periods of time. Clin Endocrinol. 1999;50(2):171–6.CrossRef
140.
Zurück zum Zitat Mirza F, Canalis E. Management of endocrine disease: secondary osteoporosis: pathophysiology and management. Eur J Endocrinol. 2015;173(3):R131–51.PubMedPubMedCentralCrossRef Mirza F, Canalis E. Management of endocrine disease: secondary osteoporosis: pathophysiology and management. Eur J Endocrinol. 2015;173(3):R131–51.PubMedPubMedCentralCrossRef
141.
Zurück zum Zitat Galliford TM, Murphy E, Williams AJ, Bassett JH, Williams GR. Effects of thyroid status on bone metabolism: a primary role for thyroid stimulating hormone or thyroid hormone? Minerva Endocrinol. 2005;30(4):237–46.PubMed Galliford TM, Murphy E, Williams AJ, Bassett JH, Williams GR. Effects of thyroid status on bone metabolism: a primary role for thyroid stimulating hormone or thyroid hormone? Minerva Endocrinol. 2005;30(4):237–46.PubMed
142.
Zurück zum Zitat Karner I, Hrgović Z, Sijanović S, Buković D, Klobucar A, Usadel KH, et al. Bone mineral density changes and bone turnover in thyroid carcinoma patients treated with supraphysiologic doses of thyroxine. Eur J Med Res. 2005;10(11):480–8.PubMed Karner I, Hrgović Z, Sijanović S, Buković D, Klobucar A, Usadel KH, et al. Bone mineral density changes and bone turnover in thyroid carcinoma patients treated with supraphysiologic doses of thyroxine. Eur J Med Res. 2005;10(11):480–8.PubMed
143.
Zurück zum Zitat Lee MY, Park JH, Bae KS, Jee YG, Ko AN, Han YJ, et al. Bone mineral density and bone turnover markers in patients on long-term suppressive levothyroxine therapy for differentiated thyroid cancer. Ann Surg Treat Res. 2014;86(2):55–60.PubMedPubMedCentralCrossRef Lee MY, Park JH, Bae KS, Jee YG, Ko AN, Han YJ, et al. Bone mineral density and bone turnover markers in patients on long-term suppressive levothyroxine therapy for differentiated thyroid cancer. Ann Surg Treat Res. 2014;86(2):55–60.PubMedPubMedCentralCrossRef
144.
Zurück zum Zitat Tauchmanovà L, Nuzzo V, Del Puente A, Fonderico F, Esposito-Del Puente A, Padulla S, et al. Reduced bone mass detected by bone quantitative ultrasonometry and DEXA in pre- and postmenopausal women with endogenous subclinical hyperthyroidism. Maturitas. 2004;48(3):299–306.PubMedCrossRef Tauchmanovà L, Nuzzo V, Del Puente A, Fonderico F, Esposito-Del Puente A, Padulla S, et al. Reduced bone mass detected by bone quantitative ultrasonometry and DEXA in pre- and postmenopausal women with endogenous subclinical hyperthyroidism. Maturitas. 2004;48(3):299–306.PubMedCrossRef
145.
Zurück zum Zitat Faber J, Galløe AM. Changes in bone mass during prolonged subclinical hyperthyroidism due to L-thyroxine treatment: a meta-analysis. Eur J Endocrinol. 1994;130(4):350–6.PubMedCrossRef Faber J, Galløe AM. Changes in bone mass during prolonged subclinical hyperthyroidism due to L-thyroxine treatment: a meta-analysis. Eur J Endocrinol. 1994;130(4):350–6.PubMedCrossRef
146.
Zurück zum Zitat Garin MC, Arnold AM, Lee JS, Robbins J, Cappola AR. Subclinical thyroid dysfunction and hip fracture and bone mineral density in older adults: the cardiovascular health study. J Clin Endocrinol Metab. 2014;99(8):2657–64.PubMedPubMedCentralCrossRef Garin MC, Arnold AM, Lee JS, Robbins J, Cappola AR. Subclinical thyroid dysfunction and hip fracture and bone mineral density in older adults: the cardiovascular health study. J Clin Endocrinol Metab. 2014;99(8):2657–64.PubMedPubMedCentralCrossRef
147.
Zurück zum Zitat Waring AC, Harrison S, Fink HA, Samuels MH, Cawthon PM, Zmuda JM, et al. Prospective study of thyroid function, bone loss, and fractures in older men: the MrOS study. J Bone Miner Res. 2013;28(3):472–9.PubMedPubMedCentralCrossRef Waring AC, Harrison S, Fink HA, Samuels MH, Cawthon PM, Zmuda JM, et al. Prospective study of thyroid function, bone loss, and fractures in older men: the MrOS study. J Bone Miner Res. 2013;28(3):472–9.PubMedPubMedCentralCrossRef
148.
Zurück zum Zitat Sugitani I, Fujimoto Y. Effect of postoperative thyrotropin suppressive therapy on bone mineral density in patients with papillary thyroid carcinoma: a prospective controlled study. Surgery. 2011;150(6):1250–7.PubMedCrossRef Sugitani I, Fujimoto Y. Effect of postoperative thyrotropin suppressive therapy on bone mineral density in patients with papillary thyroid carcinoma: a prospective controlled study. Surgery. 2011;150(6):1250–7.PubMedCrossRef
149.
Zurück zum Zitat Kim CW, Hong S, Oh SH, Lee JJ, Han JY, Hong S, et al. Change of bone mineral density and biochemical markers of bone turnover in patients on suppressive levothyroxine therapy for differentiated thyroid carcinoma. J Bone Metab. 2015;22(3):135–41.PubMedPubMedCentralCrossRef Kim CW, Hong S, Oh SH, Lee JJ, Han JY, Hong S, et al. Change of bone mineral density and biochemical markers of bone turnover in patients on suppressive levothyroxine therapy for differentiated thyroid carcinoma. J Bone Metab. 2015;22(3):135–41.PubMedPubMedCentralCrossRef
150.
Zurück zum Zitat Segna D, Bauer DC, Feller M, Schneider C, Fink HA, Aubert CE, et al. Association between subclinical thyroid dysfunction and change in bone mineral density in prospective cohorts. Intern Med. 2018;283(1):56–72.CrossRef Segna D, Bauer DC, Feller M, Schneider C, Fink HA, Aubert CE, et al. Association between subclinical thyroid dysfunction and change in bone mineral density in prospective cohorts. Intern Med. 2018;283(1):56–72.CrossRef
151.
Zurück zum Zitat Abrahamsen B, Jørgensen HL, Laulund AS, Nybo M, Brix TH, Hegedüs L. Low serum thyrotropin level and duration of suppression as a predictor of major osteoporotic fractures-the OPENTHYRO register cohort. J Bone Miner Res. 2014;29(9):2040–50.PubMedCrossRef Abrahamsen B, Jørgensen HL, Laulund AS, Nybo M, Brix TH, Hegedüs L. Low serum thyrotropin level and duration of suppression as a predictor of major osteoporotic fractures-the OPENTHYRO register cohort. J Bone Miner Res. 2014;29(9):2040–50.PubMedCrossRef
152.
Zurück zum Zitat Vadiveloo T, Donnan PT, Cochrane L, Leese GP. The thyroid epidemiology, audit, and research study (TEARS): morbidity in patients with endogenous subclinical hyperthyroidism. J Clin Endocrinol Metab. 2011;96(5):1344–51.PubMedCrossRef Vadiveloo T, Donnan PT, Cochrane L, Leese GP. The thyroid epidemiology, audit, and research study (TEARS): morbidity in patients with endogenous subclinical hyperthyroidism. J Clin Endocrinol Metab. 2011;96(5):1344–51.PubMedCrossRef
153.
Zurück zum Zitat Turner MR, Camacho X, Fischer HD, Austin PC, Anderson GM, Rochon PA, et al. Levothyroxine dose and risk of fractures in older adults: nested case-control study. BMJ. 2011;342(apr28 2):d2238.PubMedPubMedCentralCrossRef Turner MR, Camacho X, Fischer HD, Austin PC, Anderson GM, Rochon PA, et al. Levothyroxine dose and risk of fractures in older adults: nested case-control study. BMJ. 2011;342(apr28 2):d2238.PubMedPubMedCentralCrossRef
154.
Zurück zum Zitat Heemstra KA, Hamdy NA, Romijn JA, Smit JW. The effects of thyrotropin-suppressive therapy on bone metabolism in patients with well-differentiated thyroid carcinoma. Thyroid. 2006;16(6):583–91.PubMedCrossRef Heemstra KA, Hamdy NA, Romijn JA, Smit JW. The effects of thyrotropin-suppressive therapy on bone metabolism in patients with well-differentiated thyroid carcinoma. Thyroid. 2006;16(6):583–91.PubMedCrossRef
155.
Zurück zum Zitat Wirth CD, Blum MR, da Costa BR, Baumgartner C, Collet TH, Medici M, et al. Subclinical thyroid dysfunction and the risk for fractures: a systematic review and meta-analysis. Ann Intern Med. 2014;161(3):189–99.PubMedPubMedCentralCrossRef Wirth CD, Blum MR, da Costa BR, Baumgartner C, Collet TH, Medici M, et al. Subclinical thyroid dysfunction and the risk for fractures: a systematic review and meta-analysis. Ann Intern Med. 2014;161(3):189–99.PubMedPubMedCentralCrossRef
156.
Zurück zum Zitat Refetoff S, Weiss RE, Usala SJ. The syndromes of resistance to thyroid hormone. Endocr Rev. 1999;14(3):348–99. Refetoff S, Weiss RE, Usala SJ. The syndromes of resistance to thyroid hormone. Endocr Rev. 1999;14(3):348–99.
157.
Zurück zum Zitat Refetoff S, Dumitrescu AM. Syndromes of reduced sensitivity to thyroid hormone: genetic defects in hormone receptors, cell transporters and deiodination. Best Pract Res Clin Endocrinol Metab. 2007;21(2):277–305.PubMedCrossRef Refetoff S, Dumitrescu AM. Syndromes of reduced sensitivity to thyroid hormone: genetic defects in hormone receptors, cell transporters and deiodination. Best Pract Res Clin Endocrinol Metab. 2007;21(2):277–305.PubMedCrossRef
158.
Zurück zum Zitat Beck-Peccoz P, Chatterjee VK. The variable clinical phenotype in thyroid hormone resistance syndrome. Thyroid. 1994;4(2):225–32.PubMedCrossRef Beck-Peccoz P, Chatterjee VK. The variable clinical phenotype in thyroid hormone resistance syndrome. Thyroid. 1994;4(2):225–32.PubMedCrossRef
159.
Zurück zum Zitat Moran C, Chatterjee K. Resistance to thyroid hormone due to defective thyroid receptor alpha. Best Pract Res Clin Endocrinol Metab. 2015;29(4):647–57.PubMedPubMedCentralCrossRef Moran C, Chatterjee K. Resistance to thyroid hormone due to defective thyroid receptor alpha. Best Pract Res Clin Endocrinol Metab. 2015;29(4):647–57.PubMedPubMedCentralCrossRef
160.
Zurück zum Zitat Demir K, van Gucht AL, Büyükinan M, Çatlı G, Ayhan Y, Baş VN, et al. Diverse genotypes and phenotypes of three novel thyroid hormone receptor-α mutations. J Clin Endocrinol Metab. 2016;101(8):2945–54.PubMedCrossRef Demir K, van Gucht AL, Büyükinan M, Çatlı G, Ayhan Y, Baş VN, et al. Diverse genotypes and phenotypes of three novel thyroid hormone receptor-α mutations. J Clin Endocrinol Metab. 2016;101(8):2945–54.PubMedCrossRef
161.
Zurück zum Zitat Murphy E, Glüer CC, Reid DM, Felsenberg D, Roux C, Eastell R, et al. Thyroid function within the upper normal range is associated with reduced bone mineral density and an increased risk of nonvertebral fractures in healthy euthyroid postmenopausal women. J Clin Endocrinol Metab. 2010;95(7):3173–81.PubMedCrossRef Murphy E, Glüer CC, Reid DM, Felsenberg D, Roux C, Eastell R, et al. Thyroid function within the upper normal range is associated with reduced bone mineral density and an increased risk of nonvertebral fractures in healthy euthyroid postmenopausal women. J Clin Endocrinol Metab. 2010;95(7):3173–81.PubMedCrossRef
162.
Zurück zum Zitat Morris MS. The association between serum thyroid-stimulating hormone in its reference range and bone status in postmenopausal American women. Bone. 2007;40(4):1128–34.PubMedCrossRef Morris MS. The association between serum thyroid-stimulating hormone in its reference range and bone status in postmenopausal American women. Bone. 2007;40(4):1128–34.PubMedCrossRef
163.
Zurück zum Zitat Hwangbo Y, Kim JH, Kim SW, Park YJ, Park DJ, Kim SY, et al. High-normal free thyroxine levels are associated with low trabecular bone scores in euthyroid postmenopausal women. Osteoporos Int. 2016;27(2):457–62.PubMedCrossRef Hwangbo Y, Kim JH, Kim SW, Park YJ, Park DJ, Kim SY, et al. High-normal free thyroxine levels are associated with low trabecular bone scores in euthyroid postmenopausal women. Osteoporos Int. 2016;27(2):457–62.PubMedCrossRef
164.
Zurück zum Zitat Leader A, Ayzenfeld RH, Lishner M, Cohen E, Segev D, Hermoni D. Thyrotropin levels within the lower normal range are associated with an increased risk of hip fractures in euthyroid women, but not men, over the age of 65 years. J Clin Endocrinol Metab. 2014;99(8):2665–73.PubMedCrossRef Leader A, Ayzenfeld RH, Lishner M, Cohen E, Segev D, Hermoni D. Thyrotropin levels within the lower normal range are associated with an increased risk of hip fractures in euthyroid women, but not men, over the age of 65 years. J Clin Endocrinol Metab. 2014;99(8):2665–73.PubMedCrossRef
165.
Zurück zum Zitat Roef G, Lapauw B, Goemaere S, Zmierczak H, Fiers T, Kaufman JM, et al. Thyroid hormone status within the physiological range affects bone mass and density in healthy men at the age of peak bone mass. Eur J Endocrinol. 2011;164(6):1027–34.PubMedCrossRef Roef G, Lapauw B, Goemaere S, Zmierczak H, Fiers T, Kaufman JM, et al. Thyroid hormone status within the physiological range affects bone mass and density in healthy men at the age of peak bone mass. Eur J Endocrinol. 2011;164(6):1027–34.PubMedCrossRef
166.
Zurück zum Zitat van Rijn LE, Pop VJ, Williams GR. Low bone mineral density is related to high physiological levels of free thyroxine in peri-menopausal women. Eur J Endocrinol. 2014;170(3):461–8.PubMedCrossRef van Rijn LE, Pop VJ, Williams GR. Low bone mineral density is related to high physiological levels of free thyroxine in peri-menopausal women. Eur J Endocrinol. 2014;170(3):461–8.PubMedCrossRef
167.
Zurück zum Zitat Noh HM, Park YS, Lee J, Lee W. A cross-sectional study to examine the correlation between serum TSH levels and the osteoporosis of the lumbar spine in healthy women with normal thyroid function. Osteoporos Int. 2015;26(3):997–1003.PubMedCrossRef Noh HM, Park YS, Lee J, Lee W. A cross-sectional study to examine the correlation between serum TSH levels and the osteoporosis of the lumbar spine in healthy women with normal thyroid function. Osteoporos Int. 2015;26(3):997–1003.PubMedCrossRef
Metadaten
Titel
Skeletal Effects of Thyroid Hormones
verfasst von
Bence Bakos
Istvan Takacs
Paula H. Stern
Peter Lakatos
Publikationsdatum
24.04.2018
Verlag
Springer US
Erschienen in
Clinical & Translational Metabolism / Ausgabe 2/2018
Print ISSN: 1534-8644
Elektronische ISSN: 2948-2445
DOI
https://doi.org/10.1007/s12018-018-9246-z

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.