Skip to main content
Erschienen in: Odontology 2/2020

03.07.2019 | Review Article

Estrogen signaling impacts temporomandibular joint and periodontal disease pathology

verfasst von: Jennifer L. Robinson, Pamela M. Johnson, Karolina Kister, Michael T. Yin, Jing Chen, Sunil Wadhwa

Erschienen in: Odontology | Ausgabe 2/2020

Einloggen, um Zugang zu erhalten

Abstract

Women experience a higher incidence of oral diseases including periodontal diseases and temporomandibular joint disease (TMD) implicating the role of estrogen signaling in disease pathology. Fluctuating levels of estrogen during childbearing age potentiates facial pain, high estrogen levels during pregnancy promote gingivitis, and low levels of estrogen during menopause predisposes the TMJ to degeneration and increases alveolar bone loss. In this review, an overview of estrogen signaling pathways in vitro and in vivo that regulate pregnancy-related gingivitis, TMJ homeostasis, and alveolar bone remodeling is provided. Deciphering the specific estrogen signaling pathways for individual oral diseases is crucial for potential new drug therapies to promote and maintain healthy tissue.
Literatur
1.
Zurück zum Zitat Jin LJ, et al. Global burden of oral diseases: emerging concepts, management and interplay with systemic health. Oral Dis. 2016;22(7):609–19.PubMed Jin LJ, et al. Global burden of oral diseases: emerging concepts, management and interplay with systemic health. Oral Dis. 2016;22(7):609–19.PubMed
2.
Zurück zum Zitat Kessler JL. A literature review on women’s oral health across the life span. Nurs Womens Health. 2017;21(2):108–21.PubMed Kessler JL. A literature review on women’s oral health across the life span. Nurs Womens Health. 2017;21(2):108–21.PubMed
3.
Zurück zum Zitat Bueno CH, et al. Gender differences in temporomandibular disorders in adult populational studies: a systematic review and meta-analysis. J Oral Rehabil. 2018;45(9):720–9.PubMed Bueno CH, et al. Gender differences in temporomandibular disorders in adult populational studies: a systematic review and meta-analysis. J Oral Rehabil. 2018;45(9):720–9.PubMed
4.
Zurück zum Zitat Cauley JA. Estrogen and bone health in men and women. Steroids. 2015;99(Pt A):11–5.PubMed Cauley JA. Estrogen and bone health in men and women. Steroids. 2015;99(Pt A):11–5.PubMed
5.
Zurück zum Zitat Chidi-Ogbolu N, Baar K. Effect of estrogen on musculoskeletal performance and injury risk. Front Physiol. 2018;9:1834.PubMed Chidi-Ogbolu N, Baar K. Effect of estrogen on musculoskeletal performance and injury risk. Front Physiol. 2018;9:1834.PubMed
6.
Zurück zum Zitat Ohrbach R, et al. Clinical findings and pain symptoms as potential risk factors for chronic TMD: descriptive data and empirically identified domains from the OPPERA case-control study. J Pain. 2011;12(11 Suppl):27–45. Ohrbach R, et al. Clinical findings and pain symptoms as potential risk factors for chronic TMD: descriptive data and empirically identified domains from the OPPERA case-control study. J Pain. 2011;12(11 Suppl):27–45.
7.
Zurück zum Zitat Manfredini D, et al. Research diagnostic criteria for temporomandibular disorders: a systematic review of axis I epidemiologic findings. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;112(4):453–62.PubMed Manfredini D, et al. Research diagnostic criteria for temporomandibular disorders: a systematic review of axis I epidemiologic findings. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;112(4):453–62.PubMed
8.
Zurück zum Zitat LeResche L. Epidemiology of temporomandibular disorders: implications for the investigation of etiologic factors. Crit Rev Oral Biol Med. 1997;8(3):291–305.PubMed LeResche L. Epidemiology of temporomandibular disorders: implications for the investigation of etiologic factors. Crit Rev Oral Biol Med. 1997;8(3):291–305.PubMed
9.
Zurück zum Zitat LeResche L, et al. Use of exogenous hormones and risk of temporomandibular disorder pain. Pain. 1997;69(1–2):153–60.PubMed LeResche L, et al. Use of exogenous hormones and risk of temporomandibular disorder pain. Pain. 1997;69(1–2):153–60.PubMed
10.
Zurück zum Zitat Warren MP, Fried JL. Temporomandibular disorders and hormones in women. Cells Tissues Organs. 2001;169(3):187–92.PubMed Warren MP, Fried JL. Temporomandibular disorders and hormones in women. Cells Tissues Organs. 2001;169(3):187–92.PubMed
11.
Zurück zum Zitat Slade GD, et al. Signs and symptoms of first-onset TMD and sociodemographic predictors of its development: the OPPERA prospective cohort study. J Pain. 2013;14(12 Suppl):T20.e1-3–32.e1-3. Slade GD, et al. Signs and symptoms of first-onset TMD and sociodemographic predictors of its development: the OPPERA prospective cohort study. J Pain. 2013;14(12 Suppl):T20.e1-3–32.e1-3.
12.
Zurück zum Zitat Slade GD, et al. Painful temporomandibular disorder: decade of discovery from OPPERA studies. J Dent Res. 2016;95(10):1084–92.PubMedPubMedCentral Slade GD, et al. Painful temporomandibular disorder: decade of discovery from OPPERA studies. J Dent Res. 2016;95(10):1084–92.PubMedPubMedCentral
13.
Zurück zum Zitat Macfarlane TV, et al. Oro-facial pain in the community: prevalence and associated impact. Commun Dent Oral Epidemiol. 2002;30(1):52–60. Macfarlane TV, et al. Oro-facial pain in the community: prevalence and associated impact. Commun Dent Oral Epidemiol. 2002;30(1):52–60.
14.
Zurück zum Zitat Lovgren A, et al. Temporomandibular pain and jaw dysfunction at different ages covering the lifespan—a population based study. Eur J Pain. 2016;20(4):532–40.PubMed Lovgren A, et al. Temporomandibular pain and jaw dysfunction at different ages covering the lifespan—a population based study. Eur J Pain. 2016;20(4):532–40.PubMed
15.
Zurück zum Zitat Maixner W, et al. Overlapping chronic pain conditions: implications for diagnosis and classification. J Pain. 2016;17(9 Suppl):T93–107.PubMedPubMedCentral Maixner W, et al. Overlapping chronic pain conditions: implications for diagnosis and classification. J Pain. 2016;17(9 Suppl):T93–107.PubMedPubMedCentral
16.
Zurück zum Zitat Schiffman E, et al. Diagnostic criteria for temporomandibular disorders (DC/TMD) for clinical and research applications: recommendations of the international RDC/TMD Consortium Network* and Orofacial Pain Special Interest Groupdagger. J Oral Facial Pain Headache. 2014;28(1):6–27.PubMedPubMedCentral Schiffman E, et al. Diagnostic criteria for temporomandibular disorders (DC/TMD) for clinical and research applications: recommendations of the international RDC/TMD Consortium Network* and Orofacial Pain Special Interest Groupdagger. J Oral Facial Pain Headache. 2014;28(1):6–27.PubMedPubMedCentral
17.
Zurück zum Zitat Guarda-Nardini L, et al. Age-related differences in temporomandibular disorder diagnoses. Cranio. 2012;30(2):103–9.PubMed Guarda-Nardini L, et al. Age-related differences in temporomandibular disorder diagnoses. Cranio. 2012;30(2):103–9.PubMed
18.
Zurück zum Zitat Back K, et al. Relation between osteoporosis and radiographic and clinical signs of osteoarthritis/arthrosis in the temporomandibular joint: a population-based, cross-sectional study in an older Swedish population. Gerodontology. 2017;34(2):187–94.PubMed Back K, et al. Relation between osteoporosis and radiographic and clinical signs of osteoarthritis/arthrosis in the temporomandibular joint: a population-based, cross-sectional study in an older Swedish population. Gerodontology. 2017;34(2):187–94.PubMed
19.
Zurück zum Zitat Jagur O, et al. Relationship between radiographic changes in the temporomandibular joint and bone mineral density: a population based study. Stomatologija. 2011;13(2):42–8.PubMed Jagur O, et al. Relationship between radiographic changes in the temporomandibular joint and bone mineral density: a population based study. Stomatologija. 2011;13(2):42–8.PubMed
20.
Zurück zum Zitat Dervis E. Oral implications of osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2005;100(3):349–56.PubMed Dervis E. Oral implications of osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2005;100(3):349–56.PubMed
21.
Zurück zum Zitat Brett KM, Madans JH. Use of postmenopausal hormone replacement therapy: estimates from a nationally representative cohort study. Am J Epidemiol. 1997;145(6):536–45.PubMed Brett KM, Madans JH. Use of postmenopausal hormone replacement therapy: estimates from a nationally representative cohort study. Am J Epidemiol. 1997;145(6):536–45.PubMed
22.
Zurück zum Zitat Martin MD, et al. Intubation risk factors for temporomandibular joint/facial pain. Anesth Prog. 2007;54(3):109–14.PubMedPubMedCentral Martin MD, et al. Intubation risk factors for temporomandibular joint/facial pain. Anesth Prog. 2007;54(3):109–14.PubMedPubMedCentral
23.
Zurück zum Zitat Lora VR, et al. Prevalence of temporomandibular disorders in postmenopausal women and relationship with pain and HRT. Braz Oral Res. 2016;30(1):e100.PubMed Lora VR, et al. Prevalence of temporomandibular disorders in postmenopausal women and relationship with pain and HRT. Braz Oral Res. 2016;30(1):e100.PubMed
24.
Zurück zum Zitat Nekora-Azak A, et al. Estrogen replacement therapy among postmenopausal women and its effects on signs and symptoms of temporomandibular disorders. Cranio. 2008;26(3):211–5.PubMed Nekora-Azak A, et al. Estrogen replacement therapy among postmenopausal women and its effects on signs and symptoms of temporomandibular disorders. Cranio. 2008;26(3):211–5.PubMed
25.
Zurück zum Zitat Hatch JP, et al. Is use of exogenous estrogen associated with temporomandibular signs and symptoms? J Am Dent Assoc. 2001;132(3):319–26.PubMed Hatch JP, et al. Is use of exogenous estrogen associated with temporomandibular signs and symptoms? J Am Dent Assoc. 2001;132(3):319–26.PubMed
26.
Zurück zum Zitat Mayoral VA, Espinosa IA, Montiel AJ. Association between signs and symptoms of temporomandibular disorders and pregnancy (case control study). Acta Odontol Latinoam. 2013;26(1):3–7.PubMed Mayoral VA, Espinosa IA, Montiel AJ. Association between signs and symptoms of temporomandibular disorders and pregnancy (case control study). Acta Odontol Latinoam. 2013;26(1):3–7.PubMed
27.
Zurück zum Zitat Ivković N, et al. Relationship between symptoms of temporomandibular disorders and estrogen levels in women with different menstrual status. J Oral Facial Pain Headache. 2018;32(2):151–8.PubMed Ivković N, et al. Relationship between symptoms of temporomandibular disorders and estrogen levels in women with different menstrual status. J Oral Facial Pain Headache. 2018;32(2):151–8.PubMed
28.
Zurück zum Zitat LeResche L, et al. Musculoskeletal orofacial pain and other signs and symptoms of temporomandibular disorders during pregnancy: a prospective study. J Orofac Pain. 2005;19(3):193–201.PubMed LeResche L, et al. Musculoskeletal orofacial pain and other signs and symptoms of temporomandibular disorders during pregnancy: a prospective study. J Orofac Pain. 2005;19(3):193–201.PubMed
29.
Zurück zum Zitat Turner JA, et al. Targeting temporomandibular disorder pain treatment to hormonal fluctuations: a randomized clinical trial. Pain. 2011;152(9):2074–84.PubMedPubMedCentral Turner JA, et al. Targeting temporomandibular disorder pain treatment to hormonal fluctuations: a randomized clinical trial. Pain. 2011;152(9):2074–84.PubMedPubMedCentral
30.
Zurück zum Zitat Almarza AJ, et al. Preclinical animal models for temporomandibular joint tissue engineering. Tissue Eng Part B Rev. 2018;24(3):171–8.PubMedPubMedCentral Almarza AJ, et al. Preclinical animal models for temporomandibular joint tissue engineering. Tissue Eng Part B Rev. 2018;24(3):171–8.PubMedPubMedCentral
31.
Zurück zum Zitat Juran CM, Dolwick MF, McFetridge PS. Engineered microporosity: enhancing the early regenerative potential of decellularized temporomandibular joint discs. Tissue Eng Part A. 2015;21(3–4):829–39.PubMedPubMedCentral Juran CM, Dolwick MF, McFetridge PS. Engineered microporosity: enhancing the early regenerative potential of decellularized temporomandibular joint discs. Tissue Eng Part A. 2015;21(3–4):829–39.PubMedPubMedCentral
32.
Zurück zum Zitat Rees L. The structure and function of the mandibular joint. Br Dent J. 1954;96(6):125–33. Rees L. The structure and function of the mandibular joint. Br Dent J. 1954;96(6):125–33.
33.
Zurück zum Zitat Nakano T, Scott PG. Changes in the chemical composition of the bovine temporomandibular joint disc with age. Arch Oral Biol. 1996;41(8–9):845–53.PubMed Nakano T, Scott PG. Changes in the chemical composition of the bovine temporomandibular joint disc with age. Arch Oral Biol. 1996;41(8–9):845–53.PubMed
34.
Zurück zum Zitat Almarza AJ, et al. Biochemical analysis of the porcine temporomandibular joint disc. Br J Oral Maxillofac Surg. 2006;44(2):124–8.PubMed Almarza AJ, et al. Biochemical analysis of the porcine temporomandibular joint disc. Br J Oral Maxillofac Surg. 2006;44(2):124–8.PubMed
35.
Zurück zum Zitat Shengyi T, Xu Y. Biomechanical properties and collagen fiber orientation of TMJ discs in dogs: part 1. Gross anatomy and collagen fiber orientation of the discs. J Craniomandib Disord Facial Oral Pain. 1991;5(1):28–34. Shengyi T, Xu Y. Biomechanical properties and collagen fiber orientation of TMJ discs in dogs: part 1. Gross anatomy and collagen fiber orientation of the discs. J Craniomandib Disord Facial Oral Pain. 1991;5(1):28–34.
36.
Zurück zum Zitat Minarelli AM, Del Santo JM, Liberti EA. The structure of the human temporomandibular joint disc: a scanning electron microscopy study. J Orofac Pain. 1997;11(2):95–100.PubMed Minarelli AM, Del Santo JM, Liberti EA. The structure of the human temporomandibular joint disc: a scanning electron microscopy study. J Orofac Pain. 1997;11(2):95–100.PubMed
37.
Zurück zum Zitat Nakano T, Scott PG. A quantitative chemical study of glycosaminoglycans in the articular disc of the bovine temporomandibular joint. Arch Oral Biol. 1989;34(9):749–57.PubMed Nakano T, Scott PG. A quantitative chemical study of glycosaminoglycans in the articular disc of the bovine temporomandibular joint. Arch Oral Biol. 1989;34(9):749–57.PubMed
38.
Zurück zum Zitat Detamore MS, et al. Quantitative analysis and comparative regional investigation of the extracellular matrix of the porcine temporomandibular joint disc. Matrix Biol. 2005;24(1):45–57.PubMedPubMedCentral Detamore MS, et al. Quantitative analysis and comparative regional investigation of the extracellular matrix of the porcine temporomandibular joint disc. Matrix Biol. 2005;24(1):45–57.PubMedPubMedCentral
39.
Zurück zum Zitat Axelsson S, Holmlund A, Hjerpe A. Glycosaminoglycans in normal and osteoarthrotic human temporomandibular joint disks. Acta Odontol Scand. 1992;50(2):113–9.PubMed Axelsson S, Holmlund A, Hjerpe A. Glycosaminoglycans in normal and osteoarthrotic human temporomandibular joint disks. Acta Odontol Scand. 1992;50(2):113–9.PubMed
40.
Zurück zum Zitat Allen KD, Athanasiou KA. Tissue engineering of the TMJ disc: a review. Tissue Eng. 2006;12(5):1183–96.PubMed Allen KD, Athanasiou KA. Tissue engineering of the TMJ disc: a review. Tissue Eng. 2006;12(5):1183–96.PubMed
41.
Zurück zum Zitat Detamore MS, et al. Cell type and distribution in the porcine temporomandibular joint disc. J Oral Maxillofac Surg. 2006;64(2):243–8.PubMedPubMedCentral Detamore MS, et al. Cell type and distribution in the porcine temporomandibular joint disc. J Oral Maxillofac Surg. 2006;64(2):243–8.PubMedPubMedCentral
42.
Zurück zum Zitat Wright GJ, et al. Tensile biomechanical properties of human temporomandibular joint disc: effects of direction, region and sex. J Biomech. 2016;49(16):3762–9.PubMedPubMedCentral Wright GJ, et al. Tensile biomechanical properties of human temporomandibular joint disc: effects of direction, region and sex. J Biomech. 2016;49(16):3762–9.PubMedPubMedCentral
43.
Zurück zum Zitat Wright GJ, et al. Electrical conductivity method to determine sexual dimorphisms in human temporomandibular disc fixed charge density. Ann Biomed Eng. 2018;46(2):310–7.PubMed Wright GJ, et al. Electrical conductivity method to determine sexual dimorphisms in human temporomandibular disc fixed charge density. Ann Biomed Eng. 2018;46(2):310–7.PubMed
44.
Zurück zum Zitat Wadhwa S, Kapila S. TMJ disorders: future innovations in diagnostics and therapeutics. J Dent Educ. 2008;72(8):930–47.PubMedPubMedCentral Wadhwa S, Kapila S. TMJ disorders: future innovations in diagnostics and therapeutics. J Dent Educ. 2008;72(8):930–47.PubMedPubMedCentral
45.
Zurück zum Zitat Jing Y, et al. Chondrocytes directly transform into bone cells in mandibular condyle growth. J Dent Res. 2015;94(12):1668–75.PubMedPubMedCentral Jing Y, et al. Chondrocytes directly transform into bone cells in mandibular condyle growth. J Dent Res. 2015;94(12):1668–75.PubMedPubMedCentral
46.
Zurück zum Zitat Luder HU. Age changes in the articular tissue of human mandibular condyles from adolescence to old age: a semiquantitative light microscopic study. Anat Rec. 1998;251(4):439–47.PubMed Luder HU. Age changes in the articular tissue of human mandibular condyles from adolescence to old age: a semiquantitative light microscopic study. Anat Rec. 1998;251(4):439–47.PubMed
47.
Zurück zum Zitat Gepstein A, et al. Association of metalloproteinases, tissue inhibitors of matrix metalloproteinases, and proteoglycans with development, aging, and osteoarthritis processes in mouse temporomandibular joint. Histochem Cell Biol. 2003;120(1):23–32.PubMed Gepstein A, et al. Association of metalloproteinases, tissue inhibitors of matrix metalloproteinases, and proteoglycans with development, aging, and osteoarthritis processes in mouse temporomandibular joint. Histochem Cell Biol. 2003;120(1):23–32.PubMed
48.
Zurück zum Zitat Silbermann M, Livne E. Age-related degenerative changes in the mouse mandibular joint. J Anat. 1979;129(Pt 3):507–20.PubMedPubMedCentral Silbermann M, Livne E. Age-related degenerative changes in the mouse mandibular joint. J Anat. 1979;129(Pt 3):507–20.PubMedPubMedCentral
49.
Zurück zum Zitat McDaniel JS, et al. Transcriptional regulation of proteoglycan 4 by 17beta-estradiol in immortalized baboon temporomandibular joint disc cells. Eur J Oral Sci. 2014;122(2):100–8.PubMedPubMedCentral McDaniel JS, et al. Transcriptional regulation of proteoglycan 4 by 17beta-estradiol in immortalized baboon temporomandibular joint disc cells. Eur J Oral Sci. 2014;122(2):100–8.PubMedPubMedCentral
50.
Zurück zum Zitat Kapila S, Xie Y. Targeted induction of collagenase and stromelysin by relaxin in unprimed and beta-estradiol-primed diarthrodial joint fibrocartilaginous cells but not in synoviocytes. Lab Invest. 1998;78(8):925–38.PubMed Kapila S, Xie Y. Targeted induction of collagenase and stromelysin by relaxin in unprimed and beta-estradiol-primed diarthrodial joint fibrocartilaginous cells but not in synoviocytes. Lab Invest. 1998;78(8):925–38.PubMed
51.
Zurück zum Zitat Naqvi T, et al. Relaxin’s induction of metalloproteinases is associated with the loss of collagen and glycosaminoglycans in synovial joint fibrocartilaginous explants. Arthritis Res Ther. 2005;7(1):R1–11.PubMed Naqvi T, et al. Relaxin’s induction of metalloproteinases is associated with the loss of collagen and glycosaminoglycans in synovial joint fibrocartilaginous explants. Arthritis Res Ther. 2005;7(1):R1–11.PubMed
52.
Zurück zum Zitat Hashem G, et al. Relaxin and beta-estradiol modulate targeted matrix degradation in specific synovial joint fibrocartilages: progesterone prevents matrix loss. Arthritis Res Ther. 2006;8(4):R98.PubMedPubMedCentral Hashem G, et al. Relaxin and beta-estradiol modulate targeted matrix degradation in specific synovial joint fibrocartilages: progesterone prevents matrix loss. Arthritis Res Ther. 2006;8(4):R98.PubMedPubMedCentral
53.
Zurück zum Zitat Talwar RM, et al. Effects of estrogen on chondrocyte proliferation and collagen synthesis in skeletally mature articular cartilage. J Oral Maxillofac Surg. 2006;64(4):600–9.PubMed Talwar RM, et al. Effects of estrogen on chondrocyte proliferation and collagen synthesis in skeletally mature articular cartilage. J Oral Maxillofac Surg. 2006;64(4):600–9.PubMed
54.
Zurück zum Zitat Cheng P, et al. Effects of estradiol on proliferation and metabolism of rabbit mandibular condylar cartilage cells in vitro. Chin Med J (Engl). 2003;116(9):1413–7. Cheng P, et al. Effects of estradiol on proliferation and metabolism of rabbit mandibular condylar cartilage cells in vitro. Chin Med J (Engl). 2003;116(9):1413–7.
55.
Zurück zum Zitat Yasuoka T, et al. Effect of estrogen replacement on temporomandibular joint remodeling in ovariectomized rats. J Oral Maxillofac Surg. 2000;58(2):189–96.PubMed Yasuoka T, et al. Effect of estrogen replacement on temporomandibular joint remodeling in ovariectomized rats. J Oral Maxillofac Surg. 2000;58(2):189–96.PubMed
56.
Zurück zum Zitat Chen J, et al. Estrogen via estrogen receptor beta partially inhibits mandibular condylar cartilage growth. Osteoarthr Cartil. 2014;22(11):1861–8.PubMedPubMedCentral Chen J, et al. Estrogen via estrogen receptor beta partially inhibits mandibular condylar cartilage growth. Osteoarthr Cartil. 2014;22(11):1861–8.PubMedPubMedCentral
57.
Zurück zum Zitat Robinson JL, et al. Estrogen promotes mandibular condylar fibrocartilage chondrogenesis and inhibits degeneration via estrogen receptor alpha in female mice. Sci Rep. 2018;8(1):8527.PubMedPubMedCentral Robinson JL, et al. Estrogen promotes mandibular condylar fibrocartilage chondrogenesis and inhibits degeneration via estrogen receptor alpha in female mice. Sci Rep. 2018;8(1):8527.PubMedPubMedCentral
58.
Zurück zum Zitat Figueroba SR, et al. Dependence of cytokine levels on the sex of experimental animals: a pilot study on the effect of oestrogen in the temporomandibular joint synovial tissues. Int J Oral Maxillofac Surg. 2015;44(11):1368–75.PubMed Figueroba SR, et al. Dependence of cytokine levels on the sex of experimental animals: a pilot study on the effect of oestrogen in the temporomandibular joint synovial tissues. Int J Oral Maxillofac Surg. 2015;44(11):1368–75.PubMed
59.
Zurück zum Zitat Grogan SP, et al. Relevance of meniscal cell regional phenotype to tissue engineering. Connect Tissue Res. 2017;58(3–4):259–70.PubMed Grogan SP, et al. Relevance of meniscal cell regional phenotype to tissue engineering. Connect Tissue Res. 2017;58(3–4):259–70.PubMed
60.
Zurück zum Zitat Gunja NJ, Athanasiou KA. Passage and reversal effects on gene expression of bovine meniscal fibrochondrocytes. Arthritis Res Ther. 2007;9(5):R93.PubMedPubMedCentral Gunja NJ, Athanasiou KA. Passage and reversal effects on gene expression of bovine meniscal fibrochondrocytes. Arthritis Res Ther. 2007;9(5):R93.PubMedPubMedCentral
61.
Zurück zum Zitat Beato M, Herrlich P, Schutz G. Steroid hormone receptors: many actors in search of a plot. Cell. 1995;83(6):851–7.PubMed Beato M, Herrlich P, Schutz G. Steroid hormone receptors: many actors in search of a plot. Cell. 1995;83(6):851–7.PubMed
62.
Zurück zum Zitat Marino M, Galluzzo P, Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr Genomics. 2006;7(8):497–508.PubMedPubMedCentral Marino M, Galluzzo P, Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr Genomics. 2006;7(8):497–508.PubMedPubMedCentral
63.
64.
Zurück zum Zitat Manolagas SC, Kousteni S. Perspective: nonreproductive sites of action of reproductive hormones. Endocrinology. 2001;142(6):2200–4.PubMed Manolagas SC, Kousteni S. Perspective: nonreproductive sites of action of reproductive hormones. Endocrinology. 2001;142(6):2200–4.PubMed
65.
Zurück zum Zitat Milam SB, et al. Sexual dimorphism in the distribution of estrogen receptors in the temporomandibular joint complex of the baboon. Oral Surg Oral Med Oral Pathol. 1987;64(5):527–32.PubMed Milam SB, et al. Sexual dimorphism in the distribution of estrogen receptors in the temporomandibular joint complex of the baboon. Oral Surg Oral Med Oral Pathol. 1987;64(5):527–32.PubMed
66.
Zurück zum Zitat Wang W, Hayami T, Kapila S. Female hormone receptors are differentially expressed in mouse fibrocartilages. Osteoarthr Cartil. 2009;17(5):646–54.PubMed Wang W, Hayami T, Kapila S. Female hormone receptors are differentially expressed in mouse fibrocartilages. Osteoarthr Cartil. 2009;17(5):646–54.PubMed
67.
Zurück zum Zitat Yu SB, et al. The effects of age and sex on the expression of oestrogen and its receptors in rat mandibular condylar cartilages. Arch Oral Biol. 2009;54(5):479–85.PubMed Yu SB, et al. The effects of age and sex on the expression of oestrogen and its receptors in rat mandibular condylar cartilages. Arch Oral Biol. 2009;54(5):479–85.PubMed
68.
Zurück zum Zitat Ahmad N, et al. 17beta-estradiol induces MMP-9 and MMP-13 in TMJ fibrochondrocytes via estrogen receptor alpha. J Dent Res. 2018;97(9):1023–30.PubMedPubMedCentral Ahmad N, et al. 17beta-estradiol induces MMP-9 and MMP-13 in TMJ fibrochondrocytes via estrogen receptor alpha. J Dent Res. 2018;97(9):1023–30.PubMedPubMedCentral
69.
Zurück zum Zitat Robinson JL, et al. Estrogen receptor alpha mediates mandibular condylar cartilage growth in male mice. Orthod Craniofac Res. 2017;20(Suppl 1):167–71.PubMedPubMedCentral Robinson JL, et al. Estrogen receptor alpha mediates mandibular condylar cartilage growth in male mice. Orthod Craniofac Res. 2017;20(Suppl 1):167–71.PubMedPubMedCentral
70.
Zurück zum Zitat Vinel A, et al. Respective role of membrane and nuclear estrogen receptor (ER) α in the mandible of growing mice: implications for ERα modulation. J Bone Miner Res. 2018;33(8):1520–31.PubMedPubMedCentral Vinel A, et al. Respective role of membrane and nuclear estrogen receptor (ER) α in the mandible of growing mice: implications for ERα modulation. J Bone Miner Res. 2018;33(8):1520–31.PubMedPubMedCentral
71.
Zurück zum Zitat Kamiya Y, et al. Increased mandibular condylar growth in mice with estrogen receptor beta deficiency. J Bone Miner Res. 2013;28(5):1127–34.PubMed Kamiya Y, et al. Increased mandibular condylar growth in mice with estrogen receptor beta deficiency. J Bone Miner Res. 2013;28(5):1127–34.PubMed
72.
Zurück zum Zitat Robinson JL, et al. Sex differences in the estrogen-dependent regulation of temporomandibular joint remodeling in altered loading. Osteoarthr Cartil. 2017;25(4):533–43.PubMed Robinson JL, et al. Sex differences in the estrogen-dependent regulation of temporomandibular joint remodeling in altered loading. Osteoarthr Cartil. 2017;25(4):533–43.PubMed
73.
Zurück zum Zitat Ye T, et al. Differential effects of high-physiological oestrogen on the degeneration of mandibular condylar cartilage and subchondral bone. Bone. 2018;111:9–22.PubMed Ye T, et al. Differential effects of high-physiological oestrogen on the degeneration of mandibular condylar cartilage and subchondral bone. Bone. 2018;111:9–22.PubMed
74.
Zurück zum Zitat Torres-Chavez KE, et al. Sexual dimorphism on cytokines expression in the temporomandibular joint: the role of gonadal steroid hormones. Inflammation. 2011;34(5):487–98.PubMed Torres-Chavez KE, et al. Sexual dimorphism on cytokines expression in the temporomandibular joint: the role of gonadal steroid hormones. Inflammation. 2011;34(5):487–98.PubMed
75.
Zurück zum Zitat Wang XD, et al. Estrogen aggravates iodoacetate-induced temporomandibular joint osteoarthritis. J Dent Res. 2013;92(10):918–24.PubMed Wang XD, et al. Estrogen aggravates iodoacetate-induced temporomandibular joint osteoarthritis. J Dent Res. 2013;92(10):918–24.PubMed
76.
Zurück zum Zitat Xue XT, et al. Sexual dimorphism of estrogen-sensitized synoviocytes contributes to gender difference in temporomandibular joint osteoarthritis. Oral Dis. 2018;24(8):1503–13.PubMed Xue XT, et al. Sexual dimorphism of estrogen-sensitized synoviocytes contributes to gender difference in temporomandibular joint osteoarthritis. Oral Dis. 2018;24(8):1503–13.PubMed
77.
Zurück zum Zitat Okuda T, et al. The effect of ovariectomy on the temporomandibular joints of growing rats. J Oral Maxillofac Surg. 1996;54(10):1201–10.PubMed Okuda T, et al. The effect of ovariectomy on the temporomandibular joints of growing rats. J Oral Maxillofac Surg. 1996;54(10):1201–10.PubMed
78.
Zurück zum Zitat Vetvik KG, MacGregor EA. Sex differences in the epidemiology, clinical features, and pathophysiology of migraine. Lancet Neurol. 2017;16(1):76–87.PubMed Vetvik KG, MacGregor EA. Sex differences in the epidemiology, clinical features, and pathophysiology of migraine. Lancet Neurol. 2017;16(1):76–87.PubMed
79.
80.
Zurück zum Zitat Kim K, Wojczynska A, Lee JY. The incidence of osteoarthritic change on computed tomography of Korean temporomandibular disorder patients diagnosed by RDC/TMD; a retrospective study. Acta Odontol Scand. 2016;74(5):337–42.PubMed Kim K, Wojczynska A, Lee JY. The incidence of osteoarthritic change on computed tomography of Korean temporomandibular disorder patients diagnosed by RDC/TMD; a retrospective study. Acta Odontol Scand. 2016;74(5):337–42.PubMed
81.
Zurück zum Zitat Alexiou K, Stamatakis H, Tsiklakis K. Evaluation of the severity of temporomandibular joint osteoarthritic changes related to age using cone beam computed tomography. Dentomaxillofac Radiol. 2009;38(3):141–7.PubMed Alexiou K, Stamatakis H, Tsiklakis K. Evaluation of the severity of temporomandibular joint osteoarthritic changes related to age using cone beam computed tomography. Dentomaxillofac Radiol. 2009;38(3):141–7.PubMed
82.
Zurück zum Zitat Agerberg G, Bergenholtz A. Craniomandibular disorders in adult populations of West Bothnia, Sweden. Acta Odontol Scand. 1989;47(3):129–40.PubMed Agerberg G, Bergenholtz A. Craniomandibular disorders in adult populations of West Bothnia, Sweden. Acta Odontol Scand. 1989;47(3):129–40.PubMed
83.
Zurück zum Zitat Lindberg MK, et al. Estrogen receptor specificity for the effects of estrogen in ovariectomized mice. J Endocrinol. 2002;174(2):167–78.PubMed Lindberg MK, et al. Estrogen receptor specificity for the effects of estrogen in ovariectomized mice. J Endocrinol. 2002;174(2):167–78.PubMed
84.
Zurück zum Zitat Wang S, et al. Identification of α2-macroglobulin as a master inhibitor of cartilage-degrading factors that attenuates the progression of posttraumatic osteoarthritis. Arthritis Rheum. 2014;66(7):1843–53. Wang S, et al. Identification of α2-macroglobulin as a master inhibitor of cartilage-degrading factors that attenuates the progression of posttraumatic osteoarthritis. Arthritis Rheum. 2014;66(7):1843–53.
85.
Zurück zum Zitat Herber CB, et al. Estrogen signaling in arcuate Kiss1 neurons suppresses a sex-dependent female circuit promoting dense strong bones. Nat Commun. 2019;10(1):163.PubMedPubMedCentral Herber CB, et al. Estrogen signaling in arcuate Kiss1 neurons suppresses a sex-dependent female circuit promoting dense strong bones. Nat Commun. 2019;10(1):163.PubMedPubMedCentral
86.
Zurück zum Zitat Coogan JS, et al. Determination of sex differences of human cadaveric mandibular condyles using statistical shape and trait modeling. Bone. 2018;106:35–41.PubMed Coogan JS, et al. Determination of sex differences of human cadaveric mandibular condyles using statistical shape and trait modeling. Bone. 2018;106:35–41.PubMed
87.
Zurück zum Zitat Kim DG, et al. Sex dependent mechanical properties of the human mandibular condyle. J Mech Behav Biomed Mater. 2017;71:184–91.PubMed Kim DG, et al. Sex dependent mechanical properties of the human mandibular condyle. J Mech Behav Biomed Mater. 2017;71:184–91.PubMed
88.
89.
Zurück zum Zitat Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366(9499):1809–20.PubMed Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366(9499):1809–20.PubMed
90.
Zurück zum Zitat Armitage GC. Periodontal diagnoses and classification of periodontal diseases. Periodontol. 2000;2004(34):9–21. Armitage GC. Periodontal diagnoses and classification of periodontal diseases. Periodontol. 2000;2004(34):9–21.
91.
Zurück zum Zitat Figuero E, et al. Effect of pregnancy on gingival inflammation in systemically healthy women: a systematic review. J Clin Periodontol. 2013;40(5):457–73.PubMed Figuero E, et al. Effect of pregnancy on gingival inflammation in systemically healthy women: a systematic review. J Clin Periodontol. 2013;40(5):457–73.PubMed
92.
Zurück zum Zitat Ali I, et al. Oral health and oral contraceptive—is it a shadow behind broad day light? A systematic review. J Clin Diagn Res. 2016;10(11):ZE01–6.PubMedPubMedCentral Ali I, et al. Oral health and oral contraceptive—is it a shadow behind broad day light? A systematic review. J Clin Diagn Res. 2016;10(11):ZE01–6.PubMedPubMedCentral
93.
Zurück zum Zitat Socransky SS, et al. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25(2):134–44.PubMed Socransky SS, et al. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25(2):134–44.PubMed
94.
Zurück zum Zitat Hajishengallis G, Lamont RJ. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol. 2012;27(6):409–19.PubMedPubMedCentral Hajishengallis G, Lamont RJ. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol. 2012;27(6):409–19.PubMedPubMedCentral
95.
Zurück zum Zitat Kumar PS. Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria? Periodontol 2000. 2013;61(1):103–24.PubMed Kumar PS. Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria? Periodontol 2000. 2013;61(1):103–24.PubMed
96.
Zurück zum Zitat Wu M, Chen SW, Jiang SY. Relationship between gingival inflammation and pregnancy. Mediat Inflamm. 2015;2015:623427. Wu M, Chen SW, Jiang SY. Relationship between gingival inflammation and pregnancy. Mediat Inflamm. 2015;2015:623427.
98.
Zurück zum Zitat Balan P, et al. Keystone species in pregnancy gingivitis: a snapshot of oral microbiome during pregnancy and postpartum period. Front Microbiol. 2018;9:2360.PubMedPubMedCentral Balan P, et al. Keystone species in pregnancy gingivitis: a snapshot of oral microbiome during pregnancy and postpartum period. Front Microbiol. 2018;9:2360.PubMedPubMedCentral
99.
Zurück zum Zitat Mor G, Cardenas I. The immune system in pregnancy: a unique complexity. Am J Reprod Immunol. 2010;63(6):425–33.PubMedPubMedCentral Mor G, Cardenas I. The immune system in pregnancy: a unique complexity. Am J Reprod Immunol. 2010;63(6):425–33.PubMedPubMedCentral
100.
Zurück zum Zitat Kovats S. Estrogen receptors regulate innate immune cells and signaling pathways. Cell Immunol. 2015;294(2):63–9.PubMedPubMedCentral Kovats S. Estrogen receptors regulate innate immune cells and signaling pathways. Cell Immunol. 2015;294(2):63–9.PubMedPubMedCentral
101.
Zurück zum Zitat Wu M, et al. Sex hormones enhance gingival inflammation without affecting IL-1β and TNF-α in periodontally healthy women during pregnancy. Mediat Inflamm. 2016;2016:4897890. Wu M, et al. Sex hormones enhance gingival inflammation without affecting IL-1β and TNF-α in periodontally healthy women during pregnancy. Mediat Inflamm. 2016;2016:4897890.
102.
Zurück zum Zitat Bieri RA, et al. Gingival fluid cytokine expression and subgingival bacterial counts during pregnancy and postpartum: a case series. Clin Oral Investig. 2013;17(1):19–28.PubMed Bieri RA, et al. Gingival fluid cytokine expression and subgingival bacterial counts during pregnancy and postpartum: a case series. Clin Oral Investig. 2013;17(1):19–28.PubMed
103.
Zurück zum Zitat LaMonte MJ, et al. Five-year changes in periodontal disease measures among postmenopausal females: the Buffalo Osteoperio study. J Periodontol. 2013;84(5):572–84.PubMed LaMonte MJ, et al. Five-year changes in periodontal disease measures among postmenopausal females: the Buffalo Osteoperio study. J Periodontol. 2013;84(5):572–84.PubMed
105.
Zurück zum Zitat Wang Y, et al. Association of serum 17beta-estradiol concentration, hormone therapy, and alveolar crest height in postmenopausal women. J Periodontol. 2015;86(4):595–605.PubMedPubMedCentral Wang Y, et al. Association of serum 17beta-estradiol concentration, hormone therapy, and alveolar crest height in postmenopausal women. J Periodontol. 2015;86(4):595–605.PubMedPubMedCentral
106.
Zurück zum Zitat Ucer S, et al. The effects of aging and sex steroid deficiency on the murine skeleton are independent and mechanistically distinct. J Bone Miner Res. 2017;32(3):560–74.PubMed Ucer S, et al. The effects of aging and sex steroid deficiency on the murine skeleton are independent and mechanistically distinct. J Bone Miner Res. 2017;32(3):560–74.PubMed
108.
Zurück zum Zitat Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30–44.PubMedPubMedCentral Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30–44.PubMedPubMedCentral
109.
Zurück zum Zitat Taubman MA, Kawai T. Involvement of T-lymphocytes in periodontal disease and in direct and indirect induction of bone resorption. Crit Rev Oral Biol Med. 2001;12(2):125–35.PubMed Taubman MA, Kawai T. Involvement of T-lymphocytes in periodontal disease and in direct and indirect induction of bone resorption. Crit Rev Oral Biol Med. 2001;12(2):125–35.PubMed
110.
Zurück zum Zitat Brunetti G, et al. T cells support osteoclastogenesis in an in vitro model derived from human periodontitis patients. J Periodontol. 2005;76(10):1675–80.PubMed Brunetti G, et al. T cells support osteoclastogenesis in an in vitro model derived from human periodontitis patients. J Periodontol. 2005;76(10):1675–80.PubMed
111.
Zurück zum Zitat Khosla S. Minireview: the OPG/RANKL/RANK system. Endocrinology. 2001;142(12):5050–5.PubMed Khosla S. Minireview: the OPG/RANKL/RANK system. Endocrinology. 2001;142(12):5050–5.PubMed
112.
Zurück zum Zitat Crotti T, et al. Receptor activator NF kappaB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. J Periodontal Res. 2003;38(4):380–7.PubMed Crotti T, et al. Receptor activator NF kappaB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. J Periodontal Res. 2003;38(4):380–7.PubMed
113.
Zurück zum Zitat Kawai T, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol. 2006;169(3):987–98.PubMedPubMedCentral Kawai T, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol. 2006;169(3):987–98.PubMedPubMedCentral
114.
Zurück zum Zitat Hughes DE, et al. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat Med. 1996;2(10):1132–6.PubMed Hughes DE, et al. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat Med. 1996;2(10):1132–6.PubMed
115.
Zurück zum Zitat Riggs BL. The mechanisms of estrogen regulation of bone resorption. J Clin Investig. 2000;106(10):1203–4 (Comment).PubMed Riggs BL. The mechanisms of estrogen regulation of bone resorption. J Clin Investig. 2000;106(10):1203–4 (Comment).PubMed
116.
Zurück zum Zitat D’Amelio P, et al. Estrogen deficiency increases osteoclastogenesis up-regulating T cells activity: a key mechanism in osteoporosis. Bone. 2008;43(1):92–100.PubMed D’Amelio P, et al. Estrogen deficiency increases osteoclastogenesis up-regulating T cells activity: a key mechanism in osteoporosis. Bone. 2008;43(1):92–100.PubMed
117.
Zurück zum Zitat Cenci S, et al. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Investig. 2000;106(10):1229–37.PubMed Cenci S, et al. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Investig. 2000;106(10):1229–37.PubMed
118.
Zurück zum Zitat Ronderos M, et al. Associations of periodontal disease with femoral bone mineral density and estrogen replacement therapy: cross-sectional evaluation of US adults from NHANES III. J Clin Periodontol. 2000;27(10):778–86.PubMed Ronderos M, et al. Associations of periodontal disease with femoral bone mineral density and estrogen replacement therapy: cross-sectional evaluation of US adults from NHANES III. J Clin Periodontol. 2000;27(10):778–86.PubMed
120.
Zurück zum Zitat Jönsson D, et al. Beneficial effects of hormone replacement therapy on periodontitis are vitamin D associated. J Periodontol. 2013;84(8):1048–57.PubMed Jönsson D, et al. Beneficial effects of hormone replacement therapy on periodontitis are vitamin D associated. J Periodontol. 2013;84(8):1048–57.PubMed
Metadaten
Titel
Estrogen signaling impacts temporomandibular joint and periodontal disease pathology
verfasst von
Jennifer L. Robinson
Pamela M. Johnson
Karolina Kister
Michael T. Yin
Jing Chen
Sunil Wadhwa
Publikationsdatum
03.07.2019
Verlag
Springer Singapore
Erschienen in
Odontology / Ausgabe 2/2020
Print ISSN: 1618-1247
Elektronische ISSN: 1618-1255
DOI
https://doi.org/10.1007/s10266-019-00439-1

Weitere Artikel der Ausgabe 2/2020

Odontology 2/2020 Zur Ausgabe

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Zahnmedizin und bleiben Sie gut informiert – ganz bequem per eMail.