Download PDF
Horm Metab Res 2006; 38(4): 279-290
DOI: 10.1055/s-2006-925348
Review
© Georg Thieme Verlag KG Stuttgart · New York

The Role of Plasma-binding Proteins in the Cellular Uptake of Lipophilic Vitamins and Steroids

T.  K.  Andreassen1
  • 1 Department of Medical Biochemistry, University of Aarhus, Denmark
Further Information

Publication History

Received 19 October 2005

Accepted after revision 20 February 2006

Publication Date:
15 May 2006 (online)

Also available at
    Permissions and Reprints

Abstract

Steroid hormones and many other lipophilic compounds are believed to enter cells solely by free diffusion through the plasma membrane. However, recent work using a megalin-deficient mouse model has identified a new endocytic pathway responsible for the delivery of steroids to renal and gonadal tissues. This review describes these new pathways for uptake of 25-hydroxy-vitamin-D3 and the gonadal sex-steroids (17β-estradiol and testosterone) bound to vitamin D-binding protein and sex hormone-binding globulin respectively. Furthermore examples of other lipophilic molecules that enter cells by receptor-mediated pathways will be presented and the receptors responsible for their uptake described.

Key words

SHBG · DBP · steroids · lipophilic molecules · binding proteins · receptor-mediated endocytosis · uptake · transport

References

  • 1 Beato M, Klug J. Steroid hormone receptors: an update.  Hum Reprod Update. 2000;  6 225-236
    CrossrefPubMedGoogle Scholar
  • 2 Mendel C M. The free hormone hypothesis: a physiologically based mathematical model.  Endocr Rev. 1989;  10 232-274
    PubMedGoogle Scholar
  • 3 Siiteri P K, Murai J T, Hammond G L, Nisker J A, Raymoure W J, Kuhn R W. The serum transport of steroid hormones.  Recent Prog Horm Res. 1982;  38 457-510
    PubMedGoogle Scholar
  • 4 Dunn J F, Nisula B C, Rodbard D. Transport of steroid hormones: binding of 21 endogenous steroids to both testosterone-binding globulin and corticosteroid-binding globulin in human plasma. J. Clin.  Endocrinol Metab. 1981;  53 58-68
    CrossrefPubMedGoogle Scholar
  • 5 Avvakumov G V, Zhuk N I, Strel'chyonok O A. Subcellular distribution and selectivity of the protein-binding component of the recognition system for sex-hormone-binding protein-estradiol complex in human decidual endometrium.  Biochim Biophys Acta. 1986;  881 489-498
    PubMedGoogle Scholar
  • 6 Hryb D J, Khan M S, Romas N A, Rosner W. The control of the interaction of sex hormone-binding globulin with its receptor by steroid hormones.  J Biol Chem. 1990;  265 6048-6054
    PubMedGoogle Scholar
  • 7 Fortunati N, Fissore F, Fazzari A, Berta L, Varvello L, Frairia R. Receptor for sex steroid-binding protein of endometrium membranes: solubilization, partial characterization, and role of estradiol in steroid-binding protein-soluble receptor interaction.  Steroids. 1992;  57 464-470
    CrossrefPubMedGoogle Scholar
  • 8 Joseph D R. Structure, Function and regulation of androgen binding protein/sex hormone-binding globulin.  Vit Horm. 1994;  49 197-280
    PubMedGoogle Scholar
  • 9 Krupenko S, Krupenko N I, Danzo B J. Interaction of sex hormone-binding globulin with plasma membranes from the rat epididymis and other tissues.  J Steroid Biochem Molec Biol. 1994;  51 115-124
    CrossrefPubMedGoogle Scholar
  • 10 Porto C S, Lazari M FM, Abreu , LC , Bardin C W, Gunsalus G L. Receptors for androgen-binding proteins:internalization and intracellular signalling.  J Steroid Biochem Molec Biol. 1995;  53 561-565
    CrossrefPubMedGoogle Scholar
  • 11 Hryb D J, Khan M S, Romas N A, Rosner W. Solubilization and partial characterization of the sex hormone-binding globulin receptor from human prostate.  J Biol Chem. 1989;  264 5378-5383
    PubMedGoogle Scholar
  • 12 Porto C S, Abreu L C, Gunsalus G L, Bardin C W. Binding of sex-hormone-binding globulin (SHBG) to testicular membranes and solubilized receptors.  Mol Cell Endocrinol. 1992;  89 33-38
    CrossrefPubMedGoogle Scholar
  • 13 Hryb D J, Khan M S, Rosner W. Testosterone-estradiol-binding globulin binds to human prostatic cell membranes.  Biochem Biophys Res Commun. 1985;  128 432-440
    CrossrefPubMedGoogle Scholar
  • 14 Porto C S, Gunsalus G L, Bardin C W, Phillips D M, Musto N A. Receptor-mediated endocytosis of an extracellular steroid-binding protein (TeBG) in MCF-7 human breast cancer cells.  Endocrinology. 1991;  129 436-445
    PubMedGoogle Scholar
  • 15 Gerard A, Nya A E, Egloff M, Domingo M, Degrelle H, Gerard H. Endocytosis of human sex steroid-binding protein in monkey germ cells.  Ann N Y Acad Sci. 1991;  637 258-276
    PubMedGoogle Scholar
  • 16 Gerard A, Khanfri J, Gueant J L, Fremont S, Nicolas J P, Grignon G, Gerard H. Electron microscope radioautographic evidence of in vivo androgen-binding protein internalization in the rat epididymis principal cells.  Endocrinology. 1988;  122 1297-1307
    PubMedGoogle Scholar
  • 17 Hryb D J, Khan M S, Romas N A, Rosner W. Specific binding of human corticosteroid-binding globulin to cell membranes.  Proc Natl Acad Sci USA. 1986;  83 3253-3256
    PubMedGoogle Scholar
  • 18 Strel’chyonok O A, Avvakumov G V. Interaction of human CBG with cell membranes.  J Steroid Biochem Mol Biol. 1991;  40 795-803
    CrossrefPubMedGoogle Scholar
  • 19 Maitra U S, Khan M S, Rosner W. Corticosteroid-binding globulin receptor of the rat hepatic membrane - solubilization, partial characterization, and the effect of steroids on binding.  Endocrinology. 1993;  133 1817-1822
    CrossrefPubMedGoogle Scholar
  • 20 Strel'chyonok O A, Avvakumov G V. Evidence for the presence of specific binding sites for transcortin in human liver plasma membranes.  Biochim Biophys Acta. 1983;  755 514-517
    PubMedGoogle Scholar
  • 21 Avvakumov G V, Krupenko S A, Strel'chyonok O A. Study of the transcortin binding to human endometrium plasma membrane.  Biochim Biophys Acta. 1989;  984 143-150
    CrossrefPubMedGoogle Scholar
  • 22 Avvakumov G, Krupenko S A, Strel'chyonok O A. Study of the transcortin binding to human endometrium plasma membrane.  Biochim Biophys Acta. 1989;  984 143-150
    CrossrefPubMedGoogle Scholar
  • 23 Krupenko S A, Avvakumov G V, Strel'chyonok O A. On the functional form of transcortin recognizing subunit of transcortin membrane receptor.  FEBS. 1991;  281 152-154
    CrossrefPubMedGoogle Scholar
  • 24 Hsu B R-S, Siiteri P K, Kuhn R W. Interactions between corticosteroid-binding globulin (CBG) and target tissues. In: Forest MG, Pugeat M. (eds) Binding Proteins of Steroid Hormones. London, Paris; Libbey Eurotext 1986: 577-591
    Google Scholar
  • 25 Kuhn R W. Corticosteroid-binding globulin interactions with target cells and plasma membranes.  Ann N Y Acad Sci. 1988;  538 146-158
    CrossrefPubMedGoogle Scholar
  • 26 Nakhla A M, Khan M S, Rosner W. Induction of adenylate cyclase in a mammary carcinoma cell line by human corticosteroid-binding globulin.  Biochem Biophys Res Com. 1988;  153 1012-1018
    CrossrefPubMedGoogle Scholar
  • 27 StrelŽchyonok O A, Avvakumov G V. Specific steroid-binding glycoproteins of human blood plasma: novel data on their structure and function.  J Steroid Biochem. 1990;  35 519-534
    CrossrefPubMedGoogle Scholar
  • 28 Noé G, Cheng Y C, Dakiké M, Croxatto H B. Tissue uptake of human sex hormone-binding globulin and its influence on ligand kinetics in the adult female rat.  Biol Reprod. 1992;  47 970-976
    CrossrefPubMedGoogle Scholar
  • 29 Rosner W, Hryb D J, Khan M S, Nakhla A M, Romas N A. Sex hormone-binding globulin mediates steroid hormone signal transduction at the plasma membrane.  J Steroid Biochem Mol Biol. 1999;  69 481-485
    CrossrefPubMedGoogle Scholar
  • 30 Breuner C W, Orchinik M. Plasma binding proteins as mediators of corticosteroid action in vertebrates.  J Endocrinol. 2002;  5 99-112
    PubMedGoogle Scholar
  • 31 Nakhla A M, Khan M S, Romas N P, Rosner W. Estradiol causes the rapid accumulation of cAMP in human prostate.  Proc Natl Acad Sci USA. 1994;  91 5402-5405
    PubMedGoogle Scholar
  • 32 Fortunati N, Becchis M, Catalano M G, Comba A, Ferrera P, Raineri M, Berta L, Frairia R. Sex hormone-binding globulin, its membrane receptor, and breast cancer: a new approach to the modulation of estradiol action in neoplastic cells.  J Steroid Biochem Mol Biol. 1999;  69 473-479
    CrossrefPubMedGoogle Scholar
  • 33 Nakhla A M, Leonard J, Hryb D J, Rosner W. Sex hormone-binding globulin receptor signal transduction proceeds via a G protein.  Steroids. 1999;  64 213-216
    CrossrefPubMedGoogle Scholar
  • 34 Nykjaer A, Dragun D, Walther D, Vorum H, Jacobsen C, Herz J, Melsen F, Christensen E I, Willnow T E. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3.  Cell. 1999;  96 507-515
    CrossrefPubMedGoogle Scholar
  • 35 White P, Cooke N. The multifunctional properties and characteristics of vitamin D-binding protein.  Trends Endocrinol Metab. 2000;  11 320-327
    PubMedGoogle Scholar
  • 36 Bikle D D, Gee E, Halloran B, Kowalski M A, Ryzen E, Haddad J G. Assessment of the free fraction of 25-hydroxy-vitamin D in serum and its regulation by albumin and the vitamin D-binding protein.  J Clin Endocrinol Metab. 1986;  63 954-959
    CrossrefPubMedGoogle Scholar
  • 37 Safadi F F, Thornton P, Magiera H, Hollis B W, Gentile M, Haddad J G, Liebhaber S A, Cooke N E. Osteopathy and resistance to vitamin D toxicity in mice null for vitamin D binding protein.  J Clin Invest. 1999;  103 239-251
    PubMedGoogle Scholar
  • 38 Leheste J R, Melsen F, Wellner M, Jansen P, Schlichting U, Renner-Muller I, Andreassen T T, Wolf E, Bachmann S, Nykjaer A, Willnow T E. Hypocalcemia and osteopathy in mice with kidney-specific megalin gene defect.  FASEB J. 2003;  17 247-249
    PubMedGoogle Scholar
  • 39 Hilpert J, Wogensen L, Thykjaer T, Wellner M, Schlichting U, Orntoft T F, Bachmann S, Nykjaer A, Willnow T E. Expression profiling confirms the role of endocytic receptor megalin in renal vitamin D3 metabolism.  Kidney Int. 2002;  62 1672-1681
    CrossrefPubMedGoogle Scholar
  • 40 Nykjaer A, Fyfe J C, Kozyraki R, Leheste J R, Jacobsen C, Nielsen M S, Verroust P J, Aminoff M, de la Chapelle A, Moestrup S K, Ray R, Gliemann J, Willnow T E, Christensen E I. Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25-(OH) vitamin D3.  Proc Natl Acad Sci USA. 2001;  98 13 895-13 900
    PubMedGoogle Scholar
  • 41 Hammes A, Andreassen T K, Spoelgen R, Raila J, Hubner N, Schulz H, Metzger J, Schweigert F J, Luppa P B, Nykjaer A, Willnow T E. Role of endocytosis in cellular uptake of sex steroids.  Cell. 2005;  122 751-762
    CrossrefPubMedGoogle Scholar
  • 42 Sullivan P M, Petrusz P, Szpirer C, Joseph D R. Alternative processing of androgen-binding protein RNA transcripts in fetal rat liver. Identification of a transcript formed by trans splicing.  J Biol Chem. 1991;  266 143-154
    PubMedGoogle Scholar
  • 43 Westphal U. Steroid-protein interactions II.  Monogr Endocrinol. 1986;  27 1-603
    PubMedGoogle Scholar
  • 44 Willnow T W, Nykjaer A, Herz J. Lipoprotein receptors: new roles for ancient proteins.  Nat Cell Biol. 1999;  1 E157-E162
    CrossrefPubMedGoogle Scholar
  • 45 Rodriguez I, Araki K, Khatib K, Martinou J C, Vassalli P. Mouse vaginal opening is an apoptosis-dependent process which can be prevented by the overexpression of Bcl2.  Dev Biol. 1997;  184 115-121
    CrossrefPubMedGoogle Scholar
  • 46 Ashby J, Owens W, Deghenghi R, Odum J. Concept evaluation: an assay for receptor-mediated and biochemical antiestrogens using pubertal rats.  Regul Toxicol Pharmacol. 2002;  35 393-397
    CrossrefPubMedGoogle Scholar
  • 47 Husmann D A, McPhaul M J. Time-specific androgen blockade with flutamide inhibits testicular descent in the rat.  Endocrinology. 1991;  129 1409-1416
    PubMedGoogle Scholar
  • 48 Emmen J M, McLuskey A, Grootegoed J A, Brinkmann A O. Androgen action during male sex differentiation includes suppression of cranial suspensory ligament development.  Hum Reprod. 1998;  13 1272-1280
    CrossrefPubMedGoogle Scholar
  • 49 van der Schoot P, Elger W. Androgen-induced prevention of the outgrowth of cranial gonadal suspensory ligaments in fetal rats.  J Androl. 1992;  13 534-542
    PubMedGoogle Scholar
  • 50 Ikeda K, Arao Y, Otsuka H, Kikuchi A, Kayama F. Estrogen and phytoestrogen regulate the mRNA expression of adrenomedullin and adrenomedullin receptor components in the rat uterus.  Mol Cell Endocrinol. 2004;  223 27-34
    CrossrefPubMedGoogle Scholar
  • 51 Kumar A P, Piedrafita F J, Reynolds W F. Peroxisome proliferator-activated receptor gamma ligands regulate myeloperoxidase expression in macrophages by an estrogen-dependent mechanism involving the -463GA promoter polymorphism.  J Biol Chem. 2004;  279 8300-8315
    PubMedGoogle Scholar
  • 52 Green M H, Green J B. Dynamics and control of plasma retinol. In: Blonhoff R (ed) Vitamin A in Health and Disease. New York; Marcel Dekker 1994: 119-133
    Google Scholar
  • 53 Blomhoff R, Berg T, Norum K R. Transfer of retinol from parenchymal to stellate cells in liver is mediated by retinol-binding protein.  Proc Natl Acad Sci USA. 1988;  85 3455-3458
    PubMedGoogle Scholar
  • 54 Senoo H, Smeland S, Malaba L, Bjerknes T, Stang E, Roos N, Berg T, Norum K R, Blomhoff R. Transfer of retinol-binding protein from HepG2 human hepatoma cells to cocultured rat stellate cells.  Proc Natl Acad Sci USA. 1993;  90 3616-3620
    PubMedGoogle Scholar
  • 55 Christensen E I, Moskaug J Ø, Vorum H, Jacobsen C, Gundersen T E, Nykjaer A, Blomhoff R, Willnow T E, Moestrup S K. Evidence for an essential role of megalin in transepithelial transport of retinal.  J Am Soc Nephrol. 1999;  10 685-695
    PubMedGoogle Scholar
  • 56 Pfeffer B A, Clark V M, Flannery J G, Bok D. Membrane receptors for retinol binding protein in cultured human retinal pigment epithelium.  Invest Ophthalmol Vis Sci. 1986;  27 1031-1040
    PubMedGoogle Scholar
  • 57 Ward S J, Chambon P, Ong D E, Båvik C. A retinol-binding protein receptor-mediated mechanism for uptake of vitamin A to postimplantation rat embryos.  Biol Reprod. 1997;  57 751-755
    CrossrefPubMedGoogle Scholar
  • 58 Sundaram M, Sivaprasadarao A, DeSousa M M, Findlay J B. The transfer of retinol from serum retinol-binding protein to cellular retinol-binding protein is mediated by a membrane receptor.  J Biol Chem. 1998;  273 3336-3342
    CrossrefPubMedGoogle Scholar
  • 59 Sousa , MM , Norden A GW, Jacobsen C, Willnow T E, Christensen E I, Thakker R V, Verroust P J, Moestrup S K, Saraiva M J. Evidence for the role of megalin in renal uptake of transthyretin.  J Biol Chem. 2000;  275 38 176-38 181
    PubMedGoogle Scholar
  • 60 Quadro L, Blaner W S, Salchow D J, Vogel S, Piantedosi R, Gouras P, Freeman S, Cosma M P, Colantuoni V, Gottesman M E. Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein.  EMBO J. 1999;  18 4633-4644
    CrossrefPubMedGoogle Scholar
  • 61 Kragh-Hansen U, Chuang V T, Otagiri M. Practical aspects of the ligand-binding and enzymatic properties of human serum albumin.  Biol Pharm Bull. 2002;  25 695-704
    CrossrefPubMedGoogle Scholar
  • 62 Quinlan G J, Martin G S, Evans T W. Albumin: biochemical properties and therapeutic potential.  Hepatology. 2005;  41 1211-1219
    CrossrefPubMedGoogle Scholar
  • 63 Antohe F, Serban G, Radulescu L, Simionescu M. Transcytosis of albumin in endothelial cells is brefeldin A-independent.  Endothelium. 1997;  5 125-136
    PubMedGoogle Scholar
  • 64 Weisiger R, Gollan J, Ockner R. Receptor for albumin on the liver cell surface may mediate uptake of fatty acids and other albumin-bound substances.  Science. 1981;  211 1048-1051
    PubMedGoogle Scholar
  • 65 Hutter J F, Piper H M, Spieckermann P G. Myocardial fatty acid oxidation: evidence for an albumin-receptor-mediated membrane transfer of fatty acids.  Basic Res Cardiol. 1984;  79 274-282
    CrossrefPubMedGoogle Scholar
  • 66 Christensen E I, Nielsen S. Features of protein handling in the kidney proximal tubule.  Semin Nephrol. 199 l ;  11 414-439
    PubMedGoogle Scholar
  • 67 Cui S, Verroust P J, Moestrup S K, Christensen E I. Megalin/gp330 mediates uptake of albumin in renal proximal tubule.  Am J Physiol. 1996;  271 F900-F907
    PubMedGoogle Scholar
  • 68 Zhai X Y, Nielsen R, Birn H, Drumm K, Mildenberger S, Freudinger R, Moestrup S K, Verroust P J, Christensen E I, Gekle M. Cubilin- and megalin-mediated uptake of albumin in cultured proximal tubule cells of opossum kidney.  Kidney Int. 2000;  58 1523-1533
    CrossrefPubMedGoogle Scholar
  • 69 Koot B G, Houwen R, Pot D J, Nauta J. Congenital analbuminaemia: biochemical and clinical implications. A case report and literature review.  Eur J Pediatr. 2004;  163 664-670
    PubMedGoogle Scholar
  • 70 Gitlin D, Boesman M. Sites of serum alpha-fetoprotein synthesis in the human and in the rat.  J Clin Invest. 1967;  46 1010-1016
    PubMedGoogle Scholar
  • 71 Deutsch H F. Chemistry and biology of α-fetoprotein.  Adv cancer Res. 1991;  56 253-312
    PubMedGoogle Scholar
  • 72 Geuskens M, Dupressoir T, Uriel J. A study, by electron microscopy, of the specific uptake of alpha-fetoprotein by mouse embryonic fibroblasts in relation to in vitro aging, and by human mammary epithelial tumour cells in comparison with normal donorsŽ cells. J.  Submicrosc Cytol Pathol. 1991;  23 59-66
    PubMedGoogle Scholar
  • 73 Lorenzo , HC , Geuskens M, Macho A, Lachkar S, Verdiere-Sahuque M, Pineiro A, Uriel J. Alpha-fetoprotein binding and uptake by primary cultures of human skeletal muscle.  Tumour biol. 1996;  17 251-260
    PubMedGoogle Scholar
  • 74 Uriel J, Naval J, Larborda J. α-fetoprotein-mediated transfer of arachidonic acid into cultured cloned cells derived from a rat rhabdomyosarcoma.  J Biol Chem. 1987;  262 3579-3585
    PubMedGoogle Scholar
  • 75 Suzuki Y, Zeng C QY, Alpert E. Isolation and partial characterization of a specific alpha-fetoprotein receptor on human monocytes.  J Clin Invest. 1992;  90 1530-1536
    PubMedGoogle Scholar
  • 76 Kanevsky V Yu, Pozdnyakova L P, Aksenova O A, Severin S E, Katukov V Yu, Severin E S. Isolation and characterization of AFP-binding proteins from tumor and fetal human tissues.  Biochem Mol Biol Int. 1997;  41 1143-1151
    PubMedGoogle Scholar
  • 77 Aussel C, Laliberte F, Masseyeff R. Alpha-fetoprotein favours accumulation of estrone but not arachidonic acid into the fetal and new-born rat brain.  Life Sci. 1985;  36 479-484
    CrossrefPubMedGoogle Scholar
  • 78 Döhler K D. The pre- and postnatal influence of hormones and neurotransmitters on sexual differentiation of the mammalian hypothalamus.  Int Rev Cytol. 1991;  131 1-57
    PubMedGoogle Scholar
  • 79 Gabant P, Forrester L, Nichols J, VanReeth T, DeMees C, Pajack B, Watt A, Smitz J, Alexandre H, Szpirer C, Szpirer J. Alpha-fetoprotein, the major fetal serum protein, is not essential for embryonic development but is required for female fertility.  Proc Natl Acad Sci U S A. 2002;  99 12 865-12 870
    PubMedGoogle Scholar
  • 80 Singh G, Katyal S L, Gottron S A. Antigenic, molecular and functional heterogeneity of Clara cell secretory proteins in the rat.  Biochim Biophys Acta. 1985;  829 156-163
    PubMedGoogle Scholar
  • 81 Beier H M. The discovery of uteroglobin and its significance for reproductive biology and endocrinology.  Ann N Y Acad Sci. 2000;  923 9-24
    PubMedGoogle Scholar
  • 82 Pattabiraman N, Matthews J H, Ward K B, Mantile-Selvaggi G, Miele L, Mukherjee A B. Crystal structure analysis of recombinant human uteroglobin and molecular modeling of ligand binding.  Ann NY Acad Sci. 2000;  923 113-127
    PubMedGoogle Scholar
  • 83 Stripp B R, Lund J, Mango G W, Doyen K C, Johnston C, Hultenby K, Nord M, Whitsett J. Clara cell secretory protein: a determinant of PCB bioaccumulation in mammals.  Am J Physiol. 1996;  271 L656-L664
    PubMedGoogle Scholar
  • 84 Robinson D H, Kirk K L, Benos D J. Macromolecular transport in rabbit blastocysts: evidence for a specific uteroglobin transport system.  Mol Cell Endocrinol. 1989;  63 227-237
    CrossrefPubMedGoogle Scholar
  • 85 Bochskanl R, Thie M, Kirchner C. Progesterone dependent uptake of uteroglobin by rabbit endometrium.  Histochemistry. 1984;  80 581-589
    PubMedGoogle Scholar
  • 86 Burmeister R, Bøe I-M, Nykjaer A, Jacobsen C, Moestrup S K, Verroust P, Christensen E I, Lund J, Willnow T E. A two-receptor pathway for catabolism of Clara cell secretory protein in the kidney.  J Biol Chem. 2001;  276 13 295-13 301
    PubMedGoogle Scholar
  • 87 Davis P J, Spaulding S W, Gregerman R I. The three thyroxine-binding proteins in rat serum: binding capacities and effects of binding inhibitors.  Endocrinology. 1970;  87 978-986
    PubMedGoogle Scholar
  • 88 Vranckx R, Rouaze M, Savu L, Nunez E A, Beaumont C, Flink I L. The hepatic biosynthesis of rat thyroxine binding globulin (TBG): demonstration, ontogenesis, and up-regulation in experimental hypothyroidism.  Biochem Biophys Res Commun. 1990;  167 317-322
    CrossrefPubMedGoogle Scholar
  • 89 Soprano D R, Herbert J, Soprano K J, Schon E A, Goodman D S. Demonstration of transthyretin mRNA in the brain and other extrahepatic tissues in the rat.  J Biol Chem. 1985;  260 11 793-11 798
    PubMedGoogle Scholar
  • 90 Devino C M, Schussler G C. Binding of thyroxine transthyretine complexes to specific cell-surface receptors.  Clin Res. 1989;  37 357A
    PubMedGoogle Scholar
  • 91 Devino C M, Schussler G C. Receptor-mediated uptake and internalization of transthyretin.  J Biol Chem. 1990;  265 1425-1429
    PubMedGoogle Scholar
  • 92 Sousa M M, Saraiva M J. Internalization of transthyretin - evidence of a novel yet unidentified receptor-associated protein (RAP)-sensitive receptor.  J Biol Chem. 2001;  276 14 420-14 425
    PubMedGoogle Scholar
  • 93 Devino C M, Schussler G C. Transthyretin receptors on human astrocytoma cells.  J Clin Endocrinol Metab. 1990;  71 1265-1268
    PubMedGoogle Scholar
  • 94 Kuchler-Bopp S, Dietrich J-B, Zaepfel M, Delaunoy J-P. Receptor-mediated endocytosis of transthyretin by ependymoma cells.  Brain Res. 2000;  870 185-194
    CrossrefPubMedGoogle Scholar
  • 95 Episkopou V, Maeda S, Nishiguchi S, Shimada K, Gaitanaris G A, Gottesman M E, Robertson E J. Disruption of the transthyretin gene results in mice with depressed levels of plasma retinol and thyroid hormone.  Proc Natl Acad Sci USA. 1993;  90 2375-2379
    PubMedGoogle Scholar
  • 96 Palha J A, Episkopou V, Maeda S, Shimada K, Gottesman M E, Saraiva M JM. Thyroid hormone metabolism in a transthyretin-null mouse strain.  J Biol Chem. 1994;  269 33 135-33 139
    PubMedGoogle Scholar
  • 97 Hashizume K, Sakurai A, Miyamoto T, Yamauchi K, Hishii Y. Effect of thyroxine-binding globulin (TBG) on thyroxine (T4) uptake by human peripheral mononuclear cells: evidence of TBG-dependent uptake of T4. .  Endocrinol Japon. 1986;  33 665-674
    PubMedGoogle Scholar
  • 98 Carvalho G A, Weiss R E, Refetoff S. Complete thyroxine-binding globulin (TBG) deficiency produced by a mutation in acceptor splice site causing frameshift and early termination of translation (TBG-Kankakee).  J Clin Endocrinol Metab. 1998;  83 3604-3608
    CrossrefPubMedGoogle Scholar
  • 99 Raila J, Willnow T E, Schweigert F J. Megalin-mediated reuptake of retinol in the kidneys of mice is essential for vitamin A homeostasis.  J Nutr. 2005;  135 2512-2516
    PubMedGoogle Scholar
  • 100 Ahrentsen O D, Jensen H K, Johnsen S G. Sex-hormone-binding globulin deficiency.  Lancet. 1982;  2 377
    PubMedGoogle Scholar
  • 101 Botwood N, Hamilton-Fairley D, Kiddy D, Robinson S, Franks S. Sex hormone-binding globulin and female reproductive function.  J Steroid Biochem Mol Biol. 1995;  53 529-531
    CrossrefPubMedGoogle Scholar
  • 102 Torpy D J, Bachmann A W, Grice J E, Fitzgerald S P, Phillips P J, Whitworth J A, Jackson R V. Familial corticosteroid-binding globulin deficiency due to a novel null mutation: association with fatigue and relative hypotension.  J Clin Endocrinol Metab. 2001;  86 3692-3700
    CrossrefPubMedGoogle Scholar
  • 103 Christensen E I, Birn H. Megalin and cubilin: Multifunctional endocytic receptors.  Nature rev. 2002;  3 258-268
    PubMedGoogle Scholar
  • 104 Willnow T E. The low density lipoprotein receptor gene family: multiple roles in lipid metabolism.  J Mol Med. 1999;  77 306-315
    CrossrefPubMedGoogle Scholar
  • 105 Nykjaer A, Willnow T E. The low-density lipoprotein receptor gene family: a cellular swiss army knife?.  Trends cell biol. 2002;  12 273-280
    CrossrefPubMedGoogle Scholar
  • 106 Argraves W S, Morales C R. Immunolocalization of cubilin, megalin, apolipoprotein J, and apolipoprotein A-I in the uterus and oviduct.  Mol reprod dev. 2004;  69 419-427
    CrossrefPubMedGoogle Scholar
  • 107 van Praet O, Argraves W S, Morales C R. Co-expression and interaction of cubilin and megalin in the adult male reproductive system.  Mol reprod dev. 2003;  64 129-135
    CrossrefPubMedGoogle Scholar
  • 108 Zheng G, Bachinsky D R, Stamenkovic I, Strickland D K, Brown D, Andres G, McCluskey R T. Organ distribution in rats of two members of the low-density lipoprotein receptor gene family, Gp330 and LRP/α2MR, and the receptor-associated proein (RAP).  J Histochem Cytochem. 1994;  42 531-542
    PubMedGoogle Scholar
  • 109 Moestrup S K, Verroust P J. Megalin- and cubilin-mediated endocytosis of protein-bound vitamins, lipids, and hormones in polarized epithelia.  Ann Rev nutr. 2001;  21 407-428
    PubMedGoogle Scholar
  • 110 Seetharam B, Christensen E I, Moestrup S K, Hammond T G, Verroust P J. Identification of rat yolk sac target protein of teratogenic antibodies, gp280, as intrinsic factor-cobalamin receptor.  J Clin Invest. 1997;  99 2317-2322
    PubMedGoogle Scholar
  • 111 Fyfe J C, Madsen M, Hojrup P, Christensen E I, Tanner S M, delaChapelle A, He Q, Moestrup S K. The functional cobalamin (vitamin B12)-intrinsic factor receptor is a novel complex of cubilin and amnionless.  Blood. 2004;  103 1573-1579
    CrossrefPubMedGoogle Scholar
  • 112 Kim D H, Iijima H, Goto K, Sakai J, Ishii H, Kim H J, Suzuki H, Kondo H, Saeki S, Yamamoto T. Human apolipoprotein E receptor 2. A novel lipoprotein receptor of the low density lipoprotein receptor family predominantly expressed in brain.  J Biol Chem. 1996;  271 8373-8380
    CrossrefPubMedGoogle Scholar
  • 113 Stockinger W, Brandes C, Fasching D, Hermann M, Gotthardt M, Herz J, Schneider W J, Nimpf J. The Reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2.  J Biol Chem. 2000;  275 25 625-25 632
    PubMedGoogle Scholar
  • 114 Oka K, Ishimura-Oka K, Chu M-J, Sullivan M, Krushkal J, Li W-H, Chan L. Mouse very-low-density-lipoprotein receptor (VLDLR) cDNA cloning, tissue-specific expression and evolutionary relationship with the low-density-lipoprotein receptor.  Eur J Biochem. 1994;  224 975-982
    CrossrefPubMedGoogle Scholar
  • 115 Gåfvels M E, Paavola L G, Boyd C O, Nolan P M, Wittmaack F, Chawla A, Lazar M A, Bucan M, Angelin B O, Strauss III J F. Cloning of a complementary deoxyribonucleic acid encoding the murine homolog of the very low density lipoprotein/apolipoprotein-E receptor: expression pattern and assignment of the gene to mouse chromosome 19.  Endocrinology. 1994;  135 387-394
    CrossrefPubMedGoogle Scholar
  • 116 Goldstein J L, Brown M S. The low-density lipprotein pathway and its relation to atherosclerosis.  Ann Rev Biochem. 1977;  46 897-930
    CrossrefPubMedGoogle Scholar
  • 117 Sivaprasadarao A, Boudjelal M, Findlay J B. Solubilization and purification of the retinol-binding protein receptor from human placental membranes.  Biochem J. 1994;  302 245-251
    PubMedGoogle Scholar
  • 118 Ottonello S, Petrucco S, Maraini G. Vitamin A uptake from retinol-binding protein in a cell-free system from pigment epithelial cells of bovine retina. Retinol transfer from plasma retinol-binding protein to cytoplasmic retinol-binding protein with retinyl-ester formation as the intermediate step.  J Biol Chem. 1987;  262 3975-3981
    PubMedGoogle Scholar
  • 119 Acton S, Rigotti A, Landschulz K T, Xu S, Hobbs H H, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor.  Science. 1996;  271 518-520
    CrossrefPubMedGoogle Scholar
  • 120 Temel R E, Trigatti B, DeMattos R B, Azhar S, Krieger M, Williams D L. Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells.  Proc Natl Acad Sci U S A. 1997;  94 13 600-13 605
    PubMedGoogle Scholar
  • 121 Benvenga S, Robbins J. Enhancement of thyroxine entry into low density lipoprotein (LDL) receptor-competent fibroblasts by LDL: an additional mode of entry of thyroxine into cells.  Endocrinology. 1990;  126 933-941
    PubMedGoogle Scholar
  • 122 Wathne K O, Carlander B, Norum K R, Blomhoff R. Uptake of retinyl ester in HL-60 cells via the low-density-lipoprotein-receptor pathway.  Biochem J. 1989;  257 239-244
    PubMedGoogle Scholar
  • 123 Shireman R B, Wei C I. Uptake of 2,3,7,8-tetrachlorodibenzo-p-dioxin from plasma lipoproteins by cultured human fibroblasts.  Chem Biol Interact. 1986;  58 1-12
    PubMedGoogle Scholar
  • 124 Mangelsdorf I, Buff K, Berndt J. Uptake of persistent environmental chemicals by cultured human cells.  Biochem Pharmacol. 1987;  36 2071-2078
    CrossrefPubMedGoogle Scholar
  • 125 Lewis J G, Bagley C J, Elder P A, Bachmann A W, Torpy D J. Plasma free cortisol fraction reflects levels of functioning corticosteroid-binding globulin.  Clin Chim Acta. 2005;  359 189-194
    CrossrefPubMedGoogle Scholar
  • 126 Danan J L, Delorme A C, Ripoche M A, Bouillon R, Van Baelen H, Mathieu H. Presence of immunoreactive vitamin D-binding protein in rat yolk sac endodermal cells.  Endocrinology. 1985;  117 243-247
    PubMedGoogle Scholar
  • 127 Guoth M, Murgia A, Smith R M, Prystowsky M B, Cooke N E, Haddad J G. Cell surface vitamin D-binding protein (GC-globulin) is acquired from plasma.  Endocrinology. 1990;  127 2313-2321
    PubMedGoogle Scholar
  • 128 Geuskens M, Torres J M, Esteban C, Uriel J. Endocytosis of three serum proteins of a multigene family and of arachidonic acid in human lectin-stimulated T lymphocytes.  Microsc Res Tech. 1994;  28 297-307
    CrossrefPubMedGoogle Scholar
  • 129 Porto C S, Musto N A, Bardin C W, Gunsalus G L. Binding of an extracellular steroid-binding globulin to membranes and soluble receptors from human breast cancer cells (MCF-7 cells).  Endocrinology. 1992;  130 2931-2936
    CrossrefPubMedGoogle Scholar
  • 130 Bavik C O, Eriksson U, Allen R A, Peterson P A. Identification and partial characterization of a retinal pigment epithelial membrane receptor for plasma retinol-binding protein.  J Biol Chem. 1991;  266 14 978-14 985
    PubMedGoogle Scholar

Thomas K. Andreassen

Department of Medical Biochemistry · University of Aarhus

Ole Worms Alle · Bldg 1170 · 8000 Aarhus C · Denmark

Phone: +45(89)422873

Fax: +45(86)131160

Email: tka@biokemi.au.dk

      >