Postendocytotic Trafficking of the Follicle-Stimulating Hormone (FSH)-FSH Receptor Complex

Molecular Endocrinology

Volumn 17, Issue 11, 2003, Pages 2162-2176

  Krishnamurthy, Hanumanthappa ^a   Kishi, Hiroshi ^a   Shi, Mei ^a   Galet, Colette ^a   Bhaskaran, Ravi Sankar ^a   Hirakawa, Takashi ^a   Ascoli, Mario ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CHORIONIC GONADOTROPIN; FOLLITROPIN; FOLLITROPIN RECEPTOR; LUTEINIZING HORMONE;

ANIMAL CELL; ARTICLE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELL STRAIN 193T; CELL STRAIN KK 1; CELL STRAIN MSC 1; CELL SURFACE; ENDOCYTOSIS; ENDOSOME; GENETIC TRANSFECTION; GRANULOSA CELL; HORMONE RECEPTOR INTERACTION; HUMAN; HUMAN CELL; IMAGING; INTERNALIZATION; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR DOWN REGULATION; RECYCLING; SERTOLI CELL;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHORIONIC GONADOTROPIN; DOWN-REGULATION; ENDOCYTOSIS; FOLLICLE STIMULATING HORMONE; HUMANS; KIDNEY; MACROMOLECULAR SUBSTANCES; MALE; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RECEPTORS, FSH; RECEPTORS, GONADOTROPIN; SEQUENCE DELETION; SERTOLI CELLS;

ANIMALIA;

EID: 0242267063     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2003-0118     Document Type: Article

References (61)

1. Hsu SY, Hsueh AJ 2000 Discovering new hormones, receptors, and signaling mediators in the genomic era. Mol Endocrinol 14:594-604
2. Hsu SY, Nakabayashi K, Nishi S, Kumagai J, Kudo M, Sherwood OD, Hsueh AJW 2002 Activation of orphan receptors by the hormone relaxin. Science 295:671-675
3. Kumagai J, Hsu SY, Matsumi H, Roh J-S, Fu P, Wade JD, Bathgate RAD, Hsueh AJW 2002 INSL3/Leydig insulin-like peptide activates the LGR8 receptor important in testis descent. J Biol Chem 277:31283-31286
4. Pierce JG, Parsons TF 1981 Glycoprotein hormones: structure and function. Annu Rev Biochem 50:465-495
5. Hearn MTW, Gomme PT 2000 Molecular architecture and biorecognition process of the cystine knot protein superfamily. I. The glycoprotein hormones. J Mol Recog 13:223-278
6. Miller WE, Lefkowitz RJ 2001 Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr Opin Cell Biol 13:139-145
7. Ferguson SSG 2001 Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev 53:1-24
8. Tsao P, Cao T, von Zastrow M 2001 Role of endocytosis in mediating downregulation of G-protein-coupled receptors. Trends Pharmacol Sci 22:91-96
9. Sorkin A, von Zastrow M 2002 Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 3:600-614
10. Ascoli M 1982 Internalization and degradation of receptor-bound human choriogonadotropin in Leydig tumor cells. Fate of the hormone subunits. J Biol Chem 257: 13306-13311
11. Ascoli M 1984 Lysosomal accumulation of the hormone-receptor complex during receptor-mediated endocytosis of human choriogonadotropin. J Cell Biol 99:1242-1250
12. Ascoli M, Segaloff DL 1987 On the fates of receptor-bound human ovine luteinizing hormone and human choriogonadotropin in cultured Leydig tumor cells. Demonstration of similar rates of internalization. Endocrinology 120:1161-1172
13. Kishi M, Liu X, Hirakawa T, Reczek D, Bretscher A, Ascoli M 2001 Identification of two distinct structural motifs that, when added to the C-terminal tail of the rat lutropin receptor, redirect the internalized hormone-receptor complex from a degradation to a recycling pathway. Mol Endocrinol 15:1624-1635
14. Ghinea N, Vuhai MT, Groyer-Picard M-T, Houllier A, Schoëvaërt D, Milgrom E 1992 Pathways of internalization of the hCG/LH receptor: immunoelectron microscopic studies in Leydig cells and transfected L cells. J Cell Biol 118:1347-1358
15. Baratti-Elbaz C, Chinea N, Lahuna O, Loosfelt H, Pichon C, Milgrom E 1999 Internalization and recycling pathways of the thyrotropin receptor. Mol Endocrinol 13: 1751-1765
16. Beau I, Groyer-Picard M-T, Le Bivic A, Vannier B, Loosfelt H, Milgrom E, Misrahi M 1998 The basolateral localization signal of the follicle-stimulating hormone receptor. J Biol Chem 273:18610-18616
17. Beau I, Misrahi M, Gross B, Vannier B, Loosfelt H, Vu Hai MT, Pichon C, Milgrom E 1997 Basolateral localization and transcytosis of gonadotropin and thyrotropin receptors expressed in Madin-Darby canine kidney cells. J Biol Chem 272:5241-5248
18. Fletcher PW, Reichert Jr LE 1984 Cellular processing of follicle-stimulating hormone by Sertoli cells in serum-free culture. Mol Cell Endocrinol 34:39-49
19. Galet C, Min L, Narayanan R, Kishi M, Weigel NL, Ascoli M 2003 Identification of a transferable two amino acid motif (GT) present in the C-terminal tail of the human lutropin receptor that redirects internalized G protein-coupled receptors from a degradation to a recycling pathway. Mol Endocrinol 17:411-422
20. Vannier B, Loosfelt H, Meduri G, Pichon C, Milgrom E 1996 Anti-human FSH receptor monoclonal antibodies: immunochemical and immunocytochemical characterization of the receptor. Biochemistry 35:1358-1366
21. Loosfelt H, Pichon C, Jolivet A, Misrahi M, Caillou B, Jamous M, Vannier B, Milgrom E 1992 Two-subunit structure of the human thyrotropin receptor. Proc Natl Acad Sci USA 89:3765-3769
22. Misrahi M, Beau I, Ghinea N, Vannier B, Loosfelt H, Meduri G, Hai MTV, Milgrom E 1996 The LH/CG and FSH receptors: different molecular forms and intracellular traffic. Mol Cell Endocrinol 125:161-167
23. Lloyd CE, Ascoli M 1983 On the mechanisms involved in the regulation of the cell surface receptors for human choriogonadotropin and mouse epidermal growth factor in cultured Leydig tumor cells. J Cell Biol 96:521-526
24. Hoelscher SR, Sairam MR, Ascoli M 1991 The slow rate of internalization of deglycosylated hCG is not due to its inability to stimulate cAMP accumulation. Endocrinology 128:2837-2843
25. Ascoli M 1980 Degradation of the subunits of receptor-bound human choriogonadotropin by Leydig tumor cells. Biochim Biophys Acta 629:409-417
26. Nakamura K, Hipkin RW, Ascoli M 1998 The agonist-induced phosphorylation of the rat follitropin receptor (rFSHR) maps to the first and third intracellular loops. Mol Endocrinol 12:580-591
27. McGuinness MP, Linder CC, Morales CR, Heckert LL, Pikus J, Griswold MD 1994 Relationship of a mouse Sertoli cell line (MSC-1) to normal Sertoli cells. Biol Reprod 51:116-124
28. Rahman NA, Huhtaniemi IT 2001 Ovarian tumorogenesis in mice transgenic for murine inhibin α subunit promoter-driven simian virus 40 T-antigen: ontogeny, functional characteristics, and endocrine effects. Biol Reprod 64: 1122-1130
29. Novick P, Zerial M 1997 The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol 9:496-504
30. Riese RJ, Chapman HA 2000 Cathepsins and compartmentalization in antigen presentation. Curr Opin Immunol 12:107-113
31. Rozell TG, Wang H, Liu X, Segaloff DL 1995 Intracellular retention of mutant gonadotropin receptors results in loss of hormone binding activity of the follitropin receptor but not the lutropin/choriogonadotropin receptor. Mol Endocrinol 9:1727-1736
32. van Kerkhof P, Govers R, Alves dos Santos CM, Strous GJ 2000 Endocytosis and degradation of the growth hormone receptor are proteasome-dependent. J Biol Chem 275:1575-1580
33. Chaturvedi K, Bandari P, Chinen N, Howells RD 2001 Proteasome involvement in agonist-induced down-regulation of {micro} and δ opioid receptors. J Biol Chem 276:12345-12355
34. Hicke L 2001 Protein regulation by monoubiquitin. Nat Rev Mol Cell Bio 2:195-201
35. Marchese A, Benovic JL 2001 Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J Biol Chem 276:45509-45512
36. Brown MS, Goldstein JL 1986 A receptor mediated pathway for cholesterol homeostasis. Science 232:34-47
37. Mellman I 1996 Endocytosis and molecular sorting. Annu Rev Cell Biol 12:575-625
38. Koenig JA, Edwardson JM 1997 Endocytosis and recycling of G protein-coupled receptors. Trends Pharmacol Sci 18:276-287
39. Riezman H, Woodman PG, van Meer G, Marsh M 1997 Molecular mechanisms of endocytosis. Cell 91:731-738
40. Mukherjee S, Ghosh RN, Maxfield FR 1997 Endocytosis. Physiol Rev 77:759-803
41. Klausner RD, Ashwell G, van Renswoude J, Harford JB, Bridges KR 1983 Binding of apotransferrin to K562 cells: explanation of the transferrin cycle. Proc Natl Acad Sci USA 80:2263-2266
42. Dautry-Varsat A, Ciechanover A, Lodish HF 1984 pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci USA 80:2258-2262
43. Gage RM, Kim K-A, Cao TT, von Zastrow M 2001 A transplantable sorting signal that is sufficient to mediate rapid recycling of G protein-coupled receptors. J Biol Chem 276:44712-44720
44. Whistler JL, Enquist J, Marley A, Fong J, Gladher F, Tsuruda P, Murray SR, von Zastrow M 2002 Modulation of postendocytotic sorting of G protein-coupled receptors. Science 297:615-620
45. Cong M, Perry SJ, Hu LA, Hanson PI, Claing A, Lefkowitz RJ 2001 Binding of the β 2 adrenergic receptor to N-ethylmaleimide-sensitive factor regulates receptor recycling. J Biol Chem 276:45145-45152
46. Shapiro MJ, Trejo J, Zeng D, Coughlin SR 1996 Role of the thrombin receptor's cytoplasmic tail in intracellular trafficking. J Biol Chem 271:32874-32880
47. Trejo J, Coughlin SR 1999 The cytoplasmic tails of protease-activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J Biol Chem 274:2216-2224
48. Kishi H, Krishnamurthy H, Galet C, Bhaskaran RS, Ascoli M 1946 2002 Identification of a short linear sequence present in the C-terminal tail of the rat follitropin receptor that modulates arrestin-3 binding in a phosphorylation-independent fashion. J Biol Chem 277:21939-21942
49. Sprengel R, Braun T, Nikolics K, Segaloff DL, Seeburg PH 1990 The testicular receptor for follicle stimulating hormone: structure and functional expression of cloned cDNA. Mol Endocrinol 4:525-530
50. Fabritz J, Ryan S, Ascoli M 1998 Transfected cells express mostly the intracellular precursor of the lutropin/ choriogonadotropin receptor but this precursor binds choriogonadotropin with high affinity. Biochemistry 37: 664-672
51. Min L, Ascoli M 2000 Effect of activating and inactivating mutations on the phosphorylation and trafficking of the human lutropin/choriogonadotropin receptor. Mol Endocrinol 14:1797-1810
52. Margolskee R, McHenry-Rinde B, Horn R 1993 Panning transfected cells for electrophysiological studies. Biotechniques 15:906-911
53. Chen C, Okayama H 1987 High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752
54. Min L, Galet C, Ascoli M 2002 The association of arrestin-3 with the human lutropin/choriogonadotropin receptor depends mostly on receptor activation rather than on receptor phosphorylation. J Biol Chem 277:702-710
55. Krishnamurthy H, Galet C, Ascoli M 2003 The association of arrestin-3 with the follitropin receptor depends on receptor activation and phosphorylation. Mol Cell Endocrinol 204:127-140
56. Quintana J, Hipkin RW, Ascoli M 1993 A polyclonal antibody to a synthetic peptide derived from the rat FSH receptor reveals the recombinant receptor as a 74 kDa protein. Endocrinology 133:2098-2104
57. Segaloff DL, Ascoli M 1981 Removal of surface-bound human choriogonadotropin results in cessation of hormonal responses in cultured Leydig tumor cells. J Biol Chem 256:11420-11423
58. Pereira ME, Segaloff DL, Ascoli M, Eckstein F 1987 Inhibition of choriogonadotropin-activated steroidogenesis in cultured Leydig tumor cells by the Rp diastereoisomer of adenosine 3′,5′-cyclic phosphorothioate. J Biol Chem 262:6093-6100
59. Wang Z, Wang H, Ascoli M 1993 Mutation of a highly conserved acidic residue present in the second intracellular loop of G protein-coupled receptors does not impair hormone binding or signal transduction of the LH/CG receptor. Mol Endocrinol 7:85-93
60. Ascoli M, Pignataro OP, Segaloff DL 1989 The inositol phosphate/diacylglycerol pathway in MA-10 Leydig tumor cells. Activation by arginine vasopressin and lack of effect of epidermal growth factor and human choriogonadotropin. J Biol Chem 264:6674-6681
61. Ascoli M, Puett D 1978 Gonadotropin binding and stimulation of steroidogenesis in Leydig tumor cells. Proc Natl Acad Sci USA 75:99-102