Decreased degradation of internalized follicle-stimulating hormone caused by mutation of aspartic acid 6.30550 in a protein kinase-CK2 consensus sequence in the third intracellular loop of human follicle-stimulating hormone receptor

Biology of Reproduction

Volumn 84, Issue 6, 2011, Pages 1154-1163

  Kluetzman, Kerri S ^a,b   Thomas, Richard M ^b   Nechamen, Cheryl A ^b   Dias, James A ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

CK2; Endosome; Follicle stimulating hormone; FSH; FSH receptor; Lysosome; Mechanisms of hormone action

Indexed keywords

ASPARTIC ACID; CASEIN KINASE II; CYCLIC AMP; FOLLITROPIN RECEPTOR; GLYCINE; SUCROSE;

ARTICLE; BIOTRANSFORMATION; CELL STRAIN HEK293; CELL STRUCTURE; CONFOCAL MICROSCOPY; ENZYME ACTIVITY; GENE MUTATION; GENETIC TRANSFECTION; HORMONE ACTION; HORMONE BINDING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; ISOTOPE LABELING; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; WESTERN BLOTTING;

ASPARTIC ACID; CASEIN KINASE II; CONSENSUS SEQUENCE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HUMANS; MUTATION; RECEPTORS, FSH;

EID: 79958204366     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.087965     Document Type: Article

References (59)

1. Tapanainen JS, Vaskivuo T, Aittomäki K, Huhtaniemi IT. Inactivating FSH receptor mutations and gonadal dysfunction. Mol Cell Endocrinol 1998; 145:129-135.
2. Dias JA, Cohen BD, Lindau-Shepard B, Nechamen CA, Peterson AJ, Schmidt A. Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitam Horm 2002; 64:249-322.
3. Griswold MD, Heckert L, Linder C. The molecular biology of the FSH receptor. J Steroid Biochem Mol Biol 1995; 53:215-218.
4. Ulloa-Aguirre A, Zarinan T, Pasapera AM, Casas-Gonzalez P, Dias JA. Multiple facets of follicle-stimulating hormone receptor function. Endocrine 2007; 32:251-263.
5. Gromoll J, Simoni M, Nordhoff V, Behre HM, Geyter D, Nieschlag E. Functional and clinical consequences of mutations in the FSH receptor. Mol Cell Endocrinol 1996; 125:177-182.
6. Wayne C, Fan H, Cheng X, Richards J. Follicle-stimulating hormone induces multiple signaling cascades: evidence that activation of rous sarcoma oncogene, RAS, and the epidermal growth factor receptor are critical for Granulosa cell differentiation. Mol Endocrinol 2007; 21:1940-1957.
7. Hunzicker-Dunn M, Maizels ET. FSH signaling pathways in immature granulosa cells that regulate target gene expression: branching out from protein kinase A. Cell Signal 2006; 18:1351-1359.
8. Zeleznik AJ, Saxena D, Little-Ihrig L. Protein kinase B is obligatory for follicle-stimulating hormone-induced granulosa cell differentiation. Endocrinology 2003; 144:3985-3994.
9. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, Choe HW, Hofmann KP, Ernst OP. Crystal structure of opsin in its G-protein-interacting conformation. Nature 2008; 455:497-502.
10. Dias JA, Mahale SD, Nechamen CA, Davydenko O, Thomas RM, Ulloa- Aguirre A. Emerging roles for the FSH receptor adapter protein APPL1 and overlap of a putative 14-3-3tau interaction domain with a canonical G- protein interaction site. Mol Cell Endocrinol 2010; 329:17-25.
11. Troispoux C, Guillou F, Elalouf JM, Firsov D, Iacovelli L, De Blasi A, Combarnous Y, Reiter E. Involvement of G protein-coupled receptor kinases and arrestins in desensitization to follicle-stimulating hormone action. Mol Endocrinol 1999; 13:1599-1614.
12. Reiter E, Marion S, Robert F, Troispoux C, Boulay F, Guillou F, Crepieux P. Kinase-inactive G-protein-coupled receptor kinases are able to attenuate follicle-stimulating hormone-induced signaling. Biochem Biophys Res Commun 2001; 282:71-78.
13. Kara E, Crepieux P, Gauthier C, Martinat N, Piketty V, Guillou F, Reiter E. A phosphorylation cluster of five serine and threonine residues in the C- terminus of the follicle-stimulating hormone receptor is important for desensitization but not for beta-arrestin-mediated ERK activation. Mol Endocrinol 2006; 20:3014-3026.
14. Ascoli M. Functional consequences of the phosphorylation of the gonadotropin receptors. Biochem Pharmacol 1996; 52:1647-1655.
15. Nakamura K, Hipkin RW, Ascoli M. The agonist-induced phosphorylation of the rat follitropin receptor maps to the first and third intracellular loops. Mol Endocrinol 1998; 12:580-591.
16. Ferguson SS, Barak LS, Zhang J, Caron MG. G-protein-coupled receptor regulation: role of G-protein-coupled receptor kinases and arrestins. Can J Physiol Pharmacol 1996; 74:1095-1110.
17. Nakamura K, Krupnick JG, Benovic JL, Ascoli M. Signaling and phosphorylation-impaired mutants of the rat follitropin receptor reveal an activation- and phosphorylation-independent but arrestin-dependent path- way for internalization. J Biol Chem 1998; 273:24346-24354.
18. Krishnamurthy H, Galet C, Ascoli M. The association of arrestin-3 with CK2 CONSENSUS SEQUENCE IN FSHR 1163 the follitropin receptor depends on receptor activation and phosphorylation. Mol Cell Endocrinol 2003; 204:127-140.
19. Wehbi V, Tranchant T, Durand G, Musnier A, Decourtye J, Piketty V, Butnev VY, Bousfield GR, Crepieux P, Maurel MC, Reiter E. Partially deglycosylated equine LH preferentially activates beta-arrestin-dependent signaling at the follicle-stimulating hormone receptor. Mol Endocrinol 2010; 24:561-573.
20. Cohen BD, Bariteau JT, Magenis LM, Dias JA. Regulation of follitropin receptor cell surface residency by the ubiquitin-proteasome pathway. Endocrinology 2003; 144:4393-4402.
21. Pippig S, Andexinger S, Lohse MJ. Sequestration and recycling of beta 2-adrenergic receptors permit receptor resensitization. Mol Pharmacol 1995; 47:666-676.
22. Zhang J, Barak LS, Winkler KE, Caron MG, Ferguson SS. A central role for beta-arrestins and clathrin-coated vesicle-mediated endocytosis in beta2-adrenergic receptor resensitization. Differential regulation of receptor resensitization in two distinct cell types. J Biol Chem 1997; 272:27005-27014.
23. Tanowitz M, Hislop JN, von Zastrow M. Alternative splicing determines the post-endocytic sorting fate of G-protein-coupled receptors. J Biol Chem 2008; 283:35614-35621.
24. Innamorati G, Sadeghi HM, Tran NT, Birnbaumer M. A serine cluster prevents recycling of the V2 vasopressin receptor. Proc Natl Acad Sci U S A 1998; 95:2222-2226.
25. Shimizu A, Kawashima S. Kinetic study of internalization and degradation of 131I-labeled follicle-stimulating hormone in mouse Sertoli cells and its relevance to other systems. J Biol Chem 1989; 264:13632-13638.
26. Dias JA. Effect of transglutaminase substrates and polyamines on the cellular sequestration and processing of follicle-stimulating hormone by rat Sertoli cells. Biol Reprod 1986; 35:49-58.
27. Krishnamurthy H, Kishi H, Shi M, Galet C, Bhaskaran RS, Kirakawa T, Ascoli M. Postendocytotic trafficking of the follicle-stimulating hormone (FSH)-FSH receptor complex. Mol Endocrinol 2003; 17:2162-2176.
28. Gromoll J, Simoni M, Nieschlag E. An activating mutation of the follicle- stimulating hormone receptor autonomously sustains spermatogenesis in a hypophysectomized man. J Clin Endocrinol Metab 1996; 81:1367-1370.
29. 29. Allan CM, Garcia A, Spaliviero J, Jimenez M, Handelsman DJ. Maintenance of spermatogenesis by the activated human (Asp567Gly) FSH receptor during testicular regression due to hormonal withdrawal. Biol Reprod 2006; 74:938-944.
30. Lin FT, Chen W, Shenoy S, Cong M, Exum ST, Lefkowitz RJ. Phosphorylation of beta-arrestin2 regulates its function in internalization of beta(2)-adrenergic receptors. Biochemistry 2002; 41:10692-10699.
31. Korolchuk V, Banting G. Kinases in clathrin-mediated endocytosis. Biochem Soc Trans 2003; 31:857-860.
32. Dias JA, Nechamen CA, Atari R. Identifying protein interactors in gonadotropin action. Endocrine 2005; 26:241-247.
33. Torrecilla I, Spragg EJ, Poulin B, McWilliams PJ, Mistry SC, Blaukat A, Tobin AB. Phosphorylation and regulation of a G protein-coupled receptor by protein kinase CK2. J Cell Biol 2007; 177:127-137.
34. Rebholz H, Nishi A, Liebscher S, Nairn AC, Flajolet M, Greengard P. CK2 negatively regulates Gfalphags signaling. Proc Natl Acad Sci U S A 2009; 106:14096-14101.
35. Bar-Zvi D, Branton D. Clathrin-coated vesicles contain two protein kinase activities. Phosphorylation of clathrin beta-light chain by casein kinase II. J Biol Chem 1986; 261:9614-9621.
36. Cotlin LF, Siddiqui MA, Simpson F, Collawn JF. Casein kinase II activity is required for transferrin receptor endocytosis. J Biol Chem 1999; 274:30550-30556.
37. Poletto G, Vilardell J, Marin O, Pagano MA, Cozza G, Sarno S, Falques A, Itarte E, Pinna LA, Meggio F. The regulatory beta subunit of protein kinase CK2 contributes to the recognition of the substrate consensus sequence. A study with an eIF2 beta-derived peptide. Biochemistry 2008; 47:8317-8325.
38. Kelton CA, Cheng SV, Nugent NP, Schweickhardt RL, Rosenthal JL, Overton SA, Wands GD, Kuzeja JB, Luchette CA, Chappel SC. The cloning of the human follicle stimulating hormone receptor and its expression in COS-7, CHO, and Y-1 cells. Mol Cell Endocrinol 1992; 89:141-151.
39. Nechamen CA, Dias JA. Point mutations in follitropin receptor result in ER retention. Mol Cell Endocrinol 2003; 201:123-131.
40. Nechamen CA, Dias JA. Human follicle stimulating hormone receptor trafficking and hormone binding sites in the amino terminus. Mol Cell Endocrinol 2000; 166:101-110.
41. Lindau-Shepard B, Brumberg HA, Peterson AJ, Dias JA. Reversible immunoneutralization of human follitropin receptor. J Reprod Immunol 2001; 49:1-19.
42. Penner CG, Wang Z, Litchfield DW. Expression and localization of epitope-tagged protein kinase CK2. J Cell Biochem 1997; 64:525-537.
43. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994; 127:915-934.
44. Schmidt A, MacColl R, Lindau-Shepard B, Buckler DR, Dias JA. Hormone-induced conformational change of the purified soluble hormone binding domain of follitropin receptor complexed with single chain follitropin. J Biol Chem 2001; 276:23373-23381.
45. Thomas RM, Nechamen CA, Mazurkiewicz JE, Muda M, Palmer S, Dias JA. Follice-stimulating hormone receptor forms oligomers and shows evidence of carboxyl-terminal proteolytic processing. Endocrinology 2007; 148:1987-1995.
46. Allan CM, Lim P, Robson M, Spaliviero J, Handelsman DJ. Transgenic mutant D567G but not wild-type human FSH receptor overexpression provides FSH-independent and promiscuous glycoprotein hormone Sertoli cell signaling. Am J Physiol Endocrinol Metab 2009; 296:E1022-E1028.
47. Pagano MA, Poletto G, Di Maira G, Cozza G, Ruzzene M, Sarno S, Bain J, Elliott M, Moro S, Zagotto G, Meggio F, Pinna LA. Tetrabromocin- namic acid (TBCA) and related compounds represent a new class of specific protein kinase CK2 inhibitors. Chembiochem 2007; 8:129-139.
48. Oka JA, Weigel PH. Effects of hyperosmolarity on ligand processing and receptor recycling in the hepatic galactosyl receptor system. J Cell Biochem 1988; 36:169-183.
49. Nakata A, Kamiguchi H. Serine phosphorylation by casein kinase II controls endocytic L1 trafficking and axon growth. J Neurosci Res 2007; 85:723-734.
50. Nojiri M, Loyet KM, Klenchin VA, Kabachinski G, Martin TF. Caps activity in priming vesicle exocytosis requires CK2 phosphorylation. J Biol Chem 2009; 284:18707-18714.
51. Galet C, Ascoli M. A constitutively active mutant of the human lutropin receptor (hLHR-L457R) escapes lysosomal targeting and degradation. Mol Endocrinol 2006; 20:2931-2945.
52. Gage RM, Kim KA, Cao TT, von Zastrow M. A transplantable sorting signal that is sufficient to mediate rapid recycling of G protein-coupled receptors. J Biol Chem 2001; 276:44712-44720.
53. Whistler JL, Enquist J, Marley A, Fong J, Gladher F, Tsuruda P, Murray SR, Von Zastrow M. Modulation of postendocytic sorting of G protein- coupled receptors. Science 2002; 297:615-620.
54. Ascoli M. Lysosomal accumulation of the hormone-receptor complex during receptor-mediated endocytosis of human choriogonadotropin. J Cell Biol 1984; 99:1242-1250.
55. Donadeu F, Ascoli M. The differential effects of the gonadotropin receptors on aromatase expression in primary cultures of immature rat granulosa cells are highly dependent on the density of receptors expressed and the activation of the inositol phosphate cascade. Endocrinology 2005; 146:3907-3916.
56. Chaturvedi K, Bandari P, Chinen N, Howells RD. Proteasome involvement in agonist-induced down-regulation of mu and delta opioid receptors. J Biol Chem 2001; 276:12345-12355.
57. Murphy JE, Padilla BE, Hasdemir B, Cottrell GS, Bunnett NW. Endosomes: a legitimate platform for the signaling train. Proc Natl Acad Sci U S A 2009; 106:17615-17622.
58. Shenoy SK, McDonald PH, Kohout TA, Lefkowitz RJ. Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 2001; 294:1307-1313.
59. Calebiro D, Nikolaev VO, Gagliani MC, de Filippis T, Dees C, Tacchetti C, Persani L, Lohse MJ. Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 2009; 7:e1000172.