The adapter protein APPL1 links FSH receptor to inositol 1,4,5-trisphosphate production and is implicated in intracellular Ca 2+ mobilization

Endocrinology

Volumn 152, Issue 4, 2011, Pages 1691-1701

  Thomas, Richard M ^a   Nechamen, Cheryl A ^a   Mazurkiewicz, Joseph E ^b,c   Ulloa Aguirre, Alfredo ^d   Dias, James A ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c ALBANY MEDICAL COLLEGE   (United States)

^d INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTER PROTEIN CONTAINING PLECKSTRIN HOMOLOGY DOMAIN PHOSPHOTYROSINE BINDING DOMAIN AND LEUCINE ZIPPER MOTIF; ADAPTOR PROTEIN; ALANINE; CALCIUM ION; CYCLIC AMP; ESTRADIOL; FOLLITROPIN; FOLLITROPIN RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE; MUTANT PROTEIN; PROGESTERONE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CONTROLLED STUDY; GRANULOSA CELL; HORMONE BINDING; HUMAN; HUMAN CELL; KIDNEY CELL; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOTTING, WESTERN; CALCIUM; CELL LINE; CYCLIC AMP; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; HUMANS; IMMUNOPRECIPITATION; INOSITOL 1,4,5-TRISPHOSPHATE; MUTATION; PROGESTERONE; PROTEIN BINDING; RATS; RECEPTORS, FSH;

EID: 79953171125     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-1353     Document Type: Article

References (56)

1. Dias JA, Cohen BD, Lindau-Shepard B, Nechamen CA, Peterson AJ, Schmidt A 2002 Molecular, structural, and cellular biology of follitropin and follitropin receptor. Vitam Horm 64:249-322 (Pubitemid 135763167)
2. Fan QR, Hendrickson WA 2005 Structure of human follicle-stimulating hormone in complex with its receptor. Nature 433:269-277
3. Simoni M, Gromoll J, Nieschlag E 1997 The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev 18:739-773 (Pubitemid 28009566)
4. Stocco DM, Wang X, Jo Y, Manna PR 2005 Multiple Signaling Pathways Regulating Steroidogenesis and Steroidogenic Acute Regulatory Protein Expression: More Complicated than We Thought. Mol Endocrinol 19:2647-2659 (Pubitemid 41577240)
5. Tremblay JJ, Hamel F, Viger RS 2002 Protein kinase A-dependent cooperation between GATA and CCAAT/enhancer-binding protein transcription factors regulates steroidogenic acute regulatory protein promoter activity. Endocrinology 143:3935-3945 (Pubitemid 35244373)
6. Richards JS 2001 New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol Endocrinol 15:209-218 (Pubitemid 32128702)
7. Bos JL 2006 Epac proteins: multi-purpose cAMP targets. Trends Biochem Sci 31:680-686 (Pubitemid 44791945)
8. Gonzalez-Robayna IJ, Falender AE, Ochsner S, Firestone GL, Richards JS 2000 Follicle-Stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-lnduced kinase (Sgk): evidence for A kinase-independent signaling by FSH in granulosa cells. Mol Endocrinol 14: 1283-1300 (Pubitemid 32260488)
9. Hunzicker-Dunn M, Maizels ET 2006 FSH signaling pathways in immature granulosa cells that regulate target gene expression: branching out from protein kinase A. Cell Signal 18:1351-1359
10. Zeleznik AJ, Saxena D, Little-Ihrig L 2003 Protein kinase B is obligatory for follicle-stimulating hormone-induced granulosa cell differentiation. Endocrinology 144:3985-3994 (Pubitemid 37088754)
11. McDonald CA, Millena AC, Reddy S, Finlay S, Vizcarra J, Khan SA, Davis JS 2006 Follicle-stimulating hormone-induced aromatase in immature rat Sertoli cells requires an active phosphatidylinositol 3-kinase pathway and is inhibited via the mitogen-activated protein kinase signaling pathway. Mol Endocrinol 20: 608-618 (Pubitemid 43291212)
12. Maizels ET, Cottom J, Jones JC, Hunzicker-Dunn M 1998 Follicle stimulating hormone (FSH) activates the p38 mitogen-activated protein kinase pathway, inducing small heat shock protein phosphorylation and cell rounding in immature rat ovarian granulosa cells. Endocrinology 139:3353-3356 (Pubitemid 28512368)
13. Cameron MR, Foster JS, Bukovsky A, Wimalasena J 1996 Activation of mitogen-activated protein kinases by gonadotropins and cyclic adenosine 5′-monophosphates in porcine granulosa cells. Biol Reprod 55:111-119 (Pubitemid 26293147)
14. Das S, Maizels ET, DeManno D, St CE, Adam SA, Hunzicker-Dunn M 1996 A stimulatory role of cyclic adenosine 3′,5′-monophosphate in follicle-stimulating hormone-activated mitogen-activated protein kinase signaling pathway in rat ovarian granulosa cells. Endocrinology 137:967-974
15. Cottom J, Salvador LM, Maizels ET, Reierstad S, Park Y, Carr DW, Davare MA, Hell JW, Palmer SS, Dent P, Kawakatsu H, Ogata M, Hunzicker-Dunn M 2003 Follicle-stimulating hormone activates extracellular signal-regulated kinase but not extracellular signal-regulated kinase kinase through a 100-kDa phosphotyrosine phosphatase. J Biol Chem 278:7167-7179 (Pubitemid 36800716)
16. Choi KC, Kang SK, Tai CJ, Auersperg N, Leung PC 2002 Follicle-stimulating hormone activates mitogen-activated protein kinase in preneoplastic and neoplastic ovarian surface epithelial cells. J Clin Endocrinol Metab 87:2245-2253 (Pubitemid 34521516)
17. Flores JA, Veldhuis JD, Leong DA 1990 Follicle-stimulating hormone evokes an increase in intracellular free calcium ion concentrations in single ovarian (granulosa) cells. Endocrinology 127:3172-3179
18. Flores JA, Leong DA, Veldhuis JD 1992 Is the calcium signal induced by follicle-stimulating hormone in swine granulosa cells mediated by adenosine cyclic 3′,5′-monophosphate-dependent protein kinase? Endocrinology 130:1862-1866
19. Gorczynska E, Spaliviero J, Handelsman DJ 1996 Cyclic adenosine 3′,5′-monophosphate-independent regulation of cytosolic calcium in Sertoli cells. Endocrinology 137:2617-2625
20. Grasso P, Reichert Jr LE 1989 Follicle-stimulating hormone receptor-mediated uptake of 45 Ca2+ by proteoliposomes and cultured rat sertoli cells: evidence for involvement of voltage-activated and voltage-independent calcium channels. Endocrinology 125:3029-3036 (Pubitemid 20010679)
21. Grasso P, Reichert Jr LE 1990 Follicle-stimulating hormone receptor-mediated uptake of 45Ca2+ by cultured rat Sertoli cells does not require activation of cholera toxin- or pertussis toxin-sensitive guanine nucleotide binding proteins or adenylate cyclase. Endocrinology 127:949-956 (Pubitemid 20248143)
22. 2+-influx. Mol Endocrinol 20:2514-2527
23. Gorczynska E, Handelsman DJ 1991 The role of calcium in follicle-stimulating hormone signal transduction in Sertoli cells. J BiolChem 266:23739-23744 (Pubitemid 21908859)
24. 2+ channels in rat sertoli cells. Endocrinology 149:1031-1037
25. Donadeu FX, Ascoli M 2005 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 146:3907-3916 (Pubitemid 41175761)
26. Andric N, Ascoli M 2006 A delayed gonadotropin-dependent and growth factor-mediated activation of the extracellular signal-regulated kinase 1/2 cascade negatively regulates aromatase expression in granulosa cells. Mol Endocrinol 20:3308-3320 (Pubitemid 44833573)
27. Ulloa-Aguirre A, Uribe A, Zarinan T, Bustos-Jaimes I, Perez-Solis MA, Dias JA 2007 Role of the intracellular domains of the human FSH receptor in G(alphaS) protein coupling and receptor expression. Mol Cell Endocrinol 260- 262:153-162 (Pubitemid 44792348)
28. Cohen BD, Nechamen CA, Dias JA 2004 Human follitropin receptor (FSHR) interacts with the adapter protein 14-3-3τ. Mol Cell Endocrinol 220:1-7 (Pubitemid 38757876)
29. Nechamen CA, Thomas RM, Cohen BD, Acevedo G, Poulikakos PI, Testa JR, Dias JA 2004 Human follicle-stimulating hormone (FSH) receptor interacts with the adaptor protein APPL1 in HEK293 cells: potential involvement of the PI3K pathway in FSH signaling. Biol Reprod 71:629-636 (Pubitemid 38970540)
30. Nechamen CA, Thomas RM, Dias JA 2007 APPL1, APPL2, Akt2 and FOXO1a interact with FSHR in a potential signaling complex. Mol Cell Endocrinol 260-262:93-99 (Pubitemid 44792336)
31. Lindau-Shepard B, Brumberg HA, Peterson AJ, Dias JA 2001 Reversible immunoneutralization of human follitropin receptor. J Reprod Immunol 49:1-19 (Pubitemid 32007945)
32. Miller JH 1972 Experiments in molecular genetics. Cold Spring Harbor Laboratory: 352-355
33. Kelton CA, Cheng SV, Nugent NP, Schweickhardt RL, Rosenthal JL, Overton SA, Wands GD, Kuzeja JB, Luchette CA, Chappel SC 1992 The cloning of the human follicle stimulating hormone receptor and its expression in COS-7, CHO, and Y-1 cells. Mol Cell Endocrinol 89:141-151
34. Nechamen CA, Dias JA 2003 Point mutations in follitropin receptor result in ER retention. Mol Cell Endocrinol 201:123-131 (Pubitemid 36434288)
35. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
36. Bjerrum OJ, Schafer-Nielsen C 1986 Buffer systems and transfer parameters for semi-dry electroblotting with horizontal apparatus. Analytical Electrophoresis. Deerfield Beach, FL: VCH Publishers; 315
37. Nechamen CA, Dias JA 2000 Human follicle stimulating hormone receptor trafficking and hormone binding sites in the amino terminus. Mol Cell Endocrinol 166:101-110
38. Mahale SD, Cavanagh J, Schmidt A, MacColl R, Dias JA 2001 Autologous biological response modification of the gonadotropin receptor. J Biol Chem 276:12410-12419
39. Liu WK, Burleigh BD, Ward DN 1981 Steroid and plasminogen activator production by cultured rat granulosa cells in response to hormone treatment. Mol Cell Endocrinol 21:63-73 (Pubitemid 11209677)
40. Ulloa-Aguirre A, Stanislaus D, Arora V, Vaananen J, Brothers S, Janovick JA, Conn PM 1998 The third intracellular loop of the rat gonadotropin-releasing hormone receptor couples the receptor to Gs- and Gq/11-mediated signal transduction pathways: evidence from loop fragment transfection in GGH3 cells. Endocrinology 139: 2472-2478 (Pubitemid 28513774)
41. Thomas RM, Nechamen CA, Mazurkiewicz JE, Muda M, Palmer S, Dias JA 2007 Follice-stimulating hormone receptor forms oligomers and shows evidence of carboxyl-terminal proteolytic processing. Endocrinology 148:1987-1995 (Pubitemid 46997064)
42. Timossi C, Maldonado D, Vizcaino A, Lindau-Shepard B, Conn PM, Ulloa-Aguirre A 2002 Structural determinants in the second intracellular loop of the human follicle-stimulating hormone receptor are involved in G(s) protein activation. Mol Cell Endocrinol 189:157-168 (Pubitemid 34229173)
43. Nishi Y, Yanase T, Mu Y, Oba K, Ichino I, Saito M, Nomura M, Mukasa C, Okabe T, Goto K, Takayanagi R, Kashimura Y, Haji M, Nawata H 2001 Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor. Endocrinology 142:437-445
44. Yu FQ, Han CS, Yang W, Jin X, Hu ZY, Liu YX 2005 Activation of the p38 MAPK pathway by follicle-stimulating hormone regulates steroidogenesis in granulosa cells differentially. J Endocrinol 186:85-96 (Pubitemid 41015667)
45. Babu PS, Krishnamurthy H, Chedrese PJ, Sairam MR 2000 Activation of extracellular-regulated kinase pathways in ovarian granulosa cells by the novel growth factor type 1 follicle-stimulating hormone receptor: role in hormone signaling and cell proliferation. J Biol Chem 275:27615-27626
46. Berridge MJ 1993 Inositol trisphosphate and calcium signalling. Nature 361:315-325 (Pubitemid 23041621)
47. Touyz RM, Jiang L, Ram Sairam M 2000 Follicle-stimulating hormone mediated calcium signaling by the alternatively spliced growth factor type I receptor. Biol Reprod 62:1067-1074 (Pubitemid 30173823)
48. Suh PG, Park JI, Manzoli L, Cocco L, Peak JC, Katan M, Fukami K, Kataoka T, Yun S, Ryu SH 2008 Multiple roles of phosphoinositide-specific phospholipase C isozymes. BMB Rep 41:415-434 (Pubitemid 351914885)
49. Feng JF, Rhee SG, Im MJ 1996 Evidence that phospholipase delta1 is the effector in the Gh (transglutaminase II)-mediated signaling. J Biol Chem 271:16451-16454 (Pubitemid 26238993)
50. 2+ in isolated bovine luteal cells. J Biol Chem 262:8515-8521
51. Laurent E, Mockel J, Van SJ, Graff I, Dumont JE 1987 Dual activation by thyrotropin of the phospholipase C and cyclic AMP cascades in human thyroid. Mol Cell Endocrinol 52:273-278 (Pubitemid 17106989)
52. Tan Y, You H, Coffey FJ, Wiest DL, Testa JR 2010 Appl1 is dispensable for Akt signaling in vivo and mouse T-cell development. Genesis 48:531-539
53. Tan Y, You H, Wu C, Altomare DA, Testa JR 2010 Appl1 is dispensable for mouse development, and loss of Appl1 has growth factor-selective effects on Akt signaling in murine embryonic fibroblasts. J Biol Chem 285:6377-6389
54. Nechamen CA, Thomas RM, Dias JA 2007 APPL1, APPL2, Akt2 and FOXO1a interact with FSHR in a potential signaling complex. Mol Cell Endocrinol 260:93-99 (Pubitemid 44792336)
55. Deepa SS, Dong LQ 2009 APPL1: role in adiponectin signaling and beyond. Am J Physiol Endocrinol Metab 296:E22-E36
56. Nishi Y, Yanase T, Mu YM, Oba K, Ichino I, Saito M, Nomura M, Mukasa C, Okabe T, Goto K, Takayanagi R, Kashimura Y, Haji M, Nawata H 2001 Establishment and characterization of a steroidogenic human granulosa-like tumor cell line, KGN, that expresses functional follicle-stimulating hormone receptor. Endocrinology 142:437-445 (Pubitemid 32183706)