Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway

Molecular Endocrinology

Volumn 22, Issue 4, 2008, Pages 924-936

  Panigone, Sara ^a,b   Hsieh, Minnie ^a,c   Fu, Maoyong ^a   Persani, Luca ^b   Conti, Marco ^a,c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; AMPHIREGULIN; BETACELLULIN; CYCLIC AMP; EPIDERMAL GROWTH FACTOR; EPIREGULIN; FORSKOLIN; ILOMASTAT; LUTEINIZING HORMONE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NEUTRALIZING ANTIBODY; PROTEINASE INHIBITOR; TAPI 1; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GRANULOSA CELL; HORMONE ACTION; IMMUNOPRECIPITATION; OOCYTE MATURATION; OVULATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIPEPTIDES; EPIDERMAL GROWTH FACTOR; FEMALE; GLYCOPROTEINS; HYDROXAMIC ACIDS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUTEINIZING HORMONE; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; OOCYTES; OVARIAN FOLLICLE; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TYRPHOSTINS;

EID: 41649091053     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2007-0246     Document Type: Article

References (43)

1. Richards JS 2001 New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol Endocrinol 15:209-218
2. Conti M 2002 Specificity of the cyclic adenosine 3′,5′- monophosphate signal in granulosa cell function. Biol Reprod 67:1653-1661
3. Wayne CM, Fan HY, Cheng X, Richards JS 2007 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 21:1940-1957
4. Peng XR, Hsueh AJ, LaPolt PS, Bjersing L, Ny T 1991 Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 129:3200-3207
5. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682-684
6. Ashkenazi H, Cao X, Motola S, Popliker M, Conti M, Tsafriri A 2005 Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146:77-84
7. Sekiguchi T, Mizutani T, Yamada K, Kajitani T, Yazawa T, Yoshino M, Miyamoto K 2004 Expression of epiregulin and amphiregulin in the rat ovary. J Mol Endocrinol 33:281-291
8. 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
9. Jo M, Curry Jr TE 2006 Luteinizing hormone-induced RUNX1 regulates the expression of genes in granulosa cells of rat periovulatory follicles. Mol Endocrinol 20:2156-2172
10. Tirone E, D'Alessandris C, Hascall VC, Siracusa G, Salustri A 1997 Hyaluronan synthesis by mouse cumulus cells is regulated by interactions between follicle-stimulating hormone (or epidermal growth factor) and a soluble oocyte factor (or transforming growth factor β1). J Biol Chem 272:4787-4794
11. Orly J, Rei Z, Greenberg NM, Richards JS 1994 Tyrosine kinase inhibitor AG18 arrests follicle-stimulating hormone-induced granulosa cell differentiation: use of reverse transcriptase-polymerase chain reaction assay for multiple messenger ribonucleic acids. Endocrinology 134:2336-2346
12. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M 2007 Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27:1914-1924
13. Holbro T, Hynes NE 2004 ErbB receptors: directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 44:195-217
14. Yarden Y, Sliwkowski MX 2001 Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2:127-137
15. Daaka Y, Luttrell LM, Lefkowitz RJ 1997 Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A. Nature 390:88-91
16. Liebmann C 2001 Regulation of MAP kinase activity by peptide receptor signalling pathway: paradigms of multiplicity. Cell Signal 13:777-785
17. Lopez-Ilasaca M, Crespo P, Pellici PG, Gutkind JS, Wetzker R 1997 Linkage of G protein-coupled receptors to the MAPK signaling pathway through PI 3-kinase γ. Science 275:394-397
18. Daub H, Weiss FU, Wallasch C, Ullrich A 1996 Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379:557-560
19. Wetzker R, Bohmer FD 2003 Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat Rev Mol Cell Biol 4:651-657
20. Daub H, Wallasch C, Lankenau A, Herrlich A, Ullrich A 1997 Signal characteristics of G protein-transactivated EGF receptor. EMBO J 16:7032-7044
21. Bokemeyer D, Schmitz U, Kramer HJ 2000 Angiotensin II-induced growth of vascular smooth muscle cells requires an Src-dependent activation of the epidermal growth factor receptor. Kidney Int 58:549-558
22. Luttrell LM, Della Rocca GJ, van Biesen T, Luttrell DK, Lefkowitz RJ 1997 Gβγ subunits mediate Src-dependent phosphorylation of the epidermal growth factor receptor. A scaffold for G protein-coupled receptor-mediated Ras activation. J Biol Chem 272:4637-4644
23. Zwick E, Daub H, Aoki N, Yamaguchi-Aoki Y, Tinhofer I, Maly K, Ullrich A 1997 Critical role of calcium-dependent epidermal growth factor receptor transactivation in PC12 cell membrane depolarization and bradykinin signaling. J Biol Chem 272:24767-24770
24. Eguchi S, Numaguchi K, Iwasaki H, Matsumoto T, Yamakawa T, Utsunomiya H, Motley ED, Kawakatsu H, Owada KM, Hirata Y, Marumo F, Inagami T 1998 Calcium-dependent epidermal growth factor receptor transactivation mediates the angiotensin II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. J Biol Chem 273:8890-8896
25. i elevation can substitute for receptor activation. J Biol Chem 273:23110-23117
26. Tsai W, Morielli AD, Peralta EG 1997 The m1 muscarinic acetylcholine receptor transactivates the EGF receptor to modulate ion channel activity. EMBO J 16:4597-4605
27. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A 1999 EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402:884-888
28. Fischer OM, Hart S, Gschwind A, Ullrich A 2003 EGFR signal transactivation in cancer cells. Biochem Soc Trans 31:1203-1208
29. Rojas M, Yao S, Lin YZ 1996 Controlling epidermal growth factor (EGF)-stimulated Ras activation in intact cells by a cell-permeable peptide mimicking phosphorylated EGF receptor. J Biol Chem 271:27456-27461
30. Downward J, Parker P, Waterfield MD 1984 Autophosphorylation sites on the epidermal growth factor receptor. Nature 311:483-485
31. Saito T, Okada S, Ohshima K, Yamada E, Sato M, Uehara Y, Shimizu H, Pessin JE, Mori M 2004 Differential activation of epidermal growth factor (EGF) receptor downstream signaling pathways by betacellulin and EGF. Endocrinology 145:4232-4243
32. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ 2002 Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143:2221-2232
33. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS 2006 Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 20:1352-1365
34. Freimann S, Ben-Ami I, Dantes A, Ron-El R, Amsterdam A 2004 EGF-like factor epiregulin and amphiregulin expression is regulated by gonadotropins/cAMP in human ovarian follicular cells. Biochem Biophys Res Commun 324:829-834
35. Stover DR, Becker M, Liebetanz J, Lydon NB 1995 Src phosphorylation of the epidermal growth factor receptor at novel sites mediates receptor interaction with Src and P85α. J Biol Chem 270:15591-15597
36. Sela-Abramovich S, Chorev E, Galiani D, Dekel N 2005 Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. Endocrinology 146:1236-1244
37. Fan HY, Huo LJ, Chen DY, Schatten H, Sun QY 2004 Protein kinase C and mitogen-activated protein kinase cascade in mouse cumulus cells: cross talk and effect on meiotic resumption of oocyte. Biol Reprod 70:1178-1187
38. Su YQ, Denegre JM, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ 2003 Oocyte-dependent activation of mitogen-activated protein kinase (ERK1/2) in cumulus cells is required for the maturation of the mouse oocyte-cumulus cell complex. Dev Biol 263:126-138
39. Kalma Y, Granot I, Galiani D, Barash A, Dekel N 2004 Luteinizing hormone-induced connexin 43 down-regulation: inhibition of translation. Endocrinology 145:1617-1624
40. Singh AB, Harris RC 2005 Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal 17:1183-1193
41. 2+ signalling by epidermal growth factor receptor. FEBS Lett 461:217-222
42. Park OK, Mayo KE 1991 Transient expression of progesterone receptor messenger RNA in ovarian granulosa cells after the preovulatory luteinizing hormone surge. Mol Endocrinol 5:967-978
43. Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW, Richards JS 2000 Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc Natl Acad Sci USA 97:4689-4694