LH-induced neuregulin 1 (nrg1) type iii transcripts control granulosa cell differentiation and oocyte maturation

Molecular Endocrinology

Volumn 25, Issue 1, 2011, Pages 104-116

  Noma, Noritaka ^a   Kawashima, Ikko ^a,b   Fan, Heng Yu ^b   Fujita, Youko ^a   Kawai, Tomoko ^a   Tomoda, Yoshinori ^a   Mihara, Toshihiro ^a   Richards, JoAnne S ^b   Shimada, Masayuki ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIREGULIN; CCAAT ENHANCER BINDING PROTEIN BETA; CHORIONIC GONADOTROPIN; EPIDERMAL GROWTH FACTOR RECEPTOR; LUTEINIZING HORMONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEU DIFFERENTIATION FACTOR; PROGESTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; CUMULUS CELL; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION; GENETIC TRANSCRIPTION; GRANULOSA CELL; HORMONE SYNTHESIS; LUTEINIZATION; MOUSE; NONHUMAN; OOCYTE MATURATION; OVULATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELLS, CULTURED; CHORIONIC GONADOTROPIN; CUMULUS CELLS; EMBRYONIC DEVELOPMENT; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION; GLYCOPROTEINS; GRANULOSA CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; LUTEINIZING HORMONE; MICE; MOLECULAR SEQUENCE DATA; NEUREGULIN-1; OOCYTES; OVULATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, MESSENGER; TIME FACTORS;

EID: 78650889081     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0225     Document Type: Article

References (62)

1. Richards JS 1994 Hormonal control of gene expression in the ovary. Endocr Rev 15: 725-751
2. Richards JS, Russell DL, Robker RL, Dajee M, Alliston TN 1998 Molecular mechanisms of ovulation and luteinization. Mol Cell Endocrinol 145: 47-54
3. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O 1993 Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A 190: 11162-11166
4. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, SmithiesO1998 Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 95: 15677-15682
5. Robker RL, Richards JS 1998 Hormone-induced proliferation and differentiation of granulosa cells: A coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol Endocrinol 12: 924-940
6. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery Jr CA, Shyamala G, Conneely OM, O'Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9: 2266-2278
7. 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
8. Richards JS 2001 New signaling pathways for hormones and cyclic adenosine 3',5'-monophosphate action in endocrine cells. Mol Endocrinol 15: 209-218
9. Conti M, Hsieh M, Park JY, Su YQ 2006 Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol 20: 715-723
10. Dekel N 2009 Master regulators of female fertility. N Engl J Med 361: 718-719
11. Fan HY, Liu Z, Shimada M, Sterneck E, Johnson PF, Hedrick SM, Richards JS 2009 MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324: 938-941
12. 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
13. Park Y, Maizels ET, Feiger ZJ, Alam H, Peters CA, Woodruff TK, Unterman TG, Lee EJ, Jameson JL, Hunzicker-Dunn M 2005 Induction of cyclin D2 in rat granulosa cells requires FSH-dependent relief from FOXO1 repression coupled with positive signals from Smad. J Biol Chem 280: 9135-9148
14. Fan HY, Liu Z, Cahill N, Richards JS 2008 Targeted disruption of Pten in ovarian granulosa cells enhances ovulation and extends the life span of luteal cells. Mol Endocrinol 22: 2128-2140
15. Alam H, Weck J, Maizels E, Park Y, Lee EJ, Ashcroft M, Hunzicker- DunnM2009 Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxiainducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology 150: 915-928
16. Fan HY, Shimada M, Liu Z, Cahill N, Noma N, Wu Y, Gossen J, Richards JS 2008 Selective expression of KrasG12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation. Development 135: 2127-2137
17. Fan HY, Richards JS 2010 Minirevew: Physiological and pathological actions of RAS in the ovary. Mol Endocrinol 24: 286-298
18. 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
19. 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
20. 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
21. Espey LL, Richards JS 2002 Temporal and spatial patterns of ovarian gene transcription following an ovulatory dose of gonadotropin in the rat. Biol Reprod 67: 1662-1670
22. 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
23. Downs SM, Chen J 2008 EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes. Mol Reprod Dev 75: 105-114
24. Motola S, Popliker M, Tsafriri A 2008 Response of follicle cells to ovulatory stimuli within the follicle and in primary culture. Mol Cell Endocrinol 282: 26-31
25. Reizel Y, Elbaz J, Dekel N 2010 Sustained activity of the EGF receptor is an absolute requisite for LH-induced oocyte maturation and cumulus expansion. Mol Endocrinol 24: 402-411
26. Citri A, Yarden Y 2006 EGF-ERBB signalling: Towards the systems level. Nat Rev Mol Cell Biol 7: 505-516
27. Wallasch C, Weiss FU, Niederfellner G, Jallal B, Issing W, Ullrich A 1995 Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3. EMBO J 14: 4267-4275
28. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, Klapper L, Lavi S, Seger R, Ratzkin BJ, Sela M, Yarden Y 1996 Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J 15: 2452-2467 (Pubitemid 26151185)
29. Pinkas-Kramarski R, Shelly M, Glathe S, Ratzkin BJ, Yarden Y 1996 Neu differentiation factor/neuregulin isoforms activate distinct receptor combinations. J Biol Chem 271: 19029-19032
30. Rahmatullah M, Schroering A, Rothblum K, Stahl RC, Urban B, Carey DJ 1998 Synergistic regulation of Schwann cell proliferation by heregulin and forskolin. Mol Cell Biol 18: 6245-6252
31. Kita YA, Barff J, Luo Y, Wen D, Brankow D, Hu S, Liu N, Prigent SA, Gullick WJ, Nicolson M 1994 NDF/heregulin stimulates the phosphorylation of Her3/erbB3. FEBS Lett 349: 139-143
32. Shirakabe K, Wakatsuki S, Kurisaki T, Fujisawa-Sehara A 2001 Roles of Meltrin beta /ADAM19 in the processing of neuregulin. J Biol Chem 276: 9352-9358
33. Meyer D, Yamaai T, Garratt A, Riethmacher-Sonnenberg E, Kane D, Theill LE, Birchmeier C 1997 Isoform-specific expression and function of neuregulin. Development 124: 3575-3586
34. Murphy BD 2000 Models of luteinization. Biol Reprod 63: 2-11
35. Hsieh M, Boerboom D, Shimada M, Lo Y, Parlow AF, Luhmann UF, Berger W, Richards JS 2005 Mice null for Frizzled4 (Fzd4+/-) are infertile and exhibit impaired corpora lutea formation and function. Biol Reprod 73: 1135-1146
36. Santiskulvong C, Rozengurt E 2003 Galardin (GM 6001), a broadspectrum matrix metalloproteinase inhibitor, blocks bombesinand LPA-induced EGF receptor transactivation and DNA synthesis in rat-1 cells. Exp Cell Res 290: 437-446
37. 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
38. Falls DL 2003 Neuregulins: Functions, forms, and signaling strategies. Exp Cell Res 284: 14-30
39. Esper RM, Pankonin MS, Loeb JA 2006 Neuregulins: Versatile growth and differentiation factors in nervous system development and human disease. Brain Res Rev 51: 161-175
40. Nave KA, Salzer JL 2006 Axonal regulation of myelination by neuregulin 1. Curr Opin Neurobiol 16: 492-500
41. Hu X, Hicks CW, He W, Wong P, Macklin WB, Trapp BD, Yan R 2006 Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 9: 1520-1525
42. Savonenko AV, Melnikova T, Laird FM, Stewart KA, Price DL, Wong PC 2008 Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Proc Natl Acad Sci USA 105: 5585-5590
43. Wang JY, Miller SJ, Falls DL 2001 The N-terminal region of neuregulin isoforms determines the accumulation of cell surface and released neuregulin ectodomain. J Biol Chem 276: 2841-2851
44. Curry Jr TE, Osteen KG 2003 The matrix metalloproteinase system: Changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 24: 428-465
45. Richards JS 2005 Ovulation: New factors that prepare the oocyte for fertilization. Mol Cell Endocrinol 234: 75-79
46. Yamashita Y, Kawashima I, Yanai Y, Nishibori M, Richards JS, Shimada M 2007 Hormone-induced expression of tumor necrosis factor alpha-converting enzyme/A disintegrin and metallopro- tease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor. Endocrinology 148: 6164-6175
47. Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul DL, Lampe PD, Jaffe LA 2008 Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: One of two paths to meiotic resumption. Development 135: 3229-3238
48. Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, Wang H, Ke H, Nikolaev VO, Jaffe LA 2009 Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136: 1869-1878
49. Vaccari S, Weeks JL 2nd, Hsieh M, Menniti FS, Conti M 2009 Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod 81: 595-604
50. Han SJ, Vaccari S, Nedachi T, Andersen CB, Kovacina KS, Roth RA, Conti M 2006 Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. EMBO J 25: 5716-5725
51. Shimada M, Ito J, Yamashita Y, Okazaki T, Isobe N 2003 Phosphatidylinositol 3-kinase in cumulus cells is responsible for both suppression of spontaneous maturation and induction of gonadotropin- stimulated maturation of porcine oocytes. J Endocrinol 179: 25-34
52. Brevini TA, Cillo F, Antonini S, Gandolfi F 2007 Cytoplasmic remodelling and the acquisition of developmental competence in pig oocytes. Anim Reprod Sci 98: 23-38
53. Ferreira EM, Vireque AA, Adona PR, Meirelles FV, Ferriani RA, Navarro PA 2009 Cytoplasmic maturation of bovine oocytes: Structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71: 836-848
54. Funahashi H, Cantley TC, Day BN 1997 Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol Reprod 57: 49-53
55. Shimada M, Nishibori M, Isobe N, Kawano N, Terada T 2003 Luteinizing hormone receptor formation in cumulus cells surrounding porcine oocytes and its role during meiotic maturation of porcine oocytes. Biol Reprod 68: 1142-1149 (Pubitemid 36359101)
56. Lonergan P, Faerge I, Hyttel PM, Boland M, Fair T 2003 Ultrastructural modifications in bovine oocytes maintained in meiotic arrest in vitro using roscovitine or butyrolactone. Mol Reprod Dev 64: 369-378
57. Cross PC, Brinster RL 1970 In vitro development of mouse oocytes. Biol Reprod 3: 298-307
58. Lawlor MA, Alessi DR 2001 PKB/Akt: A key mediator of cell proliferation, survival and insulin responses? J Cell Sci 114: 2903-2910
59. Shimada M, Yanai Y, Okazaki T, Noma N, Kawashima I, Mori T, Richards JS 2008 Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization. Development 135: 2001-2011
60. Shimada M, Yanai Y, Okazaki T, Yamashita Y, Sriraman V, Wilson MC, Richards JS 2007 Synaptosomal-associated protein 25 gene expression is hormonally regulated during ovulation and is involved in cytokine/chemokine exocytosis from granulosa cells. Mol Endocrinol 21: 2487-2502
61. Doyle KM, Russell DL, Sriraman V, Richards JS 2004 Coordinate transcription of the ADAMTS-1 gene by luteinizing hormone and progesterone receptor. Mol Endocrinol 18: 2463-2478
62. Sato C, Shimada M, Mori T, Kumasako Y, Otsu E, Watanabe H, Utsunomiya T 2007 Assessment of human oocyte developmental competence by cumulus cell morphology and circulating hormone profile. Reprod Biomed Online 14: 49-56