Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation

Molecular and Cellular Biology

Volumn 27, Issue 5, 2007, Pages 1914-1924

  Hsieh, Minnie ^a   Lee, Daekee ^b,d   Panigone, Sara ^a,c   Horner, Kathleen ^a   Chen, Ruby ^a   Theologis, Alekos ^a   Lee, David C ^b,e   Threadgill, David W ^b   Conti, Marco ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^d Ewha Womans University   (South Korea)

^e UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIREGULIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIREGULIN; LUTEINIZING HORMONE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CUMULUS OOPHORUS; EXTRACELLULAR MATRIX; FEMALE; FERTILITY; GENE INDUCTION; LUTEINIZING HORMONE RELEASE; MEIOSIS; MOUSE; NONHUMAN; OVARY FOLLICLE; OVULATION; PRIORITY JOURNAL; PROPHASE; SIGNAL TRANSDUCTION; SOMATIC CELL; TRANSACTIVATION;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CHORIONIC GONADOTROPIN; EPIDERMAL GROWTH FACTOR; FEMALE; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; LUTEINIZING HORMONE; MEIOSIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; OOCYTES; OVARIAN FOLLICLE; OVARY; OVULATION; SIGNAL TRANSDUCTION; TIME FACTORS;

MAMMALIA; MUS;

EID: 33847188090     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01919-06     Document Type: Article

References (59)

1. Ashkenazi, H., X. Cao, S. Motola, M. Popliker, M. Conti, and A. Tsafriri. 2005. Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146:77-84.
2. Daub, H., F. U. Weiss, C. Wallasch, and A. Ullrich. 1996. Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379:557-560.
3. Davis, B. J., D. E. Lennard, C. A. Lee, H. F. Tiano, S. G. Morham, W. C. Wetsel, and R. Langenbach. 1999. Anovulation in cyclooxygenase-2- deficient mice is restored by prostaglandin E2 and interleukin-1β. Endocrinology 140:2685-2695.
4. Dinchuk, J. E., B. D. Car, R. J. Focht, J. J. Johnston, B. D. Jaffee, M. B. Covington, N. R. Contel, V. M. Eng, R. J. Collins, P. M. Czerniak, et al. 1995. Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase II. Nature 378:406-409.
5. Downs, S. M., S. A. Daniel, and J. J. Eppig. 1988. Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J. Exp. Zool. 245:86-96.
6. Elvin, J. A., A. T. Clark, P. Wang, N. M. Wolfman, and M. M. Matzuk. 1999. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 13:1035-1048.
7. Eppig, J. J. 1991. Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13:569-574.
8. Fowler, K., F. Walker, W. Alexander, M. Hibbs, E. Nice, R. Bohmer, G. Mann, C. Thumwood, R. Maglitto, J. Danks, R. Chetty, A. Burgess, and A. Dunn. 1995. A mutation in the epidermal growth factor receptor in waved-2 mice has a profound effect on receptor biochemistry that results in impaired lactation. Proc. Natl. Acad. Sci. USA 92:1465-1469.
9. Freimann, S., I. Ben-Ami, A. Dantes, R. Ron-El, and A. Amsterdam. 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.
10. Fülöp, C., S. Szanto, D. Mukhopadhyay, T. Bardos, R. V. Kamath, M. S. Rugg, A. J. Day, A. Salustri, V. C. Hascall, T. T. Giant, and K. Mikecz. 2003. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 130:2253-2261.
11. Gall, L., N. Chene, M. Dahirel, S. Ruffini, and C. Boulesteix. 2004. Expression of epidermal growth factor receptor in the goat cumulus-oocyte complex. Mol. Reprod. Dev. 67:439-445.
12. Gospodarowicz, D., and H. Bialecki. 1979. Fibroblast and epidermal growth factors are mitogenic agents for cultured granulosa cells of rodent, porcine, and human origin. Endocrinology 104:757-764.
13. Gschwind, A., S. Hart, O. M. Fischer, and A. Ullrich. 2003. TACE cleavage of proamphiregulin regulates GPCR-induced proliferation and motility of cancer cells. EMBO J. 22:2411-2421.
14. Harper, J. F., and G. Brooker. 1975. Femtomole sensitive radioimmunoassay for cyclic AMP and cyclic GMP after 2′0 acetylation by acetic anhydride in aqueous solution. J. Cyclic Nucleotide Res. 1:207-218.
15. Hinckley, M., S. Vaccari, K. Horner, R. Chen, and M. Conti. 2005. The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev. Biol. 287:249-261.
16. Hizaki, H., E. Segi, Y. Sugimoto, M. Hirose, T. Saji, F. Ushikubi, T. Matsuoka, Y. Noda, T. Tanaka, N. Yoshida, S. Narumiya, and A. Ichikawa. 1999. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc. Natl. Acad. Sci. USA 96:10501-10506.
17. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the mouse embryo: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
18. Holhro, T., and N. E. Hynes. 2004. ErbB receptors: directing key signaling networks throughout life. Annu. Rev. Pharmacol. Toxicol. 44:195-217.
19. Johnson, G. R., B. Kanman, M. Shoyah, and K. Stromherg. 1993. Amphiregulin induces tyrosine phosphorylation of the epidermal growth factor receptor and p185erbB2. Evidence that amphiregulin acts exclusively through the epidermal growth factor receptor at the surface of human epithelial cells. J. Biol. Chem. 268:2924-2931
20. Ko, C., M. C. Gieske, L. Al-Alem, Y. Hahn, W. Su, M. C. Gong, M. Iglarz, and Y. Koo. 2006. Endothelin-2 in ovarian follicle rupture. Endocrinology 147:1770-1779.
21. Ledent, C., I. Demeestere, D. Blum, J. Petermans, T. Hamalainen, G. Smits, and G. Vassart. 2005. Premature ovarian aging in mice deficient for Gpr3. Proc. Natl. Acad. Sci. USA 102:8922-8926.
22. Lee, D., R. S. Pearsall, S. Das, S. K. Dey, V. L. Godfrey, and D. W. Threadgill. 2004. Epiregulin is not essential for development of intestinal tumors but is required for protection from intestinal damage. Mol. Cell. Biol. 24:8907-8916.
23. Le Stunff, H., A. Mikami, P. Giussani, J. P. Hobson, P. S. Jolly, S. Milstien, and S. Spiegel. 2004. Role of sphingosine-1-phosphate phosphatase 1 in epidermal growth factor-induced chemotaxis. J. Biol. Chem. 279:34290-34297.
24. Li, B., Z. Yang, J. Hou, A. McCracken, M. A. Jennings, and M. Y. Ma. 2003. Compromised reproductive function in adult female mice selectively expressing mutant ErbB-1 tyrosine kinase receptors in astroglia. Mol. Endocrinol. 17:2365-2376.
25. Lim, H., B. C. Paria, S. K. Das, J. E. Dinchuk, R. Langenbach, J. M. Trzaskos, and S. K. Dey. 1997. Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91:197-208.
26. Luetteke, N. C., H. K. Phillips, T. H. Qiu, N. G. Copeland, H. S. Earp, N. A. Jenkins, and D. C. Lee. 1994. The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev. 8:399-413.
27. Luetteke, N. C., T. H. Qiu, S. E. Fenton, K. L. Troyer, R. F. Riedel, A. Chang, and D. C. Lee. 1999. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 126:2739-2750.
28. Matzuk, M. M., K. H. Burns, M. M. Viveiros, and J. J. Eppig. 2002. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296:2178-2180.
29. Mehlmann, L. M., Y. Saeki, S. Tanaka, T. J. Brennan, A. V. Evsikov, F. L. Pendola, B. B. Knowles, J. J. Eppig, and L. A. Jaffe. 2004. The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306:1947-1950.
30. Mondschein, J. S., and D. W. Schomberg. 1981. Growth factors modulate gonadotropin receptor induction in granulosa cell cultures. Science 211:1179-1180.
31. Moore, R. K., and S. Shimasaki. 2005. Molecular biology and physiological role of the oocyte factor, BMP-15. Mol. Cell. Endocrinol. 234:67-73.
32. Murdoch, W. J., and M. L. Gottsch. 2003. Proteolytic mechanisms in the ovulatory folliculo-luteal transformation. Connect. Tissue Res. 44:50-57.
33. Ochsner, S. A., A. J. Day, M. S. Rugg, R. M. Breyer, R. H. Gomer, and J. S. Richards. 2003. Disrupted function of tumor necrosis factor-alpha-stimulated gene 6 blocks cumulus cell-oocyte complex expansion. Endocrinology 144:4376-4384.
34. Park, J. Y., F. Richard, S. Y. Chun, J. H. Park, E. Law, K. Horner, S. L. Jin, and M. Conti. 2003. Phosphodiesterase regulation is critical for the differentiation and pattern of gene expression in granulosa cells of the ovarian follicle. Mol. Endocrinol. 17:1117-1130.
35. Park, J. Y., Y. Q. Su, M. Ariga, E. Law, S. L. Jin, and M. Conti. 2004. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682-684.
36. Park, O. K., and K. E. Mayo. 1991. Transient expression of progesterone receptor messenger RNA in ovarian granulosa cells after the preovulatory luteinizing hormone surge. Mol. Endocrinol. 5:967-978.
37. Pathak, B. G., D. J. Gilbert, C. A. Harrison, N. C. Luetteke, X. Chen, M. Klagsbrun, G. D. Plowman, N. G. Copeland, N. A. Jenkins, and D. C. Lee. 1995. Mouse chromosomal location of three EGF receptor ligands: amphiregulin (Areg), betacellulin (Etc), and heparin-binding EGF (Hegfl). Genomics 28:116-118.
38. Peng, X. R., A. J. Hsueh, P. S. LaPolt, L. Bjersing, and T. Ny. 1991. Localization of luteinizing hormone receptor messenger ribonucleic acid expression in ovarian cell types during follicle development and ovulation. Endocrinology 129:3200-3207.
39. Prenzel, N., E. Zwick, H. Daub, M. Leserer, R. Abraham, C. Wallasch, and A. Ullrich. 1999. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402:884-888.
40. Prevot, V., A. Lomniczi, G. Corfas, and S. R. Ojeda. 2005. erbB-1 and erbB-4 receptors act in concert to facilitate female sexual development and mature reproductive function. Endocrinology 146:1465-1472.
41. Prochazka, R., P. Kalab, and E. Nagyova. 2003. Epidermal growth factor-receptor tyrosine kinase activity regulates expansion of porcine oocyte-cumulus cell complexes in vitro. Biol. Reprod. 68:797-803.
42. Richards, J. S., D. L. Russell, S. Ochsner, and L. L. Espey. 2002. Ovulation: new dimensions and new regulators of the inflammatory-like response. Annu. Rev. Physiol. 64:69-92.
43. Riese, D. J., Jr., Y. Bermingham, T. M. van Raaij, S. Buckley, G. D. Plowman, and D. F. Stern. 1996. Betacellulin activates the epidermal growth factor receptor and erbB-4, and induces cellular response patterns distinct from those stimulated by epidermal growth factor or neuregulin-beta. Oncogene 12:345-353.
44. Riese, D. J., Jr., T. Komurasaki, G. D. Plowman, and D. F. Stern. 1998. Activation of ErbB4 by the bifunctional epidermal growth factor family hormone epiregulin is regulated by ErbB2. J. Biol. Chem. 273:11288-11294.
45. Roberts, R. B., L. Min, M. K. Washington, S. J. Olsen, S. H. Settle, R. J. Coffey, and D. W. Threadgill. 2002. Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis. Proc. Natl. Acad. Sci. USA 99:1521-1526.
46. Robker, R. L., D. L. Russell, L. L. Espey, J. P. Lydon, B. W. O'Malley, and J. S. Richards. 2000. Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. Proc. Natl. Acad. Sci. USA 97:4689-4694.
47. Schäfer, B., A. Gschwind, and A. Ullrich. 2004. Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 23:991-999.
48. Schomberg, D. W., J. V. May, and J. S. Mondschein. 1983. Interactions between hormones and growth factors in the regulation of granulosa cell differentiation in vitro. J. Steroid Biochem. 19:291-295.
49. Sekiguchi, T., T. Mizutani, K. Yamada, T. Kajitani, T. Yazawa, M. Yoshino, and K. Miyamoto. 2004. Expression of epiregulin and amphiregulin in the rat ovary. J. Mol. Endocrinol. 33:281-291.
50. Shimada, M., I. Hernandez-Gonzalez, I. Gonzalez-Robayna, and J. S. Richards. 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.
51. Sibilia, M., and E. F. Wagner. 1995. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269:234-238.
52. Sukocheva, O., C. Wadham, A. Holmes, N. Albanese, E. Verrier, F. Feng, A. Bernal, C. K. Derian, A. Ullrich, M. A. Vadas, and P. Xia. 2006. Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor Edg-3: the role of sphingosine kinase-1. J. Cell Biol. 173:301-310.
53. Threadgill, D. W., A. A. Dlugosz, L. A. Hansen, T. Tennenbaum, U. Lichti, D. Yee, C. LaMantia, T. Mourton, K. Herrup, R. C. Harris, et al. 1995. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269:230-234.
54. Tsafriri, A., and R. Reich. 1999. Molecular aspects of ammalian ovulation. Exp. Clin. Endocrinol. Diabetes 107:1-11.
55. Tullet, J. M. A., V. Pocock, J. H. Steel, R. White, S. Milligan, and M. G. Parker. 2005. Multiple signalling defects in the absence of RIP140 impair both cumulus expansion and follicle rupture. Endocrinology 146:4127-4137.
56. Vanderhyden, B. C., P. J. Caron, R. Buccione, and J. J. Eppig. 1990. Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140:307-317.
57. Varani, S., J. A. Elvin, C. Yan, J. DeMayo, F. J. DeMayo, H. F. Horton, M. C. Byrne, and M. M. Matzuk. 2002. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol. Endocrinol. 16:1154-1167.
58. Yan, C., P. Wang, J. DeMayo, F. J. DeMayo, J. A. Elvin, C. Carino, S. V. Prasad, S. S. Skinner, B. S. Dunbar, J. L. Dube, A. J. Celeste, and M. M. Matzuk. 2001. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 15:854-866.
59. Yarden, Y., and M. X. Sliwkowski. 2001. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2:127-137.