Activation of cumulus cell SMAD2/3 and epidermal growth factor receptor pathways are involved in porcine oocyte-cumulus cell expansion and steroidogenesis

Molecular Reproduction and Development

Volumn 78, Issue 6, 2011, Pages 391-402

  Nagyova, Eva ^a   Camaioni, Antonella ^c   Scsukova, Sona ^b   Mlynarcikova, Alzbeta ^b   Prochazka, Radek ^a   Nemcova, Lucie ^a   Salustri, Antonietta ^c  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b INSTITUTE OF EXPERIMENTAL ENDOCRINOLOGY   (Slovakia)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Hyaluronan; Oocyte cumulus complex; Progesterone

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE; FOLLITROPIN; HYALURONIC ACID; SMAD2 PROTEIN; SMAD3 PROTEIN;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; BIOSYNTHESIS; CELL EXPANSION; CONTROLLED STUDY; CUMULUS CELL; ENZYME INHIBITION; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GRANULOSA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; PROTEIN INDUCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEROIDOGENESIS; SWINE;

ANIMALS; BENZAMIDES; C-REACTIVE PROTEIN; CELL ADHESION MOLECULES; CUMULUS CELLS; DIOXOLES; EPIDERMAL GROWTH FACTOR; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCURONOSYLTRANSFERASE; HYALURONIC ACID; ISOQUINOLINES; MEIOSIS; MICE; OOCYTES; PROGESTERONE; PYRIDINES; PYRROLES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SERUM AMYLOID P-COMPONENT; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; SWINE; TYRPHOSTINS;

MUS; SUS;

EID: 79959378300     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.21312     Document Type: Article

References (64)

1. Adashi EY. 1994. Endocrinology of the ovary. Hum Reprod 9: 815-827.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.
3. 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 46: 77-84.
4. Attisano L, Wrana JL. 2000. Smads as transcriptional co-modulators. Curr Opin Cell Biol 12: 235-243.
5. Bodensteiner KJ, Clay CM, Moeller CL, Sawyer HR. 1999. Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol Reprod 60: 381-386.
6. Brown KA, Pietenpol JA, Moses HL. 2007. A tale of two proteins: Differential roles and regulation of SMAD2 and SMAD3 in TGFb signaling. J Cell Biochem 101: 9-33.
7. Buccione R, Vanderhyden BC, Caron PJ, Eppig JJ. 1990. FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev Biol 138: 16-25.
8. Conti M, Hsieh M, Park JY, Su YQ. 2006. Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol 20: 715-723.
9. Coskun S, Uzumcu M, Lin YC, Friedman CI, Alak BM. 1995. Regulation of cumulus cell steroidogenesis by the porcine oocyte and preliminary characterization of oocyte-produced factor(s). Biol Reprod 53: 670-675.
10. Diaz FJ, Wigglesworth K, Eppig JJ. 2007. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120: 1330-1340.
11. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Thompson JG, Armstrong DT, Gilchrist RB. 2007. Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod 76: 848-857.
12. Edson MA, Nagaraja AK, Matzuk MM. 2009. The mammalian ovary from genesis to revelation. Endocr Rev 30: 624-712.
13. El-Fouly MA, Cook B, Nekola M, Nalbandov AV. 1970. Role of the ovum in follicular luteinization. Endocrinology 87: 288-293.
14. Elvin JA, Yan C, Wang P, Nishimori K, Matzuk MM. 1999. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol 13: 1018-1034.
15. Elvin JA, Yan C, Matzuk MM. 2000. Oocyte-expressed TGF-beta superfamily members in female fertility. Mol Cell Endocrinol 159: 1-5.
16. Fitzpatrick SL, Sindoni DM, Shughrue PJ, Lane MV, Merchenthaler IJ, Frail DE. 1998. Expression of growth differentiation factor-9 messenger ribonucleic acid in ovarian and nonovarian rodent and human tissues. Endocrinology 139: 2571-2578.
17. Gilchrist RB, Ritter LJ, Myllymaa S, Kaivo-Oja N, Dragovic RA, Hickey TE, Ritvos O, Mottershead DG. 2006. Molecular basis of oocyte-paracrine signaling that promotes granulosa cell proliferation. J Cell Sci 119: 3811-3821.
18. Gong X, McGee EA. 2009. SMAD3 is required for normal follicular follicle-stimulating hormone responsiveness in the mouse. Biol Reprod 81: 730-738.
19. Jaatinen R, Laitinen MP, Vuojolainen K, Aaltonen J, Louhio H, Heikinheimo K, Lehtonen E, Ritvos O. 1999. Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and cDNA cloning of rat GDF-9 and its novel homolog GDF-9B. Mol Cell Endocrinol 156: 189-193.
20. Jezova M, Scsukova S, Nagyova E, Vranova J, Prochazka R, Kolena J. 2001. Effect of intraovarian factors on porcine follicular cells: Cumulus expansion, granulosa and cumulus cell progesterone production. Anim Reprod Sci 65: 115-126.
21. Kolena J, Channing CP. 1985. Stimulatory action of follicular fluid components on maturation of granulosa cells from small porcine follicles. Horm Res 21: 185-198.
22. Lee GS, Kim HS, Hwang WS, Hyun SH. 2008. Characterization of porcine growth differentiation factor-9 and its expression in oocyte maturation. Mol Reprod Dev 75: 707-714.
23. Li R, Norman RJ, Armstrong DT, Gilchrist RB. 2000. Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod 63: 839-845.
24. Li HK, Kuo TY, Yang HS, Chen LR, Li SS, Huang HW. 2008. Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos. Anim Reprod Sci 103: 312-322.
25. Looyenga BD, Hammer GD. 2007. Genetic removal of SMAD3 from inhibin-null mice attenuates tumor progression by uncoupling extracellular mitogenic signals from the cell cycle machinery. Mol Endocrinol 10: 2440-2457.
26. Mazerbourg S, Klein C, Roh J, Kaivo-Oja N, Mottershead DG, Korchynskyi O, Ritvos O, Hsueh AJ. 2004. Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5. Mol Endocrinol 18: 653-665.
27. McGrath SA, Esquela AF, Lee SJ. 1995. Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol 9: 131-136.
28. McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, Western A, Meerasahib MF, Mottershead DG, Groome NP, Ritvos O, Laitinen MP. 2005a. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129: 473-480.
29. McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, Western A, Meerasahib MF, Mottershead DG, Groome NP, Ritvos O, Laitinen MP. 2005b. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 129: 481-487.
30. Nagyova E, Prochazka R, Vanderhyden BC. 1999. Oocytectomy does not influence synthesis of hyaluronan by pig cumulus cells: Retention of hyaluronan after insulin-like growth factor-I treatment in serum-free medium. Biol Reprod 61: 569-574.
31. Nagyova E, Vanderhyden BC, Prochazka R. 2000. Secretion of paracrine factors enabling expansion of cumulus cells is developmentally regulated in pig oocytes. Biol Reprod 63: 1149-1156.
32. Nagyova E, Camaioni A, Prochazka R, Salustri A. 2004. Covalent transfer of heavy chains of inter-alpha-trypsin inhibitor family proteins to hyaluronan in in vivo and in vitro expanded porcine oocyte-cumulus complexes. Biol Reprod 71: 1838-1843.
33. Nagyova E, Camaioni A, Prochazka R, Day AJ, Salustri A. 2008. Synthesis of tumor necrosis factor alpha induced protein 6 in porcine preovulatory follicles: A study with A38 antibody. Biol Reprod 78: 903-909.
34. Nagyova E, Nemcova L, Prochazka R. 2009. Expression of tumor necrosis factor alpha-induced protein 6 messenger RNA in porcine preovulatory ovarian follicles. J Reprod Dev 55: 231-235.
35. Nemcova L, Nagyova E, Petlach M, Tomanek M, Prochazka R. 2007. Molecular mechanisms of insulin-like growth factor 1 promoted synthesis of hyaluronan in porcine oocyte-cumulus complexes. Biol Reprod 76: 1016-1024.
36. Otsuka F, Yao Z, Lee T, Yamamoto S, Erickson GF, Shimasaki S. 2000. Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem 275: 39523-39528.
37. Otsuka F, Moore RK, Shimasaki S. 2001. Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J Biol Chem 276: 32889-32895.
38. Pangas SA, Li X, Robertson EJ, Matzuk MM. 2006. Premature luteinization and cumulus cell defects in ovarian-specific SMAD4 knockout mice. Mol Endocrinol 20: 1406-1422.
39. 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.
40. Petersen M, Pardali E, van der Horst G, Cheung H, van den Hoogen C, van der Pluijm G, Ten Dijke P. 2010. SMAD2 and SMAD3 have opposing roles in breast cancer metastasis by differentially affecting tumor angiogenesis. Oncogene 29: 1351-1361.
41. Popovici RM, Krause MS, JAuckus J, Germeyer A, Brum IS, Garlanda C, Strowitzki T, Wolf M. 2008. The long pentraxin PTX3 in human endometrium: Regulation by steroids and trophoblast products. Endocrinology 149: 1136-1143.
42. Prochazka R, Nagyova E, Rimkevicova Z, Nagai T, Kikuchi K, Motlik J. 1991. Lack of effect of oocytectomy on expansion of the porcine cumulus. J Reprod Fertil 93: 569-576.
43. Prochazka R, Srsen V, Nagyova E, Miyano T, Flechon JE. 2000. Developmental regulation of effect of epidermal growth factor on porcine oocyte-cumulus cell complexes: Nuclear maturation, expansion, and F-actin remodeling. Mol Reprod Dev 56: 63-73.
44. Prochazka R, Kalab P, Nagyova E. 2003. Epidermal growth factor-receptor tyrosine kinase activity regulates expansion of porcine oocyte-cumulus cell complexes in vitro. Biol Reprod 68: 797-803.
45. Prochazka R, Nemcova L, Nagyova E, Kanka J. 2004. Expression of growth differentiation factor 9 messenger RNA in porcine growing and preovulatory ovarian follicles. Biol Reprod 71: 1290-1295.
46. Reka AK, Kurapati H, Narala VR, Bommer G, Chen J, Standiford TJ, Keshamouni VG. 2010. Peroxisome proliferator-activated receptor-{gamma} activation inhibits tumor metastasis by antagonizing SMAD3-mediated epithelial-mesenchymal transition. Mol Cancer Ther 9: 3221-3232.
47. Salustri A, Yanagishita M, Hascall VC. 1990a. Mouse oocytes regulate hyaluronan synthesis and mucification by FSH-stimulated cumulus cells. Dev Biol 138: 26-32.
48. Salustri A, Ulisse S, Yanagishita M, Hascall VC. 1990b. Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. J Biol Chem 265: 19517-19523.
49. Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck Peccoz P, Salvatori G, Mahoney DJ, Day AJ, Siracusa G, Romani L, Mantovani A. 2004. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131: 1577-1586.
50. Sasseville M, Ritter LJ, Nguyen TM, Liu F, Mottershead DG, Russell DL. 2010. Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulose and cumulus cells. J Cell Sci 123: 3166-3176.
51. Scarchilli L, Camaioni A, Bottazzi B, Negri V, Doni A, Deban L, Bastone A, Salvatori G, Mantovani A, Siracusa G, Salustri A. 2007. PTX3 interacts with inter-alpha-trypsin inhibitor: Implications for hyaluronan organization and cumulus oophorus expansion. J Biol Chem 282: 30161-30170.
52. Singh B, Zhang X, Armstrong DT. 1993. Porcine oocytes release cumulus expansion-enabling activity even though porcine cumulus expansion in vitro is independent of the oocyte. Endocrinology 132: 1860-1862.
53. Shimada M, Nishibori M, Yamashita Y, Ito J, Mori T, Richards JS. 2004. Down-regulated expression of A disintegrin and metalloproteinase with thrombospondin-like repeats-1 by progesterone receptor antagonist is associated with impaired expansion of porcine cumulus-oocyte complexes. Endocrinology 145: 4603-4614.
54. Tomic D, Miller KP, Kenny HA, Woodruff TK, Hoyer P, Flaws JA. 2004. Ovarian follicle development requires SMAD3. Mol Endocrinol 18: 2224-2240.
55. Tranguch S, Chakrabarty A, Guo Y, Wang H, Dey SK. 2007. Maternal pentraxin 3 deficiency compromises implantation in mice. Biol Reprod 77: 425-432.
56. Vanderhyden BC. 1993. Species differences in the regulation of cumulus expansion by an oocyte-secreted factor(s). J Reprod Fertil 98: 219-227.
57. Vanderhyden BC, Tonary AM. 1995. Differential regulation of progesterone and estradiol production by mouse cumulus and mural granulosa cells by a factor(s) secreted by the oocyte. Biol Reprod 53: 1243-1250.
58. Vanderhyden BC, Macdonald EA, Nagyova E, Dhawan A. 2003. Evaluation of members of the TGFbeta superfamily as candidates for the oocyte factors that control mouse cumulus expansion and steroidogenesis. Reprod Suppl 61: 55-70.
59. Varani S, Elvin JA, Yan C, De Mayo J, DeMayo FJ, Horton HF, Byrne MC, Matzuk MM. 2002. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol 16: 1154-1167.
60. 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.
61. Wrighton KH, Lin X, Feng XH. 2009. Phospho- control of TGFb superfamily signaling. Cell Res 19: 8-20.
62. 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 metaloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor. Endocrinology 148: 6164-6175.
63. Yamashita Y, Kawashima I, Gunji Y, Hishinuma M, Shimada M. 2010. Progesterone is essential for maintenance of TACE/ ADAM 17 mRNA expression, but not EGF-like factor, in cumulus cells, which enhances the EGF receptor-signaling pathway during in vitro maturation of porcine COCs. J Reprod Dev 56: 315-323.
64. Yeo CX, Gilchrist RB, Lane M. 2009. Disruption of bidirectional oocyte-cumulus paracrine signaling during in vitro maturation reduces subsequent mouse oocyte developmental competence. Biol Reprod 80: 1072-1080.