Interaction and signal transduction between oocyte and samatic cells in the ovary

Frontiers in Bioscience

Volumn 12, Issue 8, 2007, Pages 2782-2796

  Liu, Yi Xun ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Folliculogenesis; Granulosa cell; Intracellular interaction; Oocyte; Primordial follicle; Review; Signal transduction; Theca cell

Indexed keywords

ANIMALIA;

ANIMAL; CYTOLOGY; FEMALE; HUMAN; METABOLISM; OOCYTE; OVARY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; FEMALE; HUMANS; OOCYTES; OVARY; SIGNAL TRANSDUCTION;

EID: 34347242802     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/2272     Document Type: Review

References (107)

1. Peters H: Migration of gonocytes into the mammalian gonad and their differentiation. Proceedings of the Royal Society of London (B) 259, 91-101 (1970)
2. Beaumont H. M & A. M Mandl: A quantitative and cytological study of oogonia and oocytes in the foetal and neonatal rat. Proceedings of the Royal Society of London (B) 155, 557-579 (1961)
3. Borum K: Oogenesis in the mouse: a study of the meiotic prophase. Experimental Cell Research 24, 495-507 (1961)
4. Hirshfield A. N: Development of follicles in the mammalian ovary. Int Rev Cytol 124, 43-101 (1991)
5. Braw-Tal R: The initiation of follicle growth: the oocyte or the somatic cells? Molecular and Cellular. Endocrinology 187(1-2), 11-8 (2002) (Pubitemid 34441037)
6. Baker T. G: A quantitative and cytological study of germ cells in human ovaries. Proceedings of the Royal Society of London-Biological Sciences 158, 417-433 (1963)
7. De Felici M, M. L. Scaldaferri and D. Farini: Adhesion molecules for mouse primodial germ cells. Front Biosci 10, 542-551 (2005)
8. Okamura D, T. Kimura, T. Nakano, Y. Matsui: Cadherin-mediated cell interaction regulates germ cell determination in mice. Development 130, 6423-6430 (2004)
9. De Felici M: Regulation of primordial germ cell development in the mouse. Int J Dev Biol 44, 575-580 (2000)
10. De Felici M: Twenty years of research on primordial germ cells. Int J Dev Biol 45, 519-522 (2001) (Pubitemid 32452748)
11. Starz-Gaiano M, R. Lehmann: Moving towards the next generation. Mech Dev 105, 5-18 (2001) (Pubitemid 32586756)
12. McLaren A: Primordial germ cells in the mouse. Dev Bio 262, 1-15 (2003) (Pubitemid 37153101)
13. Wylie C, R. Anderson: Germ cells. In: Mouse Development. Eds: Rossant J, Tau PPL, Academic Press, 181-189 (2002)
14. Anderson R, T. K. Copeland, H. Scholer, J. Heasman, C. Wylie: The onset of germ cell migration in the mouse embryo. Mech Dev 91, 61-68 (2000) (Pubitemid 30125905)
15. Clark J. M. & E. M. Eddy: Fine structural observations on the origin and association of primordial germ cells of the mouse. Dev Biol 47, 136-155 (1975)
16. De Felici M, S. Dolci, M. Pesce: Cellular and molecular aspects of mouse primordial germ cell migration and proliferation in culture. Int J Dev Biol 36, 205-213 (1992)
17. Godin I, C. Wylie, J. Heasman: Genital ridge exert long-range effects on mouse primordial germ cell number and direction of migration in culture. Development 108, 357-363 (1990)
18. Godin I, C. Wylie: TGF1 inhibits proliferation and has a chemotropic effect on mouse primordial germ cells in culture. Development 113, 1451-1457 (1991)
19. Godin I, R. Deed, J. Cooke, K. Zsebo, M. Dexter, C. Wylie: Effects of the steel gene product on mouse primordial germ cells in culture. Nature 352, 807-809 (1991) (Pubitemid 21912435)
20. Keshet E, S. D. Lyman, D. E. Williams, D. M. Anderson, N. A. Jenkins, N. G. Copeland, L. F. Parada: Embryonic RNA expression patterns of the c-kit receptor and its cognate ligand suggest multiple functional roles in mouse development. EMBO J 9, 2425-2435 (1991) (Pubitemid 21905716)
21. Ara T, Y. Nakamura, T. Egawa, T. Sugiyama, K. Abe, T. Kishimoto, Y. Matsui, T. Nagasawa: Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci U S A 100, 5319-5323. (2003) (Pubitemid 36542703)
22. Molyneaux K. A, H. Zinszner, P. S. Kunwar, K. Schaible, J. Stebler, M. J. Sunshine, W O'Brien, E. Raz, D. Littman, C. Wylie, R. Lehmann: The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 130, 4279-4286 (2003) (Pubitemid 37185317)
23. Angst, B, C. Marcozzi & A. Magee: The cadherin superfamily: diversity in form and function. J Cell Sci 114, 629-41 (2001) (Pubitemid 32237135)
24. Bendel-Stenze M. R, M. Gomperts, R. Anderson, J. Heasman, C. Wylie: The role of cadherins during primordial germ cell migration and early gonad formation in the mouse. Mech Dev 91, 143-152 (2000) (Pubitemid 30125913)
25. Gomperts M, M. Garcia-Castro, C. Wylie, J. Heasman: Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120, 135-141 (1994) (Pubitemid 24031195)
26. Donovan P. J, D. Stott, L. A. Cairns, J. Heasman & C. Wylie: Migratory and postmigratory mouse primordial germ cells behave differently in culture. Cell 44, 831-838 (1986) (Pubitemid 16045329)
27. Molyneaux K. A, J. Stallock, K. Schaible, C. Wylie: Time-lapse analysis of living mouse germ cell migration. Dev Biol 240, 488-498 (2001) (Pubitemid 34056506)
28. Di Carlo A, M. De Felici: A role for E-cadherin in mouse primordial germ cell development. Dev Biol 226, 209-219 (2000)
29. Matzuk M. M, K. H. Burns, M. M. Viveiros & J. J. Eppig: Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178-80 (2002) (Pubitemid 34680291)
30. Jeff A. P, K. S. Michael: Kit-ligand/Stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 4262-4271 (1999)
31. Jin X, F. Q. Yu, P. Wei, Z. Y. Hu, C. S. Han & Y. X. Liu: Signal transduction of stem cell factor in promoting early follicle development. Mol Cell Endocrinil 229, 3-10 (2005) (Pubitemid 40018077)
32. Jin X, C. S. Han, F. Q. Yu, P. Wei, Z. Y. Hu & Y. X. Liu: Anti-apoptotic action of stem cell factor on oocytes in primordial follicles and its signal transduction. Mol Reprod Dev 70, 82-90 (2005) (Pubitemid 39602544)
33. Jin X, C. S. Han, X. S. Zhang, F. Q. Yu, S. H. Guo, Z. Y. Hu & Y. X. Liu: Stem cell factor modulates the expression of steroidogenesis related proteins and FSHR during ovarian follicular development. Front Biosci 10, 1573-1580 (2005) (Pubitemid 40529021)
34. Driancourt M. A, K. Reynaud, R. Cortvrindt, J. Smitz: Roles of KIT and KIT LIGAND in ovarian function. Rev Reprod 5(3), 143-52 (2000)
35. Hutt K. J, E. A. McLaughlin & M. K. Holland: Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. Mol Hum Reprod. 12(2), 61-69 (2006)
36. Flaws, J. A, A. DeSanti, K. I. Tilly, R. O. Javid, K. Kugu, A. L. Johnson, A. N. Hirshfield & J. L. Tilly: Vasoactive intestinal peptidemediated suppression of apoptosis in the ovary: poteintial mechanisms of action and evidence of a conserved anti-atretogenic role through evolution. Endocrinology 136, 4351-4359 (1995)
37. Davis R. J: The mitogen-activated protein kinase signal transduction pathway. J Biol Chem 268, 14553-14556 (1993) (Pubitemid 23206581)
38. Asselin E, Y. Wang and B. K. Tsang: X-linked inhibitor of apoptosis protein activates the phosphatidylinositol 3-kinase/Akt pathway in rat graunlosa cells during follicular development. Endocrinology 142, 2451-2457 (2001) (Pubitemid 32473101)
39. Johnson A. L, J. T. Bridgham & J. A. Swenson: Activation of the Akt/protein kinase B signaling pathway is associated with granulosa cell survival. Biol Reprod 64, 1566-1574 (2001) (Pubitemid 32373080)
40. Chun S. Y, H. Billig, J. L. Tilly, I. Furuta, A Tsafriri & A. J. Hsueh: Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor-I Endocrinology 135, 1845-1853 (1994) (Pubitemid 24363875)
41. Khamsi F. and S. Roberge: Granulosa cells of the cumulus oophorus are different from mural granulosa cells in their response to gonadotrophins and IGF-I. J. Endocrino 170, 565-73 (2001) (Pubitemid 32834322)
42. Aad P. Y, J. L. Voge, C. A. Santiago, J. R. Malayer & L. J. Spicer: Real-time RT-PCR quantification of pregnancy-associated plasma protein-A mRNA abundance in bovine granulosa and theca cells: Effects of hormones in vitro. Domest Anim Endocrinol Jan 6; [Epub ahead of print] (2006)
43. Liu Y. X & A. J. W. Hsueh: Autocrine role of endogenously-produced estrogen in the enhancement of aromatase activity, progesterone production and LH receptor in cultured rat granulosa cells. Chinese J. Physiol. Sci 1(2), 1-9 (1986)
44. Liu, Y. X & A. J. W. Hsueh: Synergism between granulosa and theca-interstitial cells in estrogen biosynthesis by gonadotropin-treated rat ovaries: Studies on the two-cel 1, two-gonadotropin hypothesis using steroid antisera. Biol Reprod 35, 27-36 (1986) (Pubitemid 17192313)
45. Yu F. Q, C. S. Han, W. Yang, X. Jin, Z. Y. Hu & Y. X. Liu: Activation of p38 MAPK pathway by FSH regulates steroidogenesis in granulosa cells differentially. J. Endocrinol 186, 85-96 (2005) (Pubitemid 41015667)
46. Yu F. Q, C. S. Han, W. Yang, X. Jin, Z. Y. Hu & Y. X. Liu: Role of ERK1/2 in FSH-induced PCNA expression and steroidogenesis in granulosa cells. Front Bioscis 10, 896-904 (2005)
47. Park Y, E. T. Maizels, Z. J. Feiger, H. Alam, C. A Peters, T. K. Woodruff, T. G. Unterman, E. J. Lee, J. L. Jameson, M Hunzicker-Dunn.: 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, 9135-48 (2005) (Pubitemid 41818225)
48. Su Y. Q, J. M. Denegre, K. Wigglesworth: Oocytedependent 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, 126-38 (2003) (Pubitemid 37268008)
49. Sela-Abramovich S, E. Chorev, D. Galiani: MAPK mediates LH-induced breakdown of communication and oocyte maturation in rat ovarian follicles. Endocrinology 146, 1236-44 (2005) (Pubitemid 40289311)
50. Gilchrist R. B, L. J. Ritter, D. T. Armstrong: Oocytesomatic cell interactions during follicle development in mammals. Anim Reprod Sci. 82-83, 431-46 (2004) (Pubitemid 39027077)
51. Plancha C. E, A. Sanfins, P. Rodrigues, D. Albrtini: Cell polarity during folliculogenesis and oogenesis. Reprod Biomed Online 10(4), 478-84 (2005) (Pubitemid 40485007)
52. Short RV: Steroids in follicular fluid and the corpus luteum of the mare. A two-cell type theory of ovarian steroid synthesis. J. Endocrinology 24, 59-63 (1962)
53. Ryan K. J, Z. Petro, J. Kaiser: Steroid formation by isolated and recombined ovarian granulosa and theca cells. J Clin Endocrinol 28, 355-358 (1968)
54. Liu Y. X: Regulation of plasminogen activator system in the ovary. Biological Signals and Receptors 8, 160-177 (1999)
55. Liu Y. X: Plasminogen activator/plasminogen activator inhibitors in ovarian physiology. Front Biosci 9, 3356-3373 (2004)
56. Liu Y. X, K. Liu, Q. Feng, H. Z. Liu, Z. Y. Hu, G. Q. Fu, Y. C. Li & T. Ny: Coordination Expression of Tissuetype Plasminogen Activator and Its Inhibitor Plasminogen Activator Inhibitor Type 1 Plays an Important Role in Ovulation in the Rhesus Monkey. Endocrinology 145, 1767-1775 (2004) (Pubitemid 38402385)
57. Liu Y. X: Interaction and regulation of plasminogen activator and their inhibitor in rat follicles during periovulatory periods. Scientia Sinica B 31, 47-57 (1988)
58. Jesse C, M. Orisaka, H. M. Wang, S. Orisaka, W. Thompson, C. Zhu, F. Kotsuji, and B. K. Tsang: Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death Front Biosci (in press) (2007)
59. Wang H, J. Y Jiang, C. Zhu, C. Peng and B. K Tsang: Role and Regulation of Nodal/Alk7 Signaling Pathway in the Control of Ovarian Follicular Atresia. Mol Endocrinol [In Press] (2006)
60. Brankin V, M. R. Mitchell, B. Webb & M. G. Hunter: Paracrine effects of oocyte secreted factors and stem cell factor on porcine granulosa and theca cells in vitro. Reprod Biol Endocrinol. Aug. 12, 1:55 (2003)
61. Shimizu T, B. C. Jayawardana, H. Nishimoto, E. Kaneko, M. Tetsuka and A. Miyamoto: Involvement of the bone morphogenetic protein/receptor system during follicle development in the bovine ovary: Hormonal regulation of the expression of bone morphogenetic protein 7 (BMP-7) and its receptors (ActRII and ALK-2). Mol Cell Endocrinol. 25;249(1-2), 78-83 (2006)
62. McNatty K. P, J. L Juengel, K. L. Reader, S. Lun, S. Myllymaa, S. B. Lawrence, A. Western, M. F. Meerasahib, D. G. Mottershead, N. P. Groome, O. Ritvos & M. P Laitinen: Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 129, 481-7 (2005) (Pubitemid 40542174)
63. Orisaka, M, S. Orisaka, J. Y. Jiang, J. Craig, Y. Wang, F. Kotsuji and B. K. Tsang: Growth Differentiation Factor-9 Is Anti-Apoptotic during Follicular Development from Preantral to Early Antral Stage. Mol Endocrinol 2006 Jun. 1; [Epub ahead of print] (2006)
64. Campbell B. K, C. J. Souza, A. J. Skinner, R. Webb & D. T. Baird: Enhanced response of granulosa and theca cells from sheep carriers of the FecB mutation in vitro to gonadotrophins and BMP-2, 4 and 6. Endocrinology. Jan 5, [Epub ahead of print] (2006)
65. Otsuka F and S. Shimasaki: A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis Proc Natl Acad Sci 99, 8060-8065 (2002) (Pubitemid 34651005)
66. Reddy P, L. J. Shen, C. Ren, K. Boman, E. Lundin, U. Ottander, P. Lindgren, Y. X. Liu, Q. Y. Sun & K. Liu: Activation of Akt (PKB) and Suppression of FKHRL1 in Mouse and Rat Oocytes by Stem Cell Factor during Follicular Activation and Development. Dev Biol 15, 281(2), 160-70 (2005) (Pubitemid 40719144)
67. Liu K: Stem cell factor (SCF)-Kit mediated phosphatidylinositol 3 (PI3) kinase signaling during mammalian oocyte growth and early follicular development Front Biosci 11, 126-135 (2006) (Pubitemid 43253480)
68. Vitt U. A, M. Hayashi, C. Klein: Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod 62, 370-7 (2000) (Pubitemid 30067338)
69. Varani S, J. A. Elvin, C. Yan: Knockout of prntraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol 16, 1154-1167 (2002) (Pubitemid 34621066)
70. Moore R. K, F. Otsuka, S. Shimasaki: Molecular basis of Bone morphogenetic protein-15 signaling in granulose cells. J Biol Chem 278, 304-310 (2003) (Pubitemid 36043577)
71. Su Y. Q, X. Wu, M. J. O'Brien: Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol 276, 64-73 (2004) (Pubitemid 39452846)
72. Otsuka F, S. Shimasaki: A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc Natl Acad Sci U S A 99, 8060-5 (2002) (Pubitemid 34651005)
73. Miyoshi T, F. Otsuka, J. Suzuki, M. Takeda, K. Inagaki, Y. Kano, H. Otani, Y. Mimura, T. Ogura & H. Makino: Mutual Regulation of Follicle-Stimulating Hormone Signaling and Bone Morphogenetic Protein System in Human Granulosa Cells. Biol Reprod. Jan 25; [Epub ahead of print) (2006)
74. Zachos N. C, R. B. Billiar, E. D. Albrecht, G. J. Pepe: Developmental regulation of follicle-stimulating hormone receptor messenger RNA expression in the baboon fetal ovary. Biol Reprod 68(5), 1911-7 (2003) (Pubitemid 36519802)
75. Manabe N, Y. Goto, F. Matsuda-Minehata, N. Inoue, A. Maeda, K. Sakamaki, T. Miyano: Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 50(5), 493-514 (2004) (Pubitemid 40631774)
76. Mihm M, P. J. Baker, J. L. Ireland, G. W. Smith, P. M. Coussens, A. C. Evans, J. J. Ireland: Molecular Evidence that Growth of Dominant Follicles Involves a Reduction in Follicle Stimulating Hormone-Dependence and an Increase in Luteinizing Hormone-Dependence in Cattle. Biol Reprod. Feb. 15; [Epub ahead of print] (2006)
77. Shao R, F. P. Zhang, E. Rung, J. J. Palvimo, I. Huhtaniemi & H. Billg: Inhibition of small ubiquitinrelated modifier-1 expression by luteinizing hormone receptor stimulation is linked to induction of progesterone receptor during ovulation in mouse granulosa cells. Endocrinology 145(1), 384-92 (2004) (Pubitemid 38094533)
78. Yan J. L, Q. Feng, H. Z. Liu, Z. Y. Hu & Y. X. Liu: Expression of tPA, LH receptor and inhibin a, BA subunits during follicular atresia in rat. Science in China C 42, 583-590 (2000)
79. Jin X & Y. X. Liu: Follicular growth, differentiation and atresia. Chinese Science Bulletin 48, 1786-90 (2003) (Pubitemid 44553052)
80. Greenaway J, P. A. Gentry, J. J. Feige, J. LaMarre and J. J. Petrik: Thrombospondin and vascular endothelial growth factor are cyclically expressed in an inverse pattern during bovine ovarian follicle development. Biol Reprod. 72(5), 1071-8 (2005) (Pubitemid 40547969)
81. Cohen B. D, C. A. Nechamen & J. A. Dias: Human follitropin receptor (FSHR) interacts with the adapter protein 14-3-3 tau. Mol Cell Endocrinol 220(1-2), 1-7 (2004) (Pubitemid 38757876)
82. Sun G. W, H. Kobayashi, M. Suzuki, N. Kanayama & T. Terao: Follicle-stimulating hormone and insulin-like growth factor I synergistically induce up-regulation of cartilage link protein (Crtl1) via activation of phosphatidylinositol-dependent kinase/Akt in rat granulosa cells. Endocrinology 144(3), 793-801 (2003) (Pubitemid 36262846)
83. Gittens J. E, K. J. Barr, B. C. Vanderhyden & G. M. Kidder: Interplay between paracrine signaling and gap junctional communication in ovarian follicles. J Cell Sci. 118, 113-122 (2005) (Pubitemid 40277109)
84. Otsuka F, R. K. Moore, S. Iemura, N. Ueno & S. Shimasaki: Follistatin inhibits the function of the oocytederived factor BMP-15. Biochem Biophys Res Commun. 289(5), 961-6 (2001) (Pubitemid 34076283)
85. Roh J. S, J. Bondestan, S. Mazerbourg, N. Kaivo-Oja, N. Groome, O. Ritvos & A. J. W Hsueh: Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 144(1), 172-8 (2003) (Pubitemid 36076106)
86. Hickey T. E, D. L. Marrocco, F. Amato, L. J. Ritter, R. J. Norman, R. B. Gichrist & D. T. Armstrong: Androgens augment the mitogenic effects of oocyte-secreted factors and growth differentiation factor 9 on porcine granulosa cells. Biol Reprod. 73(4), 825-32 (2005) (Pubitemid 41356143)
87. Freimann S, I. Ben-Ami, A. Dantes, L. Armon, A. Ben Ya'con-Klein, R. Ya'cov-Klein, L. Armon, R. Ron-EI & A. Amsterdam: Differential expression of genes coding for EGF-like factors and ADAMTS1 following gonadotropin stimulation in normal and transformed human granulosa cells. Biochem Biophys Res Commun. 333(3), 935-43 (2005) (Pubitemid 40854247)
88. Peluso J. J, A. Pappalardo, R. Losel and M. Wehling: Expression and function of PAIRBP1 within gonadotropinprimed immature rat ovaries: PAIRBP1 regulation of granulosa and luteal cell viability. Biol Reprod. 73(2), 261-70 (2005) (Pubitemid 41022785)
89. Schoenfelder M & R. Einspanier: Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol Reprod. 69(1), 269-77 (2003) (Pubitemid 36806832)
90. Meijia Z, G. L. Xia, B. Zhou and C. Wang: Gonadotropin-controlled mammal oocyte meiotic resumption. Front Biosci 12, 282-296 (2007) (Pubitemid 46852841)
91. Buccione R., B. C. Vanderhyden, P. J. Caron & J. J. Eppig: 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 (1990)
92. Salustri A, M. Yanagishita and V. C. Hascall: Mouse oocyte regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev Biol 138, 26-32 (1990)
93. Vanderhyden B. C, P. J. Caron, R. Buccione & J. J. Eppig: 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 (1990) (Pubitemid 20222469)
94. Elvin J. A, A. T. Clark, P. Wang, N. M. Wolfman & M. M. Matzuk: Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol 13, 1035-1048 (1999) (Pubitemid 30645319)
95. Ochsner S. A, D. L. Russell, A. J. Day, R. M. Breyer & J. S. Richards: Decreased expression of tumor necrosis factor-alpha-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 144, 1008-1019 (2003) (Pubitemid 36262868)
96. Sugiura K, F. L. Pendola & J. J. Eppig: Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 279, 20-30 (2005) (Pubitemid 40222166)
97. Takashi N, H. Funahashi, K. Yoshioka and K. Kikuchi: Up date of IVM/IVF/IVC in pigs. Front Biosci 11, 2565-2573 (2006)
98. Tatemoto H., N. Sakurai & N. Muto: Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol Reprod 63, 805-810 (2000) http://dx.doi.org/10.1095/biolreprod63.3.805 (Pubitemid 30659276)
99. Wang W. H and Q. Y. Sun: Meiotic spindle, spindle checkpoint and embryonic aneuploidy. Front Biosci 11, 620-636 (2006)
100. Chan G. K, S. A. Jablonski, D. A. Starr, M. L. Goldberg & T. J. Yen: Human Zw10 and ROD are mitotic checkpoint proteins that bind to kinetochores. Nat Cell Biol 2, 944-947 (2000)
101. Starr D. A, B. C. Williams, T. S. Hays & M. L. Goldberg: ZW10 helps recruit dynactin and dynein to the kinetochore. J Cell Biol 142, 763-774 (1998) (Pubitemid 28381493)
102. Howell B. J, B. F. McEwen, J. C. Canman, D. B. Hoffman, E. M. Farrar, C. L. Rieder & E. D. Salmon: Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 155, 1159-1172 (2001) (Pubitemid 34286267)
103. Basu J, E. Logarinho, S. Herrmann, H. Bousbaa, Z. Li, G. K. Chan, T. J. Yen, C. E. Sunkel & M. L. Goldberg: Localization of the Drosophila checkpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod. Chromosoma 107, 376-385 (1998) (Pubitemid 29057530)
104. Bharadwaj R & H. Yu: The spindle checkpoint, aneuploidy, and cancer. Oncogene 23, 2016-2027 (2004) (Pubitemid 38496731)
105. Chung E & R. H. Chen: Spindle checkpoint requires Mad1-bound and Mad1-free Mad2. Mol Biol Cell 13, 1501-1511 (2002) (Pubitemid 34522634)
106. Zhang D, M. Li, W. Ma, Y. Hou, Y. H. Li, S. W. Li, Q. Y. Sun & W. H. Wang: Localization of MAD1 in mouse oocytes during the first meiosis and its functions as a spindle checkpoint protein. Biol Reprod 72, 58-68 (2005) (Pubitemid 40013754)
107. Liu H. Z & Y. X. Liu: Study on the role EGF on primordial follicle initiation and devolopment. Science in China C 43(5), 535-543 (2000)