Pertinence of apoptosis markers for the improvement of in vitro fertilization (IVF)

Current Medicinal Chemistry

Volumn 16, Issue 15, 2009, Pages 1905-1916

  Haouzi, D ^a,b,c,d   Hamamah, S ^a,b,c,d  

^a HÔPITAL SAINT ELOI   (France)

^b HÔPITAL ARNAUD DE VILLENEUVE   (France)

^c INSERM   (France)

^d UNIV MONTPELLIER   (France)

Author keywords

Apoptosis markers; Diagnosis; Embryo; Genetic control; IVF; Microenvironment; Oocyte

Indexed keywords

CASPASE 2; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; FAS LIGAND; FOLLITROPIN; GENOMIC DNA; GROWTH DIFFERENTIATION FACTOR 9; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; INHIBITOR OF APOPTOSIS PROTEIN; INSULIN; LEUKEMIA INHIBITORY FACTOR; LUTEINIZING HORMONE; PHOSPHATIDYLSERINE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; SOMATOMEDIN C; STEM CELL FACTOR; SURVIVIN; TRANSFORMING GROWTH FACTOR ALPHA; X LINKED INHIBITOR OF APOPTOSIS;

APOPTOSIS; BLASTOCYST; CELL STRUCTURE; CELL SURVIVAL; CULTURE MEDIUM; CULTURE OPTIMIZATION; CUMULUS CELL; DEVELOPMENTAL STAGE; DNA FRAGMENTATION; EMBRYO CULTURE; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; FERTILIZATION IN VITRO; FETUS DEVELOPMENT; FLUORESCENCE IN SITU HYBRIDIZATION; GENE ACTIVITY; GENE OVEREXPRESSION; GENETIC MARKER; GENETIC REGULATION; GENOMIC INSTABILITY; HORMONE ACTION; HUMAN; MICROENVIRONMENT; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; OVULATION; PREGNANCY OUTCOME; PREGNANCY RATE; PREIMPLANTATION EMBRYO; PRIMORDIAL GERM CELL; PROTEIN EXPRESSION; REPRODUCTIVE SUCCESS; REVIEW; SIGNAL TRANSDUCTION;

APOPTOSIS; BIOLOGICAL MARKERS; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; HUMANS; MALE; OOCYTES; SIGNAL TRANSDUCTION;

EID: 68449104869     PISSN: 09298673     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986709788186075     Document Type: Review

References (128)

1. Hamamah, S. Oocyte and embryo quality: Is their morphology a good criterion? J. Gynecol. Obstet. Biol. Reprod., 2005, 34(7 Pt 2), 5S38-5S41.
2. Alikani, M.; Cohen, J.; Tomkin, G.; Garrisi G.J.; Mack, C.; Scott R.T. Human embryo fragmentation in vitro and its implications for pregnancy and implantation. Fertil. Steril., 1999, 71(5), 836-842.
3. Delimitreva, S.M.; Zhivkova, R.S.; Vatev, I.T.; Toncheva, D.I. Chromosomal disorders and nuclear and cell destruction in cleaving human embryos. Int. J. Dev. Biol., 2005, 49(4), 409-416.
4. Jacobson, M.D.; Weil, M.; Raff, M.C. Programmed cell death in animal development. Cell, 1997, 88(3), 347-354.
5. Kerr, J.F.; Wyllie, A.H.; Currie, A.R. Apoptosis: A basic biological phenomenon with wide ranging implications in tissue kinetics. Br. J. Cancer, 1972, 26, 239-257.
6. Wyllie, A.H.; Kerr, J.F.; Currie, A.R. Cell death: The significance of apoptosis. Int. Rev. Cytol., 1980, 68, 251-306
7. Feldmann, G.; Haouzi, D.; Moreau, A.; Durand-Schneider, A.M.; Bringuier, A.; Berson, A.; Mansouri, A.; Fau, D.; Pessayre, D. Opening of the mitochondrial permeability transition pore causes matrix expansion and outer membrane rupture in Fas-mediated hepatic apoptosis in mice. Hepatology, 2000, 31(3), 674-683.
8. Evan, G.I.; Wyllie, A.H.; Gilbert, C.S.; Littlewood, T.D.; Land, H.; Brooks, M.; Waters, C.M.; Penn, L.Z.; Hancock, D.C. Induction of apoptosis in fibroblasts by c-myc protein. Cell, 1992, 69, 119-128.
9. Van Engeland, M.; Nieland, L.J.; Ramaekers, F.C.; Schutte, B.; Reutelingsperger, C.P. Annexin V-affinity assay: A review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry, 1998, 31(1), 1-9.
10. Gold, R.; Schmied, M.; Rothe, G.; Zischler, H.; Breitschopf, H.; Wekerle, H.; Laussmann, H. Detection of DNA fragmentation in apoptosis: application of in situ nick translation to cell culture systems and tissue sections. J. Histochem. Cytochem., 1993, 41, 1023- 1030.
11. Migheli, A.; Attanasio, A.; Schiffer, D. Ultrastructural detection of DNA strand breaks in apoptotic neural cells by in situ end-labelling techniques. J. Pathol., 1995, 176, 27-35.
12. Mundle, S.D.; Gao, X.Z.; Khan, S.; Gregory, S.A.; Preisler, H.D.; Raza, A. Two in situ end labeling techniques reveal different patterns of DNA fragmentation during spontaneous apoptosis in vivo and induced apoptosis in vitro. Anticancer Res., 1995, 15, 1895-1904.
13. Hengartner, M.O.; Horvitz, H.R. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell, 1994, 76(4), 665-676.
14. Earnshaw, W.C.; Martins, L.M.; Kaufmann, S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem., 1999, 8, 383-424.
15. Cohen, G.M. Caspases: The executioners of apoptosis. Biochem. J., 1997, 326(Pt1), 1-16.
16. Thornberry, N.A. The caspase family of cysteine proteases. Br. Med. Bull., 1997, 53(3), 478-490.
17. Thornberry, N.A.; Lazebnik, Y. Caspases: Enemies within. Science, 1998, 281, 1312-1316.
18. Kumar, S. Caspase function in programmed cell death. Cell. Death. Differ., 2007, 14(1), 32-43.
19. Green, D.R.; Reed, J.C. Mitochondria and apoptosis. Science, 1998, 281(5381), 1309-1312.
20. Mignotte, B.; Vayssiere, J.L. Mitochondria and apoptosis. Eur. J. Biochem., 1998, 252(1), 1-15.
21. Danial, N.N.; Korsmeyer, S.J. Cell death: Critical control points. Cell, 2004, 116(2), 205-219.
22. Nagata, S.; Suda, T. Fas and Fas ligand: Lpr and gld mutations. Immunol. Today, 1995, 16, 39-43.
23. Thornberry, N.A.; Bull, H.G.; Calaycay, J.R.; Chapman, K.T.; Howard, A.D.; Kostura, M.J.; Miller, D.K.; Molineaux, S.M.; Weidner, J.R.; Aunins, J.; Elliston, K.O.; Ayala, J.M.; Casano, F.C.; Chin, J.; Ding, G.J.F; Egger, L.A.; Gaffney, E.P.; Limjuco, G.; Palyha, O.C.; Raju, S.M.; Rolando, A.M.; Salley, J.P.; Yamin, T.T.; Lee, T.D.; Shively, J.E.; MacCross, M.; Mumford, R.A.; Schmidt, J.A.; Tocci, M.J. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature, 1992, 356(6372), 768-774.
24. Li, H.; Zhu, H.; Xu, C.J.; Yuan, J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell, 1998, 94(4), 491-501.
25. Levy, R. Genetic regulation of preimplantation embryo survival. Int. Rev. Cytol., 2001, 210, 1-37.
26. Hardy, K.; Spanos, S.; Becker, D.; Iannelli, P.; Winston, R.M.; Stark, J. From cell death to embryo arrest: Mathematical models of human preimplantation embryo development. Proc. Natl. Acad. Sci. U.S.A., 2001, 98(4), 1655-1660.
27. de Pol, A.; Vaccina, F.; Foraboscu, A.; Cavazzuti, E.; Marzoni, L. Apoptosis of germ cells during human prenatal oogenesis. Hum. Reprod, 1997, 12, 2235-2241.
28. Vaskivuo, T.E.; Anttonen, M.; Herva, R.; Billig, H.; Dorland, M.; te Velde, E.R.; Stenback, F.; Heikinheimo, M.; Tapanainen, J.S. Survival of human ovarian follicles from fetal to adult life: Apoptosis, apoptosis-related proteins, and transcription factor GATA-4. J. Clin. Endocrinol. Metab., 2001, 86(7), 3421-3429.
29. Pepling, M.E.; Spradling, A.C. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev. Biol., 2001, 234, 339-351.
30. Ratts, V.S.; Flaws, J.A.; Kolp, R.; Sorenson, C.M.; Tilly, J.L. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology, 1995, 136(8), 3665-3668.
31. Pru JK, Tilly JL. Programmed cell death in the ovary: Insights and future prospects using genetic technologies. Mol. Endocrinol., 2001, 15, 845-853.
32. Quenby, S.M.; Gazvani, M.R.; Brazeau, C.; Neilson, J.; Lewis-Jones, D.I.; Vince, G. Oncogenes and tumour suppressor genes in first trimester human fetal development. Mol. Hum. Reprod., 1999, 5, 737-741.
33. Albamonte, M.S.; Willis, M.A.; Albamonte, M.I.; Jensen, F.; Espinosa, M.B.; Vitullo, A.D. The developing human ovary: Immunohistochemical analysis of germ-cell-specific VASA protein, BCL-2/Bax expression balance and apoptosis. Hum. Reprod., 2008, 23(8), 1895-1901.
34. Fenwick, M.A.; Hurst, P.R. Immunohistochemical localization of active caspase-3 in the mouse ovary: Growth and atresia of small follicles. Reproduction, 2002, 124, 659-665.
35. Matikainen, T.; Perez, G.I.; Zheng, T.S.; Kluzak, T.R.; Rueda, B.R.; Flavell, R.A.; Tilly, J.L. Caspase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary. Endocrinology, 2001, 142, 2468-2480.
36. Feldmann, G.; Benifla, J.L.; Madelenat, P. Apoptosis of granulosa cells as a predictive marker of in vitro fertilization success?. Gynecol. Obstet. Fertil., 2006, 34(7-8), 547-582.
37. Bergeron, L.; Perez, G.I.; Macdonald, G.; Shi, L.; Sun, Y.; Jurisicova, A.; Varmuza, S.; Latham, K.E.; Flaws, J.A.; Salter, J.C.; Hara, H.; Moskowitz, M.A.; Li, E.; Greenberg, A.; Tilly, J.L.; Yuan, J. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev., 1998, 12(9), 1304-1314.
38. Morita, Y.; Perez, G.I.; Maravei, D.V.; Tilly, K.I.; Tilly, J.L. Targeted expression of Bcl-2 in mouse oocytes inhibits ovarian follicle atresia and prevents spontaneous and chemotherapy-induced oocyte apoptosis in vitro. Mol. Endocrinol., 1999, 13, 841-850.
39. Martins da Silva, S.J.; Bayne, R.A.; Cambray, N.; Hartley, P.S.; McNeilly, A.S.; Anderson, R.A. Expression of activin subunits and receptors in the developing human ovary: Activin A promotes germ cell survival and proliferation prior to primordial follicle formation. Dev. Biol., 2004, 266, 334-345.
40. Dolci, S.; Pesce, M.; De Felici, M. Combined action of stem cell factor, leukemia inhibitory factor, and cAMP on in vitro proliferation of mouse primordial germ cells. Mol. Reprod. Dev., 1993, 35, 134-139.
41. Spears, N.; Molinek, M.D.; Robinson, L.L.; Fulton, N.; Cameron, H.; Shimoda, K.; Telfer, E.E.; Anderson, R.A.; Price, D.J. The role of neurotrophin receptors in female germ-cell survival in mouse and human. Development, 2003, 130(22), 5481-5491.
42. Perez, G.I.; Tilly, J.L. Cumulus cells are required for the increased apoptotic potential in oocytes of aged mice. Hum. Reprod., 1997, 12(12), 2781-2783.
43. Tilly, J.L. Commuting the death sentence: How oocytes strive to survive. Nat. Rev. Mol. Cell Biol., 2001, 2(11), 838-848.
44. Wu, J.; Zhang, L.; Wang, X. Maturation and apoptosis of human oocytes in vitro are age-related. Fertil. Steril., 2000, 74(6), 1137-1141.
45. Boone, D.L.; Carnegie, J.A; Rippstein, P.U.; Tsang, B.K. Induction of apoptosis in equine chorionic gonadotropin (eCG)-primed rat ovaries by anti-eCG antibody. Biol. Reprod., 1997, 57, 20-27.
46. Hurst, P.R.; Mora, J.M.; Fenwick, M.A. Caspase-3, TUNEL and ultrastructural studies of small follicles in adult human ovarian biopsies. Hum. Reprod., 2006, 21(8), 1974-1980.
47. Kim, J.M.; Boone, D.L.; Auyeung, A.; Tsang, B.K. Granulosa cell apoptosis induced at the penultimate stage of follicular development is associated with increased levels of Fas and Fas ligand in the rat ovary. Biol. Reprod., 1998, 58, 1170-1176.
48. Rubio Pomar, F.J.; Roelen, B.A.; Slot, K.A.; van Tol, H.T.; Colenbrander, B.; Teerds, K.J. Role of Fas-mediated apoptosis and follicle-stimulating hormone on the developmental capacity of bovine cumulus oocyte complexes in vitro. Biol. Reprod., 2004, 71(3), 790-796.
49. Chen, Q.; Yano, T.; Matsumi, H.; Osuga, Y.; Yano, N.; Xu, J.; Wada, O.; Koga, K.; Fujiwara, T.; Kugu, K.; Taketani, Y. Cross-Talk between Fas/Fas ligand system and nitric oxide in the pathway subserving granulosa cell apoptosis: A possible regulatory mechanism for ovarian follicle atresia. Endocrinology, 2005, 146(2), 808-815.
50. Malamitsi-Puchner, A.; Sarandakou, A.; Baka, S.; Vrachnis, N.; Kouskouni, E.; Hassiakos, D. Soluble Fas concentrations in the follicular fluid and oocyte-cumulus complex culture medium from women undergoing in vitro fertilization: Association with oocyte maturity, fertilization, and embryo quality. J. Soc. Gynecol. Investig., 2004, 11(8), 566-569.
51. Lee, KS.; Joo, B.S.; Na, Y.J.; Yoon, M.S.; Choi, O.H.; Kim, W.W. Relationships between concentrations of tumor necrosis factor-alpha and nitric oxide in follicular fluid and oocyte quality. J. Assist. Reprod. Genet., 2000, 17(4), 222-228.
52. Zolti, M.; Ben-Rafael, Z.; Meirom, R.; Shemesh, M.; Bider, D.; Mashiach, S.; Apte, R.N. Cytokine involvement in oocytes and early embryos. Fertil. Steril., 1991, 6(2), 265-272.
53. Maeda, A.; Inoue, N.; Matsuda-Minehata, F.; Goto, Y.; Cheng, Y.; Manabe, N. The role of interleukin-6 in the regulation of granulosa cell apoptosis during follicular atresia in pig ovaries. J. Reprod. Dev., 2007, 53(3), 481-490.
54. Kim, M.R.; Tilly, J.L. Current concepts in Bcl-2 family member regulation of female germ cell development and survival. Biochim. Biophys. Acta., 2004, 1644(2-3), 205-210.
55. Lin, C.F.; Chen, C.L.; Lin, Y.S. Ceramide in apoptotic signaling and anticancer therapy. Curr. Med. Chem., 2006, 13(14), 1609-1616.
56. Knudson, C.M.; Tung, K.S.; Tourtellotte, W.G.; Brown, G.A.; Korsmeyer, S.J. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science, 1995, 270(5233), 96-99.
57. Tilly, J.L.; Tilly, K.I.; Perez, G.I. The genes of cell death and cellular susceptibility to apoptosis in the ovary: A hypothesis. Cell. Death Differ., 1997, 4(3), 180-187.
58. Wang, Y.; Rippstein, P.U.; Tsang, B.K. Role and gonadotrophic regulation of X-linked inhibitor of apoptosis protein expression during rat ovarian follicular development in vitro. Biol. Reprod., 2003, 68, 610-619.
59. Schimmer, A.D. Inhibitor of apoptosis proteins: Translating basic knowledge into clinical practice. Cancer Res., 2004, 64, 7183-7190.
60. Assou, S.; Anahory, T.; Pantesco, V.; Le Carrour, T.; Pellestor, F.; Klein, B.; Reyftmann, L.; Dechaud, H.; De Vos, J.; Hamamah, S. The human cumulus--oocyte complex gene-expression profile. Hum. Reprod., 2006, 21(7), 1705-1719.
61. Yacobi, K.; Wojtowicz, A.; Tsafriri, A.; Gross, A. Gonadotropins enhance caspase-3 and -7 activity and apoptosis in the thecainterstitial cells of rat preovulatory follicles in culture. Endocrinology, 2004, 145, 1943-1951.
62. Murdoch, W. J.; Gottsch, M.L. Proteolytic mechanisms in the ovulatory folliculo-luteal transformation. Connect Tissue Res., 2003, 44, 50-57.
63. Pereda, J.; Cheviakoff, S.; Croxatto, H.B. Ultrastructure of a 4-cell human embryo developed in vivo. Hum. Reprod., 1989, 4(6), 680-688.
64. Holte, J.; Berglund, L.; Milton, K.; Garello, C.; Gennarelli, G.; Revelli, A.; Bergh, T. Construction of an evidence-based integrated morphology cleavage embryo score for implantation potential of embryos scored and transferred on day 2 after oocyte retrieval. Hum. Reprod., 2007, 22(2), 548-557.
65. Scott, L.; Finn, A.; O'Leary, T.; McLellan, S.; Hill, J. Morphologic parameters of early cleavage-stage embryos that correlate with fetal development and delivery: Prospective and applied data for increased pregnancy rates. Hum. Reprod., 2007, 22(1), 230-40.
66. della Ragione, T.; Verheyen, G.; Papanikolaou, E.G.; Van Landuyt, L.; Devroey, P.; Van Steirteghem, A. Developmental stage on day-5 and fragmentation rate on day-3 can influence the implantation potential of top- quality blastocysts in IVF cycles with single embryo transfer. Reprod. Biol. Endocrinol., 2007, 5, 2.
67. Ebner, T.; Yaman, C.; Moser, M.; Sommergruber, M.; Polz, W.; Tews, G. Embryo fragmentation in vitro and its impact on treatment and pregnancy outcome. Fertil. Steril., 2001, 76(2), 281-285.
68. Alikani, M.; Calderon, G.; Tomkin, G.; Garrisi, J.; Kokot, M.; Cohen, J. Cleavage anomalies in early human embryos and survival after prolonged culture in-vitro. Hum. Reprod., 2000, 15(12), 2634-2643.
69. Van Blerkom, J.; Davis, P.; Alexander, S. A microscopic and biochemical study of fragmentation phenotypes in stage-appropriate human embryos. Hum. Reprod., 2001, 16(4), 719-729.
70. Antczak, M.; Van Blerkom, J. Temporal and spatial aspects of fragmentation in early human embryos: Possible effects on developmental competence and association with the differential elimination of regulatory proteins from polarized domains. Hum. Reprod., 1999, 14(2), 429-447.
71. Trounson, A.; Sathananthan, A.H. The application of electron microscopy in the evaluation of two- to four-cell human embryos cultured in vitro for embryo transfer. J. In Vitro Fert. Embryo Transf., 1984, 1(3), 153-165.
72. Hardy, K. Appoptosis in the human embryo. J. Reprod. Fert., 1999, 4, 125-134.
73. Jurisicova, A.; Varmuza, S.; Casper, R.F. Programmed cell death and human embryo fragmentation. Mol. Hum. Reprod., 1995, 2(2), 93-98.
74. Hardy, K. Cell death in the mammalian blastocyst. Mol. Hum. Reprod., 1997, 3(10), 919-925.
75. Hardy, K.; Stark, J.; Winston, R.M. Maintenance of the inner cell mass in human blastocysts from fragmented embryos. Biol. Reprod., 2003, 68(4), 1165-1169.
76. Jurisicova, A.; Antenos, M.; Varmuza, S.; Tilly, J.L.; Casper, R.F. Expression of apoptosis-related genes during human preimplantation embryo development: Potential roles for the Harakiri gene product and Caspase-3 in blastomere fragmentation. Mol. Hum. Reprod., 2003, 9(3), 133-141.
77. Levy, R.; Benchaib, M.; Cordonier, H.; Guerin, J.F. Apoptosis in the pre-implantation embryo. Contracept. Fertil. Sex., 1998, 26(7-8), 536-541.
78. Moley, K.H.; Chi, M.M.; Knudson, C.M.; Korsmeyer, S.J.; Mueckler, M.M. Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways. Nat. Med., 1998, 4(12), 1421-1424.
79. Exley, G.E.; Tang, C.; McElhinny, A.S.; Warner, C.M. Expression of caspase and BCL-2 apoptotic family members in mouse preimplantation embryos. Biol. Reprod., 1999, 61(1), 231-239.
80. Metcalfe, A.D.; Hunter, H.R.; Bloor, D.J.; Lieberman, B.A.; Picton, H.M.; Leese, H.J.; Kimber, S.J.; Brison, D.R. Expression of 11 members of the BCL-2 family of apoptosis regulatory molecules during human preimplantation embryo development and fragmentation. Mol. Reprod. Dev., 2004, 68(1), 35-50.
81. Warner, CM.; Cao, W.; Exley, G.E.; McElhinny, A.S.; Alikani, M.; Cohen, J.; Scott, R.T.; Brenner, C.A. Genetic regulation of egg and embryo survival. Hum. Reprod., 1998, 13(Suppl 3), 178-190.
82. Spanos, S.; Rice, S.; Karagiannis, P.; Taylor, D.; Becker, D.L.; Winston, R.M.; Hardy, K. Caspase activity and expression of cell death genes during development of human preimplantation embryos. Reproduction, 2002, 124(3), 353-363.
83. Li, F.; Brattain, M.G. Role of the Survivin gene in pathophysiology. Am. J. Pathol., 2006, 169(1), 1-11.
84. Johnson, M.E.; Howerth, E.W. Survivin: A bifunctional inhibitor of apoptosis protein. Vet. Pathol., 2004, 41(6), 599-607
85. Uren, A.G.; Wong, L.; Pakusch, M.; Fowler, K.J.; Burrows, F.J.; Vaux, D.L.; Choo, K.H.A. Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr. Biol., 2000, 10, 1319-1328.
86. Kawamura, K.; Sato, N.; Fukuda, J.; Kodama, H.; Kumagai, J.; Tanikawa, H.; Shimizu, Y.; Tanaka, T. Survivin acts as an anti-apoptotic factor during the development of mouse preimplantation embryos. Dev. Biol., 2003, 256(2), 331-341.
87. O'Neill, C. The potential roles for embryotrophic ligands in preimplantation embryo development. Hum. Reprod. Update, 2008, 14(3), 275-288.
88. Bedaiwy, M.; Shahin, A.Y.; AbulHassan, A.M.; Goldberg, J.M.; Sharma, R.K.; Agarwal, A.; Falcone, T. Differential expression of follicular fluid cytokines: Relationship to subsequent pregnancy in IVF cycles. Reprod. Biomed. Online, 2007, 15(3), 321-325.
89. Spanos, S.; Becker, D.L.; Winston, R.M.; Hardy, K. Anti-apoptotic action of insulin-like growth factor-I during human preimplantation embryo development. Biol. Reprod., 2000, 63(5), 1413-1420.
90. Chen, C.S.; Mrksich, M.; Huang, S.; Whitesides, G.M.; Ingber, D.E. Geometric control of cell life and death. Science, 1997, 276, 1425-1428.
91. Bissell, M.J.; Radisky, D.C.; Rizki, A.; Weaver, V.M.; Petersen, O.W. The organizing principle: Microenvironmental influences in the normal and malignant breast. Differentiation, 2002, 70(9-10), 537-546.
92. Ingber, D.E. Mechanical signaling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circ. Res., 2002, 91, 877-887.
93. Radisky, D.; Muschler, J.; Bissell, M.J. Order and disorder: The role of extracellular matrix in epithelial cancer. Cancer Invest., 2002, 20, 139-153
94. Walpita, D.; Hay, E. Studying actin-dependent processes in tissue culture. Nat. Rev. Mol. Cell. Biol., 2002, 3, 137-141.
95. Weaver, V.M.; Peterson, O.W.; Wang, F.; Larabell, C.A.; Briand, P.; Damsky, C.; Bissell, M.J. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J. Cell. Biol., 1997, 137, 231-245.
96. Weaver, V.M.; Lelievre, S.; Lakins, J.N.; Chrenek, M.A.; Jones, J.C.; Giancotti, F.; Werb, Z.; Bissell, M.J. Beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell, 2002, 2, 205-216.
97. Downward, J. PI 3-kinase, Akt and cell survival. Semin. Cell. Dev. Biol., 2004, 15, 177-182.
98. Hardy, K.; Spanos, S. Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol., 2002, 172(2), 221-236.
99. Roberts, R.; Franks, S.; Hardy, K. Culture environment modulates maturation and metabolism of human oocytes. Hum. Reprod., 2002, 17(11), 2950-2956.
100. Hovatta, O.; Silye, R.; Abir, R.; Krausz, T.; Winston, R.M. Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum. Reprod., 1997, 12(5), 1032-1036.
101. Downs, S.M.; Utecht, A.M. Metabolism of radiolabeled glucose by mouse oocytes and oocyte-cumulus cell complexes. Biol. Reprod., 1999, 60(6), 1446-1452.
102. Roberts, R.; Stark, J.; Iatropoulou, A.; Becker, D.L.; Franks, S.; Hardy, K. Energy substrate metabolism of mouse cumulus-oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biol. Reprod., 2004, 71(1), 199-209.
103. Hoshino, Y.; Yokoo, M.; Yoshida, N.; Sasada, H.; Matsumoto, H.; Sato, E. Phosphatidylinositol 3-kinase and Akt participate in the FSH-induced meiotic maturation of mouse oocytes. Mol. Reprod. Dev., 2004, 69(1), 77-86.
104. Shimada, M.; Ito, J.; Yamashita, Y.; Okazaki, T.; Isobe, N. 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., 2003, 179(1), 25-34.
105. Blondin, P.; Sirard, M.A. Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev., 1995, 41(1), 54-62.
106. Dong, J.; Albertini, DF.; Nishimori, K.; Kumar, TR.; Lu, N.; Matzuk, M.M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature, 1996, 383(6600), 531-535.
107. Hayashi, M.; McGee, E.A.; Min, G.; Klein, C.; Rose, U.M.; van Duin, M.; Hsueh, A.J. Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology, 1999, 140(3), 1236-1244.
108. Nilsson, E.E.; Skinner, M.K. Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol. Reprod., 2002, 67(3), 1018-1024.
109. Gueripel, X.; Brun, V.; Gougeon, A. Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol. Reprod., 2006, 75(6), 836-843.
110. McNatty, K.P.; Reader, K.; Smith, P.; Heath, D.A.; Juengel, J.L. Control of ovarian follicular development to the gonadotrophin-dependent phase: a 2006 perspective. Soc. Reprod. Fertil., 2007, 64, 55-68.
111. Aaltonen, J.; Laitinen, M.P.; Vuojolainen, K.; Jaatinen, R.; Horelli-Kuitunen, N.; Seppa. L.; Louhio, H.; Tuuri, T.; Sjöberg, J.; Butzow, R.; Hovata, O.; Dale, L.; Ritvos, O. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab., 1999, (8), 2744-2750.
112. Hreinsson, J.G.; Scott, J.E.; Rasmussen, C.; Swahn, M.L.; Hsueh, A.J.; Hovatta, O. Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J. Clin. Endocrinol. Metab., 2002, 7(1), 316-321.
113. Lackey, B.R.; Gray, S.L.; Henricks, D.M. The insulin-like growth factor (IGF) system and gonadotropin regulation: Actions and interactions. Cytokine Growth Factor Rev., 1999, 10(3-4), 201-217.
114. Woodward, T.L.; Xie, J.; Fendrick, J.L.; Haslam, S.Z. Proliferation of mouse mammary epithelial cells in vitro: Interactions among epidermal growth factor, insulin-like growth factor I, ovarian hormones, and extracellular matrix proteins. Endocrinology, 2000, 141(10), 3578-3586.
115. Weber, G.M.; Moore, A.B.; Sullivan, C. In vitro actions of insulin-like growth factor-I on ovarian follicle maturation in white perch (Morone americana). Gen. Comp. Endocrinol., 2007, 151(2), 180-187.
116. Assou, S.; Le Carrour, T.; Tondeur, S.; Strom, S.; Gabelle, A.; Marty, S.; Nadal, L.; Pantesco, V.; Reme, T.; Hugnot, J.P.; Gasca, S.; Hovatta, O.; Hamamah, S.; Klein, B.; De Vos, J. A meta-analysis of human embryonic stem cells transcriptome integrated into a web-based expression atlas. Stem Cells, 2007, 25(4), 961-973.
117. Gasca, S.; Pellestor, F.; Assou, S.; Loup, V.; Anahory, T.; Dechaud, H., De Vos, J.; Hamamah, S. Identifying new human oocyte marker genes: A microarray approach. Reprod. Biomed. Online, 2007, 4(2), 175-183.
118. Brison, D.R.; Schultz, R.M. Increased incidence of apoptosis in transforming growth factor alpha-deficient mouse blastocysts. Biol. Reprod., 1998, 59(1), 136-144.
119. Morgan, K.; Wiemer, K.; Steuerwald, N.; Hoffman, D.; Maxson, W.; Godke, R. Use of video cinematography to assess morphological qualities of conventionally cultured and cocultured embryos. Hum. Reprod., 1995, 10(9), 2371-2376.
120. Kane, M.T.; Morgan, P.M.; Coonan, C. Peptide growth factors and preimplantation development. Hum. Reprod. Update, 1997, 3(2), 137-157.
121. Teruel, M.; Smith, R. Effect of embryo density and growth factors on in vitro preimplantation development of mouse embryos. Acta Physiol. Pharmacol. Ther. Latinoam., 1997, 47(2), 87-96.
122. Dunglison, G.F.; Barlow, D.H.; Sargent, I.L. Leukaemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium. Hum. Reprod., 1996, 11(1), 191-196.
123. Martin, K.L.; Barlow, D.H.; Sargent, I.L. Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum. Reprod., 1998, 13(6), 1645-1652.
124. Keefe, D.L.; Franco, S.; Liu, L.; Trimarchi, J.; Cao, B.; Weitzen, S.; Agarwal, S.; Blasco, M.A. Telomere length predicts embryo fragmentation after in vitro fertilization in women-toward a telomere theory of reproductive aging in women. Am. J. Obstet. Gynecol., 2005, 192(4), 1256-1260.
125. Cupisti, S.; Conn, C.M.; Fragouli, E.; Whalley, K.; Mills, J.A.; Faed, M.J.; Delhanty, J.D. Sequential FISH analysis of oocytes and polar bodies reveals aneuploidy mechanisms. Prenat. Diagn., 2003, 23, 663-668.
126. Pellestor, F.; Andréo, B.; Anahory, T.; Déchaud, H.; Hédon, B.; Hamamah, S. The cytogenetics of human oocytes: 40 years of progress. Gynecol. Obstet. Fertil., 2005, 33(5), 283-292.
127. Bermúdez, M.G.; Wells, D.; Malter, H.; Munné, S.; Cohen, J.; Steuerwald, N.M.; Expression profiles of individual human oocytes using microarray technology. Reprod. Biomed. Online, 2004, 8(3), 325-337.
128. Arraztoa, J.A.; Zhou, J.; Marcu, D.; Cheng, C.; Bonner, R.; Chen, M.; Xiang, C.; Brownstein, M.; Maisey, K.; Imarai, M.; Bondy, C. Identification of genes expressed in primate primordial oocytes. Hum. Reprod., 2005, 20(2), 476-483.