Global gene analysis of oocytes from early stages in human folliculogenesis shows high expression of novel genes in reproduction

Molecular Human Reproduction

Volumn 18, Issue 2, 2012, Pages 96-110

  Markholt, S ^a   Grondahl M L ^b   Ernst, E H ^a   Andersen, C Yding ^b   Ernst, E ^a   Lykke Hartmann, K ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b Rigshospitalet   (Denmark)

Author keywords

ATP6, TMEFF2, OPHN1 genes; Global gene analysis; Human follicullogenesis; Laser capture micro dissection; Primordial follicles

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ACTIVIN; ACTIVIN RECEPTOR 1; AURORA A KINASE; AURORA B KINASE; AURORA C KINASE; BETA ACTIN; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; FOLLISTATIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOGENIN; GLYCOPROTEIN; INHIBIN; NUCLEAR RECEPTOR NR6A1; OCTAMER TRANSCRIPTION FACTOR 4; PYRUVATE DEHYDROGENASE KINASE; SMAD1 PROTEIN; SMAD2 PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; STEM CELL FACTOR; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

ARTICLE; CELL ISOLATION; CELL POPULATION; CHILD; FEMALE; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; LASER CAPTURE MICRODISSECTION; MICROARRAY ANALYSIS; OOCYTE; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD;

CHILD; CYTOSKELETAL PROTEINS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTPASE-ACTIVATING PROTEINS; HUMANS; LASER CAPTURE MICRODISSECTION; MEMBRANE PROTEINS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; NEOPLASM PROTEINS; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OOCYTES; OOGENESIS; OVARIAN FOLLICLE; OVARIECTOMY; REPRODUCTION; TRANSCRIPTOME; YOUNG ADULT;

EID: 84856350806     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gar083     Document Type: Article

References (106)

1. Abir R, Ben-Haroush A, Melamed N, Felz C, Krissi H, Fisch B. Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults. Fertil Steril 2008; 89:1430-1440.
2. Accili D, Arden KC. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004;117:421-426.
3. Adhikari D, Flohr G, Gorre N, Shen Y, Yang H, Lundin E, Lan Z, Gambello MJ, Liu K. Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod 2009;15:765-770.
4. Andersen CY, Rosendahl M, Byskov AG, Loft A, Ottosen C, Dueholm M, Schmidt KL, Andersen AN, Ernst E. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Hum Reprod 2008;23:2266-2272.
5. Andrews PD, Knatko E, Moore WJ, Swedlow JR. Mitotic mechanics: the auroras come into view. Curr Opin Cell Biol 2003;15:672-683.
6. Baird DT, Collins J, Egozcue J, Evers LH, Gianaroli L, Leridon H, Sunde A, Templeton A, Van Steirteghem A, Cohen J et al. Fertility and ageing. Hum Reprod Update 2005;11:261-276.
7. Bayne RAL, Martins da Silva SJ, Anderson RA. Increased expression of the FIGLA transcription factor is associated with primoridal follicle formation in the fetal ovary. Mol Hum Reprod 2004;10: 372-381.
8. Billuart P, Bienvenu T, Ronce N, Des Portes V, Vinet MC, Zemni R, Carrie A, Beldjord C, Kahn A, Moraine C et al. Oligophrenin 1 encodes a rho-GAP protein involved in X-linked mental retardation. Pathol Biol 1998;46:678.
9. Bouilly J, Bachelot A, Broutin I, Touraine P, Binart N. Novel NOBOX loss-of-function mutations account for 6.2% of cases in a large primary ovarian insufficiency cohort. Hum Mutat 2011;32:1108-1113.
10. Brunet S, Verlhac MH. Positioning to get out of meiosis: the asymmetry of division. Hum Reprod Update 2011;17:68-75.
11. Bunney TD, Katan M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer 2010;10:342-352.
12. Castrillon DH, Miao LL, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003;301:215-218.
13. Chen X, Overcash R, Green T, Hoffman D, Asch AS, Ruiz-Echevarria MJ. The tumor suppressor activity of the transmembrane protein with epidermal growth factor and two follistatin motifs 2 (TMEFF2) correlates with its ability to modulate sarcosine levels. J Biol Chem 2011;286:16091-17000.
14. Choi Y, Rajkovic A. Genetics of early mammalian folliculogenesis. Cell Mol Life Sci 2006;63:579-590.
15. Choi Y, Yuan D, Rajkovic A. Germ cell-specific transcriptional regulator Sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol Reprod 2008;79:1176-1182.
16. Cohen CD, Grone HJ, Grone EF, Nelson PJ, Schlondorff D, Kretzler M. Laser microdissection and gene expression analysis on formaldehyde-fixed archival tissue. Kidney Int 2002;61:125-132.
17. Cully M, You H, Levine AJ, Mak TW. Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat Rev Cancer 2006;6:184-192.
18. Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Fertility preservation: successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin's disease. Oncologist 2007;12:1437-1442.
19. Dharma SJ, Modi DN, Nandedkar TD. Gene expression profiling during early folliculogenesis in the mouse ovary. Fertil Steril 2009; 91:2025-2036.
20. Downs SM. Regulation of the G2/M transition in rodent oocytes. Mol Reprod Dev 2010;77:566-585.
21. Espina V, Milia J, Wu G, Cowherd S, Liotta LA. Laser capture microdissection. Methods Mol Biol 2006a;319:213-229.
22. Espina V, Wulfkuhle JD, Calvert VS, VanMeter A, Zhou W, Coukos G, Geho DH, Petricoin EF III, Liotta LA. Laser-capture microdissection. Nat Protoc 2006b;1:586-603.
23. Fackelmayer FO, Richter A. hnRNP-U/SAF-A is encoded by two differentially polyadenylated mRNAs in human cells. Biochim Biophys Acta 1994;1217:232-234.
24. Fortune JE. The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim Reprod Sci 2003;78:135-163.
25. Fowler PA, Flannigan S, Mathers A, Gillanders K, Lea RG, Wood MJ, Maheshwari A, Bhattacharya S, Collie-Duguid ES, Baker PJ et al. Gene expression analysis of human fetal ovarian primordial follicle formation. J Clin Endocrinol Metab 2009;94:1427-1435.
26. Fowler PA, Anderson RA, Saunders PT, Kinnell H, Mason JI, Evans DB, Bhattacharya S, Flannigan S, Franks S, Monteiro A et al. Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary. J Clin Endocrinol Metab 2011;96:1754-1762.
27. Gallardo TD, John GB, Bradshaw K, Welt C, Reijo-Pera R, Vogt PH, Touraine P, Bione S, Toniolo D, Nelson LM et al. Sequence variation at the human FOXO3 locus: a study of premature ovarian failure and primary amenorrhea. Hum Reprod 2008;23:216-221.
28. Gery S, Sawyers CL, Agus DB, Said JW, Koeffler HP. TMEFF2 is an androgen-regulated gene exhibiting antiproliferative effects in prostate cancer cells. Oncogene 2002;21:4739-4746.
29. Gook DA, Edgar DH, Borg J, Martic M. Detection of zona pellucida proteins during human folliculogenesis. Hum Reprod 2008;23:394-402.
30. Grondahl ML, Yding Andersen C, Bogstad J, Nielsen FC, Meinertz H, Borup R. Gene expression profiles of single human mature oocytes in relation to age. Hum Reprod 2010;25:957-968.
31. Herrera L, Ottolenghi C, Garcia-Ortiz JE, Pellegrini M, Manini F, Ko MS, Nagaraja R, Forabosco A, Schlessinger D. Mouse ovary developmental RNA and protein markers from gene expression profiling. Dev Biol 2005;279:271-290.
32. Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol 1991;124:43-101.
33. Horie M, Mitsumoto Y, Kyushiki H, Kanemoto N, Watanabe A, Taniguchi Y, Nishino N, Okamoto T, Kondo M, Mori T et al. Identification and characterization of TMEFF2, a novel survival factor for hippocampal and mesencephalic neurons. Genomics 2000; 67:146-152.
34. Hosaka T, Biggs WH, Tieu D, Boyer AD, Varki NM, Cavenee WK, Arden KC. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 2004;101:2975-2980.
35. Huntriss J, Hinkins M, Picton HM. cDNA cloning and expression of the human NOBOX gene in oocytes and ovarian follicles. Mol Hum Reprod 2006;12:283-289.
36. Jagarlamudi K, Liu L, Adhikari D, Reddy P, Idahl A, Ottander U, Lundin E, Liu K. Oocyte-specific deletion of Pten in mice reveals a stage-specific function of PTEN/PI3K signaling in oocytes in controlling follicular activation. PLoS One 2009;4:e6186.
37. John GB, Shirley LJ, Gallardo TD, Castrillon DH. Specificity of the requirement for Foxo3 in primordial follicle activation. Reproduction 2007;133:855-863.
38. John GB, Gallardo TD, Shirley LJ, Castrillon DH. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 2008;321:197-204.
39. Kanemoto N, Horie M, Omori K, Nishino N, Kondo M, Noguchi K, Tanigami A. Expression of TMEFF1 mRNA in the mouse central nervous system: precise examination and comparative studies of TMEFF1 and TMEFF2. Brain Res Mol Brain Res 2001;86:48-55.
40. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006;132:191-206.
41. Kohn M, Kehrer-Sawatzki H, Steinbach P, Marshall Graves JA, Hameister H. Recruitment of old genes to new functions: evidences obtained by comparing the orthologues of human XLMR genes in mouse and chicken. Cytogenet Genome Res 2007;116:173-180.
42. Lee J, Ko M, Joo CK. Rho plays a key role in TGF-beta1-induced cytoskeletal rearrangement in human retinal pigment epithelium. J Cell Physiol 2008a;216:520-526.
43. Lee JA, Park JE, Lee DH, Park SG, Myung PK, Park BC, Cho S. G1 to S phase transition protein 1 induces apoptosis signal-regulating kinase 1 activation by dissociating 14-3-3 from ASK1. Oncogene 2008b; 27:1297-1305.
44. Li J, Kawamura K, Cheng Y, Liu S, Klein C, Duan EK, Hsueh AJ. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci USA 2010;107:10280-10284.
45. Liang LF, Soyal SM, Dean J. Figa, a germ specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 1997;124:4939-4947.
46. Liu Y, Bankaitis VA. Phosphoinositide phosphatases in cell biology and disease. Prog Lipid Res 2010;49:201-217.
47. Liu K, Rajareddy S, Liu L, Jagarlamudi K, Boman K, Selstam G, Reddy P. Control of mammalian oocyte growth and early follicular development by the oocyte PI3 kinase pathway: new roles for an old timer. Dev Biol 2006;299:1-11.
48. Liu L, Rajareddy S, Reddy P, Du C, Jagarlamudi K, Shen Y, Gunnarsson D, Selstam G, Boman K, Liu K. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a. Development 2007a;134:199-209.
49. Liu L, Rajareddy S, Reddy P, Jagarlamudi K, Du C, Shen Y, Guo Y, Boman K, Lundin E, Ottander U et al. Phosphorylation and inactivation of glycogen synthase kinase-3 by soluble kit ligand in mouse oocytes during early follicular development. J Mol Endocrinol 2007b;38:137-146.
50. Mahmoud MS, Merhi ZO, Yelian FD. Mechanisms of premature ovarian failure: reappraisal and overview. J Reprod Med 2007;52:623-629.
51. Maraldi T, Riccio M, Sena P, Marzona L, Nicoli A, La Marca A, Marmiroli S, Bertacchini J, La Sala G, De Pol A. MATER protein as substrate of PKCepsilon in human cumulus cells. Mol Hum Reprod 2009; 15:499-506.
52. Marshall OJ. PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 2004; 20:2471-2472.
53. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000;21:200-214.
54. McLaughlin EA, McIver SC. Awakening the oocyte: controlling primordial follicle development. Reproduction 2009;137:1-11.
55. McLaughlin M, Telfer EE. Oocyte development in bovine primordial follicles is promoted by activin and FSH within a two-step serum-free culture system. Reproduction 2010;139:971-978.
56. McLaughlin M, Bromfield JJ, Albertini DF, Telfer EE. Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Mol Hum Reprod 2010;16:644-653.
57. Monti M, Redi C. Oogenesis specific genes (Nobox, Oct4, Bmp15, Gdf9, Oogenesin1 and Oogenesin2) are differentially expressed during natural and gonadotropin-induced mouse follicular development. Mol Reprod Dev 2009;76:994-1003.
58. Mori N, Fujii M, Hinz M, Nakayama K, Yamada Y, Ikeda S, Yamasaki Y, Kashanchi F, Tanaka Y, Tomonaga M et al. Activation of cyclin D1 and D2 promoters by human T-cell leukemia virus type I tax protein is associated with IL-2-independent growth of T cells. Int J Cancer 2002;99:378-385.
59. Nakano-Kobayashi A, Kasri NN, Newey SE, Van Aelst L. The Rho-linked mental retardation protein OPHN1 controls synaptic vesicle endocytosis via endophilin A1. Curr Biol 2009;19:1133-1139.
60. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998;95:379-391.
61. Nigg EA. Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2001;2:21-32.
62. Pagedar NA, Wang W, Chen DH, Davis RR, Lopez I, Wright CG, Alagramam KN. Gene expression analysis of distinct populations of cells isolated from mouse and human inner ear FFPE tissue using laser capture microdissection-a technical report based on preliminary findings. Brain Res 2006;1091:289-299.
63. Pangas SA, Choi Y, Ballow DJ, Zhao Y, Westphal H, Matzuk MM, Rajkovic A. Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc Natl Acad Sci USA 2006; 103:8090-8095.
64. Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA. Stella is a maternal effect gene required for normal early development in mice. Curr Biol 2003;13:2110-2117.
65. Peluso JJ, Pappalardo A, Losel R, Wehling M. Progesterone membrane receptor component 1 expression in the immature rat ovary and its role in mediating progesterone's antiapoptotic action. Endocrinology 2006;147:3133-3140.
66. Penland SK, Keku TO, Torrice C, He X, Krishnamurthy J, Hoadley KA, Woosley JT, Thomas NE, Perou CM, Sandler RS et al. RNA expression analysis of formalin-fixed paraffin-embedded tumors. Lab Invest 2007;87:383-391.
67. Pollack SE, Furth EE, Kallen CB, Arakane F, Kiriakidou M, Kozarsky KF, Strauss JF 3rd. Localization of the steroidogenic acute regulatory protein in human tissues. J Clin Endocrinol Metab 1997;82:4243-4251.
68. Ralston A, Rossant J. The genetics of induced pluripotency. Reproduction 2010;139:35-44.
69. Ramakers GJ. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci 2002;25:191-199.
70. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008;319:611-613.
71. Reddy P, Adhikari D, Zheng W, Liang S, Hamalainen T, Tohonen V, Ogawa W, Noda T, Volarevic S, Huhtaniemi I et al. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum Mol Genet 2009;18: 2813-2824.
72. Reynaud K, Driancourt MA. Oocyte attrition. Mol Cell Endocrinol 2000; 163:101-108.
73. Richardson SJ, Senikas V, Nelson JF. Follicular depletion during the menopausal transition: evidence for accelerated loss and ultimate exhaustion. J Clin Endocrinol Metab 1987;65:1231-1237.
74. Ruchaud S, Carmena M, Earnshaw WC. Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 2007;8:798-812.
75. Schmidt KL, Byskov AG, Nyboe Andersen A, Muller J, Yding Andersen C. Density and distribution of primordial follicles in single pieces of cortex from 21 patients and in individual pieces of cortex from three entire human ovaries. Hum Reprod 2003a;18:1158-1164.
76. Schmidt KLT, Ernst E, Byskov AG, Andersen AN, Andersen CY. Survival of primordial follicles following prolonged transportation of ovarian tissue prior to cryopreservation. Hum Reprod 2003b; 18:2654-2659.
77. Schmidt KL, Larsen E, Bangsboll S, Meinertz H, Carlsen E, Andersen AN. Assisted reproduction in male cancer survivors: fertility treatment and outcome in 67 couples. Hum Reprod 2004;19:2806-2810.
78. Schuster J, Karlsson T, Karlstrom PO, Poromaa IS, Dahl N. Down-regulation of progesterone receptor membrane component 1 (PGRMC1) in peripheral nucleated blood cells associated with premature ovarian failure (POF) and polycystic ovary syndrome (PCOS). Reprod Biol Endocrinol 2010;8:58-63.
79. Sen A, Hammes SR. Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Mol Endocrinol 2010; 24:1393-1403.
80. Sena P, Riccio M, Marzona L, Nicoli A, Marsella T, Marmiroli S, Bertacchini J, Fano RA, La Sala GB, De Pol A. Human MATER localization in specific cell domains of oocytes and follicular cells. Reprod Biomed Online 2009;18:226-234.
81. Serafica MD, Goto T, Trounson AO. Transcripts from a human primordial follicle cDNA library. Hum Reprod 2005;20:2074-2091.
82. Sharif B, Na J, Lykke-Hartmann K, McLaughlin SH, Laue E, Glover DM, Zernicka-Goetz M. The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes. J Cell Sci 2010;123:4292-4300.
83. Sirotkin AV. Transcription factors and ovarian functions. J Cell Physiol 2010; 225:20-26.
84. Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005;11:461-471.
85. Small CL, Shima JE, Uzumcu M, Skinner MK, Griswold MD. Profiling gene expression during the differentiation and development of the murine embryonic gonad. Biol Reprod 2005;72:492-501.
86. Soyal SM, Amleh A, Dean J. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development 2000; 127:4645-4654.
87. Specht K, Richter T, Muller U, Walch A, Werner M, Hofler H. Quantitative gene expression analysis in microdissected archival formalin-fixed and paraffin-embedded tumor tissue. Am J Pathol 2001; 158:419-429.
88. Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP. GSEA-P: a desktop application for Gene Set Enrichment Analysis. Bioinformatics 2007;23:3251-3253.
89. Sugiura K, Su YQ, Eppig JJ. Does bone morphogenetic protein 6 (BMP6) affect female fertility in the mouse? Biol Reprod 2010;83:997-1004.
90. Sun RZ, Lei L, Cheng L, Jin ZF, Zu SJ, Shan ZY, Wang ZD, Zhang JX, Liu ZH. Expression of GDF-9, BMP-15 and their receptors in mammalian ovary follicles. J Mol Histol 2010;41:325-332.
91. Tatone C, Heizenrieder T, Di Emidio G, Treffon P, Amicarelli F, Seidel T, Eichenlaub-Ritter U. Evidence that carbonyl stress by methylglyoxal exposure induces DNA damage and spindle aberrations, affects mitochondrial integrity in mammalian oocytes and contributes to oocyte ageing. Hum Reprod 2011;26:1843-1859.
92. Teixeira Filho FL, Baracat EC, Lee TH, Suh CS, Matsui M, Chang RJ, Shimasaki S, Erickson GF. Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab 2002;87:1337-1344.
93. Tömälä RM, Jääskeläinen M, Lakkakorpi J, Liakka A, Tapanainen JS, Vaskivuo TE. Zona pellucida components are present in human fetal ovary before follicle formation. Mol Cell Endocrinol 2008;289:10-15.
94. Tong ZB, Nelson LM. A mouse gene encoding an oocyte antigen associated with autoimmune premature ovarian failure. Endocrinology 1999;140:3720-3726.
95. Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, Bondy CA, Dean J, Nelson LM. Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet 2000;26:267-268.
96. Toyoda S, Miyazaki T, Miyazaki S, Yoshimura T, Yamamoto M, Tashiro F, Yamato E, Miyazaki J. Sohlh2 affects differentiation of KIT positive oocytes and spermatogonia. Dev Biol 2009;325:238-248.
97. Tsai ZY, Singh S, Yu SL, Kao LP, Chen BZ, Ho BC, Yang PC, Li SSL. Identification of MicroRNAs regulated by activin A in human embryonic stem cells. J Cell Biochem 2010;109:93-102.
98. Uchida T, Wada K, Akamatsu T, Yonezawa M, Noguchi H, Mizoguchi A, Kasuga M, Sakamoto C. A novel epidermal growth factor-like molecule containing two follistatin modules stimulates tyrosine phosphorylation of erbB-4 in MKN28 gastric cancer cells. Biochem Biophys Res Commun 1999;266:593-602.
99. Venkatesh S, Kumar M, Sharma A, Kriplani A, Ammini AC, Talwar P, Agarwal A, Dada R. Oxidative stress and ATPase6 mutation is associated with primary ovarian insufficiency. Arch Gynecol Obstet 2010;282:313-318.
100. Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet 2003a;33: 187-191.
101. Wu X, Wang P, Brown CA, Zilinski CA, Matzuk MM. Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol Reprod 2003b;69:861-867.
102. Yan X, Yu S, Lei A, Hua J, Chen F, Li L, Xie X, Yang X, Geng W, Dou Z. The four reprogramming factors and embryonic development in mice. Cell Reprogram 2010;12:565-570.
103. Yang KT, Li SK, Chang CC, Tang CJ, Lin YN, Lee SC, Tang TK. Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Mol Biol Cell 2010;21:2371-2383.
104. Yoon SJ, Kim KH, Chung HM, Choi DH, Lee WS, Cha KY, Lee KA. Gene expression profiling of early follicular development in primordial, primary, and secondary follicles. Fertil Steril 2006;85:193-203.
105. Zhao H, Qin Y, Kovanci E, Simpson JL, Chen ZJ, Rajkovic A. Analyses of GDF9 mutation in 100 Chinese women with premature ovarian failure. Fertil Steril 2007;88:1474-1476.
106. Zuccotti M, Merico V, Cecconi S, Redi CA, Garagna S. What does it take to make a developmentally competent mammalian egg? Hum Reprod Update 2011;17:525-540.