Genetics of mammalian reproduction: Modeling the end of the germline

Annual Review of Physiology

Volumn 74, Issue , 2012, Pages 503-528

  Matzuk, Martin M ^a   Burns, Kathleen H ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gametogenesis; Preimplantation embryonic development; Transgenic mouse

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ACTIVIN RECEPTOR 2; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN A1; FIBROBLAST GROWTH FACTOR 9; FOLLISTATIN; GAMMA GLUTAMYLTRANSFERASE; GONADORELIN; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INHIBIN A; LEUKEMIA INHIBITORY FACTOR; MIXED LINEAGE LEUKEMIA PROTEIN; MUELLERIAN INHIBITING FACTOR; NUCLEAR RECEPTOR DAX 1; NUCLEOPLASMIN; OXYTOCIN RECEPTOR; PENTRAXIN 3; RETINOBLASTOMA PROTEIN; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; WNT4 PROTEIN;

ANDROGEN INSENSITIVITY SYNDROME; ARTICLE; CELL COMMUNICATION; CELL FUNCTION; CHROMOSOMAL LOCALIZATION; DIZYGOTIC TWINS; DNA DAMAGE; DNA END JOINING REPAIR; DNA METHYLATION; EMBRYO DEVELOPMENT; ENDOCRINE FUNCTION; EPIGENETICS; EXCISION REPAIR; FEMALE GENITAL SYSTEM; FRAMESHIFT MUTATION; GAMETOGENESIS; GENE FUNCTION; GENE IDENTIFICATION; GENE INACTIVATION; GENE LOCUS; GENE MUTATION; GENE PRODUCT; GERM CELL; GERM LINE GENE THERAPY; GRANULOSA CELL; HISTONE MODIFICATION; HOMOLOGOUS RECOMBINATION; HORMONE SYNTHESIS; HUMAN GENETICS; IN VIVO STUDY; INFERTILITY; INTRACELLULAR SIGNALING; LESCH NYHAN SYNDROME; LIGAND BINDING; LOSS OF FUNCTION MUTATION; MAMMALIAN GENETICS; MIXED MULLERIAN TUMOR; MOLECULAR INTERACTION; MOUSE; MUTAGENESIS; NONHUMAN; OOCYTE; OVARY FOLLICLE DEVELOPMENT; PARACRINE SIGNALING; POINT MUTATION; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PRONUCLEUS; SEX DETERMINATION; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; SOMATIC CELL; SPERMATOGENESIS; SRY GENE; TESTICULAR FEMINIZATION; TRANSGENICS; X CHROMOSOME; Y CHROMOSOME;

ADULT; ANIMALS; CHROMOSOMES, HUMAN, Y; EMBRYONIC DEVELOPMENT; FEMALE; GENETIC TECHNIQUES; GENETICS; GERM CELLS; HUMANS; INFERTILITY; MALE; MICE; MICE, TRANSGENIC; PREGNANCY; REPRODUCTION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84857250000     PISSN: 00664278     EISSN: 15451585     Source Type: Book Series    
DOI: 10.1146/annurev-physiol-020911-153248     Document Type: Article

References (171)

1. Matzuk MM, Burns K, Viveiros MM, Eppig J. 2002. Intercellular communication in the mammalian ovary: Oocytes carry the conversation. Science 296:2178-80 (Pubitemid 34680291)
2. Matzuk MM, Lamb DJ. 2002. Genetic dissection of mammalian fertility pathways. Nat. Med. 8(Suppl. 1):41-49
3. Chang H, Brown CW, Matzuk MM. 2002. Genetic analysis of the mammalian TGF-β superfamily. Endocr. Rev. 23:787-823 (Pubitemid 35454589)
4. Matzuk MM, Lamb DJ. 2008. The biology of infertility: research advances and clinical challenges. Nat. Med. 14:1197-213
5. Edson MA, Nagaraja AK, Matzuk MM. 2009. The mammalian ovary from genesis to revelation. Endocr. Rev. 30:624-712
6. Ford CE, Jones KW, Polani PE, de Almeida JC, Briggs JH. 1959. A sex-chromosome anomaly in a case of gonadal dysgenesis (Turners syndrome). Lancet 1:711-13
7. Jacobs PA, Strong JA. 1959. A case of human intersexuality having a possible XXY sex-determining mechanism. Nature 183:302-3
8. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, et al. 1990. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:240-44
9. Berta P, Hawkins JR, Sinclair AH, Taylor A, Griffiths BL, et al. 1990. Genetic evidence equating SRY and the testis-determining factor. Nature 348:448-50 (Pubitemid 120015086)
10. Koopman P, Munsterberg A, Capel B, Vivian N, Lovell-Badge R. 1990. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348:450-52 (Pubitemid 120015087)
11. Parma P, Radi O, Vidal V, Chaboissier MC, Dellambra E, et al. 2006. R-spondin1 is essential in sex determination, skin differentiation and malignancy. Nat. Genet. 38:1304-9 (Pubitemid 44646293)
12. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, et al. 2009. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139:1130-42
13. MacLaughlin DT, Donahoe PK. 2004. Sex determination and differentiation. N. Engl. J. Med. 350:367-78 (Pubitemid 38101632)
14. Veitia RA. 2010. FOXL2 versus SOX9: a lifelong "battle of the sexes. " BioEssays 32:375-80
15. Seeburg PH, Adelman JP. 1984. Characterization of cDNA for precursor of human luteinizing hormone releasing hormone. Nature 311:666-68 (Pubitemid 14000659)
16. Franco B, Guioli S, Pragliola A, Incerti B, Bardoni B, et al. 1991. A gene deleted in Kallmanns syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 353:529-36 (Pubitemid 21912544)
17. Legouis R, Hardelin JP, Levilliers J, Claverie JM, Compain S, et al. 1991. The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 67:423-35
18. Weiss J, Axelrod L, Whitcomb RW, Harris PE, Crowley WF, Jameson JL. 1992. Hypogonadism caused by a single amino acid substitution in the βsubunit of luteinizing hormone. N. Engl. J. Med. 326:179-83
19. Matthews CH, Borgato S, Beck-Peccoz P, Adams M, Tone Y, et al. 1993. Primary amenorrhoea and infertility due to a mutation in the β-subunit of follicle-stimulating hormone. Nat. Genet. 5:83-86 (Pubitemid 23261525)
20. Shenker A, Laue L, Kosugi S, Merendino JJ Jr, Minegishi T, Cutler GB Jr. 1993. A constitutively activating mutation of the luteinizing hormone receptor in familial male precocious puberty. Nature 365:652-54 (Pubitemid 23350536)
21. Aittomaki K, Lucena JLD, Pakarinen P, Sistonen P, Tapanainen J, et al. 1995. Mutation in the follicle stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 82:959-68
22. Bianco SD, Kaiser UB. 2009. The genetic and molecular basis of idiopathic hypogonadotropic hypogonadism. Nat. Rev. Endocrinol. 5:569-76
23. Lyon MF, Hawkes SG. 1970. X-linked gene for testicular feminization in the mouse. Nature 227:1217-19
24. Chang CS, Kokontis J, Liao ST. 1988. Molecular cloning of human and rat complementary DNA encoding androgen receptors. Science 240:324-26
25. Lubahn DB, Joseph DR, Sar M, Tan J, Higgs HN, et al. 1988. The human androgen receptor: complementary deoxyribonucleic acid cloning, sequence analysis and gene expression in prostate. Mol. Endocrinol. 2:1265-75 (Pubitemid 19005939)
26. Charest NJ, Zhou ZX, Lubahn DB, Olsen KL, Wilson EM, French FS. 1991. A frameshift mutation destabilizes androgen receptor messenger RNA in the Tfm mouse. Mol. Endocrinol. 5:573-81
27. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, FinkG. 1977. Gonadotrophin-releasing hormone deficiency in a mutant mouse with hypogonadism. Nature 269:338-40 (Pubitemid 8178658)
28. Mason AJ, Hayflick JS, Zoeller RT, Young WS III, Phillips HS, et al. 1986. A deletion truncating the gonadotropin-releasing hormone gene is responsible for hypogonadism in the hpg mouse. Science 234:1366-71
29. Gordon JW, Ruddle FH. 1981. Integration and stable germ line transmission of genes injected into mouse pronuclei. Science 214:1244-46 (Pubitemid 12167330)
30. Costantini F, Lacy E. 1981. Introduction of a rabbit β-globin gene into the mouse germ line. Nature 294:92-94 (Pubitemid 12208163)
31. Brinster RL, Chen HY, Trumbauer M, Senear AW, Warren R, Palmiter RD. 1981. Somatic expression of herpes thymidine kinase in mice following injection of a fusion gene into eggs. Cell 27:223-31 (Pubitemid 12205987)
32. Palmiter RD, Brinster RL, Hammer RE, Trumbauer ME, Rosenfeld MG, et al. 1982. Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature 300:611-15 (Pubitemid 13253313)
33. Palmiter RD, Norstedt G, Gelinas RE, Hammer RE, Brinster RL. 1983. Metallothionein-human GH fusion genes stimulate growth of mice. Science 222:809-14 (Pubitemid 14227548)
34. Mason AJ, Pitts SL, Nikolics K, Szonyi E, Wilcox JN, et al. 1986. The hypogonadal mouse: reproductive functions restored by gene therapy. Science 234:1372-78 (Pubitemid 17210215)
35. Kumar TR, Low MJ, Matzuk MM. 1998. Genetic rescue of follicle-stimulating hormone β-deficient mice. Endocrinology 139:289-95
36. Kuehn MR, Bradley A, Robertson EJ, Evans MJ. 1987. A potential animal model for Lesch-Nyhan syndrome through introduction of HPRT mutations into mice. Nature 326:295-98 (Pubitemid 17053753)
37. Thompson S, Clarke AR, Pow AM, Hooper ML, Melton DW. 1989. Germ line transmission and expression of a corrected HPRT gene produced by gene targeting in embryonic stem cells. Cell 56:313-21 (Pubitemid 19050303)
38. Schwartzberg PL, Goff SP, Robertson EJ. 1989. Germ-line transmission of a c-abl mutation produced by targeted gene disruption in ES cells. Science 246:799-803 (Pubitemid 19279169)
39. Zijlstra M, Li E, Sajjadi F, Subramani S, Jaenisch R. 1989. Germ-line transmission of a disrupted β2- microglobulin gene produced by homologous recombination in embryonic stem cells. Nature 342:435-38 (Pubitemid 19277519)
40. Koller BH, Hagemann LJ, Doetschman T, Hagaman JR, Huang S, et al. 1989. Germ-line transmission of a planned alteration made in a hypoxanthine phosphoribosyltransferase gene by homologous recombination in embryonic stem cells. Proc. Natl. Acad. Sci. USA 86:8927-31 (Pubitemid 20010338)
41. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, et al. 1992. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359:76-79
42. Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A. 1992. α-Inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 360:313-19 (Pubitemid 23000668)
43. Ohinata Y, Payer B, OCarroll D, Ancelin K, Ono Y, et al. 2005. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207-13 (Pubitemid 41021265)
44. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, et al. 2008. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40:1016-22
45. Matzuk MM, Lu H, Vogel H, Sellheyer K, Roop DR, Bradley A. 1995. Multiple defects and perinatally death in mice deficient in follistatin. Nature 372:360-63
46. Yao HHC, Matzuk MM, Jorgez CJ, Menke DB, Page DC, et al. 2004. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev. Dyn. 230:210-15 (Pubitemid 38669583)
47. Mathews LS, Vale WW. 1991. Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65:973-82
48. Attisano L, Wrana JL, Cheifetz S, Massague J. 1992. Novel activin receptors: Distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68:97-108
49. Willis SA, Zimmerman CM, Li LI, Mathews LS. 1996. Formation and activation by phosphorylation of activin receptor complexes. Mol. Endocrinol. 10:367-79 (Pubitemid 26112401)
50. Lewis KA, Gray PC, Blount AL, MacConell LA, Wiater E, et al. 2000. Betaglycan binds inhibin and can mediate functional antagonism of activin signalling. Nature 404:411-14 (Pubitemid 30164345)
51. Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, et al. 1995. Functional analysis of activins in mammalian development. Nature 374:354-56
52. Vassalli A, Matzuk MM, Gardner HA, Lee KF, Jaenisch R. 1994. Activin/inhibin βB subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev. 8:414-27
53. Pangas SA, Jorgez CJ, Tran M, Agno J, Li X, et al. 2007. Intraovarian activins are required for female fertility. Mol. Endocrinol. 21:2458-71 (Pubitemid 47529358)
54. Matzuk MM, Kumar TR, Bradley A. 1995. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374:356-60
55. Kumar TR, Wang Y, Lu N, Matzuk MM. 1997. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 15:201-4 (Pubitemid 27061644)
56. Matzuk MM, Finegold MJ, Mather JP, Krummen L, Lu H, Bradley A. 1994. Development of cancer cachexia-like syndrome and adrenal tumors in inhibin-deficient mice. Proc. Natl. Acad. Sci. USA 91:8817-21
57. Coerver KA, Woodruff TK, Finegold MJ, Mather J, Bradley A, Matzuk MM. 1996. Activin signaling through activin receptor type II causes the cachexia-like symptoms in inhibin-deficient mice. Mol. Endocrinol. 10:534-43
58. Behringer RR, Finegold MJ, Cate RL. 1994. Müllerian-inhibiting substance function duringmammalian sexual development. Cell 79:415-25
59. Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, et al. 1999. Control of primordial follicle recruitment by anti-M üllerian hormone in the mouse ovary. Endocrinology 140:5789-96 (Pubitemid 30645368)
60. Visser JA, de Jong FH, Laven JS, Themmen AP. 2006. Anti-Müllerian hormone: a new marker for ovarian function. Reproduction 131:1-9 (Pubitemid 43230697)
61. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. 1996. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383:531-35 (Pubitemid 26346180)
62. Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM. 1998. The bonemorphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 12:1809-17 (Pubitemid 28544177)
63. Davis GH, McEwan JC, Fennessy PF, Dodds KG, Farquhar PA. 1991. Evidence for the presence of a major gene influencing ovulation rate on the X chromosome of sheep. Biol. Reprod. 44:620-24
64. Davis GH, Bruce GD, Reid PJ. 1994. Breeding implications of the streak ovary condition in homozygous FecXI/FecXI Inverdale sheep. Proc. World Congr. Genet. Appl. Livest. Prod. , 5th, Guelph, Can. , Aug. , 19:249-52
65. Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, et al. 2000. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosagesensitive manner. Nat. Genet. 25:279-83 (Pubitemid 30437312)
66. Otsuka F, McTavish KJ, Shimasaki S. 2011. Integral role of GDF-9 and BMP-15 in ovarian function. Mol. Reprod. Dev. 78:9-21
67. Montgomery GW, Zhao ZZ, Marsh AJ, Mayne R, Treloar SA, et al. 2004. A deletionmutation in GDF9 in sisters with spontaneous DZ twins. Twin Res. 7:548-55 (Pubitemid 39643555)
68. Palmer JS, Zhao ZZ, Hoekstra C, Hayward NK, Webb PM, et al. 2006. Novel variants in growth differentiation factor 9 in mothers of dizygotic twins. J. Clin. Endocrinol. Metab. 91:4713-16 (Pubitemid 44833463)
69. Di Pasquale E, Beck-Peccoz P, Persani L. 2004. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am. J. Hum. Genet. 75:106-11 (Pubitemid 38801906)
70. 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 303:682-84 (Pubitemid 38141636)
71. Sugiura K, Su YQ, Diaz FJ, Pangas SA, Sharma S, et al. 2007. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134:2593-603 (Pubitemid 47225956)
72. Su YQ, Sugiura K, Wigglesworth K, OBrien MJ, Affourtit JP, et al. 2008. Oocyte regulation ofmetabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135:111-21 (Pubitemid 351201485)
73. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330:366-69
74. Wilson T, Wu XY, Juengel JL, Ross IK, Lumsden JM, et al. 2001. Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod. 64:1225-35 (Pubitemid 32239195)
75. Yi SE, LaPolt PS, Yoon BS, Chen JY, Lu JK, Lyons KM. 2001. The type I BMP receptor BmprIB is essential for female reproductive function. Proc. Natl. Acad. Sci. USA 98:7994-99 (Pubitemid 32642675)
76. Moore RK, Otsuka F, Shimasaki S. 2003. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J. Biol. Chem. 278:304-10 (Pubitemid 36043577)
77. Itman C, Mendis S, Barakat B, Loveland KL. 2006. All in the family: TGF-β family action in testis development. Reproduction 132:233-46 (Pubitemid 44269705)
78. Li Q, Graff JM, OConnor AE, Loveland KL, Matzuk MM. 2007. SMAD3 regulates gonadal tumorigenesis. Mol. Endocrinol. 21:2472-86 (Pubitemid 47529359)
79. Li Q, Pangas SA, Jorgez CJ, Graff JM, Weinstein M, Matzuk MM. 2008. Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol. Cell. Biol. 28:7001-11
80. Zhao G-Q, Liaw L, Hogan BLM. 1998. Bone morphogenetic protein 8A plays a role in themaintenance of spermatogenesis and the integrity of the epididymis. Development 125:1103-12 (Pubitemid 28171205)
81. Zhao GQ, Chen YX, Liu XM, Xu Z, Qi X. 2001. Mutation in Bmp7 exacerbates the phenotype of Bmp8a mutants in spermatogenesis and epididymis. Dev. Biol. 240:212-22 (Pubitemid 33141118)
82. Hu J, Chen YX, Wang D, Qi X, Li TG, et al. 2004. Developmental expression and function of Bmp4 in spermatogenesis and in maintaining epididymal integrity. Dev. Biol. 276:158-71 (Pubitemid 39456433)
83. Imbeaud S, Carre-Eusebe D, Rey R, Belville C, Josso N, Picard JY. 1994. Molecular genetics of the persistent Müllerian duct syndrome: a study of 19 families. Hum. Mol. Genet. 3:125-31
84. Imbeaud S, Belville C, Messika-Zeitoun L, Rey R, di Clemente N, et al. 1996. A 27 base-pair deletion of the anti-M üllerian type II receptor gene is the most common cause of the persistent Müllerian duct syndrome. Hum. Mol. Genet. 5:1269-77 (Pubitemid 26335844)
85. Mishina Y, Rey R, Finegold MJ, Matzuk MM, Josso N, et al. 1996. Genetic analysis of the Müllerianinhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev. 10:2577-87 (Pubitemid 26357224)
86. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR. 2002. Requirement of Bmpr1a for Müllerian duct regression during male sexual development. Nat. Genet. 32:408-10 (Pubitemid 35266116)
87. Orvis GD, Jamin SP, Kwan KM, Mishina Y, Kaartinen VM, et al. 2008. Functional redundancy of TGF- βfamily type I receptors and receptor-Smads in mediating anti-M üllerian hormone-induced Müllerian duct regression in the mouse. Biol. Reprod. 78:994-1001 (Pubitemid 351749287)
88. Settle S, Marker P, Gurley K, Sinha A, Thacker A, et al. 2001. The BMPfamily member Gdf7 is required for seminal vesicle growth, branching morphogenesis, and cytodifferentiation. Dev. Biol. 234:138-50 (Pubitemid 32477030)
89. Wang H, Dey SK. 2006. Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 7:185-99 (Pubitemid 43361530)
90. Lee KY, Jeong JW, Wang J, Ma L, Martin JF, et al. 2007. Bmp2 is critical for the murine uterine decidual response. Mol. Cell. Biol. 27:5468-78 (Pubitemid 47124399)
91. Nusslein-Volhard C, Lohs-Schardin M, Sander K, Cremer C. 1980. A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila. Nature 283:474-76 (Pubitemid 10142615)
92. Burns KH, Matzuk MM. 2006. Pre-implantation embryogenesis. In The Physiology of Reproduction, ed. J Neill, pp. 261-310. San Diego, CA: Academic
93. Li L, Baibakov B, Dean J. 2008. A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev. Cell 15:416-25
94. Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, et al. 2000. Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 26:267-68
95. van der Heijden GW, Dieker JW, Derijck AA, Muller S, Berden JH, et al. 2005. Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech. Dev. 122:1008-22 (Pubitemid 41080025)
96. Burns KH, Viveiros MM, Ren Y, Wang P, DeMayo FJ, et al. 2003. Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300:633-36 (Pubitemid 36520586)
97. Philpott A, Leno GH. 1992. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell 69:759-67
98. Philpott A, Leno GH, Laskey RA. 1991. Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell 65:569-78
99. Derijck A, van derHeijden G, Giele M, Philippens M, de Boer P. 2008. DNAdouble-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum. Mol. Genet. 17:1922-37 (Pubitemid 351865841)
100. Wossidlo M, Arand J, Sebastiano V, Lepikhov K, Boiani M, et al. 2010. Dynamic link ofDNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J. 29:1877-88
101. Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, Surani MA. 2010. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329:78-82
102. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, et al. 2011. 5- Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun. 2:241
103. Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, et al. 2003. stella is a maternal effect gene required for normal early development in mice. Curr. Biol. 13:2110-17 (Pubitemid 37502529)
104. Bortvin A, Goodheart M, Liao M, Page DC. 2004. Dppa3/Pgc7/stella is a maternal factor and is not required for germ cell specification in mice. BMC Dev. Biol. 4:2
105. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, et al. 2007. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat. Cell Biol. 9:64-71 (Pubitemid 46024198)
106. Liu H, Kim JM, Aoki F. 2004. Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131:2269-80 (Pubitemid 38877636)
107. Adenot PG, Mercier Y, Renard JP, Thompson EM. 1997. Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124:4615-25 (Pubitemid 27519256)
108. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, et al. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464:927-31
109. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, et al. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463:237-40
110. Garcia-Perez JL, Morell M, Scheys JO, Kulpa DA, Morell S, et al. 2010. Epigenetic silencing of engineered L1 retrotransposition events in human embryonic carcinoma cells. Nature 466:769-73
111. Nothias JY, Miranda M, DePamphilis ML. 1996. Uncoupling of transcription and translation during zygotic gene activation in the mouse. EMBO J. 15:5715-25 (Pubitemid 26385630)
112. Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM. 2003. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33:187-91 (Pubitemid 36177072)
113. Zheng P, Dean J. 2009. Role of Filia, a maternal effect gene, in maintaining euploidy during cleavagestage mouse embryogenesis. Proc. Natl. Acad. Sci. USA 106:7473-78
114. Sasai K, Parant JM, Brandt ME, Carter J, Adams HP, et al. 2008. Targeted disruption of Aurora A causes abnormalmitotic spindle assembly, chromosomemisalignment and embryonic lethality. Oncogene 27:4122-27 (Pubitemid 351931992)
115. Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, et al. 2001. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104:829-38 (Pubitemid 32289276)
116. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X. 2007. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449:248-51 (Pubitemid 47402375)
117. Ciccone DN, Su H, Hevi S, Gay F, Lei H, et al. 2009. KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461:415-18
118. Li X, Ito M, Zhou F, Youngson N, Zuo X, et al. 2008. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev. Cell 15:547-57
119. Schultz N, Hamra FK, Garbers DL. 2003. Amultitude of genes expressed solely inmeiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc. Natl. Acad. Sci. USA 100:12201-6 (Pubitemid 37271538)
120. Hunt PA, Hassold TJ. 2002. Sex matters in meiosis. Science 296:2181-83 (Pubitemid 34680292)
121. Tiepolo L, Zuffardi O. 1976. Localization of factors controlling spermatogenesis in the nonfluorescent portion of the human Y chromosome long arm. Hum. Genet. 34:119-24
122. Foresta C, Moro E, Ferlin A. 2001. Y chromosome microdeletions and alterations of spermatogenesis. Endocr. Rev. 22:226-39 (Pubitemid 32458160)
123. Ruggiu M, Speed R, Taggart M, McKay SJ, Kilanowski F, et al. 1997. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389:73-77 (Pubitemid 27387693)
124. Kee K, Angeles VT, Flores M, Nguyen HN, Reijo Pera RA. 2009. Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 462:222-25
125. Aston KI, Carrell DT. 2009. Genome-wide study of single-nucleotide polymorphisms associated with azoospermia and severe oligozoospermia. J. Androl. 30:711-25
126. Knauff EA, Franke L, van Es MA, van den Berg LH, van der Schouw YT, et al. 2009. Genome-wide association study in premature ovarian failure patients suggests ADAMTS19 as a possible candidate gene. Hum. Reprod. 24:2372-78
127. Behringer RR, Cate RL, Froelick GJ, Palmiter RD, Brinster RL. 1990. Abnormal sexual development in transgenic mice chronically expressing Müllerian-inhibiting substance. Nature 345:167-70
128. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. 1991. Male development of chromosomally female mice transgenic for Sry. Nature 351:117-21 (Pubitemid 21896542)
129. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-80 (Pubitemid 41613494)
130. Brown CW, Houston-Hawkins DE, Woodruff TK, Matzuk MM. 2000. Insertion of Inhbb into the Inhba locus rescues the Inhba-null phenotype and reveals new activin functions. Nat. Genet. 25:453-57 (Pubitemid 32983442)
131. Yan C, Wang P, DeMayo J, DeMayo F, Elvin J, et al. 2001. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 15:854-66 (Pubitemid 32510635)
132. Edson MA, Nalam RL, Clementi C, Franco HL, Demayo FJ, et al. 2010. Granulosa cell-expressed BMPR1A and BMPR1B have unique functions in regulating fertility but act redundantly to suppress ovarian tumor development. Mol. Endocrinol. 24:1251-66
133. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, et al. 2008. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol. Cell. Biol. 28:248-57
134. Pangas SA, Li X, Robertson EJ, Matzuk MM. 2006. Premature luteinization and cumulus cell defects in ovarian-specific Smad4 knockout mice. Mol. Endocrinol. 20:1406-22 (Pubitemid 43801240)
135. Chang H, Matzuk MM. 2001. Smad5 is required for mouse primordial germ cell development. Mech. Dev. 104:61-67 (Pubitemid 32549764)
136. Ma L, Buchold GM, Greenbaum MP, Roy A, Burns KH, et al. 2009. GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline. PLoS Genet. 5:e1000635
137. Edson MA, Lin YN, Matzuk MM. 2010. Deletion of the novel oocyte-enriched gene, Gpr149, leads to increased fertility in mice. Endocrinology 151:358-68
138. Iwamori N, Zhao M, Meistrich ML, Matzuk MM. 2011. The testis-enriched histone demethylase, KDM4D, regulates methylation of histone H3 lysine 9 during spermatogenesis in the mouse but is dispensable for fertility. Biol. Reprod. 84:1225-34
139. Andreu-Vieyra CV, Chen R, Agno JE, Glaser S, Anastassiadis K, et al. 2010. MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol. 8:e1000453
140. Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. 2004. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305:1157-59 (Pubitemid 39100329)
141. Iwamori T, Lin YN, Ma L, Iwamori N, Matzuk MM. 2011. Identification and characterization ofRBM44 as a novel intercellular bridge protein. PLoS ONE 6:e17066
142. Ballow D, Meistrich ML, Matzuk M, Rajkovic A. 2006. Sohlh1 is essential for spermatogonial differentiation. Dev. Biol. 294:161-67
143. Pangas SA, Choi Y, Ballow DJ, Zhao Y, Westphal H, et al. 2006. Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc. Natl. Acad. Sci. USA 103:8090-95 (Pubitemid 43801057)
144. Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM. 2009. Tektin 3 is required for progressive sperm motility in mice. Mol. Reprod. Dev. 76:453-59
145. Greenbaum MP, Yan W, Wu MH, Lin YN, Agno JE, et al. 2006. TEX14 is essential for intercellular bridges and fertility in male mice. Proc. Natl. Acad. Sci. USA 103:4982-87
146. Lin YN, Roy A, Yan W, Burns KH, Matzuk MM. 2007. Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol. Cell. Biol. 27:6794-805 (Pubitemid 47483630)
147. Nagaraja AK, Andreu-Vieyra C, Franco HL, Ma L, Chen R, et al. 2008. Deletion of Dicer in somatic cells of the female reproductive tract causes sterility. Mol. Endocrinol. 22:2336-52
148. Nishimori K, Young LJ, Guo Q, Wang Z, Insel TR, Matzuk MM. 1996. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc. Natl. Acad. Sci. USA 93:11699-704 (Pubitemid 26347185)
149. Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT. 2000. Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 25:284-88 (Pubitemid 30437313)
150. Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M, et al. 2005. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc. Natl. Acad. Sci. USA 102:16096-101 (Pubitemid 41552873)
151. Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, et al. 2002. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol. Endocrinol. 16:1154-67 (Pubitemid 34621066)
152. Nalam RL, Andreu-Vieyra C, Braun RE, Akiyama H, Matzuk MM. 2009. Retinoblastoma protein plays multiple essential roles in the terminal differentiation of Sertoli cells. Mol. Endocrinol. 23:1900-13
153. Andreu-Vieyra C, Chen R, Matzuk MM. 2008. Conditional deletion of the retinoblastoma (Rb) gene in ovarian granulosa cells leads to premature ovarian failure. Mol. Endocrinol. 22:2141-61
154. Tashiro F, Kanai-Azuma M, Miyazaki S, Kato M, Tanaka T, et al. 2010. Maternal-effect gene Ces5/Ooep/Moep19/Floped is essential for oocyte cytoplasmic lattice formation and embryonic development at the maternal-zygotic stage transition. Genes Cells 15:813-28
155. Tomasini R, Tsuchihara K, Wilhelm M, Fujitani M, Rufini A, et al. 2008. TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes Dev. 22:2677-91
156. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, Wolgemuth DJ. 1998. Cyclin A1 is required for meiosis in the male mouse. Nat. Genet. 20(4):377-88
157. Yan W, Ma L, Burns KH, Matzuk MM. 2004. Haploinsufficiency of kelch-like protein homolog 10 causes infertility in male mice. Proc. Natl. Acad. Sci. USA 101(20):7793-98 (Pubitemid 38658107)
158. Yan W, Ma L, Pangas SA, Burns KH, Bai Y, et al. 2005. Mice deficient in oocyte-specific oligoadenylate synthase-like protein OAS1D display reduced fertility. Mol. Cell. Biol. 25(11):4615-24 (Pubitemid 40705765)
159. Yan W, Assadi AH, Wynshaw-Boris A, Eichele G, Matzuk MM, Clark GD. 2003. Previously uncharacterized roles of platelet-activating factor acetylhydrolase 1b complex in mouse spermatogenesis. Proc. Natl. Acad. Sci. USA 100(12):7189-94 (Pubitemid 36706414)
160. Koizumi H, Yamaguchi N, Hattori M, Ishikawa TO, Aoki J, et al. 2003. Targeted disruption of intracellular type I platelet activating factor-acetylhydrolase catalytic subunits causes severe impairment in spermatogenesis. J. Biol. Chem. 278(14):12489-94 (Pubitemid 36800237)
161. Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM. 2007. Absence of tektin 4 causes asthenozoospermia and subfertility in male mice. FASEB J. 21(4):1013-25 (Pubitemid 46495691)
162. Yang J, Medvedev S, Yu J, Tang LC, Agno JE, et al. 2005. Absence of the DNA-/RNA-binding protein MSY2 results in male and female infertility. Proc. Natl. Acad. Sci. USA 102(16):5755-60 (Pubitemid 40559632)
163. Kumar TR, Wiseman AL, Kala G, Kala SV, Matzuk MM, LiebermanMW. 2000. Reproductive defects in β-glutamyl transpeptidase-deficient mice. Endocrinology 141(11):4270-77
164. Ma X, Dong Y, Matzuk MM, Kumar TR. 2004. Targeted disruption of luteinizing hormone β-subunit leads to hypogonadism, defects in gonadal steroidogenesis and infertility. Proc. Natl. Acad. Sci. USA 101(49):17294-99 (Pubitemid 39627813)
165. Yu RN, Ito M, Saunders TL, Camper SA, Jameson J. 1998. Role of Ahch in gonadal development and gametogenesis. Nat. Genet. 20(4):353-57 (Pubitemid 28541632)
166. Matzuk MM, Dionne L, Guo Q, Kumar TR, Lebovitz RM. 1998. Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology 139:4008-11 (Pubitemid 28512286)
167. Ho Y-S, Gargano M, Cao J, Bronson RT, Heimler I, Hutz RJ. 1998. Reduced fertility in female mice lacking copper-zinc superoxide dismutase. J. Biol. Chem. 273(13):7765-69 (Pubitemid 28152809)
168. Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson T. 2006. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 20(13):1744-54 (Pubitemid 43992883)
169. Kaneda M, Hirasawa R, Chiba H, Okano M, Li E, Sasaki H. 2010. Genetic evidence for Dnmt3adependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells 15(3):169-79
170. Hata K, Okano M, Lei H, Li E. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129(8):1983-93 (Pubitemid 34874213)
171. Narducci MG, Fiorenza MT, Kang SM, Bevilacqua A, Di Giacomo M, et al. 2002. TCL1 participates in early embryonic development and is overexpressed in human seminomas. Proc. Natl. Acad. Sci. USA 99(18):11712-17 (Pubitemid 34994464)