Oocyte-Specific Genes Affect Folliculogenesis, Fertilization, and Early Development

Ping Zheng; Jurrien Dean

doi:10.1055/s-2007-980218

Seminars in Reproductive Medicine, Table of Contents

Semin Reprod Med 2007; 25(4): 243-251
DOI: 10.1055/s-2007-980218

Published in 2007 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.

Oocyte-Specific Genes Affect Folliculogenesis, Fertilization, and Early Development

Ping Zheng¹ , Jurrien Dean¹

¹Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health, Bethesda, Maryland

Abstract

ABSTRACT

Although cell-autonomous genetic programs pursued by germ and somatic cells are of critical import, intimate interplays between the two cell types are also essential for normal development of the female gonad. Recent studies demonstrate that oocytes play active roles in coordinating the growth and differentiation of somatic cells during folliculogenesis and affect successful outcomes at fertilization and early development. Mouse transgenesis has been particularly useful in defining germ-cell specific genes and their roles in folliculogenesis (e.g., Dazla, Figla, Nobox, Sohlh1, Ybx2, Cpeb1, Gdf9), fertilization (e.g., Zp1, Zp2, Zp3), and preimplantation embryonic development (e.g., Npm2, Zar1, Nalp5, Dppa3). Continued identification of novel oocyte-specific genes and the annotation of their functions will provide additional insight into the genetic pathways regulating ovarian development. The knowledge gained from mouse models will no doubt benefit the understanding of human biology and treatment of reproductive failure.

KEYWORDS

Oocyte-specific genes - folliculogenesis - fertilization - preimplantation embryonic development

Full Text

References

REFERENCES

1 Koubova J, Menke D B, Zhou Q et al.. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc Natl Acad Sci USA. 2006; 103 2474-2479
2 Bowles J, Knight D, Smith C et al.. Retinoid signaling determines germ cell fate in mice. Science. 2006; 312 596-600
3 McLaren A, Southee D. Entry of mouse embryonic germ cells into meiosis. Dev Biol. 1997; 187 107-113
4 Hunt P A, Hassold T J. Sex matters in meiosis. Science. 2002; 296 2181-2183
5 Morelli M A, Cohen P E. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction. 2005; 130 761-781
6 Brambell F WR. The development and morphology of the gonads of the mouse. Part III. The growth of the follicles. Proc R Soc Lond (Biol). 1928; 103 258-272
7 Pepling M E, Spradling A C. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol. 2001; 234 339-351
8 Hirshfield A N. Development of follicles in the mammalian ovary. Int Rev Cytol. 1991; 124 43-101
9 Zuckerman S, Baker T G. The development of the ovary and the process of oogenesis. In; Zuckerman S, Weir BJ The Ovary. New York; Academic Press 1977: 41-63
10 Zamboni L, Upadhyay S. Germ cell differentiation in mouse adrenal glands. J Exp Zool. 1983; 228 173-193
11 Soyal S M, Amleh A, Dean J. FIGα, a germ-cell specific transcription factor required for ovarian follicle formation. Development. 2000; 127 4645-4654
12 Ruggiu M, Speed R, Taggart M et al.. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature. 1997; 389 73-77
13 Pangas S A, Choi Y, Ballow D J et al.. Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. Proc Natl Acad Sci USA. 2006; 103 8090-8095
14 Rajkovic A, Pangas S A, Ballow D et al.. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science. 2004; 305 1157-1159
15 Yang J, Medvedev S, Yu J et al.. Absence of the DNA-/RNA-binding protein MSY2 results in male and female infertility. Proc Natl Acad Sci USA. 2005; 102 5755-5760
16 Tay J, Richter J D. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Dev Cell. 2001; 1 201-213
17 Dong J, Albertini D F, Nishimori K et al.. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996; 383 531-535
18 Liang L, Soyal S M, Dean J. FIGα, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development. 1997; 124 4939-4949
19 Millar S E, Lader E S, Dean J. ZAP-1 DNA binding activity is first detected at the onset of zona pellucida gene expression in embryonic mouse oocytes. Dev Biol. 1993; 158 410-413
20 Ballow D, Meistrich M L, Matzuk M et al.. Sohlh1 is essential for spermatogonial differentiation. Dev Biol. 2006; 294 161-167
21 Ballow D J, Xin Y, Choi Y et al.. Sohlh2 is a germ cell-specific bHLH transcription factor. Gene Expr Patterns. 2006; 6 1014-1018
22 Zhao Y, Marin O, Hermesz E et al.. The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc Natl Acad Sci USA. 2003; 100 9005-9010
23 Mori T, Yuxing Z, Takaki H et al.. The LIM homeobox gene, L3/Lhx8, is necessary for proper development of basal forebrain cholinergic neurons. Eur J Neurosci. 2004; 19 3129-3141
24 Reijo R, Lee T Y, Salo P et al.. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nat Genet. 1995; 10 383-393
25 Cooke H J, Lee M, Kerr S et al.. A murine homologue of the human DAZ gene is autosomal and expressed only in male and female gonads. Hum Mol Genet. 1996; 5 513-516
26 Lin Y, Page D C. Dazl deficiency leads to embryonic arrest of germ cell development in XY C57BL/6 mice. Dev Biol. 2005; 288 309-316
27 Collier B, Gorgoni B, Loveridge C et al.. The DAZL family proteins are PABP-binding proteins that regulate translation in germ cells. EMBO J. 2005; 24 2656-2666
28 Padmanabhan K, Richter J D. Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev. 2006; 20 199-209
29 Yu J, Hecht N B, Schultz R M. Expression of MSY2 in mouse oocytes and preimplantation embryos. Biol Reprod. 2001; 65 1260-1270
30 Racki W J, Richter J D. CPEB controls oocyte growth and follicle development in the mouse. Development. 2006; 133 4527-4537
31 Vasudevan S, Seli E, Steitz J A. Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades. Genes Dev. 2006; 20 138-146
32 Matzuk M M, Burns K H, Viveiros M M et al.. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science. 2002; 296 2178-2180
33 Nilsson E, Parrott J A, Skinner M K. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol. 2001; 175 123-130
34 Nilsson E E, Skinner M K. Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Mol Cell Endocrinol. 2004; 214 19-25
35 Thomas F H, Vanderhyden B C. Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod Biol Endocrinol. 2006; 4 4-9
36 Yan C, Wang P, DeMayo J et al.. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol. 2001; 15 854-866
37 Elvin J A, Yan C, Wang P et al.. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol. 1999; 13 1018-1034
38 Dube J L, Wang P, Elvin J et al.. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol. 1998; 12 1809-1817
39 Laitinen M, Vuojolainen K, Jaatinen R et al.. A novel growth differentiation factor-9 (GDF-9) related factor is co- expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech Dev. 1998; 78 135-140
40 Yoshino O, McMahon H E, Sharma S et al.. A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proc Natl Acad Sci USA. 2006; 103 10678-10683
41 Familiari G, Relucenti M, Heyn R et al.. Three-dimensional structure of the zona pellucida at ovulation. Microsc Res Tech. 2006; 69 415-426
42 Bleil J D, Wassarman P M. Synthesis of zona pellucida proteins by denuded and follicle-enclosed mouse oocytes during culture in vitro. Proc Natl Acad Sci USA. 1980; 77 1029-1033
43 Bleil J D, Wassarman P M. Structure and function of the zona pellucida: Identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev Biol. 1980; 76 185-202
44 Phillips D M, Shalgi R. Surface architecture of the mouse and hamster zona pellucida and oocyte. J Ultrastruct Res. 1980; 72 1-12
45 Storey B T, Lee M A, Muller C et al.. Binding of mouse spermatozoa to the zonae pellucidae of mouse eggs in cumulus: evidence that the acrosomes remain substantially intact. Biol Reprod. 1984; 31 1119-1128
46 Cherr G N, Lambert H, Meizel S et al.. In vitro studies of the golden hamster sperm acrosome reaction: completion on the zona pellucida and induction by homologous soluble zonae pellucidae. Dev Biol. 1986; 114 119-131
47 Ward C R, Storey B T. Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev Biol. 1984; 104 287-296
48 Jungnickel M K, Marrero H, Birnbaumer L et al.. Trp2 regulates entry of Ca2 + into mouse sperm triggered by egg ZP3. Nat Cell Biol. 2001; 3 499-502
49 Herrick S B, Schweissinger D L, Kim S W et al.. The acrosomal vesicle of mouse sperm is a calcium store. J Cell Physiol. 2005; 202 663-671
50 Baibakov B, Gauthier L, Talbot P et al.. Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis. Development. 2007; 134 433-443
51 Bork P, Sander C. A large domain common to sperm receptors (Zp2 and Zp3) and TGF- beta type III receptor. FEBS Lett. 1992; 300 237-240
52 Jovine L, Qi H, Williams Z et al.. The ZP domain is a conserved module for polymerization of extracellular proteins. Nat Cell Biol. 2002; 4 457-461
53 Boja E S, Hoodbhoy T, Fales H M et al.. Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J Biol Chem. 2003; 278 34189-34202
54 Rankin T, Talbot P, Lee E et al.. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development. 1999; 126 3847-3855
55 Rankin T L, O'Brien M, Lee E et al.. Defective zonae pellucidae in Zp2 null mice disrupt folliculogenesis, fertility and development. Development. 2001; 128 1119-1126
56 Rankin T, Familari M, Lee E et al.. Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development. 1996; 122 2903-2910
57 Liu C, Litscher E S, Mortillo S et al.. Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice. Proc Natl Acad Sci USA. 1996; 93 5431-5436
58 Rankin T L, Tong Z-B, Castle P E et al.. Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development. 1998; 125 2415-2424
59 Rankin T L, Coleman J S, Epifano O et al.. Fertility and taxon-specific sperm binding persist after replacement of mouse ‘sperm receptors' with human homologues. Dev Cell. 2003; 5 33-43
60 Florman H M, Wassarman P M. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell. 1985; 41 313-324
61 Leyton L, Saling P. Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction. J Cell Biol. 1989; 108 2163-2168
62 Miller D J, Macek M B, Shur B D. Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature. 1992; 357 589-593
63 Miller D J, Gong X, Decker G et al.. Egg cortical granule N-acetylglucosaminidase is required for the mouse zona block to polyspermy. J Cell Biol. 1993; 123 1431-1440
64 Thall A D, Maly P, Lowe J B. Oocyte gal alpha 1,3gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse. J Biol Chem. 1995; 270 21437-21440
65 Lu Q, Shur B D. Sperm from β1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. Development. 1997; 124 4121-4131
66 Liu C, Litscher S, Wassarman P M. Transgenic mice with reduced numbers of functional sperm receptors on their eggs reproduce normally. Mol Biol Cell. 1995; 6 577-585
67 Liu D Y, Baker H W, Pearse M J et al.. Normal sperm-zona pellucida interaction and fertilization in vitro in alpha-1,3-galactosyltransferase gene knockout mice. Mol Hum Reprod. 1997; 3 1015-1016
68 Asano M, Furukawa K, Kido M et al.. Growth retardation and early death of beta-1,4-galactosyltransferase knockout mice with augmented proliferation and abnormal differentiation of epithelial cells. EMBO J. 1997; 16 1850-1857
69 Bleil J D, Beall C F, Wassarman P M. Mammalian sperm-egg interaction: fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2. Dev Biol. 1981; 86 189-197
70 Bauskin A R, Franken D R, Eberspaecher U et al.. Characterization of human zona pellucida glycoproteins. Mol Hum Reprod. 1999; 5 534-540
71 Dean J. Reassessing the molecular biology of sperm-egg recognition with mouse genetics. Bioessays. 2004; 26 29-38
72 Hoodbhoy T, Dean J. Insights into the molecular basis of sperm-egg recognition in mammals. Reproduction. 2004; 127 417-422
73 Wassarman P M, Jovine L, Qi H et al.. Recent aspects of mammalian fertilization research. Mol Cell Endocrinol. 2005; 234 95-103
74 Shur B D, Rodeheffer C, Ensslin M A et al.. Identification of novel gamete receptors that mediate sperm adhesion to the egg coat. Mol Cell Endocrinol. 2006; 250 137-148
75 Nakanishi T, Ikawa M, Yamada S et al.. Real-time observation of acrosomal dispersal from mouse sperm using GFP as a marker protein. FEBS Lett. 1999; 449 277-283
76 Christians E, Davis A A, Thomas S D et al.. Maternal effect of hsf1 on reproductive success. Nature. 2000; 407 693-694
77 Wu X, Viveiros M M, Eppig J J et al.. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet. 2003; 33 187-191
78 Burns K H, Viveiros M M, Ren Y et al.. Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science. 2003; 300 633-636
79 Payer B, Saitou M, Barton S C et al.. Stella is a maternal effect gene required for normal early development in mice. Curr Biol. 2003; 13 2110-2117
80 Bortvin A, Goodheart M, Liao M et al.. Dppa3/Pgc7/stella is a maternal factor and is not required for germ cell specification in mice. BMC Dev Biol. 2004; 4 2
81 Oh B, Hwang S Y, Solter D et al.. Spindlin, a major maternal transcript expressed in the mouse during the transition from oocyte to embryo. Development. 1997; 124 493-503
82 Bultman S J, Gebuhr T C, Pan H et al.. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 2006; 20 1744-1754
83 Ma J, Zeng F, Schultz R M et al.. Basonuclin: a novel mammalian maternal-effect gene. Development. 2006; 133 2053-2062
84 Tong Z B, Gold L, Pfeifer K E et al.. Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet. 2000; 26 267-268
85 Howell C Y, Bestor T H, Ding F et al.. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell. 2001; 104 829-838
86 Wu X, Wang P, Brown C A et al.. Zygote arrest 1 (Zar1) is an evolutionarily conserved gene expressed in vertebrate ovaries. Biol Reprod. 2003; 69 861-867
87 Philpott A, Leno G H, Laskey R A. Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell. 1991; 65 569-578
88 Philpott A, Leno G H. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell. 1992; 69 759-767
89 Tschopp J, Martinon F, Burns K. NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol. 2003; 4 95-104
90 Saitou M, Barton S C, Surani M A. A molecular programme for the specification of germ cell fate in mice. Nature. 2002; 418 293-300

Dr. Ping Zheng

Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Disease

National Institutes of Health, 50 South Drive, Bethesda, MD 20892

Email: zhengp@niddk.nih.gov