WEE2 is an oocyte-specific meiosis inhibitor in rhesus macaque monkeys

Biology of Reproduction

Volumn 82, Issue 6, 2010, Pages 1190-1197

  Hanna, Carol B ^a   Yao, Shan ^a   Patta, Maristela C ^a   Jensen, Jeffrey T ^a,b   Wu, Xuemei ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Gamete biology; Meiosis; Meiotic resumption; Oocyte; Oocyte development; Ovary; Rhesus macaques; WEE family; WEE2 (WEE1B)

Indexed keywords

DOUBLE STRANDED RNA; GREEN FLUORESCENT PROTEIN; PHOSPHODIESTERASE III INHIBITOR; PROTEIN KINASE; UNCLASSIFIED DRUG; WEE2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GERMINAL VESICLE; MEIOSIS; NONHUMAN; OOCYTE; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RHESUS MONKEY; TESTIS;

ANIMALS; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 3; DOWN-REGULATION; FEMALE; MACACA MULATTA; MALE; MEIOSIS; MICE; OOCYTES; PROTEIN-TYROSINE KINASES; TESTIS;

MACACA MULATTA; MUS; PRIMATES;

EID: 77953836702     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.081984     Document Type: Article

References (44)

1. Amsterdam A, Koch Y, Lieberman ME, Lindner HR. Distribution of binding sites for human chorionic gonadotropin in the preovulatory follicle of the rat. J Cell Biol 1975; 67:894-900.
2. Dekel N. Cellular, biochemical and molecular mechanisms regulating oocyte maturation. Mol Cell Endocrinol 2005; 234:19-25.
3. Morgan DO. Principles of CDK regulation. Nature 1995; 374:131-134.
4. Chesnel F, Eppig JJ. Synthesis and accumulation of p34cdc2 and cyclin B in mouse oocytes during acquisition of competence to resume meiosis. Mol Reprod Dev 1995; 40:503-508.
5. Cho WK, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool 1974; 187:383-386.
6. Masciarelli S, Horner K, Liu C, Park SH, Hinckley M, Hockman S, Nedachi T, Jin C, Conti M, Manganiello V. Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest 2004; 114:196-205.
7. Vaccari S, Horner K, Mehlmann LM, Conti M. Generation of mouse oocytes defective in cAMP synthesis and degradation: endogenous cyclic AMP is essential for meiotic arrest. Dev Biol 2008; 316:124-134.
8. Pirino G, Wescott MP, Donovan PJ. Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle 2009; 8:665-670.
9. Zhang Y, Zhang Z, Xu XY, Li XS, Yu M, Yu AM, Zong ZH, Yu BZ. Protein kinase A modulates Cdc25B activity during meiotic resumption of mouse oocytes. Dev Dyn 2008; 237:3777-3786.
10. Kimura N, Hoshino Y, Totsukawa K, Sato E. Cellular and molecular events during oocyte maturation in mammals: molecules of cumulusoocyte complex matrix and signalling pathways regulating meiotic progression. Soc Reprod Fertil Suppl 2007; 63:327-342.
11. Kovo M, Kandli-Cohen M, Ben-Haim M, Galiani D, Carr DW, Dekel N. An active protein kinase A (PKA) is involved in meiotic arrest of rat growing oocytes. Reproduction 2006; 132:33-43.
12. Dekel N. Protein phosphorylation/dephosphorylation in the meiotic cell cycle of mammalian oocytes. Rev Reprod 1996; 1:82-88. (Pubitemid 126664710)
13. Okamoto K, Sagata N. Mechanism for inactivation of the mitotic inhibitory kinase Wee1 at M phase. Proc Natl Acad Sci U S A 2007; 104:3753-3758.
14. Burrows AE, Sceurman BK, Kosinski ME, Richie CT, Sadler PL, Schumacher JM, Golden A. The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 2006; 133:697-709.
15. Han SJ, Conti M. New pathways from PKA to the Cdc2/cyclin B complex in oocytes: Wee1B as a potential PKA substrate. Cell Cycle 2006; 5:227-231.
16. Okamoto K, Nakajo N, Sagata N. The existence of two distinct Wee1 isoforms in Xenopus: implications for the developmental regulation of the cell cycle. EMBO J 2002; 21:2472-2484.
17. Booher RN, Holman PS, Fattaey A. Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity. J Biol Chem 1997; 272: 22300-22306.
18. Parker LL, Piwnica-Worms H. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 1992; 257:1955-1957.
19. Lincoln AJ, Wickramasinghe D, Stein P, Schultz RM, Palko ME, De Miguel MP, Tessarollo L, Donovan PJ. Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet 2002; 30: 446-449.
20. Mueller PR, Leise WF III.. Measurement of Wee kinase activity. Methods Mol Biol 2005; 296:299-328.
21. Nakanishi M, Ando H, Watanabe N, Kitamura K, Ito K, Okayama H, Miyamoto T, Agui T, Sasaki M. Identification and characterization of human Wee1B, a new member of the Wee1 family of Cdk-inhibitory kinases. Genes Cells 2000; 5:839-847.
22. Han SJ, Chen R, Paronetto MP, Conti M. Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr Biol 2005; 15:1670-1676.
23. Lanzendorf SE, Zelinski-Wooten MB, Stouffer RL, Wolf DP. Maturity at collection and the developmental potential of rhesus monkey oocytes. Biol Reprod 1990; 42:703-711.
24. Alak BM, Wolf DP. Rhesus monkey oocyte maturation and fertilization in vitro: roles of the menstrual cycle phase and of exogenous gonadotropins. Biol Reprod 1994; 51:879-887.
25. Macklon NS, Stouffer RL, Giudice LC, Fauser BC. The science behind 25 years of ovarian stimulation for in vitro fertilization. Endocr Rev 2006; 27: 170-207.
26. Schramm RD, Paprocki AM, VandeVoort CA. Causes of developmental failure of in vitro matured rhesus monkey oocytes: impairments in embryonic genome activation. Hum Reprod 2003; 18:826-833.
27. Stouffer RL, Zelinski-Wooten MB. Overriding follicle selection in controlled ovarian stimulation protocols: quality vs. quantity. Reprod Biol Endocrinol 2004; 2:32.
28. Zheng P, Patel B, McMenamin M, Moran E, Paprocki AM, Kihara M, Schramm RD, Latham KE. Effects of follicle size and oocyte maturation conditions on maternal messenger RNA regulation and gene expression in rhesus monkey oocytes and embryos. Biol Reprod 2005; 72:890-897.
29. Jensen JT, Zelinski-Wooten MB, Schwinof KM, Vance JE, Stouffer RL. The phosphodiesterase 3 inhibitor ORG 9935 inhibits oocyte maturation during gonadotropin-stimulated ovarian cycles in rhesus macaques. Contraception 2005; 71:68-73.
30. Boatman DE, Bavister BD. Stimulation of rhesus monkey sperm capacitation by cyclic nucleotide mediators. J Reprod Fertil 1984; 71: 357-366.
31. Wolf DP. Assisted reproductive technologies in rhesus macaques. Reprod Biol Endocrinol 2004; 2:37.
32. Wolf DP, Thormahlen S, Ramsey C, Yeoman RR, Fanton J, Mitalipov S. Use of assisted reproductive technologies in the propagation of rhesus macaque offspring. Biol Reprod 2004; 71:486-493.
33. Wu X, Chen L, Brown CA, Yan C, Matzuk MM. Interrelationship of growth differentiation factor 9 and inhibin in early folliculogenesis and ovarian tumorigenesis in mice. Mol Endocrinol 2004; 18:1509-1519.
34. 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 2003; 33:187-191.
35. Homer HA, McDougall A, Levasseur M, Murdoch AP, Herbert M. RNA interference in meiosis I human oocytes: towards an understanding of human aneuploidy. Mol Hum Reprod 2005; 11:397-404.
36. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 1988; 332:459-461.
37. Zheng P, Patel B, McMenamin M, Paprocki AM, Schramm RD, Nagl NG Jr, Wilsker D, Wang X, Moran E, Latham KE. Expression of genes encoding chromatin regulatory factors in developing rhesus monkey oocytes and preimplantation stage embryos: possible roles in genome activation. Biol Reprod 2004; 70:1419-1427.
38. Wu X. Maternal depletion of NLRP5 blocks early embryogenesis in rhesus macaque monkeys (Macaca mulatta). Hum Reprod 2009; 24:415-424.
39. Paradis F, Vigneault C, Robert C, Sirard MA. RNA interference as a tool to study gene function in bovine oocytes. Mol Reprod Dev 2005; 70:111-121.
40. Svoboda P. Long dsRNA and silent genes strike back:RNAi in mouse oocytes and early embryos. Cytogenet Genome Res 2004; 105:422-434.
41. Stein P, Zeng F, Pan H, Schultz RM. Absence of non-specific effects of RNA interference triggered by long double-stranded RNA in mouse oocytes. Dev Biol 2005; 286:464-471.
42. Nishimura T, Shimaoka T, Kano K, Naito K. Insufficient amount of Cdc2 and continuous activation of Wee1 B are the cause of meiotic failure in porcine growing oocytes. J Reprod Dev 2009; 55:553-557.
43. Shimaoka T, Nishimura T, Kano K, Naito K. Critical effect of pigWee1B on the regulation of meiotic resumption in porcine immature oocytes. Cell Cycle 2009; 8:2375-2384.
44. Oh JS, Han SJ, Conti M. Wee1B, Myt1, and Cdc25 function in distinct compartments of the mouse oocyte to control meiotic resumption. J Cell Biol 2010; 188:199-207.