Proteasomal activity is required to initiate and to sustain translational activation of messenger RNA encoding the stem-loop-binding protein during meiotic maturation in mice

Biology of Reproduction

Volumn 82, Issue 1, 2010, Pages 123-131

  Yang, Qin ^a   Allard, Patrick ^a,b   Huang, Michael ^a   Zhang, Wenling ^a,c   Clarke, Hugh J ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c The Toronto Institute for Reproductive Medicine   (Canada)

Author keywords

3 untranslated region; Gamete biology; Gametogenesis; Gene regulation; Meiotic maturation; Oocyte development; Oogenesis; Ovum; Proteasome; Protein degradation; Stem loop binding protein; Translational control

Indexed keywords

BINDING PROTEIN; CYTOPLASMIC POLYADENYLATION ELEMENT BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; POLYADENYLIC ACID; PROTEASOME; STEM LOOP BINDING PROTEIN; UNCLASSIFIED DRUG; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; CPEB1 PROTEIN, MOUSE; NUCLEAR PROTEIN; SLBP PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; FEMALE; INHIBITION KINETICS; MEIOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OOCYTE DEVELOPMENT; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA TRANSLATION; ANIMAL; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS;

MUS;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEIOSIS; MICE; MOLECULAR SEQUENCE DATA; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; NUCLEAR PROTEINS; OOCYTES; OOGENESIS; POLY A; POLYADENYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 77950346702     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.076588     Document Type: Article

References (50)

1. Kashiwabara S-i, Nakanishi T, Kimura M, Baba T. Non-canonical poly(A) polymerase in mammalian gametogenesis. Biochim Biophys Acta 2008; 1779:230-238.
2. Radford HE, Meijer HA, de Moor CH. Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim Biophys Acta 2008; 1779:217-229.
3. Mendez R, Richter JD. Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2001; 2:521-529.
4. Wickens M, Bernstein DS, Kimble J, Parker R. A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet 2002; 18:150-157.
5. De La Fuente R. Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes. Dev Biol 2006; 292:1-12.
6. Latham KE. Mechanisms and control of embryonic genome activation in mammalian embryos. Int Rev Cytol 1999; 193:71-124.
7. Dai Y, Newman B, Moor R. Translational regulation of MOS messenger RNA in pig oocytes. Biol Reprod 2005; 73:997-1003.
8. Gebauer F, Xu WH, Cooper GM, Richter JD. Translational control by cytoplasmic polyadenylation of c-Mos mRNA is necessary for oocyte maturation in the mouse. EMBO J 1994; 13:5712-5720.
9. Tay J, Hodgman R, Richter JD. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol 2000; 221:1-9.
10. Huarte J, Stutz A, Oconnell ML, Gubler P, Belin D, Darrow AL, Strickland S, Vassalli JD. Transient translational silencing by reversible mRNA deadenylation. Cell 1992; 69:1021-1030.
11. Vassalli JD, Huarte J, Belin D, Gubler P, Vassalli A, O'Connell ML, Parton LA, Rickles RJ, Strickland S. Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev 1989; 3:2163-2171.
12. Belloc E, Mendez R. A deadenylation negative feedback mechanism governs meiotic metaphase arrest Nature 2008; 452:1017-1021.
13. Wang YY, Charlesworth A, Byrd SM, Gregerson R, MacNicol MC, MacNicol AM. A novel mRNA 3′ untranslated region translational control sequence regulates Xenopus Wee1 mRNA translation. Dev Biol 2008; 317:454-466.
14. de Moor CH, Meijer H, Lissenden S. Mechanisms of translational control by the 3′ UTR in development and differentiation. Sem Cell Dev Biol 2005; 16:49-58.
15. Richter JD. CPEB: a life in translation. Trends Biochem Sci 2007; 32: 279-285.
16. Richter JD. Breaking the code of polyadenylation-induced translation. Cell 2008; 132:335-337.
17. Kim JH, Richter JD. Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol Cell 2006; 24:173-183.
18. Barkoff AF, Dickson KS, Gray NK, Wickens M. Translational control of cyclin B1 mRNA during meiotic maturation: coordinated repression and cytoplasmic polyadenylation. Dev Biol 2000; 220:97-109.
19. de Moor CH, Richter JD. Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J 1999; 18:2294-2303.
20. Stutz A, Conne B, Huarte J, Gubler P, Volkel V, Flandin P, Vassalli J-D. Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes. Genes Dev 1998; 12:2535-2548.
21. Hampl A, Eppig JJ. Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes. Development 1995; 121:925-933.
22. Huarte J, Belin D, Vassalli A, Strickland S, Vassalli JD. Meiotic maturation of mouse oocytes triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA. Genes Dev 1987; 1: 1201-1211.
23. Paules RS, Buccione R, Moschel RC, Vande Woude GF, Eppig JJ. Mouse Mos protooncogene product is present and functions during oogenesis. Proc Natl Acad Sci U S A 1989; 86:5395-5399.
24. Ledan E, Polanski Z, Terret M-E, Maro B. Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. Dev Biol 2001; 232:400-413.
25. Colledge WH, Carlton MBL, Udy GB, Evans MJ. Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature 1994; 370:65-68.
26. Hashimoto N, Watanabe N, Furuta Y, Tamemoto H, Sagata N, Yokoyama M, Okazaki K, Nagayoshi M, Takedat N, Ikawatll Y, Aizawai S. Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 1994; 370:68-71.
27. Inoue D, Ohe M, Kanemori Y, Nobui T, Sagata N. A direct link of the Mos-MAPK pathway to Erp1/Emi2 in meiotic arrest of Xenopus laevis eggs. Nature 2007; 446:1100-1104.
28. Marzluff WF. Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts. Curr Opin Cell Biol 2005; 17:274-280.
29. Wang ZF, Ingledue TC, Dominski Z, Sanchez R, Marzluff WF. Two Xenopus proteins that bind the 3′ end of histone mRNA: implications for translational control of histone synthesis during oogenesis. Mol Cell Biol 1999; 19:835-345.
30. Allard P, Champigny MJ, Skoggard S, Erkmann JA, Whitfield ML, Marzluff WF, Clarke HJ. Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo. J Cell Sci 2002; 115:4577-4586.
31. Robertson AJ, Howard JT, Dominski Z, Schnackenberg BJ, Sumerel JL, McCarthy JJ, Coffman JA, Marzluff WF. The sea urchin stem-loop-binding protein: a maternally expressed protein that probably functions in expression of multiple classes of histone mRNA. Nucleic Acids Res 2004; 32:811-818.
32. Lanzotti DJ, Kaygun H, Yang X, Duronio RJ, Marzluff WF. Developmental control of histone mRNA and dSLBP synthesis during Drosophila embryogenesis and the role of dSLBP in histone mRNA 3′ end processing in vivo. Mol Cell Biol 2002; 22:2267-2282.
33. Arnold DR, Francon P, Zhang J, Martin K, Clarke HJ. Stem-loop binding protein expressed in growing oocytes is required for accumulation of mRNAs encoding histones H3 and H4 and for early embryonic development in the mouse. Dev Biol 2008; 313:347-358.
34. Allard P, Yang Q, Marzluff WF, Clarke HJ. The stem-loop binding protein regulates translation of histone mRNA during mammalian oogenesis. Dev Biol 2005; 286:195-206.
35. Clarke HJ, Oblin C, Bustin M. Developmental regulation of chromatin composition during mouse embryogenesis: somatic histone H1 is first detectable at the 4-cell stage. Development 1992; 115:791-799.
36. Whitfield ML, Zheng LX, Baldwin A, Ohta T, Hurt MM, Marzluff WF. Stem-loop binding protein, the protein that binds the 3′ end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol Cell Biol 2000; 20:4188-4198.
37. Koseoglu MM, Graves LM, Marzluff WF. Phosphorylation of threonine 61 by cyclin A/cdk1 triggers degradation of stem-loop binding protein at the end of S phase. Mol Cell Biol 2008; 28:4469-4479.
38. Zheng LX, Dominski Z, Yang XC, Elms P, Raska CS, Borchers CH, Marzluff WF. Phosphorylation of stem-loop binding protein (SLBP) on two threonines triggers degradation of SLBP, the sole cell cycle-regulated factor required for regulation of histone mRNA processing, at the end of S phase. Mol Cell Biol 2003; 23:1590-1601.
39. Oh B, Hwang SY, McLaughlin J, Solter D, Knowles BB. Timely translation during the mouse oocyte-to-embryo transition. Development 2000; 127:3795-3803.
40. Stutz A, Conne B, Huarte J, Gubler P, Volkel V, Flandin P, Vassalli JD. Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes. Genes Dev 1998; 12:2535-2548.
41. Prasad CK, Mahadevan M, MacNicol MC, MacNicol AM. Mos 3prime UTR regulatory differences underlie species-specific temporal patterns of Mos mRNA cytoplasmic polyadenylation and translational recruitment during oocyte maturation. Mol Reprod Dev 2008; 75:1258-1268.
42. Nakanishi T, Kubota H, Ishibashi N, Kumagai S, Watanabe H, Yamashita M, Kashiwabara S-i, Miyado K, Baba T. Possible role of mouse poly(A) polymerase mGLD-2 during oocyte maturation. Dev Biol 2006; 289:115-126.
43. Mendez R, Barnard D, Richter JD. Differential mNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J 2002; 21:1833-1844.
44. Reverte CG, Ahearn MD, Hake LE. CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. Dev Biol 2001; 231:447-458.
45. Uzbekova S, Arlot-Bonnemains Y, Dupont J, Dalbies-Tran R, Papillier P, Pennetier S, Thelie A, Perreau C, Mermillod P, Prigent C, Uzbekov R. Spatio-temporal expression patterns of aurora kinases A, B, and C and cytoplasmic polyadenylation-element-binding protein in bovine oocytes during meiotic maturation. Biol Reprod 2008; 78:218-233.
46. Racki WJ, Richter JD. CPEB controls oocyte growth and follicle development in the mouse. Development 2006; 133:4527-4537.
47. Pique M, Lopez JM, Foissac S, Guigo R, Mendez R. A combinatorial code for CPE-mediated translational control. Cell 2008; 132:434-448.
48. Lu J-Y, Bergman N, Sadri N, Schneider RJ. Assembly of AUF1 with eIF4G-poly(A) binding protein complex suggests a translation function in AU-rich mRNA decay. RNA 2006; 12:883-893.
49. Zheng D, Ezzeddine N, Chen C-YA, Zhu W, He X, Shyu A-B. Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells. J Cell Biol 2008; 182:89-101.
50. Funakoshi Y, Doi Y, Hosoda N, Uchida N, Osawa M, Shimada I, Tsujimoto M, Suzuki T, Katada T, Hoshino S-i. Mechanism of mRNA deadenylation: evidence for a molecular interplay between translation termination factor eRF3 and mRNA deadenylases. Genes Dev 2007; 21: 3135-3148.