Maternally recruited DCP1A and DCP2 contribute to messenger RNA degradation during oocyte maturation and genome activation in mouse

Biology of Reproduction

Volumn 88, Issue 1, 2013, Pages

  Ma, Jun ^a   Flemr, Matyas ^b   Strnad, Hynek ^b   Svoboda, Petr ^b   Schultz, Richard M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

Gamete biology; Maternal mRNA degradation; Meiotic maturation; Mrna decapping; Oocyte maturation

Indexed keywords

DCP1A PROTEIN; DCP2 PROTEIN; MESSENGER RNA; MORPHOLINO OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; GENE ACTIVATION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; OOCYTE MATURATION; OOCYTE TO ZYGOTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA DEGRADATION; RNA INTERFERENCE;

ANIMALS; BUTADIENES; ENDORIBONUCLEASES; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NITRILES; OOCYTES; PROTEIN KINASE INHIBITORS; PURINES; RNA STABILITY; RNA, MESSENGER; TRANS-ACTIVATORS;

EID: 84876337618     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.105312     Document Type: Article

References (70)

1. Coller J, Parker R. General translational repression by activators of mRNA decapping. Cell 2005; 122:875-886.
2. Tucker M, Valencia-Sanchez MA, Staples RR, Chen J, Denis CL, Parker R. The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 2001; 104:377-386.
3. Coller J, Parker R. Eukaryotic mRNA decapping. Annu Rev Biochem 2004; 73:861-890
4. Beelman CA, Stevens A, Caponigro G, LaGrandeur TE, Hatfield L, Fortner DM, Parker R. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 1996; 382:642-646.
5. LaGrandeur TE, Parker R. Isolation and characterization of Dcp1p, the yeast mRNA decapping enzyme. EMBO J 1998; 17:1487-1496.
6. Floor SN, Jones BN, Hernandez GA, Gross JD. A split active site couples cap recognition by Dcp2 to activation. Nat Struct Mol Biol 2010; 17:1096-1101.
7. Lykke-Andersen J. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 2002; 22:8114-8121.
8. van Dijk E, Cougot N, Meyer S, Babajko S, Wahle E, Seraphin B. Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J 2002; 21:6915-6924.
9. Wang Z, Jiao X, Carr-Schmid A, Kiledjian M. The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc Natl Acad Sci U S A 2002; 99:12663-12668.
10. Cougot N, Babajko S, Seraphin B. Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 2004; 165:31-40.
11. Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J. Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell 2005; 20:905-915.
12. Ingelfinger D, Arndt-Jovin DJ, Luhrmann R, Achsel T. The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 2002; 8:1489-1501.
13. Kshirsagar M, Parker R. Identification of Edc3p as an enhancer of mRNA decapping in Saccharomyces cerevisiae. Genetics 2004; 166:729-739.
14. Bachvarova R, De Leon V. Polyadenylated RNA of mouse ova and loss of maternal RNA in early development. Dev Biol 1980; 74:1-8.
15. Bachvarova R, De Leon V, Johnson A, Kaplan G, Paynton BV. Changes in total RNA, polyadenylated RNA, and actin mRNA during meiotic maturation of mouse oocytes. Dev Biol 1985; 108:325-331.
16. Brower PT, Gizang E, Boreen SM, Schultz RM. Biochemical studies of mammalian oogenesis: synthesis and stability of various classes of RNA during growth of the mouse oocyte in vitro. Dev Biol 1981; 86:373-383.
17. Jahn CL, Baran MM, Bachvarova R. Stability of RNA synthesized by the mouse oocyte during its major growth phase. J Exp Zool 1976; 197:161-171.
18. Su YQ, Sugiura K, Woo Y, Wigglesworth K, Kamdar S, Affourtit J, Eppig JJ. Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev Biol 2007; 302:104-117.
19. DeRenzo C, Seydoux G. A clean start: degradation of maternal proteins at the oocyte-to-embryo transition. Trends Cell Biol 2004; 14:420-426.
20. Stitzel ML, Seydoux G. Regulation of the oocyte-to-zygote transition. Science 2007; 316:407-408.
21. Medvedev S, Pan H, Schultz RM. Absence of MSY2 in mouse oocytes perturbs oocyte growth and maturation, RNA stability, and the transcriptome. Biol Reprod 2011; 85:575-583.
22. Medvedev S, Yang J, Hecht NB, Schultz RM. CDC2A (CDK1)-mediated phosphorylation of MSY2 triggers maternal mRNA degradation during mouse oocyte maturation. Dev Biol 2008; 321:205-215.
23. Yu J, Deng M, Medvedev S, Yang J, Hecht NB, Schultz RM. Transgenic RNAi-mediated reduction of MSY2 in mouse oocytes results in reduced fertility. Dev Biol 2004; 268:195-206.
24. Flemr M, Ma J, Schultz RM, Svoboda P. P-body loss is concomitant with formation of a messenger RNA storage domain in mouse oocytes. Biol Reprod 2010; 82:1008-1017.
25. Mendez R, Richter JD. Translational control by CPEB: a means to the end. Nature reviews. Mol Cell Biol 2001; 2:521-529.
26. Pique M, Lopez JM, Foissac S, Guigo R, Mendez R. A combinatorial code for CPE-mediated translational control. Cell 2008; 132:434-448.
27. Radford HE, Meijer HA, de Moor CH. Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim Biophys Acta 2008; 1779:217-229.
28. Schultz RM, Montgomery RR, Belanoff JR. Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol 1983; 97:264-273.
29. Wiersma A, Hirsch B, Tsafriri A, Hanssen RG, Van de Kant M, Kloosterboer HJ, Conti M, Hsueh AJ. Phosphodiesterase 3 inhibitors suppress oocyte maturation and consequent pregnancy without affecting ovulation and cyclicity in rodents. J Clin Invest 1998; 102:532-537.
30. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 1989; 86:679-688.
31. Erbach GT, Lawitts JA, Papaioannou VE, Biggers JD. Differential growth of the mouse preimplantation embryo in chemically defined media. Biol Reprod 1994; 50:1027-1033.
32. Whitten WK. Nutrient requirements for the culture of preimplantation mouse embryo in vitro. Adv. Biosci 1971; 6:129-139.
33. Kurasawa S, Schultz RM, Kopf GS. Egg-induced modifications of the zona pellucida of mouse eggs: effects of microinjected inositol 1,4,5- trisphosphate. Dev Biol 1989; 133:295-304.
34. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
35. Svoboda P, Stein P, Hayashi H, Schultz RM. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 2000; 127:4147-4156.
36. Pan H, O'Brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol 2005; 286:493-506.
37. Kishigami S, Wakayama T. Efficient strontium-induced activation of mouse oocytes in standard culture media by chelating calcium. J Reprod Dev 2007; 53:1207-1215.
38. Zeng F, Baldwin DA, Schultz RM. Transcript profiling during preimplantation mouse development. Dev Biol 2004; 272:483-496.
39. Zeng F, Schultz RM. RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev Biol 2005; 283:40-57.
40. Swetloff A, Conne B, Huarte J, Pitetti JL, Nef S, Vassalli JD. Dcp1-bodies in mouse oocytes. Mol Biol Cell 2009; 20:4951-4961.
41. Verlhac MH, Kubiak JZ, Clarke HJ, Maro B. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 1994; 120:1017-1025.
42. Tay J, Hodgman R, Richter JD. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol 2000; 221:1-9.
43. Chen J, Melton C, Suh N, Oh JS, Horner K, Xie F, Sette C, Blelloch R, Conti M. Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev 2011; 25:755-766.
44. Nakahata S, Kotani T, Mita K, Kawasaki T, Katsu Y, Nagahama Y, Yamashita M. Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech Dev 2003; 120:865-880.
45. Padmanabhan K, Richter JD. Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev 2006; 20:199-209.
46. Sheets MD, Fox CA, Hunt T, Vande Woude G, Wickens M. The 30- untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev 1994; 8:926-938.
47. Jackson AL, Burchard J, Leake D, Reynolds A, Schelter J, Guo J, Johnson JM, Lim L, Karpilow J, Nichols K, Marshall W, Khvorova A, et al. Position-specific chemical modification of siRNAs reduces "off-target" transcript silencing. RNA 2006; 12:1197-1205.
48. Myers JW, Chi JT, Gong D, Schaner ME, Brown PO, Ferrell JE. Minimizing off-target effects by using diced siRNAs for RNA interference. J RNAi Gene Silencing 2006; 2:181-194.
49. Parsons BD, Schindler A, Evans DH, Foley E. A direct phenotypic comparison of siRNA pools and multiple individual duplexes in a functional assay. PLoS One 2009; 4:e8471.
50. Anderson EM, Birmingham A, Baskerville S, Reynolds A, Maksimova E, Leake D, Fedorov Y, Karpilow J, Khvorova A. Experimental validation of the importance of seed complement frequency to siRNA specificity. RNA 2008; 14:853-861.
51. Birmingham A, Anderson EM, Reynolds A, Ilsley-Tyree D, Leake D, Fedorov Y, Baskerville S, Maksimova E, Robinson K, Karpilow J, Marshall WS, Khvorova A. 30 UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat Methods 2006; 3:199-204.
52. Saxena S, Jonsson ZO, Dutta A. Small RNAs with imperfect match to endogenous mRNA repress translation. Implications for off-target activity of small inhibitory RNA in mammalian cells. J Biol Chem 2003; 278:44312-44319.
53. Ma J, Flemr M, Stein P, Berninger P, Malik R, Zavolan M, Svoboda P, Schultz RM. MicroRNA activity is suppressed in mouse oocytes. Curr Biol 2010; 20:265-270.
54. Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, Chen J, Blelloch R. MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol 2010; 20:271-277.
55. Schmitter D, Filkowski J, Sewer A, Pillai RS, Oakeley EJ, Zavolan M, Svoboda P, Filipowicz W. Effects of Dicer and Argonaute downregulation on mRNA levels in human HEK293 cells. Nucleic Acids Res 2006; 34:4801-4815.
56. van Dongen S, Abreu-Goodger C, Enright AJ. Detecting microRNA binding and siRNA off-target effects from expression data. Nat Methods 2008; 5:1023-1025.
57. Kubiak J, Paldi A, Weber M, Maro B. Genetically identical parthenogenetic mouse embryos produced by inhibition of the first meiotic cleavage with cytochalasin D. Development 1991; 111:763-769.
58. Vassena R, Han Z, Gao S, Baldwin DA, Schultz RM, Latham KE. Tough beginnings: alterations in the transcriptome of cloned embryos during the first two cell cycles. Dev Biol 2007; 304:75-89.
59. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 2006; 75:243-269.
60. Anger M, Stein P, Schultz RM. CDC6 requirement for spindle formation during maturation of mouse oocytes. Biol Reprod 2005; 72:188-194.
61. Murai S, Stein P, Buffone MG, Yamashita S, Schultz RM. Recruitment of Orc6l, a dormant maternal mRNA in mouse oocytes, is essential for DNA replication in 1-cell embryos. Dev Biol 2010; 341:205-212.
62. 2+ oscillatory behavior in mouse eggs. Dev Biol 2003; 254:163-171.
63. Ducibella T, Schultz RM, Ozil JP. Role of calcium signals in early development. Semin Cell Dev Biol 2006; 17:324-332.
64. Blumenthal J, Behar L, Elliott E, Ginzburg I. Dcp1a phosphorylation along neuronal development and stress. FEBS Lett 2009; 583:197-201.
65. Yoon JH, Choi EJ, Parker R. Dcp2 phosphorylation by Ste20 modulates stress granule assembly and mRNA decay in Saccharomyces cerevisiae. J Cell Biol 2010; 189:813-827.
66. Rzeczkowski K, Beuerlein K, Muller H, Dittrich-Breiholz O, Schneider H, Kettner-Buhrow D, Holtmann H, Kracht M. c-Jun N-terminal kinase phosphorylates DCP1a to control formation of P bodies.J Cell Biol 2011; 194:581-596.
67. Puschendorf M, Stein P, Oakeley EJ, Schultz RM, Peters AH, Svoboda P. Abundant transcripts from retrotransposons are unstable in fully grown mouse oocytes. Biochem Biophys Res Commun 2006; 347:36-43.
68. Muhlrad D, Decker CJ, Parker R. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 50!30 digestion of the transcript. Genes Dev 1994; 8:855-866.
69. Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z, Chen CY, Shyu AB. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 2005; 12:1054-1063.
70. Gillian-Daniel DL, Gray NK, Astrom J, Barkoff A, Wickens M. Modifications of the 50 cap of mRNAs during Xenopus oocyte maturation: independence from changes in poly(A) length and impact on translation. Mol Cell Biol 1998; 18:6152-6163.