Role of Cnot6l in maternal mRNA turnover

. 2018 Aug ; 1 (4) : e201800084. [epub] 20180716

Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30456367

Grantová podpora
R01 HD022681 NICHD NIH HHS - United States
R37 HD022681 NICHD NIH HHS - United States

Removal of poly(A) tail is an important mechanism controlling eukaryotic mRNA turnover. The major eukaryotic deadenylase complex CCR4-NOT contains two deadenylase components, CCR4 and CAF1, for which mammalian CCR4 is encoded by Cnot6 or Cnot6l paralogs. We show that Cnot6l apparently supplies the majority of CCR4 in the maternal CCR4-NOT in mouse, hamster, and bovine oocytes. Deletion of Cnot6l yielded viable mice, but Cnot6l -/- females exhibited ∼40% smaller litter size. The main onset of the phenotype was post-zygotic: fertilized Cnot6l -/- eggs developed slower and arrested more frequently than Cnot6l +/- eggs, suggesting that maternal CNOT6L is necessary for accurate oocyte-to-embryo transition. Transcriptome analysis revealed major transcriptome changes in Cnot6l -/- ovulated eggs and one-cell zygotes. In contrast, minimal transcriptome changes in preovulatory Cnot6l -/- oocytes were consistent with reported Cnot6l mRNA dormancy. A minimal overlap between transcripts sensitive to decapping inhibition and Cnot6l loss suggests that decapping and CNOT6L-mediated deadenylation selectively target distinct subsets of mRNAs during oocyte-to-embryo transition in mouse.

Zobrazit více v PubMed

Despic V, Neugebauer KM (2018) RNA tales: How embryos read and discard messages from mom. J Cell Sci 131: jcs201996 10.1242/jcs.201996 PubMed DOI

Svoboda P, Franke V, Schultz RM (2015) Sculpting the transcriptome during the oocyte-to-embryo transition in mouse. Curr Top Dev Biol 113: 305–349. 10.1016/bs.ctdb.2015.06.004 PubMed DOI

Houseley J, Tollervey D (2009) The many pathways of RNA degradation. Cell 136: 763–776. 10.1016/j.cell.2009.01.019 PubMed DOI

Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z, Chen CY, Shyu AB (2005) Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 12: 1054–1063. 10.1038/nsmb1016 PubMed DOI

Parker R, Song H (2004) The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 11: 121–127. 10.1038/nsmb724 PubMed DOI

Goldstrohm AC, Wickens M (2008) Multifunctional deadenylase complexes diversify mRNA control. Nat Rev Mol Cell Biol 9: 337–344. 10.1038/nrm2370 PubMed DOI

Bartlam M, Yamamoto T (2010) The structural basis for deadenylation by the CCR4-NOT complex. Protein Cell 1: 443–452. 10.1007/s13238-010-0060-8 PubMed DOI PMC

Yi H, Park J, Ha M, Lim J, Chang H, Kim VN (2018) PABP cooperates with the CCR4-NOT complex to promote mRNA deadenylation and block precocious decay. Mol Cell 70: 1081–1088.e1085. 10.1016/j.molcel.2018.05.009 PubMed DOI

Collart MA, Panasenko OO (2017) The Ccr4-Not complex: Architecture and structural insights. Subcell Biochem 83: 349–379. 10.1007/978-3-319-46503-6_13 PubMed DOI

Collart MA. (2016) The Ccr4-Not complex is a key regulator of eukaryotic gene expression. Wiley Interdiscip Rev RNA 7: 438–454. 10.1002/wrna.1332 PubMed DOI PMC

Doidge R, Mittal S, Aslam A, Winkler GS (2012) Deadenylation of cytoplasmic mRNA by the mammalian Ccr4-Not complex. Biochem Soc Trans 40: 896–901. 10.1042/bst20120074 PubMed DOI

Suh N, Baehner L, Moltzahn F, Melton C, Shenoy A, Chen J, Blelloch R (2010) MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol 20: 271–277. 10.1016/j.cub.2009.12.044 PubMed DOI PMC

Yu C, Ji SY, Sha QQ, Dang Y, Zhou JJ, Zhang YL, Liu Y, Wang ZW, Hu B, Sun QY, et al. (2016) BTG4 is a meiotic cell cycle-coupled maternal-zygotic-transition licensing factor in oocytes. Nat Struct Mol Biol 23: 387–394. 10.1038/nsmb.3204 PubMed DOI

Du H, Zhao Y, He J, Zhang Y, Xi H, Liu M, Ma J, Wu L (2016) YTHDF2 destabilizes m(6)A-containing RNA through direct recruitment of the CCR4-NOT deadenylase complex. Nat Commun 7: 12626 10.1038/ncomms12626 PubMed DOI PMC

Ivanova I, Much C, Di Giacomo M, Azzi C, Morgan M, Moreira PN, Monahan J, Carrieri C, Enright AJ, O'Carroll D (2017) The RNA m(6)A reader YTHDF2 is essential for the post-transcriptional regulation of the maternal transcriptome and oocyte competence. Mol Cell 67: 1059–1067.e1054. 10.1016/j.molcel.2017.08.003 PubMed DOI PMC

Ma J, Flemr M, Strnad H, Svoboda P, Schultz RM (2013) Maternally recruited DCP1A and DCP2 contribute to messenger RNA degradation during oocyte maturation and genome activation in mouse. Biol Reprod 88: 11 10.1095/biolreprod.112.105312 PubMed DOI PMC

Ma J, Fukuda Y, Schultz RM (2015) Mobilization of dormant Cnot7 mRNA promotes deadenylation of maternal transcripts during mouse oocyte maturation. Biol Reprod 93: 48 10.1095/biolreprod.115.130344 PubMed DOI PMC

Su AI, Cooke MP, Ching KA, Hakak Y, Walker JR, Wiltshire T, Orth AP, Vega RG, Sapinoso LM, Moqrich A, et al. (2002) Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci USA 99: 4465–4470. 10.1073/pnas.012025199 PubMed DOI PMC

Abe K, Yamamoto R, Franke V, Cao M, Suzuki Y, Vlahovicek K, Svoboda P, Schultz RM, Aoki F (2015) The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3′ processing. EMBO J 34: 1523–1537. 10.15252/embj.201490648 PubMed DOI PMC

Karlic R, Ganesh S, Franke V, Svobodova E, Urbanova J, Suzuki Y, Aoki F, Vlahovicek K, Svoboda P (2017) Long non-coding RNA exchange during the oocyte-to-embryo transition in mice. DNA Res 24: 129–141. 10.1093/dnares/dsx008 PubMed DOI PMC

Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E (2014) Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc Natl Acad Sci USA 111: 4139–4144. 10.1073/pnas.1321569111 PubMed DOI PMC

Xue Z, Huang K, Cai C, Cai L, Jiang CY, Feng Y, Liu Z, Zeng Q, Cheng L, Sun YE, et al. (2013) Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500: 593–597. 10.1038/nature12364 PubMed DOI PMC

Vieux KF, Clarke HJ (2018) CNOT6 regulates a novel pattern of mRNA deadenylation during oocyte meiotic maturation. Sci Rep 8: 6812 10.1038/s41598-018-25187-0 PubMed DOI PMC

Svoboda P, Fulka H, Malik R (2017) Clearance of parental products. Adv Exp Med Biol 953: 489–535. 10.1007/978-3-319-46095-6_10 PubMed DOI

Nagasawa H, Miyamoto M, Fujimoto M (1973) Reproductivity in inbred strains of mice and project for their efficient production (author's transl) (in Japanese). Jikken Dobutsu 22: 119–126. 10.1538/expanim1957.22.2_119 PubMed DOI

Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550 10.1186/s13059-014-0550-8 PubMed DOI PMC

Gebauer F, Xu W, Cooper GM, Richter JD (1994) Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J 13: 5712–5720. 10.1002/j.1460-2075.1994.tb06909.x PubMed DOI PMC

Morgan M, Much C, DiGiacomo M, Azzi C, Ivanova I, Vitsios DM, Pistolic J, Collier P, Moreira PN, Benes V, et al. (2017) mRNA 3′ uridylation and poly(A) tail length sculpt the mammalian maternal transcriptome. Nature 548: 347–351. 10.1038/nature23318 PubMed DOI PMC

Nagy A. (2003) Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.

Jankele R, Svoboda P (2014) TAL effectors: Tools for DNA targeting. Brief Funct Genomics 13: 409–419. 10.1093/bfgp/elu013 PubMed DOI PMC

Flemr M, Malik R, Franke V, Nejepinska J, Sedlacek R, Vlahovicek K, Svoboda P (2013) A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 155: 807–816. 10.1016/j.cell.2013.10.001 PubMed DOI

Lin Y, Fine EJ, Zheng Z, Antico CJ, Voit RA, Porteus MH, Cradick TJ, Bao G (2014) SAPTA: A new design tool for improving TALE nuclease activity. Nucleic Acids Res 42: e47 10.1093/nar/gkt1363 PubMed DOI PMC

Fine EJ, Cradick TJ, Zhao CL, Lin Y, Bao G (2014) An online bioinformatics tool predicts zinc finger and TALE nuclease off-target cleavage. Nucleic Acids Res 42: e42 10.1093/nar/gkt1326 PubMed DOI PMC

Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29: 15–21. 10.1093/bioinformatics/bts635 PubMed DOI PMC

Franke V, Ganesh S, Karlic R, Malik R, Pasulka J, Horvat F, Kuzman M, Fulka H, Cernohorska M, Urbanova J, et al. (2017) Long terminal repeats power evolution of genes and gene expression programs in mammalian oocytes and zygotes. Genome Res 27: 1384–1394. 10.1101/gr.216150.116 PubMed DOI PMC

Kent WJ, Zweig AS, Barber G, Hinrichs AS, Karolchik D (2010) BigWig and BigBed: Enabling browsing of large distributed datasets. Bioinformatics 26: 2204–2207. 10.1093/bioinformatics/btq351 PubMed DOI PMC

Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289–300. 10.2307/2346101 DOI

Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249–264. 10.1093/biostatistics/4.2.249 PubMed DOI

Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99: 909–917. 10.1198/016214504000000683 DOI

Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116–5121. 10.1073/pnas.091062498 PubMed DOI PMC

Winkler GS, Balacco DL (2013) Heterogeneity and complexity within the nuclease module of the Ccr4-Not complex. Front Genet 4: 296 10.3389/fgene.2013.00296 PubMed DOI PMC

Yue F, Cheng Y, Breschi A, Vierstra J, Wu W, Ryba T, Sandstrom R, Ma Z, Davis C, Pope BD, et al. (2014) A comparative encyclopedia of DNA elements in the mouse genome. Nature 515: 355–364. 10.1038/nature13992 PubMed DOI PMC

Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, et al. (2015) CDD: NCBI's conserved domain database. Nucleic Acids Res 43: D222–D226. 10.1093/nar/gku1221 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...