P-body loss is concomitant with formation of a messenger RNA storage domain in mouse oocytes
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
R01 HD022681
NICHD NIH HHS - United States
R37 HD022681
NICHD NIH HHS - United States
ME09039
PHS HHS - United States
HD22681
NICHD NIH HHS - United States
PubMed
20075394
PubMed Central
PMC2857638
DOI
10.1095/biolreprod.109.082057
PII: biolreprod.109.082057
Knihovny.cz E-zdroje
- MeSH
- buněčná diferenciace fyziologie MeSH
- cytoplazmatická granula metabolismus MeSH
- endoribonukleasy MeSH
- intracelulární prostor MeSH
- konformace proteinů MeSH
- multiproteinové komplexy metabolismus MeSH
- myši inbrední C57BL MeSH
- myši MeSH
- oocyty metabolismus MeSH
- ovarium růst a vývoj metabolismus MeSH
- proteiny vázající RNA fyziologie MeSH
- ribonukleoproteiny metabolismus MeSH
- RNA čepičky metabolismus MeSH
- RNA messenger skladovaná metabolismus MeSH
- trans-aktivátory metabolismus MeSH
- vývojová regulace genové exprese fyziologie MeSH
- vztahy mezi strukturou a aktivitou MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- endoribonukleasy MeSH
- multiproteinové komplexy MeSH
- proteiny vázající RNA MeSH
- ribonukleoproteiny MeSH
- RNA čepičky MeSH
- RNA messenger skladovaná MeSH
- smad4-interacting protein SMIF, mouse MeSH Prohlížeč
- trans-aktivátory MeSH
In mammalian somatic cells, several pathways that converge on deadenylation, decapping, and 5'-3' degradation are found in cytoplasmic foci known as P-bodies. Because controlled mRNA stability is essential for oocyte-to-zygote transition, we examined the dynamics of P-body components in mouse oocytes. We report that oocyte growth is accompanied by loss of P-bodies and a subcortical accumulation of several RNA-binding proteins, including DDX6, CPEB, YBX2 (MSY2), and the exon junction complex. These proteins form transient RNA-containing aggregates in fully grown oocytes with a surrounded nucleolus chromatin configuration. These aggregates disperse during oocyte maturation, consistent with recruitment of maternal mRNAs that occurs during this time. In contrast, levels of DCP1A are low during oocyte growth, and DCP1A does not colocalize with DDX6 in the subcortical aggregates. The amount of DCP1A markedly increases during meiosis, which correlates with the first wave of destabilization of maternal mRNAs. We propose that the cortex of growing oocytes serves as an mRNA storage compartment, which contains a novel type of RNA granule related to P-bodies.
Zobrazit více v PubMed
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. PubMed
Richter JD.CPEB: a life in translation. Trends Biochem Sci 2007; 32: 279–285. PubMed
Anderson P, Kedersha N.RNA granules. J Cell Biol 2006; 172: 803–808. PubMed PMC
Eulalio A, Behm-Ansmant I, Izaurralde E.P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 2007; 8: 9–22. PubMed
Parker R, Sheth U.P bodies and the control of mRNA translation and degradation. Mol Cell 2007; 25: 635–646. PubMed
Bashkirov VI, Scherthan H, Solinger JA, Buerstedde JM, Heyer WD.A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J Cell Biol 1997; 136: 761–773. PubMed PMC
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. PubMed PMC
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. PubMed PMC
Eystathioy T, Chan EK, Tenenbaum SA, Keene JD, Griffith K, Fritzler MJ.A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol Biol Cell 2002; 13: 1338–1351. PubMed PMC
Yang WH, Yu JH, Gulick T, Bloch KD, Bloch DB.RNA-associated protein 55 (RAP55) localizes to mRNA processing bodies and stress granules. RNA 2006; 12: 547–554. PubMed PMC
Yu JH, Yang WH, Gulick T, Bloch KD, Bloch DB.Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA 2005; 11: 1795–1802. PubMed PMC
Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E.P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 2007; 27: 3970–3981. PubMed PMC
Stalder L, Muhlemann O.Processing bodies are not required for mammalian nonsense-mediated mRNA decay. RNA 2009; 15: 1265–1273. PubMed PMC
Lin MD, Jiao X, Grima D, Newbury SF, Kiledjian M, Chou TB.Drosophila processing bodies in oogenesis. Dev Biol 2008; 322: 276–288. PubMed
Noble SL, Allen BL, Goh LK, Nordick K, Evans TC.Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development. J Cell Biol 2008; 182: 559–572. PubMed PMC
Radford HE, Meijer HA, de Moor CH.Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim Biophys Acta 2008; 1779: 217–229. PubMed PMC
Rajyaguru P, Parker R.CGH-1 and the control of maternal mRNAs. Trends Cell Biol 2009; 19: 24–28. PubMed
Standart N, Minshall N.Translational control in early development: CPEB, P-bodies and germinal granules. Biochem Soc Trans 2008; 36: 671–676. PubMed
Pepling ME, Wilhelm JE, O'Hara AL, Gephardt GW, Spradling AC.Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc Natl Acad Sci U S A 2007; 104: 187–192. PubMed PMC
McLaren A.Primordial germ cells in the mouse. Dev Biol 2003; 262: 1–15. PubMed
Svoboda P.RNA silencing in mammalian oocytes and early embryos. Curr Top Microbiol Immunol 2008; 320: 225–256. PubMed
Yu J, Hecht NB, Schultz RM.Requirement for RNA-binding activity of MSY2 for cytoplasmic localization and retention in mouse oocytes. Dev Biol 2003; 255: 249–262. PubMed
Grunwald D, Singer RH, Czaplinski K.Cell biology of mRNA decay. Methods Enzymol 2008; 448: 553–577. PubMed PMC
Bloch DB, Gulick T, Bloch KD, Yang WH.Processing body autoantibodies reconsidered. RNA 2006; 12: 707–709. PubMed PMC
Inoue A, Nakajima R, Nagata M, Aoki F.Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Hum Reprod 2008; 23: 1377–1384. PubMed
Zuccotti M, Piccinelli A, Giorgi Rossi P, Garagna S, Redi CA.Chromatin organization during mouse oocyte growth. Mol Reprod Dev 1995; 41: 479–485. PubMed
Tang F, Kaneda M, O'Carroll D, Hajkova P, Barton SC, Sun YA, Lee C, Tarakhovsky A, Lao K, Surani MA.Maternal microRNAs are essential for mouse zygotic development. Genes Dev 2007; 21: 644–648. PubMed PMC
Li L, Baibakov B, Dean J.A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev Cell 2008; 15: 416–425. PubMed PMC
Yu J, Hecht NB, Schultz RM.Expression of MSY2 in mouse oocytes and preimplantation embryos. Biol Reprod 2001; 65: 1260–1270. PubMed
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. PubMed
Herr JC, Chertihin O, Digilio L, Jha KN, Vemuganti S, Flickinger CJ.Distribution of RNA binding protein MOEP19 in the oocyte cortex and early embryo indicates pre-patterning related to blastomere polarity and trophectoderm specification. Dev Biol 2008; 314: 300–316. PubMed PMC
Weston A, Sommerville J.Xp54 and related (DDX6-like) RNA helicases: roles in messenger RNP assembly, translation regulation and RNA degradation. Nucleic Acids Res 2006; 34: 3082–3094. PubMed PMC
Gebauer F, Richter JD.Mouse cytoplasmic polyadenylylation element binding protein: an evolutionarily conserved protein that interacts with the cytoplasmic polyadenylylation elements of c-mos mRNA. Proc Natl Acad Sci U S A 1996; 93: 14602–14607. PubMed PMC
Chan CC, Dostie J, Diem MD, Feng W, Mann M, Rappsilber J, Dreyfuss G.eIF4A3 is a novel component of the exon junction complex. RNA 2004; 10: 200–209. PubMed PMC
Matsumoto K, Kwon OY, Kim H, Akao Y.Expression of rck/p54, a DEAD-box RNA helicase, in gametogenesis and early embryogenesis of mice. Dev Dyn 2005; 233: 1149–1156. PubMed
Swetloff A, Conne B, Huarte J, Pitetti JL, Nef S, Vassalli JD.Dcp1-bodies in mouse oocytes. Mol Biol Cell 2009; 20: 4951–4961. PubMed PMC
Lykke-Andersen K, Gilchrist MJ, Grabarek JB, Das P, Miska E, Zernicka-Goetz M.Maternal Argonaute 2 is essential for early mouse development at the maternal-zygotic transition. Mol Biol Cell 2008; 19: 4383–4392. PubMed PMC
Eulalio A, Huntzinger E, Izaurralde E.GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat Struct Mol Biol 2008; 15: 346–353. PubMed
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. PubMed PMC
Murchison EP, Stein P, Xuan Z, Pan H, Zhang MQ, Schultz RM, Hannon GJ.Critical roles for Dicer in the female germline. Genes Dev 2007; 21: 682–693. PubMed PMC
Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ.Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008; 453: 534–538. PubMed PMC
Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, Surani MA, Sakaki Y, Sasaki H.Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008; 453: 539–543. PubMed
Kaneda M, Tang F, O'Carroll D, Lao K, Surani MA.Essential role for Argonaute2 protein in mouse oogenesis. Epigenetics Chromatin 2009; 2: 9 PubMed PMC
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. PubMed PMC
Zheng P, Dean J.Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. Proc Natl Acad Sci U S A 2009; 106: 7473–7478. PubMed PMC
Doherty AS, Bartolomei MS, Schultz RM.Regulation of stage-specific nuclear translocation of Dnmt1o during preimplantation mouse development. Dev Biol 2002; 242: 255–266. PubMed
ncRNA BC1 influences translation in the oocyte
MicroRNA dilution during oocyte growth disables the microRNA pathway in mammalian oocytes
Localization of RNA and translation in the mammalian oocyte and embryo
Long non-coding RNA exchange during the oocyte-to-embryo transition in mice
Temporal and spatial regulation of translation in the mammalian oocyte via the mTOR-eIF4F pathway
Why mouse oocytes and early embryos ignore miRNAs?