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The Function of Maternal P-bodies During the Maturation of Mouse (Mus musculus) Oocyte |
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Abstract Processing bodies (P-bodies) are distinct foci within the cytoplasm of the eukaryotic cell consisting of many enzymes involved in mRNA turnover. P-bodies have been observed in somatic cells originating from vertebrates and invertebrates, plants and yeast. To date, P-bodies have been demonstrated to play fundamental roles in general mRNA decay, nonsense-mediated mRNA decay, adenylate-uridylate-rich element mediated mRNA decay, and microRNA induced mRNA silencing. Not all mRNAs which enter P-bodies are degraded, as it has been demonstrated that some mRNAs can exit P-bodies and re-initiate translation mRNAs are temporarily stored in stress granules. Stress granule is a similar granule of P-body. Stress granules are dense aggregations in the cytosol composed of proteins & RNAs that appear when the cell is under stress. The purpose of stress granules might be to protect RNAs from harmful conditions. Both P-bodies and stress granules play an important role in Post-transcriptional gene regulation. Fully grown mouse (Mus musculus) oocytes in Graafian follicles are transcriptionally silent during the period before the resumption of meiosis until after fertilization when most of the transcriptional reactivation occurs at the 2-cell stage. Products of the oocyte genome support oocyte growth and development before silencing and are also stored for use during the silent period to support oocyte maturation and the early stages of preimplantation embryo development. However, the maturation of oocytes needs a lot of proteins which are mainly generated from the translation of maternally stored mRNA. During the maturation of oocytes, different gene transcriptions expressed at specific time and precise regulation are vital. Oscillatory degradation and resynthesis of cyclins drive the somatic cell through its cycle, and the oocyte utilizes these same processes to control levels of cyclin B1 throughout the period of prophase I arrest. In the fully grown GV oocyte that contains high cyclin B1 levels, ubiquitin-mediated proteasomal degradation of cyclin B1 becomes key to regulating CDK1 activity and is essential during the subsequent stages of meiosis I and II. Known for its role as the driver of anaphase progression in mitosis, the anaphase-promoting complex (APC) is a multimeric E3 ubiquitin ligase, responsible for the ubiquitylation of cyclin B1 and other substrates, which thereby targets them for degradation by the 26S proteasome. The activity and substrate specificity of the APC are regulated by its binding to one of two coactivator proteins that function in a reciprocal manner to coordinate the different phases of the cell cycle. In somatic cells, there are two ways to regulate one gene expression, namely transcriptional regulation and post-transcriptional regulation. The cooperation of both two regulations ensure an orderly life activities in cells. On the contrary, transcriptional regulation does not exist during the maturation of oocytes. Post-transcription regulation is the only way to regulate one gene. Here, we review P-bodies and their function, discuss the function of maternal P-bodies in mouse oocyte maturation, come up with new models about how mRNAs are stored in maternal P-bodies and how mRNAs released from these granules, put forward that oocytes are novel model for the research of post-transcriptional regulation.
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Received: 21 April 2016
Published: 01 October 2016
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Anderson P, Kedersha N. 2009. RNA granules: post-transcriptional and epigenetic modulators of gene expression[J]. Nat Rev Mol Cell Biol, 10(6): 430-436.Anderson P, Kedersha N, Ivanov P. 2015. Stress granules, P-bodies and cancer[J]. Biochim Biophys Acta, 1849(7): 861-870.Andrei M A, Ingelfinger D, Heintzmann R, et al. 2005. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies[J]. RNA-A Publication of the RNA Society, 11(5): 717-727.Ayache J, Bénard M, Ernoult-Lange M, et al. 2015. P-body assembly requires DDX6 repression complexes rather than decay or Ataxin2/2L complexes.[J]. Molecular Biology of the Cell, 26(14): 2579-2595.Baker K E, Parker R. 2004. Nonsense-mediated mRNA decay: terminating erroneous gene expression[J]. Current Opinion in Cell Biology, 16(3): 293-299.Bartel D P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function[J]. Cell, 116(2): 281-297.Bashkirov V I, Scherthan H, Solinger J A, et al. 1997. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates[J]. Journal of Cell Biology, 136(4): 761-773.Boag P R, Atalay A, Robida S, et al. 2008. Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis[J]. Journal of Cell Biology, 182(3): 543-557.Brengues M, Parker R. 2007. Accumulation of polyadenylated mRNA, Pab1p, eIF4E, and eIF4G with P-bodies in Saccharomyces cerevisiae[J]. Molecular Biology of the Cell, 18(7): 2592-2602.Buchan J R. 2014. mRNP granules. Assembly, function, and connections with disease[J]. RNA Biology, 11(8): 1019-1030.Buchan J R, Muhlrad D, Parker R. 2008. P bodies promote stress granule assembly in Saccharomyces cerevisiae[J]. Journal of Cell Biology, 183(3): 441-455.Buchan J R, Nissan T, Parker R. 2010. Chapter 25–Analyzing P-Bodies and Stress Granules in Saccharomyces cerevisiae[J]. Methods in Enzymology, 470: 619-640.Buchan J R, Yoon J H, Parker R. 2011. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae[J]. Journal of Cell Science, 124(Pt 2): 228-239.Chu C Y, Rana T M. 2006. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54[J]. PLoS Biology, 4(7): e210.Coller J, Parker R. 2004. Eukaryotic mRNA decapping[J]. Annual Review of Biochemistry, 73: 861-890.Cougot N, Babajko S, Seraphin B. 2004. Cytoplasmic foci are sites of mRNA decay in human cells[J]. Journal of Cell Biology, 165(1): 31-40.de Moor C H, Meijer H, Lissenden S. 2005. Mechanisms of translational control by the 3' UTR in development and differentiation[J]. Seminars in Cell & Developmental Biology, 16(1): 49-58.de Moor C H, Richter J D. 1999. Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA[J]. EMBO Journal, 18(8): 2294-2303.Decker C J, Teixeira D, Parker R. 2007. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae[J]. Journal of Cell Biology, 179(3): 437-449.Dougherty J D, Tsai W C, Lloyd R E. 2015. Multiple Poliovirus Proteins Repress Cytoplasmic RNA Granules[J]. Viruses, 7(12): 6127-6140.Eulalio A, Behm-Ansmant I, Izaurralde E. 2007. P bodies: at the crossroads of post-transcriptional pathways[J]. Nat Rev Mol Cell Biol, 8(1): 9-22.Fasken M B, Corbett A H. 2005. Process or perish: quality control in mRNA biogenesis[J]. Nature Structural & Molecular Biology, 12(6): 482-488.Ferraiuolo M A, Basak S, Dostie J, et al. 2005. A role for the eIF4E-binding protein 4E-T in P-body formation and mRNA decay[J]. Journal of Cell Biology, 170(6): 913-924.Flemr M, Ma J, Schultz R M, et al. 2010. P-body loss is concomitant with formation of a messenger RNA storage domain in mouse oocytes[J]. Biology of Reproduction, 82(5): 1008-1017.Franks T M, Lykke-Andersen J. 2007. TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements[J]. Genes Dev, 21(6): 719-735.Furuno N, Nishizawa M, Okazaki K, et al. 1994. Suppression of DNA replication via Mos function during meiotic divisions in Xenopus oocytes[J]. EMBO Journal, 13(10): 2399-2410.Gaffre M, Martoriati A, Belhachemi N, et al. 2011. A critical balance between Cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes[J]. Development, 138(17): 3735-3744.Gallois-Montbrun S, Kramer B, Swanson C M, et al. 2007. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules[J]. Journal of Virology, 81(5): 2165-2178.Garneau N L, Wilusz J, Wilusz C J. 2007. The highways and byways of mRNA decay[J]. Nat Rev Mol Cell Biol, 8(2): 113-126.Hake L E, Richter J D. 1994. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation[J]. Cell, 79(4): 617-627.Hochegger H, Klotzbucher A, Kirk J, et al. 2001. New B-type cyclin synthesis is required between meiosis I and II during Xenopus oocyte maturation[J]. Development, 128(19): 3795-3807.Hoyle N P, Castelli L M, Campbell S G, et al. 2007. Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies[J]. Journal of Cell Biology, 179(1): 65-74.Ihara J, Yoshida N, Tanaka T, et al. 1998. Either cyclin B1 or B2 is necessary and sufficient for inducing germinal vesicle breakdown during frog (Rana japonica) oocyte maturation[J]. Molecular Reproduction and Development, 50(4): 499-509.Ingelfinger D, Arndt-Jovin D J, Luhrmann R, et al. 2002. The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci[J]. RNA-A Publication of the RNA Society, 8(12): 1489-1501.Jain S, Parker R. 2013. The discovery and analysis of P Bodies[J]. Advances in Experimental Medicine and Biology, 768: 23-43.Kedersha N L, Gupta M, Li W, et al. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules[J]. Journal of Cell Biology, 147(7): 1431-1442.Kedersha N, Stoecklin G, Ayodele M, et al. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling[J]. Journal of Cell Biology, 169(6): 871-884.Knowles R B, Sabry J H, Martone M E, et al. 1996. Translocation of RNA granules in living neurons[J]. Journal of Neuroscience, 16(24): 7812-7820.Kondo T, Yanagawa T, Yoshida N, et al. 1997. Introduction of cyclin B induces activation of the maturation-promoting factor and breakdown of germinal vesicle in growing zebrafish oocytes unresponsive to the maturation-inducing hormone[J]. Developmental Biology, 190(1): 142-152.Kotani T, Yasuda K, Ota R, et al. 2013. Cyclin B1 mRNA translation is temporally controlled through formation and disassembly of RNA granules[J]. Journal of Cell Biology, 202(7): 1041-1055.Kroschwald S, Maharana S, Mateju D, et al. 2015. Promiscuous interactions and protein disaggregases determine the material state of stress-inducible RNP granules[J]. eLife, 4: e6807.Kuersten S, Goodwin E B. 2003. The power of the 3' UTR: translational control and development[J]. Nature Reviews Genetics, 4(8): 626-637.Lin M D, Jiao X, Grima D, et al. 2008. Drosophila processing bodies in oogenesis[J]. Developmental Biology, 322(2): 276-288.Liu W, Yin J, Zhao G, et al. 2012. Differential regulation of cyclin B1 degradation between the first and second meiotic divisions of bovine oocytes[J]. Theriogenology, 78(6): 1171-1181.Lykke-Andersen J. 2002. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay[J]. Molecular and Cellular Biology, 22(23): 8114-8121.Malureanu L, Jeganathan K B, Jin F, et al. 2010. Cdc20 hypomorphic mice fail to counteract de novo synthesis of cyclin B1 in mitosis[J]. Journal of Cell Biology, 191(2): 313-329.Martin K C. 2004. Local protein synthesis during axon guidance and synaptic plasticity[J]. Current Opinion in Neurobiology, 14(3): 305-310.Matsumoto K, Kwon O Y, Kim H, et al. 2005. Expression of rck/p54, a DEAD-box RNA helicase, in gametogenesis and early embryogenesis of mice[J]. Dev Dyn, 233(3): 1149-1156.Mendez R, Richter J D. 2001. Translational control by CPEB: a means to the end[J]. Nat Rev Mol Cell Biol, 2(7): 521-529.Minshall N, Reiter M H, Weil D, et al. 2007. CPEB interacts with an ovary-specific eIF4E and 4E-T in early Xenopus oocytes[J]. Journal of Biological Chemistry, 282(52): 37389-37401.Mollet S, Cougot N, Wilczynska A, et al. 2008. Translationally repressed mRNA transiently cycles through stress granules during stress[J]. Molecular Biology of the Cell, 19(10): 4469-4479.Nagahama Y, Yamashita M. 2008. Regulation of oocyte maturation in fish[J]. Development Growth & Differentiation, 50 Suppl 1: S195-S219.Nakajo N, Yoshitome S, Iwashita J, et al. 2000. Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes[J]. Genes Dev, 14(3): 328-338.Nakamura A, Amikura R, Hanyu K, et al. 2001. Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis[J]. Development, 128(17): 3233-3242.Noble S L, Allen B L, Goh L K, et al. 2008. Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development[J]. Journal of Cell Biology, 182(3): 559-572.Novoa I, Gallego J, Ferreira P G, et al. 2010. Mitotic cell-cycle progression is regulated by CPEB1 and CPEB4-dependent translational control[J]. Nature Cell Biology, 12(5): 447-456.Ohn T, Kedersha N, Hickman T, et al. 2008. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly[J]. Nature Cell Biology, 10(10): 1224-1231.Parker R, Sheth U. 2007. P bodies and the control of mRNA translation and degradation[J]. Molecular Cell, 25(5): 635-646.Parker R, Song H. 2004. The enzymes and control of eukaryotic mRNA turnover[J]. Nature Structural & Molecular Biology, 11(2): 121-127.Patel P H, Barbee S A, Blankenship J T. 2016. GW-Bodies and P-Bodies Constitute Two Separate Pools of Sequestered Non-Translating RNAs[J]. PLoS One, 11(3): e150291.Pepling M E, Wilhelm J E, O'Hara A L, et al. 2007. Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body[J]. Proc Natl Acad Sci U S A, 104(1): 187-192.Racki W J, Richter J D. 2006. CPEB controls oocyte growth and follicle development in the mouse[J]. Development, 133(22): 4527-4537.Rime H, Neant I, Guerrier P, et al. 1989. 6-Dimethylaminopurine (6-DMAP), a reversible inhibitor of the transition to metaphase during the first meiotic cell division of the mouse oocyte[J]. Developmental Biology, 133(1): 169-179.Rother R P, Frank M B, Thomas P S. 1992. Purification, primary structure, bacterial expression and subcellular distribution of an oocyte-specific protein in Xenopus[J]. Eur J Biochem, 206(3): 673-683.Sagata N, Daar I, Oskarsson M, et al. 1989. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation[J]. Science, 245(4918): 643-646.Schultz R M, Wassarman P M. 1977. Biochemical studies of mammalian oogenesis: Protein synthesis during oocyte growth and meiotic maturation in the mouse[J]. Journal of Cell Science, 24: 167-194.Seto E, Yoshida-Sugitani R, Kobayashi T, et al. 2015. The Assembly of EDC4 and Dcp1a into Processing Bodies Is Critical for the Translational Regulation of IL-6[J]. PLoS One, 10(5): e123223.Sheets M D, Wu M, Wickens M. 1995. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation[J]. Nature, 374(6522): 511-516.Sheth U, Parker R. 2003. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies[J]. Science, 300(5620): 805-808.Sheth U, Parker R. 2006. Targeting of aberrant mRNAs to cytoplasmic processing bodies[J]. Cell, 125(6): 1095-1109.Stalder L, Muhlemann O. 2009. Processing bodies are not required for mammalian nonsense-mediated mRNA decay[J]. RNA-A Publication of the RNA Society, 15(7): 1265-1273.Stebbins-Boaz B, Hake L E, Richter J D. 1996. CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus[J]. EMBO Journal, 15(10): 2582-2592.Steffens A, Brautigam A, Jakoby M, et al. 2015. The BEACH Domain Protein SPIRRIG Is Essential for Arabidopsis Salt Stress Tolerance and Functions as a Regulator of Transcript Stabilization and Localization[J]. PLoS Biology, 13(7): e1002188.Stutz A, Conne B, Huarte J, et al. 1998. Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes[J]. Genes Dev, 12(16): 2535-2548.Stutz A, Huarte J, Gubler P, et al. 1997. In vivo antisense oligodeoxynucleotide mapping reveals masked regulatory elements in an mRNA dormant in mouse oocytes[J]. Molecular and Cellular Biology, 17(4): 1759-1767.Swetloff A, Conne B, Huarte J, et al. 2009. Dcp1-bodies in mouse oocytes[J]. Molecular Biology of the Cell, 20(23): 4951-4961.Tanaka K J, Ogawa K, Takagi M, et al. 2006. RAP55, a cytoplasmic mRNP component, represses translation in Xenopus oocytes[J]. Journal of Biological Chemistry, 281(52): 40096-40106.Tanaka T, Yamashita M. 1995. Pre-MPF is absent in immature oocytes of fishes and amphibians except Xenopus[J]. Development Growth & Regeneration, 37(4): 387-393.Tay J, Hodgman R, Richter J D. 2000. The control of cyclin B1 mRNA translation during mouse oocyte maturation[J]. Developmental Biology, 221(1): 1-9.Tay J, Richter J D. 2001. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice[J]. Developmental Cell, 1(2): 201-213.Teixeira D, Parker R. 2007. Analysis of P-body assembly in Saccharomyces cerevisiae[J]. Molecular Biology of the Cell, 18(6): 2274-2287.Tharun S, He W, Mayes A E, et al. 2000. Yeast Sm-like proteins function in mRNA decapping and decay[J]. Nature, 404(6777): 515-518.van Dijk E, Cougot N, Meyer S, et al. 2002. Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures[J]. EMBO Journal, 21(24): 6915-6924.Vessey J P, Vaccani A, Xie Y, et al. 2006. Dendritic localization of the translational repressor Pumilio 2 and its contribution to dendritic stress granules[J]. Journal of Neuroscience, 26(24): 6496-6508.Wilczynska A, Aigueperse C, Kress M, et al. 2005. The translational regulator CPEB1 provides a link between dcp1 bodies and stress granules[J]. Journal of Cell Science, 118(Pt 5): 981-992.Zayat V, Balcerak A, Korczynski J, et al. 2015. HAX-1: a novel p-body protein[J]. DNA and Cell Biology, 34(1): 43-54. |
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