用户名: 密码: 验证码:
Distinct subcellular localization and potential role of LINE1-ORF1P in meiotic oocytes
详细信息    查看全文
  • 作者:Yi-Bo Luo ; Li Zhang ; Zi-Li Lin ; Jun-Yu Ma ; Jialin Jia…
  • 关键词:LINE ; 1 ; ORF1P ; Oocyte meiotic maturation ; SMAD4 ; DCP1A ; body
  • 刊名:Histochemistry and Cell Biology
  • 出版年:2016
  • 出版时间:January 2016
  • 年:2016
  • 卷:145
  • 期:1
  • 页码:93-104
  • 全文大小:2,234 KB
  • 参考文献:Amatruda JF, Ross JA, Christensen B et al (2013) DNA methylation analysis reveals distinct methylation signatures in pediatric germ cell tumors. BMC Cancer 13:313. doi:10.​1186/​1471-2407-13-313 PubMed PubMedCentral CrossRef
    Anderson P, Kedersha N (2008) Stress granules: the Tao of RNA triage. Trends Biochem Sci 33:141–150. doi:10.​1016/​j.​tibs.​2007.​12.​003 PubMed CrossRef
    Banaz-Yaşar F, Steffen G, Hauschild J et al (2010) LINE-1 retrotransposition events affect endothelial proliferation and migration. Histochem Cell Biol 134:581–589. doi:10.​1007/​s00418-010-0758-y PubMed CrossRef
    Bellmann K, Charette SJ, Nadeau PJ et al (2010) The mechanism whereby heat shock induces apoptosis depends on the innate sensitivity of cells to stress. Cell Stress Chaperones 15:101–113. doi:10.​1007/​s12192-009-0126-9 PubMed PubMedCentral CrossRef
    Bellone M, Zuccotti M, Redi CA, Garagna S (2009) The position of the germinal vesicle and the chromatin organization together provide a marker of the developmental competence of mouse antral oocytes. Reproduction 138:639–643. doi:10.​1530/​REP-09-0230 PubMed CrossRef
    Beraldi R, Pittoggi C, Sciamanna I et al (2006) Expression of LINE-1 retroposons is essential for murine preimplantation development. Mol Reprod Dev 73:279–287. doi:10.​1002/​mrd.​20423 PubMed CrossRef
    Brennan K, Flanagan JM (2012) Is there a link between genome-wide hypomethylation in blood and cancer risk? Cancer Prev Res (Phila) 5:1345–1357. doi:10.​1158/​1940-6207.​CAPR-12-0316 CrossRef
    Callahan KE, Hickman AB, Jones CE et al (2012) Polymerization and nucleic acid-binding properties of human L1 ORF1 protein. Nucleic Acids Res 40:813–827. doi:10.​1093/​nar/​gkr728 PubMed PubMedCentral CrossRef
    Chen L, Dahlstrom JE, Chandra A et al (2012) Prognostic value of LINE-1 retrotransposon expression and its subcellular localization in breast cancer. Breast Cancer Res Treat 136:129–142. doi:10.​1007/​s10549-012-2246-7 PubMed PubMedCentral CrossRef
    Ciaudo C, Jay F, Okamoto I et al (2015) Correction: RNAi-dependent and independent control of LINE1 accumulation and mobility in mouse embryonic stem cells. PLoS Genet 11:e1005247. doi:10.​1371/​journal.​pgen.​1005247 PubMed PubMedCentral CrossRef
    Coticchio G (2004) Mouse oocyte meiotic resumption and polar body extrusion in vitro are differentially influenced by FSH, epidermal growth factor and meiosis-activating sterol. Hum Reprod 19:2913–2918. doi:10.​1093/​humrep/​deh514 PubMed CrossRef
    Crichton JH, Playfoot CJ, Adams IR (2014) The role of chromatin modifications in progression through mouse meiotic prophase. J Genet Genomics 41:97–106. doi:10.​1016/​j.​jgg.​2014.​01.​003 PubMed CrossRef
    Curci A, Bevilacqua A, Mangia F (1987) Lack of heat-shock response in preovulatory mouse oocytes. Dev Biol 123:154–160. doi:10.​1016/​0012-1606(87)90437-4 PubMed CrossRef
    Dai L, LaCava J, Taylor MS, Boeke JD (2014) Expression and detection of LINE-1 ORF-encoded proteins. Mob Genet Elem 4:e29319. doi:10.​4161/​mge.​29319 CrossRef
    De Andrade A, Wang M, Bonaldo MF et al (2011) Genetic and epigenetic variations contributed by Alu retrotransposition. BMC Genom 12:617. doi:10.​1186/​1471-2164-12-617 CrossRef
    Debey P, Szöllösi MS, Szöllösi D et al (1993) Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol Reprod Dev 36:59–74. doi:10.​1002/​mrd.​1080360110 PubMed CrossRef
    Ding W, Lin L, Chen B, Dai J (2006) L1 elements, processed pseudogenes and retrogenes in mammalian genomes. IUBMB Life 58:677–685. doi:10.​1080/​1521654060103485​6 PubMed CrossRef
    Ergün S, Buschmann C, Heukeshoven J et al (2004) Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues. J Biol Chem 279:27753–27763. doi:10.​1074/​jbc.​M312985200 PubMed CrossRef
    Gao X (2011) Effects of LINE-1 ORF-1p overexpression on proliferation and anchor-independent growth of SMMC7721 hepatoma cell line. J Clin Hepatol 14:323–326
    Georgiou I, Noutsopoulos D, Dimitriadou E et al (2009) Retrotransposon RNA expression and evidence for retrotransposition events in human oocytes. Hum Mol Genet 18:1221–1228. doi:10.​1093/​hmg/​ddp022 PubMed CrossRef
    Goodier JL, Ostertag EM, Du K, Kazazian HH (2001) A novel active L1 retrotransposon subfamily in the mouse. Genome Res 11:1677–1685. doi:10.​1101/​gr.​198301 PubMed PubMedCentral CrossRef
    Goodier JL, Zhang L, Vetter MR, Kazazian HH (2007) LINE-1 ORF1 protein localizes in stress granules with other RNA-binding proteins, including components of RNA interference RNA-induced silencing complex. Mol Cell Biol 27:6469–6483. doi:10.​1128/​MCB.​00332-07 PubMed PubMedCentral CrossRef
    Grandi FC, Rosser JM, An W (2013) LINE-1-derived poly(A) microsatellites undergo rapid shortening and create somatic and germline mosaicism in mice. Mol Biol Evol 30:503–512. doi:10.​1093/​molbev/​mss251 PubMed PubMedCentral CrossRef
    Gualtieri A, Andreola F, Sciamanna I et al (2013) Increased expression and copy number amplification of LINE-1 and SINE B1 retrotransposable elements in murine mammary carcinoma progression. Oncotarget 4:1882–1893PubMed PubMedCentral CrossRef
    Harris CR, Normart R, Yang Q et al (2010) Association of nuclear localization of a long interspersed nuclear element-1 protein in breast tumors with poor prognostic outcomes. Genes Cancer 1:115–124. doi:10.​1177/​1947601909360812​ PubMed PubMedCentral CrossRef
    Horký M, Kotala V, Anton M, Wesierska-Gadek J (2002) Nucleolus and apoptosis. Ann NY Acad Sci 973:258–264PubMed CrossRef
    Januszyk K, Li PW, Villareal V et al (2007) Identification and solution structure of a highly conserved C-terminal domain within ORF1p required for retrotransposition of long interspersed nuclear element-1. J Biol Chem 282:24893–24904. doi:10.​1074/​jbc.​M702023200 PubMed CrossRef
    Kaune H, Peyrache E, Williams SA (2015) Oocyte-derived Smad4 is not required for development of the oocyte or the preimplantation embryo. Theriogenology 83:897–903. doi:10.​1016/​j.​theriogenology.​2014.​11.​024 PubMed CrossRef
    Khazina E, Weichenrieder O (2009) Non-LTR retrotransposons encode noncanonical RRM domains in their first open reading frame. Proc Natl Acad Sci USA 106:731–736. doi:10.​1073/​pnas.​0809964106 PubMed PubMedCentral CrossRef
    Kim M, Geum D, Khang I et al (2002) Expression pattern of HSP25 in mouse preimplantation embryo: heat shock responses during oocyte maturation. Mol Reprod Dev 61:3–13. doi:10.​1002/​mrd.​1125 PubMed CrossRef
    Kirilyuk A, Tolstonog GV, Damert A et al (2008) Functional endogenous LINE-1 retrotransposons are expressed and mobilized in rat chloroleukemia cells. Nucleic Acids Res 36:648–665. doi:10.​1093/​nar/​gkm1045 PubMed PubMedCentral CrossRef
    Kulpa DA, Moran JV (2005) Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition. Hum Mol Genet 14:3237–3248. doi:10.​1093/​hmg/​ddi354 PubMed CrossRef
    Li X, Tripurani SK, James R, Pangas SA (2012) Minimal fertility defects in mice deficient in oocyte-expressed Smad4. Biol Reprod 86:1–6. doi:10.​1095/​biolreprod.​111.​094375 CrossRef
    Li H, Hilmarsen HT, Hossain MB et al (2013) Telomere length and LINE1 methylation is associated with chromosomal aberrations in peripheral blood. Genes Chromosomes Cancer 52:1–10. doi:10.​1002/​gcc.​22000 PubMed CrossRef
    Lucchinetti E, Feng J, da Silva R et al (2006) Inhibition of LINE-1 expression in the heart decreases ischemic damage by activation of Akt/PKB signaling. Physiol Genomics 25:314–324. doi:10.​1152/​physiolgenomics.​00251.​2005 PubMed CrossRef
    Mamo S, Gal A, Bodo S, Dinnyes A (2007) Quantitative evaluation and selection of reference genes in mouse oocytes and embryos cultured in vivo and in vitro. BMC Dev Biol 7:14. doi:10.​1186/​1471-213X-7-14 PubMed PubMedCentral CrossRef
    Martin SL (2006) The ORF1 protein encoded by LINE-1: structure and function during L1 retrotransposition. J Biomed Biotechnol 2006:1–6. doi:10.​1155/​JBB/​2006/​45621 CrossRef
    Martin SL (2010) Nucleic acid chaperone properties of ORF1p from the non-LTR retrotransposon, LINE-1. RNA Biol 7:706–711PubMed PubMedCentral CrossRef
    Milleron RS, Bratton SB (2006) Heat shock induces apoptosis independently of any known initiator caspase-activating complex. J Biol Chem 281:16991–17000. doi:10.​1074/​jbc.​M512754200 PubMed CrossRef
    Montero H, Trujillo-Alonso V (2011) Stress granules in the viral replication cycle. Viruses 3:2328–2338. doi:10.​3390/​v3112328 PubMed PubMedCentral CrossRef
    Piskareva O, Ernst C, Higgins N, Schmatchenko V (2013) The carboxy-terminal segment of the human LINE-1 ORF2 protein is involved in RNA binding. FEBS Open Bio 3:433–437. doi:10.​1016/​j.​fob.​2013.​09.​005 PubMed PubMedCentral CrossRef
    Price DK, Ayres JA, Pasqualone D et al (1992) The 5′ ends of LINE1 repeats in rabbit DNA define subfamilies and reveal a short sequence conserved between rabbits and humans. Genomics 14:320–331PubMed CrossRef
    Soares MB, Schon E, Efstratiadis A (1985) Rat LINE1: the origin and evolution of a family of long interspersed middle repetitive DNA elements. J Mol Evol 22:117–133PubMed CrossRef
    Soldani C, Bottone MG, Pellicciari C, Scovassi AI (2006) Nucleolus disassembly in mitosis and apoptosis: dynamic redistribution of phosphorylated-c-Myc, fibrillarin and Ki-67. Eur J Histochem 50:273–280PubMed
    Song AS, Najjar AM, Diller KR (2014) Thermally induced apoptosis, necrosis, and heat shock protein expression in 3D culture. J Biomech Eng 136:071006. doi:10.​1115/​1.​4027272 CrossRef
    Stanford JS, Lieberman SL, Wong VL, Ruderman JV (2003) Regulation of the G2/M transition in oocytes of xenopus tropicalis. Dev Biol 260:438–448. doi:10.​1016/​S0012-1606(03)00259-8 PubMed CrossRef
    Su Y-Q, Sugiura K, Sun F et al (2012) MARF1 regulates essential oogenic processes in mice. Science 335:1496–1499. doi:10.​1126/​science.​1214680 PubMed PubMedCentral CrossRef
    Swetloff A, Conne B, Huarte J et al (2009) Dcp1-bodies in mouse oocytes. Mol Biol Cell 20:4951–4961. doi:10.​1091/​mbc.​E09-02-0123 PubMed PubMedCentral CrossRef
    Tufarelli C, Cruickshanks HA, Meehan RR (2013) LINE-1 activation and epigenetic silencing of suppressor genes in cancer: causally related events? Mob Genet Elements 3:e26832. doi:10.​4161/​mge.​26832 PubMed PubMedCentral CrossRef
    Vasudevan S, Seli E, Steitz JA (2006) Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades. Genes Dev 20:138–146. doi:10.​1101/​gad.​1398906 PubMed CrossRef
    Wang J-Z, Sui H-S, Miao D-Q et al (2009) Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes. Reproduction 137:181–189. doi:10.​1530/​REP-08-0339 PubMed CrossRef
    Weichenrieder O, Repanas K, Perrakis A (2004) Crystal structure of the targeting endonuclease of the human LINE-1 retrotransposon. Structure 12:975–986. doi:10.​1016/​j.​str.​2004.​04.​011 PubMed CrossRef
    Xu L, Massagué J (2004) Nucleocytoplasmic shuttling of signal transducers. Nat Rev Mol Cell Biol 5:209–219. doi:10.​1038/​nrm1331 PubMed CrossRef
    Yu C, Zhang Y-L, Fan H-Y (2013) Selective Smad4 knockout in ovarian preovulatory follicles results in multiple defects in ovulation. Mol Endocrinol 27:966–978. doi:10.​1210/​me.​2012-1364 PubMed CrossRef
    Zhu W, Kuo D, Nathanson J et al (2012) Retrotransposon long interspersed nucleotide element-1 (LINE-1) is activated during salamander limb regeneration. Dev Growth Differ 54:673–685. doi:10.​1111/​j.​1440-169X.​2012.​01368.​x PubMed PubMedCentral CrossRef
    Zhu Y, Feng F, Yu J et al (2013) L1-ORF1p, a Smad4 interaction protein, promotes proliferation of HepG2 cells and tumorigenesis in mice. DNA Cell Biol 32:531–540. doi:10.​1089/​dna.​2013.​2097 PubMed CrossRef
  • 作者单位:Yi-Bo Luo (1) (2)
    Li Zhang (3)
    Zi-Li Lin (2)
    Jun-Yu Ma (1)
    Jialin Jia (2)
    Suk Namgoong (2)
    Qing-Yuan Sun (1)

    1. State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Beijing, China
    2. Department of Animal Science, Chungbuk National University, Cheongju, Korea
    3. Hebei Key Laboratory of Animal Science, Hebei Medical University, Shijiazhuang, China
  • 刊物类别:Medicine
  • 刊物主题:Medicine & Public Health
    Anatomy
    Medicine/Public Health, general
  • 出版者:Springer Berlin / Heidelberg
  • ISSN:1432-119X
文摘
LINE-1 is an autonomous non-LTR retrotransposon in mammalian genomes and encodes ORF1P and ORF2P. ORF2P has been clearly identified as the enzyme supplier needed in LINE-1 retrotransposition. However, the role of ORF1P is not well explored. In this study, we employed loss/gain-of-function approach to investigate the role of LINE1-ORF1P in mouse oocyte meiotic maturation. During mouse oocyte development, ORF1P was observed in cytoplasm as well as in nucleus at germinal vesicle (GV) stage while was localized on the spindle after germinal vesicle breakdown (GVBD). Depletion of ORF1P caused oocyte arrest at the GV stage as well as down-regulation of CDC2 and CYCLIN B1, components of the maturation-promoting factor (MPF). Further analysis demonstrated ORF1P depletion triggered DNA damage response and most of the oocytes presented altered chromatin configuration. In addition, SMAD4 showed nuclear foci signal after Orf1p dsRNA injection. ORF1P overexpression held the oocyte development at MI stage and the chromosome alignment and spindle organization were severely affected. We also found that ORF1P could form DCP1A body-like foci structure in both cytoplasm and nucleus after heat shock. Taken together, accurate regulation of ORF1P plays an essential role in mouse oocyte meiotic maturation.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700