Maternal topoisomerase II alpha, not topoisomerase II beta, enables embryonic development of zebrafish top2a -/- mutants

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• 作者：Beata Sapetto-Rebow (1)
  Sarah C McLoughlin (1) (5)
  Lynne C O’Shea (1)
  Olivia O’Leary (1)
  Jason R Willer (2)
  Yolanda Alvarez (1)
  Ross Collery (1) (6)
  Jacintha O’Sullivan (3)
  Freek Van Eeden (4)
  Carmel Hensey (1)
  Breandán N Kennedy (1)
  
• 刊名：BMC Developmental Biology
• 出版年：2011
• 出版时间：December 2011
• 年：2011
• 卷：11
• 期：1
• 全文大小：2116KB
• 参考文献：1. Roca J: plus-plus">Topoisomerase II: a fitted mechanism for the chromatin landscape. / Nucleic Acids Res 2009, plus-plus">37:721-0. p://dx.doi.org/10.1093/nar/gkn994">CrossRef
  2. Costanzo V, Shechter D, Lupardus PJ, Cimprich KA, Gottesman M, Gautier J: plus-plus">An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. / Mol Cell 2003, plus-plus">11:203-3. p://dx.doi.org/10.1016/S1097-2765(02)00799-2">CrossRef
  3. Cuvier O, Hirano T: plus-plus">A role of topoisomerase II in linking DNA replication to chromosome condensation. / J Cell Biol 2003, plus-plus">160:645-5. p://dx.doi.org/10.1083/jcb.200209023">CrossRef
  4. Cuvier O, Stanojcic S, Lemaitre JM, Mechali M: plus-plus">A topoisomerase II-dependent mechanism for resetting replicons at the S-M-phase transition. / Genes Dev 2008, plus-plus">22:860-. p://dx.doi.org/10.1101/gad.445108">CrossRef
  5. Adachi N, Kobayashi M, Koyama H: plus-plus">Cell cycle-dependent regulation of the mouse DNA topoisomerase IIalpha gene promoter. / Biochem Biophys Res Commun 1997, plus-plus">230:105-. p://dx.doi.org/10.1006/bbrc.1996.5893">CrossRef
  6. Mano MS, Rosa DD, Azambuja E De, Ismael GF, Durbecq V: plus-plus">The 17q12-q21 amplicon: Her2 and topoisomerase-IIalpha and their importance to the biology of solid tumours. / Cancer Treat Rev 2007, plus-plus">33:64-7. p://dx.doi.org/10.1016/j.ctrv.2006.10.001">CrossRef
  7. McClendon AK, Rodriguez AC, Osheroff N: plus-plus">Human topoisomerase IIalpha rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. / J Biol Chem 2005, plus-plus">280:39337-5. p://dx.doi.org/10.1074/jbc.M503320200">CrossRef
  8. McClendon AK, Osheroff N: plus-plus">DNA topoisomerase II, genotoxicity, and cancer. / Mutat Res 2007, plus-plus">623:83-7. p://dx.doi.org/10.1016/j.mrfmmm.2007.06.009">CrossRef
  9. Nitiss JL: plus-plus">DNA topoisomerase II and its growing repertoire of biological functions. / Nat Rev Cancer 2009, plus-plus">9:327-7. p://dx.doi.org/10.1038/nrc2608">CrossRef
  10. Coelho PA, Queiroz-Machado J, Carmo AM, Moutinho-Pereira S, Maiato H, Sunkel CE: plus-plus">Dual role of topoisomerase II in centromere resolution and aurora B activity. / PLoS Biol 2008, plus-plus">6:e207. p://dx.doi.org/10.1371/journal.pbio.0060207">CrossRef
  11. Nitiss JL: plus-plus">Targeting DNA topoisomerase II in cancer chemotherapy. / Nat Rev Cancer 2009, plus-plus">9:338-0. p://dx.doi.org/10.1038/nrc2607">CrossRef
  12. Jenkins JR, Ayton P, Jones T, Davies SL, Simmons DL, Harris AL, Sheer D, Hickson ID: plus-plus">Isolation of cDNA clones encoding the beta isozyme of human DNA topoisomerase II and localisation of the gene to chromosome 3p24. / Nucleic Acids Res 1992, plus-plus">20:5587-2. p://dx.doi.org/10.1093/nar/20.21.5587">CrossRef
  13. Kimura K, Saijo M, Ui M, Enomoto T: plus-plus">Growth state- and cell cycle-dependent fluctuation in the expression of two forms of DNA topoisomerase II and possible specific modification of the higher molecular weight form in the M phase. / J Biol Chem 1994, plus-plus">269:1173-.
  14. Woessner RD, Mattern MR, Mirabelli CK, Johnson RK, Drake FH: plus-plus">Proliferation- and cell cycle-dependent differences in expression of the 170 kilodalton and 180 kilodalton forms of topoisomerase II in NIH-3T3 cells. / Cell Growth Differ 1991, plus-plus">2:209-4.
  15. Capranico G, Tinelli S, Austin CA, Fisher ML, Zunino F: plus-plus">Different patterns of gene expression of topoisomerase II isoforms in differentiated tissues during murine development. / Biochim Biophys Acta 1992, plus-plus">1132:43-.
  16. Tsutsui K, Tsutsui K, Hosoya O, Sano K, Tokunaga A: plus-plus">Immunohistochemical analyses of DNA topoisomerase II isoforms in developing rat cerebellum. / J Comp Neurol 2001, plus-plus">431:228-9. p://dx.doi.org/10.1002/1096-9861(20010305)431:2<228::AID-CNE1067>3.0.CO;2-M">CrossRef
  17. Lyu YL, Lin CP, Azarova AM, Cai L, Wang JC, Liu LF: plus-plus">Role of topoisomerase IIbeta in the expression of developmentally regulated genes. / Mol Cell Biol 2006, plus-plus">26:7929-1. p://dx.doi.org/10.1128/MCB.00617-06">CrossRef
  18. Johnson M, Phua HH, Bennett SC, Spence JM, Farr CJ: plus-plus">Studying vertebrate topoisomerase 2 function using a conditional knockdown system in DT40 cells. / Nucleic Acids Res 2009, plus-plus">37:e98. p://dx.doi.org/10.1093/nar/gkp480">CrossRef
  19. Carpenter AJ, Porter AC: plus-plus">Construction, characterization, and complementation of a conditional-lethal DNA topoisomerase IIalpha mutant human cell line. / Mol Biol Cell 2004, plus-plus">15:5700-1. p://dx.doi.org/10.1091/mbc.E04-08-0732">CrossRef
  20. Akimitsu N, Adachi N, Hirai H, Hossain MS, Hamamoto H, Kobayashi M, Aratani Y, Koyama H, Sekimizu K: plus-plus">Enforced cytokinesis without complete nuclear division in embryonic cells depleting the activity of DNA topoisomerase IIalpha. / Genes Cells 2003, plus-plus">8:393-02. p://dx.doi.org/10.1046/j.1365-2443.2003.00643.x">CrossRef
  21. Tsutsui K, Tsutsui K, Sano K, Kikuchi A, Tokunaga A: plus-plus">Involvement of DNA topoisomerase IIbeta in neuronal differentiation. / J Biol Chem 2001, plus-plus">276:5769-8. p://dx.doi.org/10.1074/jbc.M008517200">CrossRef
  22. Nur EKA, Meiners S, Ahmed I, Azarova A, Lin CP, Lyu YL, Liu LF: plus-plus">Role of DNA topoisomerase IIbeta in neurite outgrowth. / Brain Res 2007, plus-plus">1154:50-0. p://dx.doi.org/10.1016/j.brainres.2007.04.029">CrossRef
  23. Lyu YL, Wang JC: plus-plus">Aberrant lamination in the cerebral cortex of mouse embryos lacking DNA topoisomerase IIbeta. / Proc Natl Acad Sci USA 2003, plus-plus">100:7123-. p://dx.doi.org/10.1073/pnas.1232376100">CrossRef
  24. Yang X, Li W, Prescott ED, Burden SJ, Wang JC: plus-plus">DNA topoisomerase IIbeta and neural development. / Science 2000, plus-plus">287:131-. p://dx.doi.org/10.1126/science.287.5450.131">CrossRef
  25. Roca J, Ishida R, Berger JM, Andoh T, Wang JC: plus-plus">Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. / Proc Natl Acad Sci USA 1994, plus-plus">91:1781-. p://dx.doi.org/10.1073/pnas.91.5.1781">CrossRef
  26. Montecucco A, Biamonti G: plus-plus">Cellular response to etoposide treatment. / Cancer Lett 2007, plus-plus">252:9-8. p://dx.doi.org/10.1016/j.canlet.2006.11.005">CrossRef
  27. Azarova AM, Lyu YL, Lin CP, Tsai YC, Lau JY, Wang JC, Liu LF: plus-plus">Roles of DNA topoisomerase II isozymes in chemotherapy and secondary malignancies. / Proc Natl Acad Sci USA 2007, plus-plus">104:11014-. p://dx.doi.org/10.1073/pnas.0704002104">CrossRef
  28. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N: plus-plus">Identification of 315 genes essential for early zebrafish development. / Proc Natl Acad Sci USA 2004, plus-plus">101:12792-. p://dx.doi.org/10.1073/pnas.0403929101">CrossRef
  29. Dovey M, Patton EE, Bowman T, North T, Goessling W, Zhou Y, Zon LI: plus-plus">Topoisomerase II alpha is required for embryonic development and liver regeneration in zebrafish. / Mol Cell Biol 2009, plus-plus">29:3746-3. p://dx.doi.org/10.1128/MCB.01684-08">CrossRef
  30. Nevin LM, Xiao T, Staub W, Baier H: plus-plus">Topoisomerase IIbeta is required for lamina-specific targeting of retinal ganglion cell axons and dendrites. / Development plus-plus">138:2457-5.
  31. Etkin LD: plus-plus">Regulation of the mid-blastula transition in amphibians. / Dev Biol (N Y 1985) 1988, plus-plus">5:209-5.
  32. Tadros W, Lipshitz HD: plus-plus">The maternal-to-zygotic transition: a play in two acts. / Development 2009, plus-plus">136:3033-2. p://dx.doi.org/10.1242/dev.033183">CrossRef
  33. Aanes H, Winata CL, Lin CH, Chen JP, Srinivasan KG, Lee SG, Lim AY, Hajan HS, Collas P, Bourque G, / et al.: plus-plus">Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. / Genome Res 2011, plus-plus">21:1328-8. p://dx.doi.org/10.1101/gr.116012.110">CrossRef
  34. Kane DA, Kimmel CB: plus-plus">The zebrafish midblastula transition. / Development 1993, plus-plus">119:447-6.
  35. Pelegri F: plus-plus">Maternal factors in zebrafish development. / Dev Dyn 2003, plus-plus">228:535-4. p://dx.doi.org/10.1002/dvdy.10390">CrossRef
  36. Murray AW: plus-plus">Cell cycle extracts. / Methods Cell Biol 1991, plus-plus">36:581-05. p://dx.doi.org/10.1016/S0091-679X(08)60298-8">CrossRef
  37. Sakaguchi A, Kikuchi A: plus-plus">Functional compatibility between isoform alpha and beta of type II DNA topoisomerase. / J Cell Sci 2004, plus-plus">117:1047-4. p://dx.doi.org/10.1242/jcs.00977">CrossRef
  38. Linka RM, Porter AC, Volkov A, Mielke C, Boege F, Christensen MO: plus-plus">C-terminal regions of topoisomerase IIalpha and IIbeta determine isoform-specific functioning of the enzymes in vivo. / Nucleic Acids Res 2007, plus-plus">35:3810-2. p://dx.doi.org/10.1093/nar/gkm102">CrossRef
  39. Hirano T, Mitchison TJ: plus-plus">Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts. / J Cell Biol 1993, plus-plus">120:601-2. p://dx.doi.org/10.1083/jcb.120.3.601">CrossRef
  40. Ikegami R, Rivera-Bennetts AK, Brooker DL, Yager TD: plus-plus">Effect of inhibitors of DNA replication on early zebrafish embryos: evidence for coordinate activation of multiple intrinsic cell-cycle checkpoints at the mid-blastula transition. / Zygote 1997, plus-plus">5:153-5.
  41. Duffy KT, McAleer MF, Davidson WR, Kari L, Kari C, Liu CG, Farber SA, Cheng KC, Mest JR, Wickstrom E, / et al.: plus-plus">Coordinate control of cell cycle regulatory genes in zebrafish development tested by cyclin D1 knockdown with morpholino phosphorodiamidates and hydroxyprolyl-phosphono peptide nucleic acids. / Nucleic Acids Res 2005, plus-plus">33:4914-1. p://dx.doi.org/10.1093/nar/gki799">CrossRef
  42. Luo K, Yuan J, Chen J, Lou Z: plus-plus">Topoisomerase IIalpha controls the decatenation checkpoint. / Nat Cell Biol 2009, plus-plus">11:204-0. p://dx.doi.org/10.1038/ncb1828">CrossRef
  43. Bower JJ, Karaca GF, Zhou Y, Simpson DA, Cordeiro-Stone M, Kaufmann WK: plus-plus">Topoisomerase IIalpha maintains genomic stability through decatenation G(2) checkpoint signaling. / Oncogene plus-plus">29:4787-9.
  44. Ikegami R, Hunter P, Yager TD: plus-plus">Developmental activation of the capability to undergo checkpoint-induced apoptosis in the early zebrafish embryo. / Dev Biol 1999, plus-plus">209:409-3. p://dx.doi.org/10.1006/dbio.1999.9243">CrossRef
  45. Pierre J St, Wright DJ, Rowe TC, Wright SJ: plus-plus">DNA topoisomerase II is essential for preimplantation mouse development. / Mol Reprod Dev 2002, plus-plus">61:347-7. p://dx.doi.org/10.1002/mrd.10015">CrossRef
  46. Li L, Zheng P, Dean J: plus-plus">Maternal control of early mouse development. / Development 2010, plus-plus">137:859-0. p://dx.doi.org/10.1242/dev.039487">CrossRef
  47. Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP, / et al.: plus-plus">The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. / Development 1996, plus-plus">123:1-6.
  
• 作者单位：Beata Sapetto-Rebow (1)
  Sarah C McLoughlin (1) (5)
  Lynne C O’Shea (1)
  Olivia O’Leary (1)
  Jason R Willer (2)
  Yolanda Alvarez (1)
  Ross Collery (1) (6)
  Jacintha O’Sullivan (3)
  Freek Van Eeden (4)
  Carmel Hensey (1)
  Breandán N Kennedy (1)
  
  1. UCD School of Biomolecular and Biomedical Science, UCD Conway Institute, University College Dublin, Dublin, Ireland
  5. Institute for Translational Medicine and Therapeutics, School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
  2. Department of Biochemistry and Molecular Biology, University of Louisville, Louisville, KY, USA
  6. Department of Cell Biology, Neurobiology & Anatomy, Medical College of Wisconsin, Milwaukee, WI, USA
  3. St. James’s Hospital, Trinity College Dublin, Dublin, Ireland
  4. Department of Biomedical Science, University of Sheffield, Sheffield, UK
  

文摘

Background Genetic alterations in human topoisomerase II alpha (TOP2A) are linked to cancer susceptibility. TOP2A decatenates chromosomes and thus is necessary for multiple aspects of cell division including DNA replication, chromosome condensation and segregation. Topoisomerase II alpha is also required for embryonic development in mammals, as mouse Top2a knockouts result in embryonic lethality as early as the 4-8 cell stage. The purpose of this study was to determine whether the extended developmental capability of zebrafish top2a mutants arises from maternal expression of top2a or compensation from its top2b paralogue. Results Here, we describe bloody minded (blm), a novel mutant of zebrafish top2a. In contrast to mouse Top2a nulls, zebrafish top2a mutants survive to larval stages (4-5 day post fertilization). Developmental analyses demonstrate abundant expression of maternal top2a but not top2b. Inhibition or poisoning of maternal topoisomerase II delays embryonic development by extending the cell cycle M-phase. Zygotic top2a and top2b are co-expressed in the zebrafish CNS, but endogenous or ectopic top2b RNA appear unable to prevent the blm phenotype. Conclusions We conclude that maternal top2a enables zebrafish development before the mid-zygotic transition (MZT) and that zebrafish top2a and top2b are not functionally redundant during development after activation of the zygotic genome.