Cisplatin-induced DNA double-strand breaks promote meiotic chromosome synapsis in PRDM9-controlled mouse hybrid sterility
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30592461
PubMed Central
PMC6324875
DOI
10.7554/elife.42511
PII: 42511
Knihovny.cz E-zdroje
- Klíčová slova
- DNA double-strand breaks, Prdm9, chromosomes, gene expression, genetics, genomics, hybrid sterility, meiosis, mouse,
- MeSH
- antitumorózní látky toxicita MeSH
- cisplatina toxicita MeSH
- dvouřetězcové zlomy DNA účinky léků MeSH
- histonlysin-N-methyltransferasa genetika metabolismus MeSH
- hybridizace genetická MeSH
- meióza účinky léků genetika MeSH
- mužská infertilita genetika MeSH
- myši inbrední C57BL MeSH
- oprava DNA MeSH
- párování chromozomů účinky léků genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- antitumorózní látky MeSH
- cisplatina MeSH
- histonlysin-N-methyltransferasa MeSH
- prdm9 protein, mouse MeSH Prohlížeč
PR domain containing 9 (Prdm9) is specifying hotspots of meiotic recombination but in hybrids between two mouse subspecies Prdm9 controls failure of meiotic chromosome synapsis and hybrid male sterility. We have previously reported that Prdm9-controlled asynapsis and meiotic arrest are conditioned by the inter-subspecific heterozygosity of the hybrid genome and we presumed that the insufficient number of properly repaired PRDM9-dependent DNA double-strand breaks (DSBs) causes asynapsis of chromosomes and meiotic arrest (Gregorova et al., 2018). We now extend the evidence for the lack of properly processed DSBs by improving meiotic chromosome synapsis with exogenous DSBs. A single injection of chemotherapeutic drug cisplatin increased frequency of RPA and DMC1 foci at the zygotene stage of sterile hybrids, enhanced homolog recognition and increased the proportion of spermatocytes with fully synapsed homologs at pachytene. The results bring a new evidence for a DSB-dependent mechanism of synapsis failure and infertility of intersubspecific hybrids.
Zobrazit více v PubMed
Altemose N, Noor N, Bitoun E, Tumian A, Imbeault M, Chapman JR, Aricescu AR, Myers SR. A map of human PRDM9 binding provides evidence for novel behaviors of PRDM9 and other zinc-finger proteins in meiosis. eLife. 2017;6:e28383. doi: 10.7554/eLife.28383. PubMed DOI PMC
Anderson LK, Reeves A, Webb LM, Ashley T. Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics. 1999;151:1569–1579. PubMed PMC
Baker CL, Kajita S, Walker M, Saxl RL, Raghupathy N, Choi K, Petkov PM, Paigen K. PRDM9 drives evolutionary erosion of hotspots in Mus musculus through haplotype-specific initiation of meiotic recombination. PLoS Genetics. 2015;11:e1004916. doi: 10.1371/journal.pgen.1004916. PubMed DOI PMC
Basu A, Krishnamurthy S. Cellular responses to Cisplatin-induced DNA damage. Journal of Nucleic Acids. 2010;2010:1–16. doi: 10.4061/2010/201367. PubMed DOI PMC
Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science. 2010;327:836–840. doi: 10.1126/science.1183439. PubMed DOI PMC
Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, Denny P, Simecek P, Forejt J. Mechanistic basis of infertility of mouse intersubspecific hybrids. PNAS. 2013;110:E468–E477. doi: 10.1073/pnas.1219126110. PubMed DOI PMC
Bhattacharyya T, Reifova R, Gregorova S, Simecek P, Gergelits V, Mistrik M, Martincova I, Pialek J, Forejt J. X chromosome control of meiotic chromosome synapsis in mouse inter-subspecific hybrids. PLoS Genetics. 2014;10:e1004088. doi: 10.1371/journal.pgen.1004088. PubMed DOI PMC
Carofiglio F, Sleddens-Linkels E, Wassenaar E, Inagaki A, van Cappellen WA, Grootegoed JA, Toth A, Baarends WM. Repair of exogenous DNA double-strand breaks promotes chromosome synapsis in SPO11-mutant mouse meiocytes, and is altered in the absence of HORMAD1. DNA Repair. 2018;63:25–38. doi: 10.1016/j.dnarep.2018.01.007. PubMed DOI
Chan Y-L, Zhang A, Weissman BP, Bishop DK. RPA resolves conflicting activities of accessory proteins during reconstitution of Dmc1-mediated meiotic recombination. Nucleic Acids Research. 2018;88 doi: 10.1093/nar/gky1160. PubMed DOI PMC
Davies B, Hatton E, Altemose N, Hussin JG, Pratto F, Zhang G, Hinch AG, Moralli D, Biggs D, Diaz R, Preece C, Li R, Bitoun E, Brick K, Green CM, Camerini-Otero RD, Myers SR, Donnelly P. Re-engineering the zinc fingers of PRDM9 reverses hybrid sterility in mice. Nature. 2016;530:171–176. doi: 10.1038/nature16931. PubMed DOI PMC
Dzur-Gejdosova M, Simecek P, Gregorova S, Bhattacharyya T, Forejt J. Dissecting the genetic architecture of F1 hybrid sterility in house mice. Evolution. 2012;66:3321–3335. doi: 10.1111/j.1558-5646.2012.01684.x. PubMed DOI
Eram MS, Bustos SP, Lima-Fernandes E, Siarheyeva A, Senisterra G, Hajian T, Chau I, Duan S, Wu H, Dombrovski L, Schapira M, Arrowsmith CH, Vedadi M. Trimethylation of histone H3 lysine 36 by human methyltransferase PRDM9 protein. Journal of Biological Chemistry. 2014;289:12177–12188. doi: 10.1074/jbc.M113.523183. PubMed DOI PMC
Faieta M, Di Cecca S, de Rooij DG, Luchetti A, Murdocca M, Di Giacomo M, Di Siena S, Pellegrini M, Rossi P, Barchi M. A surge of late-occurring meiotic double-strand breaks rescues synapsis abnormalities in spermatocytes of mice with hypomorphic expression of SPO11. Chromosoma. 2016;125:189–203. doi: 10.1007/s00412-015-0544-7. PubMed DOI PMC
Forejt J, Iványi P. Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.) Genetical Research. 1974;24:189–206. doi: 10.1017/S0016672300015214. PubMed DOI
Forejt J, Pialek J, Trachtulec Z. In: Hybrid Male Sterility Genes in the Mouse Subspecific Crosses. Macholan M, Baird S. J. E, Muclinger P, Pialek J, editors. Cambridge, United Kingdom: Cambridge University Press; 2012.
Frankenberg-Schwager M, Kirchermeier D, Greif G, Baer K, Becker M, Frankenberg D. Cisplatin-mediated DNA double-strand breaks in replicating but not in quiescent cells of the yeast Saccharomyces cerevisiae. Toxicology. 2005;212:175–184. doi: 10.1016/j.tox.2005.04.015. PubMed DOI
Goetz P, Chandley AC, Speed RM. Morphological and temporal sequence of meiotic prophase development at puberty in the male mouse. Journal of Cell Science. 1984;65:249–263. PubMed
Gregorova S, Gergelits V, Chvatalova I, Bhattacharyya T, Valiskova B, Fotopulosova V, Jansa P, Wiatrowska D, Forejt J. Modulation of Prdm9-controlled meiotic chromosome asynapsis overrides hybrid sterility in mice. eLife. 2018;7:e34282. doi: 10.7554/eLife.34282. PubMed DOI PMC
Grey C, Baudat F, de Massy B. PRDM9, a driver of the genetic map. PLOS Genetics. 2018;14:e1007479. doi: 10.1371/journal.pgen.1007479. PubMed DOI PMC
Hanneman WH, Legare ME, Sweeney S, Schimenti JC. Cisplatin increases meiotic crossing-over in mice. PNAS. 1997;94:8681–8685. doi: 10.1073/pnas.94.16.8681. PubMed DOI PMC
Inagaki A, Schoenmakers S, Baarends WM. DNA double strand break repair, chromosome synapsis and transcriptional silencing in meiosis. Epigenetics. 2010;5:255–266. doi: 10.4161/epi.5.4.11518. PubMed DOI
Johnsson A, Olsson C, Nygren O, Nilsson M, Seiving B, Cavallin-Stahl E. Pharmacokinetics and tissue distribution of cisplatin in nude mice: platinum levels and cisplatin-DNA adducts. Cancer Chemotherapy and Pharmacology. 1995;37:23–31. doi: 10.1007/BF00685625. PubMed DOI
Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S. Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes & Development. 2013;27:873–886. doi: 10.1101/gad.213652.113. PubMed DOI PMC
Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88:375–384. doi: 10.1016/S0092-8674(00)81876-0. PubMed DOI
Keeney S, Baudat F, Angeles M, Zhou ZH, Copeland NG, Jenkins NA, Manova K, Jasin M. A mouse homolog of the Saccharomyces cerevisiae meiotic recombination DNA transesterase Spo11p. Genomics. 1999;61:170–182. doi: 10.1006/geno.1999.5956. PubMed DOI
Kogo H, Tsutsumi M, Inagaki H, Ohye T, Kiyonari H, Kurahashi H. HORMAD2 is essential for synapsis surveillance during meiotic prophase via the recruitment of ATR activity. Genes to Cells. 2012;17:897–912. doi: 10.1111/gtc.12005. PubMed DOI
Lange J, Yamada S, Tischfield SE, Pan J, Kim S, Zhu X, Socci ND, Jasin M, Keeney S. The landscape of mouse meiotic double-strand break formation, processing, and repair. Cell. 2016;167:695–708. doi: 10.1016/j.cell.2016.09.035. PubMed DOI PMC
Lawrence KS, Tapley EC, Cruz VE, Li Q, Aung K, Hart KC, Schwartz TU, Starr DA, Engebrecht J. LINC complexes promote homologous recombination in part through inhibition of nonhomologous end joining. The Journal of Cell Biology. 2016;215:801–821. doi: 10.1083/jcb.201604112. PubMed DOI PMC
Li XC, Li X, Schimenti JC. Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genetics. 2007;3:e130. doi: 10.1371/journal.pgen.0030130. PubMed DOI PMC
Li R, Bitoun E, Altemose N, Davies RW, Davies B. A high-resolution map of non-crossover events in mice reveals impacts of genetic diversity on meiotic recombination. bioRxiv. 2018 doi: 10.1101/428987. PubMed DOI PMC
Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science. 2009;323:373–375. doi: 10.1126/science.1163601. PubMed DOI
Moens PB, Marcon E, Shore JS, Kochakpour N, Spyropoulos B. Initiation and resolution of interhomolog connections: crossover and non-crossover sites along mouse synaptonemal complexes. Journal of Cell Science. 2007;120:1017–1027. doi: 10.1242/jcs.03394. PubMed DOI
Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science. 2010;327:876–879. doi: 10.1126/science.1182363. PubMed DOI PMC
OAKBERG EF. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. American Journal of Anatomy. 1956;99:507–516. doi: 10.1002/aja.1000990307. PubMed DOI
Oud JL, de Jong JH, de Rooij DG. A sequential analysis of meiosis in the male mouse using a restricted spermatocyte population obtained by a hydroxyurea/triaziquone treatment. Chromosoma. 1979;71:237–248. doi: 10.1007/BF00292826. PubMed DOI
Pacheco S, Maldonado-Linares A, Marcet-Ortega M, Rojas C, Martínez-Marchal A, Fuentes-Lazaro J, Lange J, Jasin M, Keeney S, Fernández-Capetillo O, Garcia-Caldés M, Roig I. ATR is required to complete meiotic recombination in mice. Nature Communications. 2018;9:2622. doi: 10.1038/s41467-018-04851-z. PubMed DOI PMC
Paigen K, Petkov PM. PRDM9 and its role in genetic recombination. Trends in Genetics. 2018;34:291–300. doi: 10.1016/j.tig.2017.12.017. PubMed DOI PMC
Parvanov ED, Petkov PM, Paigen K. Prdm9 controls activation of mammalian recombination hotspots. Science. 2010;327:835. doi: 10.1126/science.1181495. PubMed DOI PMC
Powers NR, Parvanov ED, Baker CL, Walker M, Petkov PM, Paigen K. The meiotic recombination activator PRDM9 trimethylates both H3K36 and H3K4 at recombination hotspots in vivo. PLOS Genetics. 2016;12:e1006146. doi: 10.1371/journal.pgen.1006146. PubMed DOI PMC
Ribeiro J, Abby E, Livera G, Martini E. RPA homologs and ssDNA processing during meiotic recombination. Chromosoma. 2016;125:265–276. doi: 10.1007/s00412-015-0552-7. PubMed DOI PMC
Rinaldi VD, Bolcun-Filas E, Kogo H, Kurahashi H, Schimenti JC. The DNA damage checkpoint eliminates mouse oocytes with chromosome synapsis failure. Molecular Cell. 2017;67:1026–1036. doi: 10.1016/j.molcel.2017.07.027. PubMed DOI PMC
Romanienko PJ, Camerini-Otero RD. The mouse Spo11 gene is required for meiotic chromosome synapsis. Molecular Cell. 2000;6:975–987. doi: 10.1016/S1097-2765(00)00097-6. PubMed DOI
Salic A, Mitchison TJ. A chemical method for fast and sensitive detection of DNA synthesis in vivo. PNAS. 2008;105:2415–2420. doi: 10.1073/pnas.0712168105. PubMed DOI PMC
Schimenti J. Synapsis or silence. Nature Genetics. 2005;37:11–13. doi: 10.1038/ng0105-11. PubMed DOI
Smagulova F, Brick K, Pu Y, Camerini-Otero RD, Petukhova GV. The evolutionary turnover of recombination hot spots contributes to speciation in mice. Genes & Development. 2016;30:266–280. doi: 10.1101/gad.270009.115. PubMed DOI PMC
Storchová R, Gregorová S, Buckiová D, Kyselová V, Divina P, Forejt J. Genetic analysis of X-linked hybrid sterility in the house mouse. Mammalian Genome. 2004;15:515–524. doi: 10.1007/s00335-004-2386-0. PubMed DOI
Wang Y, Putnam CD, Kane MF, Zhang W, Edelmann L, Russell R, Carrión DV, Chin L, Kucherlapati R, Kolodner RD, Edelmann W. Mutation in Rpa1 results in defective DNA double-strand break repair, chromosomal instability and cancer in mice. Nature Genetics. 2005;37:750–755. doi: 10.1038/ng1587. PubMed DOI
Wojtasz L, Cloutier JM, Baumann M, Daniel K, Varga J, Fu J, Anastassiadis K, Stewart AF, Reményi A, Turner JM, Tóth A. Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms. Genes & Development. 2012;26:958–973. doi: 10.1101/gad.187559.112. PubMed DOI PMC
Yamada S, Kim S, Tischfield SE, Jasin M, Lange J, Keeney S. Genomic and chromatin features shaping meiotic double-strand break formation and repair in mice. Cell Cycle. 2017;16:1870–1884. doi: 10.1080/15384101.2017.1361065. PubMed DOI PMC
Zickler D, Kleckner N. Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harbor Perspectives in Biology. 2015;7:a016626. doi: 10.1101/cshperspect.a016626. PubMed DOI PMC
Genic and chromosomal components of Prdm9-driven hybrid male sterility in mice (Mus musculus)
Chromosome-wide characterization of meiotic noncrossovers (gene conversions) in mouse hybrids
Prdm9 Intersubspecific Interactions in Hybrid Male Sterility of House Mouse
Genomic Structure of Hstx2 Modifier of Prdm9-Dependent Hybrid Male Sterility in Mice