The SMC-5/6 Complex and the HIM-6 (BLM) Helicase Synergistically Promote Meiotic Recombination Intermediate Processing and Chromosome Maturation during Caenorhabditis elegans Meiosis

PLoS Genetics

Volumn 12, Issue 3, 2016, Pages

  Hong, Ye ^a   Sonneville, Remi ^a   Agostinho, Ana ^a,b   Meier, Bettina ^a   Wang, Bin ^a   Blow, J Julian ^a   Gartner, Anton ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOM SYNDROME HELICASE; BRCA1 PROTEIN; CHROMOSOME PROTEIN; CONDENSIN; PROTEIN HIM 6; PROTEIN SMC 5; PROTEIN SMC 6; UNCLASSIFIED DRUG; BRC-1 PROTEIN, C ELEGANS; CAENORHABDITIS ELEGANS PROTEIN; CELL CYCLE PROTEIN; HIM-6 PROTEIN, C ELEGANS; MULTIPROTEIN COMPLEX; SMC-5 PROTEIN, C ELEGANS; SMC-6 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; CHROMOSOME CONDENSATION; CHROMOSOME MATURATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; COMPLEX FORMATION; CONTROLLED STUDY; CROSSING OVER; GENE DELETION; GENETIC CONSERVATION; GENETIC REGULATION; MEIOTIC RECOMBINATION; NONHUMAN; ORTHOLOGY; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; ANIMAL; CHROMOSOME; GENETIC RECOMBINATION; GENETICS; HUMAN; MEIOSIS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CHROMOSOMES; HUMANS; MEIOSIS; MULTIPROTEIN COMPLEXES; RECOMBINATION, GENETIC;

EID: 84962172425     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005872     Document Type: Article

References (93)

1. Mimitou EP, Symington LS, (2009) Nucleases and helicases take center stage in homologous recombination. Trends Biochem Sci34: 264–272. doi: 10.1016/j.tibs.2009.01.01019375328
2. Baudat F, Imai Y, de Massy B, (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet14: 794–806. doi: 10.1038/nrg357324136506
3. Keeney S, Giroux CN, Kleckner N, (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell88: 375–384. 9039264
4. Humphryes N, Hochwagen A, (2014) A non-sister act: Recombination template choice during meiosis. Exp Cell Res329: 53–60. doi: 10.1016/j.yexcr.2014.08.02425158281
5. Phadnis N, Hyppa RW, Smith GR, (2011) New and old ways to control meiotic recombination. Trends Genet27: 411–421. doi: 10.1016/j.tig.2011.06.00721782271
6. Pradillo M, Santos JL, (2011) The template choice decision in meiosis: is the sister important?Chromosoma120: 447–454. doi: 10.1007/s00412-011-0336-721826413
7. Goldfarb T, Lichten M, (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol8: e1000520. doi: 10.1371/journal.pbio.100052020976044
8. Rosu S, Libuda DE, Villeneuve AM, (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science334: 1286–1289. doi: 10.1126/science.121242422144627
9. Couteau F, Zetka M, (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev cell20: 353–363. doi: 10.1016/j.devcel.2011.01.01521397846
10. Adamo A, Montemauri P, Silva N, Ward JD, Boulton SJ, et al. (2008) BRC-1 acts in the inter-sister pathway of meiotic double-strand break repair. EMBO Rep9: 287–292. doi: 10.1038/sj.embor.740116718219312
11. Bellendir SP, Sekelsky J, (2013) An elegans Solution for Crossover Formation. PLoS Genet9: e1003658. doi: 10.1371/journal.pgen.100365823874241
12. Zakharyevich K, Tang S, Ma Y, Hunter N, (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell149: 334–347. doi: 10.1016/j.cell.2012.03.02322500800
13. Matos J, Blanco MG, Maslen S, Skehel JM, West SC, (2011) Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell147: 158–172. doi: 10.1016/j.cell.2011.08.03221962513
14. Ip SC, Rass U, Blanco MG, Flynn HR, Skehel JM, et al. (2008) Identification of Holliday junction resolvases from humans and yeast. Nature456: 357–361. doi: 10.1038/nature0747019020614
15. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen J, et al. (2012) BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol Cell46: 43–53. doi: 10.1016/j.molcel.2012.02.02022500736
16. Agostinho A, Meier B, Sonneville R, Jagut M, Woglar A, et al. (2013) Combinatorial regulation of meiotic holliday junction resolution in C. elegans by HIM-6 (BLM) helicase, SLX-4, and the SLX-1, MUS-81 and XPF-1 nucleases. PLoS Genet9: e1003591. doi: 10.1371/journal.pgen.100359123901331
17. O'Neil NJ, Martin JS, Youds JL, Ward JD, Petalcorin MI, et al. (2013) Joint molecule resolution requires the redundant activities of MUS-81 and XPF-1 during Caenorhabditis elegans meiosis. PLoS Genet9: e1003582. doi: 10.1371/journal.pgen.100358223874209
18. Saito TT, Lui DY, Kim HM, Meyer K, Colaiacovo MP, (2013) Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLoS Genet9: e1003586. doi: 10.1371/journal.pgen.100358623874210
19. De Piccoli G, Torres-Rosell J, Aragon L, (2009) The unnamed complex: what do we know about Smc5-Smc6?Chromosome Res17: 251–263. doi: 10.1007/s10577-008-9016-819308705
20. Cobbe N, Heck MM, (2004) The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol Biol Evol21: 332–347. 14660695
21. Jeppsson K, Kanno T, Shirahige K, Sjogren C, (2014) The maintenance of chromosome structure: positioning and functioning of SMC complexes. Nat Rev Mol Cell Biol15: 601–614. doi: 10.1038/nrm385725145851
22. Losada A, Hirano T, (2005) Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev19: 1269–1287. 15937217
23. Fujioka Y, Kimata Y, Nomaguchi K, Watanabe K, Kohno K, (2002) Identification of a novel non-structural maintenance of chromosomes (SMC) component of the SMC5-SMC6 complex involved in DNA repair. J Biol Chem277: 21585–21591. 11927594
24. Kegel A, Sjogren C, (2010) The Smc5/6 complex: more than repair?Cold Spring Harb Symp Quant Biol75: 179–187. doi: 10.1101/sqb.2010.75.04721467147
25. Andrews EA, Palecek J, Sergeant J, Taylor E, Lehmann AR, et al. (2005) Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol Cell Biol25: 185–196. 15601841
26. Potts PR, Yu H, (2005) Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol Cell Biol25: 7021–7032. 16055714
27. Onoda F, Takeda M, Seki M, Maeda D, Tajima J, et al. (2004) SMC6 is required for MMS-induced interchromosomal and sister chromatid recombinations in Saccharomyces cerevisiae. DNA repair3: 429–439. 15010319
28. Murray JM, Carr AM, (2008) Smc5/6: a link between DNA repair and unidirectional replication?Nat Rev Mol Cell Biol9: 177–182. 18059412
29. Gomez R, Jordan PW, Viera A, Alsheimer M, Fukuda T, et al. (2013) Dynamic localization of SMC5/6 complex proteins during mammalian meiosis and mitosis suggests functions in distinct chromosome processes. J Cell Sci126: 4239–4252. doi: 10.1242/jcs.13019523843628
30. Verver DE, van Pelt AM, Repping S, Hamer G, (2013) Role for rodent Smc6 in pericentromeric heterochromatin domains during spermatogonial differentiation and meiosis. Cell Death Dis4: e749. doi: 10.1038/cddis.2013.26923907463
31. Verver DE, Langedijk NS, Jordan PW, Repping S, Hamer G, (2014) The SMC5/6 complex is involved in crucial processes during human spermatogenesis. Biol Reprod91: 22. doi: 10.1095/biolreprod.114.11859624855106
32. Copsey A, Tang S, Jordan PW, Blitzblau HG, Newcombe S, et al. (2013) Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions. PLoS Genet9: e1004071. doi: 10.1371/journal.pgen.100407124385939
33. Lilienthal I, Kanno T, Sjogren C, (2013) Inhibition of the Smc5/6 complex during meiosis perturbs joint molecule formation and resolution without significantly changing crossover or non-crossover levels. PLoS Genet9: e1003898. doi: 10.1371/journal.pgen.100389824244180
34. Xaver M, Huang L, Chen D, Klein F, (2013) Smc5/6-Mms21 prevents and eliminates inappropriate recombination intermediates in meiosis. PLoS Genet9: e1004067. doi: 10.1371/journal.pgen.100406724385936
35. Wehrkamp-Richter S, Hyppa RW, Prudden J, Smith GR, Boddy MN, (2012) Meiotic DNA joint molecule resolution depends on Nse5-Nse6 of the Smc5-Smc6 holocomplex. Nucleic Acids Res40: 9633–9646. doi: 10.1093/nar/gks71322855558
36. Huen MS, Sy SM, Chen J, (2010) BRCA1 and its toolbox for the maintenance of genome integrity. Nat Rev Mol Cell Biol11: 138–148. doi: 10.1038/nrm283120029420
37. Scully R, Chen J, Plug A, Xiao Y, Weaver D, et al. (1997) Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell88: 265–275. 9008167
38. Broering TJ, Alavattam KG, Sadreyev RI, Ichijima Y, Kato Y, et al. (2014) BRCA1 establishes DNA damage signaling and pericentric heterochromatin of the X chromosome in male meiosis. J Cell Biol205: 663–675. doi: 10.1083/jcb.20131105024914237
39. Xu X, Aprelikova O, Moens P, Deng CX, Furth PA, (2003) Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice. Development130: 2001–2012. 12642502
40. Klein HL, Symington LS, (2012) Sgs1—the maestro of recombination. Cell149: 257–259. doi: 10.1016/j.cell.2012.03.02022500794
41. Wicky C, Alpi A, Passannante M, Rose A, Gartner A, et al. (2004) Multiple genetic pathways involving the Caenorhabditis elegans Bloom's syndrome genes him-6, rad-51, and top-3 are needed to maintain genome stability in the germ line. Mol Cell Biol24: 5016–5027. 15143192
42. Grabowski MM, Svrzikapa N, Tissenbaum HA, (2005) Bloom syndrome ortholog HIM-6 maintains genomic stability in C. elegans. Mech Ageing Dev126: 1314–1321. 16181657
43. Bickel JS, Chen L, Hayward J, Yeap SL, Alkers AE, et al. (2010) Structural maintenance of chromosomes (SMC) proteins promote homolog-independent recombination repair in meiosis crucial for germ cell genomic stability. PLoS Genet6: e1001028. doi: 10.1371/journal.pgen.100102820661436
44. Alpi A, Pasierbek P, Gartner A, Loidl J, (2003) Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma112: 6–16. 12684824
45. Smolikov S, Eizinger A, Hurlburt A, Rogers E, Villeneuve AM, et al. (2007) Synapsis-defective mutants reveal a correlation between chromosome conformation and the mode of double-strand break repair during Caenorhabditis elegans meiosis. Genetics176: 2027–2033. 17565963
46. Severson AF, Ling L, van Zuylen V, Meyer BJ, (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev23: 1763–1778. doi: 10.1101/gad.180880919574299
47. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM, (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev16: 2428–2442. 12231631
48. Bhalla N, Wynne DJ, Jantsch V, Dernburg AF, (2008) ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet4: e1000235. doi: 10.1371/journal.pgen.100023518949042
49. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, et al. (2012) COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell149: 75–87. doi: 10.1016/j.cell.2012.01.05222464324
50. Hillers KJ, Villeneuve AM, (2009) Analysis of meiotic recombination in Caenorhabditis elegans. Methods Mol Biol557: 77–97. doi: 10.1007/978-1-59745-527-5_719799178
51. Davis MW, Hammarlund M, Harrach T, Hullett P, Olsen S, et al. (2005) Rapid single nucleotide polymorphism mapping in C. elegans. BMC Genomics6: 118. 16156901
52. Rockman MV, Kruglyak L, (2009) Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet5: e1000419. doi: 10.1371/journal.pgen.100041919283065
53. Rose AM, Baillie DL, (1979) A mutation in Caenorhabditis elegans that increases recombination frequency more than threefold. Nature281: 599–600. 492325
54. Schvarzstein M, Pattabiraman D, Libuda DE, Ramadugu A, Tam A, et al. (2014) DNA helicase HIM-6/BLM both promotes MutSgamma-dependent crossovers and antagonizes MutSgamma-independent interhomolog associations during caenorhabditis elegans meiosis. Genetics198: 193–207. doi: 10.1534/genetics.114.16151325053665
55. Zetka MC, Rose AM, (1995) Mutant rec-1 eliminates the meiotic pattern of crossing over in Caenorhabditis elegans. Genetics141: 1339–1349. 8601478
56. Jagut M, Hamminger P, Woglar A, Millonigg S, Paulin L, Mikl M, et al. (2016) Separable roles for a C. elegans RMI1 homolog in promoting and antagonizing meiotic crossovers ensure faithful chromosome inheritance. PLoS Biol14(3): e1002412.
57. Nabeshima K, Villeneuve AM, Colaiacovo MP, (2005) Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J Cell Biol168: 683–689. 15738262
58. Zetka MC, Kawasaki I, Strome S, Muller F, (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev13: 2258–2270. 10485848
59. Matos J, Blanco MG, West SC, (2013) Cell-cycle kinases coordinate the resolution of recombination intermediates with chromosome segregation. Cell Rep4: 76–86. doi: 10.1016/j.celrep.2013.05.03923810555
60. Torres-Rosell J, Machin F, Farmer S, Jarmuz A, Eydmann T, et al. (2005) SMC5 and SMC6 genes are required for the segregation of repetitive chromosome regions. Nat Cell Biol7: 412–419. 15793567
61. Cheok CF, Bachrati CZ, Chan KL, Ralf C, Wu L, et al. (2005) Roles of the Bloom's syndrome helicase in the maintenance of genome stability. Biochem Soc Trans33: 1456–1459. 16246145
62. Shrivastav M, De Haro LP, Nickoloff JA, (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res18: 134–147. 18157161
63. Lemmens BB, Johnson NM, Tijsterman M, (2013) COM-1 promotes homologous recombination during Caenorhabditis elegans meiosis by antagonizing Ku-mediated non-homologous end joining. PLoS Genet9: e1003276. doi: 10.1371/journal.pgen.100327623408909
64. Meier B, Cooke SL, Weiss J, Bailly AP, Alexandrov LB, et al. (2014) C. elegans whole-genome sequencing reveals mutational signatures related to carcinogens and DNA repair deficiency. Genome Res24: 1624–1636. doi: 10.1101/gr.175547.11425030888
65. Lieber MR, (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem79: 181–211. doi: 10.1146/annurev.biochem.052308.09313120192759
66. Wolters S, Ermolaeva MA, Bickel JS, Fingerhut JM, Khanikar J, et al. (2014) Loss of Caenorhabditis elegans BRCA1 promotes genome stability during replication in smc-5 mutants. Genetics196: 985–999. doi: 10.1534/genetics.113.15829524424777
67. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet33: 603–754. 10690419
68. Hirano T, (2005) Condensins: organizing and segregating the genome. Curr Biol15: R265–275. 15823530
69. Stear JH, Roth MB, (2002) Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment. Genes Dev16: 1498–1508. 12080088
70. Chan RC, Severson AF, Meyer BJ, (2004) Condensin restructures chromosomes in preparation for meiotic divisions. J Cell Biol167: 613–625. 15557118
71. Serrentino ME, Borde V, (2012) The spatial regulation of meiotic recombination hotspots: are all DSB hotspots crossover hotspots?Exp cell Res318: 1347–1352. doi: 10.1016/j.yexcr.2012.03.02522487095
72. Terasawa M, Shinohara A, Hotta Y, Ogawa H, Ogawa T, (1995) Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev9: 925–934. 7774810
73. Moens PB, Chen DJ, Shen Z, Kolas N, Tarsounas M, et al. (1997) Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma106: 207–215. 9254722
74. Franklin AE, McElver J, Sunjevaric I, Rothstein R, Bowen B, et al. (1999) Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase. Plant Cell11: 809–824. 10330467
75. Buhler C, Borde V, Lichten M, (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol5: e324. doi: 10.1371/journal.pbio.006010418076285
76. Lemmens BB, Tijsterman M, (2011) DNA double-strand break repair in Caenorhabditis elegans. Chromosoma120: 1–21. doi: 10.1007/s00412-010-0296-321052706
77. Rockmill B, Fung JC, Branda SS, Roeder GS, (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol13: 1954–1962. 14614820
78. Cromie GA, Hyppa RW, Smith GR, (2008) The fission yeast BLM homolog Rqh1 promotes meiotic recombination. Genetics179: 1157–1167. doi: 10.1534/genetics.108.08895518562672
79. McVey M, Andersen SL, Broze Y, Sekelsky J, (2007) Multiple functions of Drosophila BLM helicase in maintenance of genome stability. Genetics176: 1979–1992. 17507683
80. Moens PB, Freire R, Tarsounas M, Spyropoulos B, Jackson SP, (2000) Expression and nuclear localization of BLM, a chromosome stability protein mutated in Bloom's syndrome, suggest a role in recombination during meiotic prophase. J Cell Sci113 (Pt 4): 663–672. 10652259
81. Croteau DL, Popuri V, Opresko PL, Bohr VA, (2014) Human RecQ helicases in DNA repair, recombination, and replication. Annu Rev Biochem83: 519–552. doi: 10.1146/annurev-biochem-060713-03542824606147
82. Manthei KA, Keck JL, (2013) The BLM dissolvasome in DNA replication and repair. Cellular and molecular life sciences: CMLS70: 4067–4084. doi: 10.1007/s00018-013-1325-123543275
83. Wagner CR, Kuervers L, Baillie DL, Yanowitz JL, (2010) xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature467: 839–843. doi: 10.1038/nature0942920944745
84. Saito TT, Mohideen F, Meyer K, Harper JW, Colaiacovo MP, (2012) SLX-1 is required for maintaining genomic integrity and promoting meiotic noncrossovers in the Caenorhabditis elegans germline. PLoS Genet8: e1002888. doi: 10.1371/journal.pgen.100288822927825
85. Meneely PM, McGovern OL, Heinis FI, Yanowitz JL, (2012) Crossover distribution and frequency are regulated by him-5 in Caenorhabditis elegans. Genetics190: 1251–1266. doi: 10.1534/genetics.111.13746322267496
86. Chung G, Rose AM, Petalcorin MI, Martin JS, Kessler Z, et al. (2015) REC-1 and HIM-5 distribute meiotic crossovers and function redundantly in meiotic double-strand break formation in Caenorhabditis elegans. Genes Dev29: 1969–1979. doi: 10.1101/gad.266056.11526385965
87. Gallego-Paez LM, Tanaka H, Bando M, Takahashi M, Nozaki N, et al. (2014) Smc5/6-mediated regulation of replication progression contributes to chromosome assembly during mitosis in human cells. Mol Biol Cell25: 302–317. doi: 10.1091/mbc.E13-01-002024258023
88. Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, et al. (2008) Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev22: 194–211. doi: 10.1101/gad.161850818198337
89. Mets DG, Meyer BJ, (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell139: 73–86. doi: 10.1016/j.cell.2009.07.03519781752
90. Rinaldo C, Bazzicalupo P, Ederle S, Hilliard M, La Volpe A, (2002) Roles for Caenorhabditis elegans rad-51 in meiosis and in resistance to ionizing radiation during development. Genetics160: 471–479. 11861554
91. Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, et al. (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell130: 259–272. 17662941
92. Kaur H, De Muyt A, Lichten M, (2015) Top3-Rmi1 DNA single-strand decatenase is integral to the formation and resolution of meiotic recombination intermediates. Mol Cell57: 583–594. doi: 10.1016/j.molcel.2015.01.02025699707
93. Timmons L, Court DL, Fire A, (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene263: 103–112. 11223248