Pseudosynapsis and decreased stringency of meiotic repair pathway choice on the hemizygous sex chromosome of Caenorhabditis elegans males

Genetics

Volumn 197, Issue 2, 2014, Pages 543-560

  Checchi, Paula M ^a,b   Lawrence, Katherine S ^a   Van, Mike V ^a   Larson, Braden J ^a   Engebrecht, Joanne ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MARIST COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; COHESIN; RAD51 PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; NUCLEAR PROTEIN; RAD-51 PROTEIN, C ELEGANS; SYP-1 PROTEIN, C ELEGANS;

ANIMAL CELL; ARTICLE; AUTOSOME; CAENORHABDITIS ELEGANS; CHROMOSOME PAIRING; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEEDBACK SYSTEM; FLUORESCENCE IN SITU HYBRIDIZATION; GERM LINE; HEMIZYGOSITY; HERMAPHRODITE; HOMOLOGOUS RECOMBINATION; MALE; MEIOSIS; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROPHASE; RNA INTERFERENCE; SEX CHROMOSOME; SISTER CHROMATID; SPERMATOCYTE; X CHROMOSOME; ANIMAL; CHROMOSOME SEGREGATION; CROSSING OVER; GENETICS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; MALE; MEIOSIS; NUCLEAR PROTEINS; RAD51 RECOMBINASE; X CHROMOSOME;

EID: 84902532303     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.164152     Document Type: Article

References (90)

1. Agostinho, A., B. Meier, R. Sonneville, M. Jagut, A. Woglar 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 Genet. 9: e1003591.
2. Aguilera, A., and T. Garcia-Muse, 2013 Causes of genome instability. Annu. Rev. Genet. 47: 1-32.
3. Al-Minawi, A. Z., N. Saleh-Gohari, and T. Helleday, 2008 The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res. 36: 1-9.
4. Albertson, D. G., and J. N. Thomson, 1993 Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1: 15-26.
5. Ashley, T., A. W. Plug, J. Xu, A. J. Solari, G. Reddy et al., 1995 Dynamic changes in Rad51 distribution on chromatin during meiosis in male and female vertebrates. Chromosoma 104: 19-28.
6. Barchi, M., I. Roig, M. Di Giacomo, D. G. de Rooij, S. Keeney et al., 2008 ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes. PLoS Genet. 4: e1000076.
7. Bean, C. J., C. E. Schaner, and W. G. Kelly, 2004 Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat. Genet. 36: 100-105.
8. Bessler, J. B., E. C. Andersen, and A. M. Villeneuve, 2010 Differential localization and independent acquisition of the H3K9me2 and H3K9me3 chromatin modifications in the Caenorhabditis elegans adult germ line. PLoS Genet. 6: e1000830.
9. Bickel, J. S., L. Chen, J. Hayward, S. L. Yeap, A. E. Alkers et al., 2010 Structural maintenance of chromosomes (SMC) proteins promote homolog-independent recombination repair in meiosis crucial for germ cell genomic stability. PLoS Genet. 6: e1001028.
10. Brenner, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
11. C. elegans Sequencing Consortium, 1998 Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282: 2012-2018.
12. Carballo, J. A., S. Panizza, M. E. Serrentino, A. L. Johnson, M. Geymonat et al., 2013 Budding yeast ATM/ATR control meiotic double-strand break (DSB) levels by down-regulating Rec114, an essential component of the DSB-machinery. PLoS Genet. 9: e1003545.
13. Checchi, P. M., and J. Engebrecht, 2011 Caenorhabditis elegans histone methyltransferase MET-2 shields the male X chromosome from checkpoint machinery and mediates meiotic sex chromosome inactivation. PLoS Genet. 7: e1002267.
14. Clejan, I., J. Boerckel, and S. Ahmed, 2006 Developmental modulation of nonhomologous end joining in Caenorhabditis elegans. Genetics 173: 1301-1317.
15. Colaiacovo, M. P., A. J. MacQueen, E. Martinez-Perez, K. McDonald, A. Adamo et al., 2003 Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell 5: 463-474.
16. Couteau, F., and M. Zetka, 2005 HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 19: 2744-2756.
17. Couteau, F., K. Nabeshima, A. Villeneuve, and M. Zetka, 2004 A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr. Biol. 14: 585-592.
18. Darby, R. A., and A. V. Hine, 2005 LacI-mediated sequencespecific affinity purification of plasmid DNA for therapeutic applications. FASEB J. 19: 801-803.
19. Dernburg, A. F., K. McDonald, G. Moulder, R. Barstead, M. Dresser et al., 1998 Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.
20. Fiorenza, M. T., A. Bevilacqua, S. Bevilacqua, and F. Mangia, 2001 Growing dictyate oocytes, but not early preimplantation embryos, of the mouse display high levels of DNA homologous recombination by single-strand annealing and lack DNA nonhomologous end joining. Dev. Biol. 233: 214-224.
21. Garcia, V., S. E. Phelps, S. Gray, and M. J. Neale, 2011 Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature 479: 241-244.
22. Giroux, C. N., M. E. Dresser, and H. F. Tiano, 1989 Genetic control of chromosome synapsis in yeast meiosis. Genome 31: 88-94.
23. Goldfarb, T., and M. Lichten, 2010 Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol. 8: e1000520.
24. Gonzalez-Serricchio, A. S., and P. W. Sternberg, 2006 Visualization of C. elegans transgenic arrays by GFP. BMC Genet. 7: 36.
25. Goodyer, W., S. Kaitna, F. Couteau, J. D. Ward, S. J. Boulton et al., 2008 HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell 14: 263-274.
26. Harper, N. C., R. Rillo, S. Jover-Gil, Z. J. Assaf, N. Bhalla et al., 2011 Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev. Cell 21: 934-947.
27. Hayashi, M., G. M. Chin, and A. M. Villeneuve, 2007 C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet. 3: e191.
28. Ho, H. C., and S. M. Burgess, 2011 Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis. PLoS Genet. 7: e1002351.
29. Hodgkin, J., 1986 Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 114: 15-52.
30. Holloman, W. K., 2011 Unraveling the mechanism of BRCA2 in homologous recombination. Nat. Struct. Mol. Biol. 18: 748-754.
31. Hong, S., Y. Sung, M. Yu, M. Lee, N. Kleckner et al., 2013 The logic and mechanism of homologous recombination partner choice. Mol. Cell 51: 440-453.
32. Jaramillo-Lambert, A., M. Ellefson, A. M. Villeneuve, and J. Engebrecht, 2007 Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev. Biol. 308: 206-221.
33. Jaramillo-Lambert, A., and J. Engebrecht, 2010 A single unpaired and transcriptionally silenced X chromosome locally precludes checkpoint signaling in the Caenorhabditis elegans germ line. Genetics 184: 613-628.
34. Jaramillo-Lambert, A., Y. Harigaya, J. Vitt, A. Villeneuve, and J. Engebrecht, 2010 Meiotic errors activate checkpoints that improve gamete quality without triggering apoptosis in male germ cells. Curr. Biol. 20: 2078-2089.
35. Joyce, E. F., A. Paul, K. E. Chen, N. Tanneti, and K. S. McKim, 2012 Multiple barriers to nonhomologous DNA end joining during meiosis in Drosophila. Genetics 191: 739-746.
36. Kamath, R. S., and J. Ahringer, 2003 Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
37. Kauppi, L., M. Barchi, F. Baudat, P. J. Romanienko, S. Keeney et al., 2011 Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331: 916-920.
38. Kauppi, L., M. Barchi, J. Lange, F. Baudat, M. Jasin et al., 2013 Numerical constraints and feedback control of doublestrand breaks in mouse meiosis. Genes Dev. 27: 873-886.
39. Keeney, S., C. N. Giroux, and N. Kleckner, 1997 Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
40. Kelly, W. G., C. E. Schaner, A. F. Dernburg, M. H. Lee, S. K. Kim et al., 2002 X-chromosome silencing in the germline of C. elegans. Development 129: 479-492.
41. Kim, K. P., B. M. Weiner, L. Zhang, A. Jordan, J. Dekker et al., 2010 Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924-937.
42. Lange, J., H. Skaletsky, S. K. van Daalen, S. L. Embry, C. M. Korver et al., 2009 Isodicentric Y chromosomes and sex disorders as byproducts of homologous recombination that maintains palindromes. Cell 138: 855-869.
43. Lee, M. H., M. Ohmachi, S. Arur, S. Nayak, R. Francis et al., 2007 Multiple functions and dynamic activation of MPK-1 extracellular signal-regulated kinase signaling in Caenorhabditis elegans germline development. Genetics 177: 2039-2062.
44. Lemmens, B. B., N. M. Johnson, and M. Tijsterman, 2013 COM-1 promotes homologous recombination during Caenorhabditis elegans meiosis by antagonizing Ku-mediated non-homologous end joining. PLoS Genet. 9: e1003276.
45. Liu, H., J. K. Jang, N. Kato, and K. S. McKim, 2002 mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster. Genetics 162: 245-258.
46. MacQueen, A. J., M. P. Colaiacovo, K. McDonald, and A. M. Villeneuve, 2002 Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 16: 2428-2442.
47. Manfrini, N., I. Guerini, A. Citterio, G. Lucchini, and M. P. Longhese, 2010 Processing of meiotic DNA double strand breaks requires cyclin-dependent kinase and multiple nucleases. J. Biol. Chem. 285: 11628-11637.
48. Martin, J. S., N. Winkelmann, M. I. Pet-aletal/et-alcorin, M. J. McIlwraith, and S. J. Boulton, 2005 RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair. Mol. Cell. Biol. 25: 3127-3139.
49. Martinez-Perez, E., and A. M. Villeneuve, 2005 HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 19: 2727-2743.
50. McKee, B. D., and M. A. Handel, 1993 Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102: 71-80.
51. Mets, D. G., and B. J. Meyer, 2009 Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139: 73-86.
52. Moens, P. B., D. J. Chen, Z. Shen, N. Kolas, M. Tarsounas et al., 1997 Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106: 207-215.
53. Nabeshima, K., A. M. Villeneuve, and M. P. Colaiacovo, 2005 Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J. Cell Biol. 168: 683-689.
54. Niu, H., L. Wan, B. Baumgartner, D. Schaefer, J. Loidl et al., 2005 Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol. Biol. Cell 16: 5804-5818.
55. Niu, H., L. Wan, V. Busygina, Y. Kwon, J. A. Allen et al., 2009 Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol. Cell 36: 393-404.
56. O'Neil, N. J., J. S. Martin, J. L. Youds, J. D. Ward, M. I. Petalcorin et al., 2013 Joint molecule resolution requires the redundant activities of MUS-81 and XPF-1 during Caenorhabditis elegans meiosis. PLoS Genet. 9: e1003582.
57. Page, J., R. de la Fuente, R. Gomez, A. Calvente, A. Viera et al., 2006a Sex chromosomes, synapsis, and cohesins: a complex affair. Chromosoma 115: 250-259.
58. Page, J., A. Viera, M. T. Parra, R. de la Fuente, J. A. Suja et al., 2006b Involvement of synaptonemal complex proteins in sex chromosome segregation during marsupial male meiosis. PLoS Genet. 2: e136.
59. Pasierbek, P., M. Jantsch, M. Melcher, A. Schleiffer, D. Schweizer et al., 2001 A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 15: 1349-1360.
60. Phillips, C. M., and A. F. Dernburg, 2006 A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev. Cell 11: 817-829.
61. Pontier, D. B., and M. Tijsterman, 2009 A robust network of double-strand break repair pathways governs genome integrity during C. elegans development. Curr. Biol. 19: 1384-1388.
62. Romanienko, P. J., and R. D. Camerini-Otero, 2000 The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol. Cell 6: 975-987.
63. Rosu, S., K. A. Zawadzki, E. L. Stamper, D. E. Libuda, A. L. Reese et al., 2013 The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotescrossover assurance. PLoS Genet. 9: e1003674.
64. Saito, T. T., J. L. Youds, S. J. Boulton, and M. P. Colaiacovo, 2009 Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet. 5: e1000735.
65. Saito, T. T., D. Y. Lui, H. M. Kim, K. Meyer, and M. P. Colaiacovo, 2013 Interplay between structure-specific endonucleases for crossover control during Caenorhabditis elegans meiosis. PLoS Genet. 9: e1003586.
66. Schedl, T., and J. Kimble, 1988 fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119: 43-61.
67. Schvarzstein, M., S. M. Wignall, and A. M. Villeneuve, 2010 Coordinating cohesion, co-orientation, and congression during meiosis: lessons from holocentric chromosomes. Genes Dev. 24: 219-228.
68. Sciurano, R. B., M. I. Rahn, M. I. Pigozzi, S. B. Olmedo, and A. J. Solari, 2006 An azoospermic man with a double-strand DNA break-processing deficiency in the spermatocyte nuclei: case report. Hum. Reprod. 21: 1194-1203.
69. Severson, A. F., L. Ling, V. van Zuylen, and B. J. Meyer, 2009 The axial element protein TP-3 promotes cohesion loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev. 23: 1763-1778.
70. Shakes, D. C., J. C. Wu, P. L. Sadler, K. Laprade, L. L. Moore et al., 2009 Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet. 5: e1000611.
71. Shi, Q., E. Spriggs, L. L. Field, E. Ko, L. Barclay et al., 2001 Single sperm typing demonstrates that reduced recombination is associated with the production of aneuploid 24,XY human sperm. Am. J. Med. Genet. 99: 34-38.
72. Shin, Y. H., M. M. McGuire, and A. Rajkovic, 2013 Mouse HORMAD1 is a meiosis I checkpoint protein that modulates DNA doublestrand break repair during female meiosis. Biol. Reprod. 89: 29.
73. Smolikov, S., K. Schild-Prufert, and M. P. Colaiacovo, 2008 CRA-1 uncovers a double-strand break-dependent pathway promoting the assembly of central region proteins on chromosome axes during C. elegans meiosis. PLoS Genet. 4: e1000088.
74. Solinger, J. A., K. Kiianitsa, and W. D. Heyer, 2002 Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol. Cell 10: 1175-1188.
75. Sonneville, R., M. Querenet, A. Craig, A. Gartner, and J. J. Blow, 2012 The dynamics of replication licensing in live Caenorhabditis elegans embryos. J. Cell Biol. 196: 233-246.
76. Stamper, E. L., S. E. Rodenbusch, S. Rosu, J. Ahringer, A. M. Villeneuve et al., 2013 Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet. 9: e1003679.
77. Stergiou, L., R. Eberhard, K. Doukoumetzidis, and M. O. Hengartner, 2011 NER and HR pathways act sequentially to promote UV-Cinduced germ cell apoptosis in Caenorhabditis elegans. Cell Death Differ. 18: 897-906.
78. Terasawa, M., T. Ogawa, Y. Tsukamoto, and H. Ogawa, 2008 Sae2p phosphorylation is crucial for cooperation with Mre11p for resection of DNA double-strand break ends during meiotic recombination in Saccharomyces cerevisiae. Genes Genet. Syst. 83: 209-217.
79. Timmons, L., D. L. Court, and A. Fire, 2001 Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112.
80. Turner, J. M., 2007 Meiotic sex chromosome inactivation. Development 134: 1823-1831.
81. Tzur, Y. B., C. Egydio de Carvalho, S. Nadarajan, I. Van Bostelen, Y. Gu et al., 2012 LAB-1 targets PP1 and restricts Aurora B kinase upon entrance into meiosis to promote sister chromatid cohesion. PLoS Biol. 10: e1001378.
82. van Attikum, H., and S. M. Gasser, 2009 Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 19: 207-217.
83. Voelkel-Meiman, K., S. S. Moustafa, P. Lefrancois, A. M. Villeneuve, and A. J. MacQueen, 2012 Full-length synaptonemal complex grows continuously during meiotic prophase in budding yeast. PLoS Genet. 8: e1002993.
84. Woglar, A., A. Daryabeigi, A. Adamo, C. Habacher, T. Machacek et al., 2013 Matefin/SUN-1 phosphorylation is part of a surveillance mechanism to coordinate chromosome synapsis and recombination with meiotic progression and chromosome movement. PLoS Genet. 9: e1003335.
85. Yan, R., and B. D. McKee, 2013 The cohesion protein SOLO associates with SMC1 and is required for synapsis, recombination, homolog bias and cohesion and pairing of centromeres in Drosophila meiosis. PLoS Genet. 9: e1003637.
86. Yin, Y., and S. Smolikove, 2013 Impaired resection of meiotic double-strand breaks channels repair to nonhomologous end joining in Caenorhabditis elegans. Mol. Cell. Biol. 33: 2732-2747.
87. Yokoo, R., K. A. Zawadzki, K. Nabeshima, M. Drake, S. Arur et al., 2012 COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149: 75-87.
88. Zakharyevich, K., Y. Ma, S. Tang, P. Y. Hwang, S. Boiteux et al., 2010 Temporally and biochemically distinct activities of Exo1 during meiosis: double-strand break resection and resolution of double Holliday junctions. Mol. Cell 40: 1001-1015.
89. Zanetti, S., and A. Puoti, 2013 Sex determination in the Caenorhabditis elegans germline. Adv. Exp. Med. Biol. 757: 41-69.
90. Zhang, W., N. Miley, M. S. Zastrow, A. J. MacQueen, A. Sato et al., 2012 HAL-2 promotes homologous pairing during Caenorhabditis elegans meiosis by antagonizing inhibitory effects of synaptonemal complex precursors. PLoS Genet. 8: e1002880.