Meiotic recombination in Caenorhabditis elegans

Chromosome Research

Volumn 15, Issue 5, 2007, Pages 607-621

  Garcia Muse, Tatiana ^a   Boulton, Simon J ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Caenorhabditis elegans; Meiosis; Recombination; Synapsis; Synaptonemal complex

Indexed keywords

DOUBLE STRANDED DNA;

CAENORHABDITIS ELEGANS; CHROMOSOME PAIRING; CHROMOSOME STRUCTURE; DNA STRAND BREAKAGE; GENETIC RECOMBINATION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROPHASE; REVIEW;

ANIMALS; CAENORHABDITIS ELEGANS; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; FEMALE; GENOME, HELMINTH; MALE; MEIOSIS; MITOSIS; MODELS, GENETIC; RECOMBINATION, GENETIC; SYNAPTONEMAL COMPLEX;

CAENORHABDITIS ELEGANS; SYNAPSIS;

EID: 34547654174     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-007-1146-x     Document Type: Review

References (101)

1. Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
2. Albertson DG, Rose AM, Villeneuve AM (1997). Chromosome Organization, Mitosis and Meiosis. C. Elegans II. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
3. Alpi A, Pasierbek P, Gartner A, Loidl J (2003) Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112: 6-16.
4. Arora C, Kee K, Maleki S, Keeney S (2004) Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol Cell 13: 549-559.
5. Baker SM, Plug AW, Prolla TA et al. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13: 336-342.
6. Bishop DK, Park D, XU L, Kleckner N (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69: 439-456.
7. Bishop DK, Zickler D (2004) Early decision: meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15.
8. Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR III, Russell P (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107: 537-548.
9. Boulton SJ, Martin JS, Polanowska J, Hill DE, Gartner A, Vidal M (2004) BRCA1/BARD1 orthologs required for DNA repair in Caenorhabditis elegans. Curr Biol 14: 33-39.
10. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
11. Chan RC, Chan A, Jeon M et al. (2003) Chromosome cohesion is regulated by a clock gene paralogue TIM-1. Nature 423: 1002-1009.
12. Chen XB, Melchionna R, Denis CM et al. (2001) Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol Cell 8: 1117-1127.
13. Chin GM, Villeneuve AM (2001) C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev 15: 522-534.
14. Chua PR, Roeder GS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
15. Ciosk R, Zachariae W, Michaelis C, Shevchenko A, Mann M, Nasmyth K (1998) An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93: 1067-1076.
16. Cohen-Fix O (2001) The making and breaking of sister chromatid cohesion. Cell 106: 137-140.
17. Colaiacovo MP, MacQueen AJ, Martinez-Perez E 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.
18. Colaiacovo MP, Stanfield GM, Reddy KC, Reinke V, Kim SK, Villeneuve AM (2002) A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 162: 113-128.
19. Couteau F, Nabeshima K, Villeneuve A, Zetka M (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.
20. Couteau F, Zetka M (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19: 2744-2756.
21. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.
22. Galletto R, Amitani I, Baskin RJ, Kowalczykowski SC (2006) Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443: 875-878.
23. Gerton JL, Hawley RS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6: 477-487.
24. Goldstein P, Slaton DE (1982) The synaptonemal complexes of Caenorhabditis elegans: comparison of wild-type and mutant strains and pachytene karyotype analysis of wild-type. Chromosoma 84: 585-597.
25. Gudmundsdottir K, Lord CJ, Witt E, Tutt AN, Ashworth A (2004) DSS1 is required for RAD51 focus formation and genomic stability in mammalian cells. EMBO Rep 5: 989-993.
26. Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2: 280-291.
27. Henderson KA, Kee K, Maleki S, Santini PA, Keeney S (2006) Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125: 1321-1332.
28. Heyting C (1996) Synaptonemal complexes: structure and function. Curr Opin Cell Biol 8: 389-396.
29. Hillers KJ, Villeneuve AM (2003) Chromosome-wide control of meiotic crossing over in C. elegans. Curr Biol 13: 1641-1647.
30. Hodgking J, Horvitz HR, Brenner S (1979) Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91: 64-94.
31. Hollingsworth NM, Goetsch L, Byers B (1990) The HOP1 encodes a meiosis-specific component of yeast chromosomes. Cell 61: 73-84.
32. Hollingsworth NM, Johnson AD (1993) A conditional allele of the Saccharomyces cerevisiae HOP1 gene is suppressed by overexpression of two other meiosis-specific genes: RED1 and REC104. Genetics 133: 785-797.
33. Hollingsworth NM, Ponte L, Halsey C (1995) MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev 9: 1728-1739.
34. Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24: 7998-8006.
35. Jasin M (2002) Homologous repair of DNA damage and tumorigenesis: the BRCA connection. Oncogene 21: 8981-8993.
36. Joo C, McKinney SA, Nakamura M, Rasnik I, Myong S, Ha T (2006) Real-time observation of RecA filament dynamics with single monomer resolution. Cell 126: 515-527.
37. Kaliraman V, Mullen JR, Fricke WM, Bastin-Shanower SA, Brill SJ (2001) Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev 15: 2730-2740.
38. Kee K, Protacio RU, Arora C, Keeney S (2004) Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J 23: 1815-1824.
39. 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. Cell 88: 375-384.
40. Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM (2000) Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156: 617-630.
41. Klein F, Mahr P, Galova M et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91-103.
42. Kojic M, Kostrub CF, Buchman AR, Holloman WK (2002) BRCA2 homolog required for proficiency in DNA repair, recombination, and genome stability in Ustilago maydis. Mol Cell 10: 683-691.
43. Kojic M, Yang H, Kostrub CF, Pavletich NP, Holloman WK (2003) The BRCA2-interacting protein DSS1 is vital for DNA repair, recombination, and genome stability in Ustilago maydis. Mol Cell 12: 1043-1049.
44. Lee JY, Orr-Weaver TL (2001) The molecular basis of sister-chromatid cohesion. Annu Rev Cell Dev Biol 17: 753-777.
45. Li J, Hooker GW, Roeder GS (2006) Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required for meiotic double-strand break formation. Genetics 173: 1969-1981.
46. Liu Y, Masson JY, Shah R, O'Regan P, West SC (2004) RAD51C is required for Holliday junction processing in mammalian cells. Science 303: 243-246.
47. MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674-1687.
48. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428-2442.
49. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123: 1037-1050.
50. Marston NJ, Richards WJ, Hughes D, Bertwistle D, Marshall CJ, Ashworth A (1999) Interaction between the product of the breast cancer susceptibility gene BRCA2 and DSS1, a protein functionally conserved from yeast to mammals. Mol Cell Biol 19: 4633-4642.
51. Martin JS, Winkelmann N, Petalcorin MI, McIlwraith MJ, Boulton SJ (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.
52. Martinez-Perez E, Villeneuve AM (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19: 2727-2743.
53. Meuwissen RL, Offenberg HH, Dietrich AJ, Riesewijk A, Van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11: 5091-5100.
54. McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205: 111-128.
55. McKim KS, Peters K, Rose AM (1993) Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans. Genetics 134: 749-768.
56. Moynahan ME (2002) The cancer connection: BRCA1 and BRCA2 tumor suppression in mice and humans. Oncogene 21: 8994-9007.
57. Moynahan ME, Pierce AJ, Jasin M (2001) BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 7: 263-272.
58. 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 Biol 168: 683-689.
59. Nabeshima K, Villeneuve AM, Hillers KJ (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168: 1275-1292.
60. Niu H, Wan L, Baumgartner B, Schaefer D, Loidl J, Hollingsworth NM (2005) Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol Biol Cell 16: 5804-5818.
61. Oishi I, Iwai K, Kagohashi Y et al. (2001) Critical role of Caenorhabditis elegans homologs of Cds1 (Chk2)-related kinases in meiotic recombination. Mol Cell Biol 21: 1329-1335.
62. Page SL, Hawley RS (2003) Chromosome choreography: the meiotic ballet. Science 301: 785-789.
63. Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525-552.
64. Pasierbek P, Fodermayr M, Jantsch V, Jantsch M, Schweizer D, Loidl J (2003) The Caenorhabditis elegans SCC-3 homologue is required for meiotic synapsis and for proper chromosome disjunction in mitosis and meiosis. Exp Cell Res 289: 245-255.
65. Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15: 1349-1360.
66. Patel KJ, Yu VP, Lee H et al. (1998) Involvement of Brca2 in DNA repair. Mol Cell 1: 347-357.
67. Petalcorin MI, Sandall J, Wigley DB, Boulton SJ (2006) CeBRC-2 stimulates D-loop formation by RAD-51 and promotes DNA single-strand annealing. J Mol Biol 361: 231-242.
68. Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112: 423-440.
69. Pezza RJ, Petukhova GV, Ghirlando R, Camerini-Otero RD (2006) Molecular activities of meiosis-specific proteins Hop2, Mnd1, and the Hop2-Mnd1 complex. J Biol Chem 281: 18426-18434.
70. Phillips CM, Dernburg AF (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.
71. Phillips CM, Wong C, Bhalla N et al. (2005) HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123: 1051-1063.
72. Prieto I, Suja JA, Pezzi N et al. (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 3: 761-766.
73. Reddy KC, Villeneuve AM (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118: 439-452.
74. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21: 6984-6998.
75. 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. Genetics 160: 471-479.
76. Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11: 2600-2621.
77. Ross-MacDonald P, Roeder GS (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79: 1069-1080.
78. Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
79. Tsubouchi H, Roeder GS (2002) The Mnd1 protein forms a complex with hop2 to promote homologous chromosome pairing and meiotic double-strand break repair. Mol Cell Biol 22: 3078-3088.
80. Tutt A, Bertwistle D, Valentine J et al. (2001) Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J 20: 4704-4716.
81. Uhlmann F, Lottspeich F, Nasmyth K (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400: 37-42.
82. van den Bosch M, Bree RT, Lowndes NF (2003) The MRN complex: coordinating and mediating the response to broken chromosomes. EMBO Rep 4: 844-849.
83. van Veen JE, Hawley RS (2003) Meiosis: when even two is a crowd. Curr Biol 13: R831-R833.
84. Vazquez J, Belmont AS, Sedat JW (2002) The dynamics of homologous chromosome pairing during male Drosophila meiosis. Curr Biol 12: 1473-1483.
85. Venkitaraman AR (2000) The breast cancer susceptibility gene, BRCA2: at the crossroads between DNA replication and recombination? Phil Trans R Soc Lond B Biol Sci 355: 191-198.
86. Venkitaraman AR (2001) Functions of BRCA1 and BRCA2 in the biological response to DNA damage. J Cell Sci 114: 3591-3598.
87. Villeneuve AM (1994) A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887-902.
88. Wang F, Yoder J, Antoshechkin I, Han M (2003) Caenorhabditis elegans EVL-14/PDS-5 and SCC-3 are essential for sister chromatid cohesion in meiosis and mitosis. Mol Cell Biol 23: 7698-7707.
89. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400: 461-464.
90. Weiner BM, Kleckner N (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977-991.
91. West SC (1997) Processing of recombination intermediates by the RuvABC proteins. Annu Rev Genet 31: 213-244.
92. West SC (2003) Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 4: 435-445.
93. Wilson JH, Elledge SJ (2002) Cancer: BRCA2 enters the fray. Science 297: 1822-1823.
94. Yang H, Jeffrey PD, Miller J et al. (2002) BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297: 1837-1848.
95. Yang H, Li Q, Fan J, Holloman WK, Pavletich NP (2005) The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 433: 653-657.
96. Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271-1283.
97. 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 Dev 13: 2258-2270.
98. Zetka MC, Rose AM (1990) Sex-related differences in crossing over in Caenorhabditis elegans. Genetics 126: 355-363.
99. Zetka MC, Rose AM (1995) Mutant rec-1 eliminates the meiotic pattern of crossing over in Caenorhabditis elegans. Genetics 141: 1339-1349.
100. Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32: 619-697.
101. Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754.