Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis

Part of the Genome Dynamics and Stability book series (GENOME, volume 2)


Meiotic recombination is carried out through a specialized pathway for the formation and repair of DNA double-strand breaks made by the Spo11 protein, a relative of archaeal topoisomerase VI. This review summarizes recent studies that provide insight to the mechanism of DNA cleavage by Spo11, functional interactions of Spo11 with other proteins required for break formation, mechanisms that control the timing of recombination initiation, and evolutionary conservation and divergence of these processes.


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  1. 1.
    Agashe B, Prasad CK, Siddiqi I (2002) Identification and analysis of DYAD: a gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis. Development 129:3935–3943 PubMedGoogle Scholar
  2. 2.
    Alani E, Padmore R, Kleckner N (1990) Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61:419–436 PubMedGoogle Scholar
  3. 3.
    Araki Y, Takahashi S, Kobayashi T, Kajiho H, Hoshino S, Katada T (2001) Ski7p G protein interacts with the exosome and the Ski complex for 3′-to-5′ mRNA decay in yeast. EMBO J 20:4684–4693 PubMedGoogle Scholar
  4. 4.
    Aravind L, Leipe DD, Koonin EV (1998) Toprim—A conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins. Nucl Acids Res 26:4205–4213 PubMedGoogle Scholar
  5. 5.
    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 PubMedGoogle Scholar
  6. 6.
    Assenmacher N, Hopfner KP (2004) MRE11/RAD50/NBS1: complex activities. Chromosoma 113:157–166 PubMedGoogle Scholar
  7. 7.
    Atcheson CL, DiDomenico B, Frackman S, Esposito RE, Elder RT (1987) Isolation DNA sequence, and regulation of a meiosis-specific eukaryotic recombination gene. Proc Natl Acad Sci USA 84:8035–8039 PubMedGoogle Scholar
  8. 8.
    Baudat F, Nicolas A (1997) Clustering of meiotic double-strand breaks on yeast Chromosome III. Proc Natl Acad Sci USA 94:5213–5218 PubMedGoogle Scholar
  9. 9.
    Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6:989–998 PubMedGoogle Scholar
  10. 10.
    Baudat F, Keeney S (2001) Meiotic recombination: Making and breaking go hand in hand. Curr Biol 11:R45–R48 PubMedGoogle Scholar
  11. 11.
    Becker E, Meyer V, Madaoui H, Guerois R (2006) Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinformatics 22:1289–1292 PubMedGoogle Scholar
  12. 12.
    Bender CF et al. (2002) Cancer predisposition and hematopoietic failure in Rad50 S/S mice. Genes Dev 16:2237–2251 PubMedGoogle Scholar
  13. 13.
    Benjamin KR, Zhang C, Shokat KM, Herskowitz I (2003) Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev 17:1524–1539 PubMedGoogle Scholar
  14. 14.
    Berger JM, Fass D, Wang JC, Harrison SC (1998) Structural similarities between topoisomerases that cleave one or both DNA strands. Proc Natl Acad Sci USA 95:7876–7881 PubMedGoogle Scholar
  15. 15.
    Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–417 PubMedGoogle Scholar
  16. 16.
    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 PubMedGoogle Scholar
  17. 17.
    Bishop DK, Nikolski Y, Oshiro J, Chon J, Shinohara M, Chen X (1999) High copy number suppression of the meiotic arrest caused by a dmc1 mutation: REC114 imposes an early recombination block and RAD54 promotes a DMC1-independent DSB repair pathway. Genes Cells 4:425–444 PubMedGoogle Scholar
  18. 18.
    Bishop DK, Zickler D (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117:9–15 PubMedGoogle Scholar
  19. 19.
    Blat Y, Protacio RU, Hunter N, Kleckner N (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111:791–802 PubMedGoogle Scholar
  20. 20.
    Bleuyard JY, Gallego ME, White CI (2004) Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination. Chromosoma 113:197–203 PubMedGoogle Scholar
  21. 21.
    Borde V, Goldman ASH, Lichten M (2000) Direct coupling between meiotic DNA replication and recombination initiation. Science 290:806–809 PubMedGoogle Scholar
  22. 22.
    Borde V, Lin W, Novikov E, Petrini JH, Lichten M, Nicolas A (2004) Association of Mre11p with double-strand break sites during yeast meiosis. Mol Cell 13:389–401 PubMedGoogle Scholar
  23. 23.
    Borgne A, Murakami H, Ayte J, Nurse P (2002) The G1/S cyclin Cig2p during meiosis in fission yeast. Mol Biol Cell 13:2080–2090 PubMedGoogle Scholar
  24. 24.
    Borner GV, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45 PubMedGoogle Scholar
  25. 25.
    Bowring FJ, Yeadon PJ, Stainer RG, Catcheside DE (2006) Chromosome pairing and meiotic recombination in Neurospora crassa spo11 mutants. Curr Genet 50:115–123 PubMedGoogle Scholar
  26. 26.
    Brown JT, Bai X, Johnson AW (2000) The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6:449–457 PubMedGoogle Scholar
  27. 27.
    Budd ME, Wittrup KD, Bailey JE, Campbell JL (1989) DNA polymerase I is required for premeiotic DNA replication and sporulation but not for X-ray repair in Saccharomyces cerevisiae. Mol Cell Biol 9:365–376 PubMedGoogle Scholar
  28. 28.
    Buhler C, Gadelle D, Forterre P, Wang JC, Bergerat A (1998) Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucl Acids Res 26:5157–5162 PubMedGoogle Scholar
  29. 29.
    Buhler C, Lebbink JH, Bocs C, Ladenstein R, Forterre P (2001) DNA topoisomerase VI generates ATP-dependent double-strand breaks with two-nucleotide overhangs. J Biol Chem 276:37215–37222 PubMedGoogle Scholar
  30. 30.
    Celerin M, Merino ST, Stone JE, Menzie AM, Zolan ME (2000) Multiple roles of Spo11 in meiotic chromosome behavior. EMBO J 19:2739–2750 PubMedGoogle Scholar
  31. 31.
    Cervantes MD, Farah JA, Smith GR (2000) Meiotic DNA breaks associated with recombination in S. pombe. Mol Cell 5:883–888 PubMedGoogle Scholar
  32. 32.
    Cha RS, Weiner BM, Keeney S, Dekker J, Kleckner N (2000) Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p. Genes Dev 14:493–503 PubMedGoogle Scholar
  33. 33.
    Chahwan C, Nakamura TM, Sivakumar S, Russell P, Rhind N (2003) The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol Cell Biol 23:6564–6573 PubMedGoogle Scholar
  34. 34.
    Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369–413 PubMedGoogle Scholar
  35. 35.
    Cheng Z, Liu Y, Wang C, Parker R, Song H (2004) Crystal structure of Ski8p, a WD-repeat protein with dual roles in mRNA metabolism and meiotic recombination. Protein Sci 13:2673–2684 PubMedGoogle Scholar
  36. 36.
    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 PubMedGoogle Scholar
  37. 37.
    Chu S, Herskowitz I (1998) Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell 1:685–696 PubMedGoogle Scholar
  38. 38.
    Cliften PF et al. (2001) Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis. Genome Res 11:1175–1186 PubMedGoogle Scholar
  39. 39.
    Clouaire T, Roussigne M, Ecochard V, Mathe C, Amalric F, Girard JP (2005) The THAP domain of THAP1 is a large C2CH module with zinc-dependent sequence-specific DNA-binding activity. Proc Natl Acad Sci USA 102:6907–6912 PubMedGoogle Scholar
  40. 40.
    Colaiacovo MP 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 PubMedGoogle Scholar
  41. 41.
    Cooper KF, Mallory MJ, Egeland DB, Jarnik M, Strich R (2000) Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast. Proc Natl Acad Sci USA 97:14548–14553 PubMedGoogle Scholar
  42. 42.
    Corbett KD, Berger JM (2003) Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution. EMBO J 22:151–163 PubMedGoogle Scholar
  43. 43.
    Corbett KD, Berger JM (2004) Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu Rev Biophys Biomol Struct 33:95–118 PubMedGoogle Scholar
  44. 44.
    Corbett KD, Berger JM (2005) Structural dissection of ATP turnover in the prototypical GHL ATPase TopoVI. Structure 13:873–882 PubMedGoogle Scholar
  45. 45.
    Davis CA, Grate L, Spingola M, Ares M Jr (2000) Test of intron predictions reveals novel splice sites, alternatively spliced mRNAs and new introns in meiotically regulated genes of yeast. Nucl Acids Res 28:1700–1706 PubMedGoogle Scholar
  46. 46.
    Davis L, Smith GR (2001) Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe. Proc Natl Acad Sci USA 98:8395–8402 PubMedGoogle Scholar
  47. 47.
    de Massy B, Rocco V, Nicolas A (1995) The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae. EMBO J 14:4589–4598 PubMedGoogle Scholar
  48. 48.
    de Massy B (2003) Distribution of meiotic recombination sites. Trends Genet 19:514–522 PubMedGoogle Scholar
  49. 49.
    De Veaux LC, Hoagland NA, Smith GR (1992) Seventeen complementation groups of mutations decreasing meiotic recombination in Schizosaccharomyces pombe. Genetics 130:251–262 PubMedGoogle Scholar
  50. 50.
    de Vries FA et al. (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:1376–1389 PubMedGoogle Scholar
  51. 51.
    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 PubMedGoogle Scholar
  52. 52.
    DeVeaux LC, Smith GR (1994) Region-specific activators of meiotic recombination in Schizosaccharomyces pombe. Genes Dev 8:203–210 PubMedGoogle Scholar
  53. 53.
    DeWall KM, Davidson MK, Sharif WD, Wiley CA, Wahls WP (2005) A DNA binding motif of meiotic recombinase Rec12 (Spo11) defined by essential glycine-202, and persistence of Rec12 protein after completion of recombination. Gene 356:77–84 PubMedGoogle Scholar
  54. 54.
    Diaz RL, Alcid AD, Berger JM, Keeney S (2002) Identification of residues in yeast Spo11p critical for meiotic DNA double-strand break formation. Mol Cell Biol 22:1106–1115 PubMedGoogle Scholar
  55. 55.
    Doll E, Molnar M, Hiraoka Y, Kohli J (2005) Characterization of rec15, an early meiotic recombination gene in Schizosaccharomyces pombe. Curr Genet 48:323–333 PubMedGoogle Scholar
  56. 56.
    Dresser ME et al. (1997) DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147:533–544 PubMedGoogle Scholar
  57. 57.
    Durocher D, Jackson SP (2002) The FHA domain. FEBS Lett 513:58–66 PubMedGoogle Scholar
  58. 58.
    Dutta R, Inouye M (2000) GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25:24–28 PubMedGoogle Scholar
  59. 59.
    Ellermeier C, Smith GR (2005) Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe. Proc Natl Acad Sci USA 102:10952–10957 PubMedGoogle Scholar
  60. 60.
    Engebrecht JA, Voelkel-Meiman K, Roeder GS (1991) Meiosis-specific RNA splicing in yeast. Cell 66:1257–1268 PubMedGoogle Scholar
  61. 61.
    Evans DH, Li YF, Fox ME, Smith GR (1997) A WD repeat protein, Rec14, essential for meiotic recombination in Schizosaccharomyces pombe. Genetics 146:1253–1264 PubMedGoogle Scholar
  62. 62.
    Farah JA, Hartsuiker E, Mizuno K, Ohta K, Smith GR (2002) A 160-bp palindrome is a Rad50.Rad32-dependent mitotic recombination hotspot in Schizosaccharomyces pombe. Genetics 161:461–468 PubMedGoogle Scholar
  63. 63.
    Farah JA, Cromie G, Davis L, Steiner WW, Smith GR (2005a) Activation of an alternative, rec12 (spo11)-independent pathway of fission yeast meiotic recombination in the absence of a DNA flap endonuclease. Genetics 171:1499–1511 PubMedGoogle Scholar
  64. 64.
    Farah JA, Cromie G, Steiner WW, Smith GR (2005b) A novel recombination pathway initiated by the Mre11/Rad50/Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe. Genetics 169:1261–1274 PubMedGoogle Scholar
  65. 65.
    Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004) H2AX: the histone guardian of the genome. DNA Repair (Amst) 3:959–967 Google Scholar
  66. 66.
    Fox ME, Smith GR (1998) Control of meiotic recombination in Schizosaccharomyces pombe. Prog Nucleic Acid Res Mol Biol 61:345–378 PubMedGoogle Scholar
  67. 67.
    Friedman DB, Hollingsworth NM, Byers B (1994) Insertional mutations in the yeast HOP1 gene: evidence for multimeric assembly in meiosis. Genetics 136:449–464 PubMedGoogle Scholar
  68. 68.
    Furuse M, Nagase Y, Tsubouchi H, Murakami-Murofushi K, Shibata T, Ohta K (1998) Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J 17:6412–6425 PubMedGoogle Scholar
  69. 69.
    Gadelle D, Filee J, Buhler C, Forterre P (2003) Phylogenomics of type II DNA topoisomerases. Bioessays 25:232–242 PubMedGoogle Scholar
  70. 70.
    Gardiner JM, Bullard SA, Chrome C, Malone RE (1997) Molecular and genetic analysis of REC103, an early meiotic recombination gene in yeast. Genetics 146:1265–1274 PubMedGoogle Scholar
  71. 71.
    Gerecke EE, Zolan ME (2000) An mre11 mutant of Coprinus cinereus has defects in meiotic chromosome pairing, condensation and synapsis. Genetics 154:1125–1139 PubMedGoogle Scholar
  72. 72.
    Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD (2000) Inaugural article: global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 97:11383–11390 PubMedGoogle Scholar
  73. 73.
    Glover JN, Williams RS, Lee MS (2004) Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem Sci 29:579–585 PubMedGoogle Scholar
  74. 74.
    Gregan J et al. (2005) Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast. Curr Biol 15:1663–1669 PubMedGoogle Scholar
  75. 75.
    Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11–1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600 PubMedGoogle Scholar
  76. 76.
    Grelon M, Gendrot G, Vezon D, Pelletier G (2003) The Arabidopsis MEI1 gene encodes a protein with five BRCT domains that is involved in meiosis-specific DNA repair events independent of SPO11-induced DSBs. Plant J 35:465–475 PubMedGoogle Scholar
  77. 77.
    Hartung F, Puchta H (2000) Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucl Acids Res 28:1548–1554 PubMedGoogle Scholar
  78. 78.
    Hartung F, Puchta H (2001) Molecular characterization of homologues of both subunits A (SPO11) and B of the archaebacterial topoisomerase 6 in plants. Gene 271:81–86 PubMedGoogle Scholar
  79. 79.
    Hartung F, Angelis KJ, Meister A, Schubert I, Melzer M, Puchta H (2002) An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Curr Biol 12:1787–1791 PubMedGoogle Scholar
  80. 80.
    He F, Li X, Spatrick P, Casillo R, Dong S, Jacobson A (2003) Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol Cell 12:1439–1452 PubMedGoogle Scholar
  81. 81.
    Henderson KA, Kee K, Maleki S, Santini PA, Keeney S (2006) Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125:1321–1332 PubMedGoogle Scholar
  82. 82.
    Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500 PubMedGoogle Scholar
  83. 83.
    Hochwagen A, Tham WH, Brar GA, Amon A (2005) The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 122:861–873 PubMedGoogle Scholar
  84. 84.
    Hochwagen A, Amon A (2006) Checking your breaks: surveillance mechanisms of meiotic recombination. Curr Biol 16:R217–228 PubMedGoogle Scholar
  85. 85.
    Hopfner KP et al. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562–566 PubMedGoogle Scholar
  86. 86.
    Hopfner KP (2006) Structure and function of Rad50/SMC protein complexes in chromosome biology. In: Lankenau DH (ed) Genome Integrity: Facets and Perspectives, vol 1. Springer, Berlin Heidelberg New York Google Scholar
  87. 87.
    Hunter N (2007) Meiotic recombination. In: Aguilera A, Rothstein R (eds) Molecular Genetics of Recombination. Springer, Berlin Heidelberg New York Google Scholar
  88. 88.
    Jacobs Anderson JS, Parker R (1998) The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J 17:1497–1506 Google Scholar
  89. 89.
    Jang JK, Sherizen DE, Bhagat R, Manheim EA, McKim KS (2003) Relationship of DNA double-strand breaks to synapsis in Drosophila. J Cell Sci 116:3069–3077 PubMedGoogle Scholar
  90. 90.
    Jiao K, Salem L, Malone R (2003) Support for a meiotic recombination initiation complex: interactions among Rec102p, Rec104p, and Spo11p. Mol Cell Biol 23:5928–5938 PubMedGoogle Scholar
  91. 91.
    Jolivet S, Vezon D, Froger N, Mercier R (2006) Non conservation of the meiotic function of the Ski8/Rec103 homolog in Arabidopsis. Genes Cells 11:615–622 PubMedGoogle Scholar
  92. 92.
    Juneau K, Palm C, Miranda M, Davis RW (2007) High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing. Proc Natl Acad Sci USA 104:1522–1527 PubMedGoogle Scholar
  93. 93.
    Kauppi L, Jeffreys AJ, Keeney S (2004) Where the crossovers are: recombination distributions in mammals. Nat Rev Genet 5:413–424 PubMedGoogle Scholar
  94. 94.
    Kee K, Keeney S (2002) Functional interactions between SPO11 and REC102 during initiation of meiotic recombination in Saccharomyces cerevisiae. Genetics 160:111–122 PubMedGoogle Scholar
  95. 95.
    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 PubMedGoogle Scholar
  96. 96.
    Keeney S, Kleckner N (1995) Covalent protein-DNA complexes at the 5′ strand termini of meiosis-specific double-strand breaks in yeast. Proc Natl Acad Sci USA 92:11274–11278 PubMedGoogle Scholar
  97. 97.
    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 PubMedGoogle Scholar
  98. 98.
    Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52:1–53 PubMedGoogle Scholar
  99. 99.
    Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300:1152–1155 PubMedGoogle Scholar
  100. 100.
    Kleckner N et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci USA 101:12592–12597 PubMedGoogle Scholar
  101. 101.
    Kleckner N (2006) Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115:175–194 PubMedGoogle Scholar
  102. 102.
    Klein F 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 PubMedGoogle Scholar
  103. 103.
    Klein U, Esposito G, Baudat F, Keeney S, Jasin M (2002) Mice deficient for the type II topoisomerase-like DNA transesterase Spo11 show normal immunoglobulin somatic hypermutation and class switching. Eur J Immunol 32:316–321 PubMedGoogle Scholar
  104. 104.
    Krawchuk MD, DeVeaux LC, Wahls WP (1999) Meiotic chromosome dynamics dependent upon the rec8 +, rec10 + and rec11 + genes of the fission yeast Schizosaccharomyces pombe. Genetics 153:57–68 PubMedGoogle Scholar
  105. 105.
    Krogh BO, Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38:233–271 PubMedGoogle Scholar
  106. 106.
    Lamb TM, Mitchell AP (2001) Coupling of Saccharomyces cerevisiae early meiotic gene expression to DNA replication depends upon RPD3 and SIN3. Genetics 157:545–556 PubMedGoogle Scholar
  107. 107.
    Lankenau DH (2006) Germline double-strand break repair and gene targeting in Drosophila: A trajectory system throughout evolution. In: Egel R, Lankenau DH (eds) Genome Dynamics and Stability, Vol 1. Springer, Berlin Heidelberg New York Google Scholar
  108. 108.
    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 PubMedGoogle Scholar
  109. 109.
    Libby BJ et al. (2002) The mouse meiotic mutation mei1 disrupts chromosome synapsis with sexually dimorphic consequences for meiotic progression. Dev Biol 242:174–187 PubMedGoogle Scholar
  110. 110.
    Libby BJ, Reinholdt LG, Schimenti JC (2003) Positional cloning and characterization of Mei1, a vertebrate-specific gene required for normal meiotic chromosome synapsis in mice. Proc Natl Acad Sci USA 100:15706–15711 PubMedGoogle Scholar
  111. 111.
    Lichten M, Goldman AS (1995) Meiotic recombination hotspots. Annu Rev Genet 29:423–444 PubMedGoogle Scholar
  112. 112.
    Lin Y, Larson KL, Dorer R, Smith GR (1992) Meiotically induced rec7 and rec8 genes of Schizosaccharomyces pombe. Genetics 132:75–85 PubMedGoogle Scholar
  113. 113.
    Lin Y, Smith GR (1994) Transient, meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe. Genetics 136:769–779 PubMedGoogle Scholar
  114. 114.
    Lin Y, Smith GR (1995) An intron-containing meiosis-induced recombination gene, rec15, of Schizosaccharomyces pombe. Mol Microbiol 17:439–448 PubMedGoogle Scholar
  115. 115.
    Liu H, Jang JK, Kato N, McKim KS (2002) mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster. Genetics 162:245–258 PubMedGoogle Scholar
  116. 116.
    Liu J, Wu T-C, Lichten M (1995) The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate. EMBO J 14:4599–4608 PubMedGoogle Scholar
  117. 117.
    Loidl J (2006) S. pombe linear elements: the modest cousins of synaptonemal complexes. Chromosoma 115:260–271 PubMedGoogle Scholar
  118. 118.
    Lorenz A et al. (2004) S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J Cell Sci 117:3343–3351 PubMedGoogle Scholar
  119. 119.
    Lorenz A, Estreicher A, Kohli J, Loidl J (2006) Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe. Chromosoma 115:330–340 PubMedGoogle Scholar
  120. 120.
    Luo G et al. (1999) Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc Natl Acad Sci USA 96:7376–7381 PubMedGoogle Scholar
  121. 121.
    Madrona AY, Wilson DK (2004) The structure of Ski8p, a protein regulating mRNA degradation: Implications for WD protein structure. Protein Sci 13:1557–1565 PubMedGoogle Scholar
  122. 122.
    Mahadevaiah SK et al. (2001) Recombinational DNA double strand breaks in mice precede synapsis. Nat Genet 27:271–276 PubMedGoogle Scholar
  123. 123.
    Malapeira J, Moldon A, Hidalgo E, Smith GR, Nurse P, Ayte J (2005) A meiosis-specific cyclin regulated by splicing is required for proper progression through meiosis. Mol Cell Biol 25:6330–6337 PubMedGoogle Scholar
  124. 124.
    Malkova A, Klein F, Leung WY, Haber JE (2000) HO endonuclease-induced recombination in yeast meiosis resembles Spo11- induced events. Proc Natl Acad Sci USA 97:14500–14505 PubMedGoogle Scholar
  125. 125.
    Malone RE, Pittman DL, Nau JJ (1997) Examination of the intron in the meiosis-specific recombination gene REC114 in Saccharomyces. Mol Gen Genet 255:410–419 PubMedGoogle Scholar
  126. 126.
    Manheim EA, McKim KS (2003) The synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila. Curr Biol 13:276–285 PubMedGoogle Scholar
  127. 127.
    Martin-Castellanos C et al. (2005) A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events. Curr Biol 15:2056–2062 PubMedGoogle Scholar
  128. 128.
    Masai H, Arai K (2002) Cdc7 kinase complex: a key regulator in the initiation of DNA replication. J Cell Physiol 190:287–296 PubMedGoogle Scholar
  129. 129.
    Masison DC, Blanc A, Ribas JC, Carroll K, Sonenberg N, Wickner RB (1995) Decoying the cap mRNA degradation system by a double-stranded RNA virus and poly(A) mRNA surveillance by a yeast antiviral system. Mol Cell Biol 15:2763–2771 PubMedGoogle Scholar
  130. 130.
    Mazina OM, Mazin AV, Nakagawa T, Kolodner RD, Kowalczykowski SC (2004) Saccharomyces cerevisiae Mer3 helicase stimulates 3′-5′ heteroduplex extension by Rad51; implications for crossover control in meiotic recombination. Cell 117:47–56 PubMedGoogle Scholar
  131. 131.
    McKee AH, Kleckner N (1997) A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of a new gene SAE2. Genetics 146:797–816 PubMedGoogle Scholar
  132. 132.
    McKee BD (1998) Pairing sites and the role of chromosome pairing in meiosis and spermatogenesis in male Drosophila. Curr Top Dev Biol 37:77–115 PubMedGoogle Scholar
  133. 133.
    McKim KS et al. (1998) Meiotic synapsis in the absence of recombination. Science 279:876–878 PubMedGoogle Scholar
  134. 134.
    McKim KS, Hayashi-Hagihara A (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev 12:2932–2942 PubMedGoogle Scholar
  135. 135.
    Mehrotra S, McKim KS (2006) Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. PLoS Genet 2:e200 PubMedGoogle Scholar
  136. 136.
    Mercier R et al. (2001) SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev 15:1859–1871 PubMedGoogle Scholar
  137. 137.
    Mercier R et al. (2003) The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130:3309–3318 PubMedGoogle Scholar
  138. 138.
    Merino ST, Cummings WJ, Acharya SN, Zolan ME (2000) Replication-dependent early meiotic requirement for Spo11 and Rad50. Proc Natl Acad Sci USA 97:10477–10482 PubMedGoogle Scholar
  139. 139.
    Moens PB, Pearlman RE, Heng HH, Traut W (1998) Chromosome cores and chromatin at meiotic prophase. Curr Top Dev Biol 37:241–262 PubMedGoogle Scholar
  140. 140.
    Molnar M, Bahler J, Sipiczki M, Kohli J (1995) The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics 141:61–73 PubMedGoogle Scholar
  141. 141.
    Molnar M et al. (2001) Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe. Genetics 157:519–532 PubMedGoogle Scholar
  142. 142.
    Molnar M, Doll E, Yamamoto A, Hiraoka Y, Kohli J (2003) Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing. J Cell Sci 116:1719–1731 PubMedGoogle Scholar
  143. 143.
    Morales M, Theunissen JW, Kim CF, Kitagawa R, Kastan MB, Petrini JH (2005) The Rad50S allele promotes ATM-dependent DNA damage responses and suppresses ATM deficiency: implications for the Mre11 complex as a DNA damage sensor. Genes Dev 19:3043–3054 PubMedGoogle Scholar
  144. 144.
    Moreau S, Ferguson JR, Symington LS (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol Cell Biol 19:556–566 PubMedGoogle Scholar
  145. 145.
    Murakami H, Nurse P (2001) Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast. Nat Genet 28:290–293 PubMedGoogle Scholar
  146. 146.
    Nag DK, Pata JD, Sironi M, Flood DR, Hart AM (2006) Both conserved and non-conserved regions of Spo11 are essential for meiotic recombination initiation in yeast. Mol Genet Genomics 276:313–321 PubMedGoogle Scholar
  147. 147.
    Nakagawa T, Ogawa H (1997) Involvement of the MRE2 gene of yeast in formation of meiosis-specific double-strand breaks and crossover recombination through RNA splicing. Genes Cells 2:65–79 PubMedGoogle Scholar
  148. 148.
    Nakagawa T, Ogawa H (1999) The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control in meiosis. EMBO J 18:5714–5723 PubMedGoogle Scholar
  149. 149.
    Nandabalan K, Price L, Roeder GS (1993) Mutations in U1 snRNA bypass the requirement for a cell type-specific RNA splicing factor. Cell 73:407–415 PubMedGoogle Scholar
  150. 150.
    Nandabalan K, Roeder GS (1995) Binding of a cell-type-specific RNA splicing factor to its target regulatory sequence. Mol Cell Biol 15:1953–1960 PubMedGoogle Scholar
  151. 151.
    Neale MJ, Ramachandran M, Trelles-Sticken E, Scherthan H, Goldman ASH (2002) In Saccharomyces cerevisiae, wild-type levels of Spo11-induced double-strand breaks are required for normal regulation of single-strand resection during meiosis. Mol Cell 9:835–846 PubMedGoogle Scholar
  152. 152.
    Neale MJ, Pan J, Keeney S (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053–1057 PubMedGoogle Scholar
  153. 153.
    Nichols MD, DeAngelis K, Keck JL, Berger JM (1999) Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO J 18:6177–6188 PubMedGoogle Scholar
  154. 154.
    Ogino K et al. (2006) Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast. Proc Natl Acad Sci USA 103:8131–8136 PubMedGoogle Scholar
  155. 155.
    Ogino K, Masai H (2006) Rad3-Cds1 mediates coupling of initiation of meiotic recombination with DNA replication. Mei4-dependent transcription as a potential target of meiotic checkpoint. J Biol Chem 281:1338–1344 PubMedGoogle Scholar
  156. 156.
    Padmore R, Cao L, Kleckner N (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66:1239–1256 PubMedGoogle Scholar
  157. 157.
    Page SL, Hawley RS (2003) Chromosome choreography: the meiotic ballet. Science 301:785–789 PubMedGoogle Scholar
  158. 158.
    Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63:349–404 PubMedGoogle Scholar
  159. 159.
    Parisi S et al. (1999) Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 19:3515–3528 PubMedGoogle Scholar
  160. 160.
    Peciña A, Smith KN, Mezard C, Murakami H, Ohta K, Nicolas A (2002) Targeted stimulation of meiotic recombination. Cell 111:173–184 PubMedGoogle Scholar
  161. 161.
    Petes TD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2:360–369 PubMedGoogle Scholar
  162. 162.
    Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440 PubMedGoogle Scholar
  163. 163.
    Ponticelli AS, Smith GR (1989) Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics 123:45–54 PubMedGoogle Scholar
  164. 164.
    Prieler S, Penkner A, Borde V, Klein F (2005) The control of Spo11's interaction with meiotic recombination hotspots. Genes Dev 19:255–269 PubMedGoogle Scholar
  165. 165.
    Prinz S, Amon A, Klein F (1997) Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146:781–795 PubMedGoogle Scholar
  166. 166.
    Puizina J, Siroky J, Mokros P, Schweizer D, Riha K (2004) Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell 16:1968–1978 PubMedGoogle Scholar
  167. 167.
    Qin J, Richardson LL, Jasin M, Handel MA, Arnheim N (2004) Mouse strains with an active H2-Ea meiotic recombination hot spot exhibit increased levels of H2-Ea-specific DNA breaks in testicular germ cells. Mol Cell Biol 24:1655–1666 PubMedGoogle Scholar
  168. 168.
    Ramesh MA, Malik SB, Logsdon JM Jr (2005) A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 15:185–191 PubMedGoogle Scholar
  169. 169.
    Rasmussen SW (1977) Meiosis in Bombyx mori females. Philos Trans R Soc Lond B Biol Sci 277:343–350 PubMedGoogle Scholar
  170. 170.
    Reddy KC, Villeneuve AM (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118:439–452 PubMedGoogle Scholar
  171. 171.
    Reinholdt LG, Schimenti JC (2005) Mei1 is epistatic to Dmc1 during mouse meiosis. Chromosoma 114:127–134 PubMedGoogle Scholar
  172. 172.
    Richard GF, Kerrest A, Lafontaine I, Dujon B (2005) Comparative genomics of hemiascomycete yeasts: genes involved in DNA replication, repair, and recombination. Mol Biol Evol 22:1011–1023 PubMedGoogle Scholar
  173. 173.
    Robine N et al. (2007) Genome-wide redistribution of meiotic double-strand breaks in S. cerevisiae. Mol Cell Biol 27(5):1868–1880 PubMedGoogle Scholar
  174. 174.
    Roca J, Berger JM, Harrison SC, Wang JC (1996) DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc Natl Acad Sci USA 93:4057–4062 PubMedGoogle Scholar
  175. 175.
    Rockmill B, Roeder GS (1988) RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis. Proc Natl Acad Sci USA 85:6057–6061 PubMedGoogle Scholar
  176. 176.
    Rockmill B, Engebrecht JA, Scherthan H, Loidl J, Roeder GS (1995) The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics 141:49–59 PubMedGoogle Scholar
  177. 177.
    Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987 PubMedGoogle Scholar
  178. 178.
    Salem L, Walter N, Malone R (1999) Suppressor analysis of the Saccharomyces cerevisiae gene REC104 reveals a genetic interaction with REC102. Genetics 151:1261–1272 PubMedGoogle Scholar
  179. 179.
    Sasanuma H, Murakami H, Fukuda T, Shibata T, Nicolas A, Ohta K (2007) Meiotic association between Spo11 regulated by Rec102, Rec104 and Rec114. Nucl Acids Res 35(4):1119–1133 PubMedGoogle Scholar
  180. 180.
    Sato H et al. (2006) Polymorphic alleles of the human MEI1 gene are associated with human azoospermia by meiotic arrest. J Hum Genet 51:533–540 PubMedGoogle Scholar
  181. 181.
    Scherrer FW Jr, Spingola M (2006) A subset of Mer1p-dependent introns requires Bud13p for splicing activation and nuclear retention. RNA 12:1361–1372 PubMedGoogle Scholar
  182. 182.
    Schild D, Byers B (1978) Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae. Chromosoma 70:109–130 PubMedGoogle Scholar
  183. 183.
    Sclafani RA (2000) Cdc7p-Dbf4p becomes famous in the cell cycle. J Cell Sci 113(Pt 12):2111–2117 PubMedGoogle Scholar
  184. 184.
    Sekelsky JJ et al. (1999) Identification of novel Drosophila meiotic genes recovered in a P-element screen. Genetics 152:529–542 PubMedGoogle Scholar
  185. 185.
    Sharif WD, Glick GG, Davidson MK, Wahls WP (2002) Distinct functions of S. pombe Rec12 (Spo11) protein and Rec12-dependent crossover recombination (chiasmata) in meiosis I; and a requirement for Rec12 in meiosis II. Cell Chromosome 1:1 PubMedGoogle Scholar
  186. 186.
    Shima H, Suzuki M, Shinohara M (2005) Isolation and characterization of novel xrs2 mutations in Saccharomyces cerevisiae. Genetics 170:71–85 PubMedGoogle Scholar
  187. 187.
    Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457–470 PubMedGoogle Scholar
  188. 188.
    Smith AV, Roeder GS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136:957–967 PubMedGoogle Scholar
  189. 189.
    Smith KN, Nicolas A (1998) Recombination at work for meiosis. Curr Opin Genet Dev 8:200–211 PubMedGoogle Scholar
  190. 190.
    Smith KN, Penkner A, Ohta K, Klein F, Nicolas A (2001) B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis. Curr Biol 11:88–97 PubMedGoogle Scholar
  191. 191.
    Spingola M, Ares M (2000) A yeast intronic splicing enhancer and Nam8p are required for Mer1p-activated splicing. Mol Cell 6:329–338 PubMedGoogle Scholar
  192. 192.
    Spingola M, Armisen J, Ares M Jr (2004) Mer1p is a modular splicing factor whose function depends on the conserved U2 snRNP protein Snu17p. Nucl Acids Res 32:1242–1250 PubMedGoogle Scholar
  193. 193.
    Stacey NJ et al. (2006) Arabidopsis SPO11–2 functions with SPO11–1 in meiotic recombination. Plant J 48:206–216 PubMedGoogle Scholar
  194. 194.
    Steiner WW, Schreckhise RW, Smith GR (2002) Meiotic DNA breaks at the S. pombe recombination hot spot M26. Mol Cell 9:847–855 PubMedGoogle Scholar
  195. 195.
    Stone MD et al. (2003) Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc Natl Acad Sci USA 100:8654–8659 PubMedGoogle Scholar
  196. 196.
    Storlazzi A, Tessé S, Gargano S, James F, Kleckner N, Zickler D (2003) Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling and reductional division. Genes Dev 17:2675–2687 PubMedGoogle Scholar
  197. 197.
    Stracker TH, Theunissen JW, Morales M, Petrini JH (2004) The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst) 3:845–854 Google Scholar
  198. 198.
    Strick TR, Croquette V, Bensimon D (2000) Single-molecule analysis of DNA uncoiling by a type II topoisomerase. Nature 404:901–904 PubMedGoogle Scholar
  199. 199.
    Stuart D, Wittenberg C (1998) CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev 12:2698–2710 PubMedGoogle Scholar
  200. 200.
    Sugimoto-Shirasu K, Stacey NJ, Corsar J, Roberts K, McCann MC (2002) DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr Biol 12:1782–1786 PubMedGoogle Scholar
  201. 201.
    Sugimoto-Shirasu K, Roberts GR, Stacey NJ, McCann MC, Maxwell A, Roberts K (2005) RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc Natl Acad Sci USA 102:18736–18741 PubMedGoogle Scholar
  202. 202.
    Sun H, Treco D, Szostak JW (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64:1155–1161 PubMedGoogle Scholar
  203. 203.
    Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378 PubMedGoogle Scholar
  204. 204.
    Tessé S, Storlazzi A, Kleckner N, Gargano S, Zickler D (2003) Localization and roles of Ski8p in Sordaria macrospora meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci USA 100:12865–12870 PubMedGoogle Scholar
  205. 205.
    Theunissen JW et al. (2003) Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11 ATLD1/ATLD1 mice. Mol Cell 12:1511–1523 PubMedGoogle Scholar
  206. 206.
    Thorne LW, Byers B (1993) Stage-specific effects of X-irradiation on yeast meiosis. Genetics 134:29–42 PubMedGoogle Scholar
  207. 207.
    Tonami Y, Murakami H, Shirahige K, Nakanishi M (2005) A checkpoint control linking meiotic S phase and recombination initiation in fission yeast. Proc Natl Acad Sci USA 102:5797–5801 PubMedGoogle Scholar
  208. 208.
    Tsukamoto Y, Mitsuoka C, Terasawa M, Ogawa H, Ogawa T (2005) Xrs2p regulates Mre11p translocation to the nucleus and plays a role in telomere elongation and meiotic recombination. Mol Biol Cell 16:597–608 PubMedGoogle Scholar
  209. 209.
    Usui T, Ohta T, Oshiumi H, Tomizawa J, Ogawa H, Ogawa T (1998) Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95:705–716 PubMedGoogle Scholar
  210. 210.
    Usui T, Petrini JH, Morales M (2006) Rad50S alleles of the Mre11 complex: questions answered and questions raised. Exp Cell Res 312:2694–2699 PubMedGoogle Scholar
  211. 211.
    Valentin G, Schwob E, Della Seta F (2006) Dual role of the Cdc7-regulatory protein Dbf4 during yeast meiosis. J Biol Chem 281:2828–2834 PubMedGoogle Scholar
  212. 212.
    van Heemst D, Heyting C (2000) Sister chromatid cohesion and recombination in meiosis. Chromosoma 109:10–26 PubMedGoogle Scholar
  213. 213.
    van Hoof A, Staples RR, Baker RE, Parker R (2000) Function of the Ski4p (Csl4p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol Cell Biol 20:8230–8243 PubMedGoogle Scholar
  214. 214.
    Wahls WP (1998) Meiotic recombination hotspots: shaping the genome and insights into hypervariable minisatellite DNA change. Curr Top Dev Biol 37:37–75 PubMedCrossRefGoogle Scholar
  215. 215.
    Wan L, Zhang C, Shokat KM, Hollingsworth NM (2006) Chemical inactivation of Cdc7 kinase in budding yeast results in a reversible arrest that allows efficient cell synchronization prior to meiotic recombination. Genetics 174:1767–1774 PubMedGoogle Scholar
  216. 216.
    Wang JC (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3:430–440 PubMedGoogle Scholar
  217. 217.
    Wang L, Lewis MS, Johnson AW (2005) Domain interactions within the Ski2/3/8 complex and between the Ski complex and Ski7p. RNA 11:1291–1302 PubMedGoogle Scholar
  218. 218.
    Ward JO et al. (2003) Toward the genetics of mammalian reproduction: induction and mapping of gametogenesis mutants in mice. Biol Reprod 69:1615–1625 PubMedGoogle Scholar
  219. 219.
    Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464 PubMedGoogle Scholar
  220. 220.
    Webber HA, Howard L, Bickel SE (2004) The cohesion protein ORD is required for homologue bias during meiotic recombination. J Cell Biol 164:819–829 PubMedGoogle Scholar
  221. 221.
    Wells JL, Pryce DW, Estreicher A, Loidl J, McFarlane RJ (2006) Linear element-independent meiotic recombination in Schizosaccharomyces pombe. Genetics 174:1105–1114 PubMedGoogle Scholar
  222. 222.
    Wiltzius JJ, Hohl M, Fleming JC, Petrini JH (2005) The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat Struct Mol Biol 12:403–407 PubMedGoogle Scholar
  223. 223.
    Wu T-C, Lichten M (1994) Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science 263:515–518 PubMedGoogle Scholar
  224. 224.
    Wu T-C, Lichten M (1995) Factors that affect the location and frequency of meiosis-induced double-strand breaks in Saccharomyces cerevisiae. Genetics 140:55–66 PubMedGoogle Scholar
  225. 225.
    Xiao Y, Weaver DT (1997) Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucl Acids Res 25:2985–2991 PubMedGoogle Scholar
  226. 226.
    Xu F, Petes TD (1996) Fine-structure mapping of meiosis-specific double-strand DNA breaks at a recombination hotspot associated with an insertion of telomeric sequences upstream of the HIS4 locus in yeast. Genetics 143:1115–1125 PubMedGoogle Scholar
  227. 227.
    Xu L, Kleckner N (1995) Sequence non-specific double-strand breaks and interhomolog interactions prior to double-strand break formation at a meiotic recombination hot spot in yeast. EMBO J 14:5115–5128 PubMedGoogle Scholar
  228. 228.
    Xu L, Weiner BM, Kleckner N (1997) Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev 11:106–118 PubMedGoogle Scholar
  229. 229.
    Yamamoto M, Imai Y, Watanabe Y (1997) Mating and sporulation in Schizosaccharomyces pombe. In: Pringle JR, Broach JR, Jones EW (eds) The Molecular and Cellular Biology of the Yeast Saccharomyces: Life Cycle and Cell Biology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY, pp 1035–1106 Google Scholar
  230. 230.
    Yin Y et al. (2002) A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc Natl Acad Sci USA 99:10191–10196 PubMedGoogle Scholar
  231. 231.
    Young JA, Schreckhise RW, Steiner WW, Smith GR (2002) Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol Cell 9:253–263 PubMedGoogle Scholar
  232. 232.
    Young JA, Hyppa RW, Smith GR (2004) Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167:593–605 PubMedGoogle Scholar
  233. 233.
    Zenvirth D, Arbel T, Sherman A, Goldway M, Klein S, Simchen G (1992) Multiple sites for double-strand breaks in whole meiotic chromosomes of Saccharomyces cerevisiae. EMBO J 11:3441–3447 PubMedGoogle Scholar
  234. 234.
    Zenvirth D et al. (2003) Mammalian meiosis involves DNA double-strand breaks with 3′ overhangs. Chromosoma 111:369–376 PubMedGoogle Scholar
  235. 235.
    Zhu J, Petersen S, Tessarollo L, Nussenzweig A (2001) Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr Biol 11:105–109 PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2007

Authors and Affiliations

  1. 1.Molecular Biology ProgramMemorial Sloan-Kettering Cancer CenterNew YorkUSA

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