Home LiteratureArticle Details
PMID: 21927624 Published · ppublish English Journal Article

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

Genome dynamics and stability ·Vol. 2 ·2008-01-01 ·Pages 81-123

Keeney S

Abstract

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.

Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Keeney Scott
Molecular Biology Program, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021 USA, [email protected].
References (231)
231 references, click to expand
  1. Complex formation and functional versatility of Mre11 of budding yeast in recombination.
    Cell. 1998 Nov 25;95(5):705-16 PMID: 9845372
  2. Replication-dependent early meiotic requirement for Spo11 and Rad50.
    Proc Natl Acad Sci U S A. 2000 Sep 12;97(19):10477-82 PMID: 10973500
  3. Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe.
    Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):10952-7 PMID: 16043696
  4. Function of the ski4p (Csl4p) and Ski7p proteins in 3'-to-5' degradation of mRNA.
    Mol Cell Biol. 2000 Nov;20(21):8230-43 PMID: 11027292
  5. Sister chromatid cohesion and recombination in meiosis.
    Chromosoma. 2000;109(1-2):10-26 PMID: 10855491
  6. Clustering of meiotic double-strand breaks on yeast chromosome III.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5213-8 PMID: 9144217
  7. Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12865-70 PMID: 14563920
  8. Control of meiotic recombination in Schizosaccharomyces pombe.
    Prog Nucleic Acid Res Mol Biol. 1998;61:345-78 PMID: 9752725
  9. Comparative genomics of hemiascomycete yeasts: genes involved in DNA replication, repair, and recombination.
    Mol Biol Evol. 2005 Apr;22(4):1011-23 PMID: 15647519
  10. Cancer predisposition and hematopoietic failure in Rad50(S/S) mice.
    Genes Dev. 2002 Sep 1;16(17):2237-51 PMID: 12208847
  11. Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2.
    Genes Dev. 2003 Jun 15;17(12):1524-39 PMID: 12783856
  12. Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast.
    Proc Natl Acad Sci U S A. 2006 May 23;103(21):8131-6 PMID: 16698922
  13. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation.
    Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7376-81 PMID: 10377422
  14. Meiotic recombination hot spots and cold spots.
    Nat Rev Genet. 2001 May;2(5):360-9 PMID: 11331902
  15. Meiosis in Bombyx mori females.
    Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):343-50 PMID: 16295
  16. A checkpoint control linking meiotic S phase and recombination initiation in fission yeast.
    Proc Natl Acad Sci U S A. 2005 Apr 19;102(16):5797-801 PMID: 15805194
  17. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis.
    Genetics. 1995 Sep;141(1):61-73 PMID: 8536990
  18. Non conservation of the meiotic function of the Ski8/Rec103 homolog in Arabidopsis.
    Genes Cells. 2006 Jun;11(6):615-22 PMID: 16716192
  19. Meiotic recombination: Making and breaking go hand in hand.
    Curr Biol. 2001 Jan 23;11(2):R45-8 PMID: 11231139
  20. The structure of Ski8p, a protein regulating mRNA degradation: Implications for WD protein structure.
    Protein Sci. 2004 Jun;13(6):1557-65 PMID: 15152089
  21. Isolation, DNA sequence, and regulation of a meiosis-specific eukaryotic recombination gene.
    Proc Natl Acad Sci U S A. 1987 Nov;84(22):8035-9 PMID: 3317399
  22. Meiotic association between Spo11 regulated by Rec102, Rec104 and Rec114.
    Nucleic Acids Res. 2007;35(4):1119-33 PMID: 17264124
  23. Test of intron predictions reveals novel splice sites, alternatively spliced mRNAs and new introns in meiotically regulated genes of yeast.
    Nucleic Acids Res. 2000 Apr 15;28(8):1700-6 PMID: 10734188
  24. Positional cloning and characterization of Mei1, a vertebrate-specific gene required for normal meiotic chromosome synapsis in mice.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15706-11 PMID: 14668445
  25. Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis.
    Genome Res. 2001 Jul;11(7):1175-86 PMID: 11435399
  26. Molecular and genetic analysis of REC103, an early meiotic recombination gene in yeast.
    Genetics. 1997 Aug;146(4):1265-74 PMID: 9258672
  27. A subset of Mer1p-dependent introns requires Bud13p for splicing activation and nuclear retention.
    RNA. 2006 Jul;12(7):1361-72 PMID: 16738408
  28. Polymorphic alleles of the human MEI1 gene are associated with human azoospermia by meiotic arrest.
    J Hum Genet. 2006;51(6):533-540 PMID: 16683055
  29. Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases.
    Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8654-9 PMID: 12857958
  30. DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4057-62 PMID: 8633016
  31. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11.
    Mol Cell. 2000 Nov;6(5):989-98 PMID: 11106739
  32. Stage-specific effects of X-irradiation on yeast meiosis.
    Genetics. 1993 May;134(1):29-42 PMID: 8514137
  33. Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts.
    Genetics. 2004 Jun;167(2):593-605 PMID: 15238514
  34. Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response.
    Bioinformatics. 2006 Jun 1;22(11):1289-92 PMID: 16522671
  35. Functional interactions between SPO11 and REC102 during initiation of meiotic recombination in Saccharomyces cerevisiae.
    Genetics. 2002 Jan;160(1):111-22 PMID: 11805049
  36. Support for a meiotic recombination initiation complex: interactions among Rec102p, Rec104p, and Spo11p.
    Mol Cell Biol. 2003 Aug;23(16):5928-38 PMID: 12897161
  37. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components.
    J Cell Sci. 2004 Jul 1;117(Pt 15):3343-51 PMID: 15226405
  38. Single-molecule analysis of DNA uncoiling by a type II topoisomerase.
    Nature. 2000 Apr 20;404(6780):901-4 PMID: 10786800
  39. A mechanical basis for chromosome function.
    Proc Natl Acad Sci U S A. 2004 Aug 24;101(34):12592-7 PMID: 15299144
  40. Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes.
    EMBO J. 2004 Apr 21;23(8):1815-24 PMID: 15044957
  41. MRE11/RAD50/NBS1: complex activities.
    Chromosoma. 2004 Oct;113(4):157-66 PMID: 15309560
  42. 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. 2002 Sep 19;1(1):1 PMID: 12437782
  43. Meiotic DNA breaks at the S. pombe recombination hot spot M26.
    Mol Cell. 2002 Apr;9(4):847-55 PMID: 11983175
  44. A meiosis-specific cyclin regulated by splicing is required for proper progression through meiosis.
    Mol Cell Biol. 2005 Aug;25(15):6330-7 PMID: 16024772
  45. Covalent protein-DNA complexes at the 5' strand termini of meiosis-specific double-strand breaks in yeast.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11274-8 PMID: 7479978
  46. The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity.
    Cell. 2005 Sep 23;122(6):861-73 PMID: 16179256
  47. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80.
    Mol Cell. 1998 Apr;1(5):685-96 PMID: 9660952
  48. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans.
    Mol Cell Biol. 1999 May;19(5):3515-28 PMID: 10207075
  49. Multiple roles of Spo11 in meiotic chromosome behavior.
    EMBO J. 2000 Jun 1;19(11):2739-50 PMID: 10835371
  50. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance.
    Mol Cell Biol. 1999 Jan;19(1):556-66 PMID: 9858579
  51. Recombination at work for meiosis.
    Curr Opin Genet Dev. 1998 Apr;8(2):200-11 PMID: 9610411
  52. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation.
    Cell. 2002 Dec 13;111(6):791-802 PMID: 12526806
  53. Identification of residues in yeast Spo11p critical for meiotic DNA double-strand break formation.
    Mol Cell Biol. 2002 Feb;22(4):1106-15 PMID: 11809802
  54. Cellular roles of DNA topoisomerases: a molecular perspective.
    Nat Rev Mol Cell Biol. 2002 Jun;3(6):430-40 PMID: 12042765
  55. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation.
    Genes Dev. 2005 Jun 1;19(11):1376-89 PMID: 15937223
  56. An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants.
    Curr Biol. 2002 Oct 15;12(20):1787-91 PMID: 12401176
  57. Meiosis-specific RNA splicing in yeast.
    Cell. 1991 Sep 20;66(6):1257-68 PMID: 1840507
  58. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis.
    Cell. 1993 Feb 12;72(3):365-78 PMID: 7916652
  59. S. pombe linear elements: the modest cousins of synaptonemal complexes.
    Chromosoma. 2006 Jun;115(3):260-71 PMID: 16532354
  60. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1999 Jun;63(2):349-404 PMID: 10357855
  61. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over.
    Genes Dev. 2005 Oct 15;19(20):2488-500 PMID: 16230536
  62. The mouse meiotic mutation mei1 disrupts chromosome synapsis with sexually dimorphic consequences for meiotic progression.
    Dev Biol. 2002 Feb 15;242(2):174-87 PMID: 11820814
  63. Dual role of the Cdc7-regulatory protein Dbf4 during yeast meiosis.
    J Biol Chem. 2006 Feb 3;281(5):2828-34 PMID: 16319063
  64. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
    Cell. 1999 Jul 9;98(1):91-103 PMID: 10412984
  65. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination.
    Dev Cell. 2003 Sep;5(3):463-74 PMID: 12967565
  66. Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p.
    Genes Dev. 2000 Feb 15;14(4):493-503 PMID: 10691741
  67. An atypical topoisomerase II from Archaea with implications for meiotic recombination.
    Nature. 1997 Mar 27;386(6623):414-7 PMID: 9121560
  68. Structural similarities between topoisomerases that cleave one or both DNA strands.
    Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):7876-81 PMID: 9653108
  69. Cyclin-dependent kinase directly regulates initiation of meiotic recombination.
    Cell. 2006 Jun 30;125(7):1321-32 PMID: 16814718
  70. 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. 2005 Dec 15;19(24):3043-54 PMID: 16357220
  71. 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. 2001 Mar 1;15(5):522-34 PMID: 11238374
  72. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis.
    Cell. 1998 Aug 7;94(3):387-98 PMID: 9708740
  73. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks.
    Nature. 2005 Aug 18;436(7053):1053-7 PMID: 16107854
  74. Mice deficient for the type II topoisomerase-like DNA transesterase Spo11 show normal immunoglobulin somatic hypermutation and class switching.
    Eur J Immunol. 2002 Feb;32(2):316-21 PMID: 11807770
  75. Meiotic chromosome dynamics dependent upon the rec8(+), rec10(+) and rec11(+) genes of the fission yeast Schizosaccharomyces pombe.
    Genetics. 1999 Sep;153(1):57-68 PMID: 10471700
  76. The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination.
    Genetics. 1995 Sep;141(1):49-59 PMID: 8536989
  77. CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint.
    Genes Dev. 1998 Sep 1;12(17):2698-710 PMID: 9732268
  78. Structural dissection of ATP turnover in the prototypical GHL ATPase TopoVI.
    Structure. 2005 Jun;13(6):873-82 PMID: 15939019
  79. Targeted stimulation of meiotic recombination.
    Cell. 2002 Oct 18;111(2):173-84 PMID: 12408862
  80. HO endonuclease-induced recombination in yeast meiosis resembles Spo11-induced events.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14500-5 PMID: 11121053
  81. Wild-type levels of Spo11-induced DSBs are required for normal single-strand resection during meiosis.
    Mol Cell. 2002 Apr;9(4):835-46 PMID: 11983174
  82. Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division.
    Genes Dev. 2003 Nov 1;17(21):2675-87 PMID: 14563680
  83. Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism.
    Mol Cell. 2004 Feb 27;13(4):549-59 PMID: 14992724
  84. Where the crossovers are: recombination distributions in mammals.
    Nat Rev Genet. 2004 Jun;5(6):413-24 PMID: 15153994
  85. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis.
    Development. 2003 Jul;130(14):3309-18 PMID: 12783800
  86. Examination of the intron in the meiosis-specific recombination gene REC114 in Saccharomyces.
    Mol Gen Genet. 1997 Jul;255(4):410-9 PMID: 9267437
  87. The control of Spo11's interaction with meiotic recombination hotspots.
    Genes Dev. 2005 Jan 15;19(2):255-69 PMID: 15655113
  88. Both conserved and non-conserved regions of Spo11 are essential for meiotic recombination initiation in yeast.
    Mol Genet Genomics. 2006 Oct;276(4):313-21 PMID: 16816949
  89. A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis.
    Curr Biol. 2005 Jan 26;15(2):185-91 PMID: 15668177
  90. AtSPO11-1 is necessary for efficient meiotic recombination in plants.
    EMBO J. 2001 Feb 1;20(3):589-600 PMID: 11157765
  91. Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast.
    Curr Biol. 2005 Sep 20;15(18):1663-9 PMID: 16169489
  92. The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae.
    EMBO J. 1995 Sep 15;14(18):4589-98 PMID: 7556102
  93. Regulation of premeiotic S phase and recombination-related double-strand DNA breaks during meiosis in fission yeast.
    Nat Genet. 2001 Jul;28(3):290-3 PMID: 11431703
  94. Toprim--a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins.
    Nucleic Acids Res. 1998 Sep 15;26(18):4205-13 PMID: 9722641
  95. Meiotic effects of DNA-defective cell division cycle mutations of Saccharomyces cerevisiae.
    Chromosoma. 1978 Dec 21;70(1):109-30 PMID: 367734
  96. Linear element-independent meiotic recombination in Schizosaccharomyces pombe.
    Genetics. 2006 Nov;174(3):1105-14 PMID: 16980386
  97. SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis.
    Genes Dev. 2001 Jul 15;15(14):1859-71 PMID: 11459834
  98. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family.
    Cell. 1997 Feb 7;88(3):375-84 PMID: 9039264
  99. The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control in meiosis.
    EMBO J. 1999 Oct 15;18(20):5714-23 PMID: 10523314
  100. Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8395-402 PMID: 11459981
  101. Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required for meiotic double-strand break formation.
    Genetics. 2006 Aug;173(4):1969-81 PMID: 16783010
  102. Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases.
    Annu Rev Biophys Biomol Struct. 2004;33:95-118 PMID: 15139806
  103. DNA topoisomerases: structure, function, and mechanism.
    Annu Rev Biochem. 2001;70:369-413 PMID: 11395412
  104. B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis.
    Curr Biol. 2001 Jan 23;11(2):88-97 PMID: 11231124
  105. Extensive 3'-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site.
    Cell. 1991 Mar 22;64(6):1155-61 PMID: 2004421
  106. Coupling of Saccharomyces cerevisiae early meiotic gene expression to DNA replication depends upon RPD3 and SIN3.
    Genetics. 2001 Feb;157(2):545-56 PMID: 11156977
  107. Chromosome cores and chromatin at meiotic prophase.
    Curr Top Dev Biol. 1998;37:241-62 PMID: 9352188
  108. Region-specific activators of meiotic recombination in Schizosaccharomyces pombe.
    Genes Dev. 1994 Jan;8(2):203-10 PMID: 8299939
  109. 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. 1995 May;15(5):2763-71 PMID: 7739557
  110. DNA topoisomerase VI is essential for endoreduplication in Arabidopsis.
    Curr Biol. 2002 Oct 15;12(20):1782-6 PMID: 12401175
  111. Xrs2p regulates Mre11p translocation to the nucleus and plays a role in telomere elongation and meiotic recombination.
    Mol Biol Cell. 2005 Feb;16(2):597-608 PMID: 15548595
  112. Seventeen complementation groups of mutations decreasing meiotic recombination in Schizosaccharomyces pombe.
    Genetics. 1992 Feb;130(2):251-62 PMID: 1541389
  113. RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18736-41 PMID: 16339310
  114. A DNA binding motif of meiotic recombinase Rec12 (Spo11) defined by essential glycine-202, and persistence of Rec12 protein after completion of recombination.
    Gene. 2005 Aug 15;356:77-84 PMID: 16009511
  115. Ski7p G protein interacts with the exosome and the Ski complex for 3'-to-5' mRNA decay in yeast.
    EMBO J. 2001 Sep 3;20(17):4684-93 PMID: 11532933
  116. Phylogenomics of type II DNA topoisomerases.
    Bioessays. 2003 Mar;25(3):232-42 PMID: 12596227
  117. Toward the genetics of mammalian reproduction: induction and mapping of gametogenesis mutants in mice.
    Biol Reprod. 2003 Nov;69(5):1615-25 PMID: 12855593
  118. Mei1 is epistatic to Dmc1 during mouse meiosis.
    Chromosoma. 2005 Jul;114(2):127-34 PMID: 15928951
  119. 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. 1996 Jul;143(3):1115-25 PMID: 8807286
  120. Meiotic recombination remote from prominent DNA break sites in S. pombe.
    Mol Cell. 2002 Feb;9(2):253-63 PMID: 11864600
  121. Isolation and characterization of novel xrs2 mutations in Saccharomyces cerevisiae.
    Genetics. 2005 May;170(1):71-85 PMID: 15716496
  122. Meiotic recombination hotspots: shaping the genome and insights into hypervariable minisatellite DNA change.
    Curr Top Dev Biol. 1998;37:37-75 PMID: 9352183
  123. Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli.
    Nucleic Acids Res. 1998 Nov 15;26(22):5157-62 PMID: 9801313
  124. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination.
    Cell. 1990 May 4;61(3):419-36 PMID: 2185891
  125. Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana.
    Nucleic Acids Res. 2000 Apr 1;28(7):1548-54 PMID: 10710421
  126. Involvement of the MRE2 gene of yeast in formation of meiosis-specific double-strand breaks and crossover recombination through RNA splicing.
    Genes Cells. 1997 Jan;2(1):65-79 PMID: 9112441
  127. Recombination proteins in yeast.
    Annu Rev Genet. 2004;38:233-71 PMID: 15568977
  128. 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. 2004 Feb;24(4):1655-66 PMID: 14749381
  129. Relationship of DNA double-strand breaks to synapsis in Drosophila.
    J Cell Sci. 2003 Aug 1;116(Pt 15):3069-77 PMID: 12799415
  130. Meiotically induced rec7 and rec8 genes of Schizosaccharomyces pombe.
    Genetics. 1992 Sep;132(1):75-85 PMID: 1339382
  131. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis.
    Cell. 2004 Apr 2;117(1):29-45 PMID: 15066280
  132. Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex.
    Chromosoma. 2006 Jun;115(3):175-94 PMID: 16555016
  133. Saccharomyces cerevisiae Mer3 helicase stimulates 3'-5' heteroduplex extension by Rad51; implications for crossover control in meiotic recombination.
    Cell. 2004 Apr 2;117(1):47-56 PMID: 15066281
  134. mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved.
    Genes Dev. 1998 Sep 15;12(18):2932-42 PMID: 9744869
  135. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells.
    Nucleic Acids Res. 1997 Aug 1;25(15):2985-91 PMID: 9224597
  136. Activation of an alternative, rec12 (spo11)-independent pathway of fission yeast meiotic recombination in the absence of a DNA flap endonuclease.
    Genetics. 2005 Dec;171(4):1499-511 PMID: 16118186
  137. A novel recombination pathway initiated by the Mre11/Rad50/Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe.
    Genetics. 2005 Mar;169(3):1261-74 PMID: 15654094
  138. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice.
    Curr Biol. 2001 Jan 23;11(2):105-9 PMID: 11231126
  139. Cdc7p-Dbf4p becomes famous in the cell cycle.
    J Cell Sci. 2000 Jun;113 ( Pt 12):2111-7 PMID: 10825284
  140. Checking your breaks: surveillance mechanisms of meiotic recombination.
    Curr Biol. 2006 Mar 21;16(6):R217-28 PMID: 16546077
  141. Meiosis-induced double-strand break sites determined by yeast chromatin structure.
    Science. 1994 Jan 28;263(5146):515-8 PMID: 8290959
  142. Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11.
    EMBO J. 1999 Nov 1;18(21):6177-88 PMID: 10545127
  143. Interactions between BRCT repeats and phosphoproteins: tangled up in two.
    Trends Biochem Sci. 2004 Nov;29(11):579-85 PMID: 15501676
  144. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together.
    DNA Repair (Amst). 2004 Aug-Sep;3(8-9):845-54 PMID: 15279769
  145. The mouse Spo11 gene is required for meiotic chromosome synapsis.
    Mol Cell. 2000 Nov;6(5):975-87 PMID: 11106738
  146. Identification and analysis of DYAD: a gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis.
    Development. 2002 Aug;129(16):3935-43 PMID: 12135930
  147. The THAP domain of THAP1 is a large C2CH module with zinc-dependent sequence-specific DNA-binding activity.
    Proc Natl Acad Sci U S A. 2005 May 10;102(19):6907-12 PMID: 15863623
  148. Meiotic DNA breaks associated with recombination in S. pombe.
    Mol Cell. 2000 May;5(5):883-8 PMID: 10882124
  149. Multiple sites for double-strand breaks in whole meiotic chromosomes of Saccharomyces cerevisiae.
    EMBO J. 1992 Sep;11(9):3441-7 PMID: 1324174
  150. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis.
    Cell. 2004 Apr 2;117(1):9-15 PMID: 15066278
  151. Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination.
    Plant J. 2006 Oct;48(2):206-16 PMID: 17018031
  152. Factors that affect the location and frequency of meiosis-induced double-strand breaks in Saccharomyces cerevisiae.
    Genetics. 1995 May;140(1):55-66 PMID: 7635308
  153. Rad50S alleles of the Mre11 complex: questions answered and questions raised.
    Exp Cell Res. 2006 Aug 15;312(14):2694-9 PMID: 16857186
  154. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair.
    Nature. 2002 Aug 1;418(6897):562-6 PMID: 12152085
  155. A yeast intronic splicing enhancer and Nam8p are required for Mer1p-activated splicing.
    Mol Cell. 2000 Aug;6(2):329-38 PMID: 10983980
  156. The yeast Red1 protein localizes to the cores of meiotic chromosomes.
    J Cell Biol. 1997 Mar 10;136(5):957-67 PMID: 9060462
  157. Suppressor analysis of the Saccharomyces cerevisiae gene REC104 reveals a genetic interaction with REC102.
    Genetics. 1999 Apr;151(4):1261-72 PMID: 10101155
  158. C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination.
    Cell. 2004 Aug 20;118(4):439-52 PMID: 15315757
  159. Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination.
    Chromosoma. 2004 Oct;113(4):197-203 PMID: 15309561
  160. Characterization of rec15, an early meiotic recombination gene in Schizosaccharomyces pombe.
    Curr Genet. 2005 Nov;48(5):323-33 PMID: 16252089
  161. High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing.
    Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1522-7 PMID: 17244705
  162. Identification of novel Drosophila meiotic genes recovered in a P-element screen.
    Genetics. 1999 Jun;152(2):529-42 PMID: 10353897
  163. 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. 1995 Oct 16;14(20):5115-28 PMID: 7588640
  164. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11383-90 PMID: 11027339
  165. Molecular characterization of homologues of both subunits A (SPO11) and B of the archaebacterial topoisomerase 6 in plants.
    Gene. 2001 Jun 13;271(1):81-6 PMID: 11410368
  166. A WD repeat protein, Rec14, essential for meiotic recombination in Schizosaccharomyces pombe.
    Genetics. 1997 Aug;146(4):1253-64 PMID: 9258671
  167. The FHA domain.
    FEBS Lett. 2002 Feb 20;513(1):58-66 PMID: 11911881
  168. Mammalian meiosis involves DNA double-strand breaks with 3' overhangs.
    Chromosoma. 2003 Mar;111(6):369-76 PMID: 12644952
  169. Un ménage à quatre: the molecular biology of chromosome segregation in meiosis.
    Cell. 2003 Feb 21;112(4):423-40 PMID: 12600308
  170. Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing.
    J Cell Sci. 2003 May 1;116(Pt 9):1719-31 PMID: 12665553
  171. A 160-bp palindrome is a Rad50.Rad32-dependent mitotic recombination hotspot in Schizosaccharomyces pombe.
    Genetics. 2002 May;161(1):461-8 PMID: 12019258
  172. Direct coupling between meiotic DNA replication and recombination initiation.
    Science. 2000 Oct 27;290(5492):806-9 PMID: 11052944
  173. Ama1p is a meiosis-specific regulator of the anaphase promoting complex/cyclosome in yeast.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14548-53 PMID: 11114178
  174. Chromosome choreography: the meiotic ballet.
    Science. 2003 Aug 8;301(5634):785-9 PMID: 12907787
  175. DNA polymerase I is required for premeiotic DNA replication and sporulation but not for X-ray repair in Saccharomyces cerevisiae.
    Mol Cell Biol. 1989 Feb;9(2):365-76 PMID: 2651896
  176. 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. 2006 Jan 20;281(3):1338-44 PMID: 16286472
  177. Meiotic recombination hotspots.
    Annu Rev Genet. 1995;29:423-44 PMID: 8825482
  178. Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe.
    Genetics. 2001 Feb;157(2):519-32 PMID: 11156975
  179. An intron-containing meiosis-induced recombination gene, rec15, of Schizosaccharomyces pombe.
    Mol Microbiol. 1995 Aug;17(3):439-48 PMID: 8559063
  180. Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females.
    PLoS Genet. 2006 Nov 24;2(11):e200 PMID: 17166055
  181. Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution.
    EMBO J. 2003 Jan 2;22(1):151-63 PMID: 12505993
  182. Distribution of meiotic recombination sites.
    Trends Genet. 2003 Sep;19(9):514-22 PMID: 12957545
  183. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae.
    Cell. 1991 Sep 20;66(6):1239-56 PMID: 1913808
  184. The cohesion protein ORD is required for homologue bias during meiotic recombination.
    J Cell Biol. 2004 Mar 15;164(6):819-29 PMID: 15007062
  185. Cdc7 kinase complex: a key regulator in the initiation of DNA replication.
    J Cell Physiol. 2002 Mar;190(3):287-96 PMID: 11857444
  186. An mre11 mutant of Coprinus cinereus has defects in meiotic chromosome pairing, condensation and synapsis.
    Genetics. 2000 Mar;154(3):1125-39 PMID: 10757758
  187. H2AX: the histone guardian of the genome.
    DNA Repair (Amst). 2004 Aug-Sep;3(8-9):959-67 PMID: 15279782
  188. DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway.
    Genetics. 1997 Oct;147(2):533-44 PMID: 9335591
  189. The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint.
    Mol Cell Biol. 2003 Sep;23(18):6564-73 PMID: 12944482
  190. Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae.
    Genetics. 1997 Jul;146(3):781-95 PMID: 9215887
  191. The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo.
    RNA. 2000 Mar;6(3):449-57 PMID: 10744028
  192. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination.
    EMBO J. 1998 Nov 2;17(21):6412-25 PMID: 9799249
  193. 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. 1998 Mar 2;17(5):1497-506 PMID: 9482746
  194. Mechanism and control of meiotic recombination initiation.
    Curr Top Dev Biol. 2001;52:1-53 PMID: 11529427
  195. Chemical inactivation of cdc7 kinase in budding yeast results in a reversible arrest that allows efficient cell synchronization prior to meiotic recombination.
    Genetics. 2006 Dec;174(4):1767-74 PMID: 17057233
  196. The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate.
    EMBO J. 1995 Sep 15;14(18):4599-608 PMID: 7556103
  197. 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. 2003 Aug;35(4):465-75 PMID: 12904209
  198. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein.
    Cell. 1992 May 1;69(3):457-70 PMID: 1581961
  199. DNA topoisomerase VI generates ATP-dependent double-strand breaks with two-nucleotide overhangs.
    J Biol Chem. 2001 Oct 5;276(40):37215-22 PMID: 11485995
  200. A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):10191-6 PMID: 12119417
  201. Mutations in U1 snRNA bypass the requirement for a cell type-specific RNA splicing factor.
    Cell. 1993 Apr 23;73(2):407-15 PMID: 8477451
  202. GHKL, an emergent ATPase/kinase superfamily.
    Trends Biochem Sci. 2000 Jan;25(1):24-8 PMID: 10637609
  203. Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice.
    Mol Cell. 2003 Dec;12(6):1511-23 PMID: 14690604
  204. Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5' to 3' mRNA decay pathways in yeast.
    Mol Cell. 2003 Dec;12(6):1439-52 PMID: 14690598
  205. Domain interactions within the Ski2/3/8 complex and between the Ski complex and Ski7p.
    RNA. 2005 Aug;11(8):1291-302 PMID: 16043509
  206. Recombinational DNA double-strand breaks in mice precede synapsis.
    Nat Genet. 2001 Mar;27(3):271-6 PMID: 11242108
  207. A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events.
    Curr Biol. 2005 Nov 22;15(22):2056-62 PMID: 16303567
  208. Cohesin Rec8 is required for reductional chromosome segregation at meiosis.
    Nature. 1999 Jul 29;400(6743):461-4 PMID: 10440376
  209. Genome-wide redistribution of meiotic double-strand breaks in Saccharomyces cerevisiae.
    Mol Cell Biol. 2007 Mar;27(5):1868-80 PMID: 17189430
  210. Chromosome pairing and meiotic recombination in Neurospora crassa spo11 mutants.
    Curr Genet. 2006 Aug;50(2):115-23 PMID: 16758206
  211. Meiotic recombination-deficient mutants of Schizosaccharomyces pombe.
    Genetics. 1989 Sep;123(1):45-54 PMID: 2806887
  212. Meiotic cells monitor the status of the interhomolog recombination complex.
    Genes Dev. 1997 Jan 1;11(1):106-18 PMID: 9000054
  213. Association of Mre11p with double-strand break sites during yeast meiosis.
    Mol Cell. 2004 Feb 13;13(3):389-401 PMID: 14967146
  214. Insertional mutations in the yeast HOP1 gene: evidence for multimeric assembly in meiosis.
    Genetics. 1994 Feb;136(2):449-64 PMID: 8150275
  215. The G1/S cyclin Cig2p during meiosis in fission yeast.
    Mol Biol Cell. 2002 Jun;13(6):2080-90 PMID: 12058071
  216. mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in Drosophila melanogaster.
    Genetics. 2002 Sep;162(1):245-58 PMID: 12242237
  217. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression.
    Cell. 1992 May 1;69(3):439-56 PMID: 1581960
  218. Transient, meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe.
    Genetics. 1994 Mar;136(3):769-79 PMID: 8005432
  219. The Synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila.
    Curr Biol. 2003 Feb 18;13(4):276-85 PMID: 12593793
  220. 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. 1997 Jul;146(3):797-816 PMID: 9215888
  221. Meiotic synapsis in the absence of recombination.
    Science. 1998 Feb 6;279(5352):876-8 PMID: 9452390
  222. 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. 1999 Aug;4(8):425-44 PMID: 10526232
  223. RED1: a yeast gene required for the segregation of chromosomes during the reductional division of meiosis.
    Proc Natl Acad Sci U S A. 1988 Aug;85(16):6057-61 PMID: 3413075
  224. Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis.
    Plant Cell. 2004 Aug;16(8):1968-78 PMID: 15258261
  225. Crystal structure of Ski8p, a WD-repeat protein with dual roles in mRNA metabolism and meiotic recombination.
    Protein Sci. 2004 Oct;13(10):2673-84 PMID: 15340168
  226. Distinct cohesin complexes organize meiotic chromosome domains.
    Science. 2003 May 16;300(5622):1152-5 PMID: 12750522
  227. Binding of a cell-type-specific RNA splicing factor to its target regulatory sequence.
    Mol Cell Biol. 1995 Apr;15(4):1953-60 PMID: 7891689
  228. Pairing sites and the role of chromosome pairing in meiosis and spermatogenesis in male Drosophila.
    Curr Top Dev Biol. 1998;37:77-115 PMID: 9352184
  229. Mer1p is a modular splicing factor whose function depends on the conserved U2 snRNP protein Snu17p.
    Nucleic Acids Res. 2004 Feb 18;32(3):1242-50 PMID: 14973223
  230. Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe.
    Chromosoma. 2006 Aug;115(4):330-40 PMID: 16532353
  231. The Rad50 hook domain is a critical determinant of Mre11 complex functions.
    Nat Struct Mol Biol. 2005 May;12(5):403-7 PMID: 15852023
Article Info
Journal
Genome dynamics and stability
Abbr.
Genome Dyn Stab
ISSN
1861-3373
DOI
10.1007/7050_2007_026
Email
[email protected]
Published
2008-01-01
Pages
81-123
Language
English
Region
Germany
NLM ID
101521084
PMCID
PMC3172816
Grants
NIGMS NIH HHS · R01 GM058673 · United States
NIGMS NIH HHS · R01 GM058673-01 · United States
NICHD NIH HHS · R01 HD040916 · United States
NICHD NIH HHS · R01 HD040916-01 · United States
External Links
PubMed source DOI: 10.1007/7050_2007_026 PMC Full Text
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2