Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family

Cell

Volumn 88, Issue 3, 1997, Pages 375-384

  Keeney, Scott ^a   Giroux, Craig N ^b   Kleckner, Nancy ^a  

^a HARVARD UNIVERSITY   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE; DOUBLE STRANDED DNA; ESTERASE; GENE PRODUCT; PROTEIN SUBUNIT;

ARTICLE; DNA CLEAVAGE; DNA PROTEIN COMPLEX; DNA STRAND BREAKAGE; GENETIC CONSERVATION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

ARCHAEA; NEMATODA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES POMBE; SCHIZOSACCHAROMYCES POMBE;

EID: 0030893115     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81876-0     Document Type: Article

References (61)

1. Ajimura, M., Leem, S.-H., and Ogawa, H. (1992). Identification of new genes required for meiotic recombination in Saccharomyces cerevisiae. Genetics 133, 51-66.
2. Alani, E., Padmore, R., and 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.
3. Bergerat, A., Gadelle, D., and Forterre, P. (1994). Purification of a DNA topoisomerase II from the hyperthermophilic archaeon Sulfolobus shibatae. J. Biol. Chem. 269, 27663-27669.
4. Bernard, F., Kezdy, K.E., Van Melderen, L., Steyaert, J., Wyns, L., Pato, M.L., Higgins, P.N., and Couturier, M. (1993). The F plasmid CcdB protein induces efficient ATP-dependent DNA cleavage by gyrase. J. Mol. Biol. 234, 534-541.
5. Bishop, D.K., Park, D., Xu, L., and 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.
6. Bullard, S.A., Kim, S., Galbraith, A.M., and Malone, R.E. (1996). Double strand breaks at the HIS2 recombination hot spot in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93, 13054-13059.
7. Bult, C.J., White, O., Olsen, G.J., et al. (1996). Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 1058-1073.
8. Cao, L., Alani, E., and Kleckner, N. (1990). A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61, 1089-1101.
9. Connelly, J.C., and Leach, D.R. F. (1996). The sbcC and sbcD genes of Escherichia coli encode a nuclease involved in palindrome inviability and genetic recombination. Genes to Cells 1, 285-291.
10. de Massy, B., Rocco, V., and 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.
11. Esposito, R.E., and Esposito, M.S. (1969). The genetic control of sporulation in Saccharomyces: I. The isolation of temperature-sensitive sporulation-deficient mutants. Genetics 61, 79-89.
12. Game, J.C., Sitney, K.C., Cook, V.E., and Mortimer, R.K. (1989). Use of a ring chromosome and pulsed-field gels to study interhomolog recombination, double-strand breaks, and sister-chromatid exchange in yeast. Genetics 123, 695-713.
13. Giroux, C.N., Dresser, M.E., and Tiano, H.F. (1989). Genetic control of chromosome synapsis in yeast meiosis. Genome 31, 88-94.
14. Giroux, C.N., Misra, S., Modesti, M., and Guerreiro, J. (1993). Decision points and the genetic control of meiosis. In Meiosis II: Contemporary Approaches to the Study of Meiosis, F. P. Haseltine and S. Heyner, eds. (Washington: AAAS), pp. 1-17.
15. Hollingsworth, N.M., Goetsch, L., and Byers, B. (1990). The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61, 73-84.
16. Ivanov, E.L., Korolev, V.G., and Fabre, F. (1992). XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics 132, 651-664.
17. Ivanov, E.L., Sugawara, N., White, C.I., Fabre, F., and Haber, J.E. (1994). Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 3414-3425.
18. Johzuka, K., and Ogawa, H. (1995). Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139, 1521-1532.
19. Kaiser, C., Michaelis, S., and Mitchell, A. (1994). Methods in Yeast Genetics (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
20. Kane, S., and Roth, R. (1974). Carbohydrate metabolism during ascospore development in yeast. J. Bacteriol. 118, 8-14.
21. Keeney, S., and 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.
22. Keeney, S., and Kleckner, N. (1996). Communication between homologous chromosomes: genetic alterations at a nuclease-hypersensitive site can alter mitotic chromatin structure at that site both in cis and in trans. Genes to Cells 1, 475-489.
23. Klapholz, S., Waddell, C.S., and Esposito, R.E. (1985). The role of the SPO11 gene in meiotic recombination in yeast. Genetics 110, 187-216.
24. Kleckner, N. (1996). Meiosis: how could it work? Proc. Natl. Acad. Sci. USA 93, 8167-8174.
25. Kleckner, N., and Weiner, B. (1993). Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic, and premeiotic cells. Cold Spring Harbor Symp. Quant. Biol. 58, 553-565.
26. Lin, Y., and Smith, G.R. (1994). Transient, meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe. Genetics 136, 769-779.
27. Liu, L.F., Rowe, T.C., Yang, L., Tewey, K.M., and Chen, G.L. (1983). Cleavage of DNA by mammalian DNA topoisomerase II. J. Biol. Chem. 258, 15365-15370.
28. Liu, J., Wu, T.C., and 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.
29. Loidl, J., Klein, F., and Scherthan, H. (1994). Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J. Cell Biol. 125, 1191-1200.
30. Mao-Draayer, Y., Galbraith, A.M., Pittman, D.L., Cool, M., and Malone, R. E. (1996). Analysis of meiotic recombination pathways in the yeast Saccharomyces cerevisiae. Genetics 144, 71-86.
31. McKee, A.H.Z., and Kleckner, N. (1997). A general method for identifying recessive diploid-specific mutations in S. cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase, and characterization of a new gene, SAE2. Genetics, in press.
32. McKee, B.D., Lumsden, S.E., and Das, S. (1993). The distribution of male meiotic pairing sites on chromosome 2 of Drosophila melanogaster: meiotic pairing and segregation of 2-Y transpositions. Chromosoma 102, 180-194.
33. Menees, T.M., Ross-MacDonald, P.B., and Roeder, G.S. (1992). MEI4, a meiosis-specific yeast gene required for chromosome synapsis. Mol. Cell. Biol. 72, 1340-1351.
34. Orr-Weaver, T.L. (1995). Meiosis in Drosophila: seeing is believing. Proc. Natl. Acad. Sci. USA 92, 10443-10449.
35. Padmore, R., Cao, L., and Kleckner, N. (1991). Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66, 1239-1256.
36. Prinz, S., Amon, A., and Klein, F. (1997). Isolation of COM1, a new gene required to complete meiotic double strand break induced recombination in S. cerevisiae. Genetics, in press.
37. Raymond, W.E., and Kleckner, N. (1993). RAD50 protein of S. cerevisiae exhibits ATP-dependent DNA binding. Nucl. Acids Res. 21, 3851-3856.
38. Roca, J., Berger, J.M., and Wang, J.C. (1993). On the simultaneous binding of eukaryotic DNA topoisomerase II to a pair of double-stranded helices. J. Biol. Chem. 268, 14250-14255.
39. Rocco, V., and Nicolas, A. (1996). Sensing of DNA non-homology lowers the initiation of meiotic recombination in yeast. Genes to Cells 7, 645-661.
40. Rockmill, B., Engebrecht, J.A., Scherthan, H., Loidl, J., and Roeder, G.S. (1995). The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics 141, 49-59.
41. Roeder, G.S. (1995). Sex and the single cell: meiosis in yeast. Proc. Natl. Acad. Sci. USA 92, 10450-10456.
42. 4-(5′-uridylyl)tyrosine is the bond between the genome-linked protein and the RNA of poliovirus. Proc. Natl. Acad. Sci. USA 75, 4868-4872.
43. Schiestl, R.H., Zhu, J., and Petes, T.D. (1994). Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 4493-4500.
44. Shabarova, Z.A. (1970). Synthetic nucleotide-peptides. Prog. Nucl. Acids Res. Mol. Biol. 10, 145-182.
45. Sharples, G.J., and Leach, D.R.F. (1995). Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol. Microbiol. 17, 1215-1217.
46. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
47. Smith, A.V., and Roeder, G.S. (1997). The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol., in press.
48. Smith, R.F., and Smith, T.F. (1990). Automatic generation of primary sequence patterns from sets of related protein sequences. Proc. Natl. Acad. Sci. USA 87, 118-122.
49. Sugawara, N., and Haber, J.E. (1992). Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol. Cell. Biol. 12, 563-575.
50. Sun, H., Treco, D., Schultes, N.P., and Szostak, J.W. (1989). Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338, 87-90.
51. Sun, H., Treco, D., and Szostak, J.W. (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.
52. Thomas, C.A., Jr., Saigo, K., McLeod, E., and Ito, J. (1979). The separation of DNA segments attached to proteins. Anal. Biochem. 93, 158-166.
53. Walter, J., Dever, C.A., and Biggin, M.D. (1994). Two homeo domain proteins bind with similar specificity to a wide range of DNA sites in Drosophila embryos. Genes Dev. 8, 1678-1692.
54. Wang, J.C. (1985). DNA topoisomerases. Annu. Rev. Biochem. 54, 665-697.
55. Weiner, B., and Kleckner, N. (1994). Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77, 977-991.
56. Wilson, R., Ainscough, R., Anderson, K., et al. (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368, 32-38.
57. Xu, F., and Petes, T.D. (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.
58. Xu, L., and 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.
59. Xu, L., Weiner, B., and Kleckner, N. (1997). Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev., in press.
60. Yang, S.-W., Burgin, A.B., Jr., Huizenga, B.N., Robertson, C.A., Yao, K.C., and Nash, H.A. (1996). A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proc. Natl. Acad. Sci. USA 93, 11534-11539.
61. Zubenko, G.S., and Jones, E.W. (1981). Protein degradation, meiosis, and sporulation in proteinase-deficient mutants of Saccharomyces cerevisiae. Genetics 97, 45-64.