PP2ACdc55 is required for multiple events during meiosis I

Cell Cycle

Volumn 10, Issue 9, 2011, Pages 1420-1434

  Nolt, Jocelyn K ^a,c   Rice, Lyndi M ^a   Gallo Ebert, Christina ^a   Bisher, Margaret E ^b   Nickels, Joseph T ^a  

^a Venenum Biodesign   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

DNA replication; Homologous recombination; Meiosis; Protein phosphatase 2A

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN CDC55; PROTEIN RAD9; REGULATOR PROTEIN; UNCLASSIFIED DRUG; CDC55 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2; SACCHAROMYCES CEREVISIAE PROTEIN;

ALLELE; ARTICLE; DNA REPLICATION; GENE EXPRESSION; HOMOLOGOUS RECOMBINATION; MEIOSIS; MICROTUBULE; NONHUMAN; PACHYTENE; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; SPINDLE POLE BODY; SPOROGENESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MUTATION; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; DNA REPLICATION; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; MEIOSIS; MUTATION; PROTEIN PHOSPHATASE 2; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 79955583900     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.9.15485     Document Type: Article

References (112)

1. Handel MA, Schimenti JC. Genetics of mammalian meiosis: Regulation, dynamics and impact on fertility. Nat Rev Genet 2010; 11:124-36.
2. Hiraoka Y, Dernburg AF. The SUN rises on meiotic chromosome dynamics. Dev Cell 2009; 17:598-605.
3. Wood AJ, Severson AF, Meyer BJ. Condensin and cohesin complexity: The expanding repertoire of functions. Nat Rev Genet 2010; 11:391-404.
4. Wolgemuth DJ, Roberts SS. Regulating mitosis and meiosis in the male germ line: Critical functions for cyclins. Philos Trans R Soc Lond B Biol Sci 2010; 365:1653-62.
5. Forsburg SL. Only connect: Linking meiotic DNA replication to chromosome dynamics. Mol Cell 2002; 9:703-11. (Pubitemid 34454883)
6. Yanowitz J. Meiosis: Making a break for it. Curr Opin Cell Biol 2010.
7. Berchowitz LE, Copenhaver GP. Genetic interference: Don't stand so close to me. Curr Genomics 2010; 11:91-102.
8. Cohen PT, Brewis ND, Hughes V, Mann DJ. Protein serine/threonine phosphatases; an expanding family. FEBS Lett 1990; 268:355-9. (Pubitemid 20241342)
9. Shi Y. Serine/threonine phosphatases: Mechanism through structure. Cell 2009; 139:468-84.
10. Eichhorn PJ, Creyghton MP, Bernards R. Protein phosphatase 2A regulatory subunits and cancer. Biochim Biophys Acta 2009; 1795:1-15.
11. Janssens V, Longin S, Goris J. PP2A holoenzyme assembly: In cauda venenum (the sting is in the tail). Trends Biochem Sci 2008; 33:113-21.
12. Arroyo JD, Hahn WC. Involvement of PP2A in viral and cellular transformation. Oncogene 2005; 24:7746-55. (Pubitemid 41670676)
13. Harris SL, Levine AJ. The p53 pathway: Positive and negative feedback loops. Oncogene 2005; 24:2899-908. (Pubitemid 40638098)
14. Chen W, Possemato R, Campbell KT, Plattner CA, Pallas DC, Hahn WC. Identification of specific PP2A complexes involved in human cell transformation. Cancer Cell 2004; 5:127-36. (Pubitemid 38283799)
15. Westermarck JHW. Multiple pathways regulated by the tumor suppressor PP2A in transformation. Trends Mol Med 2008; 14:152-60.
16. Duvel K, Santhanam A, Garrett S, Schneper L, Broach JR. Multiple roles of Tap42 in mediating rapamycininduced transcriptional changes in yeast. Mol Cell 2003; 11:1467-78. (Pubitemid 36776534)
17. Schneper L, Duvel K, Broach JR. Sense and sensibility: Nutritional response and signal integration in yeast. Curr Opin Microbiol 2004; 7:624-30. (Pubitemid 39536289)
18. Lin FC, Arndt KT. The role of Saccharomyces cerevisiae type 2A phosphatase in the actin cytoskeleton and in entry into mitosis. EMBO J 1995; 14:2745-59.
19. van Zyl W, Huang W, Sneddon AA, Stark M, Camier S, Werner M, et al. Inactivation of the protein phosphatase 2A regulatory subunit A results in morphological and transcriptional defects in Saccharomyces cerevisiae. Mol Cell Biol 1992; 12:4946-59.
20. Junttila MR, Li SP, Westermarck J. Phosphatasemediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J 2008; 22:954-65. (Pubitemid 351519953)
21. van Zyl WH, Wills N, Broach JR. A general screen for mutant of Saccharomyces cerevisiae deficient in tRNA biosynthesis. Genetics 1989; 123:55-68.
22. Mellgren G, Vintermyr OK, Boe R, Doskeland SO. Hepatocyte DNA replication is abolished by inhibitors selecting protein phosphatase 2A rather than phosphatase 1. Exp Cell Res 1993; 205:293-301. (Pubitemid 23192134)
23. Lin XH, Walter J, Scheidtmann K, Ohst K, Newport J, Walter G. Protein phosphatase 2A is required for the initiation of chromosomal DNA replication. Proc Natl Acad Sci USA 1998; 95:14693-8. (Pubitemid 29003692)
24. Yan Z, Fedorov SA, Mumby MC, Williams RS. PR48, a novel regulatory subunit of protein phosphatase 2A, interacts with Cdc6 and modulates DNA replication in human cells. Mol Cell Biol 2000; 20:1021-9. (Pubitemid 30044239)
25. Chou DM, Petersen P, Walter JC, Walter G. Protein phosphatase 2A regulates binding of Cdc45 to the prereplication complex. J Biol Chem 2002; 277:40520-7. (Pubitemid 35215630)
26. Feng J, Wakeman T, Yong S, Wu X, Kornbluth S, Wang XF. Protein phosphatase 2A-dependent dephosphorylation of replication protein A is required for the repair of DNA breaks induced by replication stress. Mol Cell Biol 2009; 29:5696-709.
27. Dehde S, Rohaly G, Schub O, Nasheuer HP, Bohn W, Chemnitz J, et al. Two immunologically distinct human DNA polymerase alpha-primase subpopulations are involved in cellular DNA replication. Mol Cell Biol 2001; 21:2581-93. (Pubitemid 32222109)
28. Stark MJ, Black S, Sneddon AA, Andrews PD. Genetic analyses of yeast protein serine/threonine phosphatases. FEMS Microbiol Lett 1994; 117:121-30. (Pubitemid 24097088)
29. Ronne H, Carlberg M, Hu GZ, Nehlin JO. Protein phosphatase 2A in Saccharomyces cerevisiae: Effects on cell growth and bud morphogenesis. Mol Cell Biol 1991; 11:4876-84.
30. Healy AM, Zolnierowicz S, Stapleton AE, Goebl M, DePaoli-Roach AA, Pringle JR. CDC55, a Saccharomyces cerevisiae gene involved in cellular morphogenesis: Identification, characterization and homology to the B subunit of mammalian type 2A protein phosphatase. Mol Cell Biol 1991; 11:5767-80.
31. Shu Y, Yang H, Hallberg E, Hallberg R. Molecular genetic analysis of Rts1p, a B' regulatory subunit of Saccharomyces cerevisiae protein phosphatase 2A. Mol Cell Biol 1997; 17:3242-53.
32. Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 2006; 441:53-61.
33. Wang Y, Burke DJ. Cdc55p, the B-type regulatory subunit of protein phosphatase 2A, has multiple functions in mitosis and is required for the kinetochore/spindle checkpoint in Saccharomyces cerevisiae. Mol Cell Biol 1997; 17:620-6. (Pubitemid 27044361)
34. Yellman CM, Burke DJ. The role of Cdc55 in the spindle checkpoint is through regulation of mitotic exit in Saccharomyces cerevisiae. Mol Biol Cell 2006; 17:658-66. (Pubitemid 43191101)
35. Tang X, Wang Y. Pds1/Esp1-dependent and -independent sister chromatid separation in mutants defective for protein phosphatase 2A. Proc Natl Acad Sci USA 2006; 103:16290-5. (Pubitemid 44715189)
36. Wang Y, Ng TY. Phosphatase 2A negatively regulates mitotic exit in Saccharomyces cerevisiae. Mol Biol Cell 2006; 17:80-9. (Pubitemid 43049463)
37. Queralt E, Uhlmann F. Separase cooperates with Zds1 and Zds2 to activate Cdc14 phosphatase in early anaphase. J Cell Biol 2008; 182:873-83.
38. Visintin C, Tomson BN, Rahal R, Paulson J, Cohen M, Taunton J, et al. APC/C-Cdh1-mediated degradation of the Polo kinase Cdc5 promotes the return of Cdc14 into the nucleolus. Genes Dev 2008; 22:79-90.
39. Clift D, Bizzari F, Marston AL. Shugoshin prevents cohesin cleavage by PP2A(Cdc55)-dependent inhibition of separase. Genes Dev 2009; 23:766-80.
40. Perdiguero E, Nebreda AR. Regulation of Cdc25C activity during the meiotic G2/M transition. Cell Cycle 2004; 3:733-7. (Pubitemid 40187901)
41. Pal G, Paraz MT, Kellogg DR. Regulation of Mih1/ Cdc25 by protein phosphatase 2A and casein kinase 1. J Cell Biol 2008; 180:931-45. (Pubitemid 351398420)
42. Trinkle-Mulcahy L, Lamond AI. Mitotic phosphatases: No longer silent partners. Curr Opin Cell Biol 2006; 18:623-31. (Pubitemid 44692470)
43. Xu Z, Cetin B, Anger M, Cho US, Helmhart W, Nasmyth K, et al. Structure and function of the PP2Ashugoshin interaction. Mol Cell 2009; 35:426-41.
44. Ishiguro T, Tanaka K, Sakuno T, Watanabe Y. Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 2010; 12:500-6.
45. Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, et al. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 2006; 441:46-52.
46. Di Como CJ, Arndt KT. Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev 1996; 10:1904-16. (Pubitemid 26281685)
47. Primig M, Williams RM, Winzeler EA, Tevzadze GG, Conway AR, Hwang SY, et al. The core meiotic transcriptome in budding yeasts. Nat Genet 2000; 26:415-23.
48. Williams RM. The yeast lifecycle and DNA array technology. J Ind Microbiol Biotechnol 2002; 28:186-91.
49. Smith HE, Mitchell AP. A transcriptional cascade governs entry into meiosis in Saccharomyces cerevisiae. Mol Cell Biol 1989; 9:2142-52. (Pubitemid 19117815)
50. Mitchell AP, Driscoll SE, Smith HE. Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol Cell Biol 1990; 10:2104-10.
51. Mitchell AP. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev 1994; 58:56-70.
52. Kassir Y, Adir N, Boger-Nadjar E, Raviv NG, Rubin- Bejerano I, Sagee S, et al. Transcriptional regulation of meiosis in budding yeast. Int Rev Cytol 2003; 224:111-71. (Pubitemid 36538042)
53. Aparicio JG, Viggiani CJ, Gibson DG, Aparicio OM. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol Cell Biol 2004; 24:4769-80. (Pubitemid 38668043)
54. Brewer BJ, Fangman WL. Initiation preference at a yeast origin of replication. Proc Natl Acad Sci USA 1994; 91:3418-22. (Pubitemid 24130248)
55. Early A, Drury LS, Diffley JF. Mechanisms involved in regulating DNA replication origins during the cell cycle and in response to DNA damage. Philos Trans R Soc Lond B Biol Sci 2004; 359:31-8. (Pubitemid 38106445)
56. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9:616-27. (Pubitemid 352032926)
57. Navadgi-Patil VM, Burgers PM. A tale of two tails: Activation of DNA damage checkpoint kinase Mec1/ ATR by the 9-1-1 clamp and by Dpb11/TopBP1. DNA Repair (Amst) 2009; 8:996-1003.
58. Weber L, Byers B. A RAD9-dependent checkpoint blocks meiosis of cdc13 yeast cells. Genetics 1992; 131:55-63.
59. Zhao X, Muller EG, Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 1998; 2:329-40. (Pubitemid 128379273)
60. Murakami H, Nurse P. Meiotic DNA replication checkpoint control in fission yeast. Genes Dev 1999; 13:2581-93. (Pubitemid 29489649)
61. Hollingsworth NM. Deconstructing meiosis one kinase at a time: Polo pushes past pachytene. Genes Dev 2008; 22:2596-600.
62. Xu L, Ajimura M, Padmore R, Klein C, Kleckner N. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol 1995; 15:6572-81.
63. Knop M, Pereira G, Geissler S, Grein K, Schiebel E. The spindle pole body component Spc97p interacts with the gamma-tubulin of Saccharomyces cerevisiae and functions in microtubule organization and spindle pole body duplication. EMBO J 1997; 16:1550-64.
64. Shuster EO, Byers B. Pachytene arrest and other meiotic effects of the start mutations in Saccharomyces cerevisiae. Genetics 1989; 123:29-43. (Pubitemid 19233888)
65. Pankratz DG, Forsburg SL. Meiotic S-phase damage activates recombination without checkpoint arrest. Mol Biol Cell 2005; 16:1651-60. (Pubitemid 40471937)
66. Meier B, Ahmed S. Checkpoints: Chromosome pairing takes an unexpected twist. Curr Biol 2001; 11:865-8.
67. Baudat F, Keeney S. Meiotic recombination: Making and breaking go hand in hand. Curr Biol 2001; 11:45-8.
68. Haber JE. Recombination: A frank view of exchanges and vice versa. Curr Opin Cell Biol 2000; 12:286-92. (Pubitemid 30265056)
69. Cao L, Alani E, Kleckner N. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 1990; 61:1089-101.
70. Honigberg SM, Lee RH. Snf1 kinase connects nutritional pathways controlling meiosis in Saccharomyces cerevisiae. Mol Cell Biol 1998; 18:4548-55. (Pubitemid 28343039)
71. Lee RH, Honigberg SM. Nutritional regulation of late meiotic events in Saccharomyces cerevisiae through a pathway distinct from initiation. Mol Cell Biol 1996; 16:3222-32.
72. Baudat F, Nicolas A. Clustering of meiotic doublestrand breaks on yeast chromosome III. Proc Natl Acad Sci USA 1997; 94:5213-8. (Pubitemid 27214763)
73. Honigberg SM, Conicella C, Espositio RE. Commitment to meiosis in Saccharomyces cerevisiae: Involvement of the SPO14 gene. Genetics 1992; 130:703-16.
74. Honigberg SM, Esposito RE. Reversal of cell determination in yeast meiosis: Postcommitment arrest allows return to mitotic growth. Proc Natl Acad Sci USA 1994; 91:6559-63. (Pubitemid 24200701)
75. Menees TM, Roeder GS. MEI4, a yeast gene required for meiotic recombination. Genetics 1989; 123:675-82. (Pubitemid 20011813)
76. Klapholz S, Waddell CS, Esposito RE. The role of the SPO11 gene in meiotic recombination in yeast. Genetics 1985; 110:187-216. (Pubitemid 15116800)
77. Klapholz S, Esposito RE. Isolation of SPO12-1 and SPO13-1 from a natural variant of yeast that undergoes a single meiotic division. Genetics 1980; 96:567-88. (Pubitemid 11103701)
78. Jiao K, Salem L, Malone R. Support for a meiotic recombination initiation complex: Interactions among Rec102p, Rec104p and Spo11p. Mol Cell Biol 2003; 23:5928-38. (Pubitemid 36951353)
79. Tung KS, Hong EJ, Roeder GS. The pachytene checkpoint prevents accumulation and phosphorylation of the meiosis-specific transcription factor Ndt80. Proc Natl Acad Sci USA 2000; 97:12187-92.
80. Roeder GS, Bailis JM. The pachytene checkpoint. Trends Genet 2000; 16:395-403. (Pubitemid 30665372)
81. Lydall D, Nikolsky Y, Bishop DK, Weinert T. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 1996; 383:840-3.
82. Rockmill B, Sym M, Scherthan H, Roeder GS. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 1995; 9:2684-95.
83. Leu JY, Roeder GS. The pachytene checkpoint in S. cerevisiae depends on Swe1-mediated phosphorylation of the cyclin-dependent kinase Cdc28. Mol Cell 1999; 4:805-14.
84. Yang H, Jiang W, Gentry M, Hallberg RL. Loss of a protein phosphatase 2A regulatory subunit (Cdc55p) elicits improper regulation of Swe1p degradation. Mol Cell Biol 2000; 20:8143-56.
85. Rice LM, Plakas C, Nickels JT Jr. Loss of meiotic rereplication block in Saccharomyces cerevisiae cells defective in Cdc28p regulation. Eukaryot Cell 2005; 4:55-62.
86. Stuart D, Wittenberg C. CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev 1998; 12:2698-710. (Pubitemid 28420650)
87. Dirick L, Goetsch L, Ammerer G, Byers B. Regulation of meiotic S phase by Ime2 and a Clb5,6-associated kinase in Saccharomyces cerevisiae. Science 1998; 281:1854-7. (Pubitemid 28450506)
88. Bowdish KS, Yuan HE, Mitchell AP. Analysis of RIM11, a yeast protein kinase that phosphorylates the meiotic activator IME1. Mol Cell Biol 1994; 14:7909-19. (Pubitemid 24373540)
89. Malathi K, Xiao Y, Mitchell AP. Interaction of yeast repressor-activator protein Ume6p with glycogen synthase kinase 3 homolog Rim11p. Mol Cell Biol 1997; 17:7230-6. (Pubitemid 27505953)
90. Xiao Y, Mitchell AP. Shared roles of yeast glycogen synthase kinase 3 family members in nitrogen-responsive phosphorylation of meiotic regulator Ume6p. Mol Cell Biol 2000; 20:5447-53. (Pubitemid 30482882)
91. Gentry MS, Hallberg RL. Localization of Saccharomyces cerevisiae protein phosphatase 2A subunits throughout mitotic cell cycle. Mol Biol Cell 2002; 13:3477-92.
92. Colomina N, Gari E, Gallego C, Herrero E, Aldea M. G1 cyclins block the Ime1 pathway to make mitosis and meiosis incompatible in budding yeast. EMBO J 1999; 18:320-9. (Pubitemid 29041941)
93. Lamb TM, Mitchell AP. Coupling of Saccharomyces cerevisiae early meiotic gene expression to DNA replication depends upon RPD3 and SIN3. Genetics 2001; 157:545-56.
94. Bowdish KS, Yuan HE, Mitchell AP. Positive control of yeast meiotic genes by the negative regulator UME6. Mol Cell Biol 1995; 15:2955-61.
95. Krogh BO, Symington LS. Recombination proteins in yeast. Annu Rev Genet 2004; 38:233-71. (Pubitemid 40013729)
96. McMahill MS, Sham CW, Bishop DK. Synthesisdependent strand annealing in meiosis. PLoS Biol 2007; 5:299.
97. Kass EM, Jasin M. Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 2010; 584:3703-8.
98. Paques F, Haber JE. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 1999; 63:349-404. (Pubitemid 29264976)
99. Shinohara M, Sakai K, Ogawa T, Shinohara A. The mitotic DNA damage checkpoint proteins Rad17 and Rad24 are required for repair of double-strand breaks during meiosis in yeast. Genetics 2003; 164:855-65. (Pubitemid 36935665)
100. Chu S, Herskowitz I. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol Cell 1998; 1:685-96. (Pubitemid 128379246)
101. Hepworth SR, Friesen H, Segall J. NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae. Mol Cell Biol 1998; 18:5750-61. (Pubitemid 28450526)
102. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 2004; 431:1011-7. (Pubitemid 39434425)
103. Caspari T, Murray JM, Carr AM. Cdc2-cyclin B kinase activity links Crb2 and Rqh1-topoisomerase III. Genes Dev 2002; 16:1195-208. (Pubitemid 34553101)
104. Shrivastav M, De Haro LP, Nickoloff JA. Regulation of DNA double-strand break repair pathway choice. Cell Res 2008; 18:134-47.
105. Minshull J, Straight A, Rudner AD, Dernburg AF, Belmont A, Murray AW. Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr Biol 1996; 6:1609-20. (Pubitemid 27050228)
106. Yu HG, Koshland D. The Aurora kinase Ipl1 maintains the centromeric localization of PP2A to protect cohesin during meiosis. J Cell Biol 2007; 176:911-8. (Pubitemid 46506965)
107. Falk JE, Chan AC, Hoffmann E, Hochwagen A. A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 2010; 19:599-611.
108. Jessus C, Ozon R. Function and regulation of cdc25 protein phosphate through mitosis and meiosis. Prog Cell Cycle Res 1995; 1:215-28.
109. Marston AL, Lee BH, Amon A. The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation. Dev Cell 2003; 4:711-26. (Pubitemid 36564901)
110. Buonomo SB, Rabitsch KP, Fuchs J, Gruber S, Sullivan M, Uhlmann F, et al. Division of the nucleolus and its release of CDC14 during anaphase of meiosis I depends on separase, SPO12 and SLK19. Dev Cell 2003; 4:727-39. (Pubitemid 36564902)
111. Alani E, Padmore R, Kleckner N. Analysis of wildtype and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 1990; 61:419-36.
112. Borde V, Lin W, Novikov E, Petrini JH, Lichten M, Nicolas A. Association of Mre11p with double-strand break sites during yeast meiosis. Mol Cell 2004; 13:389-401. (Pubitemid 38229811)