A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene

EMBO Journal

Volumn 26, Issue 24, 2007, Pages 5061-5070

  Uanschou, Clemens ^a   Siwiec, Tanja ^a   Pedrosa Harand, Andrea ^a,e   Kerzendorfer, Claudia ^a,b   Sanchez Moran, Eugenio ^c   Novatchkova, Maria ^d   Akimcheva, Svetlana ^b   Woglar, Alexander ^a   Klein, Franz ^a   Schlögelhofer, Peter ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^e FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

Author keywords

Arabidopsis; CtIP; DNA repair; Meiosis; SAE2

Indexed keywords

DNA FRAGMENT; MITOMYCIN C;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; DNA REPAIR; EUKARYOTE; GENE IDENTIFICATION; GENE MUTATION; GENOME; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN INTERACTION; YEAST;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; DNA DAMAGE; DNA FRAGMENTATION; DNA REPAIR; DNA-BINDING PROTEINS; GENES, PLANT; HUMANS; MEIOSIS; MITOMYCIN; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; NUCLEIC ACID SYNTHESIS INHIBITORS; PHENOTYPE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARCHAEA; EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 37149054791     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601913     Document Type: Article

References (80)

1. Akutsu N, Iijima K, Hinata T, Tauchi H (2007) Characterization of the plant homolog of Nijmegen breakage syndrome 1: involvement in DNA repair and recombination. Biochem Biophys Res Commun 353: 394-398
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
3. Alexander MP (1969) Differential staining of aborted and non-aborted pollen. Stain Technol 44: 117-122
4. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
5. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402
6. Baroni E, Viscardi V, Cartagena-Lirola H, Lucchini G, Longhese MP (2004) The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol Cell Biol 24: 4151-4165
7. Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci Paris 316: 1194-1199
8. Becker D (1990) Binary vectors which allow the exchange of plant selectable markers and reporter genes. Nucleic Acids Res 18: 203
9. 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
10. Bhatt AM, Canales C, Dickinson HG (2001) Plant meiosis: the means to 1N. Trends Plant Sci 6: 114-121
11. Birrell GW, Brown JA, Wu HI, Giaever G, Chu AM, Davis RW, Brown JM (2002) Transcriptional response of Saccharomyces cerevisiae to DNA-damaging agents does not identify the genes that protect against these agents. Proc Natl Acad Sci USA 99: 8778-8783
12. 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
13. Bundock P, Hooykaas P (2002) Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants. Plant Cell 14: 2451-2462
14. Cartagena-Lirola H, Guerini I, Viscardi V, Lucchini G, Longhese MP (2006) Budding Yeast Sae2 is an in vivo target of the Mec1 and Tel1 checkpoint kinases during meiosis. Cell Cycle 5: 1549-1559
15. Chen PL, Liu F, Cai S, Lin X, Li A, Chen Y, Gu B, Lee EY, Lee WH (2005) Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insufficiency. Mol Cell Biol 25: 3535-3542
16. Clerici M, Mantiero D, Lucchini G, Longhese MP (2005) The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J Biol Chem 280: 38631-38638
17. Clerici M, Mantiero D, Lucchini G, Longhese MP (2006) The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep 7: 212-218
18. Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11: 1623-1634
19. D'Amours D, Jackson SP (2002) The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 3: 317-327
20. Daoudal-Cotterell S, Gallego ME, White CI (2002) The plant Rad50-Mre11 protein complex. FEBS Lett 516: 164-166
21. Deng C, Brown JA, You D, Brown JM (2005) Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics 170: 591-600
22. Deveaux Y, Alonso B, Pierrugues O, Godon C, Kazmaier M (2000) Molecular cloning and developmental expression of AtGR1, a new growth-related Arabidopsis gene strongly induced by ionizing radiation. Radiat Res 154: 355-364
23. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797
24. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P, Nussenzweig A (2003) H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4: 497-508
25. Foray N, Marot D, Gabriel A, Randrianarison V, Carr AM, Perricaudet M, Ashworth A, Jeggo P (2003) A subset of ATM-and ATR-dependent phosphorylation events requires the BRCA1 protein. EMBO J 22: 2860-2871
26. Frickey T, Lupas A (2004) CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20: 3702-3704
27. Friesner JD, Liu B, Culligan K, Britt AB (2005) Ionizing radiation-dependent gamma-H2AX focus formation requires ataxia telangiectasia mutated and ataxia telangiectasia mutated and Rad3-related. Mol Biol Cell 16: 2566-2576
28. Fusco C, Reymond A, Zervos AS (1998) Molecular cloning and characterization of a novel retinoblastoma-binding protein. Genomics 51: 351-358
29. Gallego ME, Jeanneau M, Granier F, Bouchez D, Bechtold N, White CI (2001) Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity. Plant J 25: 31-41
30. Garcia V, Bruchet H, Camescasse D, Granier F, Bouchez D, Tissier A (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15: 119-132
31. Greenberg RA, Sobhian B, Pathania S, Cantor SB, Nakatani Y, Livingston DM (2006) Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev 20: 34-46
32. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20: 589-600
33. Hartung F, Puchta H (2000) Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res 28: 1548-1554
34. 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
35. Hunter N, Kleckner N (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106: 59-70
36. 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
37. 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
38. Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52: 1-53
39. Kerzendorfer C, Vignard J, Pedrosa-Harand A, Siwiec T, Akimcheva S, Jolivet S, Sablowski R, Armstrong S, Schweizer D, Mercier R, Schlogelhofer P (2006) The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination. J Cell Sci 119: 2486-2496
40. Kucherlapati M, Yang K, Kuraguchi M, Zhao J, Lia M, Heyer J, Kane MF, Fan K, Russell R, Brown AM, Kneitz B, Edelmann W, Kolodner RD, Lipkin M, Kucherlapati R (2002) Haploinsufficiency of Flap endonuclease (Fen1) leads to rapid tumor progression. Proc Natl Acad Sci USA 99: 9924-9929
41. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, Ma H, Reiss B (2004) The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc Natl Acad Sci USA 101: 10596-10601
42. Lisby M, Barlow JH, Burgess RC, Rothstein R (2004) Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118: 699-713
43. Liu F, Lee WH (2006) CtIP activates its own and cyclin D1 promoters via the E2F/RB pathway during G1/S progression. Mol Cell Biol 26: 3124-3134
44. Lobachev KS, Gordenin DA, Resnick MA (2002) The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108: 183-193
45. Luo G, Yao MS, Bender CF, Mills M, Bladl AR, Bradley A, Petrini JH (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
46. Marchler-Bauer A, Panchenko AR, Ariel N, Bryant SH (2002) Comparison of sequence and structure alignments for protein domains. Proteins 48: 439-446
47. 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
48. Meloni AR, Smith EJ, Nevins JR (1999) A mechanism for Rb/p130-mediated transcription repression involving recruitment of the CtBP corepressor. Proc Natl Acad Sci USA 96: 9574-9579
49. Motamayor JC, Vezon D, Bajon C, Sauvanet A, Grandjean O, Marchand M, Bechtold N, Pelletier G, Horlow C (2000) Switch (swi1), an Arabidopsis thaliana mutant affected in the female meiotic switch. Sex Plant Reprod 12: 209-218
50. Nairz K, Klein F (1997) mre11S - a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev 11: 2272-2290
51. Neale MJ, Keeney S (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442: 153-158
52. Neale MJ, Pan J, Keeney S (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436: 1053-1057
53. Page J, Suja JA, Santos JL, Rufas JS (1998) Squash procedure for protein immunolocalization in meiotic cells. Chromosome Res 6: 639-642
54. Page SL, Hawley RS (2003) Chromosome choreography: the meiotic ballet. Science 301: 785-789
55. Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404
56. Prieler S, Penkner A, Borde V, Klein F (2005) The control of Spo11's interaction with meiotic recombination hotspots. Genes Dev 19: 255-269
57. 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
58. 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
59. Rattray AJ, McGill CB, Shafer BK, Strathern JN (2001) Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158: 109-122
60. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277
61. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868
62. Ross KJ, Fransz P, Jones GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: 507-516
63. Sanchez-Moran E, Santos JL, Jones GH, Franklin FC (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21: 2220-2233
64. Schaeper U, Subramanian T, Lim L, Boyd JM, Chinnadurai G (1998) Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J Biol Chem 273: 8549-8552
65. Schwacha A, Kleckner N (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123-1135
66. Shiloh Y (1998) Ataxia-telangiectasia, ATM and genomic stability: maintaining a delicate balance. Two international workshops on ataxia-telangiectasia, related disorders and the ATM protein. Biochim Biophys Acta 1378: R11-R18
67. Shinohara A, Shinohara M (2004) Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination. Cytogenet Genome Res 107: 201-207
68. Smith KN, Nicolas A (1998) Recombination at work for meiosis. Curr Opin Genet Dev 8: 200-211
69. Stacey NJ, Kuromori T, Azumi Y, Roberts G, Breuer C, Wada T, Maxwell A, Roberts K, Sugimoto-Shirasu K (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J 48: 206-216
70. Sum EY, Peng B, Yu X, Chen J, Byrne J, Lindeman GJ, Visvader JE (2002) The LIM domain protein LMO4 interacts with the cofactor CtIP and the tumor suppressor BRCA1 and inhibits BRCA1 activity. J Biol Chem 277: 7849-7856
71. Theunissen JW, Kaplan MI, Hunt PA, Williams BR, Ferguson DO, Alt FW, Petrini JH (2003) Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice. Mol Cell 12: 1511-1523
72. Tsubouchi H, Ogawa H (1998) A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol Cell Biol 18: 260-268
73. Wong AK, Ormonde PA, Pero R, Chen Y, Lian L, Salada G, Berry S, Lawrence Q, Dayananth P, Ha P, Tavtigian SV, Teng DH, Bartel PL (1998) Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene 17: 2279-2285
74. Wu HI, Brown JA, Dorie MJ, Lazzeroni L, Brown JM (2004) Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res 64: 3940-3948
75. Yin Y, Cheong H, Friedrichsen D, Zhao Y, Hu J, Mora-Garcia S, Chory J (2002) A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc Natl Acad Sci USA 99: 10191-10196
76. Yu X, Baer R (2000) Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J Biol Chem 275: 18541-18549
77. Yu X, Chen J (2004) DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol Cell Biol 24: 9478-9486
78. Yu X, Fu S, Lai M, Baer R, Chen J (2006) BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev 20: 1721-1726
79. Yu X, Wu LC, Bowcock AM, Aronheim A, Baer R (1998) The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J Biol Chem 273: 25388-25392
80. Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754