Developmental modulation of nonhomologous end joining in Caenorhabditis elegans

Genetics

Volumn 173, Issue 3, 2006, Pages 1301-1317

  Clejan, Iuval ^a,b   Boerckel, Julie ^a,b   Ahmed, Shawn ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL GENETICS; DEVELOPMENTAL STAGE; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; EMBRYO; EVOLUTIONARY HOMOLOGY; GENE MUTATION; GERM CELL; GERM LINE; GONAD DEVELOPMENT; INTESTINE CELL; LARVA; MITOSIS; NONHOMOLOGOUS END JOINING; NONHUMAN; PHENOTYPE; PHYSICAL DEVELOPMENT; PRIORITY JOURNAL; RADIATION INJURY; RNA INTERFERENCE; SOMATIC CELL; STRESS;

ANIMALS; CAENORHABDITIS ELEGANS; DNA REPAIR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; KINETOCHORES; LARVA; MODELS, BIOLOGICAL; MODELS, GENETIC; MUTATION; PHENOTYPE; RECOMBINATION, GENETIC;

CAENORHABDITIS ELEGANS;

EID: 33746420647     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.058628     Document Type: Article

References (83)

1. ADACHI, N., T. ISHINO, Y. ISHII, S. TAKEDA and H. KOYAMA, 2001 DNA ligase IV-deficient cells are more resistant to ionizing radiation in the absence of Ku70: implications for DNA doublestrand break repair. Proc. Natl. Acad. Sci. USA 98: 12109-12113.
2. AHMED, S., and J. HODGKIN, 2000 MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. Nature 403: 159-164.
3. AHMED, S., A. ALPI, M. O. HENGARTNER and A. GARTNER, 2001 C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein. Curr. Biol. 11: 1934-1944.
4. ALBERTSON, D. G., and J. N. THOMSON, 1982 The kinetochores of Caenorhabditis elegans. Chromosoma 86: 409-428.
5. ALLEN, C., J. HALBROOK and J. A. NICKOLOFF, 2003 Interactive competition between homologous recombination and non-homologous end joining. Mol. Cancer Res. 1: 913-920.
6. ALPI, A., P. PASIERBEK, A. GARTNER and J. LOIDL, 2003 Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112: 6-16.
7. ASAOKA-TAGUCHI, M., M. YAMADA, A. NAKAMURA, K. HANYU and S. KOBAYASHI, 1999 Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat. Cell Biol. 1: 431-437.
8. AYLON, Y., B. LIEFSHITZ and M. KUPIEC, 2004 The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J. 23: 4868-4875.
9. BARNES, D. E., G. STAMP, I. ROSEWELL, A. DENZEL and T. LINDAHL, 1998 Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice. Curr. Biol. 8: 1395-1398.
10. BASTIANI, C. A., S. GHARIB, M. I. SIMON and P. W. STERNBERG, 2003 Caenorhabditis elegans Gαq regulates egg-laying behavior via a PLCβ-independent and serotonin-dependent signaling pathway and likely functions both in the nervous system and in muscle. Genetics 165: 1805-1822.
11. BENDER, C. F., M. L. SIKES, R. SULLIVAN, L. E. HUYE, M. M. LE BEAU et al., 2002 Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev. 16: 2237-2251.
12. BOULTON, S. J., and S. P. JACKSON, 1996 Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15: 5093-5103.
13. BOULTON, S. J., A. GARTNER, J. REBOUL, P. VAGLIO, N. DYSON et al., 2002 Combined functional genomic maps of the C. elegans DNA damage response. Science 295: 127-131.
14. CHIN, G. M., and A. M. VILLENEUVE, 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.
15. COHEN, H. Y., S. LAVU, K. J. BITTERMAN, B. HEKKING, T. A. IMAHIYEROBO et al., 2004 Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol. Cell 13: 627-638.
16. COOPER, M. P., A. MACHWE, D. K. ORREN, R. M. BROSH, D. RAMSDEN et al., 2000 Ku complex interacts with and stimulates the Werner protein. Genes Dev. 14: 907-912.
17. DALEY, J. M., P. L. PALMBOS, D. WU and T. E. WILSON, 2005 Non-homologous end joining in yeast. Annu. Rev. Genet. 39: 431-451.
18. DE LA TORRE-RUIZ, M., and N. F. LOWNDES, 2000 The Saccharomyces cerevisiae DNA damage checkpoint is required for efficient repair of double strand breaks by non-homologous end joining. FEBS Lett. 467: 311-315.
19. DERRY, W. B., A. P. PUTZKE and J. H. ROTHMAN, 2001 Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294: 591-595.
20. ENGELS, W. R., D. M. JOHNSON-SCHLITZ, W. B. EGGLESTON and J. SVED, 1990 High-frequency P element loss in Drosophila is homolog dependent. Cell 62: 515-525.
21. FELDMANN, E., V. SCHMIEMANN, W. GOEDECKE, S. REICHENBERGER and P. PFEIFFER, 2000 DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res. 28: 2585-2596.
22. FELDMANN, H., L. DRILLER, B. MEIER, G. MAGES, J. KELLERMANN et al., 1996 HDF2, the second subunit of the Ku homologue from Saccharomyces cerevisiae. J. Biol. Chem. 271: 27765-27769.
23. FERREIRA, M. G., and J. P. COOPER, 2004 Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle. Genes Dev. 18: 2249-2254.
24. FRASER, A. G., R. S. KAMATH, P. ZIPPERLEN, M. MARTINEZ-CAMPOS, M. SOHRMANN et al., 2000 Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325-330.
25. FUKUSHIGE, T., M. J. HENDZEL, D. P. BAZETT-JONES and J. D. MCGHEE, 1999 Direct visualization of the elt-2 gut-specific GATA factor binding to a target promoter inside the living Caenorhabditis elegans embryo. Proc. Natl. Acad. Sci. USA 96: 11883-11888.
26. GARTNER, A., S. MILSTEIN, S. AHMED, J. HODGKIN and M. O. HENGARTNER, 2000 A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol. Cell 5: 435-443.
27. GLOOR, G. B., J. MORETTI, J. MOUYAL and K. J. KEELER, 2000 Distinct P-element excision products in somatic and germline cells of Drosophila melanogaster. Genetics 155: 1821-1830.
28. GORSKI, M. M., J. C. EEKEN, A. W. DE JONG, I. KLINK, M. LOOS et al., 2003 The Drosophila melanogaster DNA ligase IV gene plays a crucial role in the repair of radiation-induced DNA double-strand breaks and acts synergistically with Rad54. Genetics 165: 1929-1941.
29. HARFST, E., S. COOPER, S. NEUBAUER, L. DISTEL and U. GRAWUNDER, 2000 Normal V(D)J recombination in cells from patients with Nijmegen breakage syndrome. Mol. Immunol. 37: 915-929.
30. HARTLEY, K. O., D. GELL, G. C. SMITH, H. ZHANG, N. DIVECHA et al., 1995 DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82: 849-856.
31. HEACOCK, M., E. SPANGLER, K. RIHA, J. PUIZINA and D. E. SHIPPEN, 2004 Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO J. 23: 2304-2313.
32. HEDGECOCK, E. M., and J. G. WHITE, 1985 Polyploid tissues in the nematode Caenorhabditis elegans. Dev. Biol. 107: 128-133.
33. HERMAN, R. K., J. E. MADL and C. K. KARI, 1979 Duplications in Caenorhabditis elegans. Genetics 92: 419-435.
34. HINZ, J. M., N. A. YAMADA, E. P. SALAZAR, R. S. TEBBS and L. H. THOMPSON, 2005 Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells. DNA Rep. 4: 782-792.
35. HOFMANN, E. R., S. MILSTEIN, S. J. BOULTON, M. YE, J. J. HOFMANN et al., 2002 Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis. Curr. Biol. 12: 1908-1918.
36. HOWE, M., K. L. MCDONALD, D. G. ALBERTSON and B. J. MEYER, 2001 HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J. Cell Biol. 153: 1227-1238.
37. HUANG, J., and W. S. DYNAN, 2002 Reconstitution of the mammalian DNA double-strand break end-joining reaction reveals a requirement for an Mre11/Rad50/NBS1-containing fraction. Nucleic Acids Res. 30: 667-674.
38. IRA, G., A. PELLICIOLI, A. BALIJJA, X. WANG, S. FIORANI et al., 2004 DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431: 1011-1017.
39. JOHNSON-SCHLITZ, D. M., and W. R. ENGELS, 1993 P-element-induced interallelic gene conversion of insertions and deletions in Drosophila melanogaster. Mol. Cell. Biol. 13: 7006-7018.
40. KAMATH, R. S., M. MARTINEZ-CAMPOS, P. ZIPPERLEN, A. G. FRASER and J. AHRINGER, 2001 Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2: RESEARCH0002.
41. KARANJAWALA, Z. E., U. GRAWUNDER, C. L. HSIEH and M. R. LIEBER, 1999 The nonhomologous DNA end joining pathway is important for chromosome stability in primary fibroblasts. Curr. Biol. 9: 1501-1504.
42. KARANJAWALA, Z. E., N. ADACHI, R. A. IRVINE, E. K. OH, D. SHIBATA et al., 2002 The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants. DNA Rep. 1: 1017-1026.
43. KARATHANASIS, E., and T. E. WILSON, 2002 Enhancement of Saccharomyces cerevisiae end-joining efficiency by cell growth stage but not by impairment of recombination. Genetics 161: 1015-1027.
44. KAWASAKI, I., Y. H. SHIM, J. KIRCHNER, J. KAMINKER, W. B. WOOD et al., 1998 PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94: 635-645.
45. LEE, S. J., J. S. YOOK, S. M. HAN and H. S. KOO, 2004 A Werner syndrome protein homolog affects C. elegans development, growth rate, life span and sensitivity to DNA damage by acting at a DNA damage checkpoint. Development 131: 2565-2575.
46. LIEBER, M. R., Y. MA, U. PANNICKE and K. SCHWARZ, 2003 Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell Biol. 4: 712-720.
47. LISBY, M., R. ROTHSTEIN and U. H. MORTENSEN, 2001 Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. USA 98: 8276-8282.
48. MA, J. L., E. M. KIM, J. E. HABER and S. E. LEE, 2003 Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 23: 8820-8828.
49. MA, Y., U. PANNICKE, K. SCHWARZ and M. R. LIEBER, 2002 Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108: 781-794.
50. MADDOX, P. S., K. OEGEMA, A. DESAI and I. M. CHEESEMAN, 2004 "Holo"er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res. 12: 641-653.
51. MALONE, E. A., and J. H. THOMAS, 1994 A screen for nonconditional dauer-constitutive mutations in Caenorhabditis elegans. Genetics 136: 879-886.
52. MANOLIS, K. G., E. R. NIMMO, E. HARTSUIKER, A. M. CARR, P. A. JEGGO et al., 2001 Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 20: 210-221.
53. MARTIN, J. S., N. WINKELMANN, M. I. PETALCORIN, M. J. MCILWRAITH and S. J. BOULTON, 2005 RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair. Mol. Cell. Biol. 25: 3127-3139.
54. MCVEY, M., D. RADUT and J. J. SEKELSKY, 2004 End-joining repair of double-strand breaks in Drosophila melanogaster is largely DNA ligase IV independent. Genetics 168: 2067-2076.
55. MILLS, K. D., D. O. FERGUSON, J. ESSERS, M. ECKERSDORFF, R. KANAAR et al., 2004 Rad54 and DNA ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev. 18: 1283-1292.
56. MOORE, J. K., and J. E. HABER, 1996 Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 2164-2173.
57. O'CONNELL, K. F., C. M. LEYS and J. G. WHITE, 1998 A genetic screen for temperature-sensitive cell-division mutants of Caenorhabditis elegans. Genetics 149: 1303-1321.
58. O'DRISCOLL, M., A. R. GENNERY, J. SEIDEL, P. CONCANNON and P. A. JEGGO, 2004 An overview of three new disorders associated with genetic instability: LIG4 syndrome, RS-SCID and ATR-Seckel syndrome. DNA Rep. 3: 1227-1235.
59. PASTINK, A., J. C. EEKEN and P. H. LOHMAN, 2001 Genomic integrity and the repair of double-strand DNA breaks. Mutat. Res. 480-481: 37-50.
60. RAPP, A., and K. O. GREULICH, 2004 After double-strand break induction by UV-A, homologous recombination and nonhomologous end joining cooperate at the same DSB if both systems are available. J. Cell Sci. 117: 4935-4945.
61. REINKE, V., I. S. GIL, S. WARD and K. KAZMER, 2004 Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131: 311-323.
62. RIDDLE, D. L., M. M. SWANSON and P. S. ALBERT, 1981 Interacting genes in nematode dauer larva formation. Nature 290: 668-671.
63. RINALDO, C., P. BAZZICALUPO, S. EDERLE, M. HILLIARD and A. LA VOLPE, 2002 Roles for Caenorhabditis elegans rad-51 in meiosis and in resistance to ionizing radiation during development. Genetics 160: 471-479.
64. ROTHKAMM, K., I. KRUGER, L. H. THOMPSON and M. LOBRICH, 2003 Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23: 5706-5715.
65. SALEH-GOHARI, N., and T. HELLEDAY, 2004 Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells. Nucleic Acids Res. 32: 3683-3688.
66. SANCAR, A., L. A. LINDSEY-BOLTZ, K. UNSAL-KACMAZ and S. LINN, 2004 Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73: 39-85.
67. SCHAR, P., M. FASI and R. JESSBERGER, 2004 SMC1 coordinates DNA double-strand break repair pathways. Nucleic Acids Res. 32: 3921-3929.
68. SCHUMACHER, B., K. HOFMANN, S. BOULTON and A. GARTNER, 2001 The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr. Biol. 11: 1722-1727.
69. SHARPLESS, N. E., D. O. FERGUSON, R. C. O'HAGAN, D. H. CASTRILLON, C. LEE et al., 2001 Impaired nonhomologous end-joining provokes soft tissue sarcomas harboring chromosomal translocations, amplifications, and deletions. Mol. Cell 8: 1187-1196.
70. SIEDE, W., A. A. FRIEDL, I. DIANOVA, F. ECKARDT-SCHUPP and E. C. FRIEDBERG, 1996 The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics 142: 91-102.
71. SIMMER, F., M. TIJSTERMAN, S. PARRISH, S. P. KOUSHIKA, M. L. NONET et al., 2002 Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 12: 1317-1319.
72. SIMMER, F., C. MOORMAN, A. M. VAN DER LINDEN, E. KUIJK, P. V. VAN DEN BERGHE et al., 2003 Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol. 1: E12.
73. STRACKER, T. H., J. W. THEUNISSEN, M. MORALES and J. H. PETRINI, 2004 The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Rep. 3: 845-854.
74. STROME, S., and W. B. WOOD, 1982 Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 79: 1558-1562.
75. SU, T. T., S. D. CAMPBELL and P. H. O'FARRELL, 1998 The cell cycle program in germ cells of the Drosophila embryo. Dev. Biol. 196: 160-170.
76. SULSTON, J., and J. HODGKIN, 1988 Methods, pp. 587-606 in The Nematode Caenorhabditis elegans, edited by W. B. WOOD. Cold Spring Harbor Laboratory Press, Plainview, NY.
77. SULSTON, J. E., and H. R. HORVITZ, 1977 Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56: 110-156.
78. TAKATA, M., M. S. SASAKI, E. SONODA, C. MORRISON, M. HASHIMOTO et al., 1998 Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17: 5497-5508.
79. VOWELS, J. J., and J. H. THOMAS, 1992 Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130: 105-123.
80. WOOLLARD, A., and J. HODGKIN, 1999 Stu-7/air-2 is a C. elegans aurora homologue essential for chromosome segregation during embryonic and post-embryonic development. Mech. Dev. 82: 95-108.
81. YEO, T. C., D. XIA, S. HASSOUNEH, X. O. YANG, D. E. SABATH et al., 2000 V(D)J rearrangement in Nijmegen breakage syndrome. Mol. Immunol. 37: 1131-1139.
82. YU, X., and A. GABRIEL, 2003 Ku-dependent and Ku-independent end-joining pathways lead to chromosomal rearrangements during double-strand break repair in Saccharomyces cerevisiae. Genetics 163: 843-856.
83. YUAN, J., S. SHAHAM, S. LEDOUX, H. M. ELLIS and H. R. HORVITZ, 1993 The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75: 641-652.