Nucleotide excision repair and the degradation of RNA pol II by the Caenorhabditis elegans XPA and Rsp5 orthologues, RAD-3 and WWP-1

DNA Repair

Volumn 7, Issue 2, 2008, Pages 267-280

  Astin, Jonathan W ^a   O'Neil, Nigel J ^a   Kuwabara, Patricia E ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

C. elegans; Nucleotide excision repair; rad 3; Rsp5; Ultraviolet; wwp 1; xpa 1

Indexed keywords

AMA 1 PROTEIN; CHECKPOINT KINASE RAD3; RNA POLYMERASE II; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; WWP 1 PROTEIN; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; ENZYME DEGRADATION; ENZYME SUBUNIT; EXCISION REPAIR; GENETIC SCREENING; GENETIC TRANSCRIPTION; NONHUMAN; NONSENSE MUTATION; OXIDATIVE STRESS; PARASITE SURVIVAL; PRIORITY JOURNAL; RADIATION EXPOSURE; ULTRAVIOLET IRRADIATION; ULTRAVIOLET RADIATION; WILD TYPE;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA REPAIR; GENE COMPONENTS; LONGEVITY; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES; PARAQUAT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA POLYMERASE II; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASES; ULTRAVIOLET RAYS; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

CAENORHABDITIS ELEGANS;

EID: 37549066986     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.10.004     Document Type: Article

References (81)

1. Murakami H., and Nurse P. DNA replication and damage checkpoints and meiotic cell cycle controls in the fission and budding yeasts. Biochem. J. 349 (2000) 1-12
2. Nyberg K.A., Michelson R.J., Putnam C.W., and Weinert T.A. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36 (2002) 617-656
3. Friedberg E.C., Walker D.R., Siede W., Wood R., Schultz R., and Ellenberger T. DNA Repair and Mutagenesis (2005), ASM Press, Washington, DC
4. Andressoo J.O., Hoeijmakers J.H., and Mitchell J.R. Nucleotide excision repair disorders and the balance between cancer and aging. Cell Cycle 5 (2006) 2886-2888
5. Kraemer K.H., Patronas N.J., Schiffmann R., Brooks B.P., Tamura D., and Digiovanna J.J. Xeroderma pigmentosum, trichothiodystrophy and Cockayne syndrome: a complex genotype-phenotype relationship. Neuroscience 145 (2007) 1388-1396
6. Bootsma D., Kraemer K.H., Cleaver J.E., and Hoeijmakers J.H. The Genetic Basis of Human Cancer (2002), Mc-Graw-Hill Medical Publishing Division, New York
7. Berneburg M., and Lehmann A.R. Xeroderma pigmentosum and related disorders: defects in DNA repair and transcription. Adv. Genet. 43 (2001) 71-102
8. van der Horst G.T., van Steeg H., Berg R.J., van Gool A.J., de Wit J., Weeda G., Morreau H., Beems R.B., van Kreijl C.F., de Gruijl F.R., Bootsma D., and Hoeijmakers J.H. Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 89 (1997) 425-435
9. van Hoffen A., Natarajan A.T., Mayne L.V., van Zeeland A.A., Mullenders L.H., and Venema J. Deficient repair of the transcribed strand of active genes in Cockayne's syndrome cells. Nucleic Acids Res. 21 (1993) 5890-5895
10. Lehmann A.R. DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 85 (2003) 1101-1111
11. Giglia-Mari G., Coin F., Ranish J.A., Hoogstraten D., Theil A., Wijgers N., Jaspers N.G., Raams A., Argentini M., van der Spek P.J., Botta E., Stefanini M., Egly J.M., Aebersold R., Hoeijmakers J.H., and Vermeulen W. A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat. Genet. 36 (2004) 714-719
12. Huibregtse J.M., Yang J.C., and Beaudenon S.L. The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 94 (1997) 3656-3661
13. Beaudenon S.L., Huacani M.R., Wang G., McDonnell D.P., and Huibregtse J.M. Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell. Biol. 19 (1999) 6972-6979
14. Somesh B.P., Reid J., Liu W.F., Sogaard T.M., Erdjument-Bromage H., Tempst P., and Svejstrup J.Q. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121 (2005) 913-923
15. Somesh B.P., Sigurdsson S., Saeki H., Erdjument-Bromage H., Tempst P., and Svejstrup J.Q. Communication between distant sites in RNA polymerase II through ubiquitylation factors and the polymerase CTD. Cell 129 (2007) 57-68
16. Woudstra E.C., Gilbert C., Fellows J., Jansen L., Brouwer J., Erdjument-Bromage H., Tempst P., and Svejstrup J.Q. A Rad26-Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature 415 (2002) 929-933
17. Reid J., and Svejstrup J.Q. DNA damage-induced Def1-RNA polymerase II interaction and Def1 requirement for polymerase ubiquitylation in vitro. J. Biol. Chem. 279 (2004) 29875-29878
18. Friedberg E.C. How nucleotide excision repair protects against cancer. Nat. Rev. Cancer 1 (2001) 22-33
19. States J.C., McDuffie E.R., Myrand S.P., McDowell M., and Cleaver J.E. Distribution of mutations in the human xeroderma pigmentosum group A gene and their relationships to the functional regions of the DNA damage recognition protein. Hum. Mutat. 12 (1998) 103-113
20. Satoh M.S., Jones C.J., Wood R.D., and Lindahl T. DNA excision-repair defect of xeroderma pigmentosum prevents removal of a class of oxygen free radical-induced base lesions. Proc. Natl. Acad. Sci. USA 90 (1993) 6335-6339
21. Brooks P.J. The case for 8,5′-cyclopurine-2′-deoxynucleosides as endogenous DNA lesions that cause neurodegeneration in xeroderma pigmentosum. Neuroscience 145 (2007) 1407-1417
22. Stergiou L., and Hengartner M.O. Death and more: DNA damage response pathways in the nematode C. elegans. Cell Death Differ. 11 (2004) 21-28
23. Gartner A., Milstein S., Ahmed S., Hodgkin J., and Hengartner M.O. A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol. Cell 5 (2000) 435-443
24. Hartman P.S., and Herman R.K. Radiation-sensitive mutants of Caenorhabditis elegans. Genetics 102 (1982) 159-178
25. Ahmed S., Alpi A., Hengartner M.O., and Gartner A. C. elegans RAD-5/CLK-2 defines a new DNA damage checkpoint protein. Curr. Biol. 11 (2001) 1934-1944
26. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
27. Mello C., and Fire A. DNA transformation. Methods Cell Biol. 48 (1995) 451-482
28. Hope I.A. C. elegans a Practical Approach (1999), Oxford University Press
29. Hartman P.S. UV irradiation of wild type and radiation-sensitive mutants of the nematode Caenorhabditis elegans: fertilities, survival, and parental effects. Photochem. Photobiol. 39 (1984) 169-175
30. Greenwald I.S., and Horvitz H.R. unc-93(e1500): A behavioral mutant of Caenorhabditis elegans that defines a gene with a wild-type null phenotype. Genetics 96 (1980) 147-164
31. De Stasio E., Lephoto C., Azuma L., Holst C., Stanislaus D., and Uttam J. Characterization of revertants of unc-93(e1500) in Caenorhabditis elegans induced by N-ethyl-N-nitrosourea. Genetics 147 (1997) 597-608
32. An J.H., and Blackwell T.K. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17 (2003) 1882-1893
33. Kenyon C., Chang J., Gensch E., Rudner A., and Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 366 (1993) 461-464
34. Timmons L., Court D.L., and Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263 (2001) 103-112
35. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., and Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
36. Shen X., Ellis R.E., Lee K., Liu C.Y., Yang K., Solomon A., Yoshida H., Morimoto R., Kurnit D.M., Mori K., and Kaufman R.J. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107 (2001) 893-903
37. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
38. Park H.K., Yook J.S., Koo H.S., Choi I.S., and Ahn B. The Caenorhabditis elegans XPA homolog of human XPA. Mol. Cells 14 (2002) 50-55
39. Tanaka K., Miura N., Satokata I., Miyamoto I., Yoshida M.C., Satoh Y., Kondo S., Yasui A., Okayama H., and Okada Y. Analysis of a human DNA excision repair gene involved in group A xeroderma pigmentosum and containing a zinc-finger domain. Nature 348 (1990) 73-76
40. Hartman P.S., Hevelone J., Dwarakanath V., and Mitchell D.L. Excision repair of UV radiation-induced DNA damage in Caenorhabditis elegans. Genetics 122 (1989) 379-385
41. Miura N., Miyamoto I., Asahina H., Satokata I., Tanaka K., and Okada Y. Identification and characterization of xpac protein, the gene product of the human XPAC (xeroderma pigmentosum group A complementing) gene. J. Biol. Chem. 266 (1991) 19786-19789
42. Shimamoto T., Tanimura T., Yoneda Y., Kobayakawa Y., Sugasawa K., Hanaoka F., Oka M., Okada Y., Tanaka K., and Kohno K. Expression and functional analyses of the Dxpa gene, the Drosophila homolog of the human excision repair gene XPA. J. Biol. Chem. 270 (1995) 22452-22459
43. Ishii N., Takahashi K., Tomita S., Keino T., Honda S., Yoshino K., and Suzuki K. A methyl viologen-sensitive mutant of the nematode Caenorhabditis elegans. Mutat. Res. 237 (1990) 165-171
44. Ishii N., Fujii M., Hartman P.S., Tsuda M., Yasuda K., Senoo-Matsuda N., Yanase S., Ayusawa D., and Suzuki K. A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394 (1998) 694-697
45. Ishii N. Oxidative stress and aging in Caenorhabditis elegans. Free Radic. Res. 33 (2001) 857-864
46. Cleaver J.E., and Crowley E. UV damage, DNA repair and skin carcinogenesis. Front. Biosci. 7 (2002) d1024-d1043
47. Coohill T., Marshall T., Schubert W., and Nelson G. Ultraviolet mutagenesis of radiation-sensitive (rad) mutants of the nematode Caenorhabditis elegans. Mutat. Res. 209 (1988) 99-106
48. Hartman P.S., De Wilde D., and Dwarakanath V.N. Genetic and molecular analyses of UV radiation-induced mutations in the fem-3 gene of Caenorhabditis elegans. Photochem. Photobiol. 61 (1995) 607-614
49. Riddle D.L., and Albert P.S. Genetic and enviromental regulation of dauer larva development. In: Riddle D.L., Blumenthal T., Meyer B.J., and Priess J.R. (Eds). C. elegans II (1997), Cold Spring Harbor Laboratory Press, New York
50. Kenyon C. The plasticity of aging: insights from long-lived mutants. Cell 120 (2005) 449-460
51. Hong Y., Roy R., and Ambros V. Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125 (1998) 3585-3597
52. McIntire S.L., Reimer R.J., Schuske K., Edwards R.H., and Jorgensen E.M. Identification and characterization of the vesicular GABA transporter. Nature 389 (1997) 870-876
53. Derry W.B., Putzke A.P., and Rothman J.H. Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294 (2001) 591-595
54. Hofmann E.R., Milstein S., Boulton S.J., Ye M., Hofmann J.J., Stergiou L., Gartner A., Vidal M., and Hengartner M.O. Caenorhabditis elegans HUS-1 Is a DNA damage checkpoint protein required for genome stability and EGL-1-mediated apoptosis. Curr. Biol. 12 (2002) 1908-1918
55. Ahmed S., and Hodgkin J. MRT-2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. Nature 403 (2000) 159-164
56. Schumacher B., Hofmann K., Boulton S., and Gartner A. The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr. Biol. 11 (2001) 1722-1727
57. Aoki H., Sato S., Takanami T., Ishihara T., Katsura I., Takahashi H., and Higashitani A. Characterization of Ce-atl-1, an ATM-like gene from Caenorhabditis elegans. Mol. Gen. Genet. 264 (2000) 119-126
58. Sanford T., Golomb M., and Riddle D.L. RNA polymerase II from wild type and alpha-amanitin-resistant strains of Caenorhabditis elegans. J. Biol. Chem. 258 (1983) 12804-12809
59. Calfon M., Zeng H., Urano F., Till J.H., Hubbard S.R., Harding H.P., Clark S.G., and Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415 (2002) 92-96
60. Huang K., Johnson K.D., Petcherski A.G., Vandergon T., Mosser E.A., Copeland N.G., Jenkins N.A., Kimble J., and Bresnick E.H. A HECT domain ubiquitin ligase closely related to the mammalian protein WWP1 is essential for Caenorhabditis elegans embryogenesis. Gene 252 (2000) 137-145
61. de Vries A., van Oostrom C.T., Hofhuis F.M., Dortant P.M., Berg R.J., de Gruijl F.R., Wester P.W., van Kreijl C.F., Capel P.J., van Steeg H., et al. Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377 (1995) 169-173
62. Takahashi Y., Nakatsuru Y., Zhang S., Shimizu Y., Kume H., Tanaka K., Ide F., and Ishikawa T. Enhanced spontaneous and aflatoxin-induced liver tumorigenesis in xeroderma pigmentosum group A gene-deficient mice. Carcinogenesis 23 (2002) 627-633
63. Stergiou L., Doukoumetzidis K., Sendoel A., and Hengartner M.O. The nucleotide excision repair pathway is required for UV-C-induced apoptosis in Caenorhabditis elegans. Cell Death Differ. (2007)
64. Denver D.R., Feinberg S., Steding C., Durbin M., and Lynch M. The relative roles of three DNA repair pathways in preventing Caenorhabditis elegans mutation accumulation. Genetics 174 (2006) 57-65
65. Meyer J.N., Boyd W.A., Azzam G.A., Haugen A.C., Freedman J.H., and Van Houten B. Decline of nucleotide excision repair capacity in aging Caenorhabditis elegans. Genome Biol. 8 (2007) R70
66. Lehmann A.R. Replication of damaged DNA by translesion synthesis in human cells. FEBS Lett. 579 (2005) 873-876
67. Takanami T., Mori A., Takahashi H., and Higashitani A. Hyper-resistance of meiotic cells to radiation due to a strong expression of a single recA-like gene in Caenorhabditis elegans. Nucleic Acids Res. 28 (2000) 4232-4236
68. Hartman P., Reddy J., and Svendsen B.A. Does trans-lesion synthesis explain the UV-radiation resistance of DNA synthesis in C. elegans embryos?. Mutat. Res. 255 (1991) 163-173
69. Holway A.H., Kim S.H., La Volpe A., and Michael W.M. Checkpoint silencing during the DNA damage response in Caenorhabditis elegans embryos. J. Cell Biol. 172 (2006) 999-1008
70. Ohkumo T., Masutani C., Eki T., and Hanaoka F. Deficiency of the Caenorhabditis elegans DNA polymerase eta homologue increases sensitivity to UV radiation during germ-line development. Cell Struct. Funct. 31 (2006) 29-37
71. Reape T.J., and Burnell A.M. Dauer larva recovery in the nematode Caenorhabditis elegans -I. The effect of mRNA synthesis inhibitors on recovery, growth and pharyngeal pumping. Comp. Biochem. Physiol. B 98 (1991) 239-243
72. Kimura K.D., Tissenbaum H.A., and Liu Y.G. Ruvkun, daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277 (1997) 942-946
73. Morris J.Z., Tissenbaum H.A., and Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382 (1996) 536-539
74. Svejstrup J.Q. Rescue of arrested RNA polymerase II complexes. J. Cell Sci. 116 (2003) 447-451
75. Sieburth D., Ch'ng Q., Dybbs M., Tavazoie M., Kennedy S., Wang D., Dupuy D., Rual J.F., Hill D.E., Vidal M., Ruvkun G., and Kaplan J.M. Systematic analysis of genes required for synapse structure and function. Nature 436 (2005) 510-517
76. Mosser E.A., Kasanov J.D., Forsberg E.C., Kay B.K., Ney P.A., and Bresnick E.H. Physical and functional interactions between the transactivation domain of the hematopoietic transcription factor NF-E2 and WW domains. Biochemistry (Moscow) 37 (1998) 13686-13695
77. Komuro A., Imamura T., Saitoh M., Yoshida Y., Yamori T., Miyazono K., and Miyazawa K. Negative regulation of transforming growth factor-beta (TGF-beta) signaling by WW domain-containing protein 1 (WWP1). Oncogene 23 (2004) 6914-6923
78. Chen C., Sun X., Guo P., Dong X.Y., Sethi P., Zhou W., Zhou Z., Petros J., Frierson Jr. H.F., Vessella R.L., Atfi A., and Dong J.T. Ubiquitin E3 ligase WWP1 as an oncogenic factor in human prostate cancer. Oncogene 26 (2007) 2386-2394
79. Bregman D.B., Halaban R., van Gool A.J., Henning K.A., Friedberg E.C., and Warren S.L. UV-induced ubiquitination of RNA polymerase II: a novel modification deficient in Cockayne syndrome cells. Proc. Natl. Acad. Sci. USA 93 (1996) 11586-11590
80. Luo Z., Zheng J., Lu Y., and Bregman D.B. Ultraviolet radiation alters the phosphorylation of RNA polymerase II large subunit and accelerates its proteasome-dependent degradation. Mutat. Res. 486 (2001) 259-274
81. McKay B.C., Becerril C., and Ljungman M. P53 plays a protective role against UV- and cisplatin-induced apoptosis in transcription-coupled repair proficient fibroblasts. Oncogene 20 (2001) 6805-6808