Caffeine abolishes the ultraviolet-induced REV3 translesion replication pathway in mouse cells

International Journal of Molecular Sciences

Volumn 12, Issue 12, 2011, Pages 8513-8529

  Takezawa, Jun ^a   Aiba, Naomi ^a,c   Kajiwara, Kagemasa ^b   Yamada, Kouichi ^a  

^a NATIONAL INSTITUTE OF HEALTH AND NUTRITION   (Japan)

^b TOKAI UNIVERSITY   (Japan)

^c KANAGAWA INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Alkaline sucrose density gradient sedimentation; Caffeine; DNA polymerase ; Proteasome inhibitor; Rev3 knockout; TLS; Translesion replication

Indexed keywords

CAFFEINE; DNA POLYMERASE; DNA POLYMERASE REV3; MG 262; PROTEASOME INHIBITOR; PROTEIN P53; UNCLASSIFIED DRUG; DNA DIRECTED DNA POLYMERASE; REV3 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; EMBRYO; ENZYME ACTIVE SITE; FIBROBLAST; KNOCKOUT MOUSE; MORTALITY; MOUSE; MOUSE EMBRYO; NONHUMAN; PLASMID; UV INDUCED TRANSLESION REPLICATION; WILD TYPE; ANIMAL; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

ANIMALS; CAFFEINE; CELL LINE; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; FIBROBLASTS; MICE; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 84055217626     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms12128513     Document Type: Article

References (54)

1. Lehmann, A.R.; Niimi, A.; Ogi, T.; Brown, S.; Sabbioneda, S.; Wing, J.F.; Kannouche, P.L.; Green, C.M. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst.) 2007, 6, 891-899.
2. Prakash, S.; Prakash, L. Translesion DNA synthesis in eukaryotes: A one or two-polymerase affair. Genes Dev. 2002, 16, 1872-1883.
3. Prakash, S.; Johnson, R.E.; Prakash, L. Eukaryotic translesion synthesis DNA polymerases: Specificity of structure and function. Annu. Rev. Biochem. 2005, 74, 317-353.
4. Takezawa, J.; Ishimi, Y.; Aiba, N.; Yamada, K. Rev1, Rev3, or Rev7 siRNA abolishes ultraviolet light-induced translesion replication in HeLa cells: A comprehensive study using alkaline sucrose density gradient sedimentation. J. Nucleic Acids 2010, 2010, 750296:1-750296:12.
5. Hirota, K.; Sonoda, E.; Kawamoto, T.; Motegi, A.; Masutani, C.; Hanaoka, F.; Szuts, D.; Iwai, S.; Sale, J.E.; Lehmann, A. et al. Simultaneous disruption of two DNA polymerases, Pol- and Polζ, in avian DT40 cells unmasks the role of Pol- in cellular response to various DNA lesions. PLoS Genet. 2010, 6, e1001151:1-e1001151:13.
6. Lawrence, C.W.; Christensen, R.B. Ultraviolet-induced reversion of cyc1 alleles in radiation-sensitive strains of yeast. III. Rev3 mutant strains. Genetics 1979, 92, 397-408.
7. Gibbs, P.E.; Wang, X.D.; Li, Z.; McManus, T.P.; McGregor, W.G.; Lawrence, C.W.; Maher, V.M. The function of the human homolog of Saccharomyces cerevisiae REV1 is required for mutagenesis induced by UV light. Proc. Natl. Acad. Sci. USA 2000, 97, 4186-4191.
8. Gibbs, P.E.; McGregor, W.G.; Maher, V.M.; Nisson, P.; Lawrence, C.W. A human homolog of the Saccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase ζ. Proc. Natl. Acad. Sci. USA 1998, 95, 6876-6880.
9. Murakumo, Y.; Roth, T.; Ishii, H.; Rasio, D.; Numata, S.; Croce, C.M.; Fishel, R. A human REV7 homolog that interacts with the polymerase ζ catalytic subunit hREV3 and the spindle assembly checkpoint protein hMAD2. J. Biol. Chem. 2000, 275, 4391-4397.
10. Lawrence, C.W. Cellular roles of DNA polymerase ζ and Rev1 protein. DNA Repair (Amst.) 2002, 1, 425-435.
11. Li, Z.; Zhang, H.; McManus, T.P.; McCormick, J.J.; Lawrence, C.W.; Maher, V.M. hREV3 is essential for error-prone translesion synthesis past UV or benzo[a]pyrene diol epoxide-induced DNA lesions in human fibroblasts. Mutat. Res. 2002, 510, 71-80.
12. McNally, K.; Neal, J.A.; McManus, T.P.; McCormick, J.J.; Maher, V.M. hRev7, putative subunit of hPolζ, plays a critical role in survival, induction of mutations, and progression through S-phase, of UV(254 nm)-irradiated human fibroblasts. DNA Repair (Amst.) 2008, 7, 597-604.
13. Diaz, M.; Watson, N.B.; Turkington, G.; Verkoczy, L.K.; Klinman, N.R.; McGregor, W.G. Decreased frequency and highly aberrant spectrum of ultraviolet-induced mutations in the hprt gene of mouse fibroblasts expressing antisense RNA to DNA polymerase ζ. Mol. Cancer Res. 2003, 1, 836-847.
14. Masutani, C.; Kusumoto, R.; Iwai, S.; Hanaoka, F. Mechanisms of accurate translesion synthesis by human DNA polymerase η. EMBO J. 2000, 19, 3100-3109.
15. Cleaver, J.E.; Kraemer, K.H. Xeroderma Pigmentosum and Cockayne Syndrome. In The Metabolic and Molecular Basis of Inherited Disease, 7th ed.; Scriver, C.R., Beaudet, A.L., Sly, W.S., Valle, D., Eds.; McGraw-Hill: New York, NY, USA, 1995; pp. 4393-4419.
16. Prakash, S.; Johnson, R.E.; Washington, M.T.; Haracska, L.; Kondratick, C.M.; Prakash, L. Role of yeast and human DNA polymerase η in error-free replication of damaged DNA. Cold Spring Harb. Symp. Quant. Biol. 2000, 65, 51-59.
17. Masutani, C.; Kusumoto, R.; Yamada, A.; Dohmae, N.; Yokoi, M.; Yuasa, M.; Araki, M.; Iwai, S.; Takio, K.; Hanaoka, F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 1999, 399, 700-704.
18. Masutani, C.; Kusumoto, R.; Yamada, A.; Yuasa, M.; Araki, M.; Nogimori, T.; Yokoi, M.; Eki, T.; Iwai, S.; Hanaoka, F. Xeroderma pigmentosum variant: From a human genetic disorder to a novel DNA polymerase. Cold Spring Harb. Symp. Quant. Biol. 2000, 65, 71-80.
19. Matsuda, T.; Bebenek, K.; Masutani, C.; Hanaoka, F.; Kunkel, T.A. Low fidelity DNA synthesis by human DNA polymerase-η. Nature 2000, 404, 1011-1013.
20. Bebenek, K.; Matsuda, T.; Masutani, C.; Hanaoka, F.; Kunkel, T.A. Proofreading of DNA polymerase η-dependent replication errors. J. Biol. Chem. 2001, 276, 2317-2320.
21. Shachar, S.; Ziv, O.; Avkin, S.; Adar, S.; Wittschieben, J.; Reissner, T.; Chaney, S.; Friedberg, E.C.; Wang, Z.; Carell, T.; et al. Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J. 2009, 28, 383-393.
22. Hicks, J.K.; Chute, C.L.; Paulsen, M.T.; Ragland, R.L.; Howlett, N.G.; Gueranger, Q.; Glover, T.W.; Canman, C.E. Differential roles for DNA polymerases η, ζ, and Rev1 in lesion bypass of intrastrand versus interstrand DNA cross-links. Mol. Cell Biol. 2010, 30, 1217-1230.
23. Yoon, J.H.; Prakash, L.; Prakash, S. Highly error-free role of DNA polymerase η in the replicative bypass of UV-induced pyrimidine dimers in mouse and human cells. Proc. Natl. Acad. Sci. USA 2009, 106, 18219-18224.
24. Yoon, J.H.; Prakash, L.; Prakash, S. Error-free replicative bypass of (6-4) photoproducts by DNA polymerase ζ in mouse and human cells. Genes Dev. 2010, 24, 123-128.
25. Lehmann, A.R.; Kirk-Bell, S.; Arlett, C.F.; Paterson, M.C.; Lohman, P.H.; de Weerd-Kastelein, E.A.; Bootsma, D. Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. Proc. Natl. Acad. Sci. USA 1975, 72, 219-223.
26. Lehmann, A.R. Postreplication repair of DNA in ultraviolet-irradiated mammalian cells. J. Mol. Biol. 1972, 66, 319-337.
27. Lehmann, A.R. Postreplication repair of DNA in mammalian cells. Life Sci. 1974, 15, 2005-2016.
28. Yamada, K.; Kameyama, Y.; Inoue, S. An improved method of alkaline sucrose density gradient sedimentation to detect less than one lesion per 1 mb DNA. Mutat. Res. 1996, 364, 125-131.
29. Yamada, K.; Takezawa, J.; Ezaki, O. Translesion replication in cisplatin-treated xeroderma pigmentosum variant cells is also caffeine-sensitive: Features of the error-prone DNA polymerase(s) involved in UV-mutagenesis. DNA Repair (Amst.) 2003, 2, 909-924.
30. Takezawa, J.; Ishimi, Y.; Yamada, K. Proteasome inhibitors remarkably prevent translesion replication in cancer cells but not normal cells. Cancer Sci. 2008, 99, 863-871.
31. Kajiwara, K.; Nagasawa, H.; Shimizu-Nishikawa, S.; Ookuri, T.; Kimura, M.; Sugaya, E. Molecular characterization of seizure-related genes isolated by differential screening. Biochem. Biophys. Res. Commun. 1996, 219, 795-799.
32. Kajiwara, K.; O-Wang, J.; Sakurai, T.; Yamashita, S.; Tanaka, M.; Sato, M.; Tagawa, M.; Sugaya, E.; Nakamura, K.; Nakao, K. et al. Sez4 gene encoding an elongation subunit of DNA polymerase ζ is required for normal embryogenesis. Genes Cells 2001, 6, 99-106.
33. O-Wang, J.; Kajiwara, K.; Kawamura, K.; Kimura, M.; Miyagishima, H.; Koseki, H.; Tagawa, M. An essential role for REV3 in mammalian cell survival: Absence of REV3 induces p53-independent embryonic death. Biochem. Biophys. Res. Commun. 2002, 293, 1132-1137.
34. Zhu, F.; Zhang, M. DNA polymerase ζ: New insight into eukaryotic mutagenesis and mammalian embryonic development. World J. Gastroenterol. 2003, 9, 1165-1169.
35. Gan, G.N.; Wittschieben, J.P.; Wittschieben, B.O.; Wood, R.D. DNA polymerase zeta (pol ζ) in higher eukaryotes. Cell Res. 2008, 18, 174-183.
36. Esposito, G.; Godindagger, I.; Klein, U.; Yaspo, M.L.; Cumano, A.; Rajewsky, K. Disruption of the Rev3l-encoded catalytic subunit of polymerase ζ in mice results in early embryonic lethality. Curr. Biol. 2000, 10, 1221-1224.
37. Bemark, M.; Khamlichi, A.A.; Davies, S.L.; Neuberger, M.S. Disruption of mouse polymerase ζ (Rev3) leads to embryonic lethality and impairs blastocyst development in vitro. Curr. Biol. 2000, 10, 1213-1216.
38. Wittschieben, J.; Shivji, M.K.; Lalani, E.; Jacobs, M.A.; Marini, F.; Gearhart, P.J.; Rosewell, I.; Stamp, G.; Wood, R.D. Disruption of the developmentally regulated Rev3l gene causes embryonic lethality. Curr. Biol. 2000, 10, 1217-1220.
39. Van Sloun, P.P.; Varlet, I.; Sonneveld, E.; Boei, J.J.; Romeijn, R.J.; Eeken, J.C.; De Wind, N. Involvement of mouse Rev3 in tolerance of endogenous and exogenous DNA damage. Mol. Cell Biol. 2002, 22, 2159-2169.
40. Jansen, J.G.; Tsaalbi-Shtylik, A.; Hendriks, G.; Verspuy, J.; Gali, H.; Haracska, L.; de Wind, N. Mammalian polymerase ζ is essential for post-replication repair of UV-induced DNA lesions. DNA Repair (Amst.) 2009, 8, 1444-1451.
41. Zander, L.; Bemark, M. Immortalized mouse cell lines that lack a functional Rev3 gene are hypersensitive to UV irradiation and cisplatin treatment. DNA Repair (Amst.) 2004, 3, 743-752.
42. Wittschieben, J.P.; Reshmi, S.C.; Gollin, S.M.; Wood, R.D. Loss of DNA polymerase ζ causes chromosomal instability in mammalian cells. Cancer Res. 2006, 66, 134-142.
43. Avkin, S.; Sevilya, Z.; Toube, L.; Geacintov, N.; Chaney, S.G.; Oren, M.; Livneh, Z. p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol. Cell 2006, 22, 407-413.
44. cip1/waf1 downregulation is required for efficient PCNA ubiquitination after UV irradiation. Oncogene 2006, 25, 2829-2838.
45. Kaufmann, W.K.; Heffernan, T.P.; Beaulieu, L.M.; Doherty, S.; Frank, A.R.; Zhou, Y.; Bryant, M.F.; Zhou, T.; Luche, D.D.; Nikolaishvili-Feinberg, N.; et al. Caffeine and human DNA metabolism: The magic and the mystery. Mutat. Res. 2003, 532, 85-102.
46. Heffernan, T.P.; Kawasumi, M.; Blasina, A.; Anderes, K.; Conney, A.H.; Nghiem, P. ATR-Chk1 pathway inhibition promotes apoptosis after UV treatment in primary human keratinocytes: Potential basis for the UV protective effects of caffeine. J. Invest. Dermatol. 2009, 129, 1805-1815.
47. Ishimi, Y.; Komamura-Kohno, Y.; Karasawa-Shimizu, K.; Yamada, K. Levels of MCM4 phosphorylation and DNA synthesis in DNA replication block checkpoint control. J. Struct. Biol. 2004, 146, 234-241.
48. Despras, E.; Daboussi, F.; Hyrien, O.; Marheineke, K.; Kannouche, P.L. ATR/Chk1 pathway is essential for resumption of DNA synthesis and cell survival in UV-irradiated XP variant cells. Hum. Mol. Genet. 2010, 19, 1690-1701.
49. Niimi, A.; Brown, S.; Sabbioneda, S.; Kannouche, P.L.; Scott, A.; Yasui, A.; Green, C.M.; Lehmann, A.R. Regulation of proliferating cell nuclear antigen ubiquitination in mammalian cells. Proc. Natl. Acad. Sci. USA 2008, 105, 16125-16130.
50. Podlaska, A.; McIntyre, J.; Skoneczna, A.; Sledziewska-Gojska, E. The link between 20S proteasome activity and post-replication DNA repair in Saccharomyces cerevisiae. Mol. Microbiol. 2003, 49, 1321-1332.
51. McIntyre, J.; Podlaska, A.; Skoneczna, A.; Halas, A.; Sledziewska-Gojska, E. Analysis of the spontaneous mutator phenotype associated with 20S proteasome deficiency in S. cerevisiae. Mutat. Res. 2006, 593, 153-163.
52. Sivak, A.; Rudenko, L.; Teague, L.G. Variations among species and cell types in the effects of caffeine on mutagen-induced cytotoxicity and postreplication repair of DNA. Environ. Mutagen. 1982, 4, 143-162.
53. Johansson, F.; Lagerqvist, A.; Filippi, S.; Palitti, F.; Erixon, K.; Helleday, T.; Jenssen, D. Caffeine delays replication fork progression and enhances UV-induced homologous recombination in Chinese hamster cell lines. DNA Repair (Amst.) 2006, 5, 1449-1458.
54. We are using the following rules. Human gene symbols are italicized, with all letters in uppercase. Rodent gene symbols are italicized, with only the first letter in uppercase and the remaining letters in lowercase. Protein designations are not italicized, with all letters in uppercase.