Cloning and characterization of DNA polymerase η from Trypanosoma cruzi: Roles for translesion bypass of oxidative damage

Environmental and Molecular Mutagenesis

Volumn 50, Issue 5, 2009, Pages 375-386

  De Moura, Michelle Barbi ^a   Schamber Reis, Bruno Luiz Fonseca ^a   Silva, Danielle Gomes Passos ^a   Rajão, Matheus Andrade ^a   Macedo, Andréa Mara ^a   Franco, Glória Regina ^a   Pena, Sérgio Danilo Junho ^a   Teixeira, Santuza Maria Ribeiro ^a   Machado, Carlos Renato ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

DNA polymerase ; Functional complementation; Translesion synthesis; Trypanosoma cruzi

Indexed keywords

8 HYDROXYGUANINE; CISPLATIN; DNA DIRECTED DNA POLYMERASE ETA; HYDROGEN PEROXIDE; RECOMBINANT PROTEIN; DNA DIRECTED DNA POLYMERASE; GREEN FLUORESCENT PROTEIN; PROTOZOAL PROTEIN;

ARTICLE; DNA SYNTHESIS; GENE OVEREXPRESSION; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE; TRYPANOSOMA CRUZI; ULTRAVIOLET RADIATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CONFOCAL MICROSCOPY; DRUG EFFECT; ENZYMOLOGY; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NORTHERN BLOTTING; PHYSIOLOGY; RADIATION EXPOSURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

SACCHAROMYCES CEREVISIAE; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, NORTHERN; DNA-DIRECTED DNA POLYMERASE; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; HYDROGEN PEROXIDE; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; TRYPANOSOMA CRUZI; ULTRAVIOLET RAYS;

EID: 67549102396     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20450     Document Type: Article

References (59)

1. Albertella MR, Green CM, Lehmann AR, O'Connor MJ. 2005. A role for polymerase eta in the cellular tolerance to cisplatin-induced damage. Cancer Res 65:9799-9806. (Pubitemid 41541457)
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. (Pubitemid 20364473)
3. Camargo EP. 1964. Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Rev Inst Med Trop Sao Paulo 12:93-100.
4. Casali P, Pal Z, Xu Z, Zan H. 2006. DNA repair in antibody somatic hypermutation. Trends Immunol 27:313-321. (Pubitemid 43963473)
5. Chaney SG, Campbell SL, Bassett E, Wu Y. 2005. Recognition and processing of cisplatin- and oxaliplatin-DNA adducts. Crit Rev Oncol Hematol 53:3-11. (Pubitemid 39656106)
6. Corpet F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881-10890.
7. Costa RM, Chigancas V, Galhardo RS, Carvalho H, CF. 2003. The eukaryotic nucleotide excision repair pathway. Biochimie 85:1083-1099.
8. Coura JR. 2007. Chagas disease: What is known and what is needed- A background article. Mem Inst Oswaldo Cruz 102(Suppl.1): 113-122. (Pubitemid 350146011)
9. DaRocha WD, Silva RA, Bartholomeu DC, Pires SF, Freitas JM, Macedo AM, Vazquez MP, Levin MJ, Teixeira SM. 2004. Expression of exogenous genes in Trypanosoma cruzi: Improving vectors and electroporation protocols. Parasitol Res 92:113-120. (Pubitemid 38187004)
10. de Freitas JM, Augusto-Pinto L, Pimenta JR, Bastos-Rodrigues L, Goncalves VF, Teixeira SM, Chiari E, Junqueira AC, Fernandes O, Macedo AM, Machado CR, Pena SD. 2006. Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLoS Pathog 2:e24.
11. Delbos F, De Smet A, Faili A, Aoufouchi S, Weill JC, Reynaud CA. 2005. Contribution of DNA polymerase eta to immunoglobulin gene hypermutation in the mouse. J Exp Med 201:1191-1196. (Pubitemid 40629063)
12. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou L, Huang Y, Kindlund E, Klingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarleton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B. 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409-415.
13. Fischhaber PL, Friedberg EC. 2005. How are specialized (low-fidelity) eukaryotic polymerases selected and switched with high-fidelity polymerases during translesion DNA synthesis? DNA Repair (Amst) 4:279-283.
14. Gibbs PE, McDonald J, Woodgate R, Lawrence CW. 2005. The relative roles in vivo of Saccharomyces cerevisiae Pol eta, Pol zeta, Rev1 protein and Pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer. Genetics 169:575-582. (Pubitemid 40404295)
15. Gietz RD, Woods RA. 2002. Transformation of yeast by lithium acetate/ single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87-96. (Pubitemid 34619485)
16. Glick E, Vigna KL, Loeb LA. 2001. Mutations in human DNA polymerase eta motif II alter bypass of DNA lesions. EMBO J 20:7303-7312.
17. Gomes ML, Araujo SM, Chiari E. 1991. Trypanosoma cruzi: Growth of clones on solid medium using culture and blood forms. Mem Inst Oswaldo Cruz 86:131-132.
18. Gratchev A, Strein P, Utikal J, Sergij G. 2003. Molecular genetics of Xeroderma pigmentosum variant. Exp Dermatol 12:529-536. (Pubitemid 37270714)
19. Hanawalt PC, Ford JM, Lloyd DR. 2003. Functional characterization of global genomic DNA repair and its implications for cancer. Mutat Res 544:107-114. (Pubitemid 37487654)
20. Haracska L, Yu SL, Johnson RE, Prakash L, Prakash S. 2000. Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polymerase eta. Nat Genet 25:458-461. (Pubitemid 32983443)
21. Haracska L, Kondratick CM, Unk I, Prakash S, Prakash L. 2001a. Interaction with PCNA is essential for yeast DNA polymerase eta function. Mol Cell 8:407-415. (Pubitemid 32831557)
22. Haracska L, Washington MT, Prakash S, Prakash L. 2001b. Inefficient bypass of an abasic site by DNA polymerase eta. J Biol Chem 276:6861-6866. (Pubitemid 37373554)
23. Johansson F, Lagerqvist A, Filippi S, Palitti F, Erixon K, Helleday T, Jenssen D. 2006. Caffeine delays replication fork progression and enhances UV-induced homologous recombination in Chinese hamster cell lines. DNA Repair (Amst) 5:1449-1458. (Pubitemid 44739453)
24. Johnson RE, Prakash S, Prakash L. 1999a. Efficient bypass of a thymine- thymine dimer by yeast DNA polymerase, Poleta. Science 283:1001-1004. (Pubitemid 129505223)
25. Johnson RE, Washington MT, Prakash S, Prakash L. 1999b. Bridging the gap: A family of novel DNA polymerases that replicate faulty DNA. Proc Natl Acad Sci USA 96:12224-12226. (Pubitemid 29513481)
26. Johnson RE, Washington MT, Prakash S, Prakash L. 2000. Fidelity of human DNA polymerase eta. J Biol Chem 275:7447-7450. (Pubitemid 30159635)
27. Kannouche P, Stary A. 2003. Xeroderma pigmentosum variant and errorprone DNA polymerases. Biochimie 85:1123-1132. (Pubitemid 38142366)
28. Kaufmann WK, Heffernan TP, Beaulieu LM, Doherty S, Frank AR, Zhou Y, Bryant MF, Zhou T, Luche DD, Nikolaishvili-Feinberg N, Simpson DA, Cordeiro-Stone M. 2003. Caffeine and human DNA metabolism: The magic and the mystery. Mutat Res 532: 85-102. (Pubitemid 37487848)
29. Kawamoto T, Araki K, Sonoda E, Yamashita YM, Harada K, Kikuchi K, Masutani C, Hanaoka F, Nozaki K, Hashimoto N, Takeda S. 2005. Dual roles for DNA polymerase eta in homologous DNA recombination and translesion DNA synthesis. Mol Cell 20:793-799. (Pubitemid 41740700)
30. Kondratick CM, Washington MT, Prakash S, Prakash L. 2001. Acidic residues critical for the activity and biological function of yeast DNA polymerase eta. Mol Cell Biol 21:2018-2025. (Pubitemid 32479624)
31. Kunkel TA, Pavlov YI, Bebenek K. 2003. Functions of human DNA polymerases eta, kappa and iota suggested by their properties, including fidelity with undamaged DNA templates. DNA Repair (Amst) 2:135-149. (Pubitemid 36071501)
32. Kuraoka I, Suzuki K, Ito S, Hayashida M, Kwei JS, Ikegami T, Handa H, Nakabeppu Y, Tanaka K. 2007. RNA polymerase II bypasses 8-oxoguanine in the presence of transcription elongation factor TFIIS. DNA Repair (Amst) 6:841-851. (Pubitemid 46670099)
33. Larsen E, Kwon K, Coin F, Egly JM, Klungland A. 2004. Transcription activities at 8-oxoG lesions in DNA. DNA Repair (Amst) 3: 1457-1468. (Pubitemid 39221743)
34. Lehmann AR. 2005. Replication of damaged DNA by translesion synthesis in human cells. FEBS Lett 579:873-876. (Pubitemid 40361857)
35. Leibeling D, Laspe P, Emmert S. 2006. Nucleotide excision repair and cancer. J Mol Histol 37:225-238.
36. Lopes DO, Regis-da-Silva CG, Machado-Silva A, Macedo AM, Franco GR, Hoffmann JS, Cazaux C, Pena SD, Teixeira SM, Machado CR. 2007. Analysis of DNA polymerase activity in vitro using non-radioactive primer extension assay in an automated DNA sequencer. Genet Mol Res 6:150-155. (Pubitemid 47327855)
37. Lopes D, Schamber-Reis B, Regis-da-Silva C, Rajão M, DaRocha W, Macedo A, Franco G, Nardelli S, Schenkman S, Hoffmann J, Cazaux C, Pena S, Teixeira S, Machado C. 2008. Biochemical studies with DNA polymerase b and DNA polymerase B-PAK of Trypanosoma cruzi suggest the involvement of these proteins in mitochondrial DNA maintenance. DNA Repair (Amst) 7:1882-1892.
38. Machado CR, Augusto-Pinto L, McCulloch R, Teixeira SM. 2006. DNA metabolism and genetic diversity in Trypanosomes. Mutat Res 612:40-57. (Pubitemid 43038816)
39. Masutani C, Kusumoto R, Yamada A, Dohmae N, Yokoi M, Yuasa M, Araki M, Iwai S, Takio K, Hanaoka F. 1999. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 399:700-704. (Pubitemid 29289067)
40. Masutani C, Kusumoto R, Iwai S, Hanaoka F. 2000. Mechanisms of accurate translesion synthesis by human DNA polymerase eta. EMBO J 19:3100-3109. (Pubitemid 30386780)
41. McIlwraith MJ, Vaisman A, Liu Y, Fanning E, Woodgate R, West SC. 2005. Human DNA polymerase eta promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol Cell 20:783-792. (Pubitemid 41740699)
42. Miles MA, Toye PJ, Oswald SC, Godfrey DG. 1977. The identification by isoenzyme patterns of two distinct strain-groups of Trypanosoma cruzi, circulating independently in a rural area of Brazil. Trans R Soc Trop Med Hyg 71:217-225. (Pubitemid 8126905)
43. Murthy VK, Dibbern KM, Campbell DA. 1992. PCR amplification of mini-exon genes differentiates Trypanosoma cruzi from Trypanosoma rangeli. Mol Cell Probes 6:237-243.
44. Neuberger MS, Rada C. 2007. Somatic hypermutation: Activation-induced deaminase for C/G followed by polymerase eta for A/T. J Exp Med 204:7-10. (Pubitemid 46148749)
45. Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, Prakash L, Prakash S, Todo T, Walker GC, Wang Z, Woodgate R. 2001. The Y-family of DNA polymerases. Mol Cell 8:7-8.
46. Prakash S, Johnson RE, Prakash L. 2005. Eukaryotic translesion synthesis DNA polymerases: Specificity of structure and function. Annu Rev Biochem 74:317-353. (Pubitemid 40995510)
47. Rattray AJ, Strathern JN. 2005. Homologous recombination is promoted by translesion polymerase poleta. Mol Cell 20:658-659. (Pubitemid 41740688)
48. Regis-da-Silva CG, Freitas JM, Passos-Silva DG, Furtado C, Augusto- Pinto L, Pereira MT, DaRocha WD, Franco GR, Macedo AM, Hoffmann JS, Cazaux C, Pena SD, Teixeira SM, Machado CR. 2006. Characterization of the Trypanosoma cruzi Rad51 gene and its role in recombination events associated with the parasite resistance to ionizing radiation. Mol Biochem Parasitol 149:191-200. (Pubitemid 44403932)
49. Santiago MJ, Alejandre-Duran E, Ruiz-Rubio M. 2006. Analysis of UVinduced mutation spectra in Escherichia coli by DNA polymerase eta from Arabidopsis thaliana. Mutat Res 601:51-60. (Pubitemid 44550119)
50. Souto RP, Zingales B. 1993. Sensitive detection and strain classification of Trypanosoma cruzi by amplification of a ribosomal RNA sequence. Mol Biochem Parasitol 62:45-52. (Pubitemid 23360654)
51. Trincao J, Johnson RE, Escalante CR, Prakash S, Prakash L, Aggarwal AK. 2001. Structure of the catalytic core of S. cerevisiae DNA polymerase eta: Implications for translesion DNA synthesis. Mol Cell 8:417-426. (Pubitemid 32831558)
52. Vaisman A, Masutani C, Hanaoka F, Chaney SG. 2000. Efficient translesion replication past oxaliplatin and cisplatin GpG adducts by human DNA polymerase eta. Biochemistry 39:4575-4580. (Pubitemid 30225320)
53. van Hoffen A, Balajee AS, van Zeeland AA, Mullenders LH. 2003. Nucleotide excision repair and its interplay with transcription. Toxicology 193:79-90. (Pubitemid 37340145)
54. Vazquez MP, Levin MJ. 1999. Functional analysis of the intergenic regions of TcP2beta gene loci allowed the construction of an improved Trypanosoma cruzi expression vector. Gene 239:217-225. (Pubitemid 29512351)
55. Yang W. 2005. Portraits of a Y-family DNA polymerase. FEBS Lett 579:868-872.
56. Yuan F, Zhang Y, Rajpal DK, Wu X, Guo D, Wang M, Taylor JS, Wang Z. 2000. Specificity of DNA lesion bypass by the yeast DNA polymerase eta. J Biol Chem 275:8233-8239. (Pubitemid 30159741)
57. Yuasa MS, Masutani C, Hirano A, Cohn MA, Yamaizumi M, Nakatani Y, Hanaoka F. 2006. A human DNA polymerase eta complex containing Rad18, Rad6 and Rev1; Proteomic analysis and targeting of the complex to the chromatin-bound fraction of cells undergoing replication fork arrest. Genes Cells 11:731-744. (Pubitemid 43923345)
58. Zeng X, Winter DB, Kasmer C, Kraemer KH, Lehmann AR, Gearhart PJ. 2001. DNA polymerase eta is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat Immunol 2:537-541. (Pubitemid 33705856)
59. Zhao B, Xie Z, Shen H, Wang Z. 2004. Role of DNA polymerase eta in the bypass of abasic sites in yeast cells. Nucleic Acids Res 32:3984-3994. (Pubitemid 39199090)