Increased uracil insertion in DNA is cytotoxic and increases the frequency of mutation, double strand break formation and VSG switching in Trypanosoma brucei

DNA Repair

Volumn 11, Issue 12, 2012, Pages 986-995

  Castillo Acosta, Víctor M ^a   Aguilar Pereyra, Fernando ^a   Bart, Jean Mathieu ^a   Navarro, Miguel ^a   Ruiz Pérez, Luis M ^a   Vidal, Antonio E ^a   González Pacanowska, Dolores ^a  

^a INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

Author keywords

Deoxyuridine triphosphate nucleotidohydrolase; DUTPase; Trypanosoma brucei; UNG; Uracil; Uracil DNA glycosylase

Indexed keywords

DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; DOUBLE STRANDED DNA; URACIL; URACIL DNA GLYCOSIDASE; VARIANT SURFACE GLYCOPROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL VIABILITY; DNA DAMAGE; DNA FRAGMENTATION; DNA STRAND BREAKAGE; DOWN REGULATION; ENZYME ACTIVITY; EXCISION REPAIR; GENE DELETION; GENE FREQUENCY; GENE INSERTION; GENE MUTATION; GENETIC STABILITY; NONHUMAN; PRIORITY JOURNAL; TRYPANOSOMA BRUCEI;

DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA, PROTOZOAN; ENZYME ASSAYS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE SILENCING; GENES, PROTOZOAN; IN SITU NICK-END LABELING; MUTATION; MUTATION RATE; PYROPHOSPHATASES; TRANSFECTION; TRYPANOSOMA BRUCEI BRUCEI; URACIL; URACIL-DNA GLYCOSIDASE; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA;

TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 84869177694     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.09.007     Document Type: Article

References (52)

1. Auerbach P., Bennett R.A., Bailey E.A., Krokan H.E., Demple B. Mutagenic specificity of endogenously generated abasic sites in Saccharomyces cerevisiae chromosomal DNA. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17711-17716.
2. Blount B.C., Mack M.M., Wehr C.M., MacGregor J.T., Hiatt R.A., Wang G., Wickramasinghe S.N., Everson R.B., Ames B.N. Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:3290-3295.
3. Duthie S.J., Narayanan S., Sharp L., Little J., Basten G., Powers H. Folate, DNA stability and colo-rectal neoplasia. Proc. Nutr. Soc. 2004, 63:571-578.
4. Ahmad S.I., Kirk S.H., Eisenstark A. Thymine metabolism and thymineless death in prokaryotes and eukaryotes. Annu. Rev. Microbiol. 1998, 52:591-625.
5. Fenech M. The role of folic acid and Vitamin B12 in genomic stability of human cells. Mutat. Res. 2001, 475:57-67.
6. Di Noia J.M., Neuberger M.S. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 2007, 76:1-22.
7. Mangeat B., Turelli P., Caron G., Friedli M., Perrin L., Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 2003, 424:99-103.
8. Bishop K.N., Holmes R.K., Sheehy A.M., Malim M.H. APOBEC-mediated editing of viral RNA. Science 2004, 305:645.
9. Kim N., Jinks-Robertson S. dUTP incorporation into genomic DNA is linked to transcription in yeast. Nature 2009, 459:1150-1153.
10. el-Hajj H.H., Zhang H., Weiss B. Lethality of a dut (deoxyuridine triphosphatase) mutation in Escherichia coli. J. Bacteriol. 1988, 170:1069-1075.
11. Gadsden M.H., McIntosh E.M., Game J.C., Wilson P.J., Haynes R.H. dUTP pyrophosphatase is an essential enzyme in Saccharomyces cerevisiae. EMBO J. 1993, 12:4425-4431.
12. Dengg M., Garcia-Muse T., Gill S.G., Ashcroft N., Boulton S.J., Nilsen H. Abrogation of the CLK-2 checkpoint leads to tolerance to base-excision repair intermediates. EMBO Rep. 2006, 7:1046-1051.
13. Dubois E., Cordoba-Canero D., Massot S., Siaud N., Gakiere B., Domenichini S., Guerard F., Roldan-Arjona T., Doutriaux M.P. Homologous recombination is stimulated by a decrease in dUTPase in Arabidopsis. PLoS ONE 2011, 6:e18658.
14. Guillet M., Van Der Kemp P.A., Boiteux S. dUTPase activity is critical to maintain genetic stability in Saccharomyces cerevisiae. Nucleic Acids Res. 2006, 34:2056-2066.
15. McIntosh E.M., Haynes R.H. dUTP pyrophosphatase as a potential target for chemotherapeutic drug development. Acta Biochim. Pol. 1997, 44:159-171.
16. Ladner R.D. The role of dUTPase and uracil-DNA repair in cancer chemotherapy. Curr. Protein Pept. Sci. 2001, 2:361-370.
17. Moroz O.V., Murzin A.G., Makarova K.S., Koonin E.V., Wilson K.S., Galperin M.Y. Dimeric dUTPases, HisE, and MazG belong to a new superfamily of all-alpha NTP pyrophosphohydrolases with potential " house-cleaning" functions. J. Mol. Biol. 2005, 347:243-255.
18. Castillo-Acosta V.M., Estevez A.M., Vidal A.E., Ruiz-Perez L.M., Gonzalez-Pacanowska D. Depletion of dimeric all-alpha dUTPase induces DNA strand breaks and impairs cell cycle progression in Trypanosoma brucei. Int. J. Biochem. Cell Biol. 2008, 40:2901-2913.
19. Lindahl T., Ljungquist S., Siegert W., Nyberg B., Sperens B. DNA N-glycosidases: properties of uracil-DNA glycosidase from Escherichia coli. J. Biol. Chem. 1977, 252:3286-3294.
20. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press, Washington, DC. 2nd ed.
21. Duncan B.K., Weiss B. Specific mutator effects of ung (uracil-DNA glycosylase) mutations in Escherichia coli. J. Bacteriol. 1982, 151:750-755.
22. Impellizzeri K.J., Anderson B., Burgers P.M. The spectrum of spontaneous mutations in a Saccharomyces cerevisiae uracil-DNA-glycosylase mutant limits the function of this enzyme to cytosine deamination repair. J. Bacteriol. 1991, 173:6807-6810.
23. Chatterjee A., Singh K.K. Uracil-DNA glycosylase-deficient yeast exhibit a mitochondrial mutator phenotype. Nucleic Acids Res. 2001, 29:4935-4940.
24. Castillo-Acosta V.M., Aguilar-Pereyra F., Vidal A.E., Navarro M., Ruiz-Perez L.M., Gonzalez-Pacanowska D. Trypanosomes lacking uracil-DNA glycosylase are hypersensitive to antifolates and present a mutator phenotype. Int. J. Biochem. Cell Biol. 2012, 44:1555-1568.
25. Koehler S.E., Ladner R.D. Small interfering RNA-mediated suppression of dUTPase sensitizes cancer cell lines to thymidylate synthase inhibition. Mol. Pharmacol. 2004, 66:620-626.
26. Warner H.R., Duncan B.K., Garrett C., Neuhard J. Synthesis and metabolism of uracil-containing deoxyribonucleic acid in Escherichia coli. J. Bacteriol. 1981, 145:687-695.
27. Taylor J.E., Rudenko G. Switching trypanosome coats: what's in the wardrobe?. Trends Genet. 2006, 22:614-620.
28. Conway C., Proudfoot C., Burton P., Barry J.D., McCulloch R. Two pathways of homologous recombination in Trypanosoma brucei. Mol. Microbiol. 2002, 45:1687-1700.
29. Boothroyd C.E., Dreesen O., Leonova T., Ly K.I., Figueiredo L.M., Cross G.A., Papavasiliou F.N. A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei. Nature 2009, 459:278-281.
30. Wirtz E., Leal S., Ochatt C., Cross G.A. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 1999, 99:89-101.
31. Estevez A.M., Kempf T., Clayton C. The exosome of Trypanosoma brucei. EMBO J. 2001, 20:3831-3839.
32. Luria S.E., Delbruck M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 1943, 28:491-511.
33. Sedwick W.D., Brown O.E., Glickman B.W. Deoxyuridine misincorporation causes site-specific mutational lesions in the lacI gene of Escherichia coli. Mutat. Res. 1986, 162:7-20.
34. Morrison L.J., Marcello L., McCulloch R. Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity. Cell. Microbiol. 2009, 11:1724-1734.
35. Bekesi A., Pukancsik M., Muha V., Zagyva I., Leveles I., Hunyadi-Gulyas E., Klement E., Medzihradszky K.F., Kele Z., Erdei A., Felfoldi F., Konya E., Vertessy B.G. A novel fruitfly protein under developmental control degrades uracil-DNA. Biochem. Biophys. Res. Commun. 2007, 355:643-648.
36. Schanz S., Castor D., Fischer F., Jiricny J. Interference of mismatch and base excision repair during the processing of adjacent U/G mispairs may play a key role in somatic hypermutation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5593-5598.
37. Kow Y.W. Repair of deaminated bases in DNA. Free Radic. Biol. Med. 2002, 33:886-893.
38. Lopez-Olmos K., Hernandez M.P., Contreras-Garduno J.A., Robleto E.A., Setlow P., Yasbin R.E., Pedraza-Reyes M. Roles of endonuclease V, uracil-DNA glycosylase, and mismatch repair in Bacillus subtilis DNA base-deamination-induced mutagenesis. J. Bacteriol. 2012, 194:243-252.
39. Gates F.T., Linn S. Endonuclease V of Escherichia coli. J. Biol. Chem. 1977, 252:1647-1653.
40. Yao M., Kow Y.W. Further characterization of Escherichia coli endonuclease V. Mechanism of recognition for deoxyinosine, deoxyuridine, and base mismatches in DNA. J. Biol. Chem. 1997, 272:30774-30779.
41. He B., Qing H., Kow Y.W. Deoxyxanthosine in DNA is repaired by Escherichia coli endonuclease V. Mutat. Res. 2000, 459:109-114.
42. Kunkel T.A., Schaaper R.M., Loeb L.A. Depurination-induced infidelity of deoxyribonucleic acid synthesis with purified deoxyribonucleic acid replication proteins in vitro. Biochemistry 1983, 22:2378-2384.
43. Kim N., Mudrak S.V., Jinks-Robertson S. The dCMP transferase activity of yeast Rev1 is biologically relevant during the bypass of endogenously generated AP sites. DNA Repair (Amst) 2011, 10:1262-1271.
44. Auerbach P.A., Demple B. Roles of Rev1, Pol zeta, Pol32 and Pol eta in the bypass of chromosomal abasic sites in Saccharomyces cerevisiae. Mutagenesis 2010, 25:63-69.
45. Kouzminova E.A., Kuzminov A. Patterns of chromosomal fragmentation due to uracil-DNA incorporation reveal a novel mechanism of replication-dependent double-stranded breaks. Mol. Microbiol. 2008, 68:202-215.
46. Nitiss J., Wang J.C. DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:7501-7505.
47. Smih F., Rouet P., Romanienko P.J., Jasin M. Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res. 1995, 23:5012-5019.
48. Kouzminova E.A., Kuzminov A. Chromosomal fragmentation in dUTPase-deficient mutants of Escherichia coli and its recombinational repair. Mol. Microbiol. 2004, 51:1279-1295.
49. Kouzminova E.A., Kuzminov A. Fragmentation of replicating chromosomes triggered by uracil in DNA. J. Mol. Biol. 2006, 355:20-33.
50. Glover L., McCulloch R., Horn D. Sequence homology and microhomology dominate chromosomal double-strand break repair in African trypanosomes. Nucleic Acids Res. 2008, 36:2608-2618.
51. Glover L., Jun J., Horn D. Microhomology-mediated deletion and gene conversion in African trypanosomes. Nucleic Acids Res. 2011, 39:1372-1380.
52. Guerra-Giraldez C., Quijada L., Clayton C.E. Compartmentation of enzymes in a microbody, the glycosome, is essential in Trypanosoma brucei. J. Cell Sci. 2002, 115:2651-2658.