Overexpression of DNA polymerase zeta reduces the mitochondrial mutability caused by pathological mutations in DNA polymerase gamma in yeast

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Baruffini, Enrico ^a   Serafini, Fausta ^a   Ferrero, Iliana ^a   Lodi, Tiziana ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE GAMMA; DNA DIRECTED DNA POLYMERASE ZETA; DNA POLYMERASE MIP1; DNA POLYMERASE REV1; DNA POLYMERASE REV3; DNA POLYMERASE REV7; ISOENZYME; MITOCHONDRIAL DNA; UNCLASSIFIED DRUG; DNA DIRECTED DNA POLYMERASE BETA; DNA POLYMERASE ZETA; MIP1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVITY; FUNGAL GENE; GENE MUTATION; GENE OVEREXPRESSION; NONHUMAN; PROTEIN FUNCTION; REV1 GENE; REV3 GENE; REV7 GENE; YEAST; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; MITOCHONDRION; MUTATION; SACCHAROMYCES CEREVISIAE;

DNA POLYMERASE I; DNA, MITOCHONDRIAL; DNA-DIRECTED DNA POLYMERASE; GENE EXPRESSION; MITOCHONDRIA; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84859092589     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034322     Document Type: Article

References (81)

1. Lawrence CW, (2004) Cellular functions of DNA polymerase zeta and Rev1 protein. Adv Protein Chem 69: 167-203.
2. Nelson JR, Lawrence CW, Hinkle DC, (1996) Thymine-thymine dimer bypass by yeast DNA polymerase zeta. Science 272: 1646-1649.
3. Morrison A, Christensen RB, Alley J, Beck AK, Bernstine EG, et al. (1989) REV3, a Saccharomyces cerevisiae gene whose function is required for induced mutagenesis, is predicted to encode a non-essential DNA polymerase. J Bacteriol 171: 5659-5667.
4. Lawrence CW, Hinkle DC, (1996) DNA polymerase zeta and the control of DNA damage induced mutagenesis in eukaryotes, In: Lindahl T, editors. Cancer Surveys: Genetic Stability in Cancer, vol. 28 Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press pp. 21-31.
5. Lawrence CW, Gibbs PEM, Murante RS, Wang X-D, Li Z, et al. (2000) Roles of DNA polymerase zeta and Rev1 protein in eukaryotic mutagenesis and translesion replication, Proceedings of the Cold Spring Harbor Symposia on Quantitative Biology, vol. 65 Cold Spring Habor, NY Cold Spring Harbor Laboratory Press pp. 61-69.
6. Johnson RE, Washington MT, Haracska L, Prakash S, Prakash L, (2000) Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions. Nature 406: 1015-1019.
7. Nelson JR, Lawrence CW, Hinkle DC, (1996) Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382: 729-731.
8. Acharya N, Johnson RE, Prakash S, Prakash L, (2006) Complex formation with Rev1 enhances the proficiency of Saccharomyces cerevisiae DNA polymerase zeta for mismatch extension and for extension opposite from DNA lesions. Mol Cell Biol 26: 9555-9563.
9. Zhang H, Chatterjee A, Singh KK, (2006) Saccharomyces cerevisiae polymerase zeta functions in mitochondria. Genetics 172: 2683-2688.
10. Kalifa L, Sia EA, (2007) Analysis of Rev1p and Pol zeta in mitochondrial mutagenesis suggests an alternative pathway of damage tolerance. DNA Repair 6: 1732-1739.
11. Yakubovskaya E, Chen Z, Carrodeguas JA, Kisker C, Bogenhagen DF, (2006) Functional human mitochondrial DNA polymerase gamma forms a heterotrimer. J Biol Chem 281: 374-382.
12. Lee YS, Kennedy WD, Yin YW, (2009) Structural insight into processive human mitochondrial DNA synthesis and disease-related polymerase mutations. Cell 139: 312-324.
13. Yamanaka H, Gatanaga H, Kosalaraksa P, Matsuoka-Aizawa S, Takahashi T, et al. (2007) Novel mutation of human DNA polymerase gamma associated with mitochondrial toxicity induced by anti-HIV treatment. J Infect Dis 195: 1419-1425.
14. Chiappini F, Teicher E, Saffroy R, Debuire B, Vittecoq D, et al. (2009) Relationship between polymerase gamma (POLG) polymorphisms and antiretroviral therapy induced lipodystrophy in HIV-1 infected patients: a case-control study. Curr HIV Res 7: 244-253.
15. Saneto RP, Lee IC, Koenig MK, Bao X, Wenig SW, et al. (2010) POLG DNA testing as an emerging standard of care before instituting valproic acid therapy for pediatric seizure disorders. Seizure 19: 140-146.
16. Stewart JD, Horvath R, Baruffini E, Ferrero I, Bulst S, et al. (2010) Polymerase γ gene POLG determines the risk of sodium valproate-induced liver toxicity. Hepatology 52: 1791-1796.
17. Singh KK, Ayyasamy V, Owens KM, Koul MS, Vujcic M, (2009) Mutations in mitochondrial DNA polymerase-gamma promote breast tumorigenesis. J Hum Genet 54: 516-524.
18. Lucas P, Lasserre JP, Plissonneau J, Castroviejo M, (2004) Absence of accessory subunit in the DNA polymerase gamma purified from yeast mitochondria. Mitochondrion 4: 13-20.
19. Baruffini E, Lodi T, Dallabona C, Puglisi A, Zeviani M, et al. (2006) Genetic and chemical rescue of the Saccharomyces cerevisiae phenotype induced by mitochondrial DNA polymerase mutations associated with progressive external ophthalmoplegia in humans. Hum Mol Genet 15: 2846-2855.
20. Baruffini E, Ferrero I, Foury F, (2007) Mitochondrial DNA defects in Saccharomyces cerevisiae caused by functional interactions between DNA polymerase gamma mutations associated with disease in human. Biochim Biophys Acta 1772: 225-235.
21. Baruffini E, Horvath R, Dallabona C, Czermin B, Lamantea E, et al. (2011) Predicting the contribution of novel POLG mutations to human disease through analysis in yeast model. Mitochondrion 11: 182-190.
22. Stuart GR, Santos JH, Strand MK, Van Houten B, Copeland WC, (2006) Mitochondrial and nuclear DNA defects in Saccharomyces cerevisiae with mutations in DNA polymerase gamma associated with progressive external ophthalmoplegia. Hum Mol Genet 15: 363-374.
23. Spinazzola A, Invernizzi F, Carrara F, Lamantea E, Donati A, et al. (2009) Clinical and molecular features of mitochondrial DNA depletion syndromes. J Inherit Metab Dis 32: 143-158.
24. Stricker S, Prüss H, Horvath R, Baruffini E, Lodi T, et al. (2009) A variable neurodegenerative phenotype with Polymerase γ mutation. J Neurol Neurosurg Psychiatry 80: 1181-1182.
25. Baruffini E, Lodi T, (2010) Construction and validation of a yeast model system for studying in vivo the susceptibility to nucleoside analogues of DNA polymerase gamma allelic variants. Mitochondrion 10: 183-187.
26. Stumpf JD, Bailey CM, Spell D, Stillwagon M, Anderson KS, et al. (2010) mip1 containing mutations associated with mitochondrial disease causes mutagenesis and depletion of mtDNA in Saccharomyces cerevisiae. Hum Mol Genet 19: 2123-2133.
27. Szczepanowska K, Foury F, (2010) A cluster of pathogenic mutations in the 3′-5′ exonuclease domain of DNA polymerase gamma defines a novel module coupling DNA synthesis and degradation. Hum Mol Genet 19: 3516-3529.
28. Stumpf JD, Copeland WC, (2011) Mitochondrial DNA replication and disease: insights from DNA polymerase γ mutations. Cell Mol Life Sci 68: 219-233.
29. Dujon B, (1981) Mitochondrial genetics and functions. The Molecular Biology of the Yeast Saccharomyces, Life Cycle and Inheritance Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press pp. 505-635.
30. Contamine V, Picard M, (2000) Maintenance and integrity of the mitochondrial genome: a plethora of nuclear genes in the budding yeast. Microbiol Mol Biol Rev 64: 281-315.
31. Sor F, Fukuhara H, (1982) Identification of two erythromycin resistance mutations in the mitochondrial gene coding for the large ribosomal RNA in yeast. Nucleic Acids Res 10: 6571-6577.
32. Sor F, Fukuhara H, (1984) Erythromycin and spiramycin resistance mutations of yeast mitochondria: nature of the rib2 locus in the large ribosomal RNA gene. Nucleic Acids Res 12: 8313-8318.
33. Cui Z, Mason TL, (1989) A single nucleotide substitution at the rib2 locus of the yeast mitochondrial gene for 21 S rRNA confers resistance to erythromycin and cold-sensitive ribosome assembly. Curr Genet 16: 273-279.
34. Vanderstraeten S, Van den Brûle S, Hu J, Foury F, (1998) The role of 3′-5′ exonucleolytic proofreading and mismatch repair in yeast mitochondrial DNA error avoidance. J Biol Chem 273: 23690-23697.
35. Chi NW, Kolodner RD, (1994) The effect of DNA mismatches on the ATPase activity of MSH1, a protein in yeast mitochondria that recognizes DNA mismatches. J Biol Chem 269: 29993-29997.
36. Mieczkowski PA, Fikus MU, Ciesla Z, (1997) Characterization of a novel DNA damage-inducible gene of Saccharomyces cerevisiae, DIN7, which is a structural homolog of the RAD2 and RAD27 DNA repair genes. Mol Gen Genet 253: 655-665.
37. Mookerjee SA, Sia EA, (2006) Overlapping contributions of Msh1p and putative recombination proteins Cce1p, Din7p, and Mhr1p in large-scale recombination and genome sorting events in the mitochondrial genome of Saccharomyces cerevisiae. Mutat Res 595: 91-106.
38. Rajpal DK, Wu X, Wang Z, (2000) Alteration of ultraviolet-induced mutagenesis in yeast through molecular modulation of the REV3 and REV7 gene expression. Mutat Res 461: 133-143.
39. Lecrenier N, Foury F, (1995) Overexpression of the RNR1 gene rescues Saccharomyces cerevisiae mutants in the mitochondrial DNA polymerase-encoding MIP1 gene. Mol Gen Genet 249: 1-7.
40. Thomas BJ, Rothstein R, (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56: 619-630.
41. Baruffini E, Serafini F, Lodi T, (2009) Construction and characterization of centromeric, episomal and GFP-containing vectors for Saccharomyces cerevisiae prototrophic strains. J Biotechnol 143: 247-254.
42. Kaiser C, Michaelis S, Mitchell A, (1994) Methods in Yeast Genetics: a Laboratory Course Manual Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
43. Bonneaud N, Ozier-Kalogeropoulos O, Li GY, Labouesse M, Minvielle-Sebastia L, et al. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast 7: 609-615.
44. Gietz RD, Sugino A, (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74: 527-534.
45. Goldstein AL, McCusker JH, (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
46. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR, (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
47. Gietz RD, Woods RA, (2006) Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods Mol Biol 313: 107-120.
48. Baruffini E, Ferrero I, Foury F, (2010) In vivo analysis of mtDNA replication defects in yeast. Methods 51: 426-436.
49. Lea DE, Coulson CA, (1949) The distribution of the numbers of mutants in bacterial populations. J Genet 49: 264-285.
50. Huang ME, Rio AG, Galibert MD, Galibert F, (2002) Pol32, a subunit of Saccharomyces cerevisiae DNA polymerase delta, suppresses genomic deletions and is involved in the mutagenic bypass pathway. Genetics 160: 1409-1422.
51. Hall BM, Ma C, Liang P, Singh KK, (2009) Fluctuation AnaLysis CalculatOR (FALCOR): a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 25: 1564-1565.
52. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, et al. (1994) Current Protocols in Molecular Biology New York Wiley.
53. Sherman F, Fink GR, Hicks JB, (1986) Laboratory Course Manual for Methods in Yeast Genetics Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
54. Acharya N, Haracska L, Johnson RE, Unk I, Prakash S, et al. (2005) Complex formation of yeast Rev1 and Rev7 proteins: a novel role for the polymerase-associated domain. Mol Cell Biol 25: 9734-9740.
55. Zhao X, Muller EG, Rothstein R, (1998) A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 2: 329-340.
56. Dingwall C, Robbins J, Dilworth SM, Roberts B, Richardson WD, (1988) The nucleoplasmin nuclear location sequence is larger and more complex than that of SV-40 large T antigen. J Cell Biol 107: 841-849.
57. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691.
58. Singhal RK, Hinkle DC, Lawrence CW, (1992) The REV3 gene of Saccharomyces cerevisiae is transcriptionally regulated more like a repair gene than one encoding a DNA polymerase. Mol Gen Genet 236: 17-24.
59. Küenzi MT, Tingle MA, Halvorson HO, (1974) Sporulation of Saccharomyces cerevisiae in the absence of a functional mitochondrial genome. J Bacteriol 117: 80-88.
60. Codón AC, Gasent-Ramírez JM, Benítez T, (1995) Factors which affect the frequency of sporulation and tetrad formation in Saccharomyces cerevisiae baker's yeasts. Appl Environ Microbiol 61: 630-638.
61. Ponamarev MV, Longley MJ, Nguyen D, Kunkel TA, Copeland WC, (2002) Active site mutation in DNA polymerase gamma associated with progressive external ophthalmoplegia causes error-prone DNA synthesis. J Biol Chem 77: 15225-15228.
62. Graziewicz MA, Longley MJ, Bienstock RJ, Zeviani M, Copeland WC, (2004) Structure-function defects of human mitochondrial DNA polymerase in autosomal dominant progressive external ophthalmoplegia. Nat Struct Mol Biol 11: 770-776.
63. Graziewicz MA, Bienstock RJ, Copeland WC, (2007) The DNA polymerase gamma Y955C disease variant associated with PEO and parkinsonism mediates the incorporation and translesion synthesis opposite 7,8-dihydro-8-oxo-2′-deoxyguanosine. Hum Mol Genet 16: 2729-2739.
64. Wanrooij S, Goffart S, Pohjoismäki JL, Yasukawa T, Spelbrink JN, (2007) Expression of catalytic mutants of the mtDNA helicase Twinkle and polymerase POLG causes distinct replication stalling phenotypes. Nucleic Acids Res 35: 3238-3251.
65. Atanassova N, Fusté JM, Wanrooij S, Macao B, Goffart S, et al. (2011) Sequence-specific stalling of DNA polymerase γ and the effects of mutations causing progressive ophthalmoplegia. Hum Mol Genet 20: 1212-1223.
66. Lee JC, Straffon MJ, Jang TY, Higgins VJ, Grant CM, et al. (2001) The essential and ancillary role of glutathione in Saccharomyces cerevisiae analysed using a grande gsh1 disruptant strain. FEMS Yeast Res 1: 57-65.
67. Gibson BR, Prescott KA, Smart KA, (2008) Petite mutation in aged and oxidatively stressed ale and lager brewing yeast. Lett Appl Microbiol 46: 636-642.
68. Kaniak A, Dzierzbicki P, Rogowska AT, Malc E, Fikus M, et al. (2009) Msh1p counteracts oxidative lesion-induced instability of mtDNA and stimulates mitochondrial recombination in Saccharomyces cerevisiae. DNA Repair (Amst) 8: 318-329.
69. Euro L, Farnum GA, Palin E, Suomalainen A, Kaguni LS, (2011) Clustering of Alpers disease mutations and catalytic defects in biochemical variants reveal new features of molecular mechanism of the human mitochondrial replicase, Pol γ. Nucleic Acids Res 39: 9072-9084.
70. de Padula M, Slezak G, Auffret van Der Kemp P, Boiteux S, (2004) The post-replication repair RAD18 and RAD6 genes are involved in the prevention of spontaneous mutations caused by 7,8-dihydro-8-oxoguanine in Saccharomyces cerevisiae. Nucleic Acids Res 32: 5003-5010.
71. Haracska L, Prakash S, Prakash L, (2003) Yeast DNA polymerase zeta is an efficient extender of primer ends opposite from 7,8-dihydro-8-Oxoguanine and O6-methylguanine. Mol Cell Biol 23: 1453-1459.
72. Northam MR, Robinson HA, Kochenova OV, Shcherbakova PV, (2010) Participation of DNA polymerase zeta in replication of undamaged DNA in Saccharomyces cerevisiae. Genetics 184: 27-42.
73. Pinz KG, Shibutani S, Bogenhagen DF, (1995) Action of mitochondrial DNA polymerase gamma at sites of base loss or oxidative damage. J Biol Chem 270: 9202-9206.
74. Graziewicz MA, Sayer JM, Jerina DM, Copeland WC, (2004) Nucleotide incorporation by human DNA polymerase gamma opposite benzo[a]pyrene and benzo[c]phenanthrene diol epoxide adducts of deoxyguanosine and deoxyadenosine. Nucleic Acids Res 32: 397-405.
75. Kasiviswanathan R, Gustafson MA, Copeland WC, Meyer JN, (2011) Human mitochondrial DNA polymerase γ exhibits potential for bypass and mutagenesis at UV-induced cyclobutane thymine dimers. J Biol Chem doi: 10.1074/jbc.M111.306852 jbc.M111.306852.
76. Taylor SD, Zhang H, Eaton JS, Rodeheffer MS, Lebedeva MA, et al. (2005) The conserved Mec1/Rad53 nuclear checkpoint pathway regulates mitochondrial DNA copy number in Saccharomyces cerevisiae. Mol Biol Cell 16: 3010-3018.
77. Lebedeva MA, Shadel GS, (2007) Cell cycle- and ribonucleotide reductase-driven changes in mtDNA copy number influence mtDNA Inheritance without compromising mitochondrial gene expression. Cell Cycle 6: 2048-2057.
78. Sembongi H, Di Re M, Bokori-Brown M, Holt IJ, (2007) The yeast Holliday junction resolvase, CCE1, can restore wild-type mitochondrial DNA to human cells carrying rearranged mitochondrial DNA. Hum Mol Genet 16: 2306-2314.
79. Bulst S, Abicht A, Holinski-Feder E, Müller-Ziermann S, Koehler U, et al. (2009) In vitro supplementation with dAMP/dGMP leads to partial restoration of mtDNA levels in mitochondrial depletion syndromes. Hum Mol Genet 18: 1590-1599.
80. Filosto M, Mancuso M, Nishigaki Y, Pancrudo J, Harati Y, et al. (2003) Clinical and genetic heterogeneity in progressive external ophthalmoplegia due to mutations in polymerase gamma. Arch Neurol 60: 1279-1284.
81. Hisama FM, Mancuso M, Filosto M, DiMauro S, (2005) Progressive external ophthalmoplegia: a new family with tremor and peripheral neuropathy. Am J Med Genet A 135: 217-219.