Biochemical, cellular and molecular identification of DNA polymerase α in yeast mitochondria

Biochimie

Volumn 95, Issue 4, 2013, Pages 759-771

  Lasserre, Jean Paul ^a,c   Plissonneau, Jacqueline ^a   Velours, Christophe ^a,d   Bonneu, Marc ^b   Litvak, Simon ^a   Laquel, Patricia ^a   Castroviejo, Michel ^a  

^a University Victor Segalen   (France)

^b ESTBB   (France)

^c Institut de Biochimie et Genetique Cellulaires   (France)

^d IMAGIF   (France)

Author keywords

DNA polymerase; Mitochondria; Purification; Subcellular localization; Yeast

Indexed keywords

BIOLOGICAL MARKER; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE; MITOCHONDRIAL DNA; PROTEINASE K; SUCROSE;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL ORGANELLE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; ENZYME ANALYSIS; ENZYME LOCALIZATION; FUNGAL STRAIN; IMMUNOBLOTTING; MASS SPECTROMETRY; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SUCROSE GRADIENT; WESTERN BLOTTING; YEAST; YEAST CELL;

DNA POLYMERASE I; DNA REPLICATION; DNA, MITOCHONDRIAL; ENDOPEPTIDASE K; MITOCHONDRIA; MUTATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

ALGAE; EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 84874647970     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.11.003     Document Type: Article

References (68)

1. N. Lecrenier, and F. Foury New features of mitochondrial DNA replication system in yeast and man Gene 246 2000 37 48
2. S.P. LeDoux, and G.L. Wilson Base excision repair of mitochondrial DNA damage in mammalian cells Prog. Nucleic Acid Res. Mol. Biol. 68 2001 273 284
3. K.K. Singh, H.A. Sigala, G.K. Sikder, and C. Schwimmer Inactivation of Saccharomyces cerevisiae OGG1 gene leads to increased frequency of mitochondrial deletions Nucleic Acids Res. 29 2001 1381 1388
4. D.C. Wallace A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine Annu. Rev. Genet. 39 2005 359 407
5. G.S. Shadel Expression and maintenance of mitochondrial DNA: new insights into human disease Am. J. Pathol. 172 6 2008 1445 1456
6. E. Arnaudo, S. Shanske, S. DiMauro, E.A. Schon, C.T. Moraes, E.A. Schon, and C.T. Dalakas Depletion of muscle mitochondrial DNA in AIDS patients with zidovudine-induced myopathy The Lancet 337 1991 508 510
7. P.M. Burgers, E.V. Koonin, E. Bruford, L. Blanco, K.C. Burtis, M.F. Christman, W.C. Copeland, E.C. Friedberg, F. Hanaoka, D.C. Hinkle, C.W. Lawrence, M. Nakanishi, H. Ohmori, L. Prakash, S. Prakash, C.A. Reynaud, A. Sugino, T. Todo, Z. Wang, J.C. Weill, and R. Woodgate Eukaryotic DNA polymerases: proposal for a revised nomenclature J. Biol. Chem. 276 2001 43487 43490
8. A. Johnson, and M. O'Donnell Cellular DNA replicases: components and dynamics at the replication fork Annu. Rev. Biochem. 74 2005 283 315
9. S.D. McCulloch, and T.A. Kunkel The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases Cell. Res. 18 2008 148 161
10. U. Hübscher, G. Maga, and S. Spadari Eukaryotic DNA polymerases Annu. Rev. Biochem. 71 2002 133 163
11. L.S. Kaguni DNA polymerase γ, the mitochondrial replicase Annu. Rev. Biochem. 73 2004 293 320
12. Y. Wang, C.L. Farr, and L.S. Kaguni Accessory subunit of mitochondrial DNA polymerase from Drosophila embryos. Cloning, molecular analysis, and association in the native enzyme J. Biol. Chem. 272 1997 13640 13646
13. E. Yakubovskaya, Z. Chen, J.A. Carrodeguas, C. Kisker, and D.F. Bogenhagen Functional human mitochondrial DNA polymerase gamma forms a heterotrimer J. Biol. Chem. 281 2006 374 382
14. J.A. Carrodeguas, R. Kobayashi, S.E. Lim, W.C. Copeland, and D.F. Bogenhagen The accessory subunit of Xenopus laevis mitochondrial DNA polymerase gamma increases processivity of the catalytic subunit of human DNA polymerase gamma and is related to class II aminoacyl-tRNA synthetases Mol. Cell. Biol. 19 1999 4039 4046
15. P. Lucas, J.P. Lasserre, J. Plissonneau, and M. Castroviejo Absence of accessory subunit in the polymerase γ purified from yeast mitochondria Mitochondrion 4 2004 13 20
16. A.I.F. Torri, and P.T. Englund Purification of a mitochondrial DNA polymerase from Crithidia fasciculata J. Biol. Chem. 267 1992 4786 4792
17. A.I.F. Torri, and P.T. Englund A DNA polymerase β in the mitochondrion of the Trypanosomatid Crithidia fasciculate J. Biol. Chem. 270 1995 3495 3497
18. A.I.F. Torri, T.A. Kunkel, and P.T. Englund A β-like DNA polymerase from the mitochondrion of the trypanosomatid Crithidia fasciculata J. Biol. Chem. 269 1994 8165 8171
19. J. Fuenmayor, J. Zhang, W. Ruyechan, and N. Williams Identification and characterization of two DNA polymerase activities present in Trypanosoma brucei mitochondria J. Eukaryot. Microbiol. 45 4 1998 404 410
20. M.M. Klingbeil, S.A. Motyka, and P.T. Englund Multiple mitochondrial DNA polymerases in Trypanosoma brucei Mol. Cell 10 2002 175 186
21. J. Chandler, A.V. Vandoros, B. Mozeleski, and M.M. Klingbeil Stem-loop silencing reveals that a third mitochondrial DNA polymerase, POLID, is required for kinetoplast DNA replication in trypanosomes Eukaryot. Cell 7 2008 2141 2146
22. T.T. Saxowsky, G. Choudhary, M.M. Klingbeil, and P.T. Englund Trypanosoma brucei has two distinct mitochondrial DNA polymerase beta enzymes J. Biol. Chem. 278 2003 49095 49101
23. P. Lucas, P. Laquel-Robert, J. Plissonneau, J. Schaeffer, L. Tarrogo-Litvak, and M. Castroviejo A second DNA polymerase activity in yeast mitochondria C. R. Acad. Sci. III 320 1997 299 305
24. M. Castroviejo, D. Tharaud, L. Tarrago-Litvak, and S. Litvak Multiple deoxyribonucleic acid polymerases from quiescent wheat embryos. Purification and characterization of three enzymes from the soluble cytoplasm and one from purified mitochondria Biochem. J. 181 1979 183 191
25. A.B. Hansen, N.B. Griner, J.P. Anderson, G.C. Kujoth, T.A. Prolla, L.A. Loeb, and E. Glick Mitochondrial DNA integrity is not dependent on DNA polymerase-β activity DNA Repair [Amst] 5 1 2006 71 79
26. N.M. Camougrand, A. Cheyrou, M.F. Henry, and M.G. Guérin The alternative respiratory pathway of the yeast Candida parapsilosis: oxidation of exogenous NAD[P]H J. Gen. Microbiol. 134 1988 3195 3204
27. J. Velours, B. Guerin, and M. Duvert Preparation of an inner membrane-matrix fraction from yeast mitochondria Arch. Biochem. Biophys. 182 1977 295 304
28. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
29. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
30. W.K. Huh, J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O'Shea Global analysis of protein localization in budding yeast Nature 425 6959 2003 686 691
31. B. Westermann, and W. Neupert Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae Yeast 16 15 2000 1421 1427
32. R.D. Gietz, and R.H. Schiestl High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method Nat. Protoc. 2 2007 31 34
33. M. Akbari, T. Visnes, H.E. Krokan, and M. Otterlei Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis DNA Repair 7 2008 605 616
34. F. Foury Cloning and sequencing of the nuclear gene MIP1encoding the catalytic subunit of the yeast mitochondrial DNA polymerase J. Biol. Chem. 264 1989 20552 20560
35. M.A. Rajão, D.G. Passos-Silva, W.D. DaRocha, G.R. Franco, A.M. Macedo, S.D. Pena, S.M. Teixeira, and C.R. Machado DNA polymerase kappa from Trypanosoma cruzi localizes to the mitochondria, bypasses 8-oxoguanine lesions and performs DNA synthesis in a recombination intermediate Mol. Microbiol. 71 2009 185 197
36. H. Lodish, D. Baltimore, A. Berk, S.L. Zipursky, P. Matsudaira, and J. Darnell Moelcular Cell Biology third ed. 1995 W.H. Freeman and Company New York
37. S. Meeusen, and J. Nunnari Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome Cell Biol. 163 3 2003 503 510
38. F. Evanics, L. Maurmann, W.W. Yang, and R.N. Bose Nuclear magnetic resonance structures of the zinc finger domain of human DNA polymerase-alpha Biochim. Biophys. Acta 1651 2003 163 171
39. T. Mizuno, K. Yamagishi, H. Miyazawa, and F. Hanaoka Molecular architecture of the mouse DNA polymerase α-primase complex Mol. Cell. Biol. 19 11 1999 7886 7896
40. P. Plevani, M. Foiani, P. Valsasnini, G. Badaracco, E. Cheriathundam, and L.M. Chang Polypeptide structure of DNA primase from a yeast DNA polymerase-primase complex J. Biol. Chem. 260 1985 7102 7107
41. E.E. Biswas, P.H. Chen, W. Gray, Y.H. Li, S. Ray, and S.B. Biswas Purification and characterization of a yeast DNA polymerase alpha complex with associated primase, 5′ > 3′ exonuclease, and DNA-dependent ATPase activities Biochemistry 32 1993 3013 3019
42. S. Wanrooij, J.M. Fusté, G. Farge, Y. Shi, C.M. Gustafsson, and M. Falkenberg Human mitochondrial RNA polymerase primes lagging-strand DNA synthesis in vitro Proc. Natl. Acad. Sci. U. S. A. 105 2008 11122 11127
43. L.L. Stohl, and D.A. Clayton Inactivation of Saccharomyces cerevisiae OGG1 gene leads to increased frequency of mitochondrial deletions Mol. Cell. Biol. 12 1992 2561 2569
44. E.D. Wong, J.A. Wagner, S.W. Gorsich, J.M. McCaffery, J. Shaw, and J. Nunnari The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria J. Cell. Biol. 151 2000 341 352
45. H. Zhang, A. Chatterjee, and K.K. Singh Saccharomyces cerevisiae polymerase zeta functions in mitochondria Genetics 105 2006 2683 2688
46. L. Kalifa, and E.A. Sia Analysis of Rev1p and pol ζ in mitochondrial mutagenesis suggests an alternative pathway of damage tolerance DNA Repair [Amst]. 6 12 2007 1732 1739
47. A. Sickmann, J. Reinders, Y. Wagner, C. Joppich, R. Zahedi, H.E. Meyer, B. Schönfisch, I. Perschil, A. Chacinska, B. Guiard, P. Rehling, N. Pfanner, and C. Meisinger The proteome of Saccharomyces cerevisiae mitochondria Proc. Natl. Acad. Sci. U. S. A. 100 2003 13207 13212
48. M. Bohnert, N. Pfanner, and M. van der Laan A dynamic machinery for import of mitochondrial precursor proteins FEBS Lett. 581 2007 2802 2810
49. N. Bolender, A. Sickmann, R. Wagner, C. Meisinger, and N. Pfanner Multiple pathways for sorting mitochondrial precursor proteins EMBO Rep. 9 2008 42 49
50. M.F. Bauer, S. Hofmann, W. Neupert, and M. Brunner Protein translocation into mitochondria: the role of TIM complexes Trends Cell. Biol. 10 2000 25 31
51. S.A. Paschen, and W. Neupert Protein import into mitochondria IUBMB Life 52 2001 101 112
52. C.J. Danpure How can the products of a single gene be localized to more than one intracellular compartment? Trends Cell Biol. 5 1995 230 238
53. S. Karniely, and O. Pines Single translation-dual destination: mechanisms of dual protein targeting in eukaryote BO Rep. 6 5 1995 420 425
54. R. Vongsamphanh, P.K. Fortier, and D. Ramotar Pir1p mediates translocation of the yeast Apn1p endonuclease into the mitochondria to maintain genomic stability Mol. Cell. Biol. 21 2001 1647 1655
55. K. Diekert, A.I. de Kroon, U. Ahting, B. Niggemeyer, W. Neupert, B. de Kruijff, and R. Lill Apocytochrome C requires the TOM complex for translocation across the mitochondrial outer membrane EMBO J. 20 2001 5626 5635
56. T.K. Biswas, and G.S. Getz Import of yeast mitochondrial transcription factor [Mtf1p] via a nonconventional pathway J. Biol. Chem. 277 2002 45704 45714
57. T.K. Biswas, and G.S. Getz Requirement of different mitochondrial targeting sequences of the yeast mitochondrial transcription factor Mtf1p when synthesized in alternative translation systems Biochem. J. 383 2004 383 391
58. F. Ling, A. Hori, and T. Shibata DNA recombination-initiation plays a role in the extremely biased inheritance of yeast [rho-] mitochondrial DNA that contains the replication origin ori5 Mol. Cell. Biol. 27 2007 1133 1145
59. M. Kucej, and R.A. Butow Evolutionary tinkering with mitochondrial nucleoids Trends Cell Biol. 17 2007 586 592
60. X.M. Zuo, G.D. Clark-Walker, and X.J. Chen The mitochondrial nucleoid protein, Mgm101p, of Saccharomyces cerevisiae is involved in the maintenance of rho[+] and ori/rep-devoid petite genomes but is not required for hypersuppressive rho[-] mtDNA Genetics 160 2002 1389 1400
61. J.M. Gerhold, A. Aun, T. Sedman, P. Joers, and J. Sedman Strand invasion structures in the inverted repeat of Candida albicans mitochondrial DNA reveal a role for homologous recombination in replication Mol. Cell 39 2010 851 861
62. A.J. Bendich The size and form of chromosomes are constant in the nucleus, but highly variable in bacteria, mitochondria and chloroplasts Bioassays 29 2007 474 483
63. I.J. Holt Mitochondrial DNA replication and repair: all a flap Trends Biochem. Sci. 34 2009 358 365
64. J.L.O. Pohjoisäki, and S. Goffart Of circles, forks and humanity: topological organisation and replication of mammalian mitochondrial DNA Biossays 33 2011 290 299
65. A.J. Bendich The end of the circle for yeast mitochondrial DNA Mol. Cell 39 2010 831 832
66. K. Viikov, P. Väljamäe, and J. Sedman Yeast mitochondrial DNA polymerase is a highly processive single-subunit enzyme Mitochondrion 11 1 2011 119 126
67. M.N. Rossi, M. Carbone, C. Mostocotto, C. Mancone, M. Tripodi, R. Maione, and P. Amati Mitochondrial localization of PARP-1 requires interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity J. Biol. Chem. 284 2009 31616 31624
68. F. Dantzer, H.P. Nasheuer, J.L. Vonesch, G. de Murcia, and J. Ménissier-de Murcia Functional association of poly[ADP-ribose] polymerase with DNA polymerase alpha-primase complex: a link between DNA strand break detection and DNA replication Nucleic Acids Res. 26 1998 1891 1898