Yeast mitochondrial DNA polymerase is a highly processive single-subunit enzyme

Mitochondrion

Volumn 11, Issue 1, 2011, Pages 119-126

  Viikov, Katrin ^a   Väljamäe, Priit ^a   Sedman, Juhan ^a  

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

DNA polymerase ; Mip1; Processivity; Strand displacement DNA synthesis; Yeast mtDNA replication

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE; MITOCHONDRIAL DNA; PROTEIN MIP1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVITY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN POLYMERIZATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE;

CATALYTIC DOMAIN; DNA POLYMERASE I; DNA REPLICATION; DNA, MITOCHONDRIAL; DNA-DIRECTED DNA POLYMERASE; MITOCHONDRIA; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 78650008112     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2010.08.007     Document Type: Article

References (55)

1. Andraos N., Tabor S., Richardson C.C. The highly processive DNA polymerase of bacteriophage T5. Role of the unique N and C termini. J. Biol. Chem. 2004, 279:50609-50618.
2. Bambara R.A., Fay P.J., Mallaber L.M. Methods of analyzing processivity. Meth. Enzymol. 1995, 262:270-280.
3. Baruffini E., Lodi T., Dallabona C., Foury F. A single nucleotide polymorphism in the DNA polymerase gamma gene of Saccharomyces cerevisiae laboratory strains is responsible for increased mitochondrial DNA mutability. Genetics 2007, 177(2):1227-1231.
4. Bernad A., Blanco L., Lazaro J.M., Martin G., Salas M. A conserved 3″-5″ exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell 1989, 59:219-228.
5. Biswas T.K., Sengupta P., Green R., Hakim P., Biswas B., Sen S. Properties of mitochondrial DNA polymerase in mitochondrial DNA synthesis in yeast. Acta Biochim. Pol. 1995, 42:317-324.
6. Blanco L., Bernad A., Salas M. MIP1 DNA polymerase of S. cerevisiae: structural similarity with the E. coli DNA polymerase I-type enzymes. Nucleic Acids Res. 1991, 19:955.
7. Carrodeguas J.A., Theis K., Bogenhagen D.F., Kisker C. Crystal structure and deletion analysis show that the accessory subunit of mammalian DNA polymerase gamma, Pol gamma B, functions as a homodimer. Mol. Cell 2001, 7:43-54.
8. Das S.K., Fujimura R.K. Processiveness of DNA polymerases. A comparative study using a simple procedure. J. Biol. Chem. 1979, 254:1227-1232.
9. Daum G., Bohni P.C., Schatz G. Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem. 1982, 257:13028-13033.
10. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
11. Eriksson S., Xu B., Clayton D.A. Efficient incorporation of anti-HIV deoxynucleotides by recombinant yeast mitochondrial DNA polymerase. J. Biol. Chem. 1995, 270:18929-18934.
12. Falkenberg M., Lehman I.R., Elias P. Leading and lagging strand DNA synthesis in vitro by a reconstituted herpes simplex virus type 1 replisome. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:3896-3900.
13. Farge G., Pham X.H., Holmlund T., Khorostov I., Falkenberg M. The accessory subunit B of DNA polymerase gamma is required for mitochondrial replisome function. Nucleic Acids Res. 2007, 35:902-911.
14. Foury F., Kolodynski J. Pif mutation blocks recombination between mitochondrial rho+ and rho- genomes having tandemly arrayed repeat units in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 1983, 80:5345-5349.
15. Foury F., Lahaye A. Cloning and sequencing of the PIF gene involved in repair and recombination of yeast mitochondrial DNA. EMBO J. 1987, 6:1441-1449.
16. Fujimura R.K., Roop B.C. Characterization of DNA polymerase induced by bacteriophage T5 with DNA containing single strand breaks. J. Biol. Chem. 1976, 251:2168-2174.
17. Genga A., Bianchi L., Foury F. A nuclear mutant of Saccharomyces cerevisiae deficient in mitochondrial DNA replication and polymerase activity. J. Biol. Chem. 1986, 261:9328-9332.
18. Graves S.W., Johnson A.A., Johnson K.A. Expression, purification, and initial kinetic characterization of the large subunit of the human mitochondrial DNA polymerase. Biochemistry 1998, 37:6050-6058.
19. Gray H., Wong T.W. Purification and identification of subunit structure of the human mitochondrial DNA polymerase. J. Biol. Chem. 1992, 267:5835-5841.
20. Graziewicz M.A., Longley M.J., Bienstock R.J., Zeviani M., Copeland W.C. Structure-function defects of human mitochondrial DNA polymerase in autosomal dominant progressive external ophthalmoplegia. Nat. Struct. Mol. Biol. 2004, 11:770-776.
21. Graziewicz M.A., Longley M.J., Copeland W.C. DNA polymerase gamma in mitochondrial DNA replication and repair. Chem. Rev. 2006, 106:383-405.
22. He Z.G., Rezende L.F., Willcox S., Griffith J.D., Richardson C.C. The carboxyl-terminal domain of bacteriophage T7 single-stranded DNA-binding protein modulates DNA binding and interaction with T7 DNA polymerase. J. Biol. Chem. 2003, 278:29538-29545.
23. Huber H.E., Tabor S., Richardson C.C. Escherichia coli thioredoxin stabilizes complexes of bacteriophage T7 DNA polymerase and primed templates. J. Biol. Chem. 1987, 262:16224-16232.
24. Insdorf N.F., Bogenhagen D.F. DNA polymerase gamma from Xenopus laevis. I. The identification of a high molecular weight catalytic subunit by a novel DNA polymerase photolabeling procedure. J. Biol. Chem. 1989, 264:21491-21497.
25. Ito J., Braithwaite D.K. Yeast mitochondrial DNA polymerase is related to the family A DNA polymerases. Nucleic Acids Res. 1990, 18:6716.
26. Johnson A.A., Tsai Y., Graves S.W., Johnson K.A. Human mitochondrial DNA polymerase holoenzyme: reconstitution and characterization. Biochemistry 2000, 39:1702-1708.
27. Jones E.W. Tackling the protease problem in Saccharomyces cerevisiae. Meth. Enzymol. 1991, 194:428-453.
28. Kaguni L.S. DNA polymerase gamma, the mitochondrial replicase. Annu. Rev. Biochem. 2004, 73:293-320.
29. Kasiviswanathan R., Longley M.J., Chan S.S., Copeland W.C. Disease mutations in the human mitochondrial DNA polymerase thumb subdomain impart severe defects in mitochondrial DNA replication. J. Biol. Chem. 2009, 284:19501-19510.
30. Kelman Z., Hurwitz J., O'Donnell M. Processivity of DNA polymerases: two mechanisms, one goal. Structure 1998, 6:121-125.
31. Korhonen J.A., Pham X.H., Pellegrini M., Falkenberg M. Reconstitution of a minimal mtDNA replisome in vitro. EMBO J. 2004, 23:2423-2429.
32. Kuusk S., Sedman T., Jõers P., Sedman J. Hmi1p from Saccharomyces cerevisiae mitochondria is a structure-specific DNA helicase. J. Biol. Chem. 2005, 280:24322-24329.
33. Lahaye A., Stahl H., Thines-Sempoux D., Foury F. PIF1: a DNA helicase in yeast mitochondria. EMBO J. 1991, 10:997-1007.
34. Lecrenier N., Van Der Bruggen P., Foury F. Mitochondrial DNA polymerases from yeast to man: a new family of DNA polymerases. Gene 1997, 185:147-152.
35. Lee J.B., Hite R.K., Hamdan S.M., Xie X.S., Richardson C.C., van Oijen A.M. DNA primase acts as a molecular brake in DNA replication. Nature 2006, 439(7076):621-624.
36. Lee Y.S., Kennedy W.D., Yin Y.W. Structural insight into processive human mitochondrial DNA synthesis and disease-related polymerase mutations. Cell 2009, 139:312-324.
37. Lestienne P. Evidence for a direct role of the DNA polymerase gamma in the replication of the human mitochondrial DNA in vitro. Biochem. Biophys. Res. Commun. 1987, 146:1146-1153.
38. Lim S.E., Longley M.J., Copeland W.C. The mitochondrial p55 accessory subunit of human DNA polymerase gamma enhances DNA binding, promotes processive DNA synthesis, and confers N-ethylmaleimide resistance. J. Biol. Chem. 1999, 274:38197-38203.
39. Longley M.J., Ropp P.A., Lim S.E., Copeland W.C. Characterization of the native and recombinant catalytic subunit of human DNA polymerase gamma: identification of residues critical for exonuclease activity and dideoxynucleotide sensitivity. Biochemistry 1998, 37:10529-10539.
40. Longley M.J., Graziewicz M.A., Bienstock R.J., Copeland W.C. Consequences of mutations in human DNA polymerase gamma. Gene 2005, 354:125-131.
41. Lucas P., Lasserre J.P., Plissonneau J., Castroviejo M. Absence of accessory subunit in the DNA polymerase gamma purified from yeast mitochondria. Mitochondrion 2004, 4:13-20.
42. Luoma P.T., Luo N., Löscher W.N., Farr C.L., Horvath R., Wanschitz J., Kiechl S., Kaguni L.S., Suomalainen A. Functional defects due to spacer-region mutations of human mitochondrial DNA polymerase in a family with an ataxia-myopathy syndrome. Hum. Mol. Genet. 2005, 14:1907-1920.
43. Maleszka R., Skelly P.J., Clark-Walker G.D. Rolling circle replication of DNA in yeast mitochondria. EMBO J. 1991, 10(12):3923-3929.
44. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
45. Olson M.W., Wang Y., Elder R.H., Kaguni L.S. Subunit structure of mitochondrial DNA polymerase from Drosophila embryos. Physical and immunological studies. J. Biol. Chem. 1995, 270:28932-28937.
46. O'Rourke T.W., Doudican N.A., Mackereth M.D., Doetsch P.W., Shadel G.S. Mitochondrial dysfunction due to oxidative mitochondrial DNA damage is reduced through cooperative actions of diverse proteins. Mol. Cell. Biol. 2002, 22:4086-4093.
47. Rupp S., Summers E., Lo H.J., Madhani H., Fink G. MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene. EMBO J. 1999, 18:1257-1269.
48. Sedman T., Kuusk S., Kivi S., Sedman J. A DNA helicase required for maintenance of the functional mitochondrial genome in Saccharomyces cerevisiae. Mol. Cell. Biol. 2000, 20:1816-1824.
49. Sedman T., Jõers P., Kuusk S., Sedman J. Helicase Hmi1 stimulates the synthesis of concatemeric mitochondrial DNA molecules in yeast Saccharomyces cerevisiae. Curr. Genet. 2005, 47:213-222.
50. Tabor S., Huber H.E., Richardson C.C. Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7. J. Biol. Chem. 1987, 262:16212-16223.
51. Van Goethem G., Dermaut B., Löfgren A., Martin J.J., Van Broeckhoven C. Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat. Genet. 2001, 28:211-212.
52. Vanderstraeten S., Van den Brûle S., Hu J., Foury F. The role of 3″-5″ exonucleolytic proofreading and mismatch repair in yeast mitochondrial DNA error avoidance. J. Biol. Chem. 1998, 273:23690-23697.
53. Wernette C.M., Kaguni L.S. A mitochondrial DNA polymerase from embryos of Drosophila melanogaster. Purification, subunit structure, and partial characterization. J. Biol. Chem. 1986, 261:14764-14770.
54. Yakubovskaya E., Chen Z., Carrodeguas J.A., Kisker C., Bogenhagen D.F. Functional human mitochondrial DNA polymerase gamma forms a heterotrimer. J. Biol. Chem. 2006, 281:374-382.
55. Young M.J., Theriault S.S., Li M., Court D.A. The carboxyl-terminal extension on fungal mitochondrial DNA polymerases: identification of a critical region of the enzyme from Saccharomyces cerevisiae. Yeast 2006, 23:101-116.