Association of the yeast DNA helicase Pif1p with mitochondrial membranes and mitochondrial DNA

European Journal of Cell Biology

Volumn 89, Issue 10, 2010, Pages 742-747

  Cheng, Xin ^a   Ivessa, Andreas S ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

DNA helicase; DNA replication; Mitochondrial DNA; Mitochondrial protein complex; Pif1p

Indexed keywords

HELICASE; MIP1P PROTEIN; MITOCHONDRIAL DNA; PIF1P PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE PERMEABILITY; CYTOPLASM; DNA REPLICATION; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

DNA HELICASES; DNA, MITOCHONDRIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; MITOCHONDRIAL MEMBRANES; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77955923062     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2010.06.008     Document Type: Article

References (56)

1. Amutha B., Gordon D.M., Gu Y., Pain D. A novel role of Mgm1p, a dynamin-related GTPase, in ATP synthase assembly and cristae formation/maintenance. Biochem. J. 2004, 381:19-23.
2. Arnold I., Bauer M.F., Brunner M., Neupert W., Stuart R.A. Yeast mitochondrial F1F0-ATPase: the novel subunit e is identical to Tim11. FEBS Lett. 1997, 411:195-200.
3. Berger K.H., Yaffe M.P. Mitochondrial DNA inheritance in Saccharomyces cerevisiae. Trends Microbiol. 2000, 8:508-513.
4. Bochman M.L., Sabouri N., Zakian V.A. Unwinding the functions of the Pif1 family helicases. DNA Repair (Amst) 2010, 9:237-249.
5. Boule J.B., Zakian V.A. The yeast Pif1p DNA helicase preferentially unwinds RNA DNA substrates. Nucleic Acids Res. 2007, 35:5809-5818.
6. Chen X.J., Butow R.A. The organization and inheritance of the mitochondrial genome. Nat. Rev. Genet. 2005, 6:815-825.
7. Chen X.J., Wang X., Kaufman B.A., Butow R.A. Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 2005, 307:714-717.
8. Chen X.J., Wang X., Butow R.A. Yeast aconitase binds and provides metabolically coupled protection to mitochondrial DNA. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:13738-13743.
9. Cheng X., Dunaway S., Ivessa A.S. The role of Pif1p, a DNA helicase in Saccharomyces cerevisiae, in maintaining mitochondrial DNA. Mitochondrion 2007, 7:211-222.
10. Cheng X., Qin Y., Ivessa A.S. Loss of mitochondrial DNA under genotoxic stress conditions in the absence of the yeast DNA helicase Pif1p occurs independently of the DNA helicase Rrm3p. Mol. Genet. Genomics 2009, 281:635-645.
11. 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.
12. Dimmer K.S., Jakobs S., Vogel F., Altmann K., Westermann B. Mdm31 and Mdm32 are inner membrane proteins required for maintenance of mitochondrial shape and stability of mitochondrial DNA nucleoids in yeast. J. Cell Biol. 2005, 168:103-115.
13. Doudican N.A., Song B., Shadel G.S., Doetsch P.W. Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol. Cell. Biol. 2005, 25:5196-5204.
14. Ferguson L.R., von Borstel R.C. Induction of the cytoplasmic 'petite' mutation by chemical and physical agents in Saccharomyces cerevisiae. Mutat. Res. 1992, 265:103-148.
15. Foury F., Dyck E.V. A PIF-dependent recombinogenic signal in the mitochondrial DNA of yeast. EMBO J. 1985, 4:3525-3530.
16. 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.
17. 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.
18. George T., Wen Q., Griffiths R., Ganesh A., Meuth M., Sanders C.M. Human Pif1 helicase unwinds synthetic DNA structures resembling stalled DNA replication forks. Nucleic Acids Res. 2009, 37:6491-6502.
19. Gordon D.M., Wang J., Amutha B., Pain D. Self-association and precursor protein binding of Saccharomyces cerevisiae Tom40p, the core component of the protein translocation channel of the mitochondrial outer membrane. Biochem. J. 2001, 356:207-215.
20. Hanekamp T., Thorsness M.K., Rebbapragada I., Fisher E.M., Seebart C., Darland M.R., Coxbill J.A., Updike D.L., Thorsness P.E. Maintenance of mitochondrial morphology is linked to maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Genetics 2002, 162:1147-1156.
21. Hobbs A.E., Srinivasan M., McCaffery J.M., Jensen R.E. Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J. Cell Biol. 2001, 152:401-410.
22. Ivessa A.S., Zhou J.-Q., Zakian V.A. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 2000, 100:479-489.
23. Kaufman B.A., Newman S.M., Hallberg R.L., Slaughter C.A., Perlman P.S., Butow R.A. In organello formaldehyde crosslinking of proteins to mtDNA: identification of bifunctional proteins. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:7772-7777.
24. Kucej M., Kucejova B., Subramanian R., Chen X.J., Butow R.A. Mitochondrial nucleoids undergo remodeling in response to metabolic cues. J. Cell Sci. 2008, 121:1861-1868.
25. Lahaye A., Stahl H., Thines-Sempoux D., Foury F. PIF1: a DNA helicase in yeast mitochondria. EMBO J. 1991, 10:997-1007.
26. Lahaye A., Leterme S., Foury F. PIF1 DNA helicase from Saccharomyces cerevisiae. Biochemical characterization of the enzyme. J. Biol. Chem. 1993, 268:26155-26161.
27. Lemon K.P., Grossman A.D. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 1998, 282:1516-1519.
28. Lemon K.P., Grossman A.D. Movement of replicating DNA through a stationary replisome. Mol. Cell 2000, 6:1321-1330.
29. Ling F., Shibata T. Recombination-dependent mtDNA partitioning: in vivo role of Mhr1p to promote pairing of homologous DNA. EMBO J. 2002, 21:4730-4740.
30. Ling F., Shibata T. Mhr1p-dependent concatemeric mitochondrial DNA formation for generating yeast mitochondrial homoplasmic cells. Mol. Biol. Cell 2004, 15:310-322.
31. Liu Z., Butow R.A. Mitochondrial retrograde signaling. Annu. Rev. Genet. 2006, 40:159-185.
32. Liu B., Wang J., Yaffe N., Lindsay M.E., Zhao Z., Zick A., Shlomai J., Englund P.T. Trypanosomes have six mitochondrial DNA helicases with one controlling kinetoplast maxicircle replication. Mol. Cell 2009, 35:490-501.
33. Liu B., Yildirir G., Wang J., Tolun G., Griffith J.D., Englund P.T. TbPIF1, a Trypanosoma brucei mitochondrial DNA helicase, is essential for kinetoplast minicircle replication. J. Biol. Chem. 2010, 285:7056-7066.
34. Longtine M., McKenzie A.I., Demarini D., Shah N., Wach A., Brachat A., Philippsen P., Pringle J. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998, 14:953-961.
35. Malka F., Lombes A., Rojo M. Organization, dynamics and transmission of mitochondrial DNA: focus on vertebrate nucleoids. Biochim. Biophys. Acta 2006, 1763:463-472.
36. Meeusen S., Nunnari J. Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome. J. Cell Biol. 2003, 163:503-510.
37. Meeusen S., Tieu Q., Wong E., Weiss E., Schieltz D., Yates J.R., Nunnari J. Mgm101p is a novel component of the mitochondrial nucleoid that binds DNA and is required for the repair of oxidatively damaged mitochondrial DNA. J. Cell Biol. 1999, 145:291-304.
38. Murakami H., Pain D., Blobel G. 70-kDa heat shock-related protein is one of at least two distinct cytosolic factors stimulating protein import into mitochondria. J. Cell Biol. 1988, 107:2051-2057.
39. Newman S.M., Zelenaya-Troitskaya O., Perlman P.S., Butow R.A. Analysis of mitochondrial DNA nucleoids in wild-type and a mutant strain of Saccharomyces cerevisiae that lacks the mitochondrial HMG box protein Abf2p. Nucleic Acids Res. 1996, 24:386-393.
40. Nijtmans L.G., Henderson N.S., Holt I.J. Blue Native electrophoresis to study mitochondrial and other protein complexes. Methods 2002, 26:327-334.
41. 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.
42. O'Rourke T.W., Doudican N.A., Zhang H., Eaton J.S., Doetsch P.W., Shadel G.S. Differential involvement of the related DNA helicases Pif1p and Rrm3p in mtDNA point mutagenesis and stability. Gene 2005, 354:86-92.
43. Okamoto K., Perlman P.S., Butow R.A. The sorting of mitochondrial DNA and mitochondrial proteins in zygotes: preferential transmission of mitochondrial DNA to the medial bud. J. Cell Biol. 1998, 142:613-623.
44. Piazza A., Boule J.B., Lopes J., Mingo K., Largy E., Teulade-Fichou M.P., Nicolas A. Genetic instability triggered by G-quadruplex interacting Phen-DC compounds in Saccharomyces cerevisiae. Nucleic Acids Res. 2010, (E-pub ahead of print). 10.1093/nar/gkq136.
45. Rapaport D. Biogenesis of the mitochondrial TOM complex. Trends Biochem. Sci. 2002, 27:191-197.
46. Ribeyre C., Lopes J., Boule J.B., Piazza A., Guedin A., Zakian V.A., Mergny J.L., Nicolas A. The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet. 2009, 5:e1000475.
47. Rose M.D., Winston F., Hieter P. Methods in yeast genetics: a laboratory course manual 1990, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Schiestl R.H., Gietz R.D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 1989, 16:339-346.
49. Schulz V.P., Zakian V.A. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 1994, 76:145-155.
50. Sikorski R.S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 1989, 122:19-27.
51. Southern E.M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 1975, 98:503-517.
52. Spelbrink J.N. Functional organization of mammalian mitochondrial DNA in nucleoids: history, recent developments, and future challenges. IUBMB Life 2010, 62:19-32.
53. Taylor S.D., Zhang H., Eaton J.S., Rodeheffer M.S., Lebedeva M.A., O'Rourke T.W., Siede W., Shadel G.S. The conserved Mec1/Rad53 nuclear checkpoint pathway regulates mitochondrial DNA copy number in Saccharomyces cerevisiae. Mol. Biol. Cell 2005, 16:3010-3018.
54. Van Dyck E., Foury F., Stillman B., Brill S.J. A single-stranded DNA binding protein required for mitochondrial DNA replication in S. cerevisiae is homologous to E. coli SSB. EMBO J. 1992, 11:3421-3430.
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.
56. Zhou J.-Q., Monson E.M., Teng S.-C., Schulz V.P., Zakian V.A. The Pif1p helicase, a catalytic inhibitor of telomerase lengthening of yeast telomeres. Science 2000, 289:771-774.