The mitochondrial DNA helicase TWINKLE can assemble on a closed circular template and support initiation of DNA synthesis

Nucleic Acids Research

Volumn 39, Issue 21, 2011, Pages 9238-9249

  Jemt, Elisabeth ^a   Farge, Géraldine ^b   Bäckström, Stefan ^a   Holmlund, Teresa ^c   Gustafsson, Claes M ^a,d   Falkenberg, Maria ^a,d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c KAROLINSKA INSTITUTE   (Sweden)

^d MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULAR DNA; HELICASE; MITOCHONDRIAL DNA; PRIMER DNA; SINGLE STRANDED DNA; TWINKLE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA SYNTHESIS; DNA TEMPLATE; ENZYME STRUCTURE; IN VIVO STUDY; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN FUNCTION;

DNA; DNA HELICASES; DNA REPLICATION; DNA, CIRCULAR; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NUCLEOTIDES; TEMPERATURE; TEMPLATES, GENETIC;

EID: 82255185604     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr653     Document Type: Article

References (44)

1. Spelbrink, J.N., Li, F.Y., Tiranti, V., Nikali, K., Yuan, Q.P., Tariq, M., Wanrooij, S., Garrido, N., Comi, G., Morandi, L. et al. (2001) Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet., 28, 223-231. (Pubitemid 32626024)
2. Korhonen, J.A., Gaspari, M. and Falkenberg, M. (2003) TWINKLE Has 5′-< 3′ DNA helicase activity and is specifically stimulated by mitochondrial single-stranded DNA-binding protein. J. Biol. Chem., 278, 48627-48632. (Pubitemid 41079501)
3. Korhonen, J.A., Pham, X.H., Pellegrini, M. and Falkenberg, M. (2004) Reconstitution of a minimal mtDNA replisome in vitro. EMBO J., 23, 2423-2429. (Pubitemid 38954849)
4. Falkenberg, M., Larsson, N.G. and Gustafsson, C.M. (2007) DNA replication and transcription in mammalian mitochondria. Annu. Rev. Biochem., 76, 679-699.
5. Berk, A.J. and Clayton, D.A. (1974) Mechanism of mitochondrial DNA replication in mouse L-cells: asynchronous replication of strands, segregation of circular daughter molecules, aspects of topology and turnover of an initiation sequence. J. Mol. Biol., 86, 801-824.
6. Fuste, J.M., Wanrooij, S., Jemt, E., Granycome, C.E., Cluett, T.J., Shi, Y., Atanassova, N., Holt, I.J., Gustafsson, C.M. and Falkenberg, M. (2010) Mitochondrial RNA polymerase is needed for activation of the origin of light-strand DNA replication. Mol. Cell., 37, 67-78.
7. Wong, T.W. and Clayton, D.A. (1985) In vitro replication of human mitochondrial DNA: accurate initiation at the origin of light-strand synthesis. Cell, 42, 951-958. (Pubitemid 16083725)
8. Clayton, D.A. (1991) Replication and transcription of vertebrate mitochondrial DNA. Annu. Rev. Cell Biol., 7, 453-478.
9. Gillum, A.M. and Clayton, D.A. (1979) Mechanism of mitochondrial DNA replication in mouse L-cells: RNA priming during the initiation of heavy-strand synthesis. J. Mol. Biol., 135, 353-368. (Pubitemid 10173567)
10. Cantatore, P. and Attardi, G. (1980) Mapping of nascent light and heavy strand transcripts on the physical map of HeLa cell mitochondrial DNA. Nucleic Acids Res., 8, 2605-2625. (Pubitemid 10023570)
11. Montoya, J., Christianson, T., Levens, D., Rabinowitz, M. and Attardi, G. (1982) Identification of initiation sites for heavy-strand and light-strand transcription in human mitochondrial DNA. Proc. Natl Acad. Sci. USA, 79, 7195-7199. (Pubitemid 13190454)
12. Pham, X.H., Farge, G., Shi, Y., Gaspari, M., Gustafsson, C.M. and Falkenberg, M. (2006) Conserved sequence box II directs transcription termination and primer formation in mitochondria. J. Biol. Chem., 281, 24647-24652. (Pubitemid 44274237)
13. Wanrooij, P.H., Uhler, J.P., Simonsson, T., Falkenberg, M. and Gustafsson, C.M. (2010) G-quadruplex structures in RNA stimulate mitochondrial transcription termination and primer formation. Proc. Natl Acad. Sci. USA, 107, 16072-16077.
14. Picha, K.M., Ahnert, P. and Patel, S.S. (2000) DNA binding in the central channel of bacteriophage T7 helicase-primase is a multistep process. Nucleotide hydrolysis is not required. Biochemistry, 39, 6401-6409. (Pubitemid 30347145)
15. Egelman, E.H., Yu, X., Wild, R., Hingorani, M.M. and Patel, S.S. (1995) Bacteriophage T7 helicase/primase proteins form rings around single-stranded DNA that suggest a general structure for hexameric helicases. Proc. Natl Acad. Sci. USA, 92, 3869-3873.
16. Morris, P.D. and Raney, K.D. (1999) DNA helicases displace streptavidin from biotin-labeled oligonucleotides. Biochemistry, 38, 5164-5171.
17. Davey, M.J. and O'Donnell, M. (2003) Replicative helicase loaders: ring breakers and ring makers. Curr. Biol., 13, R594-R596. (Pubitemid 36953290)
18. Bujalowski, W. (2003) Expanding the physiological role of the hexameric DnaB helicase. Trends Biochem. Sci., 28, 116-118. (Pubitemid 36293845)
19. Mott, M.L., Erzberger, J.P., Coons, M.M. and Berger, J.M. (2008) Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators. Cell, 135, 623-634.
20. Fanning, E. and Knippers, R. (1992) Structure and function of simian virus 40 large tumor antigen. Annu. Rev. Biochem., 61, 55-85.
21. Ahnert, P., Picha, K.M. and Patel, S.S. (2000) A ring-opening mechanism for DNA binding in the central channel of the T7 helicase-primase protein. EMBO J., 19, 3418-3427. (Pubitemid 30428219)
22. Farge, G., Holmlund, T., Khvorostova, J., Rofougaran, R., Hofer, A. and Falkenberg, M. (2008) The N-terminal domain of TWINKLE contributes to single-stranded DNA binding and DNA helicase activities. Nucleic Acids Res., 36, 393-403. (Pubitemid 351250432)
23. Ziebarth, T.D., Gonzalez-Soltero, R., Makowska-Grzyska, M.M., Nunez-Ramirez, R., Carazo, J.M. and Kaguni, L.S. (2010) Dynamic effects of cofactors and DNA on the oligomeric state of human mitochondrial DNA helicase. J. Biol. Chem., 285, 14639-14647.
24. Patel, S.S. and Picha, K.M. (2000) Structure and function of hexameric helicases. Annu. Rev. Biochem., 69, 651-697.
25. Matson, S.W., Tabor, S. and Richardson, C.C. (1983) The gene 4 protein of bacteriophage T7. Characterization of helicase activity. J. Biol. Chem., 258, 14017-14024. (Pubitemid 14203812)
26. Farge, G., Pham, X.H., Holmlund, T., Khorostov, I. and Falkenberg, M. (2007) The accessory subunit B of DNA polymerase gamma is required for mitochondrial replisome function. Nucleic Acids Res., 35, 902-911. (Pubitemid 46344716)
27. Korhonen, J.A., Pande, V., Holmlund, T., Farge, G., Pham, X.H., Nilsson, L. and Falkenberg, M. (2008) Structure-function defects of the TWINKLE linker region in progressive external ophthalmoplegia. J. Mol. Biol., 377, 691-705.
28. Harrington, C. and Perrino, F.W. (1995) Initiation of RNA-primed DNA synthesis in vitro by DNA polymerase alpha-primase. Nucleic Acids Res., 23, 1003-1009.
29. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York.
30. Matson, S.W. and Richardson, C.C. (1983) DNA-dependent nucleoside 5′-triphosphatase activity of the gene 4 protein of bacteriophage T7. J. Biol. Chem., 258, 14009-14016. (Pubitemid 14203811)
31. Satapathy, A.K., Crampton, D.J., Beauchamp, B.B. and Richardson, C.C. (2009) Promiscuous usage of nucleotides by the DNA helicase of bacteriophage T7: determinants of nucleotide specificity. J. Biol. Chem., 284, 14286-14295.
32. Holmlund, T., Farge, G., Pande, V., Korhonen, J., Nilsson, L. and Falkenberg, M. (2009) Structure-function defects of the twinkle amino-terminal region in progressive external ophthalmoplegia. Biochim. Biophys. Acta, 1792, 132-139.
33. Atanassova, N., Fuste, J.M., Wanrooij, S., Macao, B., Goffart, S., Backstrom, S., Farge, G., Khvorostov, I., Larsson, N.G., Spelbrink, J.N. et al. (2011) Sequence-specific stalling of DNA polymerase gamma and the effects of mutations causing progressive ophthalmoplegia. Hum. Mol. Genet., 20, 1212-1223.
34. Cha, T.A. and Alberts, B.M. (1990) Effects of the bacteriophage T4 gene 41 and gene 32 proteins on RNA primer synthesis: coupling of leading-and lagging-strand DNA synthesis at a replication fork. Biochemistry, 29, 1791-1798. (Pubitemid 20074722)
35. Falkenberg, M., Bushnell, D.A., Elias, P. and Lehman, I.R. (1997) The UL8 subunit of the heterotrimeric herpes simplex virus type 1 helicase-primase is required for the unwinding of single strand DNA-binding protein (ICP8)-coated DNA substrates. J. Biol. Chem., 272, 22766-22770. (Pubitemid 27386095)
36. Wanrooij, S., Fuste, J.M., Farge, G., Shi, Y., Gustafsson, C.M. and Falkenberg, M. (2008) Human mitochondrial RNA polymerase primes lagging-strand DNA synthesis in vitro. Proc. Natl Acad. Sci. USA, 105, 11122-11127.
37. Lee, D.Y. and Clayton, D.A. (1997) RNase mitochondrial RNA processing correctly cleaves a novel R loop at the mitochondrial DNA leading-strand origin of replication. Genes Dev., 11, 582-592. (Pubitemid 27133378)
38. Kang, D., Miyako, K., Kai, Y., Irie, T. and Takeshige, K. (1997) In vivo determination of replication origins of human mitochondrial DNA by ligation-mediated polymerase chain reaction. J. Biol. Chem., 272, 15275-15279. (Pubitemid 27255547)
39. Yu, X., Hingorani, M.M., Patel, S.S. and Egelman, E.H. (1996) DNA is bound within the central hole to one or two of the six subunits of the T7 DNA helicase. Nat. Struct. Biol., 3, 740-743. (Pubitemid 26303397)
40. Fernandez-Silva, P., Polosa, P.L., Roberti, M., Di Ponzio, B., Gadaleta, M.N., Montoya, J. and Cantatore, P. (2001) Sea urchin mtDBP is a two-faced transcription termination factor with a biased polarity depending on the RNA polymerase. Nucleic Acids Res., 29, 4736-4743. (Pubitemid 33095035)
41. Polosa, P.L., Deceglie, S., Roberti, M., Gadaleta, M.N. and Cantatore, P. (2005) Contrahelicase activity of the mitochondrial transcription termination factor mtDBP. Nucleic Acids Res., 33, 3812-3820. (Pubitemid 41418550)
42. Doda, J.N., Wright, C.T. and Clayton, D.A. (1981) Elongation of displacement-loop strands in human and mouse mitochondrial DNA is arrested near specific template sequences. Proc. Natl Acad. Sci. USA, 78, 6116-6120. (Pubitemid 12247476)
43. Madsen, C.S., Ghivizzani, S.C. and Hauswirth, W.W. (1993) Protein binding to a single termination-associated sequence in the mitochondrial DNA D-loop region. Mol. Cell. Biol., 13, 2162-2171. (Pubitemid 23097695)
44. Yang, C., Curth, U., Urbanke, C. and Kang, C. (1997) Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4A resolution. Nat. Struct. Biol., 4, 153-157. (Pubitemid 27066391)