Mitochondrial DNA replication proceeds via a 'bootlace' mechanism involving the incorporation of processed transcripts

Nucleic Acids Research

Volumn 41, Issue 11, 2013, Pages 5837-5850

  Reyes, Aurelio ^a   Kazak, Lawrence ^a   Wood, Stuart R ^a   Yasukawa, Takehiro ^a,e   Jacobs, Howard T ^b,c   Holt, Ian J ^d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b TAMPERE UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; RNA PRECURSOR;

ARTICLE; CONTROLLED STUDY; DNA CROSS LINKING; DNA RNA HYBRIDIZATION; DNA STRAND; DNA SYNTHESIS; EMBRYO; HUMAN; HUMAN CELL; LIVER MITOCHONDRION; MITOCHONDRIAL DNA REPLICATION; NONHUMAN; PRIORITY JOURNAL; RAT; RNA SYNTHESIS;

ANIMALS; CROSS-LINKING REAGENTS; DEOXYADENINE NUCLEOTIDES; DEOXYRIBONUCLEOTIDES; DNA REPLICATION; DNA, MITOCHONDRIAL; FICUSIN; HUMANS; MICE; MICE, INBRED BALB C; RNA; RNA PRECURSORS;

MAMMALIA;

EID: 84878835055     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt196     Document Type: Article

References (39)

1. Kornberg, A. and Baker, T.A. (1992) DNA Replication, 2nd edn. W. H. Freeman & Co., New York.
2. Clayton, D.A. (1982) Replication of animal mitochondrial DNA. Cell, 28, 693-705.
3. Kasamatsu, H. and Vinograd, J. (1973) Unidirectionality of replication in mouse mitochondrial DNA. Nat. New Biol., 241, 103-105.
4. Crews, S., Ojala, D., Posakony, J., Nishiguchi, J. and Attardi, G. (1979) Nucleotide sequence of a region of human mitochondrial DNA containing the precisely identified origin of replication. Nature, 277, 192-198.
5. Tapper, D.P. and Clayton, D.A. (1981) Mechanism of replication of human mitochondrial DNA. Localization of the 50 ends of nascent daughter strands. J. Biol. Chem., 256, 5109-5115.
6. Pohjoismaki, J.L., Holmes, J.B., Wood, S.R., Yang, M.Y., Yasukawa, T., Reyes, A., Bailey, L.J., Cluett, T.J., Goffart, S., Willcox, S. et al. (2010) Mammalian mitochondrial DNA replication intermediates are essentially duplex but contain extensive tracts of RNA/DNA hybrid. J. Mol. Biol., 397, 1144-1155.
7. Yang, M.Y., Bowmaker, M., Reyes, A., Vergani, L., Angeli, P., Gringeri, E., Jacobs, H.T. and Holt, I.J. (2002) Biased incorporation of ribonucleotides on the mitochondrial L-strand accounts for apparent strand-asymmetric DNA replication. Cell, 111, 495-505.
8. Yasukawa, T., Reyes, A., Cluett, T.J., Yang, M.Y., Bowmaker, M., Jacobs, H.T. and Holt, I.J. (2006) Replication of vertebrate mitochondrial DNA entails transient ribonucleotide incorporation throughout the lagging strand. EMBO J., 25, 5358-5371.
9. Kolesar, J.E., Wang, C.Y., Taguchi, Y.V., Chou, S.H. and Kaufman, B.A. (2013) Two-dimensional intact mitochondrial DNA agarose electrophoresis reveals the structural complexity of the mammalian mitochondrial genome. Nucleic Acids Res., 41, e58.
10. Reyes, A., Yang, M.Y., Bowmaker, M. and Holt, I.J. (2005) Bidirectional replication initiates at sites throughout the mitochondrial genome of birds. J. Biol. Chem., 280, 3242-3250.
11. Yasukawa, T., Yang, M.Y., Jacobs, H.T. and Holt, I.J. (2005) A bidirectional origin of replication maps to the major noncoding region of human mitochondrial DNA. Mol. Cell, 18, 651-662.
12. Reyes, A., Yasukawa, T., Cluett, T.J. and Holt, I.J. (2009) Analysis of mitochondrial DNA by two-dimensional agarose gel electrophoresis. Methods Mol. Biol., 554, 15-35.
13. Enriquez, J.A., Ramos, J., Perez-Martos, A., Lopez-Perez, M.J. and Montoya, J. (1994) Highly efficient DNA synthesis in isolated mitochondria from rat liver. Nucleic Acids Res., 22, 1861-1865.
14. Friedman, K.L. and Brewer, B.J. (1995) Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol., 262, 613-627.
15. Gadaleta, G., Pepe, G., De Candia, G., Quagliariello, C., Sbisa, E. and Saccone, C. (1989) The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J. Mol. Evol., 28, 497-516.
16. Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H., Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F. et al. (1981) Sequence and organization of the human mitochondrial genome. Nature, 290, 457-465.
17. Bayona-Bafaluy, M.P., Acin-Perez, R., Mullikin, J.C., Park, J.S., Moreno-Loshuertos, R., Hu, P., Perez-Martos, A., Fernandez-Silva, P., Bai, Y. and Enriquez, J.A. (2003) Revisiting the mouse mitochondrial DNA sequence. Nucleic Acids Res., 31, 5349-5355.
18. He, J., Cooper, H.M., Reyes, A., Di Re, M., Sembongi, H., Litwin, T.R., Gao, J., Neuman, K.C., Fearnley, I.M., Spinazzola, A. et al. (2012) Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucleic Acids Res., 40, 6109-6121.
19. Shen, C.K., Hsieh, T.S., Wang, J.C. and Hearst, J.E. (1977) Photochemical cross-linking of DNA-RNA helices by psoralen derivatives. J. Mol. Biol., 116, 661-679.
20. Arjumand, S., Arif, Z., Ali, A. and Ali, R. (1995) Native DNA fragments photocrosslinked to psoralen binds to anti-B and anti-Z DNA antibodies. Immunol. Lett., 48, 215-219.
21. Hasan, R., Ali, A. and Ali, R. (1991) Antibodies against DNApsoralen crosslink recognize unique conformation. Biochim. Biophys. Acta, 1073, 509-513.
22. Kalejta, R.F., Lin, H.B., Dijkwel, P.A. and Hamlin, J.L. (1996) Characterizing replication intermediates in the amplified CHO dihydrofolate reductase domain by two novel gel electrophoretic techniques. Mol. Cell. Biol., 16, 4923-4931.
23. Holt, I.J., Lorimer, H.E. and Jacobs, H.T. (2000) Coupled leadingand lagging-strand synthesis of mammalian mitochondrial DNA. Cell, 100, 515-524.
24. Clayton, D.A. (1984) Transcription of the mammalian mitochondrial genome. Annu. Rev. Biochem., 53, 573-594.
25. Bhat, K.S., Bhat, N.K., Kulkarni, G.R., Iyengar, A. and Avadhani, N.G. (1985) Expression of the cytochrome b-URF6-URF5 region of the mouse mitochondrial genome. Biochemistry, 24, 5818-5825.
26. Montoya, J., Gaines, G.L. and Attardi, G. (1983) The pattern of transcription of the human mitochondrial rRNA genes reveals two overlapping transcription units. Cell, 34, 151-159.
27. Attardi, G. (1985) Animal mitochondrial DNA: an extreme example of genetic economy. Int. Rev. Cytol., 93, 93-145.
28. Frick, D.N. and Richardson, C.C. (2001) DNA primases. Annu. Rev. Biochem., 70, 39-80.
29. Bowmaker, M., Yang, M.Y., Yasukawa, T., Reyes, A., Jacobs, H.T., Huberman, J.A. and Holt, I.J. (2003) Mammalian mitochondrial DNA replicates bidirectionally from an initiation zone. J. Biol. Chem., 278, 50961-50969.
30. Pomerantz, R.T. and O'Donnell, M. (2010) What happens when replication and transcription complexes collide? Cell Cycle, 9, 2537-2543.
31. Bentin, T., Cherny, D., Larsen, H.J. and Nielsen, P.E. (2005) Transcription arrest caused by long nascent RNA chains. Biochim. Biophys. Acta, 1727, 97-105.
32. 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.
33. Matsushima, Y., Garesse, R. and Kaguni, L.S. (2004) Drosophila mitochondrial transcription factor B2 regulates mitochondrial DNA copy number and transcription in schneider cells. J. Biol. Chem., 279, 26900-26905.
34. Hyvarinen, A.K., Pohjoismaki, J.L., Reyes, A., Wanrooij, S., Yasukawa, T., Karhunen, P.J., Spelbrink, J.N., Holt, I.J. and Jacobs, H.T. (2007) The mitochondrial transcription termination factor mTERF modulates replication pausing in human mitochondrial DNA. Nucleic Acids Res., 35, 6458-6474.
35. 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.
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. Wanrooij, S., Goffart, S., Pohjoismaki, J.L., Yasukawa, T. and Spelbrink, J.N. (2007) Expression of catalytic mutants of the mtDNA helicase Twinkle and polymerase POLG causes distinct replication stalling phenotypes. Nucleic Acids Res., 35, 3238-3251.
38. Bourdon, A., Minai, L., Serre, V., Jais, J.P., Sarzi, E., Aubert, S., Chretien, D., de Lonlay, P., Paquis-Flucklinger, V., Arakawa, H. et al. (2007) Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat. Genet., 39, 776-780.
39. Saada, A., Shaag, A., Mandel, H., Nevo, Y., Eriksson, S. and Elpeleg, O. (2001) Mutant mitochondrial thymidine kinase in mitochondrial DNA depletion myopathy. Nat. Genet., 29, 342-344.