In Vivo Occupancy of Mitochondrial Single-Stranded DNA Binding Protein Supports the Strand Displacement Mode of DNA Replication

PLoS Genetics

Volumn 10, Issue 12, 2014, Pages

  Miralles Fusté, Javier ^a   Shi, Yonghong ^a   Wanrooij, Sjoerd ^b   Zhu, Xuefeng ^a   Jemt, Elisabeth ^a   Persson, Örjan ^a   Sabouri, Nasim ^b   Gustafsson, Claes M ^a   Falkenberg, Maria ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

HEAVY STRAND DNA; LIGHT STRAND DNA; MITOCHONDRIAL DNA; MITOCHONDRIAL SINGLE STRANDED DNA BINDING PROTEIN; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG; C10ORF2 PROTEIN, HUMAN; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED RNA POLYMERASE; DNA HELICASE; MITOCHONDRIAL PROTEIN; POLG PROTEIN, HUMAN; POLGBETA PROTEIN, HUMAN; POLRMT PROTEIN, HUMAN; SINGLE STRANDED DNA; SSBP1 PROTEIN, HUMAN; TFAM PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; DNA REPLICATION; DNA STRUCTURE; DNA SYNTHESIS; HELA CELL LINE; MITOCHONDRION; NEXT GENERATION SEQUENCING; GENETIC RECOMBINATION; GENETICS; HUMAN; METABOLISM;

MAMMALIA;

DNA HELICASES; DNA REPLICATION; DNA, MITOCHONDRIAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; DNA-DIRECTED RNA POLYMERASES; HELA CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; RECOMBINATION, GENETIC; TRANSCRIPTION FACTORS;

EID: 84919608411     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004832     Document Type: Article

References (41)

1. Park CB, Larsson NG, (2011) Mitochondrial DNA mutations in disease and aging. J Cell Biol 193: 809–818.
2. Kukat C, Larsson NG, (2013) mtDNA makes a U-turn for the mitochondrial nucleoid. Trends Cell Biol 23: 457–463.
3. Spelbrink JN, Li FY, Tiranti V, Nikali K, Yuan QP, 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.
4. Bogenhagen DF, (2012) Mitochondrial DNA nucleoid structure. Biochim Biophys Acta 1819: 914–920.
5. Xu B, Clayton DA, (1995) A persistent RNA-DNA hybrid is formed during transcription at a phylogenetically conserved mitochondrial DNA sequence. Mol Cell Biol 15: 580–589.
6. Fuste JM, Wanrooij S, Jemt E, Granycome CE, Cluett TJ, et al. (2010) Mitochondrial RNA polymerase is needed for activation of the origin of light-strand DNA replication. Mol Cell 37: 67–78.
7. Cerritelli SM, Frolova EG, Feng C, Grinberg A, Love PE, et al. (2003) Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Molecular cell 11: 807–815.
8. Tiranti V, Rocchi M, DiDonato S, Zeviani M, (1993) Cloning of human and rat cDNAs encoding the mitochondrial single-stranded DNA-binding protein (SSB). Gene 126: 219–225.
9. Yang C, Curth U, Urbanke C, Kang C, (1997) Crystal structure of human mitochondrial single-stranded DNA binding protein at 2.4 A resolution. Nat Struct Biol 4: 153–157.
10. Genuario R, Wong TW, (1993) Stimulation of DNA polymerase gamma by a mitochondrial single-strand DNA binding protein. Cell Mol Biol Res 39: 625–634.
11. Thommes P, Farr CL, Marton RF, Kaguni LS, Cotterill S, (1995) Mitochondrial single-stranded DNA-binding protein from Drosophila embryos. Physical and biochemical characterization. J Biol Chem 270: 21137–21143.
12. Farr CL, Wang Y, Kaguni LS, (1999) Functional interactions of mitochondrial DNA polymerase and single-stranded DNA-binding protein. Template-primer DNA binding and initiation and elongation of DNA strand synthesis. J Biol Chem 274: 14779–14785.
13. Korhonen JA, Gaspari M, 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.
14. Robberson DL, Clayton DA, (1972) Replication of mitochondrial DNA in mouse L cells and their thymidine kinase - derivatives: displacement replication on a covalently-closed circular template. Proc Natl Acad Sci U S A 69: 3810–3814.
15. Bogenhagen DF, Clayton DA, (2003) The mitochondrial DNA replication bubble has not burst. Trends Biochem Sci 28: 357–360.
16. Wanrooij S, Fuste JM, Farge G, Shi Y, Gustafsson CM, et al. (2008) Human mitochondrial RNA polymerase primes lagging-strand DNA synthesis in vitro. Proc Natl Acad Sci U S A 105: 11122–11127.
17. Wanrooij S, Miralles Fuste J, Stewart JB, Wanrooij PH, Samuelsson T, et al. (2012) In vivo mutagenesis reveals that OriL is essential for mitochondrial DNA replication. EMBO Rep 13: 1130–1137.
18. Faith JJ, Pollock DD, (2003) Likelihood analysis of asymmetrical mutation bias gradients in vertebrate mitochondrial genomes. Genetics 165: 735–745.
19. Holt IJ, Lorimer HE, Jacobs HT, (2000) Coupled leading- and lagging-strand synthesis of mammalian mitochondrial DNA. Cell 100: 515–524.
20. Yasukawa T, Yang MY, Jacobs HT, Holt IJ, (2005) A bidirectional origin of replication maps to the major noncoding region of human mitochondrial DNA. Mol Cell 18: 651–662.
21. Reyes A, Kazak L, Wood SR, Yasukawa T, Jacobs HT, et al. (2013) Mitochondrial DNA replication proceeds via a 'bootlace' mechanism involving the incorporation of processed transcripts. Nucleic Acids Res 41: 5837–5850.
22. Holt IJ, Reyes A (2012) Human mitochondrial DNA replication. Cold Spring Harb Perspect Biol 4: pii: a012971
23. Takamatsu C, Umeda S, Ohsato T, Ohno T, Abe Y, et al. (2002) Regulation of mitochondrial D-loops by transcription factor A and single-stranded DNA-binding protein. EMBO Rep 3: 451–456.
24. Curth U, Urbanke C, Greipel J, Gerberding H, Tiranti V, et al. (1994) Single-stranded-DNA-binding proteins from human mitochondria and Escherichia coli have analogous physicochemical properties. Eur J Biochem 221: 435–443.
25. Korhonen JA, Pham XH, Pellegrini M, Falkenberg M, (2004) Reconstitution of a minimal mtDNA replisome in vitro. EMBO J 23: 2423–2429.
26. Wang YE, Marinov GK, Wold BJ, Chan DC, (2013) Genome-wide analysis reveals coating of the mitochondrial genome by TFAM. PloS one 8: e74513.
27. Ruhanen H, Borrie S, Szabadkai G, Tyynismaa H, Jones AW, et al. (2010) Mitochondrial single-stranded DNA binding protein is required for maintenance of mitochondrial DNA and 7S DNA but is not required for mitochondrial nucleoid organisation. Biochim Biophys Acta 1803: 931–939.
28. Asakawa S, Kumazawa Y, Araki T, Himeno H, Miura K, et al. (1991) Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. J Mol Evol 32: 511–520.
29. Yang MY, Bowmaker M, Reyes A, Vergani L, Angeli P, et al. (2002) Biased incorporation of ribonucleotides on the mitochondrial L-strand accounts for apparent strand-asymmetric DNA replication. Cell 111: 495–505.
30. Brown TA, Cecconi C, Tkachuk AN, Bustamante C, Clayton DA, (2005) Replication of mitochondrial DNA occurs by strand displacement with alternative light-strand origins, not via a strand-coupled mechanism. Genes Dev 19: 2466–2476.
31. Reyes A, Yasukawa T, Holt IJ, (2007) Analysis of replicating mitochondrial DNA by two-dimensional agarose gel electrophoresis. Methods Mol Biol 372: 219–232.
32. Robberson DL, Kasamatsu H, Vinograd J, (1972) Replication of mitochondrial DNA. Circular replicative intermediates in mouse L cells. Proc Natl Acad Sci U S A 69: 737–741.
33. Clayton DA, (1982) Replication of animal mitochondrial DNA. Cell 28: 693–705.
34. Rajala N, Gerhold JM, Martinsson P, Klymov A, Spelbrink JN, (2014) Replication factors transiently associate with mtDNA at the mitochondrial inner membrane to facilitate replication. Nucleic Acids Res 42: 952–967.
35. Maier D, Farr CL, Poeck B, Alahari A, Vogel M, et al. (2001) Mitochondrial single-stranded DNA-binding protein is required for mitochondrial DNA replication and development in Drosophila melanogaster. Mol Biol Cell 12: 821–830.
36. Van Tuyle GC, Pavco PA, (1985) The rat liver mitochondrial DNA-protein complex: displaced single strands of replicative intermediates are protein coated. The Journal of cell biology 100: 251–257.
37. Gaspari M, Falkenberg M, Larsson NG, Gustafsson CM, (2004) The mitochondrial RNA polymerase contributes critically to promoter specificity in mammalian cells. EMBO J 23: 4606–4614.
38. Holstein EM, Lydall D, (2012) Quantitative amplification of single-stranded DNA. Methods Mol Biol 920: 323–339.
39. Kukat C, Wurm CA, Spahr H, Falkenberg M, Larsson NG, et al. (2011) Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proc Natl Acad Sci U S A 108: 13534–13539.
40. Brewer BJ, Fangman WL, (1987) The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51: 463–471.
41. Brewer BJ, Fangman WL, (1988) A replication fork barrier at the 3' end of yeast ribosomal RNA genes. Cell 55: 637–643.