Mitochondrial DNA deletions are associated with non-B DNA conformations

Nucleic Acids Research

Volumn 40, Issue 16, 2012, Pages 7606-7621

  Damas, Joana ^a   Carneiro, João ^a   Gonçalves, Joana ^a   Stewart, James B ^b   Samuels, David C ^c   Amorim, António ^a   Pereira, Filipe ^a  

^a UNIVERSITY OF PORTO   (Portugal)

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

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; TRANSFER RNA;

ARTICLE; DNA CONFORMATION; DNA HAIRPIN; DNA REPLICATION ORIGIN; DNA STRAND BREAKAGE; GENE DELETION; HUMAN; MITOCHONDRIAL DNA DISORDER; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA STRUCTURE;

ANIMALS; DNA BREAKS; DNA, MITOCHONDRIAL; GENES, MITOCHONDRIAL; GENOME, MITOCHONDRIAL; HUMANS; MICE; NUCLEIC ACID CONFORMATION; RNA, TRANSFER; SEQUENCE DELETION;

MUS MUSCULUS;

EID: 84869477659     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks500     Document Type: Article

References (81)

1. Cooper, D.N., Bacolla, A., Ferec, C., Vasquez, K.M., Kehrer-Sawatzki, H. and Chen, J.M. (2011) On the sequence-directed nature of human gene mutation: the role of genomic architecture and the local DNA sequence environment in mediating gene mutations underlying human inherited disease. Hum. Mutat., 32, 1075-1099.
2. Wells, R.D. (2007) Non-B DNA conformations, mutagenesis and disease. Trends Biochem. Sci., 32, 271-278.
3. Zhao, J., Bacolla, A., Wang, G. and Vasquez, K.M. (2010) Non-B DNA structure-induced genetic instability and evolution. Cell Mol. Life Sci., 67, 43-62.
4. Bates, A. and Maxwell, A. (2005) DNA Topology. Oxford University Press, Oxford.
5. Mirkin, S.M. (2001) DNA topology: fundamentals. Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd, Chichester, West Sussex, UK.
6. Wells, R.D., Dere, R., Hebert, M.L., Napierala, M. and Son, L.S. (2005) Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res., 33, 3785-3798.
7. 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.
8. Hixson, J.E., Wong, T.W. and Clayton, D.A. (1986) Both the conserved stem-loop and divergent 5'-flanking sequences are required for initiation at the human mitochondrial origin of light-strand DNA replication. J. Biol. Chem., 261, 2384-2390.
9. Ngo, H.B., Kaiser, J.T. and Chan, D.C. (2011) The mitochondrial transcription and packaging factor Tfam imposes a U-turn on mitochondrial DNA. Nat. Struct. Mol. Biol., 18, 1290-1296.
10. Rubio-Cosials, A., Sidow, J.F., Jimenez-Menendez, N., Fernandez-Millan, P., Montoya, J., Jacobs, H.T., Coll, M., Bernado, P. and Solà, M. (2011) Human mitochondrial transcription factor A induces a U-turn structure in the light strand promoter. Nat. Struct. Mol. Biol., 18, 1281-1289.
11. Yakubovskaya, E., Mejia, E., Byrnes, J., Hambardjieva, E. and Garcia-Diaz, M. (2010) Helix unwinding and base flipping enable human MTERF1 to terminate mitochondrial transcription. Cell, 141, 982-993.
12. Pereira, F., Soares, P., Carneiro, J., Pereira, L., Richards, M.B., Samuels, D.C. and Amorim, A. (2008) Evidence for variable selective pressures at a large secondary structure of the human mitochondrial DNA control region. Mol. Biol. Evolut., 25, 2759-2770.
13. Lilley, D.M. (1980) The inverted repeat as a recognizable structural feature in supercoiled DNA molecules. Proc. Natl Acad. Sci. USA, 77, 6468-6472.
14. Panayotatos, N. and Wells, R.D. (1981) Cruciform structures in supercoiled DNA. Nature, 289, 466-470.
15. Clayton, D.A. (2003) Mitochondrial DNA replication: what we know. IUBMB Life, 55, 213-217.
16. Falkenberg, M., Larsson, N.G. and Gustafsson, C.M. (2007) DNA replication and transcription in mammalian mitochondria. Annu. Rev. Biochem., 76, 679-699.
17. Larsson, N.G. (2010) Somatic mitochondrial DNA mutations in mammalian aging. Annu. Rev. Biochem., 79, 683-706.
18. Dayn, A., Malkhosyan, S. and Mirkin, S.M. (1992) Transcriptionally driven cruciform formation in vivo. Nucleic Acids Res., 20, 5991-5997.
19. Postow, L., Crisona, N.J., Peter, B.J., Hardy, C.D. and Cozzarelli, N.R. (2001) Topological challenges to DNA replication: conformations at the fork. Proc. Natl Acad. Sci. USA, 98, 8219-8226.
20. Fisher, R.P., Lisowsky, T., Parisi, M.A. and Clayton, D.A. (1992) DNA wrapping and bending by a mitochondrial high mobility group-like transcriptional activator protein. J. Biol. Chem., 267, 3358-3367.
21. Brown, T.A., Tkachuk, A.N. and Clayton, D.A. (2008) Native R-loops persist throughout the mouse mitochondrial DNA genome. J. Biol. Chem., 283, 36743-36751.
22. Burger, G., Gray, M.W. and Lang, B.F. (2003) Mitochondrial genomes: anything goes. Trends Genet., 19, 709-716.
23. Bender, A., Krishnan, K.J., Morris, C.M., Taylor, G.A., Reeve, A.K., Perry, R.H., Jaros, E., Hersheson, J.S., Betts, J., Klopstock, T. et al. (2006) High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet., 38, 515-517.
24. Kraytsberg, Y., Kudryavtseva, E., McKee, A.C., Geula, C., Kowall, N.W. and Khrapko, K. (2006) Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet., 38, 518-520.
25. Cree, L.M., Samuels, D.C. and Chinnery, P.F. (2009) The inheritance of pathogenic mitochondrial DNA mutations. Biochim. Biophys. Acta Mol. Basis Disease, 1792, 1097-1102.
26. DiMauro, S. and Hirano, M. (2003) Mitochondrial DNA deletion syndromes. In: Pagon, R., Bird, T., Dolan, C. and Stephens, K. (eds), GeneReviews. University of Washington, Seattle.
27. Stewart, J.B., Freyer, C., Elson, J.L. and Larsson, N.G. (2008) Purifying selection of mtDNA and its implications for understanding evolution and mitochondrial disease. Nat. Rev. Genet., 9, 657-662.
28. Taylor, R.W. and Turnbull, D.M. (2005) Mitochondrial DNA mutations in human disease. Nat. Rev. Genet., 6, 389-402.
29. Guo, X., Popadin, K.Y., Markuzon, N., Orlov, Y.L., Kraytsberg, Y., Krishnan, K.J., Zsurka, G., Turnbull, D.M., Kunz, W.S. and Khrapko, K. (2010) Repeats, longevity and the sources of mtDNA deletions: evidence from 'deletional spectra'. Trends Genet., 26, 340-343.
30. Krishnan, K.J., Reeve, A.K., Samuels, D.C., Chinnery, P.F., Blackwood, J.K., Taylor, R.W., Wanrooij, S., Spelbrink, J.N., Lightowlers, R.N. and Turnbull, D.M. (2008) What causes mitochondrial DNA deletions in human cells? Nat. Genet., 40, 275-279.
31. Samuels, D.C., Schon, E.A. and Chinnery, P.F. (2004) Two direct repeats cause most human mtDNA deletions. Trends Genet., 20, 393-398.
32. Hou, J.H. and Wei, Y.H. (1996) The unusual structures of the hot-regions flanking large-scale deletions in human mitochondrial DNA. Biochem. J., 318 (Pt 3), 1065-1070.
33. Hou, J.H. and Wei, Y.H. (1998) AT-rich sequences flanking the 50-end breakpoint of the 4977-bp deletion of human mitochondrial DNA are located between two bent-inducing DNA sequences that assume distorted structure in organello. Mutat. Res., 403, 75-84.
34. Mita, S., Rizzuto, R., Moraes, C.T., Shanske, S., Arnaudo, E., Fabrizi, G.M., Koga, Y., DiMauro, S. and Schon, E.A. (1990) Recombination via flanking direct repeats is a major cause of large-scale deletions of human mitochondrial DNA. Nucleic Acids Res., 18, 561-567.
35. Nishigaki, Y., Marti, R. and Hirano, M. (2004) ND5 is a hot-spot for multiple atypical mitochondrial DNA deletions in mitochondrial neurogastrointestinal encephalomyopathy. Hum. Mol. Genet., 13, 91-101.
36. Rocher, C., Letellier, T., Copeland, W.C. and Lestienne, P. (2002) Base composition at mtDNA boundaries suggests a DNA triple helix model for human mitochondrial DNA large-scale rearrangements. Mol. Genet. Metab., 76, 123-132.
37. Schon, E.A., Rizzuto, R., Moraes, C.T., Nakase, H., Zeviani, M. and DiMauro, S. (1989) A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA. Science, 244, 346-349.
38. Zeviani, M., Servidei, S., Gellera, C., Bertini, E., DiMauro, S. and DiDonato, S. (1989) An autosomal dominant disorder with multiple deletions of mitochondrial DNA starting at the D-loop region. Nature, 339, 309-311.
39. Bacolla, A., Jaworski, A., Larson, J.E., Jakupciak, J.P., Chuzhanova, N., Abeysinghe, S.S., O'Connell, C.D., Cooper, D.N. and Wells, R.D. (2004) Breakpoints of gross deletions coincide with non-B DNA conformations. Proc. Natl Acad. Sci. USA, 101, 14162-14167.
40. Darmon, E., Eykelenboom, J.K., Lincker, F., Jones, L.H., White, M., Okely, E., Blackwood, J.K. and Leach, D.R. (2010) E. coli SbcCD and RecA control chromosomal rearrangement induced by an interrupted palindrome. Mol. Cell, 39, 59-70.
41. Inagaki, H., Ohye, T., Kogo, H., Kato, T., Bolor, H., Taniguchi, M., Shaikh, T.H., Emanuel, B.S. and Kurahashi, H. (2009) Chromosomal instability mediated by non-B DNA: cruciform conformation and not DNA sequence is responsible for recurrent translocation in humans. Genome Res., 19, 191-198.
42. Raghavan, S.C., Swanson, P.C., Wu, X., Hsieh, C.L. and Lieber, M.R. (2004) A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex. Nature, 428, 88-93.
43. Wang, G., Christensen, L.A. and Vasquez, K.M. (2006) Z-DNA-forming sequences generate large-scale deletions in mammalian cells. Proc. Natl Acad. Sci. USA, 103, 2677-2682.
44. Mani, R.S. and Chinnaiyan, A.M. (2010) Triggers for genomic rearrangements: insights into genomic, cellular and environmental influences. Nat. Rev. Genet., 11, 819-829.
45. Fan, L. and Yao, Y.G. (2011) MitoTool: a web server for the analysis and retrieval of human mitochondrial DNA sequence variations. Mitochondrion, 11, 351-356.
46. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
47. Knight, R., Maxwell, P., Birmingham, A., Carnes, J., Caporaso, J.G., Easton, B.C., Eaton, M., Hamady, M., Lindsay, H., Liu, Z. et al. (2007) PyCogent: a toolkit for making sense from sequence. Genome Biol., 8, R171.
48. Tyynismaa, H., Mjosund, K.P., Wanrooij, S., Lappalainen, I., Ylikallio, E., Jalanko, A., Spelbrink, J.N., Paetau, A. and Suomalainen, A. (2005) Mutant mitochondrial helicase Twinkle causes multiple mtDNA deletions and a late-onset mitochondrial disease in mice. Proc. Natl Acad. Sci. USA, 102, 17687-17692.
49. Markham, N.R. and Zuker, M. (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol. Biol., 453, 3-31.
50. SantaLucia, J. Jr (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc. Natl Acad. Sci. USA, 95, 1460-1465.
51. Mathews, D.H., Sabina, J., Zuker, M. and Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol., 288, 911-940.
52. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J. and Marra, M.A. (2009) Circos: an information aesthetic for comparative genomics. Genome Res., 19, 1639-1645.
53. Sadikovic, B., Wang, J., El-Hattab, A., Landsverk, M., Douglas, G., Brundage, E.K., Craigen, W.J., Schmitt, E.S. and Wong, L.J. (2010) Sequence homology at the breakpoint and clinical phenotype of mitochondrial DNA deletion syndromes. PLoS One, 5, e15687.
54. Helm, M. (2006) Post-transcriptional nucleotide modification and alternative folding of RNA. Nucleic Acids Res., 34, 721-733.
55. Holt, I.J., Harding, A.E. and Morgan-Hughes, J.A. (1988) Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature, 331, 717-719.
56. Kajander, O.A., Rovio, A.T., Majamaa, K., Poulton, J., Spelbrink, J.N., Holt, I.J., Karhunen, P.J. and Jacobs, H.T. (2000) Human mtDNA sublimons resemble rearranged mitochondrial genomes found in pathological states. Hum. Mol. Genet., 9, 2821-2835.
57. Wanrooij, S., Luoma, P., van, G.G., van, B.C., Suomalainen, A. and Spelbrink, J.N. (2004) Twinkle and POLG defects enhance age-dependent accumulation of mutations in the control region of mtDNA. Nucleic Acids Res., 32, 3053-3064.
58. Kasamatsu, H., Robberson, D.L. and Vinograd, J. (1971) A novel closed-circular mitochondrial DNA with properties of a replicating intermediate. Proc. Natl Acad. Sci. USA, 68, 2252-2257.
59. Callen, J.C., Tourte, M., Dennebouy, N. and Mounolou, J.C. (1983) Changes in D-loop frequency and superhelicity among the mitochondrial DNA molecules in relation to organelle biogenesis in oocytes of Xenopus laevis. Exp. Cell Res., 143, 115-125.
60. Antes, A., Tappin, I., Chung, S., Lim, R., Lu, B., Parrott, A.M., Hill, H.Z., Suzuki, C.K. and Lee, C.G. (2010) Differential regulation of full-length genome and a single-stranded 7S DNA along the cell cycle in human mitochondria. Nucleic Acids Res., 38, 6466-6476.
61. Holt, I.J., He, J., Mao, C.C., Boyd-Kirkup, J.D., Martinsson, P., Sembongi, H., Reyes, A. and Spelbrink, J.N. (2007) Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion, 7, 311-321.
62. Bailey, L.J., Cluett, T.J., Reyes, A., Prolla, T.A., Poulton, J., Leeuwenburgh, C. and Holt, I.J. (2009) Mice expressing an error-prone DNA polymerase in mitochondria display elevated replication pausing and chromosomal breakage at fragile sites of mitochondrial DNA. Nucleic Acids Res., 37, 2327-2335.
63. Srivastava, S. and Moraes, C.T. (2005) Double-strand breaks of mouse muscle mtDNA promote large deletions similar to multiple mtDNA deletions in humans. Hum. Mol. Genet., 14, 893-902.
64. San, M.D., Gower, D.J., Zardoya, R. and Wilkinson, M. (2006) A hotspot of gene order rearrangement by tandem duplication and random loss in the vertebrate mitochondrial genome. Mol. Biol. Evol., 23, 227-234.
65. Stanton, D.J., Daehler, L.L., Moritz, C.C. and Brown, W.M. (1994) Sequences with the potential to form stem-and-loop structures are associated with coding-region duplications in animal mitochondrial DNA. Genetics, 137, 233-241.
66. Cantatore, P., Gadaleta, M.N., Roberti, M., Saccone, C. and Wilson, A.C. (1987) Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature, 329, 853-855.
67. Juhling, F., Putz, J., Bernt, M., Donath, A., Middendorf, M., Florentz, C. and Stadler, P.F. (2012) Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements. Nucleic Acids Res., 40, 2833-2845.
68. Chuzhanova, N., Abeysinghe, S.S., Krawczak, M. and Cooper, D.N. (2003) Translocation and gross deletion breakpoints in human inherited disease and cancer II: Potential involvement of repetitive sequence elementsin secondary structure formation between DNA ends. Hum. Mutat., 22, 245-251.
69. Conrad, D.F., Pinto, D., Redon, R., Feuk, L., Gokcumen, O., Zhang, Y.J., Aerts, J., Andrews, T.D., Barnes, C., Campbell, P. et al. (2010) Origins and functional impact of copy number variation in the human genome. Nature, 464, 704-712.
70. Bzymek, M., Saveson, C.J., Feschenko, V.V. and Lovett, S.T. (1999) Slipped misalignment mechanisms of deletion formation: in vivo susceptibility to nucleases. J. Bacteriol., 181, 477-482.
71. Shoffner, J.M., Lott, M.T., Voljavec, A.S., Soueidan, S.A., Costigan, D.A. and Wallace, D.C. (1989) Spontaneous Kearns-Sayre/chronic external ophthalmoplegia plus syndrome associated with a mitochondrial DNA deletion: a slip-replication model and metabolic therapy. Proc. Natl Acad. Sci. USA, 86, 7952-7956.
72. Robberson, D.L., Kasamatsu, H. and Vinograd, J. (1972) Replication of mitochondrial DNA. Circular replicative intermediates in mouse L cells. Proc. Natl Acad. Sci. USA, 69, 737-741.
73. Buroker, N.E., Brown, J.R., Gilbert, T.A., Ohara, P.J., Beckenbach, A.T., Thomas, W.K. and Smith, M.J. (1990) Length heteroplasmy of sturgeon mitochondrial DNA -an illegitimate elongation model. Genetics, 124, 157-163.
74. Viguera, E., Canceill, D. and Ehrlich, S.D. (2001) Replication slippage involves DNA polymerase pausing and dissociation. EMBO J., 20, 2587-2595.
75. Weaver, D.T. and Depamphilis, M.L. (1982) Specific sequences in native DNA that arrest synthesis by DNA polymerase-alpha. J. Biol. Chem., 257, 2075-2086.
76. Bierne, H., Ehrlich, S.D. and Michel, B. (1997) Deletions at stalled replication forks occur by two different pathways. EMBO J., 16, 3332-3340.
77. Bzymek, M. and Lovett, S.T. (2001) Evidence for two mechanisms of palindrome-stimulated deletion in Escherichia coli: single-strand annealing and replication slipped mispairing. Genetics, 158, 527-540.
78. Glickman, B.W. and Ripley, L.S. (1984) Structural intermediates of deletion mutagenesis - A role for palindromic DNA. Proc. Natl Acad. Sci. USA Biol. Sci., 81, 512-516.
79. Madsen, C.S., Ghivizzani, S.C. and Hauswirth, W.W. (1993) In-vivo and in-vitro evidence for slipped mispairing in mammalian mitochondria. Proc. Natl Acad. Sci. USA, 90, 10409.
80. Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J.N., Rovio, A.T., Bruder, C.E., Bohlooly, Y., Gidlof, S., Oldfors, A., Wibom, R. et al. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature, 429, 417-423.
81. Tengan, C.H. and Moraes, C.T. (1998) Duplication and triplication with staggered breakpoints in human mitochondrial DNA. Biochim. Biophys. Acta, 1406, 73-80.