Two-dimensional intact mitochondrial DNA agarose electrophoresis reveals the structural complexity of the mammalian mitochondrial genome

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages

  Kolesar, Jill E ^a   Wang, Catherine Y ^a   Taguchi, Yumiko V ^a   Chou, Shih Hsuan ^a   Kaufman, Brett A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULAR DNA; DNA HYBRID; DNA TOPOISOMERASE; ETHIDIUM BROMIDE; MITOCHONDRIAL DNA; RIBONUCLEASE A; RIBONUCLEASE H; RNA; SINGLE STRANDED DNA;

AGAR GEL ELECTROPHORESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COVALENT BOND; DNA DETERMINATION; DNA REPLICATION; DNA RNA HYBRIDIZATION; DNA SEQUENCE; DNA TEMPLATE; DNA TRANSCRIPTION; EMBRYO; GENE STRUCTURE; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOCHONDRIAL GENOME; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; TWO DIMENSIONAL ELECTROPHORESIS;

ANIMALS; CELL LINE; DNA REPLICATION; DNA TOPOISOMERASES; DNA, MITOCHONDRIAL; DNA, SINGLE-STRANDED; ELECTROPHORESIS, AGAR GEL; ETHIDIUM; GENOME, MITOCHONDRIAL; HUMANS; MICE; RNA;

MAMMALIA;

EID: 84876384703     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1324     Document Type: Article

References (81)

1. Nass, M.M. (1969) Mitochondrial DNA. I. Intramitochondrial distribution and structural relations of single- and double-length circular DNA. J. Mol. Biol., 42, 521-528.
2. Nass, M.M. and NASS, S. (1963) Intramitochondrial fibers with DNA characteristics. I. fixation and electron staining reactions. J. Cell Biol., 19, 593-611.
3. Iborra, F.J., Kimura, H. and Cook, P.R. (2004) The functional organization of mitochondrial genomes in human cells. BMC Biol., 2, 9.
4. Garrido, N., Griparic, L., Jokitalo, E., Wartiovaara, J., van der Bliek, A.M. and Spelbrink, J.N. (2003) Composition and dynamics of human mitochondrial nucleoids. Mol. Biol. Cell, 14, 1583-1596.
5. Brown, T.A., Tkachuk, A.N., Shtengel, G., Kopek, B.G., Bogenhagen, D.F., Hess, H.F. and Clayton, D.A. (2011) Superresolution fluorescence imaging of mitochondrial nucleoids reveals their spatial range, limits, and membrane interaction. Mol. Cell. Biol, 31, 4994-5010.
6. Kukat, C., Wurm, C.A., Spahr, H., Falkenberg, M., Larsson, N.-G. and Jakobs, S. (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. USA, 108, 13534-13539.
7. Albring, M. and Attardi, G. (1977) Association of a protein structure of probable membrane derivation with HeLa cell mitochondrial DNA near its origin of replication. Proc. Natl Acad. Sci. USA, 74, 1348-1352.
8. Kopek, B.G., Shtengel, G., Xu, C.S., Clayton, D.A. and Hess, H.F. (2012) Correlative 3D superresolution fluorescence and electron microscopy reveal the relationship of mitochondrial nucleoids to membranes. Proc. Natl Acad. Sci. USA, 109, 6136-6141.
9. Moraes, C.T. (2001) What regulates mitochondrial DNA copy number in animal cells? Trends Genet., 17, 199-205.
10. Zeviani, M., Moraes, C.T., DiMauro, S., Nakase, H., Bonilla, E., Schon, E.A. and Rowland, L.P. (1988) Deletions of mitochondrial DNA in Kearns-Sayre syndrome. Neurology, 38, 1339-1346.
11. Wallace, D.C., Zheng, X.X., Lott, M.T., Shoffner, J.M., Hodge, J.A., Kelley, R.I., Epstein, C.M. and Hopkins, L.C. (1988) Familial mitochondrial encephalomyopathy (MERRF): genetic, pathophysiological, and biochemical characterization of a mitochondrial DNA disease. Cell, 55, 601-610.
12. Wallace, D.C. (1999) Mitochondrial diseases in man and mouse. Science, 283, 1482-1488.
13. Wong, L.-J.C. (2007) Diagnostic challenges of mitochondrial DNA disorders. Mitochondrion, 7, 45-52.
14. 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.
15. Ikebe, S., Tanaka, M., Ohno, K., Sato, W., Hattori, K., Kondo, T., Mizuno, Y. and Ozawa, T. (1990) Increase of deleted mitochondrial DNA in the striatum in Parkinson's disease and senescence. Biochem. Biophys. Res. Commun., 170, 1044-1048.
16. Maassen, J.A., 'T Hart, L.M., Van Essen, E., Heine, R.J., Nijpels, G., Jahangir Tafrechi, R.S., Raap, A.K., Janssen, G.M.C. and Lemkes, H.H.P.J. (2004) Mitochondrial diabetes: molecular mechanisms and clinical presentation. Diabetes, 53(Suppl 1), S103-S109.
17. Gauthier, B.R., Wiederkehr, A., Baquie, M., Dai, C., Powers, A.C., Kerr-Conte, J., Pattou, F., MacDonald, R.J., Ferrer, J. and Wollheim, C.B. (2009) PDX1 deficiency causes mitochondrial dysfunction and defective insulin secretion through TFAM suppression. Cell Metabolism, 10, 110-118.
18. Simmons, R.A., Suponitsky-Kroyter, I. and Selak, M.A. (2005) Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to beta-cell failure. J. Biol. Chem, 280, 28785-28791.
19. Ye, C., Shu, X.-O., Wen, W., Pierce, L., Courtney, R., Gao, Y.-T., Zheng, W. and Cai, Q. (2008) Quantitative analysis of mitochondrial DNA 4977-bp deletion in sporadic breast cancer and benign breast diseases. Breast Cancer Res. Treat., 108, 427-434.
20. Meierhofer, D., Mayr, J.A., Foetschl, U., Berger, A., Fink, K., Schmeller, N., Hacker, G.W., Hauser-Kronberger, C., Kofler, B. and Sperl, W. (2004) Decrease of mitochondrial DNA content and energy metabolism in renal cell carcinoma. Carcinogenesis, 25, 1005-1010.
21. Fan, A.X.-C., Radpour, R., Haghighi, M.M., Kohler, C., Xia, P., Hahn, S., Holzgreve, W. and Zhong, X.Y. (2009) Mitochondrial DNA content in paired normal and cancerous breast tissue samples from patients with breast cancer. J. Cancer Res. Clin. Oncol., 135, 983-989.
22. Corral-Debrinski, M., Shoffner, J.M., Lott, M.T. and Wallace, D.C. (1992) Association of mitochondrial DNA damage with aging and coronary atherosclerotic heart disease. Mutat. Res., 275, 169-180.
23. Baumer, A., Zhang, C., Linnane, A.W. and Nagley, P. (1994) Age-related human mtDNA deletions: a heterogeneous set of deletions arising at a single pair of directly repeated sequences. Am. J. Hum. Genet., 54, 618-630.
24. Singh, G., Hauswirth, W.W., Ross, W.E. and Neims, A.H. (1985) A method for assessing damage to mitochondrial DNA caused by radiation and epichlorohydrin. Mol. Pharmacol., 27, 167-170.
25. Higuchi, Y. and Linn, S. (1995) Purification of all forms of HeLa cell mitochondrial DNA and assessment of damage to it caused by hydrogen peroxide treatment of mitochondria or cells. J. Biol. Chem., 270, 7950.
26. Pohjoismäki, J.L.O., Wanrooij, S., Hyvärinen, A.K., Goffart, S., Holt, I.J., Spelbrink, J.N. and Jacobs, H.T. (2006) Alterations to the expression level of mitochondrial transcription factor A, TFAM, modify the mode of mitochondrial DNA replication in cultured human cells. Nucleic Acids Res., 34, 5815-5828.
27. Pohjoismäki, J.L.O., Goffart, S., Tyynismaa, H., Willcox, S., Ide, T., Kang, D., Suomalainen, A., Karhunen, P.J., Griffith, J.D., Holt, I.J. et al. (2009) Human heart mitochondrial DNA is organized in complex catenated networks containing abundant four-way junctions and replication forks. J. Biol. Chem., 284, 21446-21457.
28. Pohjoismäki, J.L.O., Goffart, S., Taylor, R.W., Turnbull, D.M., Suomalainen, A., Jacobs, H.T. and Karhunen, P.J. (2010) Developmental and pathological changes in the human cardiac muscle mitochondrial DNA organization, replication and copy number. PLoS One, 5, e10426.
29. MacAlpine, D.M., Perlman, P.S. and Butow, R.A. (2000) The numbers of individual mitochondrial DNA molecules and mitochondrial DNA nucleoids in yeast are co-regulated by the general amino acid control pathway. EMBO J., 19, 767-775.
30. 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.
31. Laugwitz, K.-L., Moretti, A., Lam, J., Gruber, P., Chen, Y., Woodard, S., Lin, L.-Z., Cai, C.-L., Lu, M.M., Reth, M. et al. (2005) Postnatal isl1+cardioblasts enter fully differentiated cardiomyocyte lineages. Nature, 433, 647-653.
32. Wai, T., Teoli, D. and Shoubridge, E.A. (2008) The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat. Genet., 40, 1484-1488.
33. Amthor, H., Macharia, R., Navarrete, R., Schuelke, M., Brown, S.C., Otto, A., Voit, T., Muntoni, F., Vrbóva, G., Partridge, T. et al. (2007) Lack of myostatin results in excessive muscle growth but impaired force generation. Proc. Natl Acad. Sci. USA, 104, 1835-1840.
34. Maniura-Weber, K., Goffart, S., Garstka, H.L., Montoya, J. and Wiesner, R.J. (2004) Transient overexpression of mitochondrial transcription factor A (TFAM) is sufficient to stimulate mitochondrial DNA transcription, but not sufficient to increase mtDNA copy number in cultured cells. Nucleic Acids Res., 32, 6015-6027.
35. Kajander, O.A., Karhunen, P.J., Holt, I.J. and Jacobs, H.T. (2001) Prominent mitochondrial DNA recombination intermediates in human heart muscle. EMBO Rep., 2, 1007-1012.
36. 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.
37. Wiesner, R.J., Swift, H. and Zak, R. (1991) Purification of mitochondrial DNA from total cellular DNA of small tissue samples. Gene, 98, 277-281.
38. Lehmann, R.I. (1981) Endonucleases specific for single-stranded polynucleotides. The Enzymes, 4, 193-201.
39. Shokolenko, I., Venediktova, N., Bochkareva, A., Wilson, G.L. and Alexeyev, M.F. (2009) Oxidative stress induces degradation of mitochondrial DNA. Nucleic Acids Res., 37, 2539-2548.
40. Burden, D.A., Froelich-Ammon, S.J. and Osheroff, N. (2001) Topoisomerase II-mediated cleavage of plasmid DNA. Methods Mol. Biol., 95, 283-289.
41. Rickwood, D., Chambers, J.A. and Barat, M. (1981) Isolation and preliminary characterisation of DNA-protein complexes from the mitochondria of Saccharomyces cerevisiae. Exp. Cell Res., 133, 1-13.
42. Chang, D.D. and Clayton, D.A. (1985) Priming of human mitochondrial DNA replication occurs at the light-strand promoter. Proc. Natl Acad. Sci. USA, 82, 351-355.
43. 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.
44. 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.
45. 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.
46. Struhl, K. (2001) Ribonucleases. Curr. Protoc. Mol. Biol., Chapter 3, Unit3.13.
47. Hatfield, G.W. and Benham, C.J. (2002) DNA topology-mediated control of global gene expression in Escherichia coli. Annu. Rev. Genet., 36, 175-203.
48. Leis, J.P., Berkower, I. and Hurwitz, J. (1973) Mechanism of action of ribonuclease H isolated from avian myeloblastosis virus and Escherichia coli. Proc. Natl Acad. Sci. USA, 70, 466.
49. Chang, D.D., Hauswirth, W.W. and Clayton, D.A. (1985) Replication priming and transcription initiate from precisely the same site in mouse mitochondrial DNA. EMBO J., 4, 1559-1567.
50. MacAlpine, D.M., Kolesar, J., Okamoto, K., Butow, R.A. and Perlman, P.S. (2001) Replication and preferential inheritance of hypersuppressive petite mitochondrial DNA. EMBO J., 20, 1807-1817.
51. Leibowitz, R.D. (1971) The effect of ethidium bromide on mitochondrial DNA synthesis and mitochondrial DNA structure in HeLa cells. J. Cell Biol., 51, 116-122.
52. Nass, M.M. (1970) Abnormal DNA patterns in animal mitochondria: ethidium bromide-induced breakdown of closed circular DNA and conditions leading to oligomer accumulation. Proc. Natl Acad. Sci. USA, 67, 1926-1933.
53. Nass, M.M. (1972) Differential effects of ethidium bromide on mitochondrial and nuclear DNA synthesis in vivo in cultured mammalian cells. Exp. Cell Res., 72, 211-222.
54. Holt, I.J., Lorimer, H.E. and Jacobs, H.T. (2000) Coupled leadingand lagging-strand synthesis of mammalian mitochondrial DNA. Cell, 100, 515-524.
55. Clayton, D.A. (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.
56. Banerjee, S. and Spector, D.J. (1992) Differential effect of DNA supercoiling on transcription of adenovirus genes in vitro. J. Gen. Virol., 73(Pt 10), 2631-2638.
57. Matsunaga, M. and Jaehning, J.A. (2004) Intrinsic promoter recognition by a 'core' RNA polymerase. J. Biol. Chem., 279, 44239-44242.
58. Fukuoh, A., Ohgaki, K., Hatae, H., Kuraoka, I., Aoki, Y., Uchiumi, T., Jacobs, H.T. and Kang, D. (2009) DNA conformation-dependent activities of human mitochondrial RNA polymerase. Genes Cells, 14, 1029-1042.
59. Rodeheffer, M.S. and Shadel, G.S. (2003) Multiple interactions involving the amino-terminal domain of yeast mtRNA polymerase determine the efficiency of mitochondrial protein synthesis. J. Biol. Chem., 278, 18695-18701.
60. Kaimer, C. and Graumann, P.L. (2011) Players between the worlds: multifunctional DNA translocases. Curr. Opin. Microbiol., 14, 719-725.
61. Meeusen, S. and Nunnari, J. (2003) Evidence for a two membrane-spanning autonomous mitochondrial DNA replisome. J. Cell Biol., 163, 503-510.
62. Kaufman, B.A., Kolesar, J.E., Perlman, P.S. and Butow, R.A. (2003) A function for the mitochondrial chaperonin Hsp60 in the structure and transmission of mitochondrial DNA nucleoids in Saccharomyces cerevisiae. J. Cell Biol., 163, 457-461.
63. Boldogh, I.R., Nowakowski, D.W., Yang, H.-C., Chung, H., Karmon, S., Royes, P. and Pon, L.A. (2003) A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery. Mol. Biol. Cell, 14, 4618-4627.
64. Hobbs, A.E., Srinivasan, M., McCaffery, J.M. and Jensen, R.E. (2001) Mmm1p, a mitochondrial outer membrane protein, is connected to mitochondrial DNA (mtDNA) nucleoids and required for mtDNA stability. J. Cell Biol., 152, 401-410.
65. Berger, K.H. and Yaffe, M.P. (2000) Mitochondrial DNA inheritance in Saccharomyces cerevisiae. Trends Microbiol., 8, 508-513.
66. Boesch, P., Ibrahim, N., Dietrich, A. and Lightowlers, R.N. (2010) Membrane association of mitochondrial DNA facilitates base excision repair in mammalian mitochondria. Nucleic Acids Res., 38, 1478-1488.
67. Stuart, J.A., Mayard, S., Hashiguchi, K., Souza-Pinto, N.C. and Bohr, V.A. (2005) Localization of mitochondrial DNA base excision repair to an inner membrane-Associated particulate fraction. Nucleic Acids Res., 33, 3722-3732.
68. Aamann, M.D., Sorensen, M.M., Hvitby, C., Berquist, B.R., Muftuoglu, M., Tian, J., de Souza-Pinto, N.C., Scheibye-Knudsen, M., Wilson, D.M., Stevnsner, T. et al. (2010) Cockayne syndrome group B protein promotes mitochondrial DNA stability by supporting the DNA repair association with the mitochondrial membrane. FASEB J., 24, 2334-2346.
69. Bogenhagen, D.F., Wang, Y., Shen, E.L. and Kobayashi, R. (2003) Protein components of mitochondrial DNA nucleoids in higher eukaryotes. Mol. Cell. Proteomics, 2, 1205-1216.
70. Bogenhagen, D.F. (2009) Biochemical isolation of mtDNA nucleoids from animal cells. Methods Mol. Biol., 554, 3-14.
71. Wang, Y. and Bogenhagen, D.F. (2006) Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J. Biol. Chem., 281, 25791-25802.
72. Bogenhagen, D.F., Rousseau, D. and Burke, S. (2008) The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem., 283, 3665-3675.
73. He, J., Cooper, H.M., Reyes, A., Di Re, M., Kazak, L., Wood, S.R., Mao, C.C., Fearnley, I.M., Walker, J.E. and Holt, I.J. (2012) Human C4orf14 interacts with the mitochondrial nucleoid and is involved in the biogenesis of the small mitochondrial ribosomal subunit. Nucleic Acids Res., 40, 6097-6108.
74. Cerritelli, S.M., Frolova, E.G., Feng, C., Grinberg, A., Love, P.E. and Crouch, R.J. (2003) Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Molecular Cell, 11, 807-815.
75. Chujo, T., Ohira, T., Sakaguchi, Y., Goshima, N., Nomura, N., Nagao, A. and Suzuki, T. (2012) LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria. Nucleic Acids Res., 40, 8033-8047.
76. Clayton, D.A. (1982) Replication of animal mitochondrial DNA. Cell, 28, 693-705.
77. Shadel, G.S. and Clayton, D.A. (1997) Mitochondrial DNA maintenance in vertebrates. Annu. Rev. Biochem., 66, 409-435.
78. Pohjoismäki, J.L.O., Holmes, J.B., Wood, S.R., Yang, M.-Y., Yasukawa, T., Reyes, A., Bailey, L.J., Cluett, T.J., Goffart, S., Rigby, R.E. 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.
79. Leary, S.C., Kaufman, B.A., Pellecchia, G., Guercin, G.-H., Mattman, A., Jaksch, M. and Shoubridge, E.A. (2004) Human SCO1 and SCO2 have independent, cooperative functions in copper delivery to cytochrome c oxidase. Hum. Mol. Genet., 13, 1839-1848.
80. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl Acad. Sci. USA, 81, 1991-1995.
81. Martens, P.A. and Clayton, D.A. (1979) Mechanism of mitochondrial DNA replication in mouse L-cells: localization and sequence of the light-strand origin of replication. J. Mol. Biol., 135, 327-351.