The mitochondrial nucleoid: Integrating mitochondrial DNA into cellular homeostasis

Cold Spring Harbor Perspectives in Biology

Volumn 5, Issue 5, 2013, Pages

  Gilkerson, Robert ^a   Bravo, Liliana ^a   Garcia, Iraselia ^a   Gaytan, Norma ^a   Herrera, Alan ^a   Maldonado, Alicia ^a   Quintanilla, Brandi ^a  

^a UNIVERSITY OF TEXAS PAN AMERICAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; MITOCHONDRIAL DNA;

GENETICS; HOMEOSTASIS; METABOLISM; MITOCHONDRION; PHYSIOLOGY; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; HOMEOSTASIS; MITOCHONDRIA; SIGNAL TRANSDUCTION;

EID: 84877141637     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a011080     Document Type: Article

References (70)

1. Akman H.O., Dorado B, Lopez LC, Garcia-Cazorla A, Vila M.R., Tanabe LM, Dauer WT, Bonilla E, Tanji K, Hirano M. 2008. Thymidine kinase 2 (H126N) knockin mice show the essential role of balanced deoxynucleotide pools for mitochondrial DNA maintenance. Hum Mol Genet 17: 2433-2440.
2. Alam T.I., Kanki T, Muta T, Ukaji K, Abe Y, Nakayama H, Takio K., Hamasaki N, Kang D. 2003. Human mitochondrial DNA is packaged with TFAM. Nucleic Acids Res 31: 1640-1645.
3. Albring M., Griffith J, 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 74: 1348-1352.
4. Ambro L., Pevala V, Bauer J, Kutejova E. 2012. The influence of ATP-dependent proteases on a variety of nucleoid-associated processes. J Struct Biol 179: 181-192.
5. Anderson S., Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F., et al. 1981. Sequence and organization of the human mitochondrial genome. Nature 290: 457-465.
6. Bender A., Krishnan KJ, Morris CM, Taylor GA, Reeve AK, Perry R.H., Jaros E, Hersheson JS, 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.
7. Berquist B.R., Canugovi C, Sykora P, Wilson DMIII, Bohr VA. 2012. Human Cockayne syndrome B protein reciprocally communicates with mitochondrial proteins and promotes transcriptional elongation. Nucl Acids Res 40: 8392-8405.
8. Bogenhagen D.F., Rousseau D, Burke S. 2008. The layered structure of human mitochondrial DNA nucleoids. J Biol Chem 283: 3665-3675.
9. Brown T.A., Tkachuk AN, Shtengel G, Kopek BG, Bogenhagen DF, Hess HF, Clayton DA. 2011. Superresolution fluorescence imaging of mitochondrial nucleoids reveals their spatial range, limits, and membrane interaction. Mol Cell Biol 31: 4994-5010.
10. Cambier L., Rassam P, Chabi B, Mezghenna K, Gross R, Eveno E., Auffray C, Wrutniak-Cabello C, Lajoix AD, Pomies P. 2012. M19 modulates skeletal muscle differentiation and insulin secretion in pancreatic β-cells through modulation of respiratory chain activity. PLoS ONE 7: e31815.
11. Campbell G.R., Kraytsberg Y, Krishnan KJ, Ohno N, Ziabreva I, Reeve A, Trapp BD, Newcombe J, Reynolds R, Lassmann H., et al. 2012. Clonally expanded mitochondrial DNA deletions within the choroid plexus in multiple sclerosis. Acta Neuropath 124: 209-220.
12. Chen Y., Liu Y, Dorn GW II. 2011. Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ Res 109: 1327-1331.
13. de Vries R. 2010. DNA condensation in bacteria: Interplay between macromolecular crowding and nucleoid proteins. Biochimie 92: 1715-1721.
14. DiMauro S, Schon EA. 2003. Mitochondrial respiratorychain diseases. N Engl J Med 348: 2656-2668.
15. Di Re M, Sembongi H, He J, Reyes A, Yasukawa T, Martinsson P, Bailey LJ, Goffart S, Boyd-Kirkup JD, Wong T.S., et al. 2009. The accessory subunit of mitochondrial DNA polymerase g determines the DNA content of mitochondrial nucleoids in human cultured cells. Nucl Acids Res 37: 5701-5713.
16. Ekstrand M.I., Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K, Rustin P, Gustafsson CM, Larsson NG. 2004. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Gen 13: 935-944.
17. Elliott H.R., Samuels DC, Eden JA, Relton CL, Chinnery PF. 2008. Pathogenic mitochondrial DNA mutations are common in the general population. Am J Hum Genet 83: 254-260.
18. Evans M.J., Scarpulla RC. 1990. NRF-1: A trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev 4: 1023-1034.
19. Fisher R.P., Clayton DA. 1985. A transcription factor required for promoter recognition by human mitochondrial RNA polymerase. Accurate initiation at the heavy-and lightstrand promoters dissected and reconstituted in vitro. J Biol Chem 260: 11330-11338.
20. Gilkerson R.W., Schon EA, Hernandez E, Davidson MM. 2008. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J Cell Biol 181: 1117-1128.
21. Gilkerson R.W., De Vries RL, Lebot P, Wikstrom JD, Torgyekes E, Shirihai OS, Przedborski S, Schon EA. 2012. Mitochondrial autophagy in cells with mtDNA mutations results from synergistic loss of transmembrane potential and mTORC1 inhibition. Hum Mol Genet 21: 978-990.
22. Greaves L.C., Reeve AK, Taylor RW, Turnbull DM. 2012. Mitochondrial DNA and disease. J Pathol 226: 274-286.
23. + protein ATAD3 has displacement loop binding properties and is involved in mitochondrial nucleoid organization. J Cell Biol 176: 141-146.
24. He J., Cooper HM, Reyes A, Di Re M, Sembongi H, Litwin TR, Gao J, Neuman KC, Fearnley IM, Spinazzola A, et al. 2012. Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucl Acids Res 40: 6109-6121.
25. Hokari M., Kuroda S, Kinugawa S, Ide T, Tsutsui H, Iwasaki Y. 2010. Overexpression of mitochondrial transcription factor A (TFAM) ameliorates delayed neuronal death due to transient forebrain ischemia in mice. Neuropathol 30: 401-407.
26. Iborra F.J., Kimura H, Cook PR. 2004. The functional organization of mitochondrial genomes in human cells. BMC Biol 2: 9.
27. Ikeuchi M., Matsusaka H, Kang D, Matsushima S, Ide T, Kubota T., Fujiwara T, Hamasaki N, Takeshita A, Sunagawa K, et al. 2005. Overexpression of mitochondrial transcription factor A ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 112: 683-690.
28. Kanki T., Ohgaki K, Gaspari M, Gustafsson CM, Fukuoh A, Sasaki N., Hamasaki N, Kang D. 2004. Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol Cell Biol 24: 9823-9834.
29. Karamanlidis G., Nascimben L, Couper GS, Shekar PS, del Monte F., Tian R. 2010. Defective DNA replication impairs mitochondrial biogenesis in human failing hearts. Circ Res 106: 1541-1548.
30. Kasashima K., Sumitani M, Satoh M, Endo H. 2008. Human prohibitin 1 maintains the organization and stability of the mitochondrial nucleoids. Exp Cell Res 314: 988-996.
31. Kaufman B.A., Durisic N, Mativetsky JM, Costantino S, Hancock M.A., Grutter P, Shoubridge EA. 2007. The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Mol Biol Cell 18: 3225-3236.
32. Kraytsberg Y., Kudryavtseva E, McKee AC, Geula C, Kowall NW, Khrapko K. 2006. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat Genet 38: 518-520.
33. Kucej M., Kucejova B, Subramanian R, Chen XJ, Butow RA. 2008. Mitochondrial nucleoids undergo remodeling in response to metabolic cues. J Cell Sci 121: 1861-1868.
34. Kukat C., Wurm CA, Spahr H, Falkenberg M, Larsson NG, 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 108: 13534-13539.
35. Legros F., Malka F, Frachon P, Lombes A, Rojo M. 2004. Organization and dynamics of human mitochondrial DNA. J Cell Sci 117: 2653-2662.
36. Liu T., Lu B, Lee I, Ondrovicova G, Kutejova E, Suzuki CK. 2004. DNA and RNA binding by the mitochondrial lon protease is regulated by nucleotide and protein substrate. J Biol Chem 279: 13902-13910.
37. Lu B., Yadav S, Shah PG, Liu T, Tian B, Pukszta S, Villaluna N, Kutejova E., Newlon CS, Santos JH, et al. 2007. Roles for the human ATP-dependent Lon protease in mitochondrial DNA maintenance. J Biol Chem 282: 17363-17374.
38. Maniura-Weber K, Goffart S, Garstka HL, Montoya J, Wiesner RJ. 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. Nucl Acids Res 32: 6015-6027.
39. Margineantu D.H., Gregory Cox W, Sundell L, Sherwood SW, Beechem J.M., Capaldi RA. 2002. Cell cycle dependent morphology changes and associated mitochondrial DNA redistribution in mitochondria of human cell lines. Mitochondrion 1: 425-435.
40. Matsushima Y., Kaguni LS. 2012. Matrix proteases in mitochondrial DNA function. Biochim Biophys Acta 1819: 1080-1087.
41. Matsushima Y., Goto Y, Kaguni LS. 2010a. Mitochondrial Lon protease regulates mitochondrialDNAcopy number and transcription by selective degradation of mitochondrial transcription factor A (TFAM). Proc Natl Acad Sci 107: 18410-18415.
42. Matsushima Y., Goto Y, Kaguni LS. 2010b. Mitochondrial Lon protease regulates mitochondrialDNAcopy number and transcription by selective degradation of mitochondrial transcription factor A (TFAM). Proc Natl Acad Sci 107: 18410-18415.
43. McLean JR, Cohn GL, Brandt IK, Simpson MV. 1958. Incorporation of labeled amino acids into the protein of muscleandlivermitochondria. J BiolChem233:657-663.
44. Merkwirth C., Langer T. 2009. Prohibitin function within mitochondria: Essential roles for cell proliferation and cristae morphogenesis. Biochim Biophys Acta 1793: 27-32.
45. Nass S. 1969. The significance of the structural and functional similarities of bacteria and mitochondria. Int Rev Cytol 25: 55-129.
46. Nass S., Nass MM, Hennix U. 1965. Deoxyribonucleic acid in isolated rat-liver mitochondria. Biochim Biophys Acta 95: 426-435.
47. Ngo H.B., Kaiser JT, Chan DC. 2011. The mitochondrial transcription and packaging factor Tfam imposes a Uturn on mitochondrial DNA. Nat Struct Mol Biol 18: 1290-1296.
48. Nunnari J., Suomalainen A. 2012. Mitochondria: In sickness and in health. Cell 148: 1145-1159.
49. Oskoui M., Davidzon G, Pascual J, Erazo R, Gurgel-Giannetti J, Krishna S, Bonilla E, De Vivo DC, Shanske S, DiMauro S. 2006. Clinical spectrum of mitochondrial DNA depletion due to mutations in the thymidine kinase 2 gene. Archiv Neurol 63: 1122-1126.
50. Otera H., Wang C, Cleland MM, Setoguchi K, Yokota S, Youle R.J., Mihara K. 2010. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol 191: 1141-1158.
51. Owusu-Ansah E, Yavari A, Mandal S, Banerjee U. 2008. Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat Genet 40: 356-361.
52. Parone P.A., Da Cruz S, Tondera D, Mattenberger Y, James DI, Maechler P, Barja F, Martinou JC. 2008. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS ONE 3: e3257.
53. Pohjoismaki J.L., Goffart S. 2011. Of circles, forks and humanity: Topological organisation and replication of mammalian mitochondrial DNA. Bioessays 33: 290-299.
54. Puigserver P., Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839.
55. Ritov V.B., Menshikova EV, Azuma K, Wood R, Toledo FG, Goodpaster B.H., Ruderman NB, Kelley DE. 2010. Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity. Amer J Physiol 298: E49-E58.
56. Rubio-Cosials A, Sidow JF, Jimenez-Menendez N, Fernandez-Millan P., Montoya J, Jacobs HT, Coll M, Bernado P, Sola M. 2011. Human mitochondrial transcription factor A induces a U-turn structure in the light strand promoter. Nat Struct Mol Biol 18: 1281-1289.
57. Sagan L. 1967. On the origin of mitosing cells. J Theor Biol 14: 255-274.
58. Santra S., Gilkerson RW, Davidson M, Schon EA. 2004. Ketogenic treatment reduces deleted mitochondrial DNAs in cultured human cells. Ann Neurol 56: 662-669.
59. Satoh M., Kuroiwa T. 1991. Organization of multiple nucleoids and DNA molecules in mitochondria of a human cell. Exp Cell Res 196: 137-140.
60. Scarpulla RC. 2008. Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann NYAcad Sci 1147: 321-334.
61. Schon E.A., Przedborski S. 2011. Mitochondria: The next (neurode)generation. Neuron 70: 1033-1053.
62. Shutt T.E., Bestwick M, Shadel GS. 2011. The core human mitochondrial transcription initiation complex: It only takes two to tango. Transcription 2: 55-59.
63. Sumitani M., Kasashima K, Ohta E, Kang D, Endo H. 2009. Association of a novel mitochondrial protein M19 with mitochondrial nucleoids. J Biochem 146: 725-732.
64. Tang Y., Schon EA, Wilichowski E, Vazquez-Memije ME, Davidson E., King MP. 2000. Rearrangements of human mitochondrial DNA (mtDNA): New insights into the regulation of mtDNA copy number and gene expression. Mol Biol Cell 11: 1471-1485.
65. Twig G., Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G., Stiles L, Haigh SE, Katz S, Las G, et al. 2008. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27: 433-446.
66. Van Tuyle GC, McPherson ML. 1979. A compact form of rat liver mitochondrial DNA stabilized by bound proteins. J Biol Chem 254: 6044-6053.
67. Virbasius J.V., Virbasius CA, Scarpulla RC. 1993. Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev 7: 380-392.
68. Wagatsuma A., Kotake N, Yamada S. 2011. Muscle regeneration occurs to coincide with mitochondrial biogenesis. Mol Cell Biochem 349: 139-147.
69. Wintersberger E. 1964. [DNA-dependent RNA synthesis in rat liver mitochondria]. Hoppe-Seyler's Zeit Physiol Chemie 336: 285-288.
70. Ylikallio E., Tyynismaa H, Tsutsui H, Ide T, Suomalainen A. 2010. High mitochondrial DNA copy number has detrimental effects in mice. Hum Mol Genet 19: 2695-2705.