Mitochondrial involvement in neurodegenerative diseases

IUBMB Life

Volumn 65, Issue 3, 2013, Pages 263-272

  Zsurka, Gábor ^a   Kunz, Wolfram S ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

mitochondria; neurodegenerative diseases; reactive oxygen species

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; CYTOCHROME C; DIHYDROLIPOAMIDE DEHYDROGENASE; DNA; ELECTRON TRANSFERRING FLAVOPROTEIN; GLUTATHIONE; KINESIN 1; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOFUSIN 2; OXIDOREDUCTASE; OXOGLUTARATE DEHYDROGENASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RNA; SEMIQUINONE; SUPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUITIN PROTEIN LIGASE E3;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CELL POPULATION; DEGENERATIVE DISEASE; DISEASE COURSE; EPILEPSY; GENE DELETION; HEREDITARY MOTOR SENSORY NEUROPATHY; HIPPOCAMPAL SCLEROSIS; HUMAN; HUNTINGTON CHOREA; LEBER HEREDITARY OPTIC NEUROPATHY; MELAS SYNDROME; MERRF SYNDROME; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MULTIPLE SCLEROSIS; MYOCLONUS EPILEPSY; NERVE CELL; NERVE DEGENERATION; NUCLEOTIDE SEQUENCE; OPTIC NERVE ATROPHY; PARKINSON DISEASE; PATHOGENESIS; QUALITY CONTROL; RESPIRATORY FAILURE; REVIEW; SENSORY NEUROPATHY; SPINOCEREBELLAR DEGENERATION; TEMPORAL LOBE EPILEPSY;

ADENOSINE TRIPHOSPHATE; CELL DEATH; DISEASE PROGRESSION; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; NEURODEGENERATIVE DISEASES; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRESYNAPTIC TERMINALS; REACTIVE OXYGEN SPECIES;

EID: 84874496689     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1126     Document Type: Review

References (86)

1. Astrup, J., Sorensen, P. M., and, Sorensen, H. R., (1981) Oxygen and glucose consumption relate to Na+-K+ transport in canine brain. Stroke 12, 726-730.
2. Herrington, J., Park, Y. B., Babcock, D. F., and, Hille, B., (1996) Dominant role of mitochondria in clearance of large Ca2+-loads from rat adrenal chromaffin cells. Neuron 16, 219-228.
3. Thayer, S. A., and, Miller, R. J., (1990) Regulation of intracellular free calcium concentration in single rat dorsal root ganglion neurons in vitro. J. Physiol. 425, 85-115.
4. Verstreken, P., Ly, C. V., Venken, K. J., Koh, T. W., Zhou, Y., et al. (2005) Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47, 365-378.
5. Tang, Y. G., and, Zucker, R. S., (1997) Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Neuron 18, 483-491.
6. Bindokas, V. P., Lee, C. C., Colmers, W. F., and, Miller, R. J., (1998) Changes in mitochondrial function resulting from synaptic activity in the rat hippocampal slice. J. Neurosci. 18, 4570-4587.
7. Koshiba, T., Detmer, S. A., Kaiser, J. T., Chen, H., McCaffery, J. M., et al. (2004) Structural basis of mitochondrial tethering by mitofusin complexes. Science 305, 858-862.
8. Meeusen, S., McCaffery, J. M., and, Nunnari, J., (2004) Mitochondrial fusion intermediates revealed in vitro. Science 305, 1747-1752.
9. Song, Z., Ghochani, M., McCaffery, J. M., Frey, T. G., and, Chan, D. C., (2009) Mitofusins and OPA1 mediate sequential steps in mitochondrial membrane fusion. Mol. Biol. Cell 20, 3525-3532.
10. Alexander, C., Votruba, M., Pesch, U. E., Thiselton, D. L., Mayer, S., et al. (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26, 211-215.
11. Delettre, C., Lenaers, G., Griffoin, J. M., Gigarel, N., Lorenzo, C., et al. (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26, 207-210.
12. Züchner, S., Mersiyanova, I. V., Muglia, M., Bissar-Tadmouri, N., Rochelle, J., et al. (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 36, 449-451.
13. Chen, H., Chomyn, A., and, Chan, D. C., (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280, 26185-26192.
14. Chen, H., McCaffery, J. M., and, Chan, D. C., (2007) Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130, 548-562.
15. Guo, X., Macleod, G. T., Wellington, A., Hu, F., Panchumarthi, S., et al. (2005) The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron 47, 379-393.
16. Brickley, K., Smith, M. J., Beck, M., and, Stephenson, F. A., (2005) GRIF-1 and OIP106, members of a novel gene family of coiled-coil domain proteins: association in vivo and in vitro with kinesin. J. Biol. Chem. 280, 14723-14732.
17. Glater, E. E., Megeath, L. J., Stowers, R. S., and, Schwarz, T. L., (2006) Axonal transport of mitochondria requires Milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol. 173, 545-557.
18. Fransson, A., Ruusala, A., and, Aspenstrom, P., (2003) Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J. Biol. Chem. 278, 6495-6502.
19. Rice, S. E., and, Gelfand, V. I., (2006) Paradigm lost: Milton connects kinesin heavy chain to Miro on mitochondria. J. Cell Biol. 173, 459-461.
20. Liu, X., and, Hajnõczky, G., (2009) Ca2+-dependent regulation of mitochondrial dynamics by the Miro-Milton complex. Int. J. Biochem. Cell Biol. 41, 1972-1976.
21. Yi, M., Weaver, D., and, Hajnoczky, G., (2004) Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J. Cell Biol. 167, 661-672.
22. Pilling, A. D., Horiuchi, D., Lively, C. M., and, Saxton, W. M., (2006) Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol. Biol. Cell 17, 2057-2068.
23. Osman, C., Merkwirth, C., and, Langer, T., (2009) Prohibitins and the functional compartmentalization of mitochondrial membranes. J. Cell Sci. 122, 3823-3830.
24. Xu, S., Peng, G., Wang, Y., Fang, S., and, Karbowski, M., (2011) The AAA-ATPase p97 is essential for outer mitochondrial membrane protein turnover. Mol. Biol. Cell 22, 291-300.
25. Twig, G., and, Shirihai, O. S., (2011) The interplay between mitochondrial dynamics and mitophagy. Antioxid. Redox Signal. 14, 1939-1951.
26. Gilkerson, R. W., Schon, E. A., Hernandez, E., and, Davidson, M. M., (2008) Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J. Cell Biol. 181, 1117-1128.
27. Halliwell, B., (2006) Oxidative stress and neurodegeneration: where are we now? J. Neurochem. 97, 1634-1658.
28. Balaban, R. S., Nemoto, S., and, Finkel, T., (2005) Mitochondria, oxidants, and aging. Cell 120, 483-495.
29. 2 in the production of HO: in vitro and in vivo. Free Radic. Biol. Med. 16, 29-33.
30. Klungland, A., Rosewell, I., Hollenbach, S., Larsen, E., Daly, G., et al. (1999) Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage, Proc. Natl. Acad. Sci. USA 96, 13300-13305.
31. Liu, Y., Fiskum, G., and, Schubert, D., (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80, 780-787.
32. Kudin, A. P., Bimpong-Buta, N. Y., Vielhaber, S., Elger, C. E., and, Kunz, W. S., (2004) Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 279, 4127-4135.
33. Votyakova, T. V., and, Reynolds, I. J., (2001) DeltaPsi(m)-dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 79, 266-277.
34. Genova, M. L., Ventura, B., Giuliano, G., Bovina, C., Formiggini, G., et al. (2001) The site of production of superoxide radical in mitochondrial complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2. FEBS Lett. 505, 364-368.
35. Lambert, A. J., and, Brand, M. D., (2004) Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 279, 39414-39420.
36. Boveris, A., Cadenas, E., and, Stoppani, A. O., (1976) Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem. J. 156, 435-444.
37. St-Pierre, J., Buckingham, J. A., Roebuck, S. J., and, Brand, M. D., (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44784-44790.
38. Kudin, A. P., Debska-Vielhaber, G., and, Kunz, W. S., (2005) Characterization of superoxide production sites in isolated rat brain and skeletal muscle mitochondria. Biomed. Pharmacother. 59, 163-168.
39. Guzy, R. D., Hoyos, B., Robin, E., Chen, H., Liu, L., et al. (2005) Mitochondrial complex III is required for hypoxia- induced ROS production and cellular oxygen sensing. Cell Metab. 1, 401-408.
40. Malinska, D., Kulawiak, B., Kudin, A. P., Kovacs, R., Huchzermeyer, C., et al. (2010) Complex III-dependent superoxide production of brain mitochondria contributes to seizure-related ROS formation. Biochim. Biophys. Acta 1797, 1163-1170.
41. Starkov, A. A., Fiskum, G., Chinopoulos, C., Lorenzo, B. J., Browne, S. E., et al. (2004) Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. 24, 7779-7788.
42. Tretter, L., and, Adam-Vizi, V., (2004) Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J. Neurosci. 24, 7771-7778.
43. Gal, S., Zheng, H., Fridkin, M., and, Youdim, M. B., (2005) Novel multifunctional neuroprotective iron chelator-monoamine oxidase inhibitor drugs for neurodegenerative diseases. In vivo selective brain monoamine oxidase inhibition and prevention of MPTP-induced striatal dopamine depletion. J. Neurochem. 95, 79-88.
44. Krause, K. H., (2004) Tissue distribution and putative physiological function of NOX family NADPH oxidases. Jpn. J. Infect. Dis. 57, S28-S29.
45. Abramov, A. Y., Jacobson, J., Wientjes, F., Hothersall, J., Canevari, L., et al. (2005) Expression and modulation of an NADPH oxidase in mammalian astrocytes. J. Neurosci. 25, 9176-9184.
46. Gonzales, F. J., (2005) Role of cytochrome P450 in chemical toxicity and oxidative stress: studies with CYP2E1. Mutat. Res. 569, 101-110.
47. Spencer, J. P., Jenner, P., Daniel, S. E., Lees, A. J., Marsden, D. C., et al. (1998) Conjugates of catecholamines with cysteine and GSH in Parkinson's disease: possible mechanisms of formation involving reactive oxygen species. J. Neurochem. 71, 2112-2122.
48. Bender, A., Krishnan, K. J., Morris, C. M., Taylor, G. A., Reeve, A. K., et al. (2006) High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet. 38, 515-517.
49. Kraytsberg, Y., Kudryavtseva, E., McKee, A. C., Geula, C., Kowall, N. W., et al. (2006) Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet. 38, 518-520.
50. Cooper, A. J. L., (1997) "Glutathione in the brain: disorders of glutathione metabolism." In The Molecular and Genetic Basis of Neurological Disease (, Rosenberg, R. N., Prusiner, S. B., DiMauro, S., Barchi, R. L., Kunk, L. M., eds.). pp. 1195-1230, Butterworth-Heinemann, Boston.
51. Langeveld, C. H., Schepens, E., Jongenelen, C. A. M., Stoof, J. C., Hjelle, O. P., et al. (1996) Presence of glutathione immunoreactivity in cultured neurons and astrocytes. Neuroreport 7, 1833-1836.
52. Dringen, R., Pfeiffer, B., and, Hamprecht, B., (1999) Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J. Neurosci. 19, 562-569.
53. Näpänkangas, J. P., Liimatta, E. V., Joensuu, P., Bergmann, U., Ylitalo, K., et al. Superoxide production during ischemia-reperfusion in the perfused rat heart: a comparison of two methods of measurement. J. Mol. Cell Cardiol. 53, 906-915.
54. Kudin, A. P., Zsurka, G., Elger, C. E., and, Kunz, W. S., (2009) Mitochondrial involvement in temporal lobe epilepsy. Exp. Neurol. 218, 326-332.
55. Gulyás, A. I., Buzsáki, G., Freund, T. F., and, Hirase, H., (2006) Populations of hippocampal inhibitory neurons express different levels of cytochrome c. Eur. J. Neurosci. 23, 2581-2594.
56. Schon, E. A., and, Przedborski, S., (2011) Mitochondria: the next (neurode)generation. Neuron 70, 1033-1053.
57. Zsurka, G., Hampel, K. G., Nelson, I., Jardel, C., Mirandola, S. R., et al. (2010) Severe epilepsy as the major symptom of new mutations in the mitochondrial tRNA(Phe) gene. Neurology 74, 507-512.
58. De Coo, I. F., Renier, W. O., Ruitenbeek, W., Ter Laak, H. J., Bakker, M., et al. (1999) A 4-base pair deletion in the mitochondrial cytochrome b gene associated with parkinsonism MELAS overlap syndrome. Ann. Neurol. 45, 130-133.
59. Silvestri, G., Mongini, T., Odoardi, F., Modoni, A., deRosa, G., et al. (2000) A new mtDNA mutation associated with a progressive encephalopathy and cytochrome c oxidase deficiency. Neurology 54, 1693-1696.
60. Swerdlow, R. H., Parks, J. K., Davis, J. N. II, Cassarino, D. S., Trimmer, P. A., et al. (1998) Matrilineal inheritance of complex I dysfunction in a multigenerational Parkinson's disease family. Ann. Neurol. 44, 873-881.
61. Zsurka, G., Baron, M., Stewart, J. D., Kornblum, C., Bös, M., et al. (2008) Clonally expanded mitochondrial DNA mutations in epileptic individuals with mutated DNA polymerase gamma. J. Neuropathol. Exp. Neurol. 67, 857-866.
62. Hakonen, A. H., Goffart, S., Marjavaara, S., Paetau, A., Cooper, H., et al. (2008) Infantile-onset spinocerebellar ataxia and mitochondrial recessive ataxia syndrome are associated with neuronal complex I defect and mtDNA depletion. Hum. Mol. Genet. 17, 3822-3835.
63. Schmucker, S., and, Puccio, H., (2010) Understanding the molecular mechanisms of Friedreich's ataxia to develop therapeutic approaches. Hum. Mol. Genet. 19, R103-R110.
64. Gerards, M., van den Bosch, B., Calis, C., Schoonderwoerd, K., van Engelen, K., et al. (2010) Nonsense mutations in CABC1/ADCK3 cause progressive cerebellar ataxia and atrophy. Mitochondrion 10, 510-515.
65. Jin, S. M., Lazarou, M., Wang, C., Kane, L. A., Narendra, D. P., et al. (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 191, 933-942.
66. Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D. F., Gautier, C. A., et al. (2010) PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 8, e1000298.
67. Gispert, S., Ricciardi, F., Kurz, A., Azizov, M., Hoepken, H. H., et al. (2009) Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One 4, e5777.
68. Shoffner, J. M., Lott, M. T., Voljavec, A. S., Soueidan, S. A., Costigan, D. A., et al. (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.
69. Wanrooij, S., Luoma, P., van Goethem, G., van Broeckhoven, C., Suomalainen, A., et al. (2004) Twinkle and POLG defects enhance age-dependent accumulation of mutations in the control region of mtDNA. Nucleic Acids Res. 32, 3053-3064.
70. Krishnan, K. J., Reeve, A. K., Samuels, D. C., Chinnery, P. F., Blackwood, J. K., et al. (2008) What causes mitochondrial DNA deletions in human cells? Nat. Genet. 40, 275-279.
71. 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.
72. Doda, J. N., Wright, C. T., and, Clayton, D. A., (1981) Elongation of displacement-loop strands in human and mouse mitochondrial DNA is arrested near specific template sequences. Proc. Natl. Acad. Sci. USA 78, 6116-6120.
73. Wiesner, R. J., Zsurka, G., and, Kunz, W. S., (2006) Mitochondrial DNA damage and the aging process: facts and imaginations. Free Radic. Res. 40, 1284-1294.
74. Fukui, H., and, Moraes, C. T., (2009) Mechanisms of formation and accumulation of mitochondrial DNA deletions in aging neurons. Hum. Mol. Genet. 18, 1028-1036.
75. Khrapko, K., Nekhaeva, E., Kraytsberg, Y., and, Kunz, W., (2003) Clonal expansions of mitochondrial genomes: implications for in vivo mutational spectra. Mutat. Res. 522, 13-19.
76. Greaves, L. C., Preston, S. L., Tadrous, P. J., Taylor, R. W., Barron, M. J., et al. (2006) Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission. Proc. Natl. Acad. Sci. USA 103, 714-719.
77. Van Goethem, G., Dermaut, B., Löfgren, A., Martin, J. J., and, Van Broeckhoven, C., (2001) Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat. Genet. 28, 211-212.
78. Longley, M. J., Clark, S., Yu Wai Man, C., Hudson, G., Durham, S. E., et al. (2006) Mutant POLG2 disrupts DNA polymerase gamma subunits and causes progressive external ophthalmoplegia. Am. J. Hum. Genet. 78, 1026-1034.
79. Spelbrink, J. N., Li, F. Y., Tiranti, V., Nikali, K., Yuan, Q. P., 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.
80. Vielhaber, S., Debska-Vielhaber, G., Peeva, V., Schoeler, S., Kudin, A. P., et al. Mitofusin 2 mutations affect mitochondrial function by mitochondrial DNA depletion. Acta Neuropathol., in press.
81. Amati-Bonneau, P., Valentino, M. L., Reynier, P., Gallardo, M. E., Bornstein, B., et al. (2008) OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 131, 338-351.
82. Hudson, G., Amati-Bonneau, P., Blakely, E. L., Stewart, J. D., He, L., et al. (2008) Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness and multiple mitochondrial DNA deletions: a novel disorder of mtDNA maintenance. Brain 131, 329-337.
83. Guo, X., Popadin, K. Y., Markuzon, N., Orlov, Y. L., Kraytsberg, Y., et al. (2010) Repeats, longevity and the sources of mtDNA deletions: evidence from 'deletional spectra'. Trends Genet. 26, 340-343.
84. Folbergrová, J., and, Kunz, W. S., (2012) Mitochondrial dysfunction in epilepsy. Mitochondrion 12, 35-40.
85. Campbell, G. R., Ziabreva, I., Reeve, A. K., Krishnan, K. J., Reynolds, R., et al. (2011) Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann. Neurol. 69, 481-92.
86. Campbell, G. R., Kraytsberg, Y., Krishnan, K. J., Ohno, N., Ziabreva, I., et al. (2012) Clonally expanded mitochondrial DNA deletions within the choroid plexus in multiple sclerosis. Acta Neuropathol. 124, 209-220.