Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients

Annals of Neurology

Volumn 59, Issue 3, 2006, Pages 478-489

  Dutta, Ranjan ^a   McDonough, Jennifer ^a,c   Yin, Xinghua ^a   Peterson, John ^a   Chang, Ansi ^a   Torres, Thalia ^a   Gudz, Tatyana ^a,d   Macklin, Wendy B ^a   Lewis, David A ^b   Fox, Robert J ^a   Rudick, Richard ^a   Mirnics, Karoly ^b   Trapp, Bruce D ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c KENT STATE UNIVERSITY   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE);

ADULT; AGED; ARTICLE; AUTOPSY; CELL ULTRASTRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; DEMYELINATION; DISABILITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; FEMALE; GABAERGIC SYSTEM; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; INTERNEURON; ION TRANSPORT; MALE; MITOCHONDRIAL RESPIRATION; MOTOR CORTEX; MULTIPLE SCLEROSIS; NERVE FIBER DEGENERATION; NEUROPROTECTION; NEUROTRANSMISSION; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PATHOPHYSIOLOGY; PRESYNAPTIC NERVE; PRIORITY JOURNAL;

AGED; AXONS; BLOTTING, WESTERN; DEMYELINATING DISEASES; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; FEMALE; GLUTAMATE DECARBOXYLASE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ISOENZYMES; MALE; MICROARRAY ANALYSIS; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; MITOCHONDRIAL DISEASES; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NEUROFILAMENT PROTEINS; PARVALBUMINS; POSTMORTEM CHANGES; RECEPTORS, GABA-A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPINAL CORD;

EID: 33644817756     PISSN: 03645134     EISSN: None     Source Type: Journal    
DOI: 10.1002/ana.20736     Document Type: Article

References (51)

1. Pedraza L, Huang JK, Colman DR. Organizing principles of the axoglial apparatus. Neuron 2001;30:335-344.
2. Noseworthy JH, Lucchinetti C, Rodriguez M, et al. Multiple sclerosis. N Engl J Med 2000;343:938-952.
3. Craner MJ, Newcombe J, Black JA, et al. Molecular changes in neurons in multiple sclerosis: altered axonal expression of Nav1.2 and Nav1.6 sodium channels and Na+/Ca2+ exchanger. Proc Natl Acad Sci USA 2004;101:8168-8173.
4. Stys PK. White matter injury mechanisms. Curr Mol Med 2004;4:109-126.
5. Rudick RA, Goodman A, Herndon RM, et al. Selecting relapsing remitting multiple sclerosis patients for treatment: the case for early treatment. J Neuroimmunol 1999;98:22-28.
6. Trapp BD, Ransohoff RM, Fisher E, et al. Neurodegeneration in multiple sclerosis: relationship to neurological disability. Neuroscientist 1999;5:48-57.
7. Whitney LW, Becker KG, Tresser NJ, et al. Analysis of gene expression in multiple sclerosis lesions using cDNA microarrays. Ann Neurol 1999;46:425-428.
8. Tajouri L, Mellick AS, Ashton KJ, et al. Quantitative and qualitative changes in gene expression patterns characterize the activity of plaques in multiple sclerosis. Brain Res Mol Brain Res 2003;119:170-183.
9. Lock C, Hermans G, Pedotti R, et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 2002;8:500-508.
10. Graumann U, Reynolds R, Steck AJ, et al. Molecular changes in normal appearing white matter in multiple sclerosis are characteristic of neuroprotective mechanisms against hypoxic insult. Brain Pathol 2003;13:554-573.
11. Lindberg RL, De Groot CJ, Certa U, et al. Multiple sclerosis as a generalized CNS disease-comparative microarray analysis of normal appearing white matter and lesions in secondary progressive MS. J Neuroimmunol 2004;152:154-167.
12. Mirnics K, Middleton FA, Marquez A, et al. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 2000;28:53-67.
13. Trapp BD, Peterson J, Ransohoff RM, et al. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998;338:278-285.
14. Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003;4:249-264.
15. Mirnics K, Korade Z, Arion D, et al. Presenilin-1-dependent transcriptome changes. J Neurosci 2005;25:1571-1578.
16. Lazarov O, Robinson J, Tang YP, et al. Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 2005;120:701-713.
17. Hosack DA, Dennis G Jr, Sherman BT, et al. Identifying biological themes within lists of genes with EASE. Genome Biol 2003;4:R70.
18. Triepels RH, Hanson BJ, van den Heuvel LP, et al. Human complex I defects can be resolved by monoclonal antibody analysis into distinct subunit assembly patterns. J Biol Chem 2001;276:8892-8897.
19. Krahenbuhl S, Chang M, Brass EP, et al. Decreased activities of ubiquinol:ferricytochrome c oxidoreductase (complex III) and ferrocytochrome c:oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin[c-lactam]-induced methylmalonic aciduria. J Biol Chem 1991;266:20998-21003.
20. Birch-Machin MA, Turnbull DM. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol 2001;65:97-117.
21. Stys PK, Jiang Q. Calpain-dependent neurofilament breakdown in anoxic and ischemic rat central axons. Neurosci Lett 2002;328:150-154.
22. Brazma A, Hingamp P, Quackenbush J, et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 2001;29:365-371.
23. Hendry SH, Schwark HD, Jones EG, et al. Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 1987;7:1503-1519.
24. Sarto I, Wabnegger L, Dogl E, et al. Homologous sites of GABA(A) receptor alpha(1), beta(3) and gamma(2) subunits are important for assembly. Neuropharmacology 2002;43:482-491.
25. Fritschy JM, Brunig I. Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 2003;98:299-323.
26. Wang H, Bedford FK, Brandon NJ, et al. GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 1999;397:69-72.
27. Hashimoto T, Volk DW, Eggan SM, et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 2003;23:6315-6326.
28. Bjartmar C, Kidd G, Mork S, et al. Neurological disability correlates with spinal cord axonal loss and reduce N-acetyl aspartate in chronic multiple sclerosis patients. Ann Neurol 2000;48:893-901.
29. Jiang Q, Stys PK. Calpain inhibitors confer biochemical, but not electrophysiological, protection against anoxia in rat optic nerves. J Neurochem 2000;74:2101-2107.
30. Waxman SG, Craner MJ, Black JA. Na+ channel expression along axons in multiple sclerosis and its models. Trends Pharmacol Sci 2004;25:584-591.
31. Ames A III. CNS energy metabolism as related to function. Brain Res Brain Res Rev 2000;34:42-68.
32. 2+ influx during anoxia in mammalian central nervous system white matter. Ann Neurol 1991;30:375-380.
33. O'Brien ET, Salmon ED, Erickson HP. How calcium causes microtubule depolymerization. Cell Motil Cytoskeleton 1997;36:125-135.
34. Lu F, Selak M, O'Connor J, et al. Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis. J Neurol Sci 2000;177:95-103.
35. Sarti P, Giuffre A, Barone MC, et al. Nitric oxide and cytochrome oxidase: reaction mechanisms from the enzyme to the cell. Free Radic Biol Med 2003;34:509-520.
36. Kapoor R, Davies M, Blaker PA, et al. Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann Neurol 2003;53:174-180.
37. Yun HY, Dawson VL, Dawson TM. Neurobiology of nitric oxide. Crit Rev Neurobiol 1996;10:291-316.
38. Peterson JW, Bo L, Mork S, et al. Transected neurites, apoptotic neurons and reduced inflammation in cortical MS lesions. Ann Neurol 2001;50:389-400.
39. Gehrmann J, Matsumoto Y, Kreutzberg GW. Microglia: intrinsic immuneffector cell of the brain. Brain Res Brain Res Rev 1995;20:269-287.
40. Diestel A, Aktas O, Hackel D, et al. Activation of microglial poly(ADP-ribose)-polymerase-1 by cholesterol breakdown products during neuroinflammation: a link between demyelination and neuronal damage. J Exp Med 2003;198:1729-1740.
41. Wujek J, Yin X, Fujii Y, et al. Activated microglia target neurons and strip synapses in an animal model of multiple sclerosis. Soc Neurosci Abstr 2003;529:11.
42. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 2002;5:405-414.
43. Hardingham GE, Bading H. The Yin and Yang of NMDA receptor signalling. Trends Neurosci 2003;26:81-89.
44. Liu S, Wong-Riley M. Disproportionate regulation of nuclear- and mitochondrial-encoded cytochrome oxidase subunit proteins by functional activity in neurons. Neuroscience 1995;67:197-210.
45. Blinkenberg M, Rune K, Jensen CV, et al. Cortical cerebral metabolism correlates with MRI lesion load and cognitive dysfunction in MS. Neurology 2000;54:558-564.
46. Levy LM, Ziemann U, Chen R, et al. Rapid modulation of GABA in sensorimotor cortex induced by acute deafferentation. Ann Neurol 2002;52:755-761.
47. Beer MA, Tavazoie S. Predicting gene expression from sequence. Cell 2004;117:185-198.
48. Wilusz CJ, Wilusz J. Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet 2004;20:491-497.
49. Stys PK. General mechanisms of axonal damage and its prevention. J Neurol Sci 2005;233:3-13.
50. Hains BC, Saab CY, Lo AC, et al. Sodium channel blockade with phenytoin protects spinal cord axons, enhances axonal conduction, and improves functional motor recovery after contusion SCI. Exp Neurol 2004;188:365-377.
51. Bechtold DA, Kapoor R, Smith KJ. Axonal protection using flecainide in experimental autoimmune encephalomyelitis. Ann Neurol 2004;55:607-616.