Increased mitochondrial content in remyelinated axons: Implications for multiple sclerosis

Brain

Volumn 134, Issue 7, 2011, Pages 1901-1913

  Zambonin, Jessica L ^a   Zhao, Chao ^b   Ohno, Nobuhiko ^c   Campbell, Graham R ^a   Engeham, Sarah ^a   Ziabreva, Iryna ^a   Schwarz, Nadine ^a   Lee, Sok Ee ^b   Frischer, Josa M ^d   Turnbull, Doug M ^a   Trapp, Bruce D ^c   Lassmann, Hans ^d   Franklin, Robin J M ^b   Mahad, Don J ^a,c  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c LERNER RESEARCH INSTITUTE   (United States)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

axon; demyelination; mitochondria; multiple sclerosis; remyelination

Indexed keywords

PORIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; CELL SIZE; CONTROLLED STUDY; DEMYELINATION; FEMALE; HUMAN; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MULTIPLE SCLEROSIS; MYELINATED NERVE; NERVE FIBER; NERVOUS TISSUE; NEUROFILAMENT; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; REMYELINIZATION; ULTRASTRUCTURE;

EID: 79959750950     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr110     Document Type: Article

References (45)

1. Aboul-Enein F, Krssak M, Hoftberger R, Prayer D, Kristoferitsch W. Reduced NAA-levels in the NAWM of patients with MS is a feature of progression. A study with quantitative magnetic resonance spectroscopy at 3 Tesla. PLoS One 2010; 5: e11625.
2. Amiri M, Hollenbeck PJ. Mitochondrial biogenesis in the axons of vertebrate peripheral neurons. Dev Neurobiol 2008; 68: 1348-61.
3. Andrews HE, Nichols PP, Bates D, Turnbull DM. Mitochondrial dysfunction plays a key role in progressive axonal loss in Multiple Sclerosis. Med Hypotheses 2005; 64: 669-77. (Pubitemid 40203051)
4. Caldwell PC, Hodgkin AL, Keynes RD, Shaw TL. The effects of injecting 'energy-rich' phosphate compounds on the active transport of ions in the giant axons of Loligo. J Physiol 1960; 152: 561-90.
5. Campbell GR, Ziabreva I, Reeve AK, Krishnan KJ, Reynolds R, Howell O, et al. Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann Neurol 2011; 69: 481-92.
6. Chen H, Chan DC. Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum Mol Genet 2009; 18: R169-76.
7. Coman I, Aigrot MS, Seilhean D, Reynolds R, Girault JA, Zalc B, et al. Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis. Brain 2006; 129 (Pt 12): 3186-95. (Pubitemid 44871435)
8. Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372: 1502-17.
9. Craner MJ, Newcombe J, Black JA, Hartle C, Cuzner ML, Waxman SG. 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: 8168-73. (Pubitemid 38698072)
10. DeLuca GC, Ebers GC, Esiri MM. Axonal loss in multiple sclerosis: a pathological survey of the corticospinal and sensory tracts. Brain 2004; 127 (Pt 5): 1009-18. (Pubitemid 38623038)
11. Dutta R, McDonough J, Yin X, Peterson J, Chang A, Torres T, et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 2006; 59: 478-89. (Pubitemid 43358068)
12. Felts PA, Baker TA, Smith KJ. Conduction in segmentally demyelinated mammalian central axons. J Neurosci 1997; 17: 7267-77. (Pubitemid 27413258)
13. Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, Schmidbauer M, et al. The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 2009; 132 (Pt 5): 1175-89.
14. Hollenbeck PJ, Saxton WM. The axonal transport of mitochondria. J Cell Sci 2005; 118 (Pt 23): 5411-9. (Pubitemid 43079283)
15. Howell OW, Palser A, Polito A, Melrose S, Zonta B, Scheiermann C, et al. Disruption of neurofascin localization reveals early changes preceding demyelination and remyelination in multiple sclerosis. Brain 2006; 129 (Pt 12): 3173-85. (Pubitemid 44871434)
16. Irvine KA, Blakemore WF. Remyelination protects axons from demyelination-associated axon degeneration. Brain 2008; 131 (Pt 6): 1464-77. (Pubitemid 351806463)
17. Kiryu-Seo S, Ohno N, Kidd GJ, Komuro H, Trapp BD. Demyelination increases axonal stationary mitochondrial size and the speed of axonal mitochondrial transport. J Neurosci 2010; 30: 6658-66.
18. Kornek B, Storch MK, Weissert R, Wallstroem E, Stefferl A, Olsson T, et al. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. Am J Pathol 2000; 157: 267-76. (Pubitemid 30641742)
19. Kovacs GG, Hoftberger R, Majtenyi K, Horvath R, Barsi P, Komoly S, et al. Neuropathology of white matter disease in Leber's hereditary optic neuropathy. Brain 2005; 128 (Pt 1): 35-41. (Pubitemid 40070518)
20. Kuhlmann T, Lingfeld G, Bitsch A, Schuchardt J, Bruck W. Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 2002; 125 (Pt 10): 2202-12.
21. Mahad DJ, Ziabreva I, Campbell G, Lax N, White K, Hanson PS, et al. Mitochondrial changes within axons in multiple sclerosis. Brain 2009; 132 (Pt 5): 1161-74.
22. McFarland R, Taylor RW, Turnbull DM. A neurological perspective on mitochondrial disease. Lancet Neurol 2010; 9: 829-40.
23. Miller KE, Sheetz MP. Axonal mitochondrial transport and potential are correlated. J Cell Sci 2004; 117 (Pt 13): 2791-804. (Pubitemid 38997261)
24. Morris RL, Hollenbeck PJ. The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J Cell Sci 1993; 104 (Pt 3): 917-27. (Pubitemid 23123484)
25. Mutsaers SE, Carroll WM. Focal accumulation of intra-axonal mitochondria in demyelination of the cat optic nerve. Acta Neuropathol 1998; 96: 139-43. (Pubitemid 28356526)
26. Nikolaeva MA, Mukherjee B, Stys PK. Na +-dependent sources of intra-axonal Ca2+ release in rat optic nerve during in vitro chemical ischemia. J Neurosci 2005; 25: 9960-7. (Pubitemid 41528034)
27. Patani R, Balaratnam M, Vora A, Reynolds R. Remyelination can be extensive in multiple sclerosis despite a long disease course. Neuropathol Appl Neurobiol 2007; 33: 277-87. (Pubitemid 46701044)
28. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, et al. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006; 129 (Pt 12): 3165-72. (Pubitemid 44871433)
29. Penderis J, Shields SA, Franklin RJ. Impaired remyelination and depletion of oligodendrocyte progenitors does not occur following repeated episodes of focal demyelination in the rat central nervous system. Brain 2003; 126 (Pt 6): 1382-91. (Pubitemid 36644383)
30. Prineas JW, Connell F. Remyelination in multiple sclerosis. Ann Neurol 1979; 5: 22-31. (Pubitemid 9083248)
31. Qi X, Lewin AS, Sun L, Hauswirth WW, Guy J. Mitochondrial protein nitration primes neurodegeneration in experimental autoimmune encephalomyelitis. J Biol Chem 2006; 281: 31950-62.
32. Raine CS, Wu E. Multiple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 1993; 52: 199-204. (Pubitemid 23136018)
33. Sathornsumetee S, McGavern DB, Ure DR, Rodriguez M. Quantitative ultrastructural analysis of a single spinal cord demyelinated lesion predicts total lesion load, axonal loss, and neurological dysfunction in a murine model of multiple sclerosis. Am J Pathol 2000; 157: 1365-76.
34. Shields SA, Gilson JM, Blakemore WF, Franklin RJ. Remyelination occurs as extensively but more slowly in old rats compared to young rats following gliotoxin-induced CNS demyelination. Glia 1999; 28: 77-83. (Pubitemid 29475582)
35. Smith KJ. Axonal protection in multiple sclerosis-a particular need during remyelination? Brain 2006; 129 (Pt 12): 3147-9. (Pubitemid 44871431)
36. Smith KJ. Sodium channels and multiple sclerosis: roles in symptom production, damage and therapy. Brain Pathol 2007; 17: 230-42. (Pubitemid 46466142)
37. Smith KJ, Blakemore WF, McDonald WI. The restoration of conduction by central remyelination. Brain 1981; 104: 383-404. (Pubitemid 12183328)
38. Smith KJ, Lassmann H. The role of nitric oxide in multiple sclerosis. Lancet Neurol 2002; 1: 232-41. (Pubitemid 37159185)
39. Tondera D, Grandemange S, Jourdain A, Karbowski M, Mattenberger Y, Herzig S, et al. SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J 2009; 28: 1589-600.
40. Trapp BD, Stys PK. Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis. Lancet Neurol 2009; 8: 280-91.
41. Waxman SG. Ions, energy and axonal injury: towards a molecular neurology of multiple sclerosis. Trends Mol Med 2006; 12: 192-5. (Pubitemid 43744377)
42. Waxman SG, Black JA, Stys PK, Ransom BR. Ultrastructural concomitants of anoxic injury and early post-anoxic recovery in rat optic nerve. Brain Res 1992; 574: 105-19.
43. Waxman SG, Ritchie JM. Molecular dissection of the myelinated axon. Ann Neurol 1993; 33: 121-36. (Pubitemid 23039921)
44. Witte ME, Bo L, Rodenburg RJ, Belien JA, Musters R, Hazes T, et al. Enhanced number and activity of mitochondria in multiple sclerosis lesions. J Pathol 2009; 219: 193-204.
45. Zambonin J, Engeham S, Campbell GR, Ziabreva I, Beadle NE, Taylor RW, et al. Identification and investigation of mitochondria lacking cytochrome c oxidase activity in axons. J Neurosci Methods 2010; 192: 115-20.