Oxidative stress and its impact on neurons and glia in multiple sclerosis lesions

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 3, 2016, Pages 506-510

  Lassmann, Hans ^a   van Horssen, Jack ^b  

^a Medical University of Vienna   (Austria)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Astrocytes; Microglia; Multiple sclerosis; Neurons; Oligodendrocytes; Oxidative stress

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN; PROTEIN NG2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTE; HUMAN; MACROPHAGE; MICROGLIA; MITOCHONDRION; MULTIPLE SCLEROSIS; NERVE CELL; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; STEM CELL; TISSUE DEGENERATION; TISSUE INJURY;

EID: 84957842717     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.09.018     Document Type: Article

References (55)

1. Aboul-Enein F., Rauschka H., Kornek B., Stadelmann C., Stefferl A., Brück W., Lucchinetti C.F., Schmidbauer M., Jellinger K., Lassmann H. Preferential loss of myelin associated glycoprotein reflects hypoxia-like white matter damage in stroke and inflammatory brain diseases. J. Neuropathol. Exp. Neurol. 2003, 62:25-33.
2. Aboul-Enein F., Weiser P., Höftberger R., Lassmann H., Bradl M. Transient axonal injury in the absence of demyelination: a correlate of clinical disease in acute experimental autoimmune encephalomyelitis. Acta Neuropathol. 2006, 111:539-547.
3. Barnett M.H., Prineas J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 2004, 55:458-468.
4. Baud O., Greene A.E., Li J., Wang H., Volpe J.J., Rosenberg P.A. Glutathione peroxidase-catalase cooperativity is required for reststance to hydrogen peroxide by mature rat oligodendrocytes. J. Neurosci. 2004, 24:1531-1540.
5. Breij E.C., Brink B.P., Veerhuis R., van den Berg C., Vloet R., Yan R., Dijkstra C.D., van der Valk P., Bö L. Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann. Neurol. 2008, 63:16-25.
6. Bua E., Johnson J., Herbst A., Delong B., McKenzie D., Salamat S., Aiken J.M. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am. J. Hum. Genet. 2006, 79:469-480.
7. Campbell G.R., Ziabreva I., Reeve A.K., Krishnan K.J., Reynolds R., Howell O., Lassmann H., Turnbull D.M., Mahad D.F. Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann. Neurol. 2010, 69:481-492.
8. Carvalho A.N., Lim J.L., Nijland P.G., Witte M.E., van Horssen J. Glutathione in multiple sclerosis: more than just an antioxidant?. Mult. Scler. 2014, 20:1425-1431.
9. Chang A., Tourtelotte W.W., Rudick R., Trapp B.D. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N. Engl. J. Med. 2002, 346:165-173.
10. Connor J.R., Menzies S.L. Cellular management of iron in the brain. J. Neurol. Sci. 1995, 134(Suppl):33-44.
11. Cross A.H., Manning P.T., Keeling R.M., Schmidt R.E., Misko T.P. Peroxynitrite formation within the central nervous system in active multiple sclerosis. J. Neuroimmunol. 1998, 88:45-56.
12. Fischer M.T., Sharma R., Lim J.L., Haider L., Frischer J.M., Drexhage J., Mahad D., Bradl M., van Horssen J., Lassmann H. NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain 2012, 135:886-899.
13. Fischer M.T., Wimmer I., Höftberger R., Gerlach S., Haider L., Zrzavy T., Hametner S., Mahad D., Binder C.J., Krumbholz M., Bauer J., Bradl M., Lassmann H. Disease-specific molecular events in cortical multiple sclerosis lesions. Brain 2013, 136:1799-1815.
14. French H.M., Reid M., Mamontov P., Simmons R.A., Grinspan J.B. Oxidative stress disrupts oligodendrocyte maturation. J. Neurosci. Res. 2009, 87:3076-3087.
15. Friese M.A., Schattling B., Fugger L. Mechanisms of neurodegeneration and axonal dysfunction in multiple sclerosis. Nat. Rev. Neurol. 2014, 10:225-238.
16. Frischer J.M., Weigand S.D., Guo Y., Kale N., Parisi J.E., Pirko I., Mandrekar J., Bramow S., Metz I., Brück W., Lassmann H., Lucchinetti C.F. Clinical and pathological insights into the dynamic nature of the white matter multiple sclerosis plaque. Ann. Neurol. 2015, (Epub ahead of print). 10.1002/ana.24497.
17. Fünfschilling U., Supplie L.M., Mahad D., Boretius S., Saab A.S., Edgar J., Brinkmann B.G., Kassmann C.M., Tzyetanova I.D., Möbius W., Diaz F., Meier D., Suter U., Hamprecht B., Sereda M.W., Moraes C.T., Frahm J., Goebbels S., Nave K.A. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 2012, 485:517-521.
18. Gray E., Kemp K., Hares K., Redondo J., Rice C., Scolding N., Wilkins A. Increased microglia catalase activity in multiple sclerosis grey matter. Brain Res. 2014, 1599:55-64.
19. Gray E., Thomas T.L., Betmouni S., Scolding N., Love S. Elevated activity of microglial expression of myeloperoxidase in demyelinated cerebral cortex in multiple sclerosis. Brain Pathol. 2008, 18:86-95.
20. Gray E., Thomas T.L., Betmouni S., Scolding N., Love S. Elevated myeloperoxidase activity in white matter in multiple sclerosis. Neurosci. Lett. 2008, 442:195-198.
21. Haider L., Fischer M.T., Frischer J.M., Bauer J., Hoftberger R., Botond G., Esterbauer H., Binder C.J., Witztum J.L., Lassmann H. Oxidative damage in multiple sclerosis lesions. Brain 2011, 134:1914-1924.
22. Hametner S., Wimmer I., Haider L., Pfeifenbring S., Bruck W., Lassmann H. Iron and neurodegeneration in the multiple sclerosis brain. Ann. Neurol. 2013, 74:848-861.
23. Juurlink B.H., Thorburne S.K., Hertz L. Peroxide-scavenging deficit underlies oligodendrocyte susceptibility to oxidative stress. Glia 1998, 22:371-378.
24. Li L., Tan J., Miao Y., Lei P., Zhang Q. ROS and autophagy: interactions and molecular regulatory. Cell. Mol. Neurobiol. Feb 27 2015, (Epub ahead of print).
25. Licht-Mayer S., Wimmer I., Traffehn S., Metz I., Brück W., Bauer J., Bradl M., Lassmann H. Cell type-specific Nrf2 exrpession in multiple sclerosis lesions. Acta Neuropathol. 2015, 130:263-277.
26. Lim J.L., Wilhelmus M.M., de Vires H.E., Drukarch B., Hoozemans J.J., van Horssen J. Antioxidative defense mechanisms controlled by Nrf2: state of the art and clinical perspectives in neurodegenerative diseases. Arch. Toxicol. 2014, 88:1773-1786.
27. Liu J.S.H., Zhao M.L., Brosnan C.F., Lee S.C. Expression of inducible nitric oxide synthase and nitrotyrosine in multiple sclerosis lesions. Am. J. Pathol. 2001, 158:2057-2066.
28. Lopes K.O., Sparks D.L., Streit W.J. Microglial dystrophy in the aged and Alzheimer's disease brain is associated with ferritin immunoreactivity. Glia 2008, 56:1048-1060.
29. Lucchinetti C., Bruck W., Parisi J., Scheithauer B., Rodriguez M., Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 2000, 47:707-717.
30. Mahad D., Trapp B.D., Lassmann H. Pathological mechanisms in progressive multiple sclerosis. Lancet Neurol. 2015, 14:183-193.
31. Mahad D., Ziabreva I., Lassmann H., Turnbull D. Mitochondrial defects in acute multiple sclerosis lesions. Brain 2008, 131:1722-1735.
32. Matsushita T., Masaki K., Suzuki S., Matsuoka T., Yonekawa T., Wu X.M., Tabira T., Iwaki T., Kira J. Astrocytopathy in neuromyelitis optica, multiple sclerosis and Balo's disease. Rinsho Shinkeigaku 2011, 51:898-900.
33. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
34. Nijland P.G., Witte M.E., van het Hof B., van der Pol S., Bauer J., Lassmann H., van der Valk P., de Vries H.E., van Horssen J. Astroglial PGC-1alpha increases mitochondrial antioxidant capacity and suppresses inflammation: implications for multiple sclerosis. Acta Neuropathol. Commun. 2014, 2:170.
35. Nikic I., Merkler D., Sorbara C., Brinkoetter M., Kreutzfeldt M., Bareyre F.M., Brück W., Bishop D., Misgeld T., Kerschensteiner M. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat. Med. 2011, 17:495-499.
36. Ow Y.P., Green D.R., Hao Z., Mak T.W. Cytochrome c: functions beyond respiration. Nat. Rev. Mol. Cell Biol. 2008, 9:532-542.
37. Patrikios P., Stadelmann C., Kutzelnigg A., Rauschka H., Schmidbauer M., Laursen H., Sorensen P.S., Bruck W., Lucchinetti C., Lassmann H. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006, 129(Pt. 12):3165-3172.
38. Peferoen LA, Vogel DY, Ummenthum K, Breur M, Heijnen PD, Gerritsen WH, Peferoen-Baert RM, van der Valk P, Dijkstra CD, Amor S. Activation status of human microglia is dependent on lesion formation stage and remyelination in multiple sclerosis. J. Neuropathol. Exp. Neurol. 74: 48-63.
39. Radi E., Formichi P., Battisti C., Federico A. Apoptosis and oxidative stress in neurodegenerative diseases. J. Alzheimers Dis. 2014, 42(Suppl. 3):S125-S152.
40. Schuh C., Wimmer I., Hametner S., Haider L., Van Dam A.M., Liblau R.S., Smith K.J., Probert L., Binder C.J., Bauer J., Bradl M., Mahad D., Lassmann H. Oxidative tissue injury in multiple sclerosis is only partly reflected in experimental disease models. Acta Neuropathol. 2014, 128:247-266.
41. Sharma R., Fischer M.T., Bauer J., Felts P.A., Smith K.J., Misu T., Fujihara K., Bradl M., Lassmann H. Inflammation induced by innate immunity in the central nervous system leads to primary astrocyte dysfunction followed by demyelination. Acta Neuropathol. 2010, 120:223-236.
42. Stahnke T., Stadelmann C., Netzler A., Brück W., Richter-Landsberg C. Differential up-regulation of heme oxygenase-(HSP32) in glial cells after oxidative stress and in demyelinating disorders. J. Mol. Neurosci. 2007, 32:25-37.
43. Stephenson E., Nathoo N., Mahjoub Y., Dunn J.F., Yong V.W. Iron in multiple sclerosis: roles in neurodegeneration and repair. Nat. Rev. Neurol. 2014, 10:459-468.
44. Stys P.K. General mechanisms of axonal damage and its prevention. J. Neurol. Sci. 2005, 133:3-13.
45. van Horssen J., Drexhage J., Flor T., Gerritsen W., van der Valk P., de Vries H.E. Nrf2 and DJ1 are consistently upregulated in inflammatory multiple sclerosis lesions. Free Radic. Biol. Med. 2010, 8:1283-1289.
46. Van Horssen J., Schreibelt G., Drexhage J., Hazes T., Dijkstra C.D., van der Valk P., de Vries Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic. Biol. Med. 2008, 45:1729-1737.
47. Van Horssen J., Witte M.E., Schreibelt G., de Vries H.E. Radical changes in multiple sclerosis pathogenesis. Biochim. Biophys. Acta 2011, 1812:141-150.
48. Veto S., Acs P., Bauer J., Lassmann H., Berente Z., Setalo G., Borgulya G., Sumegi B., Komoly S., Gallyas F., Illes Z. Inhibiting poly(ADP-ribose) polymerase: a potential therapy against oligodendrocyte death. Brain 2010, 133:822-834.
49. Vogel D.Y., Vereyken E.J., Glim J.E., Heijnen P.D., Moeton M., van der Valk P., Amor S., Teunissen C.E., van Horssen J., Dijkstra C.D. Macrophages in inflammatory multiple sclerosis lesions have an intermediate activation status. J. Neuroinflammation 2013, 10:35.
50. Wilhelmus M.M., van der Pol S.M., Jansen Q., Witte M.E., van der Valk P., Rozenmuller A.J., Drukarch B., de Vries H.E., van Horssen J. Association of Parkinson disease-related protein PINK1 with Alzheimer disease and multiple sclerosis lesions. Free Radic. Biol. Med. 2011, 50:469-476.
51. Witte M.E., Bol J.G., Gerritsen W.H., van der Valk P., Drukarch B., van Horssen J., Wilhelmus M.M. Parkinson's disease-associated parkin colokalizes with Alzheimer's disease and multiple sclerosis brain lesions. Neurobiol. Dis. 2009, 36:445-452.
52. Witte M.E., Nijland P.G., Drexhage J.A., Gerritsen W., Geerts D., van Het Hof B., et al. Reduced expression of PGC-1alpha partly underlies mitochondrial changes and correlates with neuronal loss in multiple sclerosis cortex. Acta Neuropathol. 2013, 125:231-243.
53. Zarruck J.G., Berard J.L., Passos dos Santos R., Kroner A., Lee J., Arosio P., David S. Expression of iron homeostasis proteins in the spinal cord in experimental autoimmune encephalomyelitis and their implications for iron accumulation. Neurobiol. Dis. 2015, (Epub ahead of print). 10.1016/j.nbd.2015.02.001.
54. Zeis T., Propst A., Steck A.J., Stadelmann C., Brück W., Schaeren-Wiemers N. Molecular changes in white matter adjacent to an active demyelinating lesion in early multiple sclerosis. Brain Pathol. 2009, 19:459-466.
55. Ziabreva I., Campbell G., Rist J., Zambonin J., Rorbach J., Wydro M.M., Lassmann H., Franklin R.J., Mahad D. Injury and differentiation following inhibition of mitochondrial respiratory chain complex IV in rat oligodendrocytes. Glia 2010, 58:1827-1837.