Cell type-specific Nrf2 expression in multiple sclerosis lesions

Acta Neuropathologica

Volumn 130, Issue 2, 2015, Pages 263-277

  Licht Mayer, Simon ^a   Wimmer, Isabella ^a   Traffehn, Sarah ^b   Metz, Imke ^b   Brück, Wolfgang ^b   Bauer, Jan ^a   Bradl, Monika ^a   Lassmann, Hans ^a  

^a Medical University of Vienna   (Austria)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

BG12; Demyelination; Fumarate; Multiple sclerosis; Neurodegeneration; Nrf2; Oxidative stress

Indexed keywords

APOPTOSIS INDUCING FACTOR; FUMARIC ACID; HEME OXYGENASE 1; MYELIN; TRANSCRIPTION FACTOR NRF2; NFE2L2 PROTEIN, HUMAN;

ADULT; AGED; APOPTOSIS; ARTICLE; BRAIN HYPOXIA; CENTRAL NERVOUS SYSTEM; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL GRAY MATTER; DEMYELINATING DISEASE; FEMALE; GRAY MATTER; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MICROARRAY ANALYSIS; MIDDLE AGED; MULTIPLE SCLEROSIS; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; PROGRESSIVE MULTIFOCAL LEUKOENCEPHALOPATHY; PROTEIN EXPRESSION; UPREGULATION; VERY ELDERLY; WHITE MATTER LESION; ACUTE DISEASE; BRAIN; CELL DEATH; CELL NUCLEUS; COHORT ANALYSIS; METABOLISM; NERVE CELL; NERVE DEGENERATION; PATHOLOGY; PHYSIOLOGY; WHITE MATTER;

ACUTE DISEASE; ADULT; AGED; AGED, 80 AND OVER; BRAIN; CELL DEATH; CELL NUCLEUS; COHORT STUDIES; FEMALE; HUMANS; MALE; MICROARRAY ANALYSIS; MIDDLE AGED; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; NERVE DEGENERATION; NEURONS; NF-E2-RELATED FACTOR 2; OLIGODENDROGLIA; OXIDATIVE STRESS; WHITE MATTER;

EID: 84937812498     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-015-1452-x     Document Type: Article

References (46)

1. Barnett MH, Prineas JW (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 55:458–468. doi:10.1002/ana.20016
2. Bauer J, Elger CE, Hans VH, Schramm J, Urbach H, Lassmann H, Bien CG (2007) Astrocytes are a specific immunological target in Rasmussen’s encephalitis. Ann Neurol 62:67–80. doi:10.1002/ana.21148
3. Bell KF, Al-Mubarak B, Martel MA, McKay S, Wheelan N, Hasel P, Markus NM, Baxter P, Deighton RF, Serio A, Bilican B, Chowdhry S, Meakin PJ, Ashford ML, Wyllie DJ, Scannevin RH, Chandran S, Hayes JD, Hardingham GE (2015) Neuronal development is promoted by weakened intrinsic antioxidant defences due to epigenetic repression of Nrf2. Nat Commun 6:7066. doi:10.1038/ncomms8066
4. Bizzozero OA, DeJesus G, Callahan K, Pastuszyn A (2005) Elevated protein carbonylation in the brain white matter and gray matter of patients with multiple sclerosis. J Neurosci Res 81:687–695. doi:10.1002/jnr.20587
5. Bruck W, Porada P, Poser S, Rieckmann P, Hanefeld F, Kretzschmar HA, Lassmann H (1995) Monocyte/macrophage differentiation in early multiple sclerosis lesions. Ann Neurol 38:788–796. doi:10.1002/ana.410380514
6. Burdo J, Schubert D, Maher P (2008) Glutathione production is regulated via distinct pathways in stressed and non-stressed cortical neurons. Brain Res 1189:12–22. doi:10.1016/j.brainres.2007.10.077
7. Calabrese M, Poretto V, Favaretto A, Alessio S, Bernardi V, Romualdi C, Rinaldi F, Perini P, Gallo P (2012) Cortical lesion load associates with progression of disability in multiple sclerosis. Brain 135:2952–2961. doi:10.1093/brain/aws246
8. Campbell GR, Mahad DJ (2011) Mitochondria as crucial players in demyelinated axons: lessons from neuropathology and experimental demyelination. Autoimmune Dis 2011:262847. doi:10.4061/2011/262847
9. Chorley BN, Campbell MR, Wang X, Karaca M, Sambandan D, Bangura F, Xue P, Pi J, Kleeberger SR, Bell DA (2012) Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoid X receptor alpha. Nucleic Acids Res 40:7416–7429. doi:10.1093/nar/gks409
10. Cordova EJ, Martinez-Hernandez A, Uribe-Figueroa L, Centeno F, Morales-Marin M, Koneru H, Coleman MA, Orozco L (2014) The NRF2-KEAP1 pathway is an early responsive gene network in arsenic exposed lymphoblastoid cells. PLoS One 9:e88069. doi:10.1371/journal.pone.0088069
11. de Vries HE, Witte M, Hondius D, Rozemuller AJ, Drukarch B, Hoozemans J, van Horssen J (2008) Nrf2-induced antioxidant protection: a promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med 45:1375–1383. doi:10.1016/j.freeradbiomed.2008.09.001
12. Eftekharpour E, Holmgren A, Juurlink BH (2000) Thioredoxin reductase and glutathione synthesis is upregulated by t-butylhydroquinone in cortical astrocytes but not in cortical neurons. Glia 31:241–248
13. Eshaghi A, Bodini B, Ridgway GR, Garcia-Lorenzo D, Tozer DJ, Sahraian MA, Thompson AJ, Ciccarelli O (2014) Temporal and spatial evolution of grey matter atrophy in primary progressive multiple sclerosis. Neuroimage 86:257–264. doi:10.1016/j.neuroimage.2013.09.059
14. Fischer MT, Sharma R, Lim JL, Haider L, Frischer JM, Drexhage J, Mahad D, Bradl M, van Horssen J, Lassmann H (2012) NADPH oxidase expression in active multiple sclerosis lesions in relation to oxidative tissue damage and mitochondrial injury. Brain 135:886–899. doi:10.1093/brain/aws012
15. Fischer MT, Wimmer I, Hoftberger R, Gerlach S, Haider L, Zrzavy T, Hametner S, Mahad D, Binder CJ, Krumbholz M, Bauer J, Bradl M, Lassmann H (2013) Disease-specific molecular events in cortical multiple sclerosis lesions. Brain 136:1799–1815. doi:10.1093/brain/awt110
16. Fox RJ, Miller DH, Phillips JT, Hutchinson M, Havrdova E, Kita M, Yang M, Raghupathi K, Novas M, Sweetser MT, Viglietta V, Dawson KT (2012) Placebo-controlled phase 3 study of oral BG-12 or glatiramer in multiple sclerosis. N Engl J Med 367:1087–1097. doi:10.1056/NEJMoa1206328
17. Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, Schmidbauer M, Laursen H, Sorensen PS, Lassmann H (2009) The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 132:1175–1189. doi:10.1093/brain/awp070
18. Gold R, Kappos L, Arnold DL, Bar-Or A, Giovannoni G, Selmaj K, Tornatore C, Sweetser MT, Yang M, Sheikh SI, Dawson KT (2012) Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N Engl J Med 367:1098–1107. doi:10.1056/NEJMoa1114287
19. Gold R, Schmied M, Giegerich G, Breitschopf H, Hartung HP, Toyka KV, Lassmann H (1994) Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab Invest 71:219–225
20. Gray E, Thomas TL, Betmouni S, Scolding N, Love S (2008) Elevated myeloperoxidase activity in white matter in multiple sclerosis. Neurosci Lett 444:195–198. doi:10.1016/j.neulet.2008.08.035
21. Haider L, Fischer MT, Frischer JM, Bauer J, Hoftberger R, Botond G, Esterbauer H, Binder CJ, Witztum JL, Lassmann H (2011) Oxidative damage in multiple sclerosis lesions. Brain 134:1914–1924. doi:10.1093/brain/awr128
22. Hametner S, Wimmer I, Haider L, Pfeifenbring S, Bruck W, Lassmann H (2013) Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol 74:848–861. doi:10.1002/ana.23974
23. Hoftberger R, Fink S, Aboul-Enein F, Botond G, Olah J, Berki T, Ovadi J, Lassmann H, Budka H, Kovacs GG (2010) Tubulin polymerization promoting protein (TPPP/p25) as a marker for oligodendroglial changes in multiple sclerosis. Glia 58:1847–1857. doi:10.1002/glia.21054
24. Johnson DA, Amirahmadi S, Ward C, Fabry Z, Johnson JA (2010) The absence of the pro-antioxidant transcription factor Nrf2 exacerbates experimental autoimmune encephalomyelitis. Toxicol Sci 114:237–246. doi:10.1093/toxsci/kfp274
25. King G, Payne S, Walker F, Murray GI (1997) A highly sensitive detection method for immunohistochemistry using biotinylated tyramine. J Pathol 183:237–241. doi:10.1002/(SICI)1096-9896(199710)183:2<237:AID-PATH893>3.0.CO;2-0
26. Lassmann H (2011) Review: the architecture of inflammatory demyelinating lesions: implications for studies on pathogenesis. Neuropathol Appl Neurobiol 37:698–710. doi:10.1111/j.1365-2990.2011.01189.x
27. Lassmann H, van Horssen J (2011) The molecular basis of neurodegeneration in multiple sclerosis. FEBS Lett 585:3715–3723. doi:10.1016/j.febslet.2011.08.004
28. Linker RA, Lee DH, Ryan S, van Dam AM, Conrad R, Bista P, Zeng W, Hronowsky X, Buko A, Chollate S, Ellrichmann G, Bruck W, Dawson K, Goelz S, Wiese S, Scannevin RH, Lukashev M, Gold R (2011) Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain 134:678–692. doi:10.1093/brain/awq386
29. Mahad D, Ziabreva I, Lassmann H, Turnbull D (2008) Mitochondrial defects in acute multiple sclerosis lesions. Brain 131:1722–1735. doi:10.1093/brain/awn105
30. Mahad DH, Trapp BD, Lassmann H (2015) Pathological mechanisms in progressive multiple sclerosis. Lancet Neurol 14:183–193. doi:10.1016/S1474-4422(14)70256-X
31. Metz I, Traffehn S, Strassburger-Krogias K, Keyvani K, Bergmann M, Nolte K, Weber MS, Bartsch T, Gold R, Bruck W (2015) Glial cells express nuclear nrf2 after fumarate treatment for multiple sclerosis and psoriasis. Neurol Neuroimmunol Neuroinflamm 2:e99. doi:10.1212/nxi.0000000000000099
32. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13. doi:10.1042/BJ20081386
33. Nijland PG, Witte ME, van het Hof B, van der Pol S, Bauer J, Lassmann H, van der Valk P, de Vries HE, van Horssen J (2014) Astroglial PGC-1alpha increases mitochondrial antioxidant capacity and suppresses inflammation: implications for multiple sclerosis. Acta Neuropathol Commun 2:170. doi:10.1186/s40478-014-0170-2
34. Palinski W, Horkko S, Miller E, Steinbrecher UP, Powell HC, Curtiss LK, Witztum JL (1996) Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J Clin Invest 98:800–814. doi:10.1172/JCI118853
35. Parodi B, Rossi S, Morando S, Cordano C, Bragoni A, Motta C, Usai C, Wipke BT, Scannevin RH, Mancardi GL, Centonze D, Kerlero de Rosbo N, Uccelli A (2015) Fumarates modulate microglia activation through a novel HCAR2 signaling pathway and rescue synaptic dysregulation in inflamed CNS. Acta Neuropathol. doi:10.1007/s00401-015-1422-3
36. Ramsey CP, Glass CA, Montgomery MB, Lindl KA, Ritson GP, Chia LA, Hamilton RL, Chu CT, Jordan-Sciutto KL (2007) Expression of Nrf2 in neurodegenerative diseases. J Neuropathol Exp Neurol 66:75–85. doi:10.1097/nen.0b013e31802d6da9
37. Scannevin RH, Chollate S, Jung MY, Shackett M, Patel H, Bista P, Zeng W, Ryan S, Yamamoto M, Lukashev M, Rhodes KJ (2012) Fumarates promote cytoprotection of central nervous system cells against oxidative stress via the nuclear factor (erythroid-derived 2)-like 2 pathway. J Pharmacol Exp Ther 341:274–284. doi:10.1124/jpet.111.190132
38. Schilling S, Goelz S, Linker R, Luehder F, Gold R (2006) Fumaric acid esters are effective in chronic experimental autoimmune encephalomyelitis and suppress macrophage infiltration. Clin Exp Immunol 145:101–107. doi:10.1111/j.1365-2249.2006.03094.x
39. Schreibelt G, van Horssen J, van Rossum S, Dijkstra CD, Drukarch B, de Vries HE (2007) Therapeutic potential and biological role of endogenous antioxidant enzymes in multiple sclerosis pathology. Brain Res Rev 56:322–330. doi:10.1016/j.brainresrev.2007.07.005
40. Stahnke T, Richter-Landsberg C, Stadelmann C, Netzler A, Brück W (2007) Differential upregulation of heme oxygenase-1 (HSP32) in glial cells after oxidative stress and in demyelinating disorders. J Mol Neurosci 32:25–37. doi:10.1007/s12031-007-0005-8
41. van Horssen J, Drexhage JA, Flor T, Gerritsen W, van der Valk P, de Vries HE (2010) Nrf2 and DJ1 are consistently upregulated in inflammatory multiple sclerosis lesions. Free Radic Biol Med 49:1283–1289. doi:10.1016/j.freeradbiomed.2010.07.013
42. van Horssen J, Schreibelt G, Bo L, Montagne L, Drukarch B, van Muiswinkel FL, de Vries HE (2006) NAD(P)H:quinone oxidoreductase 1 expression in multiple sclerosis lesions. Free Radic Biol Med 41:311–317. doi:10.1016/j.freeradbiomed.2006.04.013
43. van Horssen J, Schreibelt G, Drexhage J, Hazes T, Dijkstra CD, van der Valk P, de Vries HE (2008) Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 45:1729–1737. doi:10.1016/j.freeradbiomed.2008.09.023
44. Veto S, Acs P, Bauer J, Lassmann H, Berente Z, Setalo G Jr, Borgulya G, Sumegi B, Komoly S, Gallyas F Jr, Illes Z (2010) Inhibiting poly(ADP-ribose) polymerase: a potential therapy against oligodendrocyte death. Brain 133:822–834. doi:10.1093/brain/awp337
45. Witte ME, Nijland PG, Drexhage JA, Gerritsen W, Geerts D, van Het Hof B, Reijerkerk A, de Vries HE, van der Valk P, van Horssen J (2013) Reduced expression of PGC-1alpha partly underlies mitochondrial changes and correlates with neuronal loss in multiple sclerosis cortex. Acta Neuropathol 125:231–243. doi:10.1007/s00401-012-1052-y
46. Zucker SN, Fink EE, Bagati A, Mannava S, Bianchi-Smiraglia A, Bogner PN, Wawrzyniak JA, Foley C, Leonova KI, Grimm MJ, Moparthy K, Ionov Y, Wang J, Liu S, Sexton S, Kandel ES, Bakin AV, Zhang Y, Kaminski N, Segal BH, Nikiforov MA (2014) Nrf2 amplifies oxidative stress via induction of Klf9. Mol Cell 53:916–928. doi:10.1016/j.molcel.2014.01.033