PERK activation preserves the viability and function of remyelinating oligodendrocytes in immune-mediated demyelinating diseases

American Journal of Pathology

Volumn 184, Issue 2, 2014, Pages 507-519

  Lin, Yifeng ^a,b   Huang, Guangcun ^a,b   Jamison, Stephanie ^a,b   Li, Jin ^c   Harding, Heather P ^d   Ron, David ^d   Lin, Wensheng ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CUPRIZONE; GAMMA INTERFERON; MYELIN; PANCREATIC ENDOPLASMIC RETICULUM KINASE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DEMYELINATING DISEASE; DEMYELINATION; ENZYME ACTIVATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNE RESPONSE; MALE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REMYELINIZATION; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; AXONS; CELL DEATH; CELL SURVIVAL; CUPRIZONE; CYTOPROTECTION; DEMYELINATING DISEASES; EIF-2 KINASE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME ACTIVATION; INFLAMMATION; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MYELIN SHEATH; OLIGODENDROGLIA; SIGNAL TRANSDUCTION; TACROLIMUS; TREMOR;

EID: 84892179950     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.10.009     Document Type: Article

References (58)

1. R.J. Franklin, and C. Ffrench-Constant Remyelination in the CNS: from biology to therapy Nat Rev Neurosci 9 2008 839 855
2. M.R. Kotter, C. Stadelmann, and H.P. Hartung Enhancing remyelination in disease-can we wrap it up? Brain 134 2011 1882 1900
3. K. Zhang, and R.J. Kaufman From endoplasmic-reticulum stress to the inflammatory response Nature 454 2008 455 462
4. W. Lin, and B. Popko Endoplasmic reticulum stress in disorders of myelinating cells Nat Neurosci 12 2009 379 385
5. G.S. Hotamisligil Endoplasmic reticulum stress and the inflammatory basis of metabolic disease Cell 140 2010 900 917
6. I. Tabas, and D. Ron Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress Nat Cell Biol 13 2011 184 190
7. C. Hetz The unfolded protein response: controlling cell fate decisions under ER stress and beyond Nat Rev Mol Cell Biol 13 2012 89 102
8. W. Lin, S.L. Bailey, H. Ho, H.P. Harding, D. Ron, S.D. Miller, and B. Popko The integrated stress response prevents demyelination by protecting oligodendrocytes against immune-mediated damage J Clin Invest 117 2007 448 456
9. A.N. Mháille, S. McQuaid, A. Windebank, P. Cunnea, J. McMahon, A. Samali, and U. FitzGerald Increased expression of endoplasmic reticulum stress-related signaling pathway molecules in multiple sclerosis lesions J Neuropathol Exp Neurol 67 2008 200 211
10. P. Cunnea, A.N. Mháille, S. McQuaid, M. Farrell, J. McMahon, and U. Fitzgerald Expression profiles of endoplasmic reticulum stress-related molecules in demyelinating lesions and multiple sclerosis Mult Scler 17 2011 808 818
11. W. Lin, Y. Lin, J. Li, A.G. Fenstermaker, W.S. Way, B. Clayton, S. Jamison, H.P. Harding, D. Ron, and B. Popko Oligodendrocyte-specific activation of PERK signaling protects mice against experimental autoimmune encephalomyelitis J Neurosci 33 2013 5980 5991
12. M. Bradl, and H. Lassmann Oligodendrocytes: biology and pathology Acta Neuropathol 119 2010 37 53
13. J.R. Lees, and A.H. Cross A little stress is good: IFN-gamma, demyelination, and multiple sclerosis J Clin Invest 117 2007 297 299
14. W. Lin, A. Kemper, J.L. Dupree, H.P. Harding, D. Ron, and B. Popko Interferon-gamma inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress Brain 129 2006 1306 1318
15. W. Lin, H.P. Harding, D. Ron, and B. Popko Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-gamma J Cell Biol 169 2005 603 612
16. W. Lin, A. Kemper, K.D. McCarthy, P. Pytel, J.P. Wang, I.L. Campbell, M.F. Utset, and B. Popko Interferon-gamma induced medulloblastoma in the developing cerebellum J Neurosci 24 2004 10074 10083
17. W. Lin, and Y. Lin Interferon-γ inhibits central nervous system myelination through both STAT1-dependent and STAT1-independent pathways J Neurosci Res 88 2010 2569 2577
18. W. Lin, P.E. Kunkler, H.P. Harding, D. Ron, R.P. Kraig, and B. Popko Enhanced integrated stress response promotes myelinating oligodendrocyte survival in response to interferon-gamma Am J Pathol 173 2008 1508 1517
19. R.L. Sidman, J.B. Abervine, and E.T. Pierce Atlas of the Mouse Brain and Spinal Cord 1971 Harvard University Press Cambridge
20. H.P. Harding, Y. Zhang, and D. Ron Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase Nature 397 1999 271 274
21. S.J. Marciniak, and D. Ron Endoplasmic reticulum stress signaling in disease Physiol Rev 86 2006 1133 1149
22. P.D. Lu, C. Jousse, S.J. Marciniak, Y. Zhang, I. Novoa, D. Scheuner, R.J. Kaufman, D. Ron, and H.P. Harding Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2 EMBO J 23 2004 169 179
23. B. Fuss, B. Mallon, T. Phan, C. Ohlemeyer, F. Kirchhoff, A. Nishiyama, and W.B. Macklin Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein Dev Biol 218 2000 259 274
24. B. Fuss, F.S. Afshari, R.J. Colello, and W.B. Macklin Normal CNS myelination in transgenic mice overexpressing MHC class I H-2L(d) in oligodendrocytes Mol Cell Neurosci 18 2001 221 234
25. N. Baumann, and D. Pham-Dinh Biology of oligodendrocyte and myelin in the mammalian central nervous system Physiol Rev 81 2001 871 927
26. H.P. Harding, I. Novoa, Y. Zhang, H. Zeng, R. Wek, M. Schapira, and D. Ron Regulated translation initiation controls stress-induced gene expression in mammalian cells Mol Cell 6 2000 1099 1108
27. L. Codarri, A. Fontana, and B. Becher Cytokine networks in multiple sclerosis: lost in translation Curr Opin Neurol 23 2010 205 211
28. B. Popko, and K.D. Baerwald Oligodendroglial response to the immune cytokine interferon gamma Neurochem Res 24 1999 331 338
29. J. Goverman Autoimmune T cell responses in the central nervous system Nat Rev Immunol 9 2009 393 407
30. C.W. Woo, D. Cui, J. Arellano, B. Dorweiler, H. Harding, K.A. Fitzgerald, D. Ron, and I. Tabas Adaptive suppression of the ATF4-CHOP branch of the unfolded protein response by toll-like receptor signalling Nat Cell Biol 11 2009 1473 1480
31. J.S. Chang, S. Ocvirk, E. Berger, S. Kisling, U. Binder, A. Skerra, A.S. Lee, and D. Haller Endoplasmic reticulum stress response promotes cytotoxic phenotype of CD8αβ+ intraepithelial lymphocytes in a mouse model for Crohn's disease-like ileitis J Immunol 189 2012 1510 1520
32. R.W. Alfa, M.H. Tuszynski, and A. Blesch A novel inducible tyrosine kinase receptor to regulate signal transduction and neurite outgrowth J Neurosci Res 87 2009 2624 2631
33. S.P. Fancy, J.R. Chan, S.E. Baranzini, R.J. Franklin, and D.H. Rowitch Myelin regeneration: a recapitulation of development? Annu Rev Neurosci 34 2011 21 43
34. G.K. Matsushima, and P. Morell The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system Brain Pathol 11 2001 107 116
35. A. Denic, A.J. Johnson, A.J. Bieber, A.E. Warrington, M. Rodriguez, and I. Pirko The relevance of animal models in multiple sclerosis research Pathophysiology 18 2011 21 29
36. B.J. van der Star, D.Y. Vogel, M. Kipp, F. Puentes, D. Baker, and S. Amor In vitro and in vivo models of multiple sclerosis CNS Neurol Disord Drug Targets 11 2012 570 588
37. A. Chakrabarty, M.M. Danley, and S.M. LeVine Immunohistochemical localization of phosphorylated protein kinase R and phosphorylated eukaryotic initiation factor-2 alpha in the central nervous system of SJL mice with experimental allergic encephalomyelitis J Neurosci Res 76 2004 822 833
38. M. Buntinx, P. Stinissen, P. Steels, M. Ameloot, and J. Raus Immune-mediated oligodendrocyte injury in multiple sclerosis: molecular mechanisms and therapeutic interventions Crit Rev Immunol 22 2002 391 424
39. J.W. Prineas, R.O. Barnard, E.E. Kwon, L.R. Sharer, and E.S. Cho Multiple sclerosis: remyelination of nascent lesions Ann Neurol 33 1993 137 151
40. B. Cannella, D. Pitt, E. Capello, and C.S. Raine Insulin-like growth factor-1 fails to enhance central nervous system myelin repair during autoimmune demyelination Am J Pathol 157 2000 933 943
41. C.N. Madhavarao, J.R. Moffett, R.A. Moore, R.E. Viola, M.A. Namboodiri, and D.M. Jacobowitz Immunohistochemical localization of aspartoacylase in the rat central nervous system J Comp Neurol 472 2004 318 329
42. G. Locatelli, S. Wörtge, T. Buch, B. Ingold, F. Frommer, B. Sobottka, M. Krüger, K. Karram, C. Bühlmann, I. Bechmann, F.L. Heppner, A. Waisman, and B. Becher Primary oligodendrocyte death does not elicit anti-CNS immunity Nat Neurosci 15 2012 543 550
43. V.O. Mallet, C. Mitchell, J.E. Guidotti, P. Jaffray, M. Fabre, D. Spencer, D. Arnoult, A. Kahn, and H. Gilgenkrantz Conditional cell ablation by tight control of caspase-3 dimerization in transgenic mice Nat Biotechnol 20 2002 1234 1239
44. T. Neff, P.A. Horn, V.E. Valli, A.M. Gown, S. Wardwell, B.L. Wood, C. von Kalle, M. Schmidt, L.J. Peterson, J.C. Morris, R.E. Richard, T. Clackson, H.P. Kiem, and C.A. Blau Pharmacologically regulated in vivo selection in a large animal Blood 100 2002 2026 2031
45. C.D. Steel, W.K. Kim, L.D. Sanford, L.L. Wellman, S. Burnett, N. Van Rooijen, and R.P. Ciavarra Distinct macrophage subpopulations regulate viral encephalitis but not viral clearance in the CNS J Neuroimmunol 226 2010 81 92
46. E.M. Frohman, M.K. Racke, and C.S. Raine Multiple sclerosis-the plaque and its pathogenesis N Engl J Med 354 2006 942 955
47. A. Gow, and L. Wrabetz CHOP and the endoplasmic reticulum stress response in myelinating glia Curr Opin Neurobiol 19 2009 505 510
48. C.M. Southwood, J. Garbern, W. Jiang, and A. Gow The unfolded protein response modulates disease severity in Pelizaeus-Merzbacher disease Neuron 36 2002 585 596
49. S.Z. Hasnain, R. Lourie, I. Das, A.C. Chen, and M.A. McGuckin The interplay between endoplasmic reticulum stress and inflammation Immunol Cell Biol 90 2012 260 270
50. S.E. Pfeiffer, A.E. Warrington, and R. Bansal The oligodendrocyte and its many cellular processes Trends Cell Biol 3 1993 191 197
51. G.C. Scheper, C.G. Proud, and M.S. van der Knaap Defective translation initiation causes vanishing of cerebral white matter Trends Mol Med 12 2006 159 166
52. M.S. van der Knaap, J.C. Pronk, and G.C. Scheper Vanishing white matter disease Lancet Neurol 5 2006 413 423
53. M. Bugiani, I. Boor, J.M. Powers, G.C. Scheper, and M.S. van der Knaap Leukoencephalopathy with vanishing white matter: a review J Neuropathol Exp Neurol 69 2010 987 996
54. C.G. Proud eIF2 and the control of cell physiology Semin Cell Dev Biol 16 2005 3 12
55. S.H. Burnett, E.J. Kershen, J. Zhang, L. Zeng, S.C. Straley, A.M. Kaplan, and D.A. Cohen Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene J Leukoc Biol 75 2004 612 623
56. H. Batoulis, M.S. Recks, K. Addicks, and S. Kuerten Experimental autoimmune encephalomyelitis-achievements and prospective advances APMIS 119 2011 819 830
57. B.D. Trapp, and K.A. Nave Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci 31 2008 247 269
58. J. Herz, F. Zipp, and V. Siffrin Neurodegeneration in autoimmune CNS inflammation Exp Neurol 225 2010 9 17