Potential for cell-mediated immune responses in mouse models of Pelizaeus-Merzbacher disease

Brain Sciences

Volumn 3, Issue 4, 2013, Pages 1417-1444

  Southwood, Cherie M ^a   Fykkolodziej, Bozena ^a   Dachet, Fabien ^a   Gow, Alexander ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chemokines; Cytokines; Lymphoid; Microarrays; Myelin synthesis deficient; Myeloid; Rumpshaker

Indexed keywords

BETA 2 MICROGLOBULIN; CATALASE; CD68 ANTIGEN; FC RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN G; INTERCELLULAR ADHESION MOLECULE 1; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MYELIN BASIC PROTEIN; PEROXIREDOXIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SIALOADHESIN; SUCCINATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 3;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOFLUORESCENCE IMAGING; BIOINFORMATICS; CASE REPORT; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; MACROPHAGE; MALE; METABOLIC STRESS; MICROARRAY ANALYSIS; MICROGLIA; MISSENSE MUTATION; MOUSE; NONHUMAN; NORTHERN BLOTTING; OLIGODENDROGLIA; OXIDATIVE STRESS; PELIZAEUS MERZBACHER DISEASE; POLYMERASE CHAIN REACTION; UNFOLDED PROTEIN RESPONSE;

EID: 84963933446     PISSN: None     EISSN: 20763425     Source Type: Journal    
DOI: 10.3390/brainsci3041417     Document Type: Article

References (79)

1. Glass, C.K.; Saijo, K.; Winner, B.; Marchetto, M.C.; Gage, F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140, 918-934.
2. Frank-Cannon, T.C.; Alto, L.T.; McAlpine, F.E.; Tansey, M.G. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol. Neurodegener. 2009, 4, doi:10.1186/1750-1326-4-47.
3. Block, M.L.; Hong, J.S. Microglia and inflammation-mediated neurodegeneration: Multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76, 77-98.
4. Merson, T.D.; Binder, M.D.; Kilpatrick, T.J. Role of cytokines as mediators and regulators of microglial activity in inflammatory demyelination of the CNS. Neuromol. Med. 2010, 12, 99-132.
5. Napoli, I.; Neumann, H. Protective effects of microglia in multiple sclerosis. Exp. Neurol. 2009, 225, 24-28.
6. Van Noort, J.M.; van den Elsen, P.J.; van Horssen, J.; Geurts, J.J.; van der Valk, P.; Amor, S. Preactive multiple sclerosis lesions offer novel clues for neuroprotective therapeutic strategies. CNS Neurol. Disord. Drug Targets 2011, 10, 68-81.
7. Gow, A.; Sharma, R. The unfolded protein response in protein aggregating diseases. Neuromol. Med. 2003, 4, 73-94.
8. Gow, A.; Friedrich, V.L.; Lazzarini, R.A. Many naturally occurring mutations of myelin proteolipid protein impair its intracellular transport. J. Neurosci. Res. 1994, 37, 574-583.
9. Gow, A.; Lazzarini, R.A. A cellular mechanism governing the severity of Pelizaeus-Merzbacher disease. Nat. Genet. 1996, 13, 422-428.
10. Barrie, J.A.; Montague, P.; Karim, S.; Kirkham, D.; Nave, K.A.; Anderson, T.J.; Griffiths, I.R.; McLaughlin, M. Modulation of rumpshaker phenotype with wild-type PLP/DM20 suggests several pathogenic mechanisms. J. Neurosci. Res. 2010, 88, 2135-2145.
11. Matus, S.; Lisbona, F.; Torres, M.; Leon, C.; Thielen, P.; Hetz, C. The stress rheostat: An interplay between the unfolded protein response (UPR) and autophagy in neurodegeneration. Curr. Mol. Med. 2008, 8, 157-172.
12. Gow, A.; Wrabetz, L. CHOP and the endoplasmic reticulum stress response in myelinating glia. Curr. Opin. Neurobiol. 2009, 19, 1-6.
13. Lin, W.; Popko, B. Endoplasmic reticulum stress in disorders of myelinating cells. Nat. Neurosci. 2009, 12, 379-385.
14. Katayama, T.; Imaizumi, K.; Manabe, T.; Hitomi, J.; Kudo, T.; Tohyama, M. Induction of neuronal death by ER stress in Alzheimer's disease. J. Chem. Neuroanat. 2004, 28, 67-78.
15. Paschen, W.; Mengesdorf, T. Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium 2005, 38, 409-415.
16. Salminen, A.; Kauppinen, A.; Suuronen, T.; Kaarniranta, K.; Ojala, J. ER stress in Alzheimer's disease: A novel neuronal trigger for inflammation and Alzheimer's pathology. J. Neuroinflamm. 2009, 6, 41-53.
17. Uehara, T. Accumulation of misfolded protein through nitrosative stress linked to neurodegenerative disorders. Antioxid. Redox Signal. 2007, 9, 597-601.
18. Wang, H.Q.; Takahashi, R. Expanding insights on the involvement of endoplasmic reticulum stress in Parkinson's disease. Antioxid. Redox Signal. 2007, 9, 553-561.
19. Southwood, C.M.; Garbern, J.; Jiang, W.; Gow, A. The unfolded protein response modulates disease severity in Pelizaeus-Merzbacher disease. Neuron 2002, 36, 585-596.
20. Gow, A.; Southwood, C.M.; Lazzarini, R.A. Disrupted proteolipid protein trafficking results in oligodendrocyte apoptosis in an animal model of Pelizaeus-Merzbacher disease. J. Cell Biol. 1998, 140, 925-934.
21. Gow, A. Protein Misfolding as a Disease Determinant. In Myelin Biology and Disorders; Lazzarini, R.A., Ed.; Elsevier: Amsterdam, The Netherlands, 2004; Volume 1, pp. 877-885.
22. Tatar, C.L.; Appikatla, S.; Bessert, D.A.; Paintlia, A.S.; Singh, I.; Skoff, R.P. Increased Plp1 gene expression leads to massive microglial cell activation and inflammation throughout the brain. ASN Neuro 2010, 2, e00043.
23. Lin, W.; Kemper, A.; Dupree, J.L.; Harding, H.P.; Ron, D.; Popko, B. Interferon-γ inhibits central nervous system remyelination through a process modulated by endoplasmic reticulum stress. Brain 2006, 129, 1306-1318.
24. Southwood, C.M.; Gow, A. Molecular mechanisms of disease stemming from mutations in the proteolipid protein gene. Microsc. Res. Tech. 2001, 52, 700-708.
25. Zhang, K.; Kaufman, R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008, 454, 455-462.
26. Deng, J.; Lu, P.D.; Zhang, Y.; Scheuner, D.; Kaufman, R.J.; Sonenberg, N.; Harding, H.P.; Ron, D. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 2004, 24, 10161-10168.
27. Pahl, H.L.; Baeuerle, P.A. Activation of NF-κB by ER stress requires both Ca2+ and reactive oxygen intermediates as messengers. FEBS Lett. 1996, 392, 129-136.
28. Urano, F.; Wang, X.; Bertolotti, A.; Zhang, Y.; Chung, P.; Harding, H.P.; Ron, D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287, 664-666.
29. Wu, S.; Tan, M.; Hu, Y.; Wang, J.L.; Scheuner, D.; Kaufman, R.J. Ultraviolet light activates NFkappaB through translational inhibition of IkappaBα synthesis. J. Biol. Chem. 2004, 279, 34898-34902.
30. Zhang, K.; Shen, X.; Wu, J.; Sakaki, K.; Saunders, T.; Rutkowski, D.T.; Back, S.H.; Kaufman, R.J. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 2006, 124, 587-599.
31. Lin, W.; Bailey, S.L.; Ho, H.; Harding, H.P.; Ron, D.; Miller, S.D.; Popko, B. The integrated stress response prevents demyelination by protecting oligodendrocytes against immune-mediated damage. J. Clin. Invest. 2007, 117, 448-456.
32. Leder, C.; Schwab, N.; Ip, C.W.; Kroner, A.; Nave, K.A.; Dornmair, K.; Martini, R.; Wiendl, H. Clonal expansions of pathogenic CD8+ effector cells in the CNS of myelin mutant mice. Mol. Cell. Neurosci. 2007, 36, 416-424.
33. Lin, W.; Harding, H.P.; Ron, D.; Popko, B. Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-gamma. J. Cell Biol. 2005, 169, 603-612.
34. Kettenmann, H.; Hanisch, U.K.; Noda, M.; Verkhratsky, A. Physiology of microglia. Physiol. Rev. 2011, 91, 461-553.
35. Kreutzberg, G.W. Microglia: A sensor for pathological events in the CNS. Trends Neurosci. 1996, 19, 312-318.
36. Ramprasad, M.P.; Terpstra, V.; Kondratenko, N.; Quehenberger, O.; Steinberg, D. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 1996, 93, 14833-14838.
37. Deininger, M.H.; Pater, S.; Strik, H.; Meyermann, R. Macrophage/microglial cell subpopulations in glioblastoma multiforme relapses are differentially altered by radiochemotherapy. J. Neurooncol. 2001, 55, 141-147.
38. Caffo, M.; Caruso, G.; Germano, A.; Galatioto, S.; Meli, F.; Tomasello, F. CD68 and CR3/43 immunohistochemical expression in secretory meningiomas. Neurosurgery 2005, 57, 551-557.
39. Al-Saktawi, K.; McLaughlin, M.; Klugmann, M.; Schneider, A.; Barrie, J.A.; McCulloch, M.C.; Montague, P.; Kirkham, D.; Nave, K.A.; Griffiths, I.R. Genetic background determines phenotypic severity of the Plp rumpshaker mutation. J. Neurosci. Res. 2003, 72, 12-24.
40. Fanarraga, M.L.; Sommer, I.U.; Griffiths, I.R.; Montague, P.; Groome, N.P.; Nave, K.A.; Schneider, A.; Brophy, P.J.; Kennedy, P.G. Oligodendrocyte development and differentiation in the rumpshaker mutation. Glia 1993, 9, 146-156.
41. Gardinier, M.V.; Macklin, W.B. Myelin proteolipid protein gene expression in jimpy and jimpy (msd) mice. J. Neurochem. 1988, 51, 360-369.
42. Huang, D.W.; Sherman, B.T.; Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4, 44-57.
43. Amadou, C.; Kumanovics, A.; Jones, E.P.; Lambracht-Washington, D.; Yoshino, M.; Lindahl, K.F. The mouse major histocompatibility complex: Some assembly required. Immunol. Rev. 1999, 167, 211-221.
44. Kruger, E.; Kloetzel, P.M. Immunoproteasomes at the interface of innate and adaptive immune responses: Two faces of one enzyme. Curr. Opin. Immunol. 2012, 24, 77-83.
45. Jang, E.; Lee, S.; Kim, J.H.; Kim, J.H.; Seo, J.W.; Lee, W.H.; Mori, K.; Nakao, K.; Suk, K. Secreted protein lipocalin-2 promotes microglial M1 polarization. FASEB J. 2013, 27, 1176-1190.
46. Glass, W.G.; Hickey, M.J.; Hardison, J.L.; Liu, M.T.; Manning, J.E.; Lane, T.E. Antibody targeting of the CC chemokine ligand 5 results in diminished leukocyte infiltration into the central nervous system and reduced neurologic disease in a viral model of multiple sclerosis. J. Immunol. 2004, 172, 4018-4025.
47. Coles, A.J.; Twyman, C.L.; Arnold, D.L.; Cohen, J.A.; Confavreux, C.; Fox, E.J.; Hartung, H.P.; Havrdova, E.; Selmaj, K.W.; Weiner, H.L.; et al. Alemtuzumab for patients with relapsing multiple sclerosis after disease-modifying therapy: A randomised controlled phase 3 trial. Lancet 2012, 380, 1829-1839.
48. Ip, C.W.; Kroner, A.; Crocker, P.R.; Nave, K.A.; Martini, R. Sialoadhesin deficiency ameliorates myelin degeneration and axonopathic changes in the CNS of PLP overexpressing mice. Neurobiol. Dis. 2007, 25, 105-111.
49. Ip, C.W.; Kroner, A.; Groh, J.; Huber, M.; Klein, D.; Spahn, I.; Diem, R.; Williams, S.K.; Nave, K.A.; Edgar, J.M.; et al. Neuroinflammation by cytotoxic T-lymphocytes impairs retrograde axonal transport in an oligodendrocyte mutant mouse. PLoS One 2012, 7, e42554.
50. Mitchell, L.S.; Gillespie, S.C.; McAllister, F.; Fanarraga, M.L.; Kirkham, D.; Kelly, B.; Brophy, P.J.; Griffiths, I.R.; Montague, P.; Kennedy, P.G. Developmental expression of major myelin protein genes in the CNS of X-linked hypomyelinating mutant rumpshaker. J. Neurosci. Res. 1992, 33, 205-217.
51. Gibson, G.E.; Blass, J.P.; Beal, M.F.; Bunik, V. The α-ketoglutarate-dehydrogenase complex: A mediator between mitochondria and oxidative stress in neurodegeneration. Mol. Neurobiol. 2005, 31, 43-63.
52. Scarpulla, R.C.; Vega, R.B.; Kelly, D.P. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol. Metab. 2012, 23, 459-466.
53. Katsuoka, F.; Motohashi, H.; Engel, J.D.; Yamamoto, M. Nrf2 transcriptionally activates the mafG gene through an antioxidant response element. J. Biol. Chem. 2005, 280, 4483-4490.
54. Sorce, S.; Krause, K.H.; Jaquet, V. Targeting NOX enzymes in the central nervous system: Therapeutic opportunities. Cell. Mol. Life Sci. 2012, 69, 2387-2407.
55. Joshi, G.; Johnson, J.A. The Nrf2-ARE pathway: A valuable therapeutic target for the treatment of neurodegenerative diseases. Recent Pat. CNS Drug Discov. 2012, 7, 218-229.
56. Zhang, M.; An, C.; Gao, Y.; Leak, R.K.; Chen, J.; Zhang, F. Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Prog. Neurobiol. 2013, 100, 30-47.
57. Melo, A.; Monteiro, L.; Lima, R.M.; Oliveira, D.M.; Cerqueira, M.D.; El-Bacha, R.S. Oxidative stress in neurodegenerative diseases: Mechanisms and therapeutic perspectives. Oxid. Med. Cell. Longev. 2011, 2011, e467180.
58. Ienco, E.C.; LoGerfo, A.; Carlesi, C.; Orsucci, D.; Ricci, G.; Mancuso, M.; Siciliano, G. Oxidative stress treatment for clinical trials in neurodegenerative diseases. J. Alzheimers Dis. 2011, 24, 111-126.
59. Ghandour, M.; Skoff, R. Expression of galactocerebroside in developing normal and jimpy oligodendrocytes in situ. J. Neurocytol. 1988, 17, 485-498.
60. Rutkowski, D.T.; Wu, J.; Back, S.H.; Callaghan, M.U.; Ferris, S.P.; Iqbal, J.; Clark, R.; Miao, H.; Hassler, J.R.; Fornek, J.; et al. UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev. Cell 2008, 15, 829-840.
61. Ozcan, U.; Cao, Q.; Yilmaz, E.; Lee, A.H.; Iwakoshi, N.N.; Ozdelen, E.; Tuncman, G.; Gorgun, C.; Glimcher, L.H.; Hotamisligil, G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306, 457-461.
62. Schroder, M.; Kaufman, R.J. Divergent roles of IRE1α and PERK in the unfolded protein response. Curr. Mol. Med. 2006, 6, 5-36.
63. Cunnea, P.; Mhaille, A.N.; McQuaid, S.; Farrell, M.; McMahon, J.; FitzGerald, U. Expression profiles of endoplasmic reticulum stress-related molecules in demyelinating lesions and multiple sclerosis. Mult. Scler. 2011, 17, 808-818.
64. Gorman, M.P.; Golomb, M.R.; Walsh, L.E.; Hobson, G.M.; Garbern, J.Y.; Kinkel, R.P.; Darras, B.T.; Urion, D.K.; Eksioglu, Y.Z. Steroid-responsive neurologic relapses in a child with a proteolipid protein-1 mutation. Neurology 2007, 68, 1305-1307.
65. Warshawsky, I.; Rudick, R.A.; Staugaitis, S.M.; Natowicz, M.R. Primary progressive multiple sclerosis as a phenotype of a PLP1 gene mutation. Ann. Neurol. 2005, 58, 470-473.
66. Grundtner, R.; Dornmair, K.; Dahm, R.; Flugel, A.; Kawakami, N.; Zeitelhofer, M.; Schoderboeck, L.; Nosov, M.; Selzer, E.; Willheim, M.; et al. Transition from enhanced T cell infiltration to inflammation in the myelin-degenerative central nervous system. Neurobiol. Dis. 2007, 28, 261-275.
67. Kim, B.; Jeong, H.K.; Kim, J.H.; Lee, S.Y.; Jou, I.; Joe, E.H. Uridine 5-diphosphate induces chemokine expression in microglia and astrocytes through activation of the P2Y6 receptor. J. Immunol. 2011, 186, 3701-3709.
68. Vela, J.M.; Dalmau, I.; Acarin, L.; Gonzalez, B.; Castellano, B. Microglial cell reaction in the gray and white matter in spinal cords from jimpy mice. An enzyme histochemical study at the light and electron microscope level. Brain Res. 1995, 694, 287-298.
69. Wolf, M.K.; Kardon, G.B.; Adcock, L.H.; Billings-Gagliardi, S. Hypomyelinated mutant mice. V. Relationship between jp and jpmsd re-examined on identical genetic backgrounds. Brain Res. 1983, 271, 121-129.
70. Colbert, R.A.; DeLay, M.L.; Klenk, E.I.; Layh-Schmitt, G. From HLA-B27 to spondyloarthritis: A journey through the ER. Immunol. Rev. 2010, 233, 181-202.
71. Nagaraju, K.; Casciola-Rosen, L.; Lundberg, I.; Rawat, R.; Cutting, S.; Thapliyal, R.; Chang, J.; Dwivedi, S.; Mitsak, M.; Chen, Y.W.; et al. Activation of the endoplasmic reticulum stress response in autoimmune myositis: Potential role in muscle fiber damage and dysfunction. Arthritis Rheum. 2005, 52, 1824-1835.
72. Nagaraju, K.; Raben, N.; Loeffler, L.; Parker, T.; Rochon, P.J.; Lee, E.; Danning, C.; Wada, R.; Thompson, C.; Bahtiyar, G.; et al. Conditional up-regulation of MHC class I in skeletal muscle leads to self-sustaining autoimmune myositis and myositis-specific autoantibodies. Proc. Natl. Acad. Sci. USA 2000, 97, 9209-9214.
73. Schneider, A.; Montague, P.; Griffiths, I.; Fanarraga, M.; Kennedy, P.; Brophy, P.; Nave, K.A. Uncoupling of hypomyelination and glial cell death by a mutation in the proteolipid protein gene. Nature 1992, 358, 758-761.
74. Gencic, S.; Hudson, L.D. Conservative amino acid substitution in the myelin proteolipid protein of jimpymsd mice. J. Neurosci. 1990, 10, 117-124.
75. Kobayashi, H.; Hoffman, E.P.; Marks, H.G. The rumpshaker mutation in spastic paraplegia. Nat. Genet. 1994, 7, 351-352.
76. Yamamoto, T.; Nanba, E.; Zhang, H.; Sasaki, M.; Komaki, H.; Takeshita, K. Jimpymsd mouse mutation and connatal Pelizaeus-Merzbacher disease. Am. J. Med. Genet. 1998, 75, 439-440.
77. Readhead, C.; Schneider, A.; Griffiths, I.R.; Nave, K.A. Premature arrest of myelin formation in transgenic mice with increased proteolipid protein gene dosage. Neuron 1994, 12, 583-595.
78. Sharma, R.; Jiang, H.; Zhong, L.; Tseng, J.; Gow, A. Minimal role for activating transcription factor 3 in the oligodendrocyte unfolded protein response in vivo. J. Neurochem. 2007, 102, 1703-1712.
79. Chirgwin, J.M.; Przybyla, A.E.; MacDonald, R.J.; Rutter, W.J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 1979, 18, 5294-5299.