Animal models of MS reveal multiple roles of microglia in disease pathogenesis

Neurology Research International

Volumn 2011, Issue , 2011, Pages

  Gao, Zhen ^a   Tsirka, Stella E ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84865174013     PISSN: 20901852     EISSN: 20901860     Source Type: Journal    
DOI: 10.1155/2011/383087     Document Type: Review

References (87)

1. S. Dhib-Jalbut, "Pathogenesis of myelin/oligodendrocyte damage in multiple sclerosis," Neurology, vol. 68, no. 22, supplement 3, pp. S13-S54, 2007.
2. T. Holmoy and A. L. Hestvik, "Multiple sclerosis: immunopathogenesis and controversies in defining the cause," Current Opinion in Infectious Diseases, vol. 21, no. 3, pp. 271-278, 2008. (Pubitemid 351634399)
3. R. P. Lisak, "Neurodegeneration in multiple sclerosis: defining the problem," Neurology, vol. 68, no. 22, supplement 3, pp. S5-S12, 2007. (Pubitemid 46848606)
4. J. M. Fletcher, S. J. Lalor, C. M. Sweeney, N. Tubridy, and K. H. G. Mills, "T cells in multiple sclerosis and experimental autoimmune encephalomyelitis," Clinical and Experimental Immunology, vol. 162, no. 1, pp. 1-11, 2010.
5. D. Centonze, L. Muzio, S. Rossi et al., "Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis," Journal of Neuroscience, vol. 29, no. 11, pp. 3442-3452, 2009.
6. J.M. van Noort, P. J. van den Elsen, J. van Horssen, J. J. Geurts, P. van der Valk, and S. Amor, "Preactive multiple sclerosis lesions offer novel clues for neuroprotective therapeutic strategies," CNS & Neurological Disorders Drug Targets, vol. 10, no. 1, pp. 68-81, 2011.
7. P. M. Matthews, E. Pioro, S. Narayanan et al., "Assessment of lesion pathology in multiple sclerosis using quantitative MRI morphometry and magnetic resonance spectroscopy," Brain, vol. 119, no. 3, pp. 715-722, 1996. (Pubitemid 26237171)
8. D. Pitt, P. Werner, and C. S. Raine, "Glutamate excitotoxicity in a model of multiple sclerosis," Nature Medicine, vol. 6, no. 1, pp. 67-70, 2000. (Pubitemid 30048528)
9. M. H. Barnett and J. W. Prineas, "Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion," Annals of Neurology, vol. 55, no. 4, pp. 458-468, 2004. (Pubitemid 38391962)
10. B. Hemmer, J. J. Archelos, and H. P. Hartung, "New concepts in the immunopathogenesis of multiple sclerosis," Nature Reviews Neuroscience, vol. 3, no. 4, pp. 291-301, 2002. (Pubitemid 135706608)
11. S. Kuerten and D. N. Angelov, "Comparing the CNS morphology and immunobiology of different EAE models in C57BL/6 mice-a step towards understanding the complexity of multiple sclerosis," Annals of Anatomy, vol. 190, no. 1, pp. 1-15, 2008.
12. 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, vol. 18, no. 1, pp. 21-29, 2011.
13. E.M. Chastain,D. S. Duncan, J.M. Rodgers, and S. D.Miller, "The role of antigen presenting cells in multiple sclerosis," Biochimica et Biophysica Acta, vol. 1812, no. 2, pp. 265-274, 2011.
14. M. K. Matyszak and V. H. Perry, "Delayed-type hypersensitivity lesions in the central nervous system are prevented by inhibitors of matrix metalloproteinases," Journal of Neuroimmunology, vol. 69, no. 1-2, pp. 141-149, 1996. (Pubitemid 26305639)
15. O. Torkildsen, L. A. Brunborg, K.-M. Myhr, and L. Bo, "The cuprizone model for demyelination," Acta Neurologica Scandinavica, vol. 117, supplement 188, pp. 72-76, 2008. (Pubitemid 351606183)
16. W. F. Blakemore and R. J. M. Franklin, "Remyelination in experimental models of toxin-induced demyelination," Current Topics inMicrobiology and Immunology, vol. 318, pp. 193-212, 2008.
17. L. Steinman and S. S. Zamvil, "How to successfully apply animal studies in experimental allergic encephalomyelitis to research on multiple sclerosis," Annals of Neurology, vol. 60, no. 1, pp. 12-21, 2006.
18. N. Koning, B. M. J. Uitdehaag, I. Huitinga, and R. M. Hoek, "Restoring immune suppression in the multiple sclerosis brain," Progress in Neurobiology, vol. 89, no. 4, pp. 359-368, 2009.
19. N. Koning, L. Bö, R. M. Hoek, and I. Huitinga, "Downregulation of macrophage inhibitory molecules in multiple sclerosis lesions," Annals of Neurology, vol. 62, no. 5, pp. 504-514, 2007. (Pubitemid 350308775)
20. R. A. Farrell and G. Giovannoni, "Current and future role of interferon beta in the therapy of multiple sclerosis," Journal of Interferon and Cytokine Research, vol. 30, no. 10, pp. 715-726, 2010.
21. J. S.Wolinsky, "The use of glatiramer acetate in the treatment of multiple sclerosis," Advances in Neurology, vol. 98, pp. 273-292, 2006.
22. M. Bhasin, M. Wu, and S. E. Tsirka, "Modulation of microglial/ macrophage activation by macrophage inhibitory factor (TKP) or tuftsin (TKPR) attenuates the disease course of experimental autoimmune encephalomyelitis, " BMC Immunology, vol. 8, article 10, 2007.
23. U. K. Hanisch and H. Kettenmann, "Microglia: active sensor and versatile effector cells in the normal and pathologic brain," Nature Neuroscience, vol. 10, no. 11, pp. 1387-1394, 2007. (Pubitemid 350014685)
24. F. L. Heppner, M. Greter, D. Marino et al., "Experimental autoimmune encephalomyelitis repressed by microglial paralysis," Nature Medicine, vol. 11, no. 2, pp. 146-152, 2005. (Pubitemid 40321349)
25. I. Napoli and H. Neumann, "Protective effects of microglia in multiple sclerosis," Experimental Neurology, vol. 225, no. 1, pp. 24-28, 2010.
26. M. Prinz and A. Mildner, "Microglia in the CNS: immigrants from another world," Glia, vol. 59, no. 2, pp. 177-187, 2011.
27. N. Stence, M. Waite, and M. E. Dailey, "Dynamics of microglial activation: A confocal time-lapse analysis in hippocampal slices," Glia, vol. 33, no. 3, pp. 256-266, 2001. (Pubitemid 32219134)
28. K. A. Kigerl, J. C. Gensel, D. P. Ankeny, J. K. Alexander, D. J. Donnelly, and P. G. Popovich, "Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord," Journal of Neuroscience, vol. 29, no. 43, pp. 13435-13444, 2009.
29. J. Mikita, N. Dubourdieu-Cassagno, M. S. Deloire et al., "Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Amelioration of clinical status by M2 activated monocyte administration," Multiple Sclerosis, vol. 17, no. 1, pp. 2-15, 2011.
30. M. Wu and S. E. Tsirka, "Endothelial NOS-deficient mice reveal dual roles for nitric oxide during experimental autoimmune encephalomyelitis," Glia, vol. 57, no. 11, pp. 1204-1215, 2009.
31. Z. Zhang, Z. Y. Zhang, J. Schittenhelm, Y.Wu, R. Meyermann, and H. J. Schluesener, "Parenchymal accumulation of CD163+ macrophages/microglia inmultiple sclerosis brains," Journal of Neuroimmunology, vol. 237, no. 1-2, pp. 73-79, 2011.
32. C. Marik, P. A. Felts, J. Bauer, H. Lassmann, and K. J. Smith, "Lesion genesis in a subset of patients with multiple sclerosis: A role for innate immunity?" Brain, vol. 130, no. 11, pp. 2800-2815, 2007. (Pubitemid 350033973)
33. A.Defaux,M. G. Zurich, P.Honegger, and F.Monnet-Tschudi, "Minocycline promotes remyelination in aggregating rat brain cell cultures after interferon-gamma plus lipopolysaccharideinduced demyelination," Neuroscience, vol. 187, pp. 84-92, 2011.
34. S. Rasmussen, J. Imitola, A. Ayuso-Sacido et al., "Reversible neural stem cell niche dysfunction in a model of multiple sclerosis," Annals of Neurology, vol. 69, no. 5, pp. 878-891, 2011.
35. O. Butovsky, G. Landa, G. Kunis et al., "Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis," Journal of Clinical Investigation, vol. 116, no. 4, pp. 905-915, 2006.
36. A. C. Murphy, S. J. Lalor, M. A. Lynch, and K. H. G. Mills, "Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis," Brain, Behavior, and Immunity, vol. 24, no. 4, pp. 641-651, 2010.
37. I. M. Stromnes, L. M. Cerretti, D. Liggitt, R. A. Harris, and J. M. Goverman, "Differential regulation of central nervous system autoimmunity by T H1 and TH17 cells," Nature Medicine, vol. 14, no. 3, pp. 337-342, 2008. (Pubitemid 351347910)
38. B. Almolda, B. Gonzalez, and B. Castellano, "Antigen presentation in EAE: role of microglia, macrophages and dendritic cells," Frontiers in Bioscience, vol. 16, no. 3, pp. 1157-1171, 2011.
39. B. Becher, I. Bechmann, and M. Greter, "Antigen presentation in autoimmunity and CNS inflammation: how T iymphocytes recognize the brain," Journal ofMolecular Medicine, vol. 84,no. 7, pp. 532-543, 2006. (Pubitemid 43992845)
40. R. Gandhi, A. Laroni, and H. L. Weiner, "Role of the innate immune system in the pathogenesis of multiple sclerosis," Journal of Neuroimmunology, vol. 221, no. 1-2, pp. 7-14, 2010.
41. H. G. Fischer and G. Reichmann, "Brain dendritic cells and macrophages/microglia in central nervous system inflammation," Journal of Immunology, vol. 166, no. 4, pp. 2717-2726, 2001. (Pubitemid 32173513)
42. A. L. Zozulya, B. D. Clarkson, S. Ortler, Z. Fabry, and H. Wiendl, "The role of dendritic cells in CNS autoimmunity," Journal of Molecular Medicine, vol. 88, no. 6, pp. 535-544, 2010.
43. G. Raivich and R. Banati, "Brain microglia and bloodderived macrophages: molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease," Brain Research Reviews, vol. 46, no. 3, pp. 261-281, 2004. (Pubitemid 39574328)
44. E. A. Boyle and P. L. McGeer, "Cellular immune response in multiple sclerosis plaques," American Journal of Pathology, vol. 137, no. 3, pp. 575-584, 1990. (Pubitemid 20280987)
45. J. G. Pope, C. L. Vanderlugt, S. M. Rahbe, H. L. Lipton, and S. D. Miller, "Characterization of and functional antigen presentation by central nervous system mononuclear cells from mice infected with Theiler's murine encephalomyelitis virus," Journal of Virology, vol. 72, no. 10, pp. 7762-7771, 1998. (Pubitemid 28421766)
46. D. S. Duncan and S. D. Miller, "CNS expression of B7-H1 regulates pro-inflammatory cytokine production and alters severity of Theiler's virus-induced demyelinating disease," Plos One, vol. 6, no. 4, Article ID e18548, 2011.
47. B. Almolda, B. Gonzalez, and B. Castellano, "Activated microglial cells acquire an immature dendritic cell phenotype and may terminate the immune response in an acute model of EAE," Journal of Neuroimmunology, vol. 223, no. 1-2, pp. 39-54, 2010.
48. C. Blank, J. Kuball, S. Voelkl et al., "Blockade of PD-L1 (B7-H1) augments human tumor-specific T cell responses in vitro," International Journal of Cancer, vol. 119, no. 2, pp. 317-327, 2006.
49. R. De Simone, A. Giampaolo, B. Giometto et al., "The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions," Journal of Neuropathology and Experimental Neurology, vol. 54, no. 2, pp. 175-187, 1995.
50. T. Magnus, B. Schreiner, T. Korn et al., "Microglial expression of the B7 family member B7 homolog 1 confers strong immune inhibition: implications for immune responses and autoimmunity in the CNS," Journal of Neuroscience, vol. 25, no. 10, pp. 2537-2546, 2005. (Pubitemid 40365165)
51. S. Ortler, C. Leder, M. Mittelbronn et al., "B7-H1 restricts neuroantigen-specific T cell responses and confines inflammatory CNS damage: implications for the lesion pathogenesis of multiple sclerosis," European Journal of Immunology, vol. 38, no. 6, pp. 1734-1744, 2008.
52. E. J.McMahon, S. L. Bailey, C. V. Castenada,H.Waldner, and S. D. Miller, "Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis," Nature Medicine, vol. 11, no. 3, pp. 335-339, 2005. (Pubitemid 40460563)
53. M. V. Dhodapkar, R. M. Steinman, J. Krasovsky, C. Munz, and N. Bhardwaj, "Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells," Journal of Experimental Medicine, vol. 193, no. 2, pp. 233-238, 2001. (Pubitemid 32524454)
54. M.G. Roncarolo, M. K. Levings, and C. Traversari, "Differentiation of T regulatory cells by immature dendritic cells," Journal of Experimental Medicine, vol. 193, no. 2, pp. F5-F9, 2001. (Pubitemid 32524446)
55. T. D. Merson,M. D. Binder, and T. J. Kilpatrick, "Role of cytokines as mediators and regulators of microglial activity in inflammatory demyelination of the CNS," NeuroMolecular Medicine, vol. 12, no. 2, pp. 99-132, 2010.
56. C. A. Colton and D. M. Wilcock, "Assessing activation states in microglia," CNS and Neurological Disorders, vol. 9, no. 2, pp. 174-191, 2010.
57. S. Ebert, J. Gerber, S. Bader et al., "Dose-dependent activation of microglial cells by Toll-like receptor agonists alone and in combination," Journal of Neuroimmunology, vol. 159, no. 1-2, pp. 87-96, 2005. (Pubitemid 40126180)
58. J. Bauer, T. Sminia, F. G.Wouterlood, and C. D. Dijkstra, "Phagocytic activity ofmacrophages andmicroglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis," Journal of Neuroscience Research, vol. 38, no. 4, pp. 365-375, 1994. (Pubitemid 24209426)
59. W. W. Li, A. Setzu, C. Zhao, and R. J. M. Franklin, "Minocycline- mediated inhibition of microglia activation impairs oligodendrocyte progenitor cell responses and remyelination in a non-immune model of demyelination," Journal of Neuroimmunology, vol. 158, no. 1-2, pp. 58-66, 2005. (Pubitemid 39626071)
60. S. Pluchino, L. Muzio, J. Imitola et al., "Persistent inflammation alters the function of the endogenous brain stem cell compartment," Brain, vol. 131, no. 10, pp. 2564-2578, 2008.
61. O. Butovsky, Y. Ziv, A. Schwartz et al., "Microglia activated by IL-4 or IFN-? differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells," Molecular and Cellular Neuroscience, vol. 31, no. 1, pp. 149-160, 2006. (Pubitemid 43049908)
62. O. Einstein, D. Karussis,N. Grigoriadis et al., "Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis," Molecular and Cellular Neuroscience, vol. 24, no. 4, pp. 1074-1082, 2003. (Pubitemid 38091518)
63. O. Einstein, N. Fainstein, I. Vaknin et al., "Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression," Annals of Neurology, vol. 61, no. 3, pp. 209-218, 2007. (Pubitemid 46557345)
64. S. Pluchino, A. Quattrini, E. Brambilla et al., "Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis," Nature, vol. 422, no. 6933, pp. 688-694, 2003. (Pubitemid 36514101)
65. J. Yang, Z. Jiang, D. C. Fitzgerald et al., "Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis," Journal of Clinical Investigation, vol. 119, no. 12, pp. 3678-3691, 2009.
66. K. S. Carbajal, C. Schaumburg, R. Strieter, J. Kane, and T. E. Lane, "Migration of engrafted neural stem cells is mediated by CXCL12 signaling through CXCR4 in a viralmodel ofmultiple sclerosis," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 24, pp. 11068-11073, 2010.
67. D. Michel-Monigadon, P. Brachet, I. Neveu, and P. Naveilhan, "Immunoregulatory properties of neural stem cells," Immunotherapy, vol. 3, supplement 4, pp. 39-41, 2011.
68. N. Fainstein, I. Vaknin, O. Einstein et al., "Neural precursor cells inhibit multiple inflammatory signals," Molecular and Cellular Neuroscience, vol. 39, no. 3, pp. 335-341, 2008.
69. J. Das Sarma, B. Ciric, R.Marek et al., "Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis," Journal of Neuroinflammation, vol. 6, article 14, 2009.
70. J. K. Olson and S. D.Miller, "Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs," Journal of Immunology, vol. 173, no. 6, pp. 3916-3924, 2004. (Pubitemid 39280755)
71. E. A. Eugenin, K. Osiecki, L. Lopez, H. Goldstein, T. M. Calderon, and J. W. Berman, "CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the blood-brain barrier: A potential mechanism of HIV-CNS invasion and NeuroAIDS," Journal of Neuroscience, vol. 26, no. 4, pp. 1098-1106, 2006. (Pubitemid 43237041)
72. M. A. Lee, S. Smith, J. Palace, and P. M. Matthews, "Defining multiple sclerosis disease activity using MRI T2-weighted difference imaging," Brain, vol. 121, no. 11, pp. 2095-2102, 1998. (Pubitemid 28497907)
73. P. S. Sorensen, B. Wanscher, C. V. Jensen et al., "Intravenous immunoglobulin G reduces MRI activity in relapsing multiple sclerosis," Neurology, vol. 50, no. 5, pp. 1273-1281, 1998. (Pubitemid 28240339)
74. J. E. Simpson, J. Newcombe, M. L. Cuzner, and M. N. Woodroofe, "Expression of monocyte chemoattractant protein-1 and other chemokines by resident glia and inflammatory cells in multiple sclerosis lesions," Journal of Neuroimmunology, vol. 84, no. 2, pp. 238-249, 1998. (Pubitemid 28248412)
75. B. S. Kim, J. P. Palma, D. Kwon, and A. C. Fuller, "Innate immune response induced by Theiler's murine encephalomyelitis virus infection," Immunologic Research, vol. 31, no. 1, pp. 1-12, 2005. (Pubitemid 40065420)
76. J. Das, G. Ren, L. Zhang et al., "Transforming growth factor ? is dispensable for the molecular orchestration of Th17 cell differentiation," Journal of ExperimentalMedicine, vol. 206, no. 11, pp. 2407-2416, 2009.
77. H. Zhou, B. M. Lapointe, S. R. Clark, L. Zbytnuik, and P. Kubes, "A requirement for microglial TLR4 in leukocyte recruitment into brain in response to lipopolysaccharide," Journal of Immunology, vol. 177, no. 11, pp. 8103-8110, 2006. (Pubitemid 44846329)
78. I. Shaked, Z. Porat, R. Gersner, J. Kipnis, and M. Schwartz, "Early activation of microglia as antigen-presenting cells correlates with T cell-mediated protection and repair of the injured central nervous system," Journal of Neuroimmunology, vol. 146, no. 1-2, pp. 84-93, 2004. (Pubitemid 38032959)
79. S. Rotshenker, "Microglia and macrophage activation and the regulation of complement-receptor-3 (CR3/MAC-1)-mediated myelin phagocytosis in injury and disease," Journal of Molecular Neuroscience, vol. 21, no. 1, pp. 65-72, 2003. (Pubitemid 37204874)
80. M. E. Smith, "Phagocytic properties of microglia in vitro: implications for a role in multiple sclerosis and EAE," Microscopy Research and Technique, vol. 54, no. 2, pp. 81-94, 2001. (Pubitemid 32645873)
81. S. Rotshenker, "The role of Galectin-3/MAC-2 in the activation of the innate-immune function of phagocytosis in microglia in injury and disease," Journal of Molecular Neuroscience, vol. 39, no. 1-2, pp. 99-103, 2009.
82. M. Gitik, S. L. Zaltsman, P.-A.Oldenborg et al., "Myelin downregulates myelin phagocytosis by microglia and macrophages through interactions between CD47 on myelin and SIRPalpha (signal regulatory protein-alpha) on phagocytes," Journal of Neuroinflammation, vol. 8, article 24, 2011.
83. M. E. Smith, K. Van Der Maesen, and F. P. Somera, "Macrophage and microglial responses to cytokines in vitro: phagocytic activity, proteolytic enzyme release, and free radical production," Journal of Neuroscience Research, vol. 54, no. 1, pp. 68-78, 1998. (Pubitemid 28447190)
84. K. Takahashi, M. Prinz, M. Stagi, O. Chechneva, and H. Neumann, "TREM2-transduced myeloid precursors mediate nervous tissue debris clearance and facilitate recovery in an animal model of multiple sclerosis," Plos Medicine, vol. 4, no. 4, article e124, 2007.
85. C. D. Schmid, L. N. Sautkulis, P. E. Danielson et al., "Heterogeneous expression of the triggering receptor expressed on myeloid cells-2 on adult murine microglia," Journal of Neurochemistry, vol. 83, no. 6, pp. 1309-1320, 2002. (Pubitemid 35477470)
86. K. Takahashi, C. D. Rochford, and H. Neumann, "Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2," Journal of Experimental Medicine, vol. 201, no. 4, pp. 647-657, 2005. (Pubitemid 40289554)
87. L. Piccio, C. Buonsanti,M.Mariani et al., "Blockade of TREM-2 exacerbates experimental autoimmune encephalomyelitis," European Journal of Immunology, vol. 37, no. 5, pp. 1290-1301, 2007. (Pubitemid 46927833)