Macrophage migration inhibitory factor potentiates autoimmune-mediated neuroinflammation

Journal of Immunology

Volumn 191, Issue 3, 2013, Pages 1043-1054

  Cox, Gina Mavrikis ^a   Kithcart, Aaron P ^a   Pitt, David ^a   Guan, Zhen ^b   Alexander, Jessica ^b   Williams, Jessica L ^a   Shawler, Todd ^a   Dagia, Nilesh M ^a   Popovich, Phillip G ^b   Satoskar, Abhay R ^a   Whitacre, Caroline C ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Piramal Enterprises Limited   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE MIGRATION INHIBITION FACTOR; MYELIN; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; IMMUNE RESPONSE; MACROPHAGE; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION;

ADULT; AGED; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; MULTIPLE SCLEROSIS; NITRIC OXIDE SYNTHASE TYPE II; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84880661535     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200485     Document Type: Article

References (72)

1. Wingerchuk, D. M., C. F. Lucchinetti, and J. H. Noseworthy. 2001. Multiple sclerosis: current pathophysiological concepts. Lab. Invest. 81: 263-281.
2. Imitola, J., T. Chitnis, and S. J. Khoury. 2006. Insights into the molecular pathogenesis of progression in multiple sclerosis: potential implications for future therapies. Arch. Neurol. 63: 25-33.
3. Lassmann, H. 2007. Multiple sclerosis: is there neurodegeneration independent from inflammation? J. Neurol. Sci. 259: 3-6.
4. Trapp, B. D., and K. A. Nave. 2008. Multiple sclerosis: an immune or neurodegenerative disorder? Annu. Rev. Neurosci. 31: 247-269.
5. Hagman, S., M. Raunio, M. Rossi, P. Dastidar, and I. Elovaara. 2011. Diseaseassociated inflammatory biomarker profiles in blood in different subtypes of multiple sclerosis: prospective clinical and MRI follow-up study. J. Neuroimmunol. 234: 141-147.
6. Heppner, F. L., M. Greter, D. Marino, J. Falsig, G. Raivich, N. Hövelmeyer, A. Waisman, T. Rülicke, M. Prinz, J. Priller, et al. 2005. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 11: 146-152.
7. Benveniste, E. N. 1997. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J. Mol. Med. 75: 165-173.
8. Chitnis, T. 2007. The role of CD4 T cells in the pathogenesis of multiple sclerosis. Int. Rev. Neurobiol. 79: 43-72.
9. Cross, A. H., B. Cannella, C. F. Brosnan, and C. S. Raine. 1990. Homing to central nervous system vasculature by antigen-specific lymphocytes. I. Localization of 14C-labeled cells during acute, chronic, and relapsing experimental allergic encephalomyelitis. Lab. Invest. 63: 162-170.
10. Bauer, J., T. Sminia, F. G. Wouterlood, and C. D. Dijkstra. 1994. Phagocytic activity of macrophages and microglial cells during the course of acute and chronic relapsing experimental autoimmune encephalomyelitis. J. Neurosci. Res. 38: 365-375.
11. Ajami, B., J. L. Bennett, C. Krieger, K. M. McNagny, and F. M. Rossi. 2011. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci. 14: 1142-1149.
12. Ponomarev, E. D., L. P. Shriver, K. Maresz, and B. N. Dittel. 2005. Microglial cell activation and proliferation precedes the onset of CNS autoimmunity. J. Neurosci. Res. 81: 374-389.
13. Rasmussen, S., J. Imitola, A. Ayuso-Sacido, Y. Wang, S. C. Starossom, P. Kivisäkk, B. Zhu, M. Meyer, R. T. Bronson, J. M. Garcia-Verdugo, and S. J. Khoury. 2011. Reversible neural stem cell niche dysfunction in a model of multiple sclerosis. Ann. Neurol. 69: 878-891.
14. Barnett, M. H., and J. W. Prineas. 2004. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 55: 458-468.
15. Brosnan, C. F., M. B. Bornstein, and B. R. Bloom. 1981. The effects of macrophage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis. J. Immunol. 126: 614-620.
16. Huitinga, I., N. van Rooijen, C. J. de Groot, B. M. Uitdehaag, and C. D. Dijkstra. 1990. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J. Exp. Med. 172: 1025-1033.
17. Bauer, J., I. Huitinga, W. Zhao, H. Lassmann, W. F. Hickey, and C. D. Dijkstra. 1995. The role of macrophages, perivascular cells, and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. Glia 15: 437-446.
18. David, J. R. 1966. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-Antigen interaction. Proc. Natl. Acad. Sci. USA 56: 72-77.
19. Merk, M., S. Zierow, L. Leng, R. Das, X. Du, W. Schulte, J. Fan, H. Lue, Y. Chen, H. Xiong, et al. 2011. The D-dopachrome tautomerase (DDT) gene product is a cytokine and functional homolog of macrophage migration inhibitory factor (MIF). Proc. Natl. Acad. Sci. USA 108: E577-E585.
20. Calandra, T., and T. Roger. 2003. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 3: 791-800.
21. Mitchell, R. A., H. Liao, J. Chesney, G. Fingerle-Rowson, J. Baugh, J. David, and R. Bucala. 2002. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc. Natl. Acad. Sci. USA 99: 345-350.
22. Calandra, T., J. Bernhagen, R. A. Mitchell, and R. Bucala. 1994. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J. Exp. Med. 179: 1895-1902.
23. Gregory, J. L., E. F. Morand, S. J. McKeown, J. A. Ralph, P. Hall, Y. H. Yang, S. R. McColl, and M. J. Hickey. 2006. Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J. Immunol. 177: 8072-8079.
24. Bernhagen, J., R. Krohn, H. Lue, J. L. Gregory, A. Zernecke, R. R. Koenen, M. Dewor, I. Georgiev, A. Schober, L. Leng, et al. 2007. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat. Med. 13: 587-596.
25. de Jong, Y. P., A. C. Abadia-Molina, A. R. Satoskar, K. Clarke, S. T. Rietdijk, W. A. Faubion, E. Mizoguchi, C. N. Metz, M. Alsahli, T. ten Hove, et al. 2001. Development of chronic colitis is dependent on the cytokine MIF. [Published erratum appears in 2002 Nat. Immunol. 3: 407.]
26. Nat. Immunol. 2: 1061-1066.
27. Mikulowska, A., C. N. Metz, R. Bucala, and R. Holmdahl. 1997. Macrophage migration inhibitory factor is involved in the pathogenesis of collagen type IIinduced arthritis in mice. J. Immunol. 158: 5514-5517.
28. Powell, N. D., T. L. Papenfuss, M. A. McClain, I. E. Gienapp, T. M. Shawler, A. R. Satoskar, and C. C. Whitacre. 2005. Cutting edge: macrophage migration inhibitory factor is necessary for progression of experimental autoimmune encephalomyelitis. J. Immunol. 175: 5611-5614.
29. Denkinger, C. M., M. Denkinger, J. J. Kort, C. Metz, and T. G. Forsthuber. 2003. In vivo blockade of macrophage migration inhibitory factor ameliorates acute experimental autoimmune encephalomyelitis by impairing the homing of encephalitogenic T cells to the central nervous system. J. Immunol. 170: 1274-1282.
30. Kithcart, A. P., G. M. Cox, T. Sielecki, A. Short, J. Pruitt, T. Papenfuss, T. Shawler, I. Gienapp, A. R. Satoskar, and C. C. Whitacre. 2010. A small-molecule inhibitor of macrophage migration inhibitory factor for the treatment of inflammatory disease. FASEB J. 24: 4459-4466. 10.1096/fj.4410- 162347.
31. Ogata, A., J. Nishihira, T. Suzuki, K. Nagashima, and K. Tashiro. 1998. Identification of macrophage migration inhibitory factor mRNA expression in neural cells of the rat brain by in situ hybridization. Neurosci. Lett. 246: 173-177.
32. Bacher,M.,A.Meinhardt,H.Y. Lan,F. S.Dhabhar,W.Mu, C.N.Metz, J.A.Chesney, D. Gemsa, T. Donnelly, R. C. Atkins, and R. Bucala. 1998. MIF expression in the rat brain: implications for neuronal function. Mol. Med. 4: 217-230.
33. Bacher, M., C. N. Metz, T. Calandra, K. Mayer, J. Chesney, M. Lohoff, D. Gemsa, T. Donnelly, and R. Bucala. 1996. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc. Natl. Acad. Sci. USA 93: 7849-7854.
34. Bacher, M., E. Weihe, B. Dietzschold, A. Meinhardt, H. Vedder, D. Gemsa, and M. Bette. 2002. Borna disease virus-induced accumulation of macrophage migration inhibitory factor in rat brain astrocytes is associated with inhibition of macrophage infiltration. Glia 37: 291-306.
35. Niino, M., A. Ogata, S. Kikuchi, K. Tashiro, and J. Nishihira. 2000. Macrophage migration inhibitory factor in the cerebrospinal fluid of patients with conventional and optic-spinal forms of multiple sclerosis and neuro-Behçet's disease. J. Neurol. Sci. 179: 127-131.
36. Bozza, M., A. R. Satoskar, G. Lin, B. Lu, A. A. Humbles, C. Gerard, and J. R. David. 1999. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J. Exp. Med. 189: 341-346.
37. Bettelli, E., M. Pagany, H. L. Weiner, C. Linington, R. A. Sobel, and V. K. Kuchroo. 2003. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197: 1073-1081.
38. Williams, J. L., A. P. Kithcart, K. M. Smith, T. Shawler, G. M. Cox, and C. C. Whitacre. 2011. Memory cells specific for myelin oligodendrocyte glycoprotein (MOG) govern the transfer of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 234: 84-92.
39. Dagia, N. M., D. V. Kamath, P. Bhatt, R. D. Gupte, S. S. Dadarkar, L. Fonseca, G. Agarwal, A. Chetrapal-Kunwar, S. Balachandran, S. Srinivasan, et al. 2009. A fluorinated analog of ISO-1 blocks the recognition and biological function of MIF and is orally efficacious in a murine model of colitis. Eur. J. Pharmacol. 607: 201-212.
40. Popovich, P. G., P. Wei, and B. T. Stokes. 1997. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 377: 443-464.
41. Beck, K. D., H. X. Nguyen, M. D. Galvan, D. L. Salazar, T. M. Woodruff, and A. J. Anderson. 2010. Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 133: 433-447.
42. Kigerl, K. A., W. Lai, S. Rivest, R. P. Hart, A. R. Satoskar, and P. G. Popovich. 2007. Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J. Neurochem. 102: 37-50.
43. Ejarque-Ortiz, A., M. G. Medina, J. M. Tusell, A. P. Pérez- González, J. Serratosa, and J. Saura. 2007. Upregulation of CCAAT/enhancer binding protein beta in activated astrocytes and microglia. Glia 55: 178-188.
44. Berger, T., S. Weerth, K. Kojima, C. Linington, H. Wekerle, and H. Lassmann. 1997. Experimental autoimmune encephalomyelitis: the antigen specificity of T lymphocytes determines the topography of lesions in the central and peripheral nervous system. Lab. Invest. 76: 355-364.
45. Sedgwick, J. D., S. Schwender, H. Imrich, R. Dörries, G. W. Butcher, and V. ter Meulen. 1991. Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc. Natl. Acad. Sci. USA 88: 7438-7442.
46. Ponomarev, E. D., T. Veremeyko, N. Barteneva, A. M. Krichevsky, and H. L. Weiner. 2011. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-A-PU.1 pathway. Nat. Med. 17: 64-70.
47. Feng, R., S. C. Desbordes, H. Xie, E. S. Tillo, F. Pixley, E. R. Stanley, and T. Graf. 2008. PU.1 and C/EBPalpha/beta convert fibroblasts into macrophagelike cells. Proc. Natl. Acad. Sci. USA 105: 6057-6062.
48. Pope, R. M., A. Leutz, and S. A. Ness. 1994. C/EBP beta regulation of the tumor necrosis factor alpha gene. J. Clin. Invest. 94: 1449-1455.
49. Tsai, V. W., M. G. Mohammad, O. Tolhurst, S. N. Breit, P. E. Sawchenko, and D. A. Brown. 2011. CCAAT/enhancer binding protein-d expression by dendritic cells regulates CNS autoimmune inflammatory disease. J. Neurosci. 31: 17612-17621.
50. Kerschensteiner, M., C. Stadelmann, B. S. Buddeberg, D. Merkler, F. M. Bareyre, D. C. Anthony, C. Linington, W. Brück, and M. E. Schwab. 2004. Targeting experimental autoimmune encephalomyelitis lesions to a predetermined axonal tract system allows for refined behavioral testing in an animal model of multiple sclerosis. Am. J. Pathol. 164: 1455-1469.
51. Arjona, A., H. G. Foellmer, T. Town, L. Leng, C. McDonald, T. Wang, S. J. Wong, R. R. Montgomery, E. Fikrig, and R. Bucala. 2007. Abrogation of macrophage migration inhibitory factor decreases West Nile virus lethality by limiting viral neuroinvasion. J. Clin. Invest. 117: 3059-3066.
52. Mizue, Y., S. Ghani, L. Leng, C. McDonald, P. Kong, J. Baugh, S. J. Lane, J. Craft, J. Nishihira, S. C. Donnelly, et al. 2005. Role for macrophage migration inhibitory factor in asthma. Proc. Natl. Acad. Sci. USA 102: 14410-14415.
53. Tran, E. H., K. Hoekstra, N. van Rooijen, C. D. Dijkstra, and T. Owens. 1998. Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice. J. Immunol. 161: 3767-3775.
54. Martiney, J. A., A. J. Rajan, P. C. Charles, A. Cerami, P. C. Ulrich, S. Macphail, K. J. Tracey, and C. F. Brosnan. 1998. Prevention and treatment of experimental autoimmune encephalomyelitis by CNI-1493, a macrophage-deactivating agent. J. Immunol. 160: 5588-5595.
55. Ponomarev, E. D., L. P. Shriver, and B. N. Dittel. 2006. CD40 expression by microglial cells is required for their completion of a two-step activation process during central nervous system autoimmune inflammation. J. Immunol. 176: 1402-1410.
56. Becher, B., B. G. Durell, and R. J. Noelle. 2003. IL-23 produced by CNSresident cells controls T cell encephalitogenicity during the effector phase of experimental autoimmune encephalomyelitis. J. Clin. Invest. 112: 1186-1191.
57. Ford, A. L., E. Foulcher, F. A. Lemckert, and J. D. Sedgwick. 1996. Microglia induce CD4 T lymphocyte final effector function and death. J. Exp. Med. 184: 1737-1745.
58. Selmaj, K. W., and C. S. Raine. 1988. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23: 339-346.
59. Weber, M. S., T. Prod'homme, S. Youssef, S. E. Dunn, C. D. Rundle, L. Lee, J. C. Patarroyo, O. Stüve, R. A. Sobel, L. Steinman, and S. S. Zamvil. 2007. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat. Med. 13: 935-943.
60. Mitchell, R. A., C. N. Metz, T. Peng, and R. Bucala. 1999. Sustained mitogenactivated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF): regulatory role in cell proliferation and glucocorticoid action. J. Biol. Chem. 274: 18100-18106.
61. Kleemann, R., A. Hausser, G. Geiger, R. Mischke, A. Burger-Kentischer, O. Flieger, F. J. Johannes, T. Roger, T. Calandra, A. Kapurniotu, et al. 2000. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 408: 211-216.
62. Leng, L., C. N. Metz, Y. Fang, J. Xu, S. Donnelly, J. Baugh, T. Delohery, Y. Chen, R. A. Mitchell, and R. Bucala. 2003. MIF signal transduction initiated by binding to CD74. J. Exp. Med. 197: 1467-1476.
63. Atsumi, T., Y. R. Cho, L. Leng, C. McDonald, T. Yu, C. Danton, E. G. Hong, R. A. Mitchell, C. Metz, H. Niwa, et al. 2007. The proinflammatory cytokine macrophage migration inhibitory factor regulates glucose metabolism during systemic inflammation. J. Immunol. 179: 5399-5406.
64. Pérez-Capote, K., J. Saura, J. Serratosa, and C. Solá. 2006. Expression of C/EBPalpha and C/EBPbeta in glial cells in vitro after inducing glial activation by different stimuli. Neurosci. Lett. 410: 25-30.
65. Sandhir, R., and N. E. Berman. 2010. Age-dependent response of CCAAT/enhancer binding proteins following traumatic brain injury in mice. Neurochem. Int. 56: 188-193.
66. Østergaard, C., and T. Benfield. 2009. Macrophage migration inhibitory factor in cerebrospinal fluid from patients with central nervous system infection. Crit. Care 13: R101.
67. Bacher, M., O. Deuster, B. Aljabari, R. Egensperger, F. Neff, F. Jessen, J. Popp, C. Noelker, J. P. Reese, Y. Al-Abed, and R. Dodel. 2010. The role of macrophage migration inhibitory factor in Alzheimer's disease. Mol. Med. 16: 116-121.
68. Simmons, R. D., and D. O. Willenborg. 1990. Direct injection of cytokines into the spinal cord causes autoimmune encephalomyelitis-like inflammation. J. Neurol. Sci. 100: 37-42.
69. Phillips, L. M., and L. A. Lampson. 1999. Site-specific control of T cell traffic in the brain: T cell entry to brainstem vs. hippocampus after local injection of IFNgamma. J. Neuroimmunol. 96: 218-227.
70. Calandra, T., J. Bernhagen, C. N. Metz, L. A. Spiegel, M. Bacher, T. Donnelly, A. Cerami, and R. Bucala. 1995. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377: 68-71.
71. Correale, J., M. Fiol, and W. Gilmore. 2006. The risk of relapses in multiple sclerosis during systemic infections. Neurology 67: 652-659.
72. Fairweather, D., S. Frisancho-Kiss, and N. R. Rose. 2005. Viruses as adjuvants for autoimmunity: evidence from Coxsackievirus-induced myocarditis. Rev. Med. Virol. 15: 17-27.