Preferential recruitment of neutrophils into the cerebellum and brainstem contributes to the atypical experimental autoimmune encephalomyelitis phenotype

Journal of Immunology

Volumn 195, Issue 3, 2015, Pages 841-852

  Liu, Yudong ^a   Holdbrooks, Andrew T ^a   Meares, Gordon P ^a   Buckley, Jessica A ^a   Benveniste, Etty N ^a   Qin, Hongwei ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL2 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA; CHEMOKINE; CHEMOKINE RECEPTOR CXCR2; IL1B PROTEIN, MOUSE; INTERLEUKIN 23; INTERLEUKIN 6; NOS2 PROTEIN, MOUSE; SOCS3 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; BRAIN STEM; CELL INFILTRATION; CEREBELLUM; CONTROLLED STUDY; CYTOKINE RELEASE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNOPATHOGENESIS; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CYTOLOGY; ENZYME ACTIVATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; NEUTROPHIL;

ANIMALS; BRAIN STEM; CEREBELLUM; CHEMOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME ACTIVATION; INTERLEUKIN-1BETA; INTERLEUKIN-23; INTERLEUKIN-6; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RECEPTORS, INTERLEUKIN-8B; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84937688537     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1403063     Document Type: Article

References (65)

1. Goverman, J. 2009. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9: 393-407.
2. Bhat, R., and L. Steinman. 2009. Innate and adaptive autoimmunity directed to the central nervous system. Neuron 64: 123-132.
3. Qin, H., W.-I. Yeh, P. De Sarno, A. T. Holdbrooks, Y. Liu, M. T. Muldowney, S. L. Reynolds, L. L. Yanagisawa, T. H. I. Fox, III, K. Park, et al. 2012. Signal transducer and activator of transcription-3/suppressor of cytokine signaling-3 (STAT3/SOCS3) axis in myeloid cells regulates neuroinflammation. Proc. Natl. Acad. Sci. USA 109: 5004-5009.
4. Voskuhl, R. R., R. S. Peterson, B. Song, Y. Ao, L. B. Morales, S. Tiwari-Woodruff, and M. V. Sofroniew. 2009. Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J. Neurosci. 29: 11511-11522.
5. Argaw, A. T., L. Asp, J. Zhang, K. Navrazhina, T. Pham, J. N. Mariani, S. Mahase, D. J. Dutta, J. Seto, E. G. Kramer, et al. 2012. Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J. Clin. Invest. 122: 2454-2468.
6. Mayo, L., S. A. Trauger, M. Blain, M. Nadeau, B. Patel, J. I. Alvarez, I. D. Mascanfroni, A. Yeste, P. Kivisäkk, K. Kallas, et al. 2014. Regulation of astrocyte activation by glycolipids drives chronic CNS inflammation. Nat. Med. 20: 1147-1156.
7. McColl, S. R., M. A. Staykova, A. Wozniak, S. Fordham, J. Bruce, and D. O. Willenborg. 1998. Treatment with anti-granulocyte antibodies inhibits the effector phase of experimental autoimmune encephalomyelitis. J. Immunol. 161: 6421-6426.
8. Carlson, T., M. Kroenke, P. Rao, T. E. Lane, and B. Segal. 2008. The Th17-ELR + CXC chemokine pathway is essential for the development of central nervous system autoimmune disease. J. Exp. Med. 205: 811-823.
9. Steinbach, K., M. Piedavent, S. Bauer, J. T. Neumann, and M. A. Friese. 2013. Neutrophils amplify autoimmune central nervous system infiltrates by maturing local APCs. J. Immunol. 191: 4531-4539.
10. Christy, A. L., M. E. Walker, M. J. Hessner, and M. A. Brown. 2013. Mast cell activation and neutrophil recruitment promotes early and robust inflammation in the meninges in EAE. J. Autoimmun. 42: 50-61.
11. Yi, H., C. Guo, X. Yu, D. Zuo, and X. Y. Wang. 2012. Mouse CD11b+Gr-1+ myeloid cells can promote Th17 cell differentiation and experimental autoimmune encephalomyelitis. J. Immunol. 189: 4295-4304.
12. Liu, L., A. Belkadi, L. Darnall, T. Hu, C. Drescher, A. C. Cotleur, D. Padovani-Claudio, T. He, K. Choi, T. E. Lane, et al. 2010. CXCR2-positive neutrophils are essential for cuprizone-induced demyelination: relevance to multiple sclerosis. Nat. Neurosci. 13: 319-326.
13. Semple, B. D., T. Kossmann, and M. C. Morganti-Kossmann. 2010. Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J. Cereb. Blood Flow Metab. 30: 459-473.
14. Nyga?rdas, P. T., J. A. Määttä, and A. E. Hinkkanen. 2000. Chemokine expression by central nervous system resident cells and infiltrating neutrophils during experimental autoimmune encephalomyelitis in the BALB/c mouse. Eur. J. Immunol. 30: 1911-1918.
15. Naegele, M., K. Tillack, S. Reinhardt, S. Schippling, R. Martin, and M. Sospedra. 2012. Neutrophils in multiple sclerosis are characterized by a primed phenotype. J. Neuroimmunol. 242: 60-71.
16. Ishizu, T., M. Osoegawa, F. J. Mei, H. Kikuchi, M. Tanaka, Y. Takakura, M. Minohara, H. Murai, F. Mihara, T. Taniwaki, and J. Kira. 2005. Intrathecal activation of the IL-17/IL-8 axis in opticospinal multiple sclerosis. Brain 128: 988-1002.
17. Lucchinetti, C. F., R. N. Mandler, D. McGavern, W. Bruck, G. Gleich, R. M. Ransohoff, C. Trebst, B. Weinshenker, D. Wingerchuk, J. E. Parisi, and H. Lassmann. 2002. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 125: 1450-1461.
18. Rumble, J. M., A. K. Huber, G. Krishnamoorthy, A. Srinivasan, D. A. Giles, X. Zhang, L. Wang, and B. M. Segal. 2015. Neutrophil-related factors as biomarkers in EAE and MS. J. Exp. Med. 212: 23-35.
19. Breij, E. C., B. P. Brink, R. Veerhuis, C. van den Berg, R. Vloet, R. Yan, C. D. Dijkstra, P. van der Valk, and L. Bö. 2008. Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann. Neurol. 63: 16-25.
20. Metz, I., S. D. Weigand, B. F. Popescu, J. M. Frischer, J. E. Parisi, Y. Guo, H. Lassmann, W. Brück, and C. F. Lucchinetti. 2014. Pathologic heterogeneity persists in early active multiple sclerosis lesions. Ann. Neurol. 75: 728-738.
21. Amezcua, L., A. Lerner, K. Ledezma, D. Conti, M. Law, L. Weiner, and A. Langer-Gould. 2013. Spinal cord lesions and disability in Hispanics with multiple sclerosis. J. Neurol. 260: 2770-2776.
22. Raine, C. S., L. B. Barnett, A. Brown, T. Behar, and D. E. McFarlin. 1980. Neuropathology of experimental allergic encephalomyelitis in inbred strains of mice. Lab. Invest. 43: 150-157.
23. Bettelli, E., B. Sullivan, S. J. Szabo, R. A. Sobel, L. H. Glimcher, and V. K. Kuchroo. 2004. Loss of T-bet, but not STAT1, prevents the development of experimental autoimmune encephalomyelitis. J. Exp. Med. 200: 79-87.
24. Wensky, A. K., G. C. Furtado, M. C. Marcondes, S. Chen, D. Manfra, S. A. Lira, D. Zagzag, and J. J. Lafaille. 2005. IFN-gamma determines distinct clinical outcomes in autoimmune encephalomyelitis. J. Immunol. 174: 1416-1423.
25. Stromnes, I. M., L. M. Cerretti, D. Liggitt, R. A. Harris, and J. M. Goverman. 2008. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 14: 337-342.
26. Simmons, S. B., D. Liggitt, and J. M. Goverman. 2014. Cytokine-regulated neutrophil recruitment is required for brain but not spinal cord inflammation during experimental autoimmune encephalomyelitis. J. Immunol. 193: 555-563.
27. Stoolman, J. S., P. C. Duncker, A. K. Huber, and B. M. Segal. 2014. Site-specific chemokine expression regulates central nervous system inflammation and determines clinical phenotype in autoimmune encephalomyelitis. J. Immunol. 193: 564-570.
28. Mantovani, A., M. A. Cassatella, C. Costantini, and S. Jaillon. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11: 519-531.
29. Werner, J. L., M. A. Gessner, L. M. Lilly, M. P. Nelson, A. E. Metz, D. Horn, C. W. Dunaway, J. Deshane, D. D. Chaplin, C. T. Weaver, et al. 2011. Neutrophils produce interleukin 17A (IL-17A) in a dectin-1- and IL-23-dependent manner during invasive fungal infection. Infect. Immun. 79: 3966-3977.
30. Zindl, C. L., J. F. Lai, Y. K. Lee, C. L. Maynard, S. N. Harbour, W. Ouyang, D. D. Chaplin, and C. T. Weaver. 2013. IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc. Natl. Acad. Sci. USA 110: 12768-12773.
31. Määttä, J. A., U. R. Sjöholm, P. T. Nyga?rdas, A. A. Salmi, and A. E. Hinkkanen. 1998. Neutrophils secreting tumor necrosis factor alpha infiltrate the central nervous system of BALB/c mice with experimental autoimmune encephalomyelitis. J. Neuroimmunol. 90: 162-175.
32. Ryan, S. O., J. L. Johnson, and B. A. Cobb. 2013. Neutrophils confer T cell resistance to myeloid-derived suppressor cell-mediated suppression to promote chronic inflammation. J. Immunol. 190: 5037-5047.
33. Croker, B. A., D. L. Krebs, J.-G. Zhang, S. Wormald, T. A. Willson, E. G. Stanley, L. Robb, C. J. Greenhalgh, I. Förster, B. E. Clausen, et al. 2003. SOCS3 negatively regulates IL-6 signaling in vivo. Nat. Immunol. 4: 540-545.
34. Liu, Y., A. T. Holdbrooks, P. De Sarno, A. L. Rowse, L. L. Yanagisawa, B. C. McFarland, L. E. Harrington, C. Raman, S. Sabbaj, E. N. Benveniste, and H. Qin. 2014. Therapeutic efficacy of suppressing the Jak/STAT pathway in multiple models of experimental autoimmune encephalomyelitis. J. Immunol. 192: 59-72.
35. Bento, A. F., D. F. Leite, R. F. Claudino, D. B. Hara, P. C. Leal, and J. B. Calixto. 2008. The selective nonpeptide CXCR2 antagonist SB225002 ameliorates acute experimental colitis in mice. J. Leukoc. Biol. 84: 1213-1221.
36. Baker, B. J., K. W. Park, H. Qin, X. Ma, and E. N. Benveniste. 2010. IL-27 inhibits OSM-mediated TNF-A and iNOS gene expression in microglia. Glia 58: 1082-1093.
37. Ritzman, A. M., J. M. Hughes-Hanks, V. A. Blaho, L. E. Wax, W. J. Mitchell, and C. R. Brown. 2010. The chemokine receptor CXCR2 ligand KC (CXCL1) mediates neutrophil recruitment and is critical for development of experimental Lyme arthritis and carditis. Infect. Immun. 78: 4593-4600.
38. Dogan, R. N., A. Elhofy, and W. J. Karpus. 2008. Production of CCL2 by central nervous system cells regulates development of murine experimental autoimmune encephalomyelitis through the recruitment of TNF- and iNOS-expressing macrophages and myeloid dendritic cells. J. Immunol. 180: 7376-7384.
39. Perrin, P. J., C. A. Rumbley, R. L. Beswick, E. Lavi, and S. M. Phillips. 2000. Differential cytokine and chemokine production characterizes experimental autoimmune meningitis and experimental autoimmune encephalomyelitis. Clin. Immunol. 94: 114-124.
40. Chou, R. C., N. D. Kim, C. D. Sadik, E. Seung, Y. Lan, M. H. Byrne, B. Haribabu, Y. Iwakura, and A. D. Luster. 2010. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 33: 266-278.
41. Yoshimura, T., and M. Takahashi. 2007. IFN-gamma-mediated survival enables human neutrophils to produce MCP-1/CCL2 in response to activation by TLR ligands. J. Immunol. 179: 1942-1949.
42. Sarchielli, P., A. Orlacchio, F. Vicinanza, G. P. Pelliccioli, M. Tognoloni, C. Saccardi, and V. Gallai. 1997. Cytokine secretion and nitric oxide production by mononuclear cells of patients with multiple sclerosis. J. Neuroimmunol. 80: 76-86.
43. Acar, G., F. Idiman, E. Idiman, G. Kirkali, H. Cakmakc?i, and S. Ozakbas?. 2003. Nitric oxide as an activity marker in multiple sclerosis. J. Neurol. 250: 588-592.
44. Rejdak, K., M. J. Eikelenboom, A. Petzold, E. J. Thompson, Z. Stelmasiak, R. H. Lazeron, F. Barkhof, C. H. Polman, B. M. Uitdehaag, and G. Giovannoni. 2004. CSF nitric oxide metabolites are associated with activity and progression of multiple sclerosis. Neurology 63: 1439-1445.
45. Redford, E. J., R. Kapoor, and K. J. Smith. 1997. Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 120: 2149-2157.
46. Bjartmar, C., J. R. Wujek, and B. D. Trapp. 2003. Axonal loss in the pathology of MS: consequences for understanding the progressive phase of the disease. J. Neurol. Sci. 206: 165-171.
47. Wujek, J. R., C. Bjartmar, E. Richer, R. M. Ransohoff, M. Yu, V. K. Tuohy, and B. D. Trapp. 2002. Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J. Neuropathol. Exp. Neurol. 61: 23-32.
48. van Waesberghe, J. H., W. Kamphorst, C. J. De Groot, M. A. van Walderveen, J. A. Castelijns, R. Ravid, G. J. Lycklama à Nijeholt, P. van der Valk, C. H. Polman, A. J. Thompson, and F. Barkhof. 1999. Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann. Neurol. 46: 747-754.
49. Kapoor, R., M. Davies, P. A. Blaker, S. M. Hall, and K. J. Smith. 2003. Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann. Neurol. 53: 174-180.
50. Smith, K. J., R. Kapoor, S. M. Hall, and M. Davies. 2001. Electrically active axons degenerate when exposed to nitric oxide. Ann. Neurol. 49: 470-476.
51. Soulika, A. M., E. Lee, E. McCauley, L. Miers, P. Bannerman, and D. Pleasure. 2009. Initiation and progression of axonopathy in experimental autoimmune encephalomyelitis. J. Neurosci. 29: 14965-14979.
52. Pachner, A. R. 2011. Experimental models of multiple sclerosis. Curr. Opin. Neurol. 24: 291-299.
53. Attfield, K. E., C. A. Dendrou, and L. Fugger. 2012. Bridging the gap from genetic association to functional understanding: the next generation of mouse models of multiple sclerosis. Immunol. Rev. 248: 10-22.
54. Davie, C. A., G. J. Barker, S. Webb, P. S. Tofts, A. J. Thompson, A. E. Harding, W. I. McDonald, and D. H. Miller. 1995. Persistent functional deficit in multiple sclerosis and autosomal dominant cerebellar ataxia is associated with axon loss. Brain 118: 1583-1592.
55. Naismith, R. T., K. Trinkaus, and A. H. Cross. 2006. Phenotype and prognosis in African-Americans with multiple sclerosis: a retrospective chart review. Mult. Scler. 12: 775-781.
56. Quintana, A., M. Müller, R. F. Frausto, R. Ramos, D. R. Getts, E. Sanz, M. J. Hofer, M. Krauthausen, N. J. King, J. Hidalgo, and I. L. Campbell. 2009. Site-specific production of IL-6 in the central nervous system retargets and enhances the inflammatory response in experimental autoimmune encephalomyelitis. J. Immunol. 183: 2079-2088.
57. Garcia-Bonilla, L., J. M. Moore, G. Racchumi, P. Zhou, J. M. Butler, C. Iadecola, and J. Anrather. 2014. Inducible nitric oxide synthase in neutrophils and endothelium contributes to ischemic brain injury in mice. J. Immunol. 193: 2531-2537.
58. Bö, L., T. M. Dawson, S. Wesselingh, S. Mörk, S. Choi, P. A. Kong, D. Hanley, and B. D. Trapp. 1994. Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann. Neurol. 36: 778-786.
59. Rejdak, K., A. Petzold, Z. Stelmasiak, and G. Giovannoni. 2008. Cerebrospinal fluid brain specific proteins in relation to nitric oxide metabolites during relapse of multiple sclerosis. Mult. Scler. 14: 59-66.
60. Fox, R. J., D. H. Miller, J. T. Phillips, M. Hutchinson, E. Havrdova, M. Kita, M. Yang, K. Raghupathi, M. Novas, M. T. Sweetser, et al. 2012. Placebocontrolled phase 3 study of oral BG-12 or glatiramer in multiple sclerosis. N. Engl. J. Med. 367: 1087-1097.
61. Gold, R., L. Kappos, D. L. Arnold, A. Bar-Or, G. Giovannoni, K. Selmaj, C. Tornatore, M. T. Sweetser, M. Yang, S. I. Sheikh, K. T. Dawson, et al. 2012. Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N. Engl. J. Med. 367: 1098-1107.
62. Chen, H., J. C. Assmann, A. Krenz, M. Rahman, M. Grimm, C. M. Karsten, J. Köhl, S. Offermanns, N. Wettschureck, and M. Schwaninger. 2014. Hydroxycarboxylic acid receptor 2 mediates dimethyl fumarate's protective effect in EAE. J. Clin. Invest. 124: 2188-2192.
63. Wong, P. K., P. J. Egan, B. A. Croker, K. O'Donnell, N. A. Sims, S. Drake, H. Kiu, E. J. McManus, W. S. Alexander, A. W. Roberts, and I. P. Wicks. 2006. SOCS-3 negatively regulates innate and adaptive immune mechanisms in acute IL-1-dependent inflammatory arthritis. J. Clin. Invest. 116: 1571-1581.
64. Croker, B. A., D. Metcalf, L. Robb, W. Wei, S. Mifsud, L. DiRago, L. A. Cluse, K. D. Sutherland, L. Hartley, E. Williams, et al. 2004. SOCS3 is a critical physiological negative regulator of G-CSF signaling and emergency granulopoiesis. Immunity 20: 153-165.
65. Németh, T., and A. Mócsai. 2012. The role of neutrophils in autoimmune diseases. Immunol. Lett. 143: 9-19.