Regulation of neuroinflammation: The role of CXCL10 in lymphocyte infiltration during autoimmune encephalomyelitis

Journal of Cellular Biochemistry

Volumn 92, Issue 2, 2004, Pages 213-222

  Klein, Robyn S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmunity; Central nervous system; Chemokine; Lymphocyte; Trafficking

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON INDUCIBLE PROTEIN 10; ALPHA CHEMOKINE; CXC CHEMOKINE IP 10; CXC CHEMOKINE IP-10;

ALLERGIC ENCEPHALOMYELITIS; BIOLOGICAL MODEL; CENTRAL NERVOUS SYSTEM DISEASE; HUMAN; LYMPHOCYTIC INFILTRATION; LYMPHOID TISSUE; NEURITIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CELL MOTION; CYTOLOGY; DEMYELINATING DISEASE; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE; METABOLISM;

ANIMALIA;

ANIMALS; CELL MOVEMENT; CHEMOKINES, CXC; DEMYELINATING AUTOIMMUNE DISEASES, CNS; HUMANS; INFLAMMATION; LYMPHOCYTES;

EID: 16544384933     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20052     Document Type: Review

References (64)

1. Albanesi C, Scarponi C, Sebastiani S, Cavani A, Federici M, De Pita O, Puddu P, Girolomoni G. 2000. IL-4 enhances keratinocyte expression of CXCR3 agonistic chemokines. J Immunol 165:1395-1402.
2. Alt C, Laschinger M, Engelhardt B. 2002. Functional expression of the lymphoid chemokines CCL19 (ELC) and CCL 21 (SLC) at the blood-brain barrier suggests their involvement in G-protein-dependent lymphocyte recruitment into the central nervous system during experimental autoimmune encephalomyelitis. Eur J Immunol 32:2133-2144.
3. Asensio VC, Kincaid C, Campbell IL. 1999a. Chemokines and the inflammatory response to viral infection in the central nervous system with a focus on lymphocytic choriomeningitis virus. J Neurovirol 5:65-75.
4. Asensio VC, Lassmann S, Pagenstecher A, Steffensen SC, Henriksen SJ, Campbell IL. 1999b. C10 is a novel chemokine expressed in experimental inflammatory demyelinating disorders that promotes recruitment of macrophages to the central nervous system. Am J Pathol 154:1181-1191.
5. Balashov KE, Rottman JB, Weiner HL, Hancock WW. 1999. CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc Natl Acad Sci USA 96:6873-6878.
6. Bennetts BH, Teutsch SM, Buhler MM, Heard RN, Stewart GJ. 1997. The CCR5 deletion mutation fails to protect against multiple sclerosis. Hum Immunol 58:52-59.
7. Boztug K, Carson MJ, Pham-Mitchell N, Asensio VC, DeMartino J, Campbell IL. 2002. Leukocyte infiltration, but not neurodegeneration, in the CNS of transgenic mice with astrocyte production of the CXC chemokine ligand 10. J Immunol 169:1505-1515.
8. Campbell JD, Hayglass KT. 2000. T cell chemokine receptor expression in human Th1- and Th2-associated diseases. Arch immunol Ther Exp 48:451-456.
9. Carr DJ. 1998. Increased levels of IFN-gamma in the trigeminal ganglion correlate with protection against HSV-1-induced encephalitis following subcutaneous administration with androstenediol. J Neuroimmunol 89:160-167.
10. Chen BP, Kuziel WA, Lane TE. 2001. Lack of CCR2 results in increased mortality and impaired leukocyte activation and trafficking following infection of the central nervous system with a neurotropic coronavirus. J Immunol 167: 4585-4592.
11. Columba-Cabezas S, Serafini B, Ambrosini E, Sanchez M, Penna G, Adorini L, Aloisi F. 2002. Induction of macrophage-derived chemokine/CCL22 expression in experimental autoimmune encephalomyelitis and cultured microglia: Implications for disease regulation. J Neuroimmunol 130:10-21.
12. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD. 2002. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol 168: 3195-3204.
13. Fife BT, Kennedy KJ, Paniagua MC, Lukacs NW, Kunkel SL, Luster AD, Karpus WJ. 2001a. CXCL10 (IFN-gamma-inducible protein-10) control of encephalitogenic CD4+ T cell accumulation in the central nervous system during experimental autoimmune encephalomyelitis. J Immunol 166:7617-7624.
14. Fife BT, Paniagua MC, Lukacs NW, Kunkel SL, Karpus WJ. 2001b. Selective CC chemokine receptor expression by central nervous system-infiltrating encephalitogenic T cells during experimental autoimmune encephalomyelitis. J Neurosci Res 66:705-714.
15. Fischer FR, Santambrogio L, Luo Y, Berman MA, Hancock WW, Dorf ME. 2000. Modulation of experimental autoimmune encephalomyelitis: Effect of altered peptide ligand on chemokine and chemokine receptor expression. J Neuroimmunol 110:195-208.
16. Gangur V, Simons FE, Hayglass KT. 1998. Human IP-10 selectively promotes dominance of polyclonally activated and environmental antigen-driven IFN-gamma over IL-4 responses. FASEB J 12:705-713.
17. Gao P, Zhou XY, Yashiro-Ohtani Y, Yang YF, Sugimoto N, Ono S, Nakanishi T, Obika S, Imanishi T, Egawa T, Nagasawa T, Fujiwara H, Hamaoka T. 2003. The unique target specificity of a nonpeptide chemokine receptor antagonist: Selective blockade of two Th1 chemokine receptors CCR5 and CXCR3. J Leukoc Biol 73:273-280.
18. Glass WG, Lane TE. 2003. Functional expression of chemokine receptor CCR5 on CD4(+) T cells during virus-induced central nervous system disease. J Virol 77:191-198.
19. Glass WG, Liu MT, Kuziel WA, Lane TE. 2001. Reduced macrophage infiltration and demyelination in mice lacking the chemokine receptor CCR5 following infection with a neurotropic coronavirus. Virology 288:8-17.
20. Godiska R, Chantry D, Dietsch GN, Gray PW. 1995. Chemokine expression in murine experimental allergic encephalomyelitis. J Neuroimmunol 58:167-176.
21. Hamilton NH, Banyer JL, Hapel AJ, Mahalingam S, Ramsay AJ, Ramshaw IA, Thomson SA. 2002. IFN-gamma regulates murine interferon-inducible T cell alpha chemokine (I-TAC) expression in dendritic cell lines and during experimental autoimmune encephalomyelitis (EAE). Scand J Immunol 55:171-177.
22. Hancock WW, Gao W, Csizmadia V, Faia KL, Shemmeri N, Luster AD. 2001. Donor-derived IP-10 initiates development of acute allograft rejection. J Exp Med 193:975-980.
23. Hickey WF. 2001. Basic principles of immunological surveillance of the normal central nervous system. Glia 36:118-124.
24. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM. 2001. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J Exp Med 193:713-726.
25. Hvas J, McLean C, Justesen J, Kannourakis G, Steinman L, Oksenberg JR, Bernard CC. 1997. Perivascular T cells express the pro-inflammatory chemokine RANTES mRNA in multiple sclerosis lesions. Scand J Immunol 46:195-203.
26. Johnston C, Jiang W, Chu T, Levine B. 2001. Identification of genes involved in the host response to neurovirulent alphavirus infection. J Virol 75:10431-10445.
27. Kantor R, Bakhanashvili M, Achiron A. 2003. A mutated CCR5 gene may have favorable prognostic implications in MS. Neurology 61:238-240.
28. Karpus WJ, Lukacs NW, McRae BL, Strieter RM, Kunkel SL, Miller SD. 1995. An important role for the chemokine macrophage inflammatory protein-1 alpha in the pathogenesis of the T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis. J Immunol 155:5003-5010.
29. Klein RS, Izikson L, Means T, Gibson HD, Lin E, Sobels RA, Weiner HA, Luster AD. 2004. IP-10/CXCL10-independent induction of experimental autoimmune encephalomyelitis. J Immunol 172:550-559.
30. Lane TE, Asensio VC, Yu N, Paoletti AD, Campbell IL, Buchmeier MJ. 1998. Dynamic regulation of alpha- and beta-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J Immunol 160:970-978.
31. Lane TE, Liu MT, Chen BP, Asensio VC, Samawi RM, Paoletti AD, Campbell IL, Kunkel SL, Fox HS, Buchmeier MJ. 2000. A central role for CD4(+) T cells and RANTES in virus-induced central nervous system inflammation and demyelination. J Virol 74:1415-1424.
32. Letendre SL, Lanier ER, McCutchan JA. 1999. Cerebrospinal fluid beta chemokine concentrations in neurocognitively impaired individuals infected with human immunodeficiency virus type 1. J Infect Dis 180:310-319.
33. Liu MT, Armstrong D, Hamilton TA, Lane TE. 2001a. Expression of Mig (monokine induced by interferon-gamma) is important in T lymphocyte recruitment and host defense following viral infection of the central nervous system. J Immunol 166:1790-1795.
34. Liu MT, Chen BP, Oertel P, Buchmeier MJ, Hamilton TA, Armstrong DA, Lane TE. 2001b. The CXC chemokines IP-10 and Mig are essential in host defense following infection with a neurotropic coronavirus. Adv Exp Med Biol 494:323-327.
35. Liu MT, Keirstead HS, Lane TE. 2001c. Neutralization of the chemokine CXCL10 reduces inflammatory cell invasion and demyelination and improves neurological function in a viral model of multiple sclerosis. J Immunol 167:4091-4097.
36. Luster AD. 1998. Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med 338:436-445.
37. Manchester M, Eto DS, Oldstone MB. 1999. Characterization of the inflammatory response during acute measles encephalitis in NSE-CD46 transgenic mice. J Neuroimmunol 96:207-217.
38. Martin R, McFarland HF. 1995. Immunological aspects of experimental allergic encephalomyelitis and multiple sclerosis. Crit Rev Clin Lab Sci 32:121-182.
39. Matsui M, Weaver J, Proudfoot AE, Wujek JR, Wei T, Richer E, Trapp BD, Rao A, Ransohoff RM. 2002. Treatment of experimental autoimmune encephalomyelitis with the chemokine receptor antagonist Met-RANTES. J Neuroimmunol 128:16-22.
40. Miller DH, Khan OA, Sheremata WA, Blumhardt LD, Rice GP, Libonati MA, Willmer-Hulme AJ, Dalton CM, Miszkiel KA, O'Connor PW. 2003. A controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 348:15-23.
41. Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C. 2002. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci 202:13-23.
42. Misu T, Onodera H, Fujihara K, Matsushima K, Yoshie O, Okita N, Takase S, Itoyama Y. 2001. Chemokine receptor expression on T cells in blood and cerebrospinal fluid at relapse and remission of multiple sclerosis: Imbalance of Th1/Th2-associated chemokine signaling. J Neuroimmunol 114:207-212.
43. Miyagishi R, Kikuchi S, Takayama C, Inoue Y, Tashiro K. 1997. Identification of cell types producing RANTES, MIP-1 alpha and MIP-1 beta in rat experimental autoimmune encephalomyelitis by in situ hybridization. J Neuroimmunol 77:17-26.
44. Morimoto K, Hooper DC, Bornhorst A, Corisdeo S, Bette M, Fu ZF, Schafer MK, Koprowski H, Weihe E, Dietzschold B. 1996. Intrinsic responses to Borna disease virus infection of the central nervous system. Proc Natl Acad Sci USA 93:13345-13350.
45. Narumi S, Kaburaki T, Yoneyama H, Iwamura H, Kobayashi Y, Matsushima K. 2002. Neutralization of IFN-inducible protein 10/CXCL10 exacerbates experimental autoimmune encephalomyelitis. Eur J Immunol 32:1784-1791.
46. Poliani PL, Brok H, Furlan R, Ruffini F, Bergami A, Desina G, Marconi PC, Rovaris M, Uccelli A, Glorioso JC, Penna G, Adorini L, Comi G, t Hart B, Martino G. 2001. Delivery to the central nervous system of a nonreplicative herpes simplex type 1 vector engineered with the interleukin 4 gene protects rhesus monkeys from hyperacute autoimmune encephalomyelitis. Hum Gene Ther 12:905-920.
47. Ransohoff RM, Hamilton TA, Tani M, Stoler MH, Shick HE, Major JA, Estes ML, Thomas DM, Tuohy VK. 1993. Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J 7:592-600.
48. Ransohoff RM, Kivisakk P, Kidd G. 2003. Three or more routes for leukocyte migration into the central nervous system. Nat Immunol 3:569-581.
49. Rauer M, Pagenstecher A, Schulte-Monting J, Sauder C. 2002. Upregulation of chemokine receptor gene expression in brains of Borna disease virus (BDV)-infected rats in the absence and presence of inflammation. J Neurovirol 8:168-179.
50. Rosler A, Pohl M, Braune HJ, Oertel WH, Gemsa D, Sprenger H. 1998. Time course of chemokines in the cerebrospinal fluid and serum during herpes simplex type 1 encephalitis. J Neurol Sci 157:82-89.
51. Rossi D, Zlotnik A. 2000. The biology of chemokines and their receptors. Annu Rev Immunol 18:217-242.
52. Rottman JB, Slavin AJ, Silva R, Weiner HL, Gerard CG, Hancock WW. 2000. Leukocyte recruitment during onset of experimental allergic encephalomyelitis is CCR1 dependent. Eur J Immunol 30:2372-2377.
53. Salmaggi A, Gelati M, Dufour A, Corsini E, Pagano S, Baccalini R, Ferrero E, Scabini S, Silei V, Ciusani E, De Rossi M. 2002. Expression and modulation of IFN-gamma-inducible chemokines (IP-10, Mig, and I-TAC) in human brain endothelium and astrocytes: Possible relevance for the immune invasion of the central nervous system and the pathogenesis of multiple sclerosis. J Interferon Cytokine Res 22:631-640.
54. Sasseville VG, Smith MM, Mackay CR, Pauley DR, Mansfield KG, Ringler DJ, Lackner AA. 1996. Chemokine expression in simian immunodeficiency virus-induced AIDS encephalitis. Am J Pathol 149: 1459-1467.
55. Sauder C, Hallensleben W, Pagenstecher A, Schneckenburger S, Biro L, Pertlik D, Hausmann J, Suter M, Staeheli P. 2000. Chemokine gene expression in astrocytes of Borna disease virus-infected rats and mice in the absence of inflammation. J Virol 74:9267-9280.
56. Seeldrayers PA, Syha J, Morrissey SP, Stodal H, Vass K, Jung S, Gneiting T, Lassmann H, Haase A, Hartung HP, Toyka KV. 1993. Magnetic resonance imaging investigation of blood-brain barrier damage in adoptive transfer experimental autoimmune encephalomyelitis. J Neuroimmunol 46:199-206.
57. Sorensen TL, Tani M, Jensen J, Pierce V, Lucchinetti C, Folcik VA, Qin S, Rottman J, Sellebjerg F, Strieter RM, Frederiksen JL, Ransohoff RM. 1999. Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 103:807-815.
58. Swanborg RH. 1995. Experimental autoimmune encephalomyelitis in rodents as a model for human demyelinating disease. Clin Immunol Immunopathol 77:4-13.
59. Tran EH, Kuziel WA, Owens T. 2000. Induction of experimental autoimmune encephalomyelitis in C57BL/6 mice deficient in either the chemokine macrophage inflammatory protein-lalpha or its CCR5 receptor. Eur J Immunol 30:1410-1415.
60. Trifilo MJ, Lane TE. 2003. Adenovirus-mediated expression of CXCL10 in the central nervous system results in T-cell recruitment and limited neuropathology. J Neurovirol 9:315-324.
61. Westmoreland SV, Rottman JB, Williams KC, Lackner AA, Sasseville VG. 1998. Chemokine receptor expression on resident and inflammatory cells in the brain of macaques with simian immunodeficiency virus encephalitis. Am J Pathol 152:659-665.
62. Wildbaum G, Netzer N, Karin N. 2002. Plasmid DNA encoding IFN-gamma-inducible protein 10 redirects antigen-specific T cell polarization and suppresses experimental autoimmune encephalomyelitis. J Immunol 168:5885-5892.
63. Yoneyama H, Narumi S, Zhang Y, Murai M, Baggiolini M, Lanzavecchia A, Ichida T, Asakura H, Matsushima K. 2002. Pivotal role of dendritic cell-derived CXCL10 in the retention of T helper cell 1 lymphocytes in secondary lymph nodes. J Exp Med 195:1257-1266.
64. Youssef S, Wildbaum G, Maor G, Lanir N, Gour-Lavie A, Grabie N, Karin N. 1998. Long-lasting protective immunity to experimental autoimmune encephalomyelitis following vaccination with naked DNA encoding C-C chemokines. J Immunol 161:3870-3879.