Opposing roles for CXCR3 signaling in central nervous system versus ocular inflammation mediated by the astrocyte-targeted production of IL-12

American Journal of Pathology

Volumn 179, Issue 5, 2011, Pages 2346-2359

  Krauthausen, Marius ^a   Ellis, Sally L ^b   Zimmermann, Julian ^a   Sarris, Maria ^c   Wakefield, Denis ^c   Heneka, Michael T ^a   Campbell, Iain L ^b   Mller, Marcus ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD3 ANTIGEN; CHEMOKINE RECEPTOR CXCR3; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1; INTERLEUKIN 12; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ATAXIA; ATROPHY; CATARACT; CENTRAL NERVOUS SYSTEM; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENCEPHALITIS; EYE INFLAMMATION; IMMUNE RESPONSE; LENS DISEASE; MOUSE; MUELLER CELL; NATURAL KILLER CELL; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA CELL; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; BLINDNESS; CEREBELLAR ATAXIA; ENCEPHALITIS; ENDOPHTHALMITIS; EYE DISEASES; GENOTYPE; IMMUNITY, CELLULAR; INTERFERON-GAMMA; INTERLEUKIN-12; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; PHOSPHORYLATION; RECEPTORS, CCR5; RECEPTORS, CXCR3; RECEPTORS, INTERLEUKIN-12; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT4 TRANSCRIPTION FACTOR;

EID: 80054981620     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.07.041     Document Type: Article

References (50)

1. S. Rivest Regulation of innate immune responses in the brain Nat Rev Immunol 9 2009 429 439
2. C.D. Conrady, D.A. Drevets, and D.J.J. Carr Herpes simplex type I (HSV-1) infection of the nervous system: is an immune response a good thing? J Neuroimmunol 220 2010 1 9
3. R. Gandhi, A. Laroni, and H.L. Weiner Role of the innate immune system in the pathogenesis of multiple sclerosis J Neuroimmunol 221 2010 7 14
4. I.F. Charo, and R.M. Ransohoff The many roles of chemokines and chemokine receptors in inflammation N Engl J Med 354 2006 610 621
5. A.E. Cardona, M. Li, L. Liu, C. Savarin, and R.M. Ransohoff Chemokines in and out of the central nervous system: much more than chemotaxis and inflammation J Leukoc Biol 84 2008 587 594
6. M. Mller, S. Carter, M.J. Hofer, and I.L. Campbell Review: the chemokine receptor CXCR3 and its ligands CXCL9 CXCL10 and CXCL11 in neuroimmunity: a tale of conflict and conundrum Neuropathol Appl Neurobiol 36 2010 368 387
7. L. Liu, M.K. Callahan, D.R. Huang, and R.M. Ransohoff Chemokine receptor CXCR3: an unexpected enigma Curr Top Dev Biol 68 2005 149
8. K. Biber, I. Dijkstra, C. Trebst, C.J.A. De Groot, R.M. Ransohoff, and H. Boddeke Functional expression of CXCR3 in cultured mouse and human astrocytes and microglia Neurosci 112 2002 487 497
9. A. Rappert, I. Bechmann, T. Pivneva, J. Mahlo, K. Biber, C. Nolte, A.D. Kovac, C. Gerard, H.W. Boddeke, R. Nitsch, and H. Kettenmann CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion J Neurosci 24 2004 8500
10. M. Cella, D. Jarrossay, F. Facchetti, O. Alebardi, H. Nakajima, A. Lanzavecchia, and M. Colonna Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon Nat Med 5 1999 919 923
11. Y. Weng, S.J. Siciliano, K.E. Waldburger, A. Sirotina-Meisher, M.J. Staruch, B.L. Daugherty, S.L. Gould, M.S. Springer, and J.A. DeMartino Binding and functional properties of recombinant and endogenous CXCR3 chemokine receptors J Biol Chem 273 1998 18288 18291
12. M. Loetscher, P. Loetscher, N. Brass, E. Meese, and B. Moser Lymphocyte-specific chemokine receptor CXCR3: regulation, chemokine binding and gene localization Eur J Immunol 28 1998 3696 3705
13. K.E. Cole, C.A. Strick, T.J. Paradis, K.T. Ogborne, M. Loetscher, R.P. Gladue, W. Lin, J.G. Boyd, B. Moser, D.E. Wood, B.G. Sahagan, and K. Neote Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3 J Exp Med 187 1998 2009 2021
14. I.A. Ferber, S. Brocke, C. Taylor-Edwards, W. Ridgway, C. Dinisco, L. Steinman, D. Dalton, and C.G. Fathman Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE) J Immunol 156 1996 5 7
15. A.D. Luster, J.C. Unkeless, and J.V. Ravetch Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins Nature 315 1985 672 676
16. T.S. Kim, B.Y. Kang, M.H. Lee, Y.K. Choe, and S.Y. Hwang Inhibition of interleukin-12 production by auranofin, an anti-rheumatic gold compound, deviates CD4(+) T cells from the Th1 to the Th2 pathway Br J Pharmacol 134 2001 571 578
17. M. Loetscher, B. Gerber, P. Loetscher, S.A. Jones, L. Piali, I. Clark-Lewis, M. Baggiolini, and B. Moser Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes J Exp Med 184 1996 963 969
18. T.L. Sørensen, C. Trebst, P. Kiviskk, K.L. Klaege, A. Majmudar, R. Ravid, H. Lassmann, D.B. Olsen, R.M. Strieter, R.M. Ransohoff, and F. Sellebjerg Multiple sclerosis: a study of CXCL10 and CXCR3 co-localization in the inflamed central nervous system J Neuroimmunol 127 2002 59 68
19. P. Kiviskk, C. Trebst, Z. Liu, B.H. Tucky, T.L. Sørensen, R.A. Rudick, M. Mack, and R.M. Ransohoff T-cells in the cerebrospinal fluid express a similar repertoire of inflammatory chemokine receptors in the absence or presence of CNS inflammation: implications for CNS trafficking Clin Exp Immunol 129 2002 510 518
20. K.E. Balashov, J.B. Rottman, H.L. Weiner, and W.W. Hancock 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 U S A 96 1999 6873 6878
21. B.T. Fife, K.J. Kennedy, M.C. Paniagua, N.W. Lukacs, S.L. Kunkel, A.D. Luster, and W.J. Karpus 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 2001 7617 7624
22. S. Narumi, T. Kaburaki, H. Yoneyama, H. Iwamura, Y. Kobayashi, and K. Matsushima Neutralization of IFN-inducible protein 10/CXCL10 exacerbates experimental autoimmune encephalomyelitis Eur J Immunol 32 2002 1784 1791
23. R.S. Klein, L. Izikson, T. Means, H.D. Gibson, E. Lin, R.A. Sobel, H.L. Weiner, and A.D. Luster IFN-inducible protein 10/CXC chemokine ligand 10-independent induction of experimental autoimmune encephalomyelitis J Immunol 172 2004 550 559
24. M. Mller, S.L. Carter, M.J. Hofer, P. Manders, D.R. Getts, M.T. Getts, A. Dreykluft, B. Lu, C. Gerard, N.J.C. King, and I.L. Campbell CXCR3 signaling reduces the severity of experimental autoimmune encephalomyelitis by controlling the parenchymal distribution of effector and regulatory T cells in the central nervous system J Immunol 179 2007 2774 2786
25. A. Pagenstecher, S. Lassmann, M.J. Carson, C.L. Kincaid, A.K. Stalder, and I.L. Campbell Astrocyte-targeted expression of IL-12 induces active cellular immune responses in the central nervous system and modulates experimental allergic encephalomyelitis J Immunol 164 2000 4481 4492
26. M. Hofer, J. Hausmann, P. Staeheli, and A. Pagenstecher Cerebral expression of interleukin-12 induces neurological disease via differential pathways and recruits antigen-specific T cells in virus-infected mice Am J Pathol 165 2004 949 958
27. W.W. Hancock, B. Lu, W. Gao, V. Csizmadia, K. Faia, J.A. King, S.T. Smiley, M. Ling, N.P. Gerard, and C. Gerard Requirement of the chemokine receptor CXCR3 for acute allograft rejection J Exp Med 192 2000 1515 1520
28. A. Quintana, M. Muller, R.F. Frausto, R. Ramos, D.R. Getts, E. Sanz, M.J. Hofer, M. Krauthausen, N.J.C. King, J. Hidalgo, and I.L. Campbell Site-specific production of IL-6 in the central nervous system retargets and enhances the inflammatory response in experimental autoimmune encephalomyelitis J Immunol 183 2009 2079 2088
29. S.S. Ousman, and I.L. Campbell Regulation of murine interferon regulatory factor gene expression in the central nervous system determined by multiprobe RNase protection assay Methods Mol Med 116 2005 115
30. K.P. Dudov, and R.P. Perry The gene family encoding the mouse ribosomal protein L32 contains a uniquely expressed intron-containing gene and an unmutated processed gene Cell 37 1984 457 468
31. S. Schrum, P. Probst, B. Fleischer, and P.F. Zipfel Synthesis of the CC-chemokines MIP-1alpha, MIP-1beta, and RANTES is associated with a type 1 immune response J Immunol 157 1996 3598 3604
32. F. Sallusto, A. Lanzavecchia, and C.R. Mackay Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses Immunol Today 19 1998 568 574
33. F. Malecaze, S. Clamens, V. Simorre-Pinatel, A. Mathis, P. Chollet, C. Favard, F. Bayard, and J. Plouet Detection of vascular endothelial growth factor messenger RNA and vascular endothelial growth factor-like activity in proliferative diabetic retinopathy Arch Ophthalmol 112 1994 1476 1482
34. T.A. Rupprecht, U. Koedel, B. Muhlberger, B. Wilske, A. Fontana, and H. Pfister CXCL11 is involved in leucocyte recruitment to the central nervous system in neuroborreliosis J Neurol 252 2005 820 823
35. S.Z. Lepej, O.D. Rode, T. Jeren, A. Vince, A. Remenar, and B. Barsi Increased expression of CXCR3 and CCR5 on memory CD4+ T-cells migrating into the cerebrospinal fluid of patients with neuroborreliosis: the role of CXCL10 and CXCL11 J Neuroimmunol 163 2005 128 134
36. I. Tsunoda, T.E. Lane, J. Blackett, and R.S. Fujinami Distinct roles for IP-10/CXCL10 in three animal models: Theiler's virus infection EAE, and MHV infection, for multiple sclerosis: implication of differing roles for IP-10 Mult Scler 10 2004 26 34
37. L.P. Liu, D.R. Huang, M. Matsui, T.T. He, T. Hu, J. DeMartino, B. Lu, C. Gerard, and R.M. Ransohoff Severe disease, unaltered leukocyte migration, and reduced IFN-gamma production in CXCR3-/- mice with experimental autoimmune encephalomyelitis J Immunol 176 2006 4399 4409
38. J.H. Xie, N. Nomura, M. Lu, S. Chen, G.E. Koch, Y. Weng, R. Rosa, J. Di Salvo, J. Mudgett, L.B. Peterson, L.S. Wicker, and J.A. DeMartino Antibody-mediated blockade of the CXCR3 chemokine receptor results in diminished recruitment of T helper 1 cells into sites of inflammation J Leukoc Biol 73 2003 771 780
39. P. Gao, X. Zhou, Y. Yashiro-Ohtani, Y. Yang, N. Sugimoto, S. Ono, T. Nakanishi, S. Obika, T. Imanishi, T. Egawa, T. Nagasawa, H. Fujiwara, and T. Hamaoka The unique target specificity of a nonpeptide chemokine receptor antagonist: selective blockade of two Th1 chemokine receptors CCR5 and CXCR3 J Leukoc Biol 73 2003 273 280
40. M.K. Gately, L.M. Renzetti, J. Magram, A.S. Stern, L. Adorini, U. Gubler, and D.H. Presky The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses Annu Rev Immunol 16 1998 495 521
41. C. Wenner, M. Guler, S. Macatonia, A. O'Garra, and K. Murphy Roles of IFN-gamma and IFN-alpha in IL-12-induced T helper cell-1 development J Immunol 156 1996 1442 1447
42. T. Komatsu, Z. Bi, and C.S. Reiss Interferon-gamma induced type I nitric oxide synthase activity inhibits viral replication in neurons J Neuroimmunol 68 1996 101 108
43. G.K. Binder, and D.E. Griffin Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons Science 293 2001 303 306
44. D.A. Chesler, and C.S. Reiss The role of IFN-[gamma] in immune responses to viral infections of the central nervous system Cytokine Growth Factor Rev 13 2002 441 454
45. K. Boztug, M.J. Carson, N. Pham-Mitchell, V.C. Asensio, J. DeMartino, and I.L. Campbell Leukocyte infiltration, but not neurodegeneration, in the CNS of transgenic mice with astrocyte production of the CXC chemokine ligand 10 J Immunol 169 2002 1505 1515
46. K.D. Geiger, and N.E. Sarvetnick Transgenic expression of IFN-g in the eye as a model for studying ocular inflammatory disease Methods 10 1996 392 405
47. J.E. Christensen, A. Nansen, T. Moos, B. Lu, C. Gerard, J.P. Christensen, and A.R. Thomsen Efficient T-cell surveillance of the CNS requires expression of the CXC chemokine receptor 3 J Neurosci 24 2004 4849 4858
48. T.J. D'Orazio, and J.Y. Niederkorn A novel role for TGF-β and IL-10 in the induction of immune privilege J Immunol 160 1998 2089 2098
49. I. Galea, I. Bechmann, and V.H. Perry What is immune privilege (not) Trends Immunol 28 2007 12 18
50. I. Petrai, K. Rombouts, L. Lasagni, F. Annunziato, L. Cosmi, R.G. Romanelli, C. Sagrinati, B. Mazzinghi, M. Pinzani, S. Romagnani, P. Romagnani, and F. Marra Activation of p38 (MAPK) mediates the angiostatic effect of the chemokine receptor CXCR3-B Int J Biochem Cell Biol 40 2008 1764 1774