A destructive feedback loop mediated by CXCL10 in central nervous system inflammatory disease

Annals of Neurology

Volumn 78, Issue 4, 2015, Pages 619-629

  Roberts, Wendy K ^a,e   Blachère, Nathalie E ^a   Frank, Mayu O ^a   Dousmanis, Athanasios ^b   Ransohoff, Richard M ^c,f   Darnell, Robert B ^a,d  

^a ROCKEFELLER UNIVERSITY   (United States)

^b Department of Medicine   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d NEW YORK GENOME CENTER   (United States)

^e UNIVERSITY OF NEW ENGLAND   (United States)

^f BIOGEN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL3 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GAMMA INTERFERON RECEPTOR; PREDNISONE; TACROLIMUS; AUTACOID; BIOLOGICAL MARKER; CXCL10 PROTEIN, HUMAN; IMMUNOSUPPRESSIVE AGENT;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID ANALYSIS; CLINICAL ARTICLE; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; HUMAN; HUMAN CELL; INTERFERON PRODUCTION; LEUKOCYTE COUNT; MIDDLE AGED; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PARANEOPLASTIC NEUROPATHY; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CENTRAL NERVOUS SYSTEM DISEASES; CEREBROSPINAL FLUID; DRUG EFFECTS; INFLAMMATION; KNOCKOUT MOUSE; MALE; PARANEOPLASTIC SYNDROMES, NERVOUS SYSTEM; PHYSIOLOGY;

AGED; ANIMALS; BIOMARKERS; CENTRAL NERVOUS SYSTEM DISEASES; CHEMOKINE CXCL10; FEEDBACK, PHYSIOLOGICAL; FEMALE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; PARANEOPLASTIC SYNDROMES, NERVOUS SYSTEM; TACROLIMUS;

EID: 84942372122     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24494     Document Type: Article

References (39)

1. Darnell RB, Posner JB,. Paraneoplastic syndromes affecting the nervous system. Semin Oncol 2006; 33: 270-298.
2. Darnell RB,. Onconeural antigens and the paraneoplastic neurologic disorders: at the intersection of cancer, immunity, and the brain. Proc Natl Acad Sci U S A 1996; 93: 4529-4536.
3. Roberts WK, Darnell RB,. Neuroimmunology of the paraneoplastic neurological degenerations. Curr Opin Immunol 2004; 16: 616-622.
4. Albert ML, Austin LM, Darnell RB,. Detection and treatment of activated T cells in the cerebrospinal fluid of patients with paraneoplastic cerebellar degeneration. Ann Neurol 2000; 47: 9-17.
5. Albert ML, Darnell JC, Bender A, et al., Tumor-specific killer cells in paraneoplastic cerebellar degeneration. Nat Med 1998; 4: 1321-1324.
6. Roberts WK, Deluca IJ, Thomas A, et al., Patients with lung cancer and paraneoplastic Hu syndrome harbor HuD-specific type 2 CD8+ T cells. J Clin Invest 2009; 119: 2042-2051.
7. Orange D, Frank M, Tian S, Dousmanis A, et al., Cellular immune suppression in paraneoplastic neurologic syndromes targeting intracellular antigens. Arch Neurol 2012; 69: 1132-1140.
8. Schreiber S, Crabtree G,. The mechanism of action of cyclosporin A and FK506. Immunol Today 1992; 13: 136-142.
9. Sawada S, Suzuki G, Kawase Y, Takaku F,. Novel immunosuppressive agent, FK506. In vitro effects on the cloned T cell activation. J Immunol 1987; 139: 1797-1803.
10. Snyder SH, Lai MM, Burnett PE,. Immunophilins in the nervous system. Neuron 1998; 21: 283-294.
11. Klein RS, Lin E, Zhang B, et al., Neuronal CXCL10 directs CD8+ T cell recruitment and control of West Nile virus encephalitis. J Virol 2005; 79: 11457-11466.
12. Engelhardt B, Ransohoff RM,. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 2005; 26: 485-495.
13. Sørensen T, Trebst C, Kivisakk P, et al., Multiple sclerosis: a study of CXCL10 and CXCR3 co-localization in the inflamed central nervous system. J Neuroimmunol 2002; 127: 59-68.
14. Blachere NE, Darnell RB, Albert ML,. Apoptotic cells deliver processed antigen to dendritic cells for cross-presentation. PLoS Biol 2005; 3: e185.
15. Sorensen TL, Tani M, Jensen J, et al., Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J Clin Invest 1999; 103: 807-815.
16. Chang CC, Omarjee S, Lim A, et al., Chemokine levels and chemokine receptor expression in the blood and the cerebrospinal fluid of HIV-infected patients with cryptococcal meningitis and cryptococcosis-associated immune reconstitution inflammatory syndrome. J Infect Dis 2013; 208: 1604-1612.
17. Kamat A, Lyons JL, Misra V, et al., Monocyte activation markers in cerebrospinal fluid associated with impaired neurocognitive testing in advanced HIV infection. J Acquir Immune Defic Syndr 2012; 60: 234-243.
18. Henningsson AJ, Tjernberg I, Malmvall BE, et al., Indications of Th1 and Th17 responses in cerebrospinal fluid from patients with Lyme neuroborreliosis: a large retrospective study. J Neuroinflammation 2011; 8: 36.
19. Dufour JH, Dziejman M, Liu MT, et al., 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 2002; 168: 3195-3204.
20. Luster AD, Ravetch JV,. Biochemical characterization of a gamma interferon-inducible cytokine (IP-10). J Exp Med 1987; 166: 1084-1097.
21. Wang J, Campbell IL,. Innate STAT1-dependent genomic response of neurons to the antiviral cytokine alpha interferon. J Virol 2005; 79: 8295-8302.
22. Balashov KE, Rottman JB, Weiner HL, Hancock WW,. 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 1999; 96: 6873-6878.
23. Santomasso BD, Roberts WK, Thomas A, et al., A T cell receptor associated with naturally occurring human tumor immunity. Proc Natl Acad Sci U S A 2007; 104: 19073-19078.
24. Groom JR, Richmond J, Murooka TT, et al., CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 2012; 37: 1091-1103.
25. Flynn G, Maru S, Loughlin J, et al., Regulation of chemokine receptor expression in human microglia and astrocytes. J Neuroimmunol 2003; 136: 84-93.
26. Millward JM, Caruso M, Campbell IL, et al., IFN-gamma-induced chemokines synergize with pertussis toxin to promote T cell entry to the central nervous system. J Immunol 2007; 178: 8175-8182.
27. Gangur V, Simons FE, Hayglass KT,. Human IP-10 selectively promotes dominance of polyclonally activated and environmental antigen-driven IFN-gamma over IL-4 responses. FASEB J 1998; 12: 705-713.
28. Liu L, Huang D, Matsui M, et al., Severe disease, unaltered leukocyte migration, and reduced IFN-gamma production in CXCR3-/- mice with experimental autoimmune encephalomyelitis. J Immunol 2006; 176: 4399-4409.
29. Groom JR, Luster AD,. CXCR3 in T cell function. Exp Cell Res 2011; 317: 620-631.
30. Klein RS, Izikson L, Means T, et al., IFN-inducible protein 10/CXC chemokine ligand 10-independent induction of experimental autoimmune encephalomyelitis. J Immunol 2004; 172: 550-559.
31. Park C, Lee S, Cho IH, et al., TLR3-mediated signal induces proinflammatory cytokine and chemokine gene expression in astrocytes: differential signaling mechanisms of TLR3-induced IP-10 and IL-8 gene expression. Glia 2006; 53: 248-256.
32. Glabinski AR, Tani M, Strieter RM, et al., Synchronous synthesis of alpha- and beta-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic experimental autoimmune encephalomyelitis. Am J Pathol 1997; 150: 617-630.
33. Matsuda S, Shibasaki F, Takehana K, et al., Two distinct action mechanisms of immunophilin-ligand complexes for the blockade of T cell activation. EMBO Rep 2000; 1: 428-434.
34. Orange DE, Blachere NE, Fak J, et al., Dendritic cells loaded with FK506 kill T cells in an antigen-specific manner and prevent autoimmunity in vivo. Elife 2013; 2: e00105.
35. Gold BG, Voda J, Yu X, et al., FK506 and a nonimmunosuppressant derivative reduce axonal and myelin damage in experimental autoimmune encephalomyelitis: neuroimmunophilin ligand-mediated neuroprotection in a model of multiple sclerosis. J Neurosci Res 2004; 77: 367-377.
36. Inamura N, Hashimoto M, Nakahara K, et al., Immunosuppressive effect of FK506 on experimental allergic encephalomyelitis in rats. Int J Immunopharmacol 1988; 10: 991-995.
37. Chang KT, Lin HY, Kuo CH, Hung CH,. Tacrolimus suppresses atopic dermatitis-associated cytokines and chemokines in monocytes. J Microbiol Immunol Infect. http://dx.doi.org/10.1016/j.jmii.2014.07.006 (in press).
38. Cristillo AD, Macri MJ, Bierer BE,. Differential chemokine expression profiles in human peripheral blood T lymphocytes: dependence on T cell coreceptor and calcineurin signaling. Blood 2003; 101: 216-225.
39. Bailey SL, Schreiner B, McMahon EJ, Miller SD,. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE. Nat Immunol 2007; 8: 172-180.