Gamma interferon signaling in macrophage lineage cells regulates central nervous system inflammation and chemokine production

Journal of Virology

Volumn 83, Issue 17, 2009, Pages 8604-8615

  Lin, Adora A ^a   Tripathi, Pulak K ^a   Sholl, Allyson ^a   Jordan, Michael B ^a   Hildeman, David A ^a,b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GAMMA INTERFERON RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOREXIA; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL LINEAGE; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME REGULATION; HEMATOPOIETIC CELL; IMMUNOREGULATION; INFLAMMATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T CELL DEPLETION; TRANSGENIC MOUSE; VIRUS INFECTION; WEIGHT REDUCTION; ANIMAL; BIOSYNTHESIS; BODY WEIGHT; C57BL MOUSE; HUMAN; IMMUNOLOGY; MOUSE MUTANT; PATHOLOGY;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MUS; MUS MUSCULUS;

ANIMALS; ANOREXIA; BODY WEIGHT; CD4-POSITIVE T-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM; CHEMOKINES; HUMANS; INFLAMMATION; INTERFERON-GAMMA; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION;

EID: 69249211171     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02477-08     Document Type: Article

References (82)

1. Ahmed, R., A. Salmi, L. D. Butler, J. M. Chiller, and M. B. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice: role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160:521-540.
2. Asensio, V. C., and I. L. Campbell. 1997. Chemokine gene expression in the brains of mice with lymphocytic choriomeningitis. J. Virol. 71:7832-7840.
3. Banisadr, G., F. Queraud-Lesaux, M. C. Boutterin, D. Pelaprat, B. Zalc, W. Rostene, F. Haour, and S. M. Parsadaniantz. 2002. Distribution, cellular localization, and functional role of CCR2 chemokine receptors in adult rat brain. J. Neurochem. 81:257-269. (Pubitemid 34809350)
4. Barnes, D. A., M. Huston, R. Holmes, E. N. Benveniste, V. W. Yong, P. Scholz, and H. D. Perez. 1996. Induction of RANTES expression by astrocytes and astrocytoma cell lines. J. Neuroimmunol. 71:207-214. (Pubitemid 26413274)
5. Benveniste, E. N. 1992. Inflammatory cytokines within the central nervous system: sources, function, and mechanism of action. Am. J. Physiol. 263:C1-C16.
6. Buchmeier, M. J., R. M. Welsh, F. J. Dutko, and M. B. Oldstone. 1980. The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv. Immunol. 30:275-331.
7. Campbell, I. L., M. V. Hobbs, P. Kemper, and M. B. Oldstone. 1994. Cerebral expression of multiple cytokine genes in mice with lymphocytic choriomeningitis. J. Immunol. 152:716-723. (Pubitemid 24072975)
8. Ceredig, R., J. E. Allan, Z. Tabi, F. Lynch, and P. C. Doherty. 1987. Phenotypic analysis of the inflammatory exudate in murine lymphocytic choriomeningitis. J. Exp. Med. 165:1539-1551.
9. + effector T cells involved in immune surveillance of the lymphocytic choriomeningitis virus-infected central nervous system. J. Immunol. 176:4235-4243.
10. Crawford, F., H. Kozono, J. White, P. Marrack, and J. Kappler. 1998. Detection of antigen-specific T cells with multivalent soluble class II MHC covalent peptide complexes. Immunity 8:675-682. (Pubitemid 28294514)
11. Crotty, S., M. M. McCausland, R. D. Aubert, E. J. Wherry, and R. Ahmed. 2006. Hypogammaglobulinemia and exacerbated CD8 T-cell-mediated immunopathology in SAP-deficient mice with chronic LCMV infection mimics human XLP disease. Blood 108:3085-3093.
12. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742. (Pubitemid 23114658)
13. + T cell-mediated inflammation in the central nervous system of virus-infected mice. J. Immunol. 175:1767-1775.
14. Dhillon, N. K., F. Peng, R. M. Ransohoff, and S. Buch. 2007. PDGF syner-gistically enhances IFN-gamma-induced expression of CXCL10 in bloodderived macrophages: implications for HIV dementia. J. Immunol. 179: 2722-2730.
15. Dighe, A. S., D. Campbell, C. S. Hsieh, S. Clarke, D. R. Greaves, S. Gordon, K. M. Murphy, and R. D. Schreiber. 1995. Tissue-specific targeting of cytokine unresponsiveness in transgenic mice. Immunity 3:657-666.
16. Dighe, A. S., M. A. Farrar, and R. D. Schreiber. 1993. Inhibition of cellular responsiveness to interferon-gamma (IFN gamma) induced by overexpression of inactive forms of the IFN gamma receptor. J. Biol. Chem. 268:10645-10653.
17. Doherty, P. C., S. Hou, and P. J. Southern. 1993. Lymphocytic choriomeningitis virus induces a chronic wasting disease in mice lacking class I major histocompatibility complex glycoproteins. J. Neuroimmunol. 46:11-17.
18. Doherty, P. C., and R. M. Zinkernagel. 1974. T-cell-mediated immunopathology in viral infections. Transplant Rev. 19:89-120.
19. Dominguez-Punaro, M. C., M. Segura, M. M. Plante, S. Lacouture, S. Rivest, and M. Gottschalk. 2007. Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J. Immunol. 179:1842-1854.
20. Farina, C., M. Krumbholz, T. Giese, G. Hartmann, F. Aloisi, and E. Meinl. 2005. Preferential expression and function of Toll-like receptor 3 in human astrocytes. J. Neuroimmunol. 159:12-19. (Pubitemid 40126172)
21. Fleming, J. O., J. Y. Ting, S. A. Stohlman, and L. P. Weiner. 1983. Improvements in obtaining and characterizing mouse cerebrospinal fluid: application to mouse hepatitis virus-induced encephalomyelitis. J. Neuroimmunol. 4:129-140.
22. + T cells compared. J. Immunol. 154:4309-4321.
23. Frei, K., T. P. Leist, A. Meager, P. Gallo, D. Leppert, R. M. Zinkernagel, and A. Fontana. 1988. Production of B-cell stimulatory factor-2 and interferon gamma in the central nervous system during viral meningitis and encephalitis. Evaluation in a murine model infection and in patients. J. Exp. Med. 168:449-453.
24. Fung-Leung, W. P., T. M. Kundig, R. M. Zinkernagel, and T. W. Mak. 1991. Immune response against lymphocytic choriomeningitis virus infection in mice without CD8 expression. J. Exp. Med. 174:1425-1429.
25. Gerard, C., and B. J. Rollins. 2001. Chemokines and disease. Nat. Immunol. 2:108-115.
26. Glabinski, A. R., M. Krakowski, Y. Han, T. Owens, and R. M. Ransohoff. 1999. Chemokine expression in GKO mice (lacking interferon-gamma) with experimental autoimmune encephalomyelitis. J. Neurovirol. 5:95-101.
27. Glabinski, A. R., M. Tani, R. M. Strieter, V. K. Tuohy, and R. M. Ransohoff. 1997. 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. 150:617-630.
28. Glabinski, A. R., M. Tani, V. K. Tuohy, R. J. Tuthill, and R. M. Ransohoff. 1995. Central nervous system chemokine mRNA accumulation follows initial leukocyte entry at the onset of acute murine experimental autoimmune encephalomyelitis. Brain Behav. Immun. 9:315-330.
29. Glabinski, A. R., V. K. Tuohy, and R. M. Ransohoff. 1998. Expression of chemokines RANTES, MIP-1α, and GRO-α correlates with inflammation in acute experimental autoimmune encephalomyelitis. Neuroimmunomodulation 5:166-171.
30. Haring, J. S., V. P. Badovinac, M. R. Olson, S. M. Varga, and J. T. Harty. 2005. In vivo generation of pathogen-specific Th1 cells in the absence of the IFN-γ receptor. J. Immunol. 175:3117-3122.
31. Hayashi, M., Y. Luo, J. Laning, R. M. Strieter, and M. E. Dorf. 1995. Production and function of monocyte chemoattractant protein-1 and other beta-chemokines in murine glial cells. J. Neuroimmunol. 60:143-150.
32. Hedegaard, C. J., M. Krakauer, K. Bendtzen, H. Lund, F. Sellebjerg, and C. H. Nielsen. 2008. T helper cell type 1 (Th1), Th2, and Th17 responses to myelin basic protein and disease activity in multiple sclerosis. Immunology 125:161-169.
33. Hildeman, D., and D. Muller. 2000. Immunopathologic weight loss in intracranial LCMV infection initiated by the anorexigenic effects of IL-1β. Viral Immunol. 13:273-285. (Pubitemid 30728971)
34. Hirsch, M. S., F. A. Murphy, and M. D. Hicklin. 1968. Immunopathology of lymphocytic choriomeningitis viurs infection of newborn mice: antithymocyte serum effects on glomerulonephritis and wasting disease. J. Exp. Med. 127: 757-766.
35. + T-cell memory. Nat. Med. 7:913-919.
36. Hurwitz, A. A., W. D. Lyman, and J. W. Berman. 1995. Tumor necrosis factor alpha and transforming growth factor beta upregulate astrocyte expression of monocyte chemoattractant protein-1. J. Neuroimmunol. 57:193-198.
37. Kagi, D., B. Ledermann, K. Burki, P. Seiler, B. Odermatt, K. J. Olsen, E. R. Podack, R. M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369:31-37. (Pubitemid 24144352)
38. Kamperschroer, C., and D. G. Quinn. 2002. The role of proinflammatory cytokines in wasting disease during lymphocytic choriomeningitis virus infection. J. Immunol. 169:340-349. (Pubitemid 34686154)
39. Karman, J., C. Ling, M. Sandor, and Z. Fabry. 2004. Dendritic cells in the initiation of immune responses against central nervous system-derived antigens. Immunol. Lett. 92:107-115.
40. + T cells. Science 248:1227-1230.
41. Lane, T. E., J. L. Hardison, and K. B. Walsh. 2006. Functional diversity of chemokines and chemokine receptors in response to viral infection of the central nervous system. Curr. Top. Microbiol. Immunol. 303:1-27.
42. + T cells and RANTES in virus-induced central nervous system inflammation and demyelination. J. Virol. 74:1415-1424.
43. Lang, R., R. L. Rutschman, D. R. Greaves, and P. J. Murray. 2002. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J. Immunol. 168:3402-3411. (Pubitemid 34250404)
44. Langer, J. A., and S. Pestka. 1988. Interferon receptors. Immunol. Today 9:393-400.
45. Lathey, J. L., and M. B. Oldstone. 1988. Weight loss in obese mice persistently infected with lymphocytic choriomeningitis virus is not associated with elevated tumor necrosis factor/cachectin activity in peritoneal macrophages. Am. J. Pathol. 132:586-592.
46. 2-microglobulin gene. J. Virol. 67:332-339.
47. Li, H., Z. Gang, H. Yuling, X. Luokun, X. Jie, L. Hao, W. Li, H. Chunsong, L. Junyan, J. Mingshen, J. Youxin, G. Feili, J. Boquan, and T. Jinquan. 2006. Different neurotropic pathogens elicit neurotoxic CCR9- or neurosupportive CXCR3-expressing microglia. J. Immunol. 177:3644-3656. (Pubitemid 44359896)
48. Marques, C. P., S. Hu, W. Sheng, and J. R. Lokensgard. 2006. Microglial cells initiate vigorous yet non-protective immune responses during HSV-1 brain infection. Virus Res. 121:1-10.
49. Milanes-Virelles, M. T., I. Garcia-Garcia, Y. Santos-Herrera, M. Valdes-Quintana, C. M. Valenzuela-Silva, G. Jimenez-Madrigal, T. I. Ramos-Gomez, I. Bello-Rivero, N. Fernandez-Olivera, R. B. Sanchez-de la Osa, C. Rodriguez-Acosta, L. Gonzalez-Mendez, G. Martinez-Sanchez, and P. A. Lopez-Saura. 2008. Adjuvant interferon gamma in patients with pulmonary atypical mycobacteriosis: a randomized, double-blind, placebo-controlled study. BMC Infect. Dis. 8:17.
50. Millward, J. M., M. Caruso, I. L. Campbell, J. Gauldie, and T. Owens. 2007. IFN-γ-induced chemokines synergize with pertussis toxin to promote T cell entry to the central nervous system. J. Immunol. 178:8175-8182.
51. Muhlethaler-Mottet, A., W. Di Berardino, L. A. Otten, and B. Mach. 1998. Activation of the MHC class II transactivator CIITA by interferon-gamma requires cooperative interaction between Stat1 and USF-1. Immunity 8:157-166. (Pubitemid 28123743)
52. 2-microglobulin-deficient mice. Immunology 86:162-167.
53. 2-microglobulin-deficient mice. Science 255:1576-1578.
54. Owens, T. 2003. The enigma of multiple sclerosis: inflammation and neuro-degeneration cause heterogeneous dysfunction and damage. Curr. Opin. Neurol. 16:259-265.
55. Oxenius, A., M. F. Bachmann, P. G. Ashton-Rickardt, S. Tonegawa, R. M. Zinkernagel, and H. Hengartner. 1995. Presentation of endogenous viral proteins in association with major histocompatibility complex class II: on the role of intracellular compartmentalization, invariant chain and the TAP transporter system. Eur. J. Immunol. 25:3402-3411.
56. Plata-Salaman, C. R., and J. P. Borkoski. 1994. Chemokines/intercrines and central regulation of feeding. Am. J. Physiol. 266:R1711-R1715.
57. + T cells. Int. Immunol. 5:1193-1198.
58. Rady, P. L., P. Cadet, T. K. Bui, S. K. Tyring, S. Baron, G. J. Stanton, and T. K. Hughes. 1995. Production of interferon gamma messenger RNA by cells of non-immune origin. Cytokine 7:793-798.
59. Ransohoff, R. M., P. Kivisakk, and G. Kidd. 2003. Three or more routes for leukocyte migration into the central nervous system. Nat. Rev. Immunol. 3:569-581.
60. Ransohoff, R. M., L. Liu, and A. E. Cardona. 2007. Chemokines and chemokine receptors: multipurpose players in neuroinflammation. Int. Rev. Neurobiol. 82:187-204.
61. Refaeli, Y., L. Van Parijs, S. I. Alexander, and A. K. Abbas. 2002. Interferon gamma is required for activation-induced death of T lymphocytes. J. Exp. Med. 196:999-1005.
62. Reichmann, G., M. Schroeter, S. Jander, and H. G. Fischer. 2002. Dendritic cells and dendritic-like microglia in focal cortical ischemia of the mouse brain. J. Neuroimmunol. 129:125-132. (Pubitemid 34874917)
63. Remington, L. T., A. A. Babcock, S. P. Zehntner, and T. Owens. 2007. Microglial recruitment, activation, and proliferation in response to primary demyelination. Am. J. Pathol. 170:1713-1724.
64. Rowe, W. P. 1956. Protective effect of pre-irradiation on lymphocytic choriomeningitis infection in mice. Proc. Soc. Exp. Biol. Med. 92:194-198.
65. Sarmiento, M., A. L. Glasebrook, and F. W. Fitch. 1980. IgG or IgM monoclonal antibodies reactive with different determinants on the molecular complex bearing Lyt 2 antigen block T cell-mediated cytolysis in the absence of complement. J. Immunol. 125:2665-2672. (Pubitemid 11204170)
66. Schwartz, M. W., S. C. Woods, D. Porte, Jr., R. J. Seeley, and D. G. Baskin. 2000. Central nervous system control of food intake. Nature 404:661-671. (Pubitemid 30205071)
67. Sedgwick, J. D., S. Schwender, H. Imrich, R. Dorries, 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.
68. Simard, A. R., and S. Rivest. 2004. Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. FASEB J. 18:998-1000.
69. Strack, A., V. C. Asensio, I. L. Campbell, D. Schluter, and M. Deckert. 2002. Chemokines are differentially expressed by astrocytes, microglia and inflammatory leukocytes in Toxoplasma encephalitis and critically regulated by interferon-gamma. Acta Neuropathol. 103:458-468. (Pubitemid 36075341)
70. Sun, Q. H., J. P. Peng, H. F. Xia, and Y. Yang. 2007. IFN-gamma promotes apoptosis of the uterus and placenta in pregnant rat and human cytotrophoblast cells. J. Interferon Cytokine Res. 27:567-578.
71. Titus, R. G., R. Ceredig, J. C. Cerottini, and J. A. Louis. 1985. Therapeutic effect of anti-L3T4 monoclonal antibody GK1.5 on cutaneous leishmaniasis in genetically-susceptible BALB/c mice. J. Immunol. 135:2108-2114.
72. Tran, E. H., W. A. Kuziel, and T. Owens. 2000. Induction of experimental autoimmune encephalomyelitis in C57BL/6 mice deficient in either the chemokine macrophage inflammatory protein-1α or its CCR5 receptor. Eur. J. Immunol. 30:1410-1415.
73. Tsunoda, I., T. E. Lane, J. Blackett, and R. S. Fujinami. 2004. 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. 10:26-34.
74. Vanguri, P., and J. M. Farber. 1994. IFN and virus-inducible expression of an immediate-early gene, crg-2/IP-10, and a delayed gene, I-A alpha in astrocytes and microglia. J. Immunol. 152:1411-1418. (Pubitemid 24983782)
75. Welsh, R. M., Jr., and W. F. Doe. 1980. Cytotoxic cells induced during lymphocytic choriomeningitis virus infection of mice: natural killer cell activity in cultured spleen leukocytes concomitant with T-cell-dependent immune interferon production. Infect. Immun. 30:473-483.
76. + T-cell precursor frequency leads to competition for IFN-gamma thereby degrading memory cell quantity and quality. J. Immunol. 180:6777-6785.
77. + T-cell responses. J. Immunol. 175:5624-5628.
78. Wojciechowski, S., M. B. Jordan, Y. Zhu, J. White, A. J. Zajac, and D. A. Hildeman. 2006. Bim mediates apoptosis of CD127(lo) effector T cells and limits T-cell memory. Eur. J. Immunol. 36:1694-1706.
79. Xiao, B. G., C. G. Ma, L. Y. Xu, H. Link, and C. Z. Lu. 2008. IL-12/IFN-γ/NO axis plays critical role in development of Th1-mediated experimental autoimmune encephalomyelitis. Mol. Immunol. 45:1191-1196.
80. Yadav, M. C., E. M. Burudi, M. Alirezaei, C. C. Flynn, D. D. Watry, C. M. Lanigan, and H. S. Fox. 2007. IFN-γ-induced IDO and WRS expression in microglia is differentially regulated by IL-4. Glia 55:1385-1396.
81. Yamamoto, M., T. Kiyota, M. Horiba, J. L. Buescher, S. M. Walsh, H. E. Gendelman, and T. Ikezu. 2007. Interferon-gamma and tumor necrosis factor-alpha regulate amyloid-beta plaque deposition and beta-secretase expression in Swedish mutant APP transgenic mice. Am. J. Pathol. 170:680-692.
82. Zhang, B., Y. K. Chan, B. Lu, M. S. Diamond, and R. S. Klein. 2008. CXCR3 mediates region-specific antiviral T-cell trafficking within the central nervous system during West Nile virus encephalitis. J. Immunol. 180:2641-2649.