CXCR3-deficiency protects influenza-infected CCR5-deficient mice from mortality

European Journal of Immunology

Volumn 38, Issue 12, 2008, Pages 3376-3387

  Fadel, Shaza A ^a   Bromley, Shannon K ^a   Medoff, Benjamin D ^a   Luster, Andrew D ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Chemokines; Lung inflammation; T cells; Virology

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR5; GAMMA INTERFERON; MONOCYTE CHEMOTACTIC PROTEIN 1; CHEMOKINE RECEPTOR CCR5; CXCR3 PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; FEMALE; INFECTION PREVENTION; INFLAMMATORY CELL; INFLUENZA; LYMPHOCYTE FUNCTION; MALE; MEMORY T LYMPHOCYTE; MONONUCLEAR PHAGOCYTE; MORTALITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESPIRATORY TRACT INFECTION; SURVIVAL; WILD TYPE; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; GENETICS; IMMUNOLOGY; INFLUENZA VIRUS A; LYMPHOCYTE; METABOLISM; MOUSE; MOUSE MUTANT; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; SURVIVAL RATE;

ANIMALS; CELL MOVEMENT; FEMALE; INFLUENZA A VIRUS; LYMPHOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, CCR5; RECEPTORS, CXCR3; SURVIVAL RATE;

EID: 59749094882     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838628     Document Type: Article

References (45)

1. Doherty, P. C., Turner, S. J., Webby, R. G. and Thomas, P. G., Influenza and the challenge for immunology. Nat. Immunol. 2006. 7: 449-455.
2. Viola, A. and Luster, A. D., Chemokines and their receptors: Drug targets in immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 2008. 48: 171-197.
3. Lederman, M. M., Penn-Nicholson, A. P., Cho, M. and Mosier, D., Biology of CCR5 and its role in HIV infection and treatment. JAMA 2006. 296: 815-826.
4. Dawson, T. C., Beck, M. A., Kuziel, W. A., Henderson, F. and Maeda, N., Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am. J. Pathol. 2000. 156: 1951-1959.
5. Wareing, M. D., Lyon, A. B., Lu, B., Gerard, C. and Sarawar, S. R., Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. J. Leukoc. Biol. 2004. 76: 886-895.
6. + T cells depend on tissue origin and microbial stimulus. J. Immunol. 2006. 176: 557-566.
7. Tyner, J. W., Uchida, O., Kajiwara, N., Kim, E. Y., Patel, A. C., O'Sullivan, M. P., Walter, M. J. et al., CCL5-CCR5 interaction provides antiapoptotic signals for macrophage survival during viral infection. Nat. Med. 2005. 11: 1180-1187.
8. + T cells. J. Exp. Med. 2007. 204: 1625-1636.
9. Taqueti, V. R., Grabie, N., Colvin, R., Pang, H., Jarolim, P., Luster, A. D., Glimcher, L. H. and Lichtman, A. H., T-bet controls pathogenicity of CTLs in the heart by separable effects on migration and effector activity. J. Immunol. 2006. 177: 5890-5901.
10. Thomas, S. Y., Hou, R., Boyson, J. E., Means, T. K., Hess, C., Olson, D. P., Strominger, J. L. et al., CD1d-restricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J. Immunol. 2003. 171: 2571-2580.
11. Medoff, B. D., Wain, J. C., Seung, E., Jackobek, R., Means, T. K., Ginns, L. C., Farber, J. M. and Luster, A. D., CXCR3 and its ligands in a murine model of obliterative bronchiolitis: Regulation and function. J. Immunol. 2006. 176: 7087-7095.
12. Rahangdale, S., Morgan, R., Heijens, C., Ryan, T. C., Yamasaki, H., Bentley, E., Sullivan, E. et al., Chemokine receptor CXCR3 desensitization by IL-16/CD4 signaling is dependent on CCR5 and intact membrane cholesterol. J. Immunol. 2006. 176: 2337-2345.
13. Algood, H. M. and Flynn, J. L., CCR5-deficient mice control Mycobacterium tuberculosis infection despite increased pulmonary lymphocytic infiltration. J. Immunol. 2004. 173: 3287-3296.
14. + T-cell mechanisms in the control of respiratory virus infections. Immunol. Rev. 1997. 159: 105-117.
15. + T cells during pulmonary influenza virus infection. J. Immunol. 2004. 173: 1209-1218.
16. + cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J. Exp. Med. 1998. 188: 223-232.
17. Wiley, J. A., Cerwenka, A., Harkema, J. R., Dutton, R. W. and Harmsen, A. G., Production of interferon-gamma by influenza hemagglutinin-specific CD8 effector T cells influences the development of pulmonary immunopathology. Am. J. Pathol. 2001. 158: 119-130.
18. Small, B. A., Dressel, S. A., Lawrence, C. W., Drake, D. R., 3rd, Stoler, M. H., Enelow, R. I. and Braciale, T. J., CD8(+) T cell-mediated injury in vivo progresses in the absence of effector T cells. J. Exp. Med. 2001. 194: 1835-1846.
19. + T cells. J. Immunol. 2004. 173: 721-725.
20. Topham, D. J., Castrucci, M. R., Wingo, F. S., Belz, G. T. and Doherty, P. C., The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J. Immunol. 2001. 167: 6983-6990.
21. Grayson, M. H., Ramos, M. S., Rohlfing, M. M., Kitchens, R., Wang, H. D., Gould, A., Agapov, E. and Holtzman, M. J., Controls for lung dendritic cell maturation and migration during respiratory viral infection. J. Immunol. 2007. 179: 1438-1448.
22. + T cell-dendritic cell interaction. Nature 2006. 440: 890-895.
23. + T cell effectors that cause myocarditis. J. Clin. Invest. 2003. 111: 671-680.
24. Kohlmeier, J. E., Miller, S. C., Smith, J., Lu, B., Gerard, C., Cookenham, T., Roberts, A. D. and Woodland, D. L., The chemokine receptor CCR5 plays a key role in the early memory CD81 T cell response to respiratory virus infections. Immunity 2008. 29: 101-113.
25. + monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J. Immunol. 2008. 180: 2562-2572.
26. Cantor, J. and Haskins, K., Recruitment and activation of macrophages by pathogenic CD4lT cells in type 1 diabetes: Evidence for involvement of CCR8 and CCL1. J. Immunol. 2007. 179: 5760-5767.
27. Menke, J., Zeller, G. C., Kikawada, E., Means, T. K., Huang, X. R., Lan, H. Y., Lu, B. et al., CXCL9, but not CXCL10, promotes CXCR3-dependent immune-mediated kidney disease. J. Am. Soc. Nephrol. 2008. 19: 1177-1189.
28. Ramos, C. D., Canetti, C., Souto, J. T., Silva, J. S., Hogaboam, C. M., Ferreira, S. H. and Cunha, F. Q., MIP-1alpha[CCL3] acting on the CCR1 receptor mediates neutrophil migration in immune inflammation via sequential release of TNF-alpha and LTB4. J. Leukoc. Biol. 2005. 78: 167-177.
29. Wells, M. A., Albrecht, P. and Ennis, F. A., Recovery from a viral respiratory infection. I. Influenza pneumonia in normal and T-deficient mice. J. Immunol. 1981. 126: 1036-1041.
30. Loetscher, M., Gerber, B., Loetscher, P., Jones, S. A., Piali, L., Clark-Lewis, I., Baggiolini, M. and Moser, B., Chemokine receptor specific for IP10 and mig: Structure, function, and expression in activated T-lymphocytes. J. Exp. Med. 1996. 184: 963-969.
31. + T cells into the interstitium of the normal lung. J. Clin. Invest. 2005. 115: 3473-3483.
32. + T cell-mediated inflammation in the central nervous system of virus-infected mice. J. Immunol. 2005. 175: 1767-1775.
33. Nansen, A., Christensen, J. P., Andreasen, S. O., Bartholdy, C., Christensen, J. E. and Thomsen, A. R., The role of CC chemokine receptor 5 in antiviral immunity. Blood 2002. 99: 1237-1245.
34. Holst, P. J., Orskov, C., Qvortrup, C., Christensen, J. P. and Thomsen, A. R., CCR5 and CXCR3 are dispensable for liver infiltration, but CCR5 protects against virus-induced T-cell mediated hepatic steatosis. J . Virol. 2007. 81: 10101-10112
35. - regulatory T cells to sites of Leishmania major infection favors pathogen persistence. J. Exp. Med. 2006. 203: 2451-2460.
36. Zhao, M. Q., Stoler, M. H., Liu, A. N., Wei, B., Soguero, C., Hahn, Y. S. and Enelow, R. I., Alveolar epithelial cell chemokine expression triggered by antigen-specific cytolytic CD8(+) T cell recognition. J. Clin. Invest. 2000. 106: R49-R58.
37. Sakai, S., Kawamata, H.,Mantani, N., Kogure, T., Shimada, Y., Terasawa, K., Sakai, T., Imanishi, N. and Ochiai, H., Therapeutic effect of antimacrophage inflammatory protein 2 antibody on influenza virus-induced pneumonia in mice. J. Virol. 2000. 74: 2472-2476.
38. Cella, M., Facchetti, F., Lanzavecchia, A. and Colonna, M., Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat. Immunol. 2000. 1: 305-310.
39. Gazit, R., Gruda, R., Elboim,M., Arnon, T. I., Katz, G., Achdout, H., Hanna, J. et al., Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat. Immunol. 2006. 7: 517-523.
40. Kindberg, E., Mickiene, A., Ax, C., Akerlind, B., Vene, S., Lindquist, L., Lundkvist, A. and Svensson, L., A deletion in the chemokine receptor 5 (CCR5) gene is associated with tickborne encephalitis. J. Infect. Dis. 2008. 197: 266-269.
41. Lim, J. K., Louie, C. Y., Glaser, C., Jean, C., Johnson, B., Johnson, H., McDermott, D. H. and Murphy, P. M., Genetic deficiency of chemokine receptor CCR5 is a strong risk factor for symptomatic West Nile virus infection: A meta-analysis of 4 cohorts in the US epidemic. J. Infect. Dis. 2008. 197: 262-265.
42. Gulick, R. M., Su, Z., Flexner, C., Hughes, M. D., Skolnik, P. R., Wilkin, T. J., Gross, R. et al., Phase 2 study of the safety and efficacy of vicriviroc, a CCR5 inhibitor, in HIV-1-infected, treatment-experienced patients: AIDS clinical trials group 5211. J. Infect. Dis. 2007. 196: 304-312.
43. Hancock, W. W., Lu, B., Gao, W., Csizmadia, V., Faia, K., King, J. A., Smiley, S. T. et al., Requirement of the chemokine receptor CXCR3 for acute allograft rejection. J. Exp. Med. 2000. 192: 1515-1520.
44. Khan, I.A., Thomas, S. Y., Moretto, M. M., Lee, F. S., Islam, S. A., Combe, C., Schwartzman, J. D. and Luster, A. D., CCR5 is essential for NK cell trafficking and host survival following Toxoplasma gondii infection. PLoS Pathog. 2006. 2: 484-500.
45. Reed, L. J. and Muench, H., A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 1937. 27: 493-497.