Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus

doi:10.1084/jem.168.3.1163

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Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus

MJ Cannon, PJ Openshaw and BA Askonas
Division of Immunology, National Institute for Medical Research, London, United Kingdom.

We have examined the function of class I MHC-restricted cytotoxic T cells in experimental respiratory syncytial virus (RSV) infection of BALB/c mice by transfer of T cell line MJC-A2 and CTL clone E8a into RSV-infected mice. The T cell line cleared pulmonary RSV infection within 5 d in persistently infected gamma-irradiated mice, but caused acute respiratory disease. This was only seen in infected mice and was often lethal after transfer of greater than 3 x 10(6) CTL. Lower numbers of CTL produced less severe disease but still cleared lung RSV, albeit over a longer time course (up to 10 d). Clearance of lung RSV in immunocompetent mice by the T cell line and CTL clone was again accompanied by acute and sometimes lethal respiratory disease. Bronchoalveolar lavage showed severe lung hemorrhage and frequent neutrophil efflux in mice with CTL-augmented disease.
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Bukreyev, A., Serra, M. E., Laham, F. R., Melendi, G. A., Kleeberger, S. R., Collins, P. L., Polack, F. P. (2006). The Cysteine-Rich Region and Secreted Form of the Attachment G Glycoprotein of Respiratory Syncytial Virus Enhance the Cytotoxic T-Lymphocyte Response despite Lacking Major Histocompatibility Complex Class I-Restricted Epitopes.. J. Virol. 80: 5854-5861 [Abstract] [Full Text]
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O'Donnell, R, Breen, D, Wilson, S, Djukanovic, R (2006). Inflammatory cells in the airways in COPD. Thorax 61: 448-454 [Abstract] [Full Text]
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Harcourt, J., Alvarez, R., Jones, L. P., Henderson, C., Anderson, L. J., Tripp, R. A. (2006). Respiratory Syncytial Virus G Protein and G Protein CX3C Motif Adversely Affect CX3CR1+ T Cell Responses. J. Immunol. 176: 1600-1608 [Abstract] [Full Text]
Openshaw, P. J. M. (2005). Antiviral Immune Responses and Lung Inflammation after Respiratory Syncytial Virus Infection. Proc Am Thorac Soc 2: 121-125 [Abstract] [Full Text]
O'Sullivan, S. M. (2005). Asthma Death, CD8+ T Cells, and Viruses. Proc Am Thorac Soc 2: 162-165 [Abstract] [Full Text]
Openshaw, P. J. M., Tregoning, J. S. (2005). Immune Responses and Disease Enhancement during Respiratory Syncytial Virus Infection. Clin. Microbiol. Rev. 18: 541-555 [Abstract] [Full Text]
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Hakamada, T., Funatsuki, K., Morita, H., Ugajin, T., Nakamura, I., Ishiko, H., Matsuzaki, Y., Tanaka, N., Imawari, M. (2004). Identification of novel hepatitis C virus-specific cytotoxic T lymphocyte epitopes by ELISpot assay using peptides with human leukocyte antigen-A*2402-binding motifs. J. Gen. Virol. 85: 1521-1531 [Abstract] [Full Text]
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Rutigliano, J. A., Johnson, T. R., Hollinger, T. N., Fischer, J. E., Aung, S., Graham, B. S. (2004). Treatment with Anti-LFA-1 Delays the CD8+ Cytotoxic-T-Lymphocyte Response and Viral Clearance in Mice with Primary Respiratory Syncytial Virus Infection. J. Virol. 78: 3014-3023 [Abstract] [Full Text]
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Viuff, B., Tjornehoj, K., Larsen, L. E., Rontved, C. M., Uttenthal, A., Ronsholt, L., Alexandersen, S. (2002). Replication and Clearance of Respiratory Syncytial Virus: Apoptosis Is an Important Pathway of Virus Clearance after Experimental Infection with Bovine Respiratory Syncytial Virus. Am. J. Pathol. 161: 2195-2207 [Abstract] [Full Text]
Johnson, T. R., Hong, S., Van Kaer, L., Koezuka, Y., Graham, B. S. (2002). NK T Cells Contribute to Expansion of CD8+ T Cells and Amplification of Antiviral Immune Responses to Respiratory Syncytial Virus. J. Virol. 76: 4294-4303 [Abstract] [Full Text]
Licon Luna, R. M., Lee, E., Mullbacher, A., Blanden, R. V., Langman, R., Lobigs, M. (2002). Lack of both Fas Ligand and Perforin Protects from Flavivirus-Mediated Encephalitis in Mice. J. Virol. 76: 3202-3211 [Abstract] [Full Text]
Zhang, Y., Wang, Y., Gilmore, X., Xu, K., Wyde, P. R., Mbawuike, I. N. (2002). An Aged Mouse Model for RSV Infection and Diminished CD8+ CTL Responses. Exp. Biol. Med. 227: 133-140 [Abstract] [Full Text]
Look, D. C., Walter, M. J., Williamson, M. R., Pang, L., You, Y., Sreshta, J. N., Johnson, J. E., Zander, D. S., Brody, S. L. (2001). Effects of Paramyxoviral Infection on Airway Epithelial Cell Foxj1 Expression, Ciliogenesis, and Mucociliary Function. Am. J. Pathol. 159: 2055-2069 [Abstract] [Full Text]
MAESTRELLI, P., SAETTA, M., MAPP, C. E., FABBRI, L. M. (2001). Remodeling in Response to Infection and Injury . Airway Inflammation and Hypersecretion of Mucus in Smoking Subjects with Chronic Obstructive Pulmonary Disease. Am. J. Respir. Crit. Care Med. 164: S76-80 [Abstract] [Full Text]
Aung, S., Rutigliano, J. A., Graham, B. S. (2001). Alternative Mechanisms of Respiratory Syncytial Virus Clearance in Perforin Knockout Mice Lead to Enhanced Disease. J. Virol. 75: 9918-9924 [Abstract] [Full Text]
Chang, J., Srikiatkhachorn, A., Braciale, T. J. (2001). Visualization and Characterization of Respiratory Syncytial Virus F-Specific CD8+ T Cells During Experimental Virus Infection. J. Immunol. 167: 4254-4260 [Abstract] [Full Text]
KANNER, R. E., ANTHONISEN, N. R., CONNETT, J. E. (2001). Lower Respiratory Illnesses Promote FEV1 Decline in Current Smokers But Not Ex-Smokers with Mild Chronic Obstructive Pulmonary Disease . Results from the Lung Health Study. Am. J. Respir. Crit. Care Med. 164: 358-364 [Abstract] [Full Text]
ZHU, J., QIU, Y. S., MAJUMDAR, S., GAMBLE, E., MATIN, D., TURATO, G., FABBRI, L. M., BARNES, N., SAETTA, M., JEFFERY, P. K. (2001). Exacerbations of Bronchitis . Bronchial Eosinophilia and Gene Expression for Interleukin-4, Interleukin-5, and Eosinophil Chemoattractants. Am. J. Respir. Crit. Care Med. 164: 109-116 [Abstract] [Full Text]
Jamaluddin, M., Wang, S., Garofalo, R. P., Elliott, T., Casola, A., Baron, S., Brasier, A. R. (2001). IFN-{beta} mediates coordinate expression of antigen-processing genes in RSV-infected pulmonary epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L248-L257 [Abstract] [Full Text]
Simmons, C. P., Hussell, T., Sparer, T., Walzl, G., Openshaw, P., Dougan, G. (2001). Mucosal Delivery of a Respiratory Syncytial Virus CTL Peptide with Enterotoxin-Based Adjuvants Elicits Protective, Immunopathogenic, and Immunoregulatory Antiviral CD8+ T Cell Responses. J. Immunol. 166: 1106-1113 [Abstract] [Full Text]
Hussell, T., Openshaw, P. J. M. (2000). IL-12-Activated NK Cells Reduce Lung Eosinophilia to the Attachment Protein of Respiratory Syncytial Virus But Do Not Enhance the Severity of Illness in CD8 T Cell-Immunodeficient Conditions. J. Immunol. 165: 7109-7115 [Abstract] [Full Text]
Brandenburg, A. H., de Waal, L., Timmerman, H. H., Hoogerhout, P., de Swart, R. L., Osterhaus, A. D. M. E. (2000). HLA Class I-Restricted Cytotoxic T-Cell Epitopes of the Respiratory Syncytial Virus Fusion Protein. J. Virol. 74: 10240-10244 [Abstract] [Full Text]
Goulder, P. J. R., Lechner, F., Klenerman, P., McIntosh, K., Walker, B. D. (2000). Characterization of a Novel Respiratory Syncytial Virus-Specific Human Cytotoxic T-Lymphocyte Epitope. J. Virol. 74: 7694-7697 [Abstract] [Full Text]
Dawson, T. C., Beck, M. A., Kuziel, W. A., Henderson, F., Maeda, N. (2000). Contrasting Effects of CCR5 and CCR2 Deficiency in the Pulmonary Inflammatory Response to Influenza A Virus. Am. J. Pathol. 156: 1951-1959 [Abstract] [Full Text]
Diaz, P. T., King, M. A., Pacht, E. R., Wewers, M. D., Gadek, J. E., Nagaraja, H. N., Drake, J., Clanton, T. L. (2000). Increased Susceptibility to Pulmonary Emphysema among HIV-Seropositive Smokers. ANN INTERN MED 132: 369-372 [Abstract] [Full Text]
Zaia, J. A., Sissons, J.G. P., Riddell, S., Diamond, D. J., Wills, M.R., Carmichael, A.J., Weekes, M.P., Gandhi, M., La Rosa, C., Villacres, M., Lacey, S., Markel, S., Sun, J. (2000). Status of Cytomegalovirus Prevention and Treatment in 2000. ASH Education Book 2000: 339-355 [Abstract] [Full Text]
KEMENY, D. M., VYAS, B., VUKMANOVIC-STEJIC, M., THOMAS, M. J., NOBLE, A., LOH, L.-C., O'CONNOR, B. J. (1999). CD8+ T Cell Subsets and Chronic Obstructive Pulmonary Disease. Am. J. Respir. Crit. Care Med. 160: S33-37 [Abstract] [Full Text]
Shankar, P., Xu, Z., Lieberman, J. (1999). Viral-Specific Cytotoxic T Lymphocytes Lyse Human Immunodeficiency Virus-Infected Primary T Lymphocytes by the Granule Exocytosis Pathway. Blood 94: 3084-3093 [Abstract] [Full Text]
ABERLE, J. H., ABERLE, S. W., DWORZAK, M. N., MANDL, C. W., REBHANDL, W., VOLLNHOFER, G., KUNDI, M., POPOW-KRAUPP, T. (1999). Reduced Interferon-gamma Expression in Peripheral Blood Mononuclear Cells of Infants with Severe Respiratory Syncytial Virus Disease. Am. J. Respir. Crit. Care Med. 160: 1263-1268 [Abstract] [Full Text]
Van Epps, H. L., Schmaljohn, C. S., Ennis, F. A. (1999). Human Memory Cytotoxic T-Lymphocyte (CTL) Responses to Hantaan Virus Infection: Identification of Virus-Specific and Cross-Reactive CD8+ CTL Epitopes on Nucleocapsid Protein. J. Virol. 73: 5301-5308 [Abstract] [Full Text]
Domachowske, J. B., Rosenberg, H. F. (1999). Respiratory Syncytial Virus Infection: Immune Response, Immunopathogenesis, and Treatment. Clin. Microbiol. Rev. 12: 298-309 [Abstract] [Full Text]
Gern, J. E., Busse, W. W. (1999). Association of Rhinovirus Infections with Asthma. Clin. Microbiol. Rev. 12: 9-18 [Abstract] [Full Text]
Selin, L. K., Varga, S. M., Wong, I. C., Welsh, R. M. (1998). Protective Heterologous Antiviral Immunity and Enhanced Immunopathogenesis Mediated by Memory T Cell Populations. J. Exp. Med. 188: 1705-1715 [Abstract] [Full Text]
Tripp, R. A., Anderson, L. J. (1998). Cytotoxic T-Lymphocyte Precursor Frequencies in BALB/c Mice after Acute Respiratory Syncytial Virus (RSV) Infection or Immunization with a Formalin-Inactivated RSV Vaccine. J. Virol. 72: 8971-8975 [Abstract] [Full Text]
Mankowski, J. L., Carter, D. L., Spelman, J. P., Nealen, M. L., Maughan, K. R., Kirstein, L. M., Didier, P. J., Adams, R. J., Murphey-Corb, M., Zink, M. C. (1998). Pathogenesis of Simian Immunodeficiency Virus Pneumonia : An Immunopathological Response to Virus. Am. J. Pathol. 153: 1123-1130 [Abstract] [Full Text]
Moskophidis, D., Kioussis, D. (1998). Contribution of �Virus-specific CD8+ Cytotoxic T Cells to Virus Clearance or Pathologic Manifestations of Influenza Virus Infection in a T Cell Receptor Transgenic Mouse Model. J. Exp. Med. 188: 223-232 [Abstract] [Full Text]
Dudas, R. A., Karron, R. A. (1998). Respiratory Syncytial Virus Vaccines. Clin. Microbiol. Rev. 11: 430-439 [Abstract] [Full Text]
SAETTA, M., Di�STEFANO, A., TURATO, G., FACCHINI, F.�M., CORBINO, L., MAPP, C.�E., MAESTRELLI, P., CIACCIA, A., FABBRI, L.�M. (1998). CD8+ T-Lymphocytes in Peripheral Airways of Smokers with Chronic Obstructive Pulmonary Disease. Am. J. Respir. Crit. Care Med. 157: 822-826 [Abstract] [Full Text]
Srikiatkhachorn, A., Braciale, T. J. (1997). Virus-specific CD8+ T Lymphocytes Downregulate T Helper Cell Type 2�Cytokine Secretion and Pulmonary Eosinophilia during Experimental Murine Respiratory Syncytial Virus Infection. J. Exp. Med. 186: 421-432 [Abstract] [Full Text]
Tobery, T. W., Siliciano, R. F. (1997). Targeting of HIV-1 Antigens for Rapid Intracellular Degradation Enhances Cytotoxic T Lymphocyte (CTL) Recognition and the Induction of De Novo CTL Responses In Vivo After Immunization. J. Exp. Med. 185: 909-920 [Abstract] [Full Text]
Oehen, S, Hengartner, H, Zinkernagel, R. (1991). Vaccination for disease. Science 251: 195-198 [Abstract]