- About this Journal ·
- Abstracting and Indexing ·
- Advance Access ·
- Aims and Scope ·
- Annual Issues ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 876314, 14 pages
Influenza Virus Specific CD8+ T Cells Exacerbate Infection Following High Dose Influenza Challenge of Aged Mice
1Wistar Institute, Philadelphia, PA 19104, USA
2Drexel University, Philadelphia, PA 19104, USA
3Columbia University, New York, NY 10027, USA
4Graduate Group of the University of Pennsylvania, Philadelphia, PA 19104, USA
5Cheyney University, Thornbury Township, PA 19139, USA
6Boehringer Ingelheim GMBH, Ridgefield, CT D6877, USA
7Department of Microbiology and Institute for Immunology, University of Pennsylvania, Philadelphia, PA 19104, USA
Received 3 April 2013; Revised 3 June 2013; Accepted 4 June 2013
Academic Editor: Kelvin To
Copyright © 2013 E. M. Parzych et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- A. K. Bennett, “Older age underwriting: frisky vs frail,” Journal of Insurance Medicine, vol. 36, no. 1, pp. 74–83, 2004.
- W. W. Thompson, D. K. Shay, E. Weintraub et al., “Influenza-associated hospitalizations in the United States,” Journal of the American Medical Association, vol. 292, no. 11, pp. 1333–1340, 2004.
- W. W. Thompson, D. K. Shay, E. Weintraub et al., “Mortality associated with influenza and respiratory syncytial virus in the United States,” Journal of the American Medical Association, vol. 289, no. 2, pp. 179–186, 2003.
- J. P. Janssens and K. H. Krause, “Pneumonia in the very old,” The Lancet Infectious Diseases, vol. 4, no. 2, pp. 112–124, 2004.
- D. J. Stott, W. F. Carman, and A. G. Elder, “Influenza in old age,” Age and Ageing, vol. 30, no. 5, pp. 361–363, 2001.
- D. C. Ekiert, G. Bhabha, M. A. Elsliger et al., “Antibody recognition of a highly conserved influenza virus epitope,” Science, vol. 324, no. 5924, pp. 246–251, 2009.
- T. T. Wang, G. S. Tan, R. Hai et al., “Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 44, pp. 18979–18984, 2010.
- S. J. Fleishman, T. A. Whitehead, D. C. Ekiert et al., “Computational design of proteins targeting the conserved stem region of influenza hemagglutinin,” Science, vol. 332, no. 6031, pp. 816–821, 2011.
- K. Mozdzanowska, J. Feng, M. Eid et al., “Induction of influenza type A virus-specific resistance by immunization of mice with a synthetic multiple antigenic peptide vaccine that contains ectodomains of matrix protein 2,” Vaccine, vol. 21, no. 19-20, pp. 2616–2626, 2003.
- S. Neirynck, T. Deroo, X. Saelens, P. Vanlandschoot, W. M. Jou, and W. Fiers, “A universal influenza A vaccine based on the extracellular domain of the M2 protein,” Nature Medicine, vol. 5, no. 10, pp. 1157–1163, 1999.
- J. B. Ulmer, T. M. Fu, R. R. Deck et al., “Protective CD4+ and CD8+ T cells against influenza virus induced by vaccination with nucleoprotein DNA,” Journal of Virology, vol. 72, no. 7, pp. 5648–5653, 1998.
- J. W. Yewdell, J. R. Bennink, G. L. Smith, and B. Moss, “Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 6, pp. 1785–1789, 1985.
- S. L. Epstein, “Prior H1N1 influenza infection and susceptibility of cleveland family study participants during the H2N2 pandemic of 1957: an experiment of nature,” Journal of Infectious Diseases, vol. 193, no. 1, pp. 49–53, 2006.
- L. DiMenna, B. Latimer, E. Parzych et al., “Augmentation of primary influenza A virus-specific CD8+ T cell responses in aged mice through blockade of an immunoinhibitory pathway,” The Journal of Immunology, vol. 184, no. 10, pp. 5475–5484, 2010.
- V. Decman, B. J. Laidlaw, L. J. DiMenna et al., “Cell-intrinsic defects in the proliferative response of antiviral memory CD8 T cells in aged mice upon secondary infection,” The Journal of Immunology, vol. 184, no. 9, pp. 5151–5159, 2010.
- V. Decman, B. J. Laidlaw, T. A. Doering et al., “Defective CD8 T cell responses in aged mice are due to quantitative and qualitative changes in virus-specific precursors,” The Journal of Immunology, vol. 188, no. 4, pp. 1933–1941, 2012.
- M. E. Weksler, “Changes in the B-cell repertoire with age,” Vaccine, vol. 18, no. 16, pp. 1624–1628, 2000.
- D. Frasca, A. Diaz, M. Romero, A. M. Landin, and B. B. Blomberg, “Age effects on B cells and humoral immunity in humans,” Ageing Research Reviews, vol. 10, no. 3, pp. 330–335, 2011.
- S. M. Eaton, E. M. Burns, K. Kusser, T. D. Randall, and L. Haynes, “Age-related defects in CD4 T cell cognate helper function lead to reductions in humoral responses,” Journal of Experimental Medicine, vol. 200, no. 12, pp. 1613–1622, 2004.
- L. Lazuardi, B. Jenewein, A. M. Wolf, G. Pfister, A. Tzankov, and B. Grubeck-Loebenstein, “Age-related loss of naïve T cells and dysregulation of T-cell/B-cell interactions in human lymph nodes,” Immunology, vol. 114, no. 1, pp. 37–43, 2005.
- X. Yang, J. Stedra, and J. Cerny, “Relative contribution of T and B cells to hypermutation and selection of the antibody repertoire in germinal centers of aged mice,” Journal of Experimental Medicine, vol. 183, no. 3, pp. 959–970, 1996.
- N. P. Weng, A. N. Akbar, and J. Goronzy, “CD28- T cells: their role in the age-associated decline of immune function,” Trends in Immunology, vol. 30, no. 7, pp. 306–312, 2009.
- C. Franceschi, M. Bonafè, and S. Valensin, “Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space,” Vaccine, vol. 18, no. 16, pp. 1717–1720, 2000.
- E. J. Yager, M. Ahmed, K. Lanzer, T. D. Randall, D. L. Woodland, and M. A. Blackman, “Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus,” Journal of Experimental Medicine, vol. 205, no. 3, pp. 711–723, 2008.
- D. Zhou, T. L. Wu, M. O. Lasaro et al., “A universal influenza A vaccine based on adenovirus expressing matrix-2 ectodomain and nucleoprotein protects mice from lethal challenge,” Molecular Therapy, vol. 18, no. 12, pp. 2182–2189, 2010.
- Z. F. Kapasi, K. Murali-Krishna, M. L. McRae, and R. Ahmed, “Defective generation but normal maintenance of memory T cells in old mice,” European Journal of Immunology, vol. 32, no. 6, pp. 1567–1573, 2002.
- R. A. Daynes, E. Y. Enioutina, and D. C. Jones, “Role of redox imbalance in the molecular mechanisms responsible for immunosenescence,” Antioxidants and Redox Signaling, vol. 5, no. 5, pp. 537–548, 2003.
- P. A. Scherle, G. Palladino, and W. Gerhard, “Mice can recover from pulmonary influenza virus infection in the absence of class I-restricted cytotoxic T cells,” The Journal of Immunology, vol. 148, no. 1, pp. 212–217, 1992.
- M. W. LaMere, H.-T. Lam, A. Moquin et al., “Contributions of antinucleoprotein IgG to heterosubtypic immunity against influenza virus,” The Journal of Immunology, vol. 186, no. 7, pp. 4331–4339, 2011.
- J. Feng, M. Zhang, K. Mozdzanowska et al., “Influenza A virus infection engenders a poor antibody response against the ectodomain of matrix protein 2,” Virology Journal, vol. 3, article no. 102, 2006.
- S. Alam and A. J. Sant, “Infection with seasonal influenza virus elicits CD4 T cells specific for genetically conserved epitopes that can be rapidly mobilized for protective immunity to pandemic H1N1 influenza virus,” Journal of Virology, vol. 85, no. 24, pp. 13310–13321, 2011.
- J. R. Teijaro, D. Turner, Q. Pham, E. J. Wherry, L. Lefrançois, and D. L. Farber, “Cutting edge: tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection,” The Journal of Immunology, vol. 187, no. 11, pp. 5510–5514, 2011.
- T. M. Wilkinson, C. K. F. Li, C. S. C. Chui et al., “Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans,” Nature Medicine, vol. 18, no. 2, pp. 274–280, 2012.
- S. Ashraf, W. Kong, S. Wang, J. Yang, and R. Curtiss III, “Protective cellular responses elicited by vaccination with influenza nucleoprotein delivered by a live recombinant attenuated Salmonella vaccine,” Vaccine, vol. 29, no. 23, pp. 3990–4002, 2011.
- S. L. Epstein, W. P. Kong, J. A. Misplon et al., “Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein,” Vaccine, vol. 23, no. 46-47, pp. 5404–5410, 2005.
- L. Guo, M. Zheng, Y. Ding et al., “Protection against multiple influenza A virus subtypes by intranasal administration of recombinant nucleoprotein,” Archives of Virology, vol. 155, no. 11, pp. 1765–1775, 2010.
- C. M. Lawson, J. R. Bennink, N. P. Restifo, J. W. Yewdell, and B. R. Murphy, “Primary pulmonary cytotoxic T lymphocytes induced by immunization with a vaccinia virus recombinant expressing influenza A virus nucleoprotein peptide do not protect mice against challenge,” Journal of Virology, vol. 68, no. 6, pp. 3505–3511, 1994.
- M. M. Hufford, T. S. Kim, J. Sun, and T. J. Braciale, “Antiviral CD8+ T cell effector activities in situ are regulated by target cell type,” Journal of Experimental Medicine, vol. 208, no. 1, pp. 167–180, 2011.
- D. E. Karageorgopoulos, E. K. Vouloumanou, I. P. Korbila, A. Kapaskelis, and M. E. Falagas, “Age distribution of cases of 2009 (H1N1) pandemic influenza in comparison with seasonal influenza,” PLoS ONE, vol. 6, no. 7, Article ID e21690, 2011.
- K. Hancock, V. Veguilla, X. Lu et al., “Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus,” The New England Journal of Medicine, vol. 361, no. 20, pp. 1945–1952, 2009.
- M. L. B. Hillaire, S. E. van Trierum, J. H. C. M. Kreijtz et al., “Cross-protective immunity against influenza pH1N1 2009 viruses induced by seasonal influenza A (H3N2) virus is mediated by virus-specific T-cells,” Journal of General Virology, vol. 92, no. 10, pp. 2339–2349, 2011.
- P. P. Heinen, F. A. Rijsewijks, E. A. de Boer-Luitjtze, and A. T. J. Bianchi, “Vaccination of pigs with a DNA construct expressing an influenza virus M2-nucleoprotein fusion protein exacerbates disease after challenge with influenza A virus,” Journal of General Virology, vol. 83, no. 8, pp. 1851–1859, 2002.
- J. S. M. Peiris, K. P. Y. Hui, and H. L. Yen, “Host response to influenza virus: protection versus immunopathology,” Current Opinion in Immunology, vol. 22, no. 4, pp. 475–481, 2010.
- J. R. Teijaro, M. N. Njau, D. Verhoeven et al., “Costimulation modulation uncouples protection from immunopathology in memory T cell responses to influenza virus,” The Journal of Immunology, vol. 182, no. 11, pp. 6834–6843, 2009.
- G. Marcelin, J. R. Aldridge, S. Duan et al., “Fatal outcome of pandemic H1N1 2009 influenza virus infection is associated with immunopathology and impaired lung repair, not enhanced viral burden, in pregnant mice,” Journal of Virology, vol. 85, no. 21, pp. 11208–11219, 2011.
- M. P. Longhi, A. Williams, M. Wise, B. P. Morgan, and A. Gallimore, “CD59a deficiency exacerbates influenza-induced lung inflammation through complement-dependent and -independent mechanism,” European Journal of Immunology, vol. 37, no. 5, pp. 1266–1274, 2007.
- N. Schmitz, M. Kurrer, M. F. Bachmann, and M. Kopf, “Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection,” Journal of Virology, vol. 79, no. 10, pp. 6441–6448, 2005.
- C. R. Crowe, K. Chen, D. A. Pociask et al., “Critical role of IL-17RA in immunopathology of influenza infection,” The Journal of Immunology, vol. 183, no. 8, pp. 5301–5310, 2009.
- L. Xu, H. Yoon, M. Q. Zhao, J. Liu, C. V. Ramana, and R. I. Enelow, “Cutting edge: pulmonary immunopathology mediated by antigen-specific expression of TNF-α by antiviral CD8+ T cells,” The Journal of Immunology, vol. 173, no. 2, pp. 721–725, 2004.
- L. F. Pereira, A. P. de Souza, T. J. Borges, and C. Bonorino, “Impaired in vivo CD4+ T cell expansion and differentiation in aged mice is not solely due to T cell defects: decreased stimulation by aged dendritic cells,” Mechanisms of Ageing and Development, vol. 132, no. 4, pp. 187–194, 2011.
- C. P. Wong, K. R. Magnusson, and E. Ho, “Aging is associated with altered dendritic cells subset distribution and impaired proinflammatory cytokine production,” Experimental Gerontology, vol. 45, no. 2, pp. 163–169, 2010.
- N. L. La Gruta, K. Kedzierska, J. Stambas, and P. C. Doherty, “A question of self-preservation: immunopathology in influenza virus infection,” Immunology and Cell Biology, vol. 85, no. 2, pp. 85–92, 2007.
- F. Zhou, S. Onizawa, A. Nagai, and K. Aoshiba, “Epithelial cell senescence impairs repair process and exacerbates inflammation after airway injury,” Respiratory Research, vol. 12, article 78, 2011.
- Z. Xiang, G. Gao, A. Reyes-Sandoval et al., “Novel, chimpanzee serotype 68-based adenoviral vaccine carrier for induction of antibodies to a transgene product,” Journal of Virology, vol. 76, no. 6, pp. 2667–2675, 2002.
- J. C. Fitzgerald, G. P. Gao, A. Reyes-Sandoval et al., “A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag,” The Journal of Immunology, vol. 170, no. 3, pp. 1416–1422, 2003.
- D. M. Brown, A. M. Dilzer, D. L. Meents, and S. L. Swain, “CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch,” The Journal of Immunology, vol. 177, no. 5, pp. 2888–2898, 2006.