Transient CD8-memory contraction: A potential contributor to latent cytomegalovirus reactivation

Journal of Leukocyte Biology

Volumn 92, Issue 5, 2012, Pages 933-937

  Campbell, Jonathan ^a   Trgovcich, Joanne ^a   Kincaid, Michelle ^a   Zimmerman, Peter D ^a   Klenerman, Paul ^b   Sims, Stuart ^b   Cook, Charles H ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Bacterial antigen; LPS; Memory inflation; Murine; Sepsis; Toll like receptor

Indexed keywords

BACTERIAL ANTIGEN; CD8 ANTIGEN; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOMEGALOVIRUS; FEMALE; FLOW CYTOMETRY; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS REACTIVATION;

ANIMALS; ANTIGENS, BACTERIAL; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; FLOW CYTOMETRY; IMMUNOLOGIC MEMORY; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIRUS ACTIVATION; VIRUS LATENCY;

BACTERIA (MICROORGANISMS); CYTOMEGALOVIRUS; HERPES; MURINAE; MUS;

EID: 84868321319     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1211635     Document Type: Article

References (40)

1. Sylwester, A. W., Mitchell, B. L., Edgar, J. B., Taormina, C, Pelte, C, Ruchti, F., Sleath, P. R., Grabstein, K H., Hosken, N. A., Kern, F., Nelson, J. A, Picker, L.J. (2005) Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 202, 673-685.
2. Pitcher, C. J., Hagen, S. I., Walker, J. M., Lum, R., Mitchell, B. L., Maino, V. C., Axthelm, M. K, Picker, L.J. (2002) Development and homeostasis ofT cell memory in rhesus macaque. J. Immunol. 168, 29-43.
3. Karrer, U., Sierro, S., Wagner, M., Oxenius, A, Hengel, H., Koszinowski, U. H., Phillips, R. E., Klenerman, P. (2003) Memory inflation: continuous accumulation of antiviral CD8+ T cells over time. J. Immunol. 170, 2022-2029.
4. Sierro, S., Rothkopf, R., Klenerman, P. (2005) Evolution of diverse antiviral CD8+ T cell populations after murine cytomegalovirus infection. Eur. J. Immunol. 35, 1113-1123.
5. Reddehase, M. J., Keil, G. M., Koszinowski, U. H. (1984) The cytolytic T lymphocyte response to the murine cytomegalovirus. II. Detection of virus replication stage-specific antigens by separate populations of in vivo active cytolytic T lymphocyte precursors. Eur. J. Immunol. 14, 56-61.
6. Reddehase, M. J., Weiland, F., Munch, K, Jonjic, S., Luske, A, Koszinowski, U. H. (1985) Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs. J. Virol. 55, 264-273.
7. Podlech, J., Holtappels, R., Pahl-Seibert, M. F., Steffens, H. P., Reddehase, M.J. (2000) Murine model of interstitial cytomegalovirus pneumonia in syngeneic bone marrow transplantation: persistence of protective pulmonary CD8-T-cell infiltrates after clearance of acute infection. J. Virol. 74, 7496-7507.
8. Pipeling, M. R., West, E. E., Osborne, C. M., Whitlock, A. B., Dropulic, L. K, Willett, M. H., Forman, M., Valsamakis, A, Orens, J. B., Moller, D. R., Lechtzin, N., Migueles, S. A, Connors, M., McDyer, J. F. (2008) Differential CMV-specific CD8+ effector T cell responses in the lung allograft predominate over the blood during human primary infection. J. Immunol. 181, 546-556.
9. Eid, A. J., Brown, R. A, Hogan, W. J., Lahr, B. D., Eckel-Passow, J. E., Litzow, M. R., Razonable, R. R. (2009) Kinetics of interferon-γ producing cytomegalovirus (CMV)-specific CD4+ and CD8+ T lymphocytes and the risk of subsequent CMV viremia after allogeneic hematopoietic stem cell transplantation. Transpl. Infect. Dis. 11, 519-528.
10. Simon, C. O., Holtappels, R., Tervo, H-M., Bohm, V., Daubner, T., Oeh-rlein-Karpi, S. A, Kuhnapfel, B., Renzaho, A., Strand, D., Podlech, J., Reddehase, M. J., Grzimek, N. K A. (2006) CD8 T cells control cytomegalovirus latency by epitope-specific sensing of transcriptional reactivation. J. Virol. 80, 10436-10456.
11. Cook, C. H., Trgovcich, J., Zimmerman, P. D., Zhang, Y., Sedmak, D. D. (2006) Lipopolysaccharide, tumor necrosis factor α, or interleukin-1β triggers reactivation of latent cytomegalovirus in immunocompetent mice. J. Virol. 80, 9151-9158.
12. Holtappels, R., Thomas, D., Podlech, J., Reddehase, M.J. (2002) Two antigenic peptides from fenes m123 and m164 of murine cytomegalovirus quantitatively dominate CD8 T-cell memory in the H-2d haplotype. J. Virol. 76, 151-164.
13. Holtappels, R., Grzimek, N. K A, Thomas, D., Reddehase, M.J. (2002) Early gene m18, a novel player in the immune response to murine cytomegalovirus. J. Gen. Virol. 83, 311-316.
14. Holtappels, R., Thomas, D., Podlech, J., Geginat, G., Steffens, H-P., Reddehase, M. J. (2000) The putative natural killer decoy early gene m04 (gp34) of murine cytomegalovirus encodes an antigenic peptide recognized by protective antiviral CD8 T cells. J. Virol. 74, 1871-1884.
15. Selin, L. K, Vergilis, K, Welsh, R. M., Nahill, S. R. (1996) Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J. Exp. Med. 183, 2489-2499.
16. McNally, J. M., Zarozinski, C. C, Lin, M-Y, Brehm, M. A, Chen, H. D., Welsh, R. M. (2001) Attrition of bystander CD8 T cells during virus-induced T-cell and interferon responses. J. Virol. 75, 5965-5976.
17. Smith, D. K, Dudani, R., Pedras-Vasconcelos, J. A., Chapdelaine, Y., van Faassen, H., Sad, S. (2002) Cross-reactive antigen is required to prevent erosion of established T cell memory and tumor immunity: a heterologous bacterial model of attrition. J. Immunol. 169, 1197-1206.
18. Kim, S-K, Welsh, R. M. (2004) Comprehensive early and lasting loss of memory CD8 T cells and functional memory during acute and persistent viral infections. J. Immunol. 172, 3139-3150.
19. Zhang, J-Y., Zhang, Z., Jin, B., Zhang, S-Y, Zhou, C-B., Fu, J-L., Wang, F-S. (2008) Cutting edge: programmed death-1 up-regulation is involved in the attrition of cytomegalovirus-specific CD8+ T cells in acute self-limited hepatitis B virus infection. J. Immunol. 181, 3741-3744.
20. Karaghiosoff, M., Steinborn, R, Kovarik, P., Kriegshauser, G., Baccarini, M., Donabauer, B., Reichart, U., Kolbe, T., Bogdan, C, Leanderson, T., Levy, D., Decker, T., Muller, M. (2003) Central role for type I interferons and Tyk2 in lipopolysaccharide-induced endotoxin shock. Nat. Immunol. 4, 471-477.
21. Hummel, M., Abecassis, M. M. (2002) A model for reactivation of CMV from latency. J. Clin. Virol. 25 (SUPPL. 2), S123-S136.
22. Reeves, M. B., Sinclair, J. H. (2010) Analysis of latent viral gene expression in natural and experimental latency models of human cytomegalovirus and its correlation with histone modifications at a latent promoter. J. Gen. Virol. 91, 599-604.
23. Liu, X-F., Yan, S., Abecassis, M., Hummel, M. (2008) Establishment of murine cytomegalovirus latency in vivo is associated with changes in histone modifications and recruitment of transcriptional repressors to the major immediate-early promoter. J. Virol. 82, 10922-10931.
24. Balakrishnan, L., Milavetz, B. (2008) HDAC inhibitors stimulate viral transcription by multiple mechanisms. Virol. J. 5, 43.
25. Hummel, M., Yan, S., Li, Z., Varghese, T. K, Abecassis, M. (2007) Transcriptional reactivation of murine cytomegalovirus ie gene expression by 5-aza-2-deoxycytidine and trichostatin A in latently infected cells despite lack of methylation of the major immediate-early promoter. J. Gen. Virol. 88, 1097-1102.
26. Liu, X-F., Yan, S., Abecassis, M., Hummel, M. (2010) Biphasic recruitment of transcriptional repressors to the murine cytomegalovirus major immediate-early promoter during the course of infection in vivo. J. Virol. 84, 3631-3643.
27. Snyder, C. M., Cho, K. S., Bonnett, E. L., van Dommelen, S., Shellam, G. R., Hill, A. B. (2008) Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29, 650-659.
28. - T cells. Eur. J. Immunol. 35, 3131-3141.
29. Munks, M. W., Cho, K. S., Pinto, A. K, Sierro, S., Klenerman, P., Hill, A. B. (2006) Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J. Immunol. 177, 450-458.
30. Hansen, S. G., Powers, C. J., Richards, R, Ventura, A. B., Ford, J. C, Siess, D., Axthelm, M. K., Nelson, J. A, Jarvis, M. A, Picker, L. J., Fruh, K (2010) Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 328, 102-106.
31. Von Muller, L., Klemm, A, Durmus, N., Weiss, M., Suger-Wiedeck, H., Schneider, M., Hampl, W., Mertens, T. (2007) Cellular immunity and active human cytomegalovirus infection in patients with septic shock. J. Infect. Dis. 196, 1288-1295.
32. Chilet, M., Aguilar, G., Benet, I., Belda, J., Tormo, N., Carbonell, J. A, Clari, M. A, Costa, E., Navarro, D. (2010) Virological and immunological features of active cytomegalovirus infection in nonimmunosup-pressed patients in a surgical and trauma intensive care unit. J. Med. Virol. 82, 1384-1391.
33. Chiche, L., Forel, J. M., Thomas, G., Farnarier, C, Vely, F., Blery, M., Papazian, L., Vivier, E. (2011) The role of natural killer cells in sepsis. J. Biomed. Biotechnol. 2011, 986491.
34. Xiao, Z., Mescher, M. F., Jameson, S. C. (2007) Detuning CD8 T cells: down-regulation of CD8 expression, tetramer binding, and response during CTL activation. J. Exp. Med. 204, 2667-2677.
35. Jabbari, A, Legge, K. L., Harty, J. T. (2006) T cell conditioning explains early disappearance of the memory CD8 T cell response to infection. J. Immunol. 177, 3012-3018.
36. Hotchkiss, R S., Coopersmith, C. M., McDunn, J. E., Ferguson, T. A (2009) The sepsis seesaw: tilting toward immunosuppression. Nat. Med. 15, 496-497.
37. Hotchkiss, R S., Tinsley, K. W., Swanson, P. E., Schmieg, R E., Hui, J. J., Chang, K. C, Osborne, D. F., Freeman, B. D., Cobb, J. P., Buch-man, T. G., Karl, I. E. (2001) Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans. J. Immunol. 166, 6952-6963.
38. Hotchkiss, R S., Tinsley, K. W., Swanson, P. E., Grayson, M. H., Osborne, D. F., Wagner, T. H., Cobb, J. P., Coopersmith, C, Karl, I. E. (2002) Depletion of dendritic cells, but not macrophages, in patients with sepsis. J. Immunol. 168, 2493-2500.
39. Polic, B., Hengel, H., Krmpotic, A, Trgovcich, J., Pavic, I., Luccaronin, P., Jonjic, S., Koszinowski, U. H. (1998) Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J. Exp. Med. 188, 1047-1054.
40. Krmpotic, A, Busch, D. H., Bubic, I., Gebhardt, F., Hengel, H., Hasan, M., Scalzo, A. A, Koszinowski, U. H., Jonjic, S. (2002) MCMV glycoprotein gp40 confers virus resistance to CD8+ T cells and NK cells in vivo. Nat. Immunol. 3, 529-535.