T cells maintain an exhausted phenotype after antigen withdrawal and population reexpansion (original) (raw)

• McDermott, A.B. & Koup, R.A. CD8+ T cells in preventing HIV infection and disease. AIDS 26, 1281–1292 (2012).
  Article CAS PubMed Google Scholar
• Rehermann, B. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J. Clin. Invest. 119, 1745–1754 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Ahmed, R., Salmi, A., Butler, L.D., Chiller, J.M. & Oldstone, M.B. 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 (1984).
  Article CAS PubMed Google Scholar
• Klenerman, P. & Hill, A. T cells and viral persistence: lessons from diverse infections. Nat. Immunol. 6, 873–879 (2005).
  Article CAS PubMed Google Scholar
• McMichael, A.J., Borrow, P., Tomaras, G.D., Goonetilleke, N. & Haynes, B.F. The immune response during acute HIV-1 infection: clues for vaccine development. Nat. Rev. Immunol. 10, 11–23 (2010).
  Article CAS PubMed Google Scholar
• Gallimore, A. et al. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 187, 1383–1393 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Zajac, A.J. et al. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188, 2205–2213 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Wherry, E.J. et al. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27, 670–684 (2007).
  Article CAS PubMed Google Scholar
• Moskophidis, D., Lechner, F., Pircher, H. & Zinkernagel, R.M. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362, 758–761 (1993).
  Article CAS PubMed Google Scholar
• Paley, M.A. et al. Progenitor and terminal subsets of CD8+ T cells cooperate to contain chronic viral infection. Science 338, 1220–1225 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Day, C.L. et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443, 350–354 (2006).
  Article CAS PubMed Google Scholar
• Blackburn, S.D. et al. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10, 29–37 (2009).
  Article CAS PubMed Google Scholar
• Barber, D.L. et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682–687 (2006).
  Article CAS PubMed Google Scholar
• Wherry, E.J. T cell exhaustion. Nat. Immunol. 12, 492–499 (2011).
  Article CAS PubMed Google Scholar
• Bowen, D.G. & Walker, C.M. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 436, 946–952 (2005).
  Article CAS PubMed Google Scholar
• Pichenot, M., Deuffic-Burban, S., Cuzin, L. & Yazdanpanah, Y. Efficacy of new antiretroviral drugs in treatment-experienced HIV-infected patients: a systematic review and meta-analysis of recent randomized controlled trials. HIV Med. 13, 148–155 (2012).
  CAS PubMed Google Scholar
• Jin, X. et al. Dramatic rise in plasma viremia after CD8+ T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189, 991–998 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Schmitz, J.E. et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283, 857–860 (1999).
  Article CAS PubMed Google Scholar
• Velu, V. et al. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458, 206–210 (2009).
  Article CAS PubMed Google Scholar
• Vezys, V. et al. Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203, 2263–2269 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Wherry, E.J., Barber, D.L., Kaech, S.M., Blattman, J.N. & Ahmed, R. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc. Natl. Acad. Sci. USA 101, 16004–16009 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Shin, H. & Wherry, E.J. CD8 T cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 19, 408–415 (2007).
  Article CAS PubMed Google Scholar
• Shin, H., Blackburn, S.D., Blattman, J.N. & Wherry, E.J. Viral antigen and extensive division maintain virus-specific CD8 T cells during chronic infection. J. Exp. Med. 204, 941–949 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Wherry, E.J., Blattman, J.N., Murali-Krishna, K., van der Most, R. & Ahmed, R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77, 4911–4927 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Dillon, S.R., Jameson, S.C. & Fink, P.J. Vβ5+ T cell receptors skew toward OVA+H-2Kb recognition. J. Immunol. 152, 1790–1801 (1994).
  CAS PubMed Google Scholar
• Miller, N.E., Bonczyk, J.R., Nakayama, Y. & Suresh, M. Role of thymic output in regulating CD8 T-cell homeostasis during acute and chronic viral infection. J. Virol. 79, 9419–9429 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Brandle, D. et al. Involvement of both T cell receptor Vα and Vβ variable region domains and α chain junctional region in viral antigen recognition. Eur. J. Immunol. 21, 2195–2202 (1991).
  Article CAS PubMed Google Scholar
• Richter, K., Brocker, T. & Oxenius, A. Antigen amount dictates CD8+ T-cell exhaustion during chronic viral infection irrespective of the type of antigen presenting cell. Eur. J. Immunol. 42, 2290–2304 (2012).
  Article CAS PubMed Google Scholar
• Mueller, S.N. & Ahmed, R. High antigen levels are the cause of T cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 106, 8623–8628 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Geginat, J., Lanzavecchia, A. & Sallusto, F. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101, 4260–4266 (2003).
  Article CAS PubMed Google Scholar
• Sallusto, F., Lenig, D., Forster, R., Lipp, M. & Lanzavecchia, A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708–712 (1999).
  Article CAS PubMed Google Scholar
• Hamann, D. et al. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186, 1407–1418 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Duraiswamy, J. et al. Phenotype, function, and gene expression profiles of programmed death-1hi CD8 T cells in healthy human adults. J. Immunol. 186, 4200–4212 (2011).
  Article CAS PubMed Google Scholar
• Baumgaertner, P. et al. Vaccination-induced functional competence of circulating human tumor-specific CD8 T-cells. Int. J. cancer cancer 130, 2607–2617 (2012).
  Article CAS Google Scholar
• Arens, R. & Schoenberger, S.P. Plasticity in programming of effector and memory CD8 T-cell formation. Immunol. Rev. 235, 190–205 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Cui, W. & Kaech, S.M. Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol. Rev. 236, 151–166 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Lefrancois, L. & Masopust, D. The road not taken: memory T cell fate 'decisions'. Nat. Immunol. 10, 369–370 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Nolz, J.C. & Harty, J.T. Protective capacity of memory CD8+ T cells is dictated by antigen exposure history and nature of the infection. Immunity 34, 781–793 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Williams, M.A. & Bevan, M.J. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25, 171–192 (2007).
  Article CAS PubMed Google Scholar
• Snyder, C.M. et al. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29, 650–659 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Blackburn, S.D., Shin, H., Freeman, G.J. & Wherry, E.J. Selective expansion of a subset of exhausted CD8 T cells by αPD-L1 blockade. Proc. Natl. Acad. Sci. USA 105, 15016–15021 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Pellegrini, M. et al. IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 144, 601–613 (2011).
  Article CAS PubMed Google Scholar
• Sharpe, A.H., Wherry, E.J., Ahmed, R. & Freeman, G.J. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat. Immunol. 8, 239–245 (2007).
  Article CAS PubMed Google Scholar
• Trautmann, L. et al. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat. Med. 12, 1198–1202 (2006).
  Article CAS PubMed Google Scholar
• Speiser, D.E. et al. Unmodified self antigen triggers human CD8 T cells with stronger tumor reactivity than altered antigen. Proc. Natl. Acad. Sci. USA 105, 3849–3854 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Frebel, H. et al. Programmed death 1 protects from fatal circulatory failure during systemic virus infection of mice. J. Exp. Med. 209, 2485–2499 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Pircher, H. et al. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 346, 629–633 (1990).
  Article CAS PubMed Google Scholar
• Battegay, M. et al. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J. Virol. Methods 33, 191–198 (1991).
  Article CAS PubMed Google Scholar
• Speiser, D.E. et al. Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J. Clin. Invest. 115, 739–746 (2005).
  Article CAS PubMed PubMed Central Google Scholar