Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge

Journal of Experimental Medicine

Volumn 203, Issue 6, 2006, Pages 1533-1541

  Mattapallil, Joseph J ^a   Douek, Daniel C ^a   Buckler White, Alicia ^a   Montefiori, David ^b   Letvin, Norman L ^c   Nabel, Gary J ^a   Roederer, Mario ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRIMER DNA;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LOSS; CELL SPECIFICITY; CELLULAR IMMUNITY; CONTROLLED STUDY; DEATH; DISEASE COURSE; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; MEMORY T LYMPHOCYTE; NONHUMAN; OUTCOME ASSESSMENT; PREDICTION; PRIORITY JOURNAL; SIMIAN VIRUS; SURVIVAL RATE; SURVIVAL TIME; VACCINATION; VIRUS INFECTION;

ANIMALS; ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; FLOW CYTOMETRY; IMMUNOLOGIC MEMORY; MACACA MULATTA; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION;

EID: 33745015013     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20060657     Document Type: Article

References (48)

1. Mattapallil, J.J., D.C. Douek, B. Hill, Y. Nishimura, M. Martin, and M. Roederer. 2005. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature. 434:1093-1097.
2. Li, Q., L. Duan, J.D. Estes, Z.M. Ma, T. Rourke, Y. Wang, C. Reilly, J. Carlis, C.J. Miller, and A.T. Haase. 2005. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature. 434:1148-1152.
3. Reynolds, M.R., E. Rakasz, P.J. Skinner, C. White, K. Abel, Z.M. Ma, L. Compton, G. Napoe, N. Wilson, C.J. Miller, et al. 2005. CD8+ T-lymphocyte response to major immunodominant epitopes after vaginal exposure to simian immunodeficiency virus: too late and too little. J. Virol. 79:9228-9235.
4. Veazey, R.S., M. DeMaria, L.V. Chalifoux, D.E. Shvetz, D.R. Pauley, H.L. Knight, M. Rosenzweig, R.P. Johnson, R.C. Desrosiers, and A.A. Lackner. 1998. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science. 280:427-431.
5. Amara, R.R., F. Villinger, J.D. Altman, S.L. Lydy, S.P. O'Neil, S.I. Staprans, D.C. Montefiori, Y. Xu, J.G. Herndon, L.S. Wyatt, et al. 2001. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science. 292:69-74.
6. Baba, T.W., V. Liska, R. Hofmann-Lehmann, J. Vlasak, W. Xu, S. Ayehunie, L.A. Cavacini, M.R. Posner, H. Katinger, G. Stiegler, et al. 2000. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6:200-206.
7. Barouch, D.H., S. Santra, J.E. Schmitz, M.J. Kuroda, T.M. Fu, W. Wagner, M. Bilska, A. Craiu, X.X. Zheng, G.R. Krivulka, et al. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science. 290:486-492.
8. Lifson, J.D., J.L. Rossio, R. Arnaout, L. Li, T.L. Parks, D.K. Schneider, R.F. Kiser, V.J. Coalter, G. Walsh, R.J. Imming, et al. 2000. Containment of simian immunodeficiency virus infection: cellular immune responses and protection from rechallenge following transient postinoculation antiretroviral treatment. J. Virol. 74:2584-2593.
9. Mascola, J.R., G. Stiegler, T.C. VanCott, H. Katinger, C.B. Carpenter, C.E. Hanson, H. Beary, D. Hayes, S.S. Frankel, D.L. Birx, and M.G. Lewis. 2000. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6:207-210.
10. Shiver, J.W., T.M. Fu, L. Chen, D.R. Casimiro, M.E. Davies, R.K. Evans, Z.Q. Zhang, A.J. Simon, W.L. Trigona, S.A. Dubey, et al. 2002. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature. 415:331-335.
11. Douek, D.C., J.M. Brenchley, M.R. Betts, D.R. Ambrozak, B.J. Hill, Y. Okamoto, J.P. Casazza, J. Kuruppu, K. Kunstman, S. Wolinsky, et al. 2002. HIV preferentially infects HIV-specific CD4+ T cells. Nature. 417:95-98.
12. Staprans, S.I., A.P. Barry, G. Silvestri, J.T. Safrit, N. Kozyr, B. Sumpter, H. Nguyen, H. McClure, D. Montefiori, J.I. Cohen, and M.B. Feinberg. 2004. Enhanced SIV replication and accelerated progression to AIDS in macaques primed to mount a CD4 T cell response to the SIV envelope protein. Proc. Natl. Acad. Sci. USA. 101:13026-13031.
13. Letvin, N.L., Y. Huang, B.K. Chakrabarti, L. Xu, M.S. Seaman, K. Beaudry, B. Korioth-Schmitz, F. Yu, D. Rohne, K.L. Martin, et al. 2004. Heterologous envelope immunogens contribute to AIDS vaccine protection in rhesus monkeys. J. Virol. 78:7490-7497.
14. Rouzioux, C., J.B. Hubert, M. Burgard, C. Deveau, C. Goujard, M. Bary, D. Sereni, J.P. Viard, J.F. Delfraissy, and L. Meyer. 2005. Early levels of HIV-1 DNA in peripheral blood mononuclear cells are predictive of disease progression independently of HIV-1 RNA levels and CD4+ T cell counts. J. Infect. Dis. 192:46-55.
15. Mattapallil, J.J., Z. Smit-McBride, M. McChesney, and S. Dandekar. 1998. Intestinal intraepithelial lymphocytes are primed for gamma interferon and MIP-1beta expression and display antiviral cytotoxic activity despite severe CD4(+) T-cell depletion in primary simian immunodeficiency virus infection. J. Virol. 72:6421-6429.
16. Mascola, J.R., A. Sambor, K. Beaudry, S. Santra, B. Welcher, M.K. Louder, T.C. Vancott, Y. Huang, B.K. Chakrabarti, W.P. Kong, et al. 2005. Neutralizing antibodies elicited by immunization of monkeys with DNA plasmids and recombinant adenoviral vectors expressing human immunodeficiency virus type 1 proteins. J. Virol. 79:771-779.
17. Haigwood, N.L., D.C. Montefiori, W.F. Sutton, J. McClure, A.J. Watson, G. Voss, V.M. Hirsch, B.A. Richardson, N.L. Letvin, S.L. Hu, and P.R. Johnson. 2004. Passive immunotherapy in simian immunodeficiency virus-infected macaques accelerates the development of neutralizing antibodies. J. Virol. 78:5983-5995.
18. Ferrantelli, F., R.A. Rasmussen, K.A. Buckley, P.L. Li, T. Wang, D.C. Montefiori, H. Katinger, G. Stiegler, D.C. Anderson, H.M. McClure, and R.M. Ruprecht. 2004. Complete protection of neonatal rhesus macaques against oral exposure to pathogenic simian-human immunodeficiency virus by human anti-HIV monoclonal antibodies. J. Infect. Dis. 189:2167-2173.
19. Ferrantelli, F., M. Kitabwalla, R.A. Rasmussen, C. Cao, T.C. Chou, H. Katinger, G. Stiegler, L.A. Cavacini, Y. Bai, J. Cotropia, et al. 2004. Potent cross-group neutralization of primary human immunodeficiency virus isolates with monoclonal antibodies-implications for acquired immunodeficiency syndrome vaccine. J. Infect. Dis. 189:71-74.
20. Mc Cann, C.M., R.J. Song, and R.M. Ruprecht. 2005. Antibodies: can they protect against HIV infection? Curr. Drug Targets Infect. Disord. 5:95-111.
21. Koup, R.A., J.T. Safrit, Y. Cao, C.A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D.D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
22. Kostense, S., S.A. Otto, G.J. Knol, E.H. Manting, N.M. Nanlohy, C. Jansen, J.M. Lange, M.H. van Oers, F. Miedema, and D. van Baarle. 2002. Functional restoration of human immunodeficiency virus and Epstein-Barr virus-specific CD8(+) T cells during highly active antiretroviral therapy is associated with an increase in CD4(+) T cells. Eur. J. Immunol. 32:1080-1089.
23. Lifson, J.D., J.L. Rossio, M. Piatak Jr., T. Parks, L. Li, R. Kiser, V. Coalter, B. Fisher, B.M. Flynn, S. Czajak, et al. 2001. Role of CD8(+) lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J. Virol. 75:10187-10199.
24. Matano, T., R. Shibata, C. Siemon, M. Connors, H.C. Lane, and M.A. Martin. 1998. Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J. Virol. 72:164-169.
25. + T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189:991-998.
26. Schmitz, J.E., M.J. Kuroda, S. Santra, V.G. Sasseville, M.A. Simon, M.A. Lifton, P. Racz, K. Tenner-Racz, M. Dalesandro, B.J. Scallon, et al. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science. 283:857-860.
27. Langlois, A.J., R.C. Desrosiers, M.G. Lewis, V.N. KewalRamani, D.R. Littman, J.Y. Zhou, K. Manson, M.S. Wyand, D.P. Bolognesi, and D.C. Montefiori. 1998. Neutralizing antibodies in sera from macaques immunized with attenuated simian immunodeficiency virus. J. Virol. 72:6950-6955.
28. Means, R.E., T. Greenough, and R.C. Desrosiers. 1997. Neutralization sensitivity of cell culture-passaged simian immunodeficiency virus. J. Virol. 71:7895-7902.
29. Musey, L., Y. Ding, M. Elizaga, R. Ha, C. Celum, and M.J. McElrath. 2003. HIV-1 vaccination administered intramuscularly can induce both systemic and mucosal T cell immunity in HIV-1-uninfected individuals. J. Immunol. 171:1094-1101.
30. Stevceva, L., X. Alvarez, A.A. Lackner, E. Tryniszewska, B. Kelsall, J. Nacsa, J. Tartaglia, W. Strober, and G. Franchini. 2002. Both mucosal and systemic routes of immunization with the live, attenuated NYVAC/simian immunodeficiency virus SIV(gpe) recombinant vaccine result in gag-specific CD8(+) T-cell responses in mucosal tissues of macaques. J. Virol. 76:11659-11676.
31. Baig, J., D.B. Levy, P.F. McKay, J.E. Schmitz, S. Santra, R.A. Subbramanian, M.J. Kuroda, M.A. Lifton, D.A. Gorgone, L.S. Wyatt, et al. 2002. Elicitation of simian immunodeficiency virus-specific cytotoxic T lymphocytes in mucosal compartments of rhesus monkeys by systemic vaccination. J. Virol. 76:11484-11490.
32. Letvin, N.L., J.R. Mascola, Y. Sun, D.A. Gorgone, A.P. Buzby, L. Xu, Z. Yang, B. Chakrabarti, S.S. Rao, J.E. Schmitz, et al. 2006. Immune correlates of survival in vaccinated monkeys after challenge with SIV. Science. In press.
33. Picker, L.J., and D.I. Watkins. 2005. HIV pathogenesis: the first cut is the deepest. Nat. Immunol. 6:430-432.
34. Douek, D.C., L.J. Picker, and R.A. Koup. 2003. T cell dynamics in HIV-1 infection. Annu. Rev. Immunol. 21:265-304.
35. Smit-McBride, Z., J.J. Mattapallil, M. McChesney, D. Ferrick, and S. Dandekar. 1998. Gastrointestinal T lymphocytes retain high potential for cytokine responses but have severe CD4(+) T-cell depletion at all stages of simian immunodeficiency virus infection compared to peripheral lymphocytes. J. Virol. 72:6646-6656.
36. + T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200:749-759.
37. Guadalupe, M., E. Reay, S. Sankaran, T. Prindiville, J. Flamm, A. McNeil, and S. Dandekar. 2003. Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J. Virol. 77:11708-11717.
38. + T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200:761-770.
39. Miller, C.J., Q. Li, K. Abel, E.Y. Kim, Z.M. Ma, S. Wietgrefe, L. La Franco-Scheuch, L. Compton, L. Duan, M.D. Shore, et al. 2005. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus. J. Virol. 79:9217-9227.
40. + memory T cells in rapidly progressive simian immunodeficiency virus infection. J. Exp. Med. 200:1299-1314.
41. Haigwood, N.L., A. Watson, W.F. Sutton, J. McClure, A. Lewis, J. Ranchalis, B. Travis, G. Voss, N.L. Letvin, S.L. Hu, et al. 1996. Passive immune globulin therapy in the SIV/macaque model: early intervention can alter disease profile. Immunol. Lett. 51:107-114.
42. Schmitz, J.E., R.P. Johnson, H.M. McClure, K.H. Manson, M.S. Wyand, M.J. Kuroda, M.A. Lifton, R.S. Khunkhun, K.J. McEvers, J. Gillis, et al. 2005. Effect of CD8+ lymphocyte depletion on virus containment after simian immunodeficiency virus SIVmac251 challenge of live attenuated SIVmac239delta3-vaccinated rhesus macaques. J. Virol. 79:8131-8141.
43. Endo, Y., T. Igarashi, Y. Nishimura, C. Buckler, A. Buckler-White, R. Plishka, D.S. Dimitrov, and M.A. Martin. 2000. Short- and long-term clinical outcomes in rhesus monkeys inoculated with a highly pathogenic chimeric simian/human immunodeficiency virus. J. Virol. 74:6935-6945.
44. Betts, M.R., D.R. Ambrozak, D.C. Douek, S. Bonhoeffer, J.M. Brenchley, J.P. Casazza, R.A. Koup, and L.J. Picker. 2001. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75:11983-11991.
45. Maecker, H.T., H.S. Dunn, M.A. Suni, E. Khatamzas, C.J. Pitcher, T. Bunde, N. Persaud, W. Trigona, T.M. Fu, E. Sinclair, et al. 2001. Use of overlapping peptide mixtures as antigens for cytokine flow cytometry. J. Immunol. Methods. 255:27-40.
46. De Rosa, S.C., L.A. Herzenberg, and M. Roederer. 2001. 11-color, 13-parameter flow cytometry: identification of human naive T cells by phenotype, function, and T-cell receptor diversity. Nat. Med. 7:245-248.
47. Pitcher, C.J., S.I. Hagen, J.M. Walker, R. Lum, B.L. Mitchell, V.C. Maino, M.K. Axthelm, and L.J. Picker. 2002. Development and homeostasis of T cell memory in rhesus macaque. J. Immunol. 168:29-43.
48. Montefiori, D.C. 2004. Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. In Current Protocols in Immunology. J.E. Coligan, A.M. Kruisbeck, D.H. Margulies, E.M. Shevach, W. Strober, and R. Coico, editors. John Wiley & Sons, Inc, New York. 12.11.11-12.11.15.