Sustained suppression of SHIV89.6P replication in macaques by vaccine-induced CD8+ memory T cells

AIDS

Volumn 22, Issue 14, 2008, Pages 1739-1748

  Yin, Jiangmei ^a   Dai, Anlan ^a   Kutzler, Michele A ^b   Shen, Anding ^c   LeCureux, Jonathan ^c   Lewis, Mark G ^d   Waldmann, Thomas ^e   Weiner, David B ^a   Boyer, Jean D ^a,f  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c CALVIN COLLEGE   (United States)

^d Research Section   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f Laboratory Medicine   (United States)

Author keywords

CD8? memory T cell; DNA vaccine; IL 15; SHIV replication; Suppression

Indexed keywords

DNA; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 15; PERFORIN; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE;

ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNE RESPONSE; MACACA; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; GENE PRODUCTS, GAG; IMMUNOLOGIC MEMORY; INTERLEUKIN-15; MACACA MULATTA; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TIME; TREATMENT OUTCOME; VACCINES, DNA; VIRUS REPLICATION;

EID: 61849103667     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32830efdae     Document Type: Article

References (40)

1. Borrow P, Lewicki H, Hahn BH, Shaw GM, OldstoneMB. Virus-specific CD8R cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 1994; 68:6103-6110.
2. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W, et al. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 1994; 68:4650-4655.
3. Reimann KA, Tenner-Racz K, Racz P, Montefiori DC, Yasutomi Y, Lin W, et al. Immunopathogenic events in acute infection of rhesus monkeys with simian immunodeficiency virus of macaques. J Virol 1994; 68:2362-2370.
4. Kuroda MJ, SchmitzJE, Charini WA, Nickerson CE, Lifton MA, Lord CI, et al. Emergence of CTL coincides with clearance of virus during primary simian immunodeficiency virus infection in rhesus monkeys. J Immunol 1999; 162:5127-5133.
5. Musey L, Hughes J, Schacker T, Shea T, Corey L, McElrath MJ. Cytotoxic-T-cell responses, viral load, and disease progression in early human immunodeficiency virus type 1 infection. N EnglJ Med 1997; 337:1267-1274.
6. OggGS,JinX, BonhoefferS, DunbarPR, Nowak MA, Monard S, et al. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998; 279:2103-2106.
7. YasutomiY, Reimann KA, Lord CI, MillerMD, Letvin NL. Simian immunodeficiency virus-specific CD8R lymphocyte response in acutely infected rhesus monkeys. J Virol 1993; 67:1707-1711.
8. Migueles SA, Laborico AC, Shupert WL, Sabbaghian MS, Rabin R, Hallahan CW, et al. HIV-specificCD8R Tcell proliferation is coupled to perforin expression and is maintained in nonpro-gressors. Nat Immunol 2002; 3:1061-1068.
9. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, Abraham J, et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8R T cells. Blood 2006; 107:4781-4789.
10. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, Blanchard J, et al. Dramatic rise in plasma viremia after CD8(R) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 1999; 189:991-998.
11. Matano T, Shibata R, Siemon C, Connors M, Lane HC, Martin MA. 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 1998; 72:164-169.
12. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, et al. Control of viremia in simian immunodeficiency virus infection by CD8R lymphocytes. Science 1999; 283:857-860.
13. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004; 22:745-763.
14. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999; 401:708-712.
15. Lanzavecchia A, Sallusto F. Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. Science 2000; 290:92-97.
16. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003; 4:225-234.
17. Boyer JD, Robinson TM, Kutzler MA, Vansant G, Hokey DA, Kumar S, et al. Protection against simian/human immunodeficiency virus (SHIV) 89.6P in macaques after coimmunization with SHIV antigen and IL-15 plasmid. Proc Natl Acad Sci USA 2007; 104:18648-18653.
18. Matano T, Kobayashi M, Igarashi H, Takeda A, Nakamura H, Kano M, et al. Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J Exp Med 2004; 199:1 709-1 718.
19. Hryniewicz A, Price DA, Moniuszko M, Boasso A, Edghill-Spano Y, West SM, et al. Interleukin-15 but not interleukin-7 abrogates vaccine-induced decrease in virus level in simian immunodeficiency virus mac251-infected macaques. J Immunol 2007; 178:3492-3504.
20. Pitcher CJ, Hagen SI, WalkerJM, Lum R, Mitchell BL, MainoVC, et al. Development and homeostasis of T cell memory in rhesus macaque. J Immunol 2002; 168:29-43.
21. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, et al. CD4R T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200:749-759.
22. NishimuraY, Igarashi T, Buckler-White A, Buckler C, Imamichi H, Goeken RM, et al. Loss of naive cells accompanies memory CD4R T-cell depletion during long-term progression to AIDS in Simian immunodeficiency virus-infected macaques. J Virol 2007; 81:893-902.
23. Veazey RS, Mansfield KG, Tham IC, Carville AC, Shvetz DE, Forand AE, Lackner AA. Dynamics of CCR5 expression by CD4(R) T cells in lymphoid tissues during simian immunodeficiency virus infection. J Virol 2000; 74:11001-11007.
24. Guadalupe M, Reay E, Sankaran S, Prindiville T, Flamm J, McNeil A, Dandekar S. Severe CD4R 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 2003; 77:11708-11717.
25. Zhang X, Sun S, Hwang I, Tough DF, Sprent J. Potent and selective stimulation of memory-phenotype CD8R T cells in vivo by IL-15. Immunity 1998; 8:591-599.
26. Becker TC, Wherry EJ, Boone D, Murali-Krishna K, Antia R, Ma A, Ahmed R. Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J Exp Med 2002; 195:1541-1548.
27. KuCC, Murakami M, Sakamoto A, KapplerJ, Marrack P. Control of homeostasis of CD8R memory T cel ls by opposing cytoki nes. Science 2000; 288:675-678.
28. Moore AC, Kong WP, Chakrabarti BK, Nabel GJ. Effects of antigen and genetic adjuvants on immune responses to human immunodeficiency virus DNA vaccines in mice. J Virol 2002; 76:243-250.
29. Oh S, Berzofsky JA, Burke DS, Waldmann TA, Perera LP. Coadministration of HIV vaccine vectors with vaccinia viruses expressing IL-15 but not IL-2 induces long-lasting cellular immunity. Proc Natl Acad Sci USA 2003; 100:3392-3397.
30. Marks-KonczalikJ, Dubois S, Losi JM, Sabzevari H, Yamada N, Feigenbaum L, et al. IL-2-induced activation-induced cell death is inhibited in IL-15 transgenic mice. Proc Natl Acad Sci USA 2000; 97:11445-11450.
31. Schluns KS, Klonowski KD, Lefrancois L. Transregulation of memory CD8 T-cell proliferation by IL-15RalphaR bone marrow-derived cells. Blood 2004; 103:988-994.
32. Waldmann TA, Dubois S, Tagaya Y. Contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for immunotherapy. Immunity 2001; 14:105-110.
33. Fehniger TA, Caligiuri MA. Interleukin 15: biology and relevance to human disease. Blood 2001; 97:14-32.
34. Rosenberg SA. Interleukin-2 and the development of immunotherapy for the treatment of patients with cancer. Cancer J Sci Am 2000; 6 (Suppl 1):S2-S7.
35. Kutzler MA, Robinson TM, Chattergoon MA, Choo DK, Choo AY, Choe PY, et al. Coimmunization with an optimized IL-15 plasmid results in enhanced function and longevity of CD8 T cells that are partially independent of CD4 T cell help. I Immunol 2005; 175:112-123.
36. ChehimiJ, Marshal l JD, SalvucciO, Frank I, Chehimi S, Kawecki S, et al. IL-15 enhances immune functions during HIV infection. I Immunol 1997; 158:5978-5987.
37. Mueller YM, Bojczuk PM, Halstead ES, Kim AH, Witek J, Altman JD, Katsikis PD. IL-15 enhances survival and function of HIV-specific CD8R T cells. Blood 2003; 101:1024-1029.
38. Mueller YM, Do DH, Altork SR, Artlett CM, Gracely EJ, Katsetos CD, et al. IL-15 treatment during acute simian immunodeficiency virus (SIV) infection increases viral set point and accelerates disease progression despite the induction of stronger SIV-specificCD8R Tcell responses. J Immunol 2008; 180:350-360.
39. Kawada M, TsukamotoT, Yamamoto H, Takeda A, Igarashi H, Watkins DI, Matano T. Long-term control of simian immunodeficiency virus replication with central memory CD4R T-cell preservation after nonsterile protection by a cytotoxic T-lymphocyte-based vaccine. J Virol 2007; 81:5202-5211.
40. Vaccari M, Trindade CJ, Venzon D, Zanetti M, Franchini G. Vaccine-induced CD8R central memory T cells in protection from simian AIDS. J Immunol 2005; 175:3502-3507.