Targeting of HIV-1 antigens for rapid intracellular degradation enhances cytotoxic T lymphocyte (CTL) recognition and the induction of de novo CTL responses in vivo after immunization

Journal of Experimental Medicine

Volumn 185, Issue 5, 1997, Pages 909-920

  Tobery, Timothy W ^a   Siliciano, Robert F ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; IMMUNIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN TARGETING; VIRUS IMMUNITY;

AIDS VACCINES; ANIMALS; ANTIGEN PRESENTATION; CELL COMPARTMENTATION; CYTOPLASM; GENE PRODUCTS, ENV; GENE PRODUCTS, NEF; HIV ANTIGENS; HIV INFECTIONS; HIV-1; HUMANS; IMMUNIZATION; MICE; MICE, INBRED BALB C; MODELS, IMMUNOLOGICAL; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; UBIQUITINS;

EID: 0030977234     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.185.5.909     Document Type: Article

References (54)

1. Klavinskis, L.S., A. Tishon, and M.B. Oldstone. 1989. Efficiency and effectiveness of cloned virus-specific cytotoxic T lymphocytes in vivo. J. Immnnol. 143:2013-2016.
2. Cannon, M.J., P.J. Openshaw, and B.A. Askonas. 1988. Cytotoxic T cells clear virus but augment lung pathology in mice infected with respiratory syncytial virus. J. Exp. Med. 168:1163-1168.
3. Riddell, S.R., K.S. Watanabe, J.M. Goodrich, C.R. Li, M.E. Agha, and P.D. Greenberg. 1992. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science (Wash. DC). 257:238-241.
4. Braciale, T.J., and V.L. Braciale. 1992. Viral antigen presentation and MHC assembly. Semin. Immunol. 4:81-84.
5. Yewdell, J.W., and J.R. Bennink. 1993. Antigen processing: a critical factor in rational vaccine design. Semin. Hematol. 30: 26-32.
6. Monaco, J.J. 1995. Pathways for the processing and presenta tion of antigens to T cells. J. Leukocyte Biol. 57:543-547.
7. Borrow, P., H. Lewicki, B.H. Hahn, G.M. Shaw, and M.B. Oldstone. 1994. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68:6103-6110.
8. 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.
9. Gallimore, A., M. Cranage, N. Cook, N. Almond, J. Bootman, E. Rud, P. Silvera, M. Dennis, T. Corcoran, J. Stott et al. 1995. Early suppression of SIV replication by CD8+ nef-specific cytotoxic T cells in vaccinated macaques. Nat. Med. 1:1167-1173.
10. Letvin, N.L., K.A. Reimann, Y. Yasutomi, D.J. Ringler, and H. Yamamoto. 1994. The SIVmac specific cytotoxic T lymphocyte response in the acutely infected rhesus monkey. Curr. Top. Microbiol. Immunol. 188:175-184.
11. Reimann, K.A., R.K. Tenner, P. Racz, D.C. Montefiori, Y. Yasutomi, W. Lin, B.J. Ransil, and N.L. Letvin. 1994. Immunopathogenic events in acute infection of rhesus monkeys with simian immunodeficiency virus of macaques. J. Virol. 68:2362-2370.
12. Yasutomi, Y., K.A. Reimann, C.I. Lord, M.D. Miller, and N.L. Letvin. 1993. Simian immunodeficiency virus-specific CD8+ lymphocyte response in acutely infected rhesus monkeys. J. Virol. 67:1707-1711.
13. Kalams, S.A., and B.D. Walker. 1994. The cytotoxic T-lymphocyte response in HIV-1 infection. Clin. Lab. Med. 14: 271-299.
14. Oldstone, M.B., A. Tishon, M. Eddleston, J.C. de la Torre, T. McKee, and J.L. Whitton. 1993. Vaccination to prevent persistent viral infection. J. Virol. 67:4372-4378.
15. Klavinskis, L.S., J.L. Whitton, E. Joly, and M.B. Oldstone. 1990. Vaccination and protection from a lethal viral infection: identification, incorporation, and use of a cytotoxic T lymphocyte glycoprotein epitope. Virology. 178:393-400.
16. Tishon, A., M. Eddleston, J.C. de la Torre, and M.B. Oldstone, 1993. Cytotoxic T lymphocytes cleanse viral gene products from individually infected neurons and lymphocytes in mice persistently infected with lymphocytic chpriomeningitis virus. Virology. 197:463-467.
17. Rowland, J.S., J. Sutton, K. Ariyoshi, T. Dong, F. Gotch, S. McAdam, D. Whitby, S. Sabally, A. Gallimore, T. Corrah et al. 1995. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat. Med. 1:59-64.
18. Langlade, D.P., N. Ngo-Giang-Huong, F. Ferchal, and E. Oksenhendler. 1994. Human immunodeficiency virus (HIV) nef-specific cytotoxic T lymphocytes in noninfected heterosexual contact of HIV-infected patients. J. Clin. Invest. 93: 1293-1297.
19. Yasutomi, Y., H.L. Robinson, S. Lu, F. Mustafa, C. Lekutis, J. Arthos, J.I. Mullins, G. Voss, K. Manson, M. Wyand et al. 1996, Simian immunodeficiency virus-specific cytotoxic T-lymphocyte induction through DNA vaccination of rhesus monkeys. J. Virol. 70:678-681.
20. Belich, M.P., and J. Trowsdale. 1995. Proteasome and class I antigen processing and presentation. Mol. Biol. Rep. 21:53-56.
21. Michalek, M.T., E.P. Grant, C. Gramm, A.L. Goldberg, and K.L. Rock. 1993. A role for the ubiquitin-dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature (Loud.). 363:552-554.
22. Rock, K.L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A.L. Goldberg. 1994. Inhibitors of the proteasomc block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell. 78:761-771.
23. Harding, C.V., J. France, R. Song, J.M. Farah, S. Chatterjee, M. Iqbal, and R. Siman. 1995. Novel dipeptide aldehydes are proteasome inhibitors and block the MHC-I antigen-processing pathway. J. Immunol. 155:1767-1775.
24. Restifo, N.P., I. Bacik, K.R. Irvine, J.W. Yewdell, B.J. McCabe, R.W. Anderson, L.C. Eisenlohr, S.A. Rosenberg, and J.R. Bennink. 1995. Antigen processing in vivo and the elicitation of primary CTL responses. J. Immunol. 154:4414-4422.
25. Deverson, E., I.R. Gow, W.J. Coadwell, J.J. Monaco, G.W. Butcher, and J.C. Howard. 1990. MHC class II region encoding proteins related to the multidrug resistance family of transmembrane transporters. Nature (Loud.). 348:738-741.
26. Trowsdale, J., I. Hanson, I. Mockridge, S. Beck, A. Town-send, and A. Kelly. 1990. Sequences encoded in the class II region of the MHC related to the "ABC" superfamily of transporters. Nature (Loud.). 348:741-744.
27. Spies, T., M. Breshnan, S. Bahram, D. Arnold, G. Blanck, E. Mellins, D. Pious, and R. DeMars. 1990. A gene in the human major histocompatibility complex class II region controlling the class I antigen presentation pathway. Nature (Lond.). 348:744-747.
28. Monaco, J.J., S. Cho, and M. Attaya. 1990. Transport protein genes in the murine MHC: possible implications for antigen processing. Science (Wash. DC). 250:1723-1726.
29. Kelly, A., S.H. Powis, L.-A. Kerr, I. Mockridge, T. Elliot, J. Bastin, B. Uchanska-Ziegler, A. Ziegler, J. Trowsdale, and A. Townsend. 1992. Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature (Loud.), 355:641-644.
30. Van Kaer, L., P.G. Ashton-Rickardt, H.L. Pleogh, and S. Tonegawa. 1992. TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell. 71:1205-1214.
31. Shepherd, J.C., T.N.M. Schumacher, P.G. Ashton-Rickardt, S. Imaeda, H.L. Pleogh, C.A. Janeway, and S. Tonegawa. 1993. Tap 1-dependent peptide translocation in vitro is ATP dependent and peptide selective. Cell. 74:577-584.
32. Neefjes, J.J., F. Momburg, and G.J. Hammerling. 1993. Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science (Wash. DC). 261:769.
33. Murray, N., and A. McMichael. 1992. Antigen presentation in virus infection. Curr. Opin. Immunol. 4:401-407.
34. Milligan, G.N., L.A. Morrison, J. Gorka, V.L. Braciale, and T.J. Braciale. 1990. The recognition of a viral antigenic moiety by class I MHC-restricted cytolytic T lymphocytes is limited by the availability of the endogenously processed antigen J. Immunol. 145:3188-3193.
35. Villanueva, M.S., P. Fischer, K. Feen, and E.G. Pamer. 1994. Efficiency of MHC class I antigen processing: a quantitative analysis. Immunity. 1:479-489.
36. Grant, E.P., M.T. Michalek, A.L. Goldberg, and K.L. Rock. 1995. Rate of antigen degradation by the ubiquitin-proteasome pathway influences MHC class I presentation. J. Immunol. 155:3750-3758.
37. Gaczynska, M., K.L. Rock, and A.L. Goldberg. 1993. Role of proteasomes in antigen presentation. Enzyme Protein. 47: 354-369.
38. Goldberg, A.L., and K.L. Rock. 1992. Proteolysis, proteasomes and antigen presentation. Nature (Loud.). 357:375-379.
39. Bachmair, A., and A. Varshavsky. 1989. The degradation signal in a short-lived protein. Cell. 56:1019-1032.
40. Varshavsky, A. 1992. The N-end rule. Cell. 69:725-735.
41. Johnson, E.S., B. Bartel, W. Seufert, and A. Varshavsky. 1992. Ubiquitin as a degradation signal. EMBO (Eur. Mol. Biol. Organ.) J. 11:497-505.
42. Townsend, A., J. Bastin, K. Gould, G. Brownlee, M. Andrew, B. Coupar, D. Boyle, S. Chan, and G. Smith. 1988. Defective presentation to class 1-restricted cytotoxic T lymphocytes in vaccinia-infected cells is overcome by enhanced degradation of antigen. J. Exp. Med. 168:1211-1224.
43. Ozkaynak, E., D. Finley, and A. Varshavsky. 1984. The yeast ubiquitin gene: head-to-tail repeats encoding a polyubiquitin precursor protein. Nature (Loud.). 312:663-666.
44. Bachmair, A., D. Finley, and A. Varshavsky. 1986. In vivo half-life of a protein is a function of its amino-tenninal residue. Science (Wash. DC). 234:179-186.
45. Townsend, A.R.M., J. Bastin, K. Could, and G.G. Brownlee. 1986. Cytotoxic T lymphocytes recognise influenza heniagglutinin that lacks a signal sequence. Nature (Lond.). 234:575-577.
46. Takahashi, K., L.C. Dai. T.R. Fuerst, W.E. Biddison. P.L. Earl, B. Moss, and F.A. Ennis. 1991. Specific lysis of human immunodeficiency virus type 1-infected cells by a HLA-A3.1 -restricted CD8+ cytotoxic T-lymphocyte clone that recognizes a conserved peptide sequence within the gp41 subunit of the envelope protein. Proc. Natl. Acad. Sci. USA. 88:10277-10281.
47. Hammond, S.A., R.P. Johnson, S.A. Kalams, B.D. Walker, M. Takiguchi, J.T. Safrit, R.A. Koup, and R.F. Siliciano. 1995. An epitope-selective, transporter associated with antigen presentation (TAP)-1/2-independem pathway and a more general TAP-1/2-dependent antigen-processing pathway allow recognition of the HIV-1 envelope glycoprotein by CD8+ CTL. J. Immunol. 154:6140-6156.
48. Hammond, S.A., R.C. Bollinger, T.W. Tobery, and R.F. Siliciano. 1993. Transporter-independent processing of HIV-1 envelope protein for recognition by CD84+ T cells. Nature (Lond,). 364:158-161.
49. Takahashi, H., J. Cohen, A. Hosmalin, K.B. Cease, R. Houghten, J.L. Cornette, C. DeLisi, B. Moss, R.N. Germain, and J.A. Berzofsky. 1988. An immunodominant epitope of the human immunodeficiency virus envelope glycoprotein gp160 recognized by class I major histocompatibility molecule-restricted murine cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA. 85:3105-3109.
50. Koenig, S., T.R. Fuerst, L.V. Wood, R.M. Woods, J.A. Suzich. G.M. Jones, V.F. de la Cruz, R.J. Davey, S. Venkatesan, B. Moss et al. 1990. Mapping the fine specificity of a cytolytic T cell response to HIV-1 nef protein. J. Immunol. 145: 127-135.
51. Goth, S., V. Nguyen, and N. Shastri. 1996. Generation of naturally processed peptide/MHC class I complexes is independent of the stability of endogenously synthesized precursors. J. Immunol. 157:1894-1904.
52. Schwartz, O., V. Marechal, S. Le Gall, F. Lemonnier, and J.M. Heard. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-342.
53. Cheynier, R., D.P. Langlade, M.R. Marescot, S. Blanche, G. Blondin, H.S. Wain, C. Griscelli, E. Vilmer, and F. Plata. 1992. Cytotoxic T lymphocyte responses in the peripheral blood of children born to human immunodeficiency virus-1-infected mothers. Eur. J. Immunol. 22:2211-2217.
54. De, M.A., C. Cirillo, and L. Moretta. 1994. Occurrence of human immunodeficiency virus type 1 (HIV-l)-specific cytolytic T cell activity in apparently uninfected children born to HIV-1-infected mothers. J. Infect. Dis. 170:1296-1299.