Differential HIV epitope processing in monocytes and CD4 T cells affects cytotoxic T lymphocyte recognition

Journal of Infectious Diseases

Volumn 200, Issue 2, 2009, Pages 236-243

  Lazaro, Estibaliz ^a   Godfrey, Sasha Blue ^a   Stamegna, Pamela ^a   Ogbechie, Tobi ^a   Kerrigan, Christopher ^a   Zhang, Mei ^a   Walker, Bruce D ^a,b   Gall, Sylvie Le ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDASE; PEPTIDE;

ANTIGEN PRESENTATION; ANTIGENICITY; ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOSOL; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MASS SPECTROMETRY; MONOCYTE; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; VIRUS INFECTION;

ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; FEMALE; HIV; HIV INFECTIONS; HUMANS; MALE; MONOCYTES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 67650649761     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/599837     Document Type: Article

References (44)

1. + cells: evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. J Virol 1997;71:3120-8.
2. Kageyama S, Tsomides TJ, Sykulev Y, Eisen HN. Variations in the number of peptide-MHC class I complexes required to activate cytotoxic T cell responses. J Immunol 1995; 154:567-76.
3. Christinck ER, Luscher MA, Barber BH, Williams DB. Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature 1991;352:67-70.
4. Reay PA, Matsui K, Haase K, Wulfing C, Chien YH, Davis MM. Determination of the relationship between T cell responsiveness and the number of MHC-peptide complexes using specific monoclonal antibodies. J Immunol 2000; 164:5626-34.
5. Sykulev Y, Joo M, Vturina I, Tsomides TJ, Eisen HN. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 1996;4:565-71.
6. Krogsgaard M, Davis MM. How T cells "see" antigen. Nat Immunol 2005; 6:239-5.
7. Addo MM, Yu XG, Rathod A, et al. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J Virol 2003;77:2081-92.
8. Altfeld M, Kalife ET, Qi Y, et al. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLos Med 2006;3:e403.
9. Frahm N, Linde C, Brander C. Identification of HIV-derived, HLA class I restricted CTL epitopes: insights into TCR repertoire, CTL escape and viral fitness. In: Korber BT, Brander C, Haynes BF, et al., eds. HIV molecular immunology 2006/2007. Los Alamos, NM: Los Alamos National Laboratory, Theoretical Biology and Biophysics, 2007.
10. - T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 2007; 13:46-53.
11. - T-cell responses: relationship to viral load in untreated HIV infection. J Virol 2001;75:11983-91.
12. - T cells in primary HIV-1 infection. J Virol 2003; 77:6867-78.
13. --T-cell responses to the Gag protein of HIV-1 correlates inversely with viral load in plasma. J Virol 2002; 76: 2298-305.
14. - T cells residing within human lymphoid tissues. Immunity 2001; 15:671-82.
15. Chun TW, Carruth L, Finzi D, et al. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 1997; 387:183-8.
16. Chun TW, Stuyver L, Mizeli SB, et al. Presence of an inducible HIV1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci USA 1997;94:13193-7.
17. + T cells. Nature 2002;417:95-8.
18. + monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J Immunol 2007; 178:6581-9.
19. + monocytes and its potential role as a source of virus in patients on highly active antiretroviral therapy. J Virol 2002;76:707-16.
20. Koenig S, Gendelman HE, Orenstein JM, et al. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 1986;233:1089-93.
21. Keele BF, Tazi L, Gartner S, et al. Characterization of the follicular dendritic cell reservoir of human immunodeficiency virus type 1. J Virol 2008;82:5548-61.
22. Goldberg A, Caseio P, Saric T, Rock KL. The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol Immunol 2002;39:147-64.
23. Saric T, Chang SC, Hattori A, et al. An IFN-gamma-induced aminopeptidase in the ER, ERAPl, trims precursors to MHC class I-presented peptides. Nat Immunol 2002;3:1169-76.
24. Serwold T, Gaw S, Shastri N. ER aminopeptidases generate a unique pool of peptides for MHC class I molecules. Nat Immunol 2001;2: 644-51.
25. Serwold T, Gonzalez F, Kim J, Jacob R, Shastri N. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 2002;419:480-3.
26. Lopez D, Gil-Torregrosa BC, Bergman C, Del Val M. Sequential cleavage by metallopeptidases and proteasomes is involved in processing HIV-1 ENV epitope for endogenous MHC class I antigen presentation. J Immunol 2000; 164:5070-7.
27. Seifer U, Maranon C, Shmueli A, et al. An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 2003;4:375-9.
28. Wherry EJ, Golovina TN, Morrison SE, et al. Re-evaluating the generation of a "proteasome-independent" MHC class I-restricted CD8 T cell epitope. J Immunol 2006; 176:2249-61.
29. Butz EA, Bevan MJ. Differential presentation of the same MHC class I epitopes by fibroblasts and dendritic cells. J Immunol 1998; 160: 2139-44.
30. - T cell immunodominance in primary and secondary influenza virus infections. J Exp Med 2003; 198:399-410.
31. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005; 307:1630-4.
32. Ossendorp F, Fu N, Camps M, et al. Differential expression regulation of the alpha and beta subunits of the PA28 proteasome activator in mature dendritic cells. J Immunol 2005; 174:7815-22.
33. Dahlmann B, Ruppert T, Kuehn L, Merforth S, Kloetzel PM. Different proteasome subtypes in a single tissue exhibit different enzymatic properties. J Mol Biol 2000;303:643-53.
34. Le Gall S, Stamegna P, Walker BD. Portable flanking sequences modulate CTL epitope processing. J Clin Invest 2007; 117:3563-75.
35. Le Gall S, Neuhof A, Rapoport TA. The ER membrane is permeable to small molecules. Mol Biol Cell 2004; 15:447-55.
36. Kisselev AF, Goldberg AL. Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol 2005;398:364-78.
37. Beninga J, Rock KL, Goldberg A. Interferon-gamma can stimulate postproteasomal trimming of the N terminus of an antigenic peptide by inducing leucine aminopeptidase. J Biol Chem 1998;273:18734-42.
38. Chang SC, Momburg F, Bhutani N, Goldberg AL. The ER aminopeptidase, ERAPl, trims precursors to lengths of MHC class I peptides by a "molecular ruler" mechanism. Proc Natl Acad Sci USA 2005; 102: 17107-12.
39. Sette A, Sidney J. Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics 1999;50:201- 12.
40. Korber BT, Brander C, Haynes BF, et al, eds. HIV molecular immunology 2008. Los Alamos, New Mexico: Los Alamos National Laboratory, Theoretical Biology and Biophysics, 2008.
41. Gavioli R, Gallerani E, Fortini C, et al. HIV-1 tat protein modulates the generation of cytotoxic T cell epitopes by modifying proteasome composition and enzymatic activity. J Immunol 2004; 173:3838-43.
42. Saveanu L, Carroll O, Lindo V, et al. Concerted peptide trimming by human ERAPl and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat Immunol 2005;6:689-97.
43. Noursadeghi M, Katz DR, Miller RF. HIV-1 infection of mononuclear phagocytic cells: the case for bacterial innate immune deficiency in AIDS. Lancet Infect Dis 2006;6:794-804.
44. Grage-Griebenow E, Fiad HD, Ernst M. Heterogeneity of human peripheral blood monocyte subsets. J Leukoc Biol 2001;69:11-20.