HIV-1 envelope resistance to proteasomal cleavage: Implications for vaccine induced immune responses

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Steers, Nicholas J ^a,b   Ratto Kim, Silvia ^a,b   de Souza, Mark S ^c   Currier, Jeffrey R ^a,b   Kim, Jerome H ^a   Michael, Nelson L ^a   Alving, Carl R ^a   Rao, Mangala ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN; EPITOPE; GAMMA INTERFERON; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; PEPTIDE; PEPTIDE FRAGMENT; PLACEBO; PROTEASOME; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; ANTIBODY RESPONSE; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DATA BASE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; MASS SPECTROMETRY; NORMAL HUMAN; PHASE 3 CLINICAL TRIAL; PROTEIN DEGRADATION; PROTEIN SUBUNIT; VIRUS ENVELOPE; VIRUS RESISTANCE;

AIDS VACCINES; AMINO ACID SEQUENCE; CATHEPSINS; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; IMMUNITY; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; MODELS, IMMUNOLOGICAL; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84864707126     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042579     Document Type: Article

References (54)

1. Cresswell P, ((2005)) Antigen processing and presentation. Immunol Rev 207:5-7.
2. Ramachandra L, Simmons D, Harding CV, ((2009)) MHC molecules and microbial antigen processing in phagosomes. Curr Opin Immunol 21:98-104.
3. Trombetta ES, Mellman I, ((2005)) Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 23:975-1028.
4. Giodini A, Albert ML, ((2010)) A whodunit: an appointment with death. Curr Opin Immunol 22:94-108.
5. Kloetzel PM, ((2001)) Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2:179-187.
6. Kloetzel PM, ((2004)) Generation of major histocompatibility complex class I antigens: functional interplay between proteasomes and TPPII. Nat Immunol 5:661-669.
7. Kloetzel PM, Ossendorp F, ((2004)) Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr Opin Immunol 16:76-81.
8. Loureiro J, Ploegh HL, ((2006)) Antigen presentation and the ubiquitin-proteasome system in host-pathogen interactions. Adv Immunol 92:225-305.
9. Rock KL, York IA, Goldberg AL, ((2004)) Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat Immunol 5:670-677.
10. Steers NJ, Currier JR, Kijak GH, di Targiani RC, Saxena A, et al. ((2011)) Cell type-specific proteasomal processing of HIV-1 Gag-p24 results in an altered epitope repertoire. J Virol 85:1541-1553.
11. Tenzer S, Stoltze L, Schonfisch B, Dengjel J, Muller M, et al. ((2004)) Quantitative analysis of prion-protein degradation by constitutive and immuno-20S proteasomes indicates differences correlated with disease susceptibility. J Immunol 172:1083-1091.
12. Seifert U, Maranon C, Shmueli A, Desoutter JF, Wesoloski L, et al. ((2003)) An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat Immunol 4:375-379.
13. Saric T, Graef CI, Goldberg AL, ((2004)) Pathway for degradation of peptides generated by proteasomes: a key role for thimet oligopeptidase and other metallopeptidases. J Biol Chem 279:46723-46732.
14. Munz C, ((2010)) Antigen processing via autophagy-not only for MHC class II presentation anymore? Curr Opin Immunol 22:89-93.
15. Boes M, van der Wel N, Peperzak V, Kim YM, Peters PJ, et al. ((2005)) In vivo control of endosomal architecture by class II-associated invariant chain and cathepsin S. Eur J Immunol 35:2552-2562.
16. Roche PA, Cresswell P, ((2011)) Proteolysis of the class II-associated invariant chain generates a peptide binding site in intracellular HLA-DR molecules. Proc. Natl. Acad. Sci. USA. 1991. 88: 3150-3154. J Immunol 187:1076-1080.
17. Chapman HA, ((2006)) Endosomal proteases in antigen presentation. Curr Opin Immunol 18:78-84.
18. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES, ((2005)) Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307:1630-1634.
19. Stern LJ, Potolicchio I, Santambrogio L, ((2006)) MHC class II compartment subtypes: structure and function. Curr Opin Immunol 18:64-69.
20. Villadangos JA, Schnorrer P, Wilson NS, ((2005)) Control of MHC class II antigen presentation in dendritic cells: a balance between creative and destructive forces. Immunol Rev 207:191-205.
21. Gavioli R, Gallerani E, Fortini C, Fabris M, Bottoni A, et al. ((2004)) HIV-1 tat protein modulates the generation of cytotoxic T cell epitopes by modifying proteasome composition and enzymatic activity. J Immunol 173:3838-3843.
22. Gavioli R, Cellini S, Castaldello A, Voltan R, Gallerani E, et al. ((2008)) The Tat protein broadens T cell responses directed to the HIV-1 antigens Gag and Env: implications for the design of new vaccination strategies against AIDS. Vaccine 26:727-737.
23. Steers NJ, Peachman KK, McClain SR, Alving CR, Rao M, ((2009)) Human immunodeficiency virus type 1 Gag p24 alters the composition of immunoproteasomes and affects antigen presentation. J Virol 83:7049-7061.
24. Stove V, Verhasselt B, ((2006)) Modelling thymic HIV-1 Nef effects. Curr HIV Res 4:57-64.
25. van Hall T, Laban S, Koppers-Lalic D, Koch J, Precup C, et al. ((2007)) The varicellovirus-encoded TAP inhibitor UL49.5 regulates the presentation of CTL epitopes by Qa-1b1. J Immunol 178:657-662.
26. Verweij MC, Ressing ME, Knetsch W, Quinten E, Halenius A, et al. ((2011)) Inhibition of mouse TAP by immune evasion molecules encoded by non-murine herpesviruses. Mol Immunol 48:835-845.
27. Hirsch C, Misaghi S, Blom D, Pacold ME, Ploegh HL, ((2004)) Yeast N-glycanase distinguishes between native and non-native glycoproteins. EMBO Rep 5:201-206.
28. Kario E, Tirosh B, Ploegh HL, Navon A, ((2008)) N-linked glycosylation does not impair proteasomal degradation but affects class I major histocompatibility complex presentation. J Biol Chem 283:244-254.
29. Adams EW, Ratner DM, Seeberger PH, Hacohen N, ((2008)) Carbohydrate-mediated targeting of antigen to dendritic cells leads to enhanced presentation of antigen to T cells. Chembiochem 9:294-303.
30. Burgdorf S, Lukacs-Kornek V, Kurts C, ((2006)) The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J Immunol 176:6770-6776.
31. Burgdorf S, Kautz A, Bohnert V, Knolle PA, Kurts C, ((2007)) Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316:612-616.
32. Leonard CK, Spellman MW, Riddle L, Harris RJ, Thomas JN, et al. ((1990)) Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J Biol Chem 265:10373-10382.
33. Zhu X, Borchers C, Bienstock RJ, Tomer KB, ((2000)) Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 39:11194-11204.
34. Turville S, Wilkinson J, Cameron P, Dable J, Cunningham AL, ((2003)) The role of dendritic cell C-type lectin receptors in HIV pathogenesis. J Leukoc Biol 74:710-718.
35. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. ((2009)) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361:2209-2220.
36. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, et al. ((2012)) Immune-correlates analysis of an HIV-1 vaccine efficacy trial. The New England Journal of Medicine 366:1275-1286.
37. Kyte J, Doolittle RF, ((1982)) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105-132.
38. de Souza MS, Ratto-Kim S, Chuenarom W, Schuetz A, Chantakulkij S, et al. ((2012)) The Thai Phase III Trial (RV144) Vaccine Regimen Induces T Cell Responses That Preferentially Target Epitopes within the V2 Region of HIV-1 Envelope. J Immunol 188:5166-5176.
39. Raska M, Takahashi K, Czernekova L, Zachova K, Hall S, et al. ((2010)) Glycosylation patterns of HIV-1 gp120 depend on the type of expressing cells and affect antibody recognition. J Biol Chem 285:20860-20869.
40. Yu B, Fonseca DP, O'Rourke SM, Berman PW, ((2010)) Protease cleavage sites in HIV-1 gp120 recognized by antigen processing enzymes are conserved and located at receptor binding sites. J Virol 84:1513-1526.
41. Didierlaurent AM, Morel S, Lockman L, Giannini SL, Bisteau M, et al. ((2009)) AS04, an aluminum salt- and TLR4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity. J Immunol 183:6186-6197.
42. Creasy BM, McCoy KL, ((2011)) Cytokines regulate cysteine cathepsins during TLR responses. Cell Immunol 267:56-66.
43. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, et al. ((2008)) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9:847-856.
44. Sakamoto T, Saito H, Ishii K, Takahashi H, Tanabe S, et al. ((2006)) Aluminum inhibits proteolytic degradation of amyloid beta peptide by cathepsin D: a potential link between aluminum accumulation and neuritic plaque deposition. FEBS Lett 580:6543-6549.
45. Lucchiari-Hartz M, Lindo V, Hitziger N, Gaedicke S, Saveanu L, et al. ((2003)) Differential proteasomal processing of hydrophobic and hydrophilic protein regions: contribution to cytotoxic T lymphocyte epitope clustering in HIV-1-Nef. Proc Natl Acad Sci U S A 100:7755-7760.
46. Karasavvas N, Billings E, Rao M, Currier J, Michael NL, et al. ((2011)) The Thai Phase III Clinical Trial (RV144) Induces the Generation of Antibodies That Target a Conserved Region Within the V2 Loop of gp120. AIDS Research and Human Retroviruses 27:A-29.
47. Zolla-Pazner S, Cardozo T, deCamp A, Haynes B, Kim J, et al. ((2011)) V2-Reactive Antibodies in RV144 Vaccinees'. Plasma AIDS Research and Human Retroviruses 27:A-21.
48. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, et al. ((2007)) CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13:46-53.
49. Julg B, Williams KL, Reddy S, Bishop K, Qi Y, et al. ((2010)) Enhanced anti-HIV functional activity associated with Gag-specific CD8 T-cell responses. J Virol 84:5540-5549.
50. Sharp ER, Willberg CB, Kuebler PJ, Abadi J, Fennelly GJ, et al. ((2011)) Immunodominance of HIV-1 specific CD8+ T-cell responses is related to disease progression rate in vertically infected adolescents. PLoS One 6:e21135.
51. Watts C, ((2004)) The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat Immunol 5:685-692.
52. Currier JR, Kuta EG, Turk E, Earhart LB, Loomis-Price L, et al. ((2002)) A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J Immunol Methods 260:157-172.
53. Ratto S, Sitz KV, Scherer AM, Manca F, Loomis LD, et al. ((1995)) Establishment and characterization of human immunodeficiency virus type 1 (HIV-1) envelope-specific CD4+ T lymphocyte lines from HIV-1-seropositive patients. J Infect Dis 171:1420-1430.
54. Roederer M, Nozzi JL, Nason MC, ((2011)) SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79:167-174.