Critical effect of Pol escape mutations associated with detrimental allele HLA-C*15: 05 on clinical outcome in HIV-1 subtype A/E infection.
Journal
AIDS (London, England)
ISSN: 1473-5571
Titre abrégé: AIDS
Pays: England
ID NLM: 8710219
Informations de publication
Date de publication:
01 01 2021
01 01 2021
Historique:
pubmed:
9
10
2020
medline:
3
3
2021
entrez:
8
10
2020
Statut:
ppublish
Résumé
The mechanism explaining the role of detrimental HLA alleles in HIV-1 infections has been investigated in very few studies. HLA-A*29:01-B*07:05-C*15:05 is a detrimental haplotype in HIV-1 subtype A/E-infected Vietnamese individuals. The accumulation of mutations at Pol 653/657 is associated with a poor clinical outcome in these individuals. However, the detrimental HLA allele and the mechanism responsible for its detrimental effect remains unknown. Therefore, in this current study we identified the detrimental HLA allele and investigated the mechanism responsible for the detrimental effect. A T-cell epitope including Pol 653/657 and its HLA restriction were identified by using overlapping HIV-1 peptides and cell lines expressing a single HLA. The effect of the mutations on the T-cell recognition of HIV-1-infected cells was investigated by using target cells infected with the mutant viruses. The effect of these mutations on the clinical outcome was analyzed in 74 HLA-C*15:05 Vietnamese infected with the subtype A/E virus. We identified HLA-C*15:05-restricted SL9 epitope including Pol 653/657. PolS653A/T/L mutations within this epitope critically impaired the T-cell recognition of HIV-1-infected cells, indicating that these mutations had escaped from the T cells. T-cell responders infected with these mutants showed significantly lower CD4 T-cell counts than those with the wild-type virus or Pol S653K/Q mutants, which are not associated with HLA-C*15:05. The accumulation of Pol S653A/T/L escape mutants critically affected the control of HIV-1 by SL9-specific T cells and led to a poor clinical outcome in the subtype A/E-infected individuals having the detrimental HLA-C*15:05 allele.
Identifiants
pubmed: 33031103
doi: 10.1097/QAD.0000000000002704
pii: 00002030-202101010-00004
pmc: PMC7752225
doi:
Substances chimiques
Epitopes, T-Lymphocyte
0
HLA-C Antigens
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
33-43Références
Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, Goedert JJ, et al. HLA and HIV-1: heterozygote advantage and B∗35-Cw∗04 disadvantage . Science 1999; 283:1748–1752.
Gao X, Nelson GW, Karacki P, Martin MP, Phair J, Kaslow R, et al. Effect of a single amino acid change in MHC class I molecules on the rate of progression to AIDS . N Engl J Med 2001; 344:1668–1675.
Jin X, Gao X, Ramanathan M Jr, Deschenes GR, Nelson GW, O’Brien SJ, et al. Human immunodeficiency virus type 1 (HIV-1)-specific CD8+-T-cell responses for groups of HIV-1-infected individuals with different HLA-B∗35 genotypes . J Virol 2002; 76:12603–12610.
Carrington M, O’Brien SJ. The influence of HLA genotype on AIDS . Annu Rev Med 2003; 54:535–551.
Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection . Nat Med 1996; 2:405–411.
O’Brien SJ, Gao X, Carrington M. HLA and AIDS: a cautionary tale . Trends Mol Med 2001; 7:379–381.
Costello C, Tang J, Rivers C, Karita E, Meizen-Derr J, Allen S, et al. HLA-B∗5703 independently associated with slower HIV-1 disease progression in Rwandan women . AIDS 1999; 13:1990–1991.
Fellay J, Ge D, Shianna KV, Colombo S, Ledergerber B, Cirulli ET, et al. Common genetic variation and the control of HIV-1 in humans . PLoS Genet 2009; 5:e1000791.
Pereyra F, Jia X, McLaren PJ, Telenti A, de Bakker PI, Walker BD, et al. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation . Science 2010; 330:1551–1557.
Leslie A, Matthews PC, Listgarten J, Carlson JM, Kadie C, Ndung’u T, et al. Additive contribution of HLA class I alleles in the immune control of HIV-1 infection . J Virol 2010; 84:9879–9888.
Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, Weale M, et al. A whole-genome association study of major determinants for host control of HIV-1 . Science 2007; 317:944–947.
Migueles SA, Sabbaghian MS, Shupert WL, Bettinotti MP, Marincola FM, Martino L, et al. HLA B∗5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors . Proc Natl Acad Sci U S A 2000; 97:2709–2714.
Naruto T, Gatanaga H, Nelson G, Sakai K, Carrington M, Oka S, et al. HLA class I-mediated control of HIV-1 in the Japanese population, in which the protective HLA-B∗57 and HLA-B∗27 alleles are absent . J Virol 2012; 86:10870–10872.
Chikata T, Tran GV, Murakoshi H, Akahoshi T, Qi Y, Naranbhai V, et al. HLA class I-mediated HIV-1 control in Vietnamese infected with HIV-1 subtype A/E . J Virol 2018; 92:e01749-17.
Lazaryan A, Song W, Lobashevsky E, Tang J, Shrestha S, Zhang K, et al. The influence of human leukocyte antigen class I alleles and their population frequencies on human immunodeficiency virus type 1 control among African Americans . Hum Immunol 2011; 72:312–318.
Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, Chetty S, et al. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA . Nature 2004; 432:769–775.
Olvera A, Ganoza C, Perez-Alvarez S, Hildebrand W, Sanchez J, Brander C. HLA-B∗35-PX and HLA-B ∗ 35-PY subtype differentiation does not predict observed differences in level of HIV control in a Peruvian MSM cohort . AIDS 2014; 28:2323–2325.
Juarez-Molina CI, Valenzuela-Ponce H, Avila-Rios S, Garrido-Rodriguez D, Garcia-Tellez T, Soto-Nava M, et al. Impact of HLA-B∗35 subtype differences on HIV disease outcome in Mexico . AIDS 2014; 28:1687–1690.
Altfeld M, Addo MM, Rosenberg ES, Hecht FM, Lee PK, Vogel M, et al. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection . AIDS 2003; 17:2581–2591.
Goulder PJ, Walker BD. HIV and HLA class I: an evolving relationship . Immunity 2012; 37:426–440.
Streeck H, Lu R, Beckwith N, Milazzo M, Liu M, Routy JP, et al. Emergence of individual HIV-specific CD8 T cell responses during primary HIV-1 infection can determine long-term disease outcome . J Virol 2014; 88:12793–12801.
Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, Moodley E, et al. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load . Nat Med 2007; 13:46–53.
Murakoshi H, Akahoshi T, Koyanagi M, Chikata T, Naruto T, Maruyama R, et al. Clinical control of HIV-1 by cytotoxic T cells specific for multiple conserved epitopes . J Virol 2015; 89:5330–5339.
Chikata T, Murakoshi H, Koyanagi M, Honda K, Gatanaga H, Oka S, et al. Control of HIV-1 by an HLA-B∗52:01-C∗12:02 protective haplotype . J Infect Dis 2017; 216:1415–1424.
Ammaranond P, van Bockel DJ, Petoumenos K, McMurchie M, Finlayson R, Middleton MG, et al. HIV immune escape at an immunodominant epitope in HLA-B∗27-positive individuals predicts viral load outcome . J Immunol 2011; 186:479–488.
Feeney ME, Tang Y, Roosevelt KA, Leslie AJ, McIntosh K, Karthas N, et al. Immune escape precedes breakthrough human immunodeficiency virus type 1 viremia and broadening of the cytotoxic T-lymphocyte response in an HLA-B27-positive long-term-nonprogressing child . J Virol 2004; 78:8927–8930.
Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M, et al. HIV evolution: CTL escape mutation and reversion after transmission . Nat Med 2004; 10:282–289.
Murakoshi H, Koyanagi M, Chikata T, Rahman MA, Kuse N, Sakai K, et al. Accumulation of Pol mutations selected by HLA-B∗52:01-C∗12:02 protective haplotype-restricted cytotoxic T lymphocytes causes low plasma viral load due to low viral fitness of mutant viruses . J Virol 2017; 91:e02082-16.
Huang J, Goedert JJ, Sundberg EJ, Cung TD, Burke PS, Martin MP, et al. HLA-B∗35-Px-mediated acceleration of HIV-1 infection by increased inhibitory immunoregulatory impulses . J Exp Med 2009; 206:2959–2966.
Matthews PC, Koyanagi M, Kloverpris HN, Harndahl M, Stryhn A, Akahoshi T, et al. Differential clade-specific HLA-B∗3501 association with HIV-1 disease outcome is linked to immunogenicity of a single Gag epitope . J Virol 2012; 86:12643–12654.
Murakoshi H, Koyanagi M, Akahoshi T, Chikata T, Kuse N, Gatanaga H, et al. Impact of a single HLA-A∗24:02-associated escape mutation on the detrimental effect of HLA-B∗35:01 in HIV-1 control . EBioMedicine 2018; 36:103–112.
Honda K, Zheng N, Murakoshi H, Hashimoto M, Sakai K, Borghan MA, et al. Selection of escape mutant by HLA-C-restricted HIV-1 Pol-specific cytotoxic T lymphocytes carrying strong ability to suppress HIV-1 replication . Eur J Immunol 2011; 41:97–106.
Yagita Y, Kuse N, Kuroki K, Gatanaga H, Carlson JM, Chikata T, et al. Distinct HIV-1 escape patterns selected by cytotoxic T cells with identical epitope specificity . J Virol 2013; 87:2253–2263.
Murakoshi H, Kuse N, Akahoshi T, Zhang Y, Chikata T, Borghan MA, et al. Broad recognition of circulating HIV-1 by HIV-1-specific cytotoxic T-lymphocytes with strong ability to suppress HIV-1 replication . J Virol 2019; 93:e01480-18.
Sato H, Tomita Y, Ebisawa K, Hachiya A, Shibamura K, Shiino T, et al. Augmentation of human immunodeficiency virus type 1 subtype E (CRF01_AE) multiple-drug resistance by insertion of a foreign 11-amino-acid fragment into the reverse transcriptase . J Virol 2001; 75:5604–5613.
Chikata T, Paes W, Akahoshi T, Partridge T, Murakoshi H, Gatanaga H, et al. Identification of immunodominant HIV-1 epitopes presented by HLA-C∗12:02, a protective allele, using an immunopeptidomics approach . J Virol 2019; 93:e00634-19.
Lin Z, Kuroki K, Kuse N, Sun X, Akahoshi T, Qi Y, et al. HIV-1 control by NK cells via reduced interaction between KIR2DL2 and HLA-C∗12:02/C∗14:03 . Cell Rep 2016; 17:2210–2220.
Van Tran G, Chikata T, Carlson JM, Murakoshi H, Nguyen DH, Tamura Y, et al. A strong association of human leukocyte antigen-associated Pol and Gag mutations with clinical parameters in HIV-1 subtype A/E infection . AIDS 2016; 30:681–689.
Neefjes JJ, Ploegh HL. Allele and locus-specific differences in cell surface expression and the association of HLA class I heavy chain with beta 2-microglobulin: differential effects of inhibition of glycosylation on class I subunit association . Eur J Immunol 1988; 18:801–810.
Snary D, Barnstable CJ, Bodmer WF, Crumpton MJ. Molecular structure of human histocompatibility antigens: the HLA-C series . Eur J Immunol 1977; 7:580–585.
Apps R, Meng Z, Del Prete GQ, Lifson JD, Zhou M, Carrington M. Relative expression levels of the HLA class-I proteins in normal and HIV-infected cells . J Immunol 2015; 194:3594–3600.
Apps R, Qi Y, Carlson JM, Chen H, Gao X, Thomas R, et al. Influence of HLA-C expression level on HIV control . Science 2013; 340:87–91.
Apps R, Del Prete GQ, Chatterjee P, Lara A, Brumme ZL, Brockman MA, et al. HIV-1 Vpu mediates HLA-C downregulation . Cell Host Microbe 2016; 19:686–695.