HIV-1 adaptation to NK cell-mediated immune pressure

PLoS Pathogens

Volumn 13, Issue 6, 2017, Pages

  Elemans, Marjet ^a   Boelen, Lies ^a   Rasmussen, Michael ^b   Buus, Søren ^b   Asquith, Becca ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA C ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; NEF PROTEIN; TRANSACTIVATOR PROTEIN; VIRUS ENVELOPE PROTEIN; VPU PROTEIN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR;

ADAPTATION; ARTICLE; CELL SELECTION; CONTROLLED STUDY; DNA POLYMORPHISM; GENE FREQUENCY; HUMAN IMMUNODEFICIENCY VIRUS 1; LIQUID SCINTILLATION COUNTING; MATHEMATICAL MODEL; NATURAL KILLER CELL; NONHUMAN; POPULATION DYNAMICS; PREDICTION; PROTEIN BINDING; PROTEIN PROCESSING; T LYMPHOCYTE; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHYSIOLOGY; VIROLOGY;

HIV INFECTIONS; HIV-1; HLA-C ANTIGENS; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; RECEPTORS, KIR;

EID: 85021832953     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006361     Document Type: Article

References (52)

1. Vilches C, Parham P, KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annual review of immunology. 2002;20:217–51. 11861603. doi: 10.1146/annurev.immunol.20.092501.134942
2. Malnati MS, Peruzzi M, Parker KC, Biddison WE, Ciccone E, Moretta A, et al. Peptide specificity in the recognition of MHC class I by natural killer cell clones. Science New York, NY. 1995;267(5200):1016–8. Epub 1995/02/17. 7863326.
3. Peruzzi M, Parker KC, Long EO, Malnati MS, Peptide sequence requirements for the recognition of HLA-B*2705 by specific natural killer cells. J Immunol. 1996;157(8):3350–6. 8871631.
4. Rajagopalan S, Long EO, The direct binding of a p58 killer cell inhibitory receptor to human histocompatibility leukocyte antigen (HLA)-Cw4 exhibits peptide selectivity. The Journal of experimental medicine. 1997;185(8):1523–8. Epub 1997/04/21. 9126935;
5. Boyington JC, Motyka SA, Schuck P, Brooks AG, Sun PD, Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature. 2000;405(6786):537–43. Epub 2000/06/13. doi: 10.1038/35014520 10850706.
6. Fadda L, Borhis G, Ahmed P, Cheent K, Pageon SV, Cazaly A, et al. Peptide antagonism as a mechanism for NK cell activation. Proc Natl Acad Sci U S A. 2010;107(22):10160–5. 20439706. doi: 10.1073/pnas.0913745107
7. Fadda L, O'Connor GM, Kumar S, Piechocka-Troch A, Gardiner CM, Carrington M, et al. Common HIV-1 Peptide Variants Mediate Differential Binding of KIR3DL1 to HLA-Bw4 Molecules. Journal of Virology. 2011;85(12):5970–4. doi: 10.1128/JVI.00412-11 21471246
8. Van Teijlingen NH, HÖLzemer A, Rner CK, GarcÍA-BeltrÁN WF, Schafer J, Fadda L, et al. Sequence variations in HIV-1 p24 Gag-derived epitopes can alter binding of KIR2DL2 to HLA- C*03:04 and modulate primary NK cell function. AIDS (London, England). 2014;28(10):1399–408. doi: 10.1097/QAD.0000000000000284 24785948
9. Matusali G, Potesta M, Santoni A, Cerboni C, Doria M, The human immunodeficiency virus type 1 Nef and Vpu proteins downregulate the natural killer cell-activating ligand PVR. J Virol. 2012;86(8):4496–504. doi: 10.1128/JVI.05788-11 22301152;
10. Cerboni C, Neri F, Casartelli N, Zingoni A, Cosman D, Rossi P, et al. Human immunodeficiency virus 1 Nef protein downmodulates the ligands of the activating receptor NKG2D and inhibits natural killer cell-mediated cytotoxicity. J Gen Virol. 2007;88(Pt 1):242–50. doi: 10.1099/vir.0.82125-0 17170457.
11. Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, Strominger JL, et al. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity. 1999;10(6):661–71. 10403641.
12. Matusali G, Tchidjou HK, Pontrelli G, Bernardi S, D'Ettorre G, Vullo V, et al. Soluble ligands for the NKG2D receptor are released during HIV-1 infection and impair NKG2D expression and cytotoxicity of NK cells. FASEB J. 2013;27(6):2440–50. doi: 10.1096/fj.12-223057 23395909.
13. Martin MP, Gao X, Lee J-H, Nelson GW, Detels R, Goedert JJ, et al. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nature genetics. 2002;31(4):429–34. doi: 10.1038/ng934 12134147
14. Pelak K, Need AC, Fellay J, Shianna KV, Feng S, Urban TJ, et al. Copy number variation of KIR genes influences HIV-1 control. PLoS biology. 2011;9(11):e1001208. 22140359. doi: 10.1371/journal.pbio.1001208
15. Martin MP, Qi Y, Gao X, Yamada E, Martin JN, Pereyra F, et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nature genetics. 2007;39(6):733–40. 17496894. doi: 10.1038/ng2035
16. Boulet S, Sharafi S, Simic N, Bruneau J, Routy JP, Tsoukas CM, et al. Increased proportion of KIR3DS1 homozygotes in HIV-exposed uninfected individuals. AIDS. 2008;22(5):595–9. doi: 10.1097/QAD.0b013e3282f56b23 18317000.
17. Boulet S, Kleyman M, Kim JY, Kamya P, Sharafi S, Simic N, et al. A combined genotype of KIR3DL1 high expressing alleles and HLA-B*57 is associated with a reduced risk of HIV infection. AIDS. 2008;22(12):1487–91. doi: 10.1097/QAD.0b013e3282ffde7e 18614872.
18. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, et al. Immune-Correlates Analysis of an HIV-1 Vaccine Efficacy Trial. New England Journal of Medicine. 2012;366(14):1275–86. doi: 10.1056/NEJMoa1113425 22475592.
19. Alter G, Heckerman D, Schneidewind A, Fadda L, Kadie CM, Carlson JM, et al. HIV-1 adaptation to NK-cell-mediated immune pressure. Nature. 2011;476(7358):96–100. 21814282. doi: 10.1038/nature10237
20. Jost S, Altfeld M, Control of Human Viral Infections by Natural Killer Cells. Annual review of immunology. 2013;31(1):163–94. doi: 10.1146/annurev-immunol-032712-100001 23298212.
21. Jost S, Altfeld M, Evasion from NK cell-mediated immune responses by HIV-1. Microbes Infect. 2012;14(11):904–15. doi: 10.1016/j.micinf.2012.05.001 22626930;
22. Holzemer A, Thobakgale CF, Jimenez Cruz CA, Garcia-Beltran WF, Carlson JM, van Teijlingen NH, et al. Selection of an HLA-C*03:04-Restricted HIV-1 p24 Gag Sequence Variant Is Associated with Viral Escape from KIR2DL3+ Natural Killer Cells: Data from an Observational Cohort in South Africa. PLoS Med. 2015;12(11):e1001900; discussion e. doi: 10.1371/journal.pmed.1001900 26575988;
23. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, Nowak MA, et al. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nature medicine. 1997;3(2):212–7. 9018241.
24. Phillips RE, Rowland-Jones S, Nixon DF, Gotch FM, Edwards JP, Ogunlesi AO, et al. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature. 1991;354(6353):453–9. 1721107. doi: 10.1038/354453a0
25. Asquith B, Edwards CT, Lipsitch M, McLean AR, Inefficient cytotoxic T lymphocyte-mediated killing of HIV-1-infected cells in vivo. PLoS biology. 2006;4(4):e90. doi: 10.1371/journal.pbio.0040090 16515366;
26. Moesta AK, Norman PJ, Yawata M, Yawata N, Gleimer M, Parham P, Synergistic polymorphism at two positions distal to the ligand-binding site makes KIR2DL2 a stronger receptor for HLA-C than KIR2DL3. J Immunol. 2008;180(6):3969–79. 18322206.
27. Hansasuta P, Dong T, Thananchai H, Weekes M, Willberg C, Aldemir H, et al. Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific. European journal of immunology. 2004;34(6):1673–9. doi: 10.1002/eji.200425089 15162437.
28. Thananchai H, Gillespie G, Martin MP, Bashirova A, Yawata N, Yawata M, et al. Cutting Edge: Allele-specific and peptide-dependent interactions between KIR3DL1 and HLA-A and HLA-B. J Immunol. 2007;178(1):33–7. 17182537.
29. Thananchai H, Makadzange T, Maenaka K, Kuroki K, Peng Y, Conlon C, et al. Reciprocal recognition of an HLA-Cw4-restricted HIV-1 gp120 epitope by CD8+ T cells and NK cells. AIDS. 2009;23(2):189–93. doi: 10.1097/QAD.0b013e32831fb55a 19098488.
30. Maiers M, Gragert L, Klitz W, High-resolution HLA alleles and haplotypes in the United States population (vol 68, pg 779, 2007). Human immunology. 2008;69(2):141-.
31. US Centers for Disease control and Prevention. Diagnoses of HIV Infection in the United States and Dependent Areas, 2000. HIV Surveillance Report. 2000;12.
32. Hoof I, Peters B, Sidney J, Pedersen L, Sette A, Lund O, et al. NetMHCpan, a method for MHC class I binding prediction beyond humans. Immunogenetics. 2009;61(1):1–13. doi: 10.1007/s00251-008-0341-z 19002680
33. Borghans JAM, Mølgaard A, de Boer RJ, Keşmir C, HLA Alleles Associated with Slow Progression to AIDS Truly Prefer to Present HIV-1 p24. PLoS ONE. 2007;2(9):e920–e. doi: 10.1371/journal.pone.0000920 17878955
34. Peters B, Bui H-H, Frankild S, Nielson M, Lundegaard C, Kostem E, et al. A community resource benchmarking predictions of peptide binding to MHC-I molecules. PLoS Comput Biol. 2006;2(6):e65. doi: 10.1371/journal.pcbi.0020065 16789818
35. Rasmussen M, Harndahl M, Stryhn A, Boucherma R, Nielsen LL, Lemonnier FA, et al. Uncovering the peptide-binding specificities of HLA-C: a general strategy to determine the specificity of any MHC class I molecule. J Immunol. 2014;193(10):4790–802. doi: 10.4049/jimmunol.1401689 25311805;
36. Harndahl M, Rasmussen M, Roder G, Buus S, Real-time, high-throughput measurements of peptide-MHC-I dissociation using a scintillation proximity assay. Journal of immunological methods. 2011;374(1–2):5–12. Epub 2010/11/04. doi: 10.1016/j.jim.2010.10.012 21044632;
37. Harndahl M, Rasmussen M, Roder G, Dalgaard Pedersen I, Sorensen M, Nielsen M, et al. Peptide-MHC class I stability is a better predictor than peptide affinity of CTL immunogenicity. European journal of immunology. 2012;42(6):1405–16. Epub 2012/06/09. doi: 10.1002/eji.201141774 22678897.
38. Frater AJ, Brown H, Oxenius A, Gunthard HF, Hirschel B, Robinson N, et al. Effective T Cell Responses Select HIV-1 Mutants and Slow Disease Progression. J Virol. 2007;81(12):6742–51. 17409157. doi: 10.1128/JVI.00022-07
39. Payne RP, Kloverpris H, Sacha JB, Brumme Z, Brumme C, Buus S, et al. Efficacious early antiviral activity of HIV Gag- and Pol-specific HLA-B 2705-restricted CD8+ T cells. J Virol. 2010;84(20):10543–57. Epub 2010/08/06. doi: 10.1128/JVI.00793-10 20686036;
40. Moore CB, John M, James IR, Christiansen FT, Witt CS, Mallal SA, Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science New York, NY. 2002;296(5572):1439–43. 12029127. doi: 10.1126/science.1069660
41. Le Gall S, Stamegna P, Walker BD, Portable flanking sequences modulate CTL epitope processing. The Journal of clinical investigation. 2007;117(11):3563–75. Epub 2007/11/03. doi: 10.1172/JCI32047 17975674;
42. Nielsen M, Lundegaard C, Blicher T, Lamberth K, Harndahl M, Justesen S, et al. NetMHCpan, a Method for Quantitative Predictions of Peptide Binding to Any HLA-A and -B Locus Protein of Known Sequence. PLoS One. 2007;2(8):e796. doi: 10.1371/journal.pone.0000796 17726526
43. Zhang H, Lundegaard C, Nielsen M, Pan-specific MHC class I predictors: a benchmark of HLA class I pan-specific prediction methods. Bioinformatics. 2009;25(1):83–9. doi: 10.1093/bioinformatics/btn579 18996943
44. Hirayasu K, Arase H, Functional and genetic diversity of leukocyte immunoglobulin-like receptor and implication for disease associations. Journal of human genetics. 2015;60(11):703–8. Epub 2015/06/05. doi: 10.1038/jhg.2015.64 26040207.
45. Bashirova AA, Martin-Gayo E, Jones DC, Qi Y, Apps R, Gao X, et al. LILRB2 interaction with HLA class I correlates with control of HIV-1 infection. PLoS Genet. 2014;10(3):e1004196. Epub 2014/03/08. doi: 10.1371/journal.pgen.1004196 24603468;
46. Norman PJ, Cook MA, Carey BS, Carrington CV, Verity DH, Hameed K, et al. SNP haplotypes and allele frequencies show evidence for disruptive and balancing selection in the human leukocyte receptor complex. Immunogenetics. 2004;56(4):225–37. Epub 2004/06/09. doi: 10.1007/s00251-004-0674-1 15185041.
47. Liepe J, Marino F, Sidney J, Jeko A, Bunting DE, Sette A, et al. A large fraction of HLA class I ligands are proteasome-generated spliced peptides. Science. 2016;354(6310):354–8. doi: 10.1126/science.aaf4384 27846572.
48. Apps R, Del Prete Gregory Q, Chatterjee P, Lara A, Brumme Zabrina L, Brockman Mark A, et al. HIV-1 Vpu Mediates HLA-C Downregulation. Cell Host & Microbe. 2016;19(5):686–95. http://doi.org/10.1016/j.chom.2016.04.005.
49. Heckerman D, Kadie C, Listgarten J, Leveraging information across HLA alleles/supertypes improves epitope prediction. J Comput Biol. 2007;14(6):736–46. doi: 10.1089/cmb.2007.R013 17691891
50. US Centers for Disease control and Prevention. Diagnoses of HIV Infection in the United States and Dependent Areas, 2013. HIV Surveillance Report. 2013;25.
51. Fryer HR, Frater J, Duda A, Roberts MG, Phillips RE, McLean AR, Modelling the evolution and spread of HIV immune escape mutants. PLoS Pathog. 2010;6(11):e1001196. doi: 10.1371/journal.ppat.1001196 21124991
52. Hilton HG, Vago L, Older Aguilar AM, Moesta AK, Graef T, Abi-Rached L, et al. Mutation at positively selected positions in the binding site for HLA-C shows that KIR2DL1 is a more refined but less adaptable NK cell receptor than KIR2DL3. J Immunol. 2012;189(3):1418–30. doi: 10.4049/jimmunol.1100431 22772445.