Evidence of HIV-1 adaptation to host HLA alleles following chimp-to-human transmission

Virology Journal

Volumn 6, Issue , 2009, Pages

  Ngandu, Nobubelo K ^a   Seoighe, Cathal ^b   Scheffler, Konrad ^c  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

HLA B ANTIGEN; PEPTIDE; HLA ANTIGEN;

ADAPTATION; AFRICA; ALLELE; ARTICLE; BINDING AFFINITY; CHIMPANZEE; CODON; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; GENE SEQUENCE; HLA SYSTEM; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; PHYLOGENY; PROTEIN TARGETING; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS GENOME; VIRUS TRANSMISSION; ZOONOSIS; ANIMAL; COMPUTER SIMULATION; DNA SEQUENCE; GENETICS; HUMAN; IMMUNOLOGY; PAN TROGLODYTES;

HUMAN IMMUNODEFICIENCY VIRUS 1; PAN;

ADAPTATION, BIOLOGICAL; ALLELES; ANIMALS; CODON; COMPUTER SIMULATION; HIV-1; HLA ANTIGENS; HUMANS; PAN TROGLODYTES; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 70350401181     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-6-164     Document Type: Article

References (54)

1. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. F Gao E Bailes DL Robertson Y Chen CM Rodenburg SF Michael LB Cummins LO Arthur M Peeters GM Shaw PM Sharp BH Hahn, Nature 1999 397 436 441 10.1038/17130 9989410
2. An African HIV-1 sequence from 1959 and implications for the origin of the epidemic. T Zhu BT Korber AJ Nahmias E Hooper PM Sharp DD Ho, Nature 1998 391 594 597 10.1038/35400 9468138
3. Timing the ancestor of the HIV-1 pandemic strains. B Korber M Muldoon J Theiler F Gao R Gupta A Lapedes BH Hahn S Wolinsky T Bhattacharya, Science 2000 288 1789 1796 10.1126/science.288.5472.1789 10846155
4. Origins and evolution of AIDS viruses. P Sharp E Bailes D Robertson F Gao B Hahn, Biol Bull 1999 196 338 342 10.2307/1542965 10390833
5. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. BF Keele JH Jones KA Terio JD Estes RS Rudicell ML Wilson Y Li GH Learn TM Beasley J Schumacher-Stankey E Wroblewski A Mosser J Raphael S Kamenya EV Lonsdorf DA Travis T Mlengeya MJ Kinsel JG Else G Silvestri J Goodall PM Sharp GM Shaw AE Pusey BH Hahn, Nature 2009 460 515 519 10.1038/nature08200 19626114
6. Understanding the benign nature of SIV infection in natural hosts. G Silvestri M Paiardini I Pandrea M Lederman D Sodora, J Clin Invest 2007 117 3148 3154 10.1172/JCI33034 17975656
7. Simian immunodeficiency virus SIVagm dynamics in African green monkeys. I Pandrea RM Ribeiro R Gautam T Gaufin M Pattison M Barnes C Monjure C Stoulig J Dufour W Cyprian G Silvestri MD Miller AS Perelson C Apetrei, J Virol 2008 82 3713 3724 10.1128/JVI.02402-07 18216122
8. Immunity in natural SIV infections. G Silvestri, Journal of INTERNAL MEDICINE 2008 10 1365 2796
9. Cytotoxic-T-cell responses, viral load, and disease progression in early human immunodeficiency virus type 1 infection. L Musey J Hughes T Schacker T Shea L Corey MJ McElrath, N Engl J Med 1997 337 1267 1274 10.1056/ NEJM199710303371803 9345075
10. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. P Lemey SL Kosakovsky Pond AJ Drummond OG Pybus B Shapiro H Barroso N Taveira A Rambaut, PLoS Comput Biol 2007 3 29 10.1371/journal.pcbi.0030029 17305421
11. Viral load and disease progression in infants infected with human immunodeficiency virus type 1. Women and Infants Transmission Study Group. WT Shearer TC Quinn P LaRussa JF Lew L Mofenson S Almy K Rich E Handelsman C Diaz M Pagano V Smeriglio LA Kalish, N Engl J Med 1997 336 1337 1342 10.1056/NEJM199705083361901 9134873
12. Human immunodeficiency virus type 1 mRNA expression in peripheral blood cells predicts disease progression independently of the numbers of CD4+ lymphocytes. K Saksela C Stevens P Rubinstein D Baltimore, Proc Natl Acad Sci USA 1994 91 1104 1108 10.1073/pnas.91.3.1104 7905630
13. Human immunodeficiency virus type 1 cellular RNA load and splicing patterns predict disease progression in a longitudinally studied cohort. NL Michael T Mo A Merzouki M O'Shaughnessy C Oster DS Burke RR Redfield DL Birx SA Cassol, J Virol 1995 69 1868 1877 7853528
14. Episodic evolution mediates interspecies transfer of a murine coronavirus. RS Baric B Yount L Hensley SA Peel W Chen, J Virol 1997 71 1946 1955 9032326
15. Adaptation of HIV-1 to its human host. LV Wain E Bailes F Bibollet-Ruche JM Decker BF Keele F Van Heuverswyn Y Li J Takehisa EM Ngole GM Shaw M Peeters BH Hahn PM Sharp, Mol Biol Evol 2007 24 1853 1860 10.1093/molbev/msm110 17545188
16. Positive selection on HIV accessory proteins and the analysis of molecular adaptation after interspecies transmission. AE Soares MA Soares CG Schrago, J Mol Evol 2008 66 598 604 10.1007/s00239-008-9112-6 18465165
17. Comparative study of adaptive molecular evolution in different human immunodeficiency virus groups and subtypes. M Choisy CH Woelk JF Guegan DL Robertson, J Virol 2004 78 1962 1970 10.1128/JVI.78.4.1962-1970.2004 14747561
18. The integration hypothesis: an evolutionary pathway to benign SIV infection. V Muller RJ De Boer, PLoS Pathog 2006 2 15 10.1371/journal.ppat. 0020015 16609728
19. The quality of chimpanzee T-cell activation and simian immunodeficiency virus/human immunodeficiency virus susceptibility achieved via antibody-mediated T-cell receptor/CD3 stimulation is a function of the anti-CD3 antibody isotype. F Bibollet-Ruche BA McKinney A Duverger FH Wagner AA Ansari O Kutsch, J Virol 2008 82 10271 10278 10.1128/JVI.01319-08 18667496
20. Lentivirus infections and mechanisms of disease resistance in chimpanzees. E Rutjens S Balla-Jhagjhoorsingh E Verschoor W Bogers G Koopman J Heeney, Front Biosci 2003 8 1134 d1145 10.2741/1125 12957818
21. The three-dimensional structure of HLA-B27 at 2.1 A resolution suggests a general mechanism for tight peptide binding to MHC. DR Madden JC Gorga JL Strominger DC Wiley, Cell 1992 70 1035 1048 10.1016/0092-8674(92)90252-8 1525820
22. MHC ligands and peptide motifs: first listing. H Rammensee T Friede S Stevanoviic, Immunogenetics 1995 41 178 228 10.1007/BF00172063 7890324
23. Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. MA Saper PJ Bjorkman DC Wiley, J Mol Biol 1991 219 277 319 10.1016/0022-2836(91)90567-P 2038058
24. How cytotoxic T cells manage to discriminate nonself from self at the nonapeptide level. S Ohno, Proc Natl Acad Sci USA 1992 89 4643 4647 10.1073/pnas.89.10.4643 1374910
25. Endogenous peptides with distinct amino acid anchor residue motifs bind to HLA-A1 and HLA-B8. M DiBrino KC Parker J Shiloach RV Turner T Tsuchida M Garfield WE Biddison JE Coligan, J Immunol 1994 152 620 631 7506728
26. The importance of secondary anchor residue motifs of HLA class I proteins: a chemometric approach. P Rovero D Riganelli D Fruci S Vigano S Pegoraro R Revoltella G Greco R Butler S Clementi N Tanigaki, Mol Immunol 1994 31 549 554 10.1016/0161-5890(94)90042-6 8190130
27. The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. A Sette A Vitiello B Reherman P Fowler R Nayersina WM Kast CJ Melief C Oseroff L Yuan J Ruppert J Sidney MF del Guercio S Southwood RT Kubo RW Chesnut HM Grey FV Chisari, J Immunol 1994 153 5586 5592 7527444
28. The influence of HLA genotype on AIDS. M Carrington SJ O'Brien, Annu Rev Med 2003 54 535 551 10.1146/annurev.med.54.101601.152346 12525683
29. New class I and II HLA alleles strongly associated with opposite patterns of progression to AIDS. H Hendel S Caillat-Zucman H Lebuanec M Carrington S O'Brien JM Andrieu F Schachter D Zagury J Rappaport C Winkler GW Nelson JF Zagury, J Immunol 1999 162 6942 6946 10352317
30. Control of human immunodeficiency virus replication by cytotoxic T lymphocytes targeting subdominant epitopes. N Frahm P Kiepiela S Adams CH Linde HS Hewitt K Sango ME Feeney MM Addo M Lichterfeld MP Lahaie E Pae AG Wurcel T Roach MA St John M Altfeld FM Marincola C Moore S Mallal M Carrington D Heckerman TM Allen JI Mullins BT Korber PJ Goulder BD Walker C Brander, Nat Immunol 2006 7 173 178 10.1038/ni1281 16369537 (Pubitemid 43135883)
31. Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple gag-specific CD8+ T-cell epitopes. I Honeyborne A Prendergast F Pereyra A Leslie H Crawford R Payne S Reddy K Bishop E Moodley K Nair SM van der N McCarthy CM Rousseau M Addo JI Mullins C Brander P Kiepiela BD Walker PJ Goulder, J Virol 2007 81 3667 3672 10.1128/JVI.02689-06 17251285
32. Frequent toggling between alternative amino acids is driven by selection in HIV-1. W Delport K Scheffler C Seoighe, PLoS Pathog 2008 4 1000242 10.1371/journal.ppat.1000242 19096508
33. HIV Sequence Compendium. T Leitner B Foley B Hahn P Marx F McCutchan J Mellors S Wolinsky B Korber, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, NM, LA-UR 2005 06-0680
34. Extensive purifying selection acting on synonymous sites in HIV-1 Group M sequences. NK Ngandu K Scheffler P Moore Z Woodman D Martin C Seoighe, Virol J 2008 5 160 10.1186/1743-422X-5-160 19105834
35. HyPhy: hypothesis testing using phylogenies. SL Kosakovsky Pond SD Frost SV Muse, Bioinformatics 2005 21 676 679 10.1093/bioinformatics/bti079 15509596
36. A structure-based approach for prediction of MHC-binding peptides. Y Altuvia H Margalit, Methods 2004 34 454 459 10.1016/j.ymeth.2004.06.008 15542371
37. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. R Nielsen Z Yang, Genetics 1998 148 929 936 9539414
38. A genetic algorithm approach to detecting lineage-specific variation in selection pressure. SL Kosakovsky Pond SD Frost, Mol Biol Evol 2005 22 478 485 10.1093/molbev/msi031 15509724
39. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Z Yang, Mol Biol Evol 1998 15 568 573 9580986
40. Association of HLA types A1-B8-DR3 and B27 with rapid and slow progression of HIV disease. AJ McNeil PL Yap SM Gore RP Brettle M McColl R Wyld S Davidson R Weightman AM Richardson JR Robertson, QJM 1996 89 177 185 8731561
41. Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration. HA Ross AG Rodrigo, J Virol 2002 76 11715 11720 10.1128/JVI.76.22.11715-11720.2002 12388731
42. The HLA Facts Book. S Marsh P Parham L Barber, Academic Press 2000 1
43. Lack of strong immune selection pressure by the immunodominant, HLA-A*0201-restricted cytotoxic T lymphocyte response in chronic human immunodeficiency virus-1 infection. C Brander KE Hartman AK Trocha NG Jones RP Johnson B Korber P Wentworth SP Buchbinder S Wolinsky BD Walker SA Kalams, J Clin Invest 1998 101 2559 2566 10.1172/JCI2405 9616227
44. Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. F Pereyra MM Addo DE Kaufmann Y Liu T Miura A Rathod B Baker A Trocha R Rosenberg E Mackey P Ueda Z Lu D Cohen T Wrin CJ Petropoulos ES Rosenberg BD Walker, J Infect Dis 2008 197 563 571 10.1086/526786 18275276
45. HLA alleles associated with slow progression to AIDS truly prefer to present HIV-1 p24. JA Borghans A Molgaard RJ De Boer C Kesmir, PLoS ONE 2007 2 920 10.1371/journal.pone.0000920 17878955
46. Frequency of HLA allele-specific peptide motifs in HIV-1 proteins correlates with the allele's association with relative rates of disease progression after HIV-1 infection. GW Nelson R Kaslow DL Mann, Proc Natl Acad Sci USA 1997 94 9802 9807 10.1073/pnas.94.18.9802 9275206
47. Role of cytotoxic T-lymphocyte-mediated immune selection in a dominant human leukocyte antigen-B8-restricted cytotoxic T-lymphocyte epitope in Nef. K Maurer EG Harrer A Goldwich K Eismann S Bergmann M Schmitt-Haendle B Spriewald SM Mueller T Harrer, J Acquir Immune Defic Syndr 2008 48 133 141 10.1097/QAI.0b013e31816fdc4a 18391752
48. HLA-B57/B*5801 HIV-1 Elite Controllers Select for Rare Gag Variants Associated with Reduced Viral Replication Capacity and Strong CTL Recognition. T Miura MA Brockman A Schneidewind M Lobritz F Pereyra A Rathod BL Block ZL Brumme CJ Brumme B Baker AC Rothchild B Li A Trocha E Cutrell N Frahm C Brander I Toth EJ Arts TM Allen BD Walker, J Virol 2008 10 2265 2308
49. Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. A Sette J Sidney, Immunogenetics 1999 50 201 212 10.1007/s002510050594 10602880
50. Human immunodeficiency virus type 1 Rev- and Tat-specific cytotoxic T lymphocyte frequencies inversely correlate with rapid progression to AIDS. CA van Baalen O Pontesilli RC Huisman AM Geretti MR Klein F de Wolf F Miedema RA Gruters AD Osterhaus, J Gen Virol 1997 78 Pt 8 1913 1918 9266987
51. Evolution of CD8+ T cell immunity and viral escape following acute HIV-1 infection. J Cao J McNevin U Malhotra MJ McElrath, J Immunol 2003 171 3837 3846 14500685
52. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. TM Allen DH O'Connor P Jing JL Dzuris BR Mothe TU Vogel E Dunphy ME Liebl C Emerson N Wilson KJ Kunstman X Wang DB Allison AL Hughes RC Desrosiers JD Altman SM Wolinsky A Sette DI Watkins, Nature 2000 407 386 390 10.1038/35036559 11014195
53. Advantage of rare HLA supertype in HIV disease progression. E Trachtenberg B Korber C Sollars TB Kepler PT Hraber E Hayes R Funkhouser M Fugate J Theiler YS Hsu K Kunstman S Wu J Phair H Erlich S Wolinsky, Nat Med 2003 9 928 935 10.1038/nm893 12819779
54. Balancing selection and heterogeneity across the classical human leukocyte antigen loci: a meta-analytic review of 497 population studies. OD Solberg SJ Mack AK Lancaster RM Single Y Tsai A Sanchez-Mazas G Thomson, Hum Immunol 2008 69 443 464 10.1016/j.humimm.2008.05.001 18638659