Whole genome deep sequencing of HIV-1 reveals the impact of early minor variants upon immune recognition during acute infection

PLoS Pathogens

Volumn 8, Issue 3, 2012, Pages

  Henn, Matthew R ^a   Boutwell, Christian L ^b   Charlebois, Patrick ^a   Lennon, Niall J ^a   Power, Karen A ^b   Macalalad, Alexander R ^a   Berlin, Aaron M ^a   Malboeuf, Christine M ^a   Ryan, Elizabeth M ^a   Gnerre, Sante ^a   Zody, Michael C ^a   Erlich, Rachel L ^a   Green, Lisa M ^a   Berical, Andrew ^b   Wang, Yaoyu ^b   Casali, Monica ^a   Streeck, Hendrik ^b   Bloom, Allyson K ^b   Dudek, Tim ^b   Tully, Damien ^b   Newman, Ruchi ^a   Axten, Karen L ^b   Gladden, Adrianne D ^b   Battis, Laura ^b   Kemper, Michael ^b   Zeng, Qiandong ^a   Shea, Terrance P ^a   Gujja, Sharvari ^a   Zedlack, Carmen ^c   Gasser, Olivier ^d   Brander, Christian ^e,f   Hess, Christoph ^d   Günthard, Huldrych F ^g   Brumme, Zabrina L ^b   Brumme, Chanson J ^b   Bazner, Suzane ^h   Rychert, Jenna ^h   Tinsley, Jake P ⁱ   Mayer, Ken H ⁱ   Rosenberg, Eric ^h   Pereyra, Florencia ^b   Levin, Joshua Z ^a   Young, Sarah K ^a   Jessen, Heiko ^c   Altfeld, Marcus ^b   Birren, Bruce W ^a   Walker, Bruce D ^b,j   Allen, Todd M ^b   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HIV Clinic Praxis Jessen   (Germany)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^g UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^h MASSACHUSETTS GENERAL HOSPITAL   (United States)

ⁱ FENWAY INSTITUTE   (United States)

^j HOWARD HUGHES MEDICAL INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; VIRUS RNA; VIRUS VACCINE;

ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; ENZYME LINKED IMMUNOSPOT ASSAY; HIGH THROUGHPUT SEQUENCING; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; NONHUMAN; PYROSEQUENCING; VIREMIA; VIRUS CELL INTERACTION; VIRUS DETECTION; VIRUS LOAD; VIRUS MUTATION; VIRUS REPLICATION; DNA MICROARRAY; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE EVASION; IMMUNOLOGY; PATHOGENICITY; SEQUENCE ANALYSIS; VIROLOGY; VIRUS GENOME;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CD8-POSITIVE T-LYMPHOCYTES; GENETIC VARIATION; GENOME, VIRAL; GENOME-WIDE ASSOCIATION STUDY; GENOMIC STRUCTURAL VARIATION; HIV INFECTIONS; HIV-1; HUMANS; IMMUNE EVASION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, VIRAL; SEQUENCE ANALYSIS, RNA; VIRAL VACCINES;

EID: 84861214061     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002529     Document Type: Article

References (65)

1. Allen TM, O'Connor DH, Jing P, Dzuris JL, Mothe BR, et al. (2000) Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407: 386-390.
2. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, et al. (1997) Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 3: 212-217.
3. Timm J, Lauer GM, Kavanagh DG, Sheridan I, Kim AY, et al. (2004) CD8 epitope escape and reversion in acute HCV infection. J Exp Med 200: 1593-1604.
4. Kwiatkowski D, Marsh K, (1997) Development of a malaria vaccine. Lancet 350: 1696-1701.
5. Allen TM, Altfeld M, Geer SC, Kalife ET, Moore C, et al. (2005) Selective escape from CD8+ T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J Virol 79: 13239-13249.
6. Price DA, Goulder PJ, Klenerman P, Sewell AK, Easterbrook PJ, et al. (1997) Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci U S A 94: 1890-1895.
7. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, et al. (2009) The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 206: 1253-1272.
8. Borrow P, Lewicki H, Wei XP, Horwitz MS, Peffer N, et al. (1997) Antiviral pressure exerted By HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 3: 205-211.
9. Richman DD, Wrin T, Little SJ, Petropoulos CJ, (2003) Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci U S A 100: 4144-4149.
10. Schneidewind A, Brockman MA, Yang R, Adam RI, Li B, et al. (2007) Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J Virol 81: 12382-12393.
11. Martinez-Picado J, Prado JG, Fry EE, Pfafferott K, Leslie A, et al. (2006) Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J Virol 80: 3617-3623.
12. Troyer RM, McNevin J, Liu Y, Zhang SC, Krizan RW, et al. (2009) Variable fitness impact of HIV-1 escape mutations to cytotoxic T lymphocyte (CTL) response. PLoS Pathog 5: e1000365.
13. Miura T, Brockman MA, Schneidewind A, Lobritz M, Pereyra F, et al. (2009) HLA-B57/B*5801 human immunodeficiency virus type 1 elite controllers select for rare gag variants associated with reduced viral replication capacity and strong cytotoxic T-lymphocyte [corrected] recognition. J Virol 83: 2743-2755.
14. Liu Y, McNevin J, Cao J, Zhao H, Genowati I, et al. (2006) Selection on the human immunodeficiency virus type 1 proteome following primary infection. J Virol 80: 9519-9529.
15. Palmer S, Kearney M, Maldarelli F, Halvas EK, Bixby CJ, et al. (2005) Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J Clin Microbiol 43: 406-413.
16. Salazar-Gonzalez JF, Bailes E, Pham KT, Salazar MG, Guffey MB, et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J Virol 82: 3952-3970.
17. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
18. Simen BB, Simons JF, Hullsiek KH, Novak RM, Macarthur RD, et al. (2009) Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J Infect Dis 199: 693-701.
19. Poon AF, Swenson LC, Dong WW, Deng W, Kosakovsky Pond SL, et al. (2010) Phylogenetic analysis of population-based and deep sequencing data to identify coevolving sites in the nef gene of HIV-1. Mol Biol Evol 27: 819-832.
20. Wang C, Mitsuya Y, Gharizadeh B, Ronaghi M, Shafer RW, (2007) Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance. Genome Res 17: 1195-1201.
21. Hedskog C, Mild M, Jernberg J, Sherwood E, Bratt G, et al. (2010) Dynamics of HIV-1 quasispecies during antiviral treatment dissected using ultra-deep pyrosequencing. PLoS One 5: e11345.
22. Tsibris AM, Korber B, Arnaout R, Russ C, Lo CC, et al. (2009) Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo. PLoS One 4: e5683.
23. Bimber BN, Burwitz BJ, O'Connor S, Detmer A, Gostick E, et al. (2009) Ultradeep pyrosequencing detects complex patterns of CD8+ T-lymphocyte escape in simian immunodeficiency virus-infected macaques. J Virol 83: 8247-8253.
24. Love TM, Thurston SW, Keefer MC, Dewhurst S, Lee HY, (2010) Mathematical Modeling of Ultradeep Sequencing Data Reveals That Acute CD8+ T-Lymphocyte Responses Exert Strong Selective Pressure in Simian Immunodeficiency Virus-Infected Macaques, but Still Fail to Clear Founder Epitope Sequences. J Virol 84: 5802-5814.
25. Bimber BN, Dudley DM, Lauck M, Becker EA, Chin EN, et al. (2010) Whole genome characterization of HIV/SIV intra-host diversity by ultra-deep pyrosequencing. J Virol 84: 12087-92.
26. Fischer W, Ganusov VV, Giorgi EE, Hraber PT, Keele BF, et al. (2010) Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One 5: e12303.
27. Mitsuya Y, Varghese V, Wang C, Liu TF, Holmes SP, et al. (2008) Minority human immunodeficiency virus type 1 variants in antiretroviral-naive persons with reverse transcriptase codon 215 revertant mutations. J Virol 82: 10747-10755.
28. Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, et al. (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407: 513-516.
29. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, et al. (2003) Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. Aids 17: 1871-1879.
30. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7557.
31. Gottlieb GS, Heath L, Nickle DC, Wong KG, Leach SE, et al. (2008) HIV-1 variation before seroconversion in men who have sex with men: analysis of acute/early HIV infection in the multicenter AIDS cohort study. J Infect Dis 197: 1011-1015.
32. Abrahams MR, Anderson JA, Giorgi EE, Seoighe C, Mlisana K, et al. (2009) Quantitating the multiplicity of infection with human immunodeficiency virus type 1 subtype C reveals a non-poisson distribution of transmitted variants. J Virol 83: 3556-3567.
33. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, et al. (2009) Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog 5: e1000274.
34. Liu Y, McNevin JP, Holte S, McElrath MJ, Mullins JI, (2011) Dynamics of viral evolution and CTL responses in HIV-1 infection. PLoS One 6: e15639.
35. Allen TM, Altfeld M, Yu XG, O'Sullivan KM, Lichterfeld M, et al. (2004) Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J Virol 78: 7069-7078.
36. Zimbwa P, Milicic A, Frater J, Scriba TJ, Willis A, et al. (2006) Precise Identification Of An Hiv-1 Antigen Processing Mutant. J Virol 81: 2031-2038.
37. Allen TM, Yu XG, Kalife ET, Reyor LL, Lichterfeld M, et al. (2005) De novo generation of escape variant-specific CD8+ T-cell responses following cytotoxic T-lymphocyte escape in chronic human immunodeficiency virus type 1 infection. J Virol 79: 12952-12960.
38. Streeck H, Li B, Poon AF, Schneidewind A, Gladden AD, et al. (2008) Immune-driven recombination and loss of control after HIV superinfection. J Exp Med 205: 1789-1796.
39. Feeney ME, Tang Y, Pfafferott K, Roosevelt KA, Draenert R, et al. (2005) HIV-1 viral escape in infancy followed by emergence of a variant-specific CTL response. J Immunol 174: 7524-7530.
40. Turnbull EL, Lopes AR, Jones NA, Cornforth D, Newton P, et al. (2006) HIV-1 epitope-specific CD8+ T cell responses strongly associated with delayed disease progression cross-recognize epitope variants efficiently. J Immunol 176: 6130-6146.
41. Brumme ZL, John M, Carlson JM, Brumme CJ, Chan D, et al. (2009) HLA-associated immune escape pathways in HIV-1 subtype B Gag, Pol and Nef proteins. PLoS One 4: e6687.
42. Kawashima Y, Pfafferott K, Frater J, Matthews P, Payne R, et al. (2009) Adaptation of HIV-1 to human leukocyte antigen class I. Nature 458: 641-645.
43. Altfeld M, Allen TM, Kalife ET, Frahm N, Addo MM, et al. (2005) The majority of currently circulating human immunodeficiency virus type 1 clade B viruses fail to prime cytotoxic T-lymphocyte responses against an otherwise immunodominant HLA-A2-restricted epitope: implications for vaccine design. J Virol 79: 5000-5005.
44. Streeck H, Jolin JS, Qi Y, Yassine-Diab B, Johnson RC, et al. (2009) Human immunodeficiency virus type 1-specific CD8+ T-cell responses during primary infection are major determinants of the viral set point and loss of CD4+ T cells. J Virol 83: 7641-7648.
45. Altfeld M, Kalife ET, Qi Y, Streeck H, Lichterfeld M, et al. (2006) HLA Alleles Associated with Delayed Progression to AIDS Contribute Strongly to the Initial CD8(+) T Cell Response against HIV-1. PLoS Med 3: e403.
46. Ferrari G, Korber B, Goonetilleke N, Liu MK, Turnbull EL, et al. (2011) Relationship between functional profile of HIV-1 specific CD8 T cells and epitope variability with the selection of escape mutants in acute HIV-1 infection. PLoS Pathog 7: e1001273.
47. Mellors J, Rinaldo C, Gupta P, White R, Todd mJ, et al. (1996) Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272: 1167-1170.
48. Friedrich TC, McDermott AB, Reynolds MR, Piaskowski S, Fuenger S, et al. (2004) Consequences of cytotoxic T-lymphocyte escape: common escape mutations in simian immunodeficiency virus are poorly recognized in naive hosts. J Virol 78: 10064-10073.
49. Bennett MS, Ng HL, Ali A, Yang OO, (2008) Cross-clade detection of HIV-1-specific cytotoxic T lymphocytes does not reflect cross-clade antiviral activity. J Infect Dis 197: 390-397.
50. Santra S, Liao HX, Zhang R, Muldoon M, Watson S, et al. (2010) Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat Med 16: 324-328.
51. Fischer W, Perkins S, Theiler J, Bhattacharya T, Yusim K, et al. (2007) Polyvalent vaccines for optimal coverage of potential T-cell epitopes in global HIV-1 variants. Nat Med 13: 100-106.
52. Brockman MA, Schneidewind A, Lahaie M, Schmidt A, Miura T, et al. (2007) Escape and compensation from early HLA-B57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J Virol 81: 12608-12618.
53. Carlson JM, Brumme ZL, Rousseau CM, Brumme CJ, Matthews P, et al. (2008) Phylogenetic dependency networks: inferring patterns of CTL escape and codon covariation in HIV-1 Gag. PLoS Comput Biol 4: e1000225.
54. Schneidewind A, Brockman MA, Sidney J, Wang YE, Chen H, et al. (2008) Structural and functional constraints limit options for cytotoxic T-lymphocyte escape in the immunodominant HLA-B27-restricted epitope in human immunodeficiency virus type 1 capsid. J Virol 82: 5594-5605.
55. Altfeld M, Allen TM, (2006) Hitting HIV where it hurts: an alternative approach to HIV vaccine design. Trends Immunol 27: 504-510.
56. Dahirel V, Shekhar K, Pereyra F, Miura T, Artyomov M, et al. (2011) From the Cover: Coordinate linkage of HIV evolution reveals regions of immunological vulnerability. Proc Natl Acad Sci U S A 108: 11530-11535.
57. Leslie A, Kavanagh D, Honeyborne I, Pfafferott K, Edwards C, et al. (2005) Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J Exp Med 201: 891-902.
58. Goepfert PA, Lumm W, Farmer P, Matthews P, Prendergast A, et al. (2008) Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J Exp Med 205: 1009-1017.
59. Chopera DR, Woodman Z, Milsana K, Mlotshwa M, Martin DP, et al. (2008) Transmission of HIV-1 CTL escape variants provides HLA mis-matched recipients with a survival advantage. PLoS Pathog 4: e1000033.
60. Alizon S, von Wyl V, Stadler T, Kouyos RD, Yerly S, et al. (2010) Phylogenetic approach reveals that virus genotype largely determines HIV set-point viral load. PLoS Pathog 6: e1001123.
61. Jordan MR, Kearney M, Palmer S, Shao W, Maldarelli F, et al. (2010) Comparison of standard PCR/cloning to single genome sequencing for analysis of HIV-1 populations. J Virol Methods 168: 114-120.
62. Smyth RP, Schlub TE, Grimm A, Venturi V, Chopra A, et al. (2010) Reducing chimera formation during PCR amplification to ensure accurate genotyping. Gene 469: 45-51.
63. Negroni M, Ricchetti M, Nouvel P, Buc H, (1995) Homologous recombination promoted by reverse transcriptase during copying of two distinct RNA templates. Proc Natl Acad Sci U S A 92: 6971-6975.
64. Rolland M, Tovanabutra S, deCamp AC, Frahm N, Gilbert PB, et al. (2011) Genetic impact of vaccination on breakthrough HIV-1 sequences from the STEP trial. Nat Med 17: 366-371.
65. Asquith B, Edwards CT, Lipsitch M, McLean AR, (2006) Inefficient cytotoxic T lymphocyte-mediated killing of HIV-1-infected cells in vivo. PLoS Biol 4: e90.