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Deep sequence analysis of HIV adaptation following vertical transmission reveals the impact of immune pressure on the evolution of HIV


Autoři: Jennifer Currenti aff001;  Abha Chopra aff002;  Mina John aff002;  Shay Leary aff002;  Elizabeth McKinnon aff002;  Eric Alves aff001;  Mark Pilkinton aff004;  Rita Smith aff004;  Louise Barnett aff004;  Wyatt J. McDonnell aff004;  Michaela Lucas aff005;  Francine Noel aff006;  Simon Mallal aff002;  Joseph A. Conrad aff007;  Spyros Kalams aff004;  Silvana Gaudieri aff001
Působiště autorů: School of Human Sciences, University of Western Australia, Crawley, Western Australia, Australia aff001;  Institute for Immunology and Infectious Diseases, Murdoch University, Murdoch, Western Australia, Australia aff002;  Department of Clinical Immunology, Royal Perth Hospital, Perth, Western Australia, Australia aff003;  Division of Infectious Diseases, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee, United States of America aff004;  School of Medicine, University of Western Australia, Crawley, Western Australia, Australia aff005;  GHESKIO Centre, Port-au-prince, Haiti aff006;  Department of Chemistry, Vanderbilt University, Nashville, Tennessee, United States of America aff007
Vyšlo v časopise: Deep sequence analysis of HIV adaptation following vertical transmission reveals the impact of immune pressure on the evolution of HIV. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008177
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008177

Souhrn

Human immunodeficiency virus (HIV) can adapt to an individual’s T cell immune response via genomic mutations that affect antigen recognition and impact disease outcome. These viral adaptations are specific to the host’s human leucocyte antigen (HLA) alleles, as these molecules determine which peptides are presented to T cells. As HLA molecules are highly polymorphic at the population level, horizontal transmission events are most commonly between HLA-mismatched donor/recipient pairs, representing new immune selection environments for the transmitted virus. In this study, we utilised a deep sequencing approach to determine the HIV quasispecies in 26 mother-to-child transmission pairs where the potential for founder viruses to be pre-adapted is high due to the pairs being haplo-identical at HLA loci. This scenario allowed the assessment of specific HIV adaptations following transmission in either a non-selective immune environment, due to recipient HLA mismatched to original selecting HLA, or a selective immune environment, mediated by matched donor/recipient HLA. We show that the pattern of reversion or fixation of HIV adaptations following transmission provides insight into the replicative cost, and likely compensatory networks, associated with specific adaptations in vivo. Furthermore, although transmitted viruses were commonly heavily pre-adapted to the child’s HLA genotype, we found evidence of de novo post-transmission adaptation, representing new epitopes targeted by the child’s T cell response. High-resolution analysis of HIV adaptation is relevant when considering vaccine and cure strategies for individuals exposed to adapted viruses via transmission or reactivated from reservoirs.

Klíčová slova:

Cell cycle and cell division – Evolutionary adaptation – Immune response – Polymerase chain reaction – T cells – Viral load – Viral replication


Zdroje

1. Boppana S, Goepfert P. Understanding the CD8 T-cell response in natural HIV control. F1000Research. 2018;7. Epub 2018/07/22. doi: 10.12688/f1000research.15029.1 30026916; PubMed Central PMCID: PMC6039933.

2. 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. doi: 10.1038/354453a0 1721107

3. Carlson JM, Du VY, Pfeifer N, Bansal A, Tan VYF, Power K, et al. Impact of pre-adapted HIV transmission. Nature medicine. 2016;22(6):606–13. doi: 10.1038/nm.4100 PMC4899163. 27183217

4. 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. 2002;296(5572):1439. doi: 10.1126/science.1069660 12029127

5. 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. Journal of Virology. 2004;78(16):8927. doi: 10.1128/JVI.78.16.8927-8930.2004 15280502

6. Mónaco DC, Dilernia DA, Fiore-Gartland A, Yu T, Prince JL, Dennis KK, et al. Balance between transmitted HLA preadapted and nonassociated polymorphisms is a major determinant of HIV-1 disease progression. The Journal of Experimental Medicine. 2016;213(10):2049–63. doi: 10.1084/jem.20151984 PMC5030801. 27551154

7. Carlson JM, Schaefer M, Monaco DC, Batorsky R, Claiborne DT, Prince J, et al. Selection bias at the heterosexual HIV-1 transmission bottleneck. Science. 2014;345(6193):1254031. doi: 10.1126/science.1254031 25013080

8. Raghwani J, Redd AD, Longosz AF, Wu C-H, Serwadda D, Martens C, et al. Evolution of HIV-1 within untreated individuals and at the population scale in Uganda. PLOS Pathogens. 2018;14(7):e1007167. doi: 10.1371/journal.ppat.1007167 30052678

9. Chopera DR, Woodman Z, Mlisana K, Mlotshwa M, Martin DP, Seoighe C, et al. Transmission of HIV-1 CTL escape variants provides HLA-mismatched recipients with a survival advantage (transmission of attenuated HIV-1 variants). PLoS Pathogens. 2008;4(3):e1000033. doi: 10.1371/journal.ppat.1000033 18369479

10. Goepfert PA, Lumm W, Farmer P, Matthews P, Prendergast A, Carlson JM, et al. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. Journal of Experimental Medicine. 2008;205(5):1009–17. doi: 10.1084/jem.20072457 18426987

11. Payne R, Muenchhoff M, Mann J, Roberts HE, Matthews P, Adland E, et al. Impact of HLA-driven HIV adaptation on virulence in populations of high HIV seroprevalence. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(50):E5393. doi: 10.1073/pnas.1413339111 25453107

12. Pillay T, Zhang H-T, Drijfhout JW, Robinson N, Brown H, Khan M, et al. Unique acquisition of cytotoxic T-lymphocyte escape mutants in infant human immunodeficiency virus type 1 infection. Journal of Virology. 2005;79(18):12100–5. doi: 10.1128/JVI.79.18.12100-12105.2005 16140787

13. Luzuriaga K, Holmes D, Hereema A, Wong J, Panicali DL, Sullivan JL. HIV-1-specific cytotoxic T lymphocyte responses in the first year of life. J Immunol. 1995;154(1):433–43. 7995957.

14. Thobakgale CF, Ramduth D, Reddy S, Mkhwanazi N, de Pierres C, Moodley E, et al. Human immunodeficiency virus-specific CD8+ T-cell activity is detectable from birth in the majority of in utero-infected infants. J Virol. 2007;81(23):12775–84. doi: 10.1128/JVI.00624-07 17881456; PubMed Central PMCID: PMC2169079.

15. Goulder PJR, Brander C, Tang Y, Tremblay C, Colbert RA, Addo MM, et al. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature. 2001;412(6844):334. doi: 10.1038/35085576 11460164.

16. Kuhn L, Abrams EJ, Palumbo P, Bulterys M, Aga R, Louie L, et al. Maternal versus paternal inheritance of HLA class I alleles among HIV-infected children: consequences for clinical disease progression. Aids. 2004;18(9):1281–9. doi: 10.1097/00002030-200406180-00006 15362660.

17. Almeida C-AM, Bronke C, Roberts SG, McKinnon E, Keane NM, Chopra A, et al. Translation of HLA-HIV associations to the cellular level: HIV adapts to inflate CD8 T cell responses against Nef and HLA-adapted variant epitopes. Journal of immunology. 2011;187(5):2502. doi: 10.4049/jimmunol.1100691 21821798

18. Ryland EG, Tang Y, Christie CD, Feeney ME. Sequence evolution of HIV-1 following mother-to-child transmission. Journal of Virology. 2010;84(23):12437–44. doi: 10.1128/JVI.01617-10 PMC2976410. 20861265

19. Carlson JM, Brumme CJ, Martin E, Listgarten J, Brockman MA, Le AQ, et al. Correlates of protective cellular immunity revealed by analysis of population-level immune escape pathways in HIV-1. Journal of virology. 2012;86(24):13202. doi: 10.1128/JVI.01998-12 23055555

20. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M, et al. HIV evolution: CTL escape mutation and reversion after transmission. Nature Medicine. 2004;10(3):282–9. doi: 10.1038/nm992 14770175.

21. Martinez-Picado J, Prado JG, Fry EE, Pfafferott K, Leslie A, Chetty S, et al. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. The Journal of Virology. 2006;80(7):3617. doi: 10.1128/JVI.80.7.3617-3623.2006 16537629

22. Schneidewind A, Tang Y, Brockman MA, Ryland EG, Dunkley-Thompson J, Steel-Duncan JC, et al. Maternal transmission of human immunodeficiency virus escape mutations subverts HLA-B57 immunodominance but facilitates viral control in the haploidentical infant. Journal of Virology. 2009;83(17):8616. doi: 10.1128/JVI.00730-09 19515764

23. Kløverpris HN, Leslie A, Goulder P. Role of HLA adaptation in HIV evolution. Frontiers in Immunology. 2016;6(665). doi: 10.3389/fimmu.2015.00665 26834742

24. Al-Mawsawi LQ, Wu NC, Olson CA, Shi VC, Qi H, Zheng X, et al. High-throughput profiling of point mutations across the HIV-1 genome. Retrovirology. 2014;11(1):124. doi: 10.1186/s12977-014-0124-6 25522661

25. John M, Heckerman D, James I, Park L, Carlson J, Chopra A, et al. Adaptive interactions between HLA and HIV-I: highly divergent selection imposed by HLA class I molecules with common supertype motifs. Journal Of Immunology. 2010;184(8):4368–77. doi: 10.4049/jimmunol.0903745 20231689

26. Reeves E, Edwards CJ, Elliott T, James E. Naturally occurring ERAP1 haplotypes encode functionally distinct alleles with fine substrate specificity. Journal of immunology (Baltimore, Md: 1950). 2013;191(1):35–43. Epub 2013/06/03. doi: 10.4049/jimmunol.1300598 23733883.

27. Kemming J, Reeves E, Nitschke K, Widmeier V, Emmerich F, Hermle T, et al. ERAP1 allotypes shape the epitope repertoire of virus-specific CD8(+) T cell responses in acute hepatitis C virus infection. Journal of hepatology. 2019;70(6):1072–81. Epub 2019/02/16. doi: 10.1016/j.jhep.2019.01.034 30769005; PubMed Central PMCID: PMC6527866.

28. Akram A, Lin A, Gracey E, Streutker CJ, Inman RD. HLA-B27, but Not HLA-B7, Immunodominance to Influenza Is ERAP Dependent. The Journal of Immunology. 2014;192(12):5520. doi: 10.4049/jimmunol.1400343 24835397

29. Brumme ZL, Kinloch NN, Sanche S, Wong A, Martin E, Cobarrubias KD, et al. Extensive host immune adaptation in a concentrated North American HIV epidemic. AIDS (London, England). 2018;32(14):1927–38. doi: 10.1097/QAD.0000000000001912 30048246.

30. Katoh J, Kawana-Tachikawa A, Shimizu A, Zhu D, Han C, Nakamura H, et al. Rapid HIV-1 Disease Progression in Individuals Infected with a Virus Adapted to Its Host Population. PLOS ONE. 2016;11(3):e0150397. doi: 10.1371/journal.pone.0150397 26953793

31. Addo MM, Yu XG, Rathod A, Cohen D, Eldridge RL, Strick D, et al. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J Virol. 2003;77(3):2081–92. doi: 10.1128/JVI.77.3.2081-2092.2003 12525643; PubMed Central PMCID: PMC140965.

32. Brumme ZL, John M, Carlson JM, Brumme CJ, Chan D, Brockman MA, et al. HLA-associated immune escape pathways in HIV-1 subtype B Gag, Pol and Nef proteins. PLoS ONE. 2009;4(8):e6687. doi: 10.1371/journal.pone.0006687 19690614

33. 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(7018):769–75. doi: 10.1038/nature03113 15592417

34. Carrington M, O'Brien SJ. The influence of HLA genotype on AIDS. Annual Review of Medicine. 2003;54(1):535–51. doi: 10.1146/annurev.med.54.101601.152346 12525683

35. Wright JK, Novitsky V, Brockman MA, Brumme ZL, Brumme CJ, Carlson JM, et al. Influence of Gag-protease-mediated replication capacity on disease progression in individuals recently infected with HIV-1 subtype C. Journal of Virology. 2011;85(8):3996. doi: 10.1128/JVI.02520-10 21289112

36. Leitman EM, Thobakgale CF, Adland E, Ansari MA, Raghwani J, Prendergast AJ, et al. Role of HIV-specific CD8+ T cells in pediatric HIV cure strategies after widespread early viral escape. The Journal of Experimental Medicine. 2017.

37. Prendergast A, Tudor-Williams G, Jeena P, Burchett S, Goulder P. International perspectives, progress, and future challenges of paediatric HIV infection. Lancet (London, England). 2007;370(9581):68–80. doi: 10.1016/s0140-6736(07)61051-4 17617274.

38. Prendergast AJ, Klenerman P, Goulder PJ. The impact of differential antiviral immunity in children and adults. Nat Rev Immunol. 2012;12(9):636–48. doi: 10.1038/nri3277 22918466.

39. Goulder PJ, Lewin SR, Leitman EM. Paediatric HIV infection: the potential for cure. Nat Rev Immunol. 2016;16(4):259–71. Epub 2016/03/15. doi: 10.1038/nri.2016.19 26972723.

40. Scott ZA, Chadwick EG, Gibson LL, Catalina MD, McManus MM, Yogev R, et al. Infrequent detection of HIV-1-specific, but not cytomegalovirus-specific, CD8(+) T cell responses in young HIV-1-infected infants. J Immunol. 2001;167(12):7134–40. Epub 2001/12/12. doi: 10.4049/jimmunol.167.12.7134 11739536.

41. Garcia-Knight MA, Slyker J, Payne BL, Pond SL, de Silva TI, Chohan B, et al. Viral Evolution and Cytotoxic T Cell Restricted Selection in Acute Infant HIV-1 Infection. Scientific reports. 2016;6:29536. Epub 2016/07/13. doi: 10.1038/srep29536 27403940; PubMed Central PMCID: PMC4941567.

42. Feeney ME, Tang Y, Pfafferott K, Roosevelt KA, Draenert R, Trocha A, et al. HIV-1 viral escape in infancy followed by emergence of a variant-specific CTL response. Journal of immunology (Baltimore, Md: 1950). 2005;174(12):7524.

43. Janes H, Friedrich DP, Krambrink A, Smith RJ, Kallas EG, Horton H, et al. Vaccine-induced gag-specific T cells are associated with reduced viremia after HIV-1 infection. J Infect Dis. 2013;208(8):1231–9. Epub 2013/07/24. doi: 10.1093/infdis/jit322 23878319; PubMed Central PMCID: PMC3778967.

44. Karlsson I, Brandt L, Vinner L, Kromann I, Andreasen LV, Andersen P, et al. Adjuvanted HLA-supertype restricted subdominant peptides induce new T-cell immunity during untreated HIV-1-infection. Clinical immunology (Orlando, Fla). 2013;146(2):120–30. doi: 10.1016/j.clim.2012.12.005 23314272.

45. Brander C, Goulder PJ, Luzuriaga K, Yang OO, Hartman KE, Jones NG, et al. Persistent HIV-1-specific CTL clonal expansion despite high viral burden post in utero HIV-1 infection. J Immunol. 1999;162(8):4796–800. Epub 1999/04/14. 10202022.

46. Weinberg A, Song L-Y, Wilkening C, Sevin A, Blais B, Louzao R, et al. Optimization and Limitations of Use of Cryopreserved Peripheral Blood Mononuclear Cells for Functional and Phenotypic T-Cell Characterization. Clinical and Vaccine Immunology. 2009;16(8):1176. doi: 10.1128/CVI.00342-08 19515870

47. Erlich RL, Jia X, Anderson S, Banks E, Gao X, Carrington M, et al. Next-generation sequencing for HLA typing of class I loci. BMC Genomics. 2011;12(1):42. doi: 10.1186/1471-2164-12-42 21244689

48. Robinson J, Halliwell JA, Hayhurst JD, Flicek P, Parham P, Marsh SGE. The IPD and IMGT/HLA database: allele variant databases. Nucleic acids research. 2015;43(Database issue):D423–D31. Epub 2014/11/20. doi: 10.1093/nar/gku1161 25414341.

49. Chessman D, Kostenko L, Lethborg T, Purcell AW, Williamson NA, Chen Z, et al. Human leukocyte antigen class I-restricted activation of CD8+ T cells provides the immunogenetic basis of a systemic drug hypersensitivity. Immunity. 2008;28(6):822–32. Epub 2008/06/14. doi: 10.1016/j.immuni.2008.04.020 18549801.

50. Leary S, Cooper D, Chopra A, Watson M. IIID VGAS—A Visual Genome Analysis Studio incorporating high performance next generation sequence analysis2013.

51. Jabara CB, Jones CD, Roach J, Anderson JA, Swanstrom R. Accurate sampling and deep sequencing of the HIV-1 protease gene using a Primer ID. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(50):20166–71. doi: 10.1073/pnas.1110064108 22135472

52. Barnard R, Chopra A, James I, Blinco J, Watson MW, Jabara CB, et al. Primer ID ultra-deep sequencing reveals dynamics of drug resistance-associated variants in breakthrough hepatitis C viruses: relevance to treatment outcome and resistance screening. Antivir Ther. 2016;21(7):567–77. Epub 2016/05/25. doi: 10.3851/IMP3056 27219495.

53. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution. 2016;33(7):1870–4. doi: 10.1093/molbev/msw054 27004904

54. de Oliveira T, Deforche K, Cassol S, Salminen M, Paraskevis D, Seebregts C, et al. An automated genotyping system for analysis of HIV-1 and other microbial sequences. Bioinformatics. 2005;21(19):3797–800. doi: 10.1093/bioinformatics/bti607 16076886

55. Berezin C, Glaser F, Rosenberg J, Paz I, Pupko T, Fariselli P, et al. ConSeq: the identification of functionally and structurally important residues in protein sequences. Bioinformatics. 2004;20(8):1322–4. doi: 10.1093/bioinformatics/bth070 14871869

56. Henikoff S, Henikoff JG. Amino acid substitution matrices from protein blocks. Proceedings of the National Academy of Sciences. 1992;89(22):10915. doi: 10.1073/pnas.89.22.10915 1438297

57. Goulder PJ, Tang Y, Brander C, Betts MR, Altfeld M, Annamalai K, et al. Functionally inert HIV-specific cytotoxic T lymphocytes do not play a major role in chronically infected adults and children. The Journal of experimental medicine. 2000;192(12):1819–32. doi: 10.1084/jem.192.12.1819 11120778.

58. Slyker JA, John-Stewart GC, Dong T, Lohman-Payne B, Reilly M, Atzberger A, et al. Phenotypic Characterization of HIV-Specific CD8+ T Cells during Early and Chronic Infant HIV-1 Infection. PLOS ONE. 2011;6(5):e20375. doi: 10.1371/journal.pone.0020375 21655252

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Hygiena a epidemiologie Infekční lékařství Laboratoř

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