A de novo approach to inferring within-host fitness effects during untreated HIV-1 infection


Autoři: Christopher J. R. Illingworth aff001;  Jayna Raghwani aff004;  David Serwadda aff006;  Nelson K. Sewankambo aff006;  Merlin L. Robb aff008;  Michael A. Eller aff008;  Andrew R. Redd aff009;  Thomas C. Quinn aff010;  Katrina A. Lythgoe aff004
Působiště autorů: Department of Genetics, University of Cambridge, Cambridge, United Kingdom aff001;  Department of Applied Mathematics and Theoretical Physics, University of Cambridge, Cambridge, United Kingdom aff002;  School of Chemical and Biological Sciences, Queen Mary University of London, London, United Kingdom aff003;  Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom aff004;  Department of Zoology, Peter Medawar Building, University of Oxford, Oxford, United Kingdom aff005;  Rakai Health Sciences Program, Kalisizo, Uganda, School of Public Health, Makerere University, Kampala, Uganda aff006;  School of Medicine, Makerere University, College of Health Sciences, Kampala, Uganda aff007;  U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, Maryland, United States of America aff008;  Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, Maryland, United States of America aff009;  Department of Medicine, Johns Hopkins School of Medicine, Johns Hopkins University, Baltimore, Maryland, United States of America aff010;  Laboratory of Immunoregulation, Division of Intramural Research, NIAID, NIH, Baltimore Maryland, United States of America aff011
Vyšlo v časopise: A de novo approach to inferring within-host fitness effects during untreated HIV-1 infection. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1008171
Kategorie: Research Article
doi: 10.1371/journal.ppat.1008171

Souhrn

In the absence of effective antiviral therapy, HIV-1 evolves in response to the within-host environment, of which the immune system is an important aspect. During the earliest stages of infection, this process of evolution is very rapid, driven by a small number of CTL escape mutations. As the infection progresses, immune escape variants evolve under reduced magnitudes of selection, while competition between an increasing number of polymorphic alleles (i.e., clonal interference) makes it difficult to quantify the magnitude of selection acting upon specific variant alleles. To tackle this complex problem, we developed a novel multi-locus inference method to evaluate the role of selection during the chronic stage of within-host infection. We applied this method to targeted sequence data from the p24 and gp41 regions of HIV-1 collected from 34 patients with long-term untreated HIV-1 infection. We identify a broad distribution of beneficial fitness effects during infection, with a small number of variants evolving under strong selection and very many variants evolving under weaker selection. The uniquely large number of infections analysed granted a previously unparalleled statistical power to identify loci at which selection could be inferred to act with statistical confidence. Our model makes no prior assumptions about the nature of alleles under selection, such that any synonymous or non-synonymous variant may be inferred to evolve under selection. However, the majority of variants inferred with confidence to be under selection were non-synonymous in nature, and in most cases were have previously been associated with either CTL escape in p24 or neutralising antibody escape in gp41. We also identified a putative new CTL escape site (residue 286 in gag), and a region of gp41 (including residues 644, 648, 655 in env) likely to be associated with immune escape. Sites inferred to be under selection in multiple hosts have high within-host and between-host diversity although not all sites with high between-host diversity were inferred to be under selection at the within-host level. Our identification of selection at sites associated with resistance to broadly neutralising antibodies (bNAbs) highlights the need to fully understand the role of selection in untreated individuals when designing bNAb based therapies.

Klíčová slova:

Alleles – Antibodies – Evolutionary immunology – Haplotypes – HIV-1 – Natural selection – Species diversity – Viral evolution


Zdroje

1. Rambaut A, Posada D, Crandall KA, Holmes EC. The causes and consequences of HIV evolution. Nat Rev Genet. 2004;5: 52–61. doi: 10.1038/nrg1246 14708016

2. Zanini F, Brodin J, Thebo L, Lanz C, Bratt G, Albert J, et al. Population genomics of intrapatient HIV-1 evolution. Elife. 2015;4. doi: 10.7554/eLife.11282 26652000

3. Lythgoe KA, Gardner A, Pybus OG, Grove J. Short-Sighted Virus Evolution and a Germline Hypothesis for Chronic Viral Infections. Trends Microbiol. 2017;25: 336–348. doi: 10.1016/j.tim.2017.03.003 28377208

4. Keating CP, Hill MK, Hawkes DJ, Smyth RP, Isel C, Le S-Y, et al. The A-rich RNA sequences of HIV-1 pol are important for the synthesis of viral cDNA. Nucleic Acids Res. 2009;37: 945–956. doi: 10.1093/nar/gkn1015 19106143

5. Snoeck J, Fellay J, Bartha I, Douek DC, Telenti A. Mapping of positive selection sites in the HIV-1 genome in the context of RNA and protein structural constraints. Retrovirology. 2011;8: 87. doi: 10.1186/1742-4690-8-87 22044801

6. Parera M, Fernàndez G, Clotet B, Martínez MA. HIV-1 protease catalytic efficiency effects caused by random single amino acid substitutions. Mol Biol Evol. 2007;24: 382–387. doi: 10.1093/molbev/msl168 17090696

7. Rihn SJ, Hughes J, Wilson SJ, Bieniasz PD. Uneven Genetic Robustness of HIV-1 Integrase. J Virol. 2014;89: 552–567. doi: 10.1128/JVI.02451-14 25339768

8. Haddox HK, Dingens AS, Bloom JD. Experimental Estimation of the Effects of All Amino-Acid Mutations to HIV’s Envelope Protein on Viral Replication in Cell Culture. PLoS Pathog. 2016;12: e1006114. doi: 10.1371/journal.ppat.1006114 27959955

9. Haddox HK, Dingens AS, Hilton SK, Overbaugh J, Bloom JD. Mapping mutational effects along the evolutionary landscape of HIV envelope. Elife. 2018;7. doi: 10.7554/eLife.34420 29590010

10. Hinkley T, Martins J, Chappey C, Haddad M, Stawiski E, Whitcomb JM, et al. A systems analysis of mutational effects in HIV-1 protease and reverse transcriptase. Nat Genet. 2011;43: 487–489. doi: 10.1038/ng.795 21441930

11. Rhee S-Y, Gonzales MJ, Kanor R, Betts BJ, Ravela J, Shafer RW. Human immunodeficiency virus reverse transcriptase and protease sequence database. Nucleic Acids Res. 2003;31: 298–303. doi: 10.1093/nar/gkg100 12520007

12. Ferguson AL, Mann JK, Omarjee S, Ndung’u T, Walker BD, Chakraborty AK. Translating HIV sequences into quantitative fitness landscapes predicts viral vulnerabilities for rational immunogen design. Immunity. 2013;38: 606–617. doi: 10.1016/j.immuni.2012.11.022 23521886

13. Barton JP, Goonetilleke N, Butler TC, Walker BD, McMichael AJ, Chakraborty AK. Relative rate and location of intra-host HIV evolution to evade cellular immunity are predictable. Nat Commun. 2016;7: 11660. doi: 10.1038/ncomms11660 27212475

14. Louie RHY, Kaczorowski KJ, Barton JP, Chakraborty AK, McKay MR. Fitness landscape of the human immunodeficiency virus envelope protein that is targeted by antibodies. Proc Natl Acad Sci U S A. 2018;115: E564–E573. doi: 10.1073/pnas.1717765115 29311326

15. 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. doi: 10.1038/nature03113 15592417

16. Matthews PC, Leslie AJ, Katzourakis A, Crawford H, Payne R, Prendergast A, et al. HLA footprints on human immunodeficiency virus type 1 are associated with interclade polymorphisms and intraclade phylogenetic clustering. J Virol. 2009;83: 4605–4615. doi: 10.1128/JVI.02017-08 19244334

17. Theys K, Feder AF, Gelbart M, Hartl M, Stern A, Pennings PS. Within-patient mutation frequencies reveal fitness costs of CpG dinucleotides and drastic amino acid changes in HIV. PLoS Genet. 2018;14: e1007420. doi: 10.1371/journal.pgen.1007420 29953449

18. Haldane JBS. The Effect of Variation of Fitness. Am Nat. 1937;71: 337–349.

19. Fernandez CS, Stratov I, De Rose R, Walsh K, Dale CJ, Smith MZ, et al. Rapid viral escape at an immunodominant simian-human immunodeficiency virus cytotoxic T-lymphocyte epitope exacts a dramatic fitness cost. J Virol. 2005;79: 5721–5731. doi: 10.1128/JVI.79.9.5721-5731.2005 15827187

20. Asquith B, Edwards CTT, Lipsitch M, McLean AR. Inefficient Cytotoxic T Lymphocyte–Mediated Killing of HIV-1–Infected Cells In Vivo. PLoS Biol. 2006;4: e90. doi: 10.1371/journal.pbio.0040090 16515366

21. Ganusov VV, De Boer RJ. Estimating Costs and Benefits of CTL Escape Mutations in SIV/HIV Infection. PLoS Comput Biol. 2006;2: e24. doi: 10.1371/journal.pcbi.0020024 16604188

22. Ganusov VV, Goonetilleke N, Liu MKP, Ferrari G, Shaw GM, McMichael AJ, et al. Fitness costs and diversity of the cytotoxic T lymphocyte (CTL) response determine the rate of CTL escape during acute and chronic phases of HIV infection. J Virol. 2011;85: 10518–10528. doi: 10.1128/JVI.00655-11 21835793

23. Kessinger TA, Perelson AS, Neher RA. Inferring HIV Escape Rates from Multi-Locus Genotype Data. Front Immunol. 2013;4. doi: 10.3389/fimmu.2013.00252 24027569

24. van Deutekom HWM, Wijnker G, de Boer RJ. The rate of immune escape vanishes when multiple immune responses control an HIV infection. J Immunol. 2013;191: 3277–3286. doi: 10.4049/jimmunol.1300962 23940274

25. Leviyang S, Ganusov VV. Broad CTL Response in Early HIV Infection Drives Multiple Concurrent CTL Escapes. PLoS Comput Biol. 2015;11: e1004492. doi: 10.1371/journal.pcbi.1004492 26506433

26. Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966;8: 269. 5980116

27. Illingworth CJR, Mustonen V. Distinguishing driver and passenger mutations in an evolutionary history categorized by interference. Genetics. 2011;189: 989–1000. doi: 10.1534/genetics.111.133975 21900272

28. Garcia V, Regoes RR. The Effect of Interference on the CD8 T Cell Escape Rates in HIV. Front Immunol. 2015;5. doi: 10.3389/fimmu.2014.00661 25628620

29. Garcia V, Feldman MW, Regoes RR. Investigating the Consequences of Interference between Multiple CD8+ T Cell Escape Mutations in Early HIV Infection. PLoS Comput Biol. 2016;12: e1004721. doi: 10.1371/journal.pcbi.1004721 26829720

30. Yang Y, Ganusov VV. Kinetics of HIV-Specific CTL Responses Plays a Minimal Role in Determining HIV Escape Dynamics. Frontiers in Immunology. 2018. doi: 10.3389/fimmu.2018.00140 29472921

31. 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 Pathog. 2018;14: e1007167. doi: 10.1371/journal.ppat.1007167 30052678

32. Illingworth CJR. Fitness Inference from Short-Read Data: Within-Host Evolution of a Reassortant H5N1 Influenza Virus. Mol Biol Evol. 2015;32: 3012–3026. doi: 10.1093/molbev/msv171 26243288

33. Asquith B, McLean AR. In vivo CD8 T cell control of immunodeficiency virus infection in humans and macaques. Proceedings of the National Academy of Sciences. 2007. pp. 6365–6370. doi: 10.1073/pnas.0700666104 17404226

34. Yang OO, Daar ES, Jamieson BD, Balamurugan A, Smith DM, Pitt JA, et al. Human immunodeficiency virus type 1 clade B superinfection: evidence for differential immune containment of distinct clade B strains. J Virol. 2005;79: 860–868. doi: 10.1128/JVI.79.2.860-868.2005 15613314

35. Watanabe K, Murakoshi H, Tamura Y, Koyanagi M, Chikata T, Gatanaga H, et al. Identification of cross-clade CTL epitopes in HIV-1 clade A/E-infected individuals by using the clade B overlapping peptides. Microbes Infect. 2013;15: 874–886. doi: 10.1016/j.micinf.2013.08.002 23968885

36. Buckheit RW 3rd, Allen TG, Alme A, Salgado M, O’Connell KA, Huculak S, et al. Host factors dictate control of viral replication in two HIV-1 controller/chronic progressor transmission pairs. Nat Commun. 2012;3: 716. doi: 10.1038/ncomms1697 22395607

37. Sipsas NV, Kalams SA, Trocha A, He S, Blattner WA, Walker BD, et al. Identification of type-specific cytotoxic T lymphocyte responses to homologous viral proteins in laboratory workers accidentally infected with HIV-1. J Clin Invest. 1997;99: 752–762. doi: 10.1172/JCI119221 9045880

38. Hoof I, Pérez CL, Buggert M, Gustafsson RKL, Nielsen M, Lund O, et al. Interdisciplinary analysis of HIV-specific CD8+ T cell responses against variant epitopes reveals restricted TCR promiscuity. J Immunol. 2010;184: 5383–5391. doi: 10.4049/jimmunol.0903516 20363973

39. Tang Y, Huang S, Dunkley-Thompson J, Steel-Duncan JC, Ryland EG, St John MA, et al. Correlates of spontaneous viral control among long-term survivors of perinatal HIV-1 infection expressing human leukocyte antigen-B57. AIDS. 2010;24: 1425–1435. doi: 10.1097/QAD.0b013e32833a2b5b 20539088

40. Miura T, Brockman MA, Schneidewind A, Lobritz M, Pereyra F, Rathod A, et al. 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. 2009;83: 2743–2755. doi: 10.1128/JVI.02265-08 19116253

41. Chopera DR, Mlotshwa M, Woodman Z, Mlisana K, de Assis Rosa D, Martin DP, et al. Virological and Immunological Factors Associated with HIV-1 Differential Disease Progression in HLA-B*58:01-Positive Individuals. Journal of Virology. 2011. pp. 7070–7080. doi: 10.1128/JVI.02543-10 21613398

42. Koup RA, Roederer M, Lamoreaux L, Fischer J, Novik L, Nason MC, et al. Priming immunization with DNA augments immunogenicity of recombinant adenoviral vectors for both HIV-1 specific antibody and T-cell responses. PLoS One. 2010;5: e9015. doi: 10.1371/journal.pone.0009015 20126394

43. 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. J Immunol. 2005;174: 7524–7530. doi: 10.4049/jimmunol.174.12.7524 15944251

44. McKinnon LR, Capina R, Peters H, Mendoza M, Kimani J, Wachihi C, et al. Clade-specific evolution mediated by HLA-B*57/5801 in human immunodeficiency virus type 1 clade A1 p24. J Virol. 2009;83: 12636–12642. doi: 10.1128/JVI.01236-09 19759140

45. Payne RP, Branch S, Kløverpris H, Matthews PC, Koofhethile CK, Strong T, et al. Differential escape patterns within the dominant HLA-B*57:03-restricted HIV Gag epitope reflect distinct clade-specific functional constraints. J Virol. 2014;88: 4668–4678. doi: 10.1128/JVI.03303-13 24501417

46. Du VY, Bansal A, Carlson J, Salazar-Gonzalez JF, Salazar MG, Ladell K, et al. HIV-1-Specific CD8 T Cells Exhibit Limited Cross-Reactivity during Acute Infection. J Immunol. 2016;196: 3276–3286. doi: 10.4049/jimmunol.1502411 26983786

47. Vollbrecht T, Brackmann H, Henrich N, Roeling J, Seybold U, Bogner JR, et al. Impact of changes in antigen level on CD38/PD-1 co-expression on HIV-specific CD8 T cells in chronic, untreated HIV-1 infection. J Med Virol. 2010;82: 358–370. doi: 10.1002/jmv.21723 20087935

48. Zhao S, Zhai S, Zhuang Y, Wang S, Huang D, Kang W, et al. Inter-clade cross-reactivity of HIV-1-specific T cell responses in human immunodeficiency virus type 1 infection in China. Curr HIV Res. 2007;5: 251–259. doi: 10.2174/157016207780076995 17346138

49. Malhotra U, Nolin J, Mullins JI, McElrath MJ. Comprehensive epitope analysis of cross-clade Gag-specific T-cell responses in individuals with early HIV-1 infection in the US epidemic. Vaccine. 2007;25: 381–390. doi: 10.1016/j.vaccine.2006.07.045 17112643

50. Kaul R, Dong T, Plummer FA, Kimani J, Rostron T, Kiama P, et al. CD8(+) lymphocytes respond to different HIV epitopes in seronegative and infected subjects. J Clin Invest. 2001;107: 1303–1310. doi: 10.1172/JCI12433 11375420

51. Aidoo M, Sawadogo S, Bile EC, Yang C, Nkengasong JN, McNicholl JM. Viral, HLA and T cell elements in cross-reactive immune responses to HIV-1 subtype A, CRF01_AE and CRF02_AG vaccine sequence in Ivorian blood donors. Vaccine. 2008. pp. 4830–4839. doi: 10.1016/j.vaccine.2008.06.097 18640166

52. Migueles SA, Laborico AC, Imamichi H, Shupert WL, Royce C, McLaughlin M, et al. The Differential Ability of HLA B*5701 Long-Term Nonprogressors and Progressors To Restrict Human Immunodeficiency Virus Replication Is Not Caused by Loss of Recognition of Autologous Viral gag Sequences. Journal of Virology. 2003. pp. 6889–6898. doi: 10.1128/jvi.77.12.6889-6898.2003 12768008

53. Blattner C, Lee JH, Sliepen K, Derking R, Falkowska E, de la Peña AT, et al. Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity. 2014;40: 669–680. doi: 10.1016/j.immuni.2014.04.008 24768348

54. Falkowska E, Le KM, Ramos A, Doores KJ, Lee JH, Blattner C, et al. Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity. 2014;40: 657–668. doi: 10.1016/j.immuni.2014.04.009 24768347

55. Hraber P, Korber B, Wagh K, Giorgi EE, Bhattacharya T, Gnanakaran S, et al. Longitudinal Antigenic Sequences and Sites from Intra-Host Evolution (LASSIE) Identifies Immune-Selected HIV Variants. Viruses. 2015;7: 5443–5475. doi: 10.3390/v7102881 26506369

56. Bricault CA, Yusim K, Seaman MS, Yoon H, Theiler J, Giorgi EE, et al. HIV-1 Neutralizing Antibody Signatures and Application to Epitope-Targeted Vaccine Design. Cell Host Microbe. 2019;26: 296. doi: 10.1016/j.chom.2019.07.016 31415756

57. Huang J, Kang BH, Pancera M, Lee JH, Tong T, Feng Y, et al. Broad and potent HIV-1 neutralization by a human antibody that binds the gp41-gp120 interface. Nature. 2014;515: 138–142. doi: 10.1038/nature13601 25186731

58. Corti D, Langedijk JPM, Hinz A, Seaman MS, Vanzetta F, Fernandez-Rodriguez BM, et al. Analysis of Memory B Cell Responses and Isolation of Novel Monoclonal Antibodies with Neutralizing Breadth from HIV-1-Infected Individuals. PLoS ONE. 2010. p. e8805. doi: 10.1371/journal.pone.0008805 20098712

59. Gnanakaran S, Daniels MG, Bhattacharya T, Lapedes AS, Sethi A, Li M, et al. Genetic signatures in the envelope glycoproteins of HIV-1 that associate with broadly neutralizing antibodies. PLoS Comput Biol. 2010;6: e1000955. doi: 10.1371/journal.pcbi.1000955 20949103

60. Haim H, Strack B, Kassa A, Madani N, Wang L, Courter JR, et al. Contribution of intrinsic reactivity of the HIV-1 envelope glycoproteins to CD4-independent infection and global inhibitor sensitivity. PLoS Pathog. 2011;7: e1002101. doi: 10.1371/journal.ppat.1002101 21731494

61. Brunel FM, Zwick MB, Cardoso RMF, Nelson JD, Wilson IA, Burton DR, et al. Structure-function analysis of the epitope for 4E10, a broadly neutralizing human immunodeficiency virus type 1 antibody. J Virol. 2006;80: 1680–1687. doi: 10.1128/JVI.80.4.1680-1687.2006 16439525

62. Nelson JD, Brunel FM, Jensen R, Crooks ET, Cardoso RMF, Wang M, et al. An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J Virol. 2007;81: 4033–4043. doi: 10.1128/JVI.02588-06 17287272

63. Chuang G-Y, Chuang GY., Acharya P, Schmidt SD, Yang Y, Louder MK, et al. Residue-Level Prediction of HIV-1 Antibody Epitopes Based on Neutralization of Diverse Viral Strains. Journal of Virology. 2013. pp. 10047–10058. doi: 10.1128/JVI.00984-13 23843642

64. Montero M, Gulzar N, Klaric K-A, Donald JE, Lepik C, Wu S, et al. Neutralizing epitopes in the membrane-proximal external region of HIV-1 gp41 are influenced by the transmembrane domain and the plasma membrane. J Virol. 2012;86: 2930–2941. doi: 10.1128/JVI.06349-11 22238313

65. Williams KL, Cortez V, Dingens AS, Gach JS, Rainwater S, Weis JF, et al. HIV-specific CD4-induced Antibodies Mediate Broad and Potent Antibody-dependent Cellular Cytotoxicity Activity and are Commonly Detected in Plasma from HIV-infected Humans. EBioMedicine. 2015. pp. 1464–1477. doi: 10.1016/j.ebiom.2015.09.001 26629541

66. Cao K, Moormann AM, Lyke KE, Masaberg C, Sumba OP, Doumbo OK, et al. Differentiation between African populations is evidenced by the diversity of alleles and haplotypes of HLA class I loci. Tissue Antigens. 2004. pp. 293–325. doi: 10.1111/j.0001-2815.2004.00192.x 15009803

67. Kijak GH, Walsh AM, Koehler RN, Moqueet N, Eller LA, Eller M, et al. HLA class I allele and haplotype diversity in Ugandans supports the presence of a major east African genetic cluster. Tissue Antigens. 2009. pp. 262–269. doi: 10.1111/j.1399-0039.2008.01192.x 19254258

68. González-Galarza FF, Takeshita LYC, Santos EJM, Kempson F, Maia MHT, da Silva ALS, et al. Allele frequency net 2015 update: new features for HLA epitopes, KIR and disease and HLA adverse drug reaction associations. Nucleic Acids Res. 2015;43: D784–8. doi: 10.1093/nar/gku1166 25414323

69. Walker B, McMichael A. The T-Cell Response to HIV. Cold Spring Harbor Perspectives in Medicine. 2012. pp. a007054–a007054. doi: 10.1101/cshperspect.a007054 23002014

70. Bar KJ, Tsao C-Y, Iyer SS, Decker JM, Yang Y, Bonsignori M, et al. Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape. PLoS Pathogens. 2012. p. e1002721. doi: 10.1371/journal.ppat.1002721 22693447

71. Herbeck JT, Nickle DC, Learn GH, Gottlieb GS, Curlin ME, Heath L, et al. Human Immunodeficiency Virus Type 1 env Evolves toward Ancestral States upon Transmission to a New Host. Journal of Virology. 2006. pp. 1637–1644. doi: 10.1128/JVI.80.4.1637-1644.2006 16439520

72. 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. pp. 282–289. doi: 10.1038/nm992 14770175

73. Friedrich TC, Dodds EJ, Yant LJ, Vojnov L, Rudersdorf R, Cullen C, et al. Reversion of CTL escape–variant immunodeficiency viruses in vivo. Nature Medicine. 2004. pp. 275–281. doi: 10.1038/nm998 14966520

74. Delport W, Scheffler K, Seoighe C. Frequent Toggling between Alternative Amino Acids Is Driven by Selection in HIV-1. PLoS Pathogens. 2008. p. e1000242. doi: 10.1371/journal.ppat.1000242 19096508

75. Frost SDW, Wrin T, Smith DM, Pond SLK, Liu Y, Paxinos E, et al. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proceedings of the National Academy of Sciences. 2005. pp. 18514–18519. doi: 10.1073/pnas.0504658102 16339909

76. Richman DD, Wrin T, Little SJ, Petropoulos CJ. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proceedings of the National Academy of Sciences. 2003. pp. 4144–4149. doi: 10.1073/pnas.0630530100 12644702

77. Zanini F, Puller V, Brodin J, Albert J, Neher RA. mutation rates and the landscape of fitness costs of HIV-1. Virus Evol. 2017;3: vex003. doi: 10.1093/ve/vex003 28458914

78. Rouzine IM, Rodrigo A, Coffin JM. Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol Mol Biol Rev. 2001;65: 151–185. doi: 10.1128/MMBR.65.1.151-185.2001 11238990

79. Lythgoe KA, Fraser C. New insights into the evolutionary rate of HIV-1 at the within-host and epidemiological levels. Proceedings of the Royal Society B: Biological Sciences. 2012. pp. 3367–3375. doi: 10.1098/rspb.2012.0595 22593106

80. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, et al. Antibody neutralization and escape by HIV-1. Nature. 2003;422: 307–312. doi: 10.1038/nature01470 12646921

81. van Gils MJ, Bunnik EM, Burger JA, Jacob Y, Schweighardt B, Wrin T, et al. Rapid escape from preserved cross-reactive neutralizing humoral immunity without loss of viral fitness in HIV-1-infected progressors and long-term nonprogressors. J Virol. 2010;84: 3576–3585. doi: 10.1128/JVI.02622-09 20071586

82. Lynch RM, Rong R, Boliar S, Sethi A, Li B, Mulenga J, et al. The B Cell Response Is Redundant and Highly Focused on V1V2 during Early Subtype C Infection in a Zambian Seroconverter. Journal of Virology. 2011. pp. 905–915. doi: 10.1128/JVI.02006-10 20980495

83. Moore PL, Ranchobe N, Lambson BE, Gray ES, Cave E, Abrahams M-R, et al. Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog. 2009;5: e1000598. doi: 10.1371/journal.ppat.1000598 19763271

84. Lynch RM, Wong P, Tran L, O’Dell S, Nason MC, Li Y, et al. HIV-1 fitness cost associated with escape from the VRC01 class of CD4 binding site neutralizing antibodies. J Virol. 2015;89: 4201–4213. doi: 10.1128/JVI.03608-14 25631091

85. Bunnik EM, Euler Z, Welkers MRA, Boeser-Nunnink BDM, Grijsen ML, Prins JM, et al. Adaptation of HIV-1 envelope gp120 to humoral immunity at a population level. Nat Med. 2010;16: 995–997. doi: 10.1038/nm.2203 20802498

86. Bouvin-Pley M, Morgand M, Moreau A, Jestin P, Simonnet C, Tran L, et al. Evidence for a continuous drift of the HIV-1 species towards higher resistance to neutralizing antibodies over the course of the epidemic. PLoS Pathog. 2013;9: e1003477. doi: 10.1371/journal.ppat.1003477 23853594

87. Bouvin-Pley M, Morgand M, Meyer L, Goujard C, Moreau A, Mouquet H, et al. Drift of the HIV-1 Envelope Glycoprotein gp120 toward Increased Neutralization Resistance over the Course of the Epidemic: a Comprehensive Study Using the Most Potent and Broadly Neutralizing Monoclonal Antibodies. Journal of Virology. 2014. pp. 13910–13917. doi: 10.1128/JVI.02083-14 25231299

88. Rademeyer C, Korber B, Seaman MS, Giorgi EE, Thebus R, Robles A, et al. Features of Recently Transmitted HIV-1 Clade C Viruses that Impact Antibody Recognition: Implications for Active and Passive Immunization. PLoS Pathog. 2016;12: e1005742. doi: 10.1371/journal.ppat.1005742 27434311

89. Stefic K, Bouvin-Pley M, Essat A, Visdeloup C, Moreau A, Goujard C, et al. Sensitivity to Broadly Neutralizing Antibodies of Recently Transmitted HIV-1 Clade CRF02_AG Viruses with a Focus on Evolution over Time. Journal of Virology. 2018. doi: 10.1128/jvi.01492-18 30404804

90. Sobel Leonard A, McClain MT, Smith GJD, Wentworth DE, Halpin RA, Lin X, et al. The effective rate of influenza reassortment is limited during human infection. PLoS Pathog. 2017;13: e1006203. doi: 10.1371/journal.ppat.1006203 28170438

91. Illingworth CJR, Mustonen V. Components of selection in the evolution of the influenza virus: linkage effects beat inherent selection. PLoS Pathog. 2012;8: e1003091. doi: 10.1371/journal.ppat.1003091 23300444

92. Illingworth CJR, Fischer A, Mustonen V. Identifying selection in the within-host evolution of influenza using viral sequence data. PLoS Comput Biol. 2014;10: e1003755. doi: 10.1371/journal.pcbi.1003755 25080215

93. Redd AD, Mullis CE, Serwadda D, Kong X, Martens C, Ricklefs SM, et al. The Rates of HIV Superinfection and Primary HIV Incidence in a General Population in Rakai, Uganda. The Journal of Infectious Diseases. 2012. pp. 267–274. doi: 10.1093/infdis/jis325 22675216

94. Illingworth CJR. SAMFIRE: multi-locus variant calling for time-resolved sequence data. Bioinformatics. 2016;32: 2208–2209. doi: 10.1093/bioinformatics/btw205 27153641

95. Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genetical Research. 1974. p. 23. doi: 10.1017/s0016672300014634 4407212

96. Schwarz G. Estimating the Dimension of a Model. Ann Stat. 1978;6: 461–464.

97. Mansky LM. The mutation rate of human immunodeficiency virus type 1 is influenced by the vpr gene. Virology. 1996;222: 391–400. doi: 10.1006/viro.1996.0436 8806523

98. Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R. Viral Mutation Rates. J Virol. 2010;84: 9733–9748. doi: 10.1128/JVI.00694-10 20660197

99. Neher RA, Leitner T. Recombination rate and selection strength in HIV intra-patient evolution. PLoS Comput Biol. 2010;6: e1000660. doi: 10.1371/journal.pcbi.1000660 20126527

100. Batorsky R, Kearney MF, Palmer SE, Maldarelli F, Rouzine IM, Coffin JM. Estimate of effective recombination rate and average selection coefficient for HIV in chronic infection. Proc Natl Acad Sci U S A. 2011;108: 5661–5666. doi: 10.1073/pnas.1102036108 21436045

101. Markowitz M, Louie M, Hurley A, Sun E, Di Mascio M, Perelson AS, et al. A novel antiviral intervention results in more accurate assessment of human immunodeficiency virus type 1 replication dynamics and T-cell decay in vivo. J Virol. 2003;77: 5037–5038. doi: 10.1128/jvi.77.8.5037-5038.2003 12663814

102. Zhao L, Illingworth CJR. Measurements of intrahost viral diversity require an unbiased diversity metric. Virus Evol. 2019;5: vey041. doi: 10.1093/ve/vey041 30723551

103. Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B, Ning J, et al. Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature. 2013;497: 643–646. doi: 10.1038/nature12162 23719463

104. de la Peña AT, de la Peña AT, Rantalainen K, Cottrell CA, Allen JD, van Gils MJ, et al. Similarities and differences between native HIV-1 envelope glycoprotein trimers and stabilized soluble trimer mimetics. PLOS Pathogens. 2019. p. e1007920. doi: 10.1371/journal.ppat.1007920 31306470

105. Humphrey W, Dalke A, Schulten K. VMD: Visual molecular dynamics. Journal of Molecular Graphics. 1996. pp. 33–38. doi: 10.1016/0263-7855(96)00018-5 8744570


Článek vyšel v časopise

PLOS Pathogens


2020 Číslo 6

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×