Relaxation of Adaptive Evolution During the HIV-1 Infection Owing to Reduction of CD4+ T Cell Counts

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2012 Jul 7

PMID 22768122

Citations 3

Authors

Elcio Leal

Jorge Casseb

Michael Hendry

Michael P Busch

Ricardo Sobhie Diaz

Affiliations

Soon will be listed here.

Abstract

Background: The first stages of HIV-1 infection are essential to establish the diversity of virus population within host. It has been suggested that adaptation to host cells and antibody evasion are the leading forces driving HIV evolution at the initial stages of AIDS infection. In order to gain more insights on adaptive HIV-1 evolution, the genetic diversity was evaluated during the infection time in individuals contaminated by the same viral source in an epidemic cluster. Multiple sequences of V3 loop region of the HIV-1 were serially sampled from four individuals: comprising a single blood donor, two blood recipients, and another sexually infected by one of the blood recipients. The diversity of the viral population within each host was analyzed independently in distinct time points during HIV-1 infection.

Results: Phylogenetic analysis identified multiple HIV-1 variants transmitted through blood transfusion but the establishing of new infections was initiated by a limited number of viruses. Positive selection (d(N)/d(S)>1) was detected in the viruses within each host in all time points. In the intra-host viruses of the blood donor and of one blood recipient, X4 variants appeared respectively in 1993 and 1989. In both patients X4 variants never reached high frequencies during infection time. The recipient, who X4 variants appeared, developed AIDS but kept narrow and constant immune response against HIV-1 during the infection time.

Conclusion: Slowing rates of adaptive evolution and increasing diversity in HIV-1 are consequences of the CD4+ T cells depletion. The dynamic of R5 to X4 shift is not associated with the initial amplitude of humoral immune response or intensity of positive selection.

Citing Articles

Is the tryptophan codon of gene vif the Achilles' heel of HIV-1?.

Villanova F, Barreiros M, Leal E PLoS One. 2020; 15(6):e0225563.

PMID: 32570272 PMC: 7308096. DOI: 10.1371/journal.pone.0225563.

HIV N-linked glycosylation site analyzer and its further usage in anchored alignment.

Shaw T, Zhang M Nucleic Acids Res. 2013; 41(Web Server issue):W454-8.

PMID: 23748959 PMC: 3692120. DOI: 10.1093/nar/gkt472.

Codon pairs of the HIV-1 vif gene correlate with CD4+ T cell count.

Bizinoto M, Yabe S, Leal E, Kishino H, de Oliveira Martins L, de Lima M BMC Infect Dis. 2013; 13:173.

PMID: 23578255 PMC: 3637627. DOI: 10.1186/1471-2334-13-173.

References

Milne I, Wright F, Rowe G, Marshall D, Husmeier D, McGuire G . TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics. 2004; 20(11):1806-7. DOI: 10.1093/bioinformatics/bth155. View

Diaz R, Zhang L, Busch M, Mosley J, Mayer A . Divergence of HIV-1 quasispecies in an epidemiologic cluster. AIDS. 1997; 11(4):415-22. DOI: 10.1097/00002030-199704000-00003. View

English S, Katzourakis A, Bonsall D, Flanagan P, Duda A, Fidler S . Phylogenetic analysis consistent with a clinical history of sexual transmission of HIV-1 from a single donor reveals transmission of highly distinct variants. Retrovirology. 2011; 8:54. PMC: 3161944. DOI: 10.1186/1742-4690-8-54. View

Leal E, Silva W, Sucupira M, Janini L, Diaz R . Molecular and structural characterization of HIV-1 subtype B Brazilian isolates with GWGR tetramer at the tip of the V3-loop. Virology. 2008; 381(2):222-9. DOI: 10.1016/j.virol.2008.08.029. View

Wei X, Decker J, Wang S, Hui H, Kappes J, Wu X . Antibody neutralization and escape by HIV-1. Nature. 2003; 422(6929):307-12. DOI: 10.1038/nature01470. View

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

Bunnik E, Quakkelaar E, van Nuenen A, Boeser-Nunnink B, Schuitemaker H . Increased neutralization sensitivity of recently emerged CXCR4-using human immunodeficiency virus type 1 strains compared to coexisting CCR5-using variants from the same patient. J Virol. 2006; 81(2):525-31. PMC: 1797458. DOI: 10.1128/JVI.01983-06. View

Dacheux L, Moreau A, Ataman-Onal Y, Biron F, Verrier B, Barin F . Evolutionary dynamics of the glycan shield of the human immunodeficiency virus envelope during natural infection and implications for exposure of the 2G12 epitope. J Virol. 2004; 78(22):12625-37. PMC: 525068. DOI: 10.1128/JVI.78.22.12625-12637.2004. View

Cicala C, Arthos J, Martinelli E, Censoplano N, Cruz C, Chung E . R5 and X4 HIV envelopes induce distinct gene expression profiles in primary peripheral blood mononuclear cells. Proc Natl Acad Sci U S A. 2006; 103(10):3746-51. PMC: 1533779. DOI: 10.1073/pnas.0511237103. View

10.

Williamson S . Adaptation in the env gene of HIV-1 and evolutionary theories of disease progression. Mol Biol Evol. 2003; 20(8):1318-25. DOI: 10.1093/molbev/msg144. View

11.

Lusso P, Earl P, Sironi F, Santoro F, Ripamonti C, Scarlatti G . Cryptic nature of a conserved, CD4-inducible V3 loop neutralization epitope in the native envelope glycoprotein oligomer of CCR5-restricted, but not CXCR4-using, primary human immunodeficiency virus type 1 strains. J Virol. 2005; 79(11):6957-68. PMC: 1112133. DOI: 10.1128/JVI.79.11.6957-6968.2005. View

12.

Frost S, Wrin T, Smith D, Kosakovsky Pond S, Liu Y, Paxinos E . Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci U S A. 2005; 102(51):18514-9. PMC: 1310509. DOI: 10.1073/pnas.0504658102. View

13.

Koot M, Schellekens P, Mulder J, Lange J, Roos M, Coutinho R . Viral phenotype and T cell reactivity in human immunodeficiency virus type 1-infected asymptomatic men treated with zidovudine. J Infect Dis. 1993; 168(3):733-6. DOI: 10.1093/infdis/168.3.733. View

14.

Leal E, Janini M, Diaz R . Selective pressures of human immunodeficiency virus type 1 (HIV-1) during pediatric infection. Infect Genet Evol. 2007; 7(6):694-707. DOI: 10.1016/j.meegid.2007.07.008. View

15.

Herbeck J, Nickle D, Learn G, Gottlieb G, Curlin M, Heath L . Human immunodeficiency virus type 1 env evolves toward ancestral states upon transmission to a new host. J Virol. 2006; 80(4):1637-44. PMC: 1367147. DOI: 10.1128/JVI.80.4.1637-1644.2006. View

16.

Fouchier R, Groenink M, Kootstra N, Tersmette M, Huisman H, Miedema F . Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J Virol. 1992; 66(5):3183-7. PMC: 241084. DOI: 10.1128/JVI.66.5.3183-3187.1992. View

17.

Huelsenbeck J, Ronquist F . MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17(8):754-5. DOI: 10.1093/bioinformatics/17.8.754. View

18.

de S Leal E, Holmes E, Zanotto P . Distinct patterns of natural selection in the reverse transcriptase gene of HIV-1 in the presence and absence of antiretroviral therapy. Virology. 2004; 325(2):181-91. DOI: 10.1016/j.virol.2004.04.004. View

19.

Zhang M, Gaschen B, Blay W, Foley B, Haigwood N, Kuiken C . Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology. 2004; 14(12):1229-46. DOI: 10.1093/glycob/cwh106. View

20.

Schuitemaker H, Koot M, Kootstra N, Dercksen M, de Goede R, van Steenwijk R . Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J Virol. 1992; 66(3):1354-60. PMC: 240857. DOI: 10.1128/JVI.66.3.1354-1360.1992. View