1887

Abstract

Human immunodeficiency virus type 1 (HIV-1) infection is established by virus variants that use the CCR5 co-receptor for entry (CCR5-tropic or R5 variants), whereas viruses that use CXCR4 as co-receptor (CXCR4-tropic or X4 variants) emerge during disease progression in approximately 50 % of infected subjects. X4 variants may have a higher fitness and their detection is usually accompanied by faster T-cell depletion and the onset of AIDS in HIV-1-positive individuals. Here, the relationship between the sequence variation of the HIV-1 V3–V5 region and positive selective pressure on R5 and X4 variants from infected subjects with CD4 T cell counts below 200 cells μl was studied. A correlation was found between genetic distance and CD4 cell count at late stages of the disease. R5 variants that co-existed with X4 variants were significantly less heterogeneous than R5 variants from subjects without X4 variants (<0·0001). Similarly, X4 variants had a significantly higher diversity than R5 variants (<0·0001), although residues under positive selection had a similar distribution pattern in both variants. Therefore, both X4 and R5 variants were subjected to high selective pressures from the host. Furthermore, the interaction between X4 and R5 variants within the same subject resulted in a purifying selection on R5 variants, which only survived as a homogeneous virus population. These results indicate that R5 variants from X4 phenotype samples were highly homogeneous and under weakly positive selective pressures. In contrast, R5 variants from R5 phenotype samples were highly heterogeneous and subject to positive selective pressures.

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2006-05-01
2019-10-19
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References

  1. Asjo, B., Morfeldt-Manson, L., Albert, J., Biberfeld, G., Karlsson, A., Lidman, K. & Fenyo, E. M. ( 1986; ). Replicative capacity of human immunodeficiency virus from patients with varying severity of HIV infection. Lancet 2, 660–662.
    [Google Scholar]
  2. Balfe, P., Simmonds, P., Ludlam, C. A., Bishop, J. O. & Brown, A. J. ( 1990; ). Concurrent evolution of human immunodeficiency virus type 1 in patients infected from the same source: rate of sequence change and low frequency of inactivating mutations. J Virol 64, 6221–6233.
    [Google Scholar]
  3. Berger, E. A., Murphy, P. M. & Farber, J. M. ( 1999; ). Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17, 657–700.[CrossRef]
    [Google Scholar]
  4. Callaway, D. S., Ribeiro, R. M. & Nowak, M. A. ( 1999; ). Virus phenotype switching and disease progression in HIV-1 infection. Proc Biol Sci 266, 2523–2530.[CrossRef]
    [Google Scholar]
  5. Campbell, T. B., Schneider, K., Wrin, T., Petropoulos, C. J. & Connick, E. ( 2003; ). Relationship between in vitro human immunodeficiency virus type 1 replication rate and virus load in plasma. J Virol 77, 12105–12112.[CrossRef]
    [Google Scholar]
  6. Cheng-Mayer, C., Seto, D., Tateno, M. & Levy, J. A. ( 1988; ). Biologic features of HIV-1 that correlate with virulence in the host. Science 240, 80–82.[CrossRef]
    [Google Scholar]
  7. Collman, R. G. & Yi, Y. ( 1999; ). Cofactors for human immunodeficiency virus entry into primary macrophages. J Infect Dis 179, S422–S426.[CrossRef]
    [Google Scholar]
  8. Dorr, P., Westby, M., Dobbs, S. & 13 other authors ( 2005; ). Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broad-spectrum anti-human immunodeficiency virus type 1 activity. Antimicrob Agents Chemother 49, 4721–4732.[CrossRef]
    [Google Scholar]
  9. Fatkenheuer, G., Pozniak, A. L., Johnson, M. A. & 15 other authors ( 2005; ). Efficacy of short-term monotherapy with maraviroc, a new CCR5 antagonist, in patients infected with HIV-1. Nat Med 11, 1170–1172.[CrossRef]
    [Google Scholar]
  10. Fauci, A. S. ( 1996; ). Host factors in the pathogenesis of HIV disease. Antibiot Chemother 48, 4–12.
    [Google Scholar]
  11. Felsenstein, J. ( 1988; ). Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22, 521–565.[CrossRef]
    [Google Scholar]
  12. Glushakova, S., Grivel, J. C., Fitzgerald, W., Sylwester, A., Zimmerberg, J. & Margolis, L. B. ( 1998; ). Evidence for the HIV-1 phenotype switch as a causal factor in acquired immunodeficiency. Nat Med 4, 346–349.[CrossRef]
    [Google Scholar]
  13. Ibanez, A., Puig, T., Elias, J., Clotet, B., Ruiz, L. & Martinez, M. A. ( 1999; ). Quantification of integrated and total HIV-1 DNA after long-term highly active antiretroviral therapy in HIV-1-infected patients. AIDS 13, 1045–1049.[CrossRef]
    [Google Scholar]
  14. Ibanez, A., Clotet, B. & Martinez, M. A. ( 2001; ). Absence of genetic diversity reduction in the HIV-1 integrated proviral LTR sequence population during successful combination therapy. Virology 282, 1–5.[CrossRef]
    [Google Scholar]
  15. Jekle, A., Keppler, O. T., De Clercq, E., Schols, D., Weinstein, M. & Goldsmith, M. A. ( 2003; ). In vivo evolution of human immunodeficiency virus type 1 toward increased pathogenicity through CXCR4-mediated killing of uninfected CD4 T cells. J Virol 77, 5846–5854.[CrossRef]
    [Google Scholar]
  16. Jensen, M. A., Li, F.-S., van't Wout, A. B. & 7 other authors ( 2003; ). Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J Virol 77, 13376–13388.[CrossRef]
    [Google Scholar]
  17. Kimata, J. T., Kuller, L., Anderson, D. B., Dailey, P. & Overbaugh, J. ( 1999; ). Emerging cytopathic and antigenic simian immunodeficiency virus variants influence AIDS progression. Nat Med 5, 535–541.[CrossRef]
    [Google Scholar]
  18. Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M. ( 2001; ). mega2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.[CrossRef]
    [Google Scholar]
  19. Kwa, D., Vingerhoed, J., Boeser, B. & Schuitemaker, H. ( 2003; ). Increased in vitro cytopathicity of CC chemokine receptor 5-restricted human immunodeficiency virus type 1 primary isolates correlates with a progressive clinical course of infection. J Infect Dis 187, 1397–1403.[CrossRef]
    [Google Scholar]
  20. Lamers, S. L., Sleasman, J. W., She, J. X., Barrie, K. A., Pomeroy, S. M., Barrett, D. J. & Goodenow, M. M. ( 1993; ). Independent variation and positive selection in env V1 and V2 domains within maternal–infant strains of human immunodeficiency virus type 1 in vivo. J Virol 67, 3951–3960.
    [Google Scholar]
  21. Llano, A., Barretina, J., Blanco, J., Gutierrez, A., Clotet, B. & Este, J. A. ( 2001; ). Stromal-cell-derived factor 1 prevents the emergence of the syncytium-inducing phenotype of HIV-1 in vivo. AIDS 15, 1890–1892.[CrossRef]
    [Google Scholar]
  22. Mansky, L. M. & Temin, H. M. ( 1995; ). Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol 69, 5087–5094.
    [Google Scholar]
  23. Markham, R. B., Wang, W. C., Weisstein, A. E. & 8 other authors ( 1998; ). Patterns of HIV-1 evolution in individuals with differing rates of CD4 T cell decline. Proc Natl Acad Sci U S A 95, 12568–12573.[CrossRef]
    [Google Scholar]
  24. McDonald, R. A., Mayers, D. L., Chung, R. C., Wagner, K. F., Ratto-Kim, S., Birx, D. L. & Michael, N. L. ( 1997; ). Evolution of human immunodeficiency virus type 1 env sequence variation in patients with diverse rates of disease progression and T-cell function. J Virol 71, 1871–1879.
    [Google Scholar]
  25. Naif, H. M., Cunningham, A. L., Alali, M., Li, S., Nasr, N., Buhler, M. M., Schols, D., de Clercq, E. & Stewart, G. ( 2002; ). A human immunodeficiency virus type 1 isolate from an infected person homozygous for CCR5Delta32 exhibits dual tropism by infecting macrophages and MT2 cells via CXCR4. J Virol 76, 3114–3124.[CrossRef]
    [Google Scholar]
  26. Nei, M. & Gojobori, T. ( 1986; ). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3, 418–426.
    [Google Scholar]
  27. Ota, T. & Nei, M. ( 1994; ). Variance and covariances of the numbers of synonymous and nonsynonymous substitutions per site. Mol Biol Evol 11, 613–619.
    [Google Scholar]
  28. Page, R. D. M. ( 1996; ). treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357–358.
    [Google Scholar]
  29. Parera, M., Ibanez, A., Clotet, B. & Martinez, M. A. ( 2004; ). Lack of evidence for protease evolution in HIV-1-infected patients after 2 years of successful highly active antiretroviral therapy. J Infect Dis 189, 1444–1451.[CrossRef]
    [Google Scholar]
  30. Pierson, T., Hoffman, T. L., Blankson, J. & 7 other authors ( 2000; ). Characterization of chemokine receptor utilization of viruses in the latent reservoir for human immunodeficiency virus type 1. J Virol 74, 7824–7833.[CrossRef]
    [Google Scholar]
  31. Rizzuto, C. & Sodroski, J. ( 2000; ). Fine definition of a conserved CCR5-binding region on the human immunodeficiency virus type 1 glycoprotein 120. AIDS Res Hum Retroviruses 16, 741–749.[CrossRef]
    [Google Scholar]
  32. Schuitemaker, H., Koot, M., Kootstra, N. A. & 7 other authors ( 1992; ). 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 66, 1354–1360.
    [Google Scholar]
  33. Shankarappa, R., Margolick, J. B., Gange, S. J. & 9 other authors ( 1999; ). Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virol 73, 10489–10502.
    [Google Scholar]
  34. Shiino, T., Kato, K., Kodaka, N., Miyakuni, T., Takebe, Y. & Sato, H. ( 2000; ). A group of V3 sequences from human immunodeficiency virus type 1 subtype E non-syncytium-inducing, CCR5-using variants are resistant to positive selection pressure. J Virol 74, 1069–1078.[CrossRef]
    [Google Scholar]
  35. Stalmeijer, E. H., Van Rij, R. P., Boeser-Nunnink, B., Visser, J. A., Naarding, M. A., Schols, D. & Schuitemaker, H. ( 2004; ). In vivo evolution of X4 human immunodeficiency virus type 1 variants in the natural course of infection coincides with decreasing sensitivity to CXCR4 antagonists. J Virol 78, 2722–2728.[CrossRef]
    [Google Scholar]
  36. Templeton, A. R., Reichert, R. A., Weisstein, A. E., Yu, X. F. & Markham, R. B. ( 2004; ). Selection in context: patterns of natural selection in the glycoprotein 120 region of human immunodeficiency virus 1 within infected individuals. Genetics 167, 1547–1561.[CrossRef]
    [Google Scholar]
  37. Tersmette, M., Gruters, R. A., de Wolf, F., de Goede, R. E., Lange, J. M., Schellekens, P. T., Goudsmit, J., Huisman, H. G. & Miedema, F. ( 1989; ). Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. J Virol 63, 2118–2125.
    [Google Scholar]
  38. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal_w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  39. Troyer, R. M., Collins, K. R., Abraha, A. & 9 other authors ( 2005; ). Changes in human immunodeficiency virus type 1 fitness and genetic diversity during disease progression. J Virol 79, 9006–9018.[CrossRef]
    [Google Scholar]
  40. van't Wout, A. B., Blaak, H., Ran, L. J., Brouwer, M., Kuiken, C. & Schuitemaker, H. ( 1998; ). Evolution of syncytium-inducing and non-syncytium-inducing biological virus clones in relation to replication kinetics during the course of human immunodeficiency virus type 1 infection. J Virol 72, 5099–5107.
    [Google Scholar]
  41. Wolfs, T. F., de Jong, J. J., Van den Berg, H., Tijnagel, J. M., Krone, W. J. & Goudsmit, J. ( 1990; ). Evolution of sequences encoding the principal neutralization epitope of human immunodeficiency virus 1 is host dependent, rapid, and continuous. Proc Natl Acad Sci U S A 87, 9938–9942.[CrossRef]
    [Google Scholar]
  42. Wolinsky, S. M., Korber, B. T., Neumann, A. U. & 7 other authors ( 1996; ). Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 272, 537–542.[CrossRef]
    [Google Scholar]
  43. Xiao, H., Neuveut, C., Tiffany, H. L., Benkirane, M., Rich, E. A., Murphy, P. M. & Jeang, K. T. ( 2000; ). Selective CXCR4 antagonism by Tat: implications for in vivo expansion of coreceptor use by HIV-1. Proc Natl Acad Sci U S A 97, 11466–11471.[CrossRef]
    [Google Scholar]
  44. Yang, Z. ( 1997; ). paml: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13, 555–556.
    [Google Scholar]
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