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An application of population genetic theory to synonymous gene sequence evolution in the human immunodeficiency virus (HIV)

Published online by Cambridge University Press:  14 April 2009

John K. Kelly
John K. Kelly
Affiliation:
Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637
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A population genetic model is developed and then applied to the synonymous gene sequence variation observed in samples of the Human Immunodeficiency Virus Type 1 (HIV-1). The samples, which were taken from several previous studies, contain sequences of the envelope glycoprotein gene (gp 120) of HIV-1. This analysis suggests that the viral population within an infected patient at any specific time is likely to be composed of close relatives. The viruses in a sample are likely to share a recent common ancestor probably due to consistent positive selection for non-synonymous mutations coupled with low recombination in this region of the genome. There is no substantial difference in synonymous evolutionary rate between samples of sequences obtained from Peripheral Blood Mononucleate Cells (PBMCs) and samples taken from blood plasma. This is likely to be due to the high rate of migration between these 2 HIV sub-populations. The mutation rate for the genetic region examined is estimated at 9·20 × 10−4 per site per month. Under the assumptions of the estimation procedure, this estimate can be bounded between 8·50 and 9·91 × 10−4 with 95% confidence. When coupled with direct estimates of mutation rate, the rate of synonymous evolution suggests that the mean number of generations per month for HIV-1 in vivo is between 1 and 4.

Type
Research Article
Information
Genetics Research , Volume 64 , Issue 1 , August 1994 , pp. 1 - 9
Copyright
Copyright © Cambridge University Press 1994

References

Bakhanashvili, M., & Hizi, A., (1992). Fidelity of reverse transcriptase of human immunodeficiency virus type 2. FEBS. Letters 306, 151–156.CrossRefGoogle ScholarPubMed
Bakahanashvili, M., & Hizi, A., (1992). Fidelity of the RNA-dependent DNA synthesis exhibited by the reverse transcriptases of human immunodeficiency virus types 1 and 2 and of murine leukemia virus: mispair extension frequencies. Biochemistry 31, 9393–9398.CrossRefGoogle Scholar
Bakhanashvili, M., & Hizi, A., (1993). The fidelity of the reverse transcriptases of human immunodeficiency viruses and murine leukemia virus, exhibited by the mispair extension frequencies, is sequence dependent and enzyme related. FEBS Letters 319, 201–205.CrossRefGoogle ScholarPubMed
Balfe, P., Simmonds, P., Ludlam, C. A., Bishop, J. O., & Brown, A. J. L., (1990). Concurrent evolution of human immunodeficiency type 1 in patients infected from the same source: rate of sequence change and low frequency of inactivating mutations. Journal of Virology 64, 6221–6233.CrossRefGoogle ScholarPubMed
Charlesworth, B., Morgan, M., & Charlesworth, D., (1994). The effect of deleterious neutral mutations on neutral molecular evolution. Genetics (in the press).Google Scholar
Chesebro, B., Nishio, J., Perryman, S., Cann, A., O'Brien, W., Chen, I. S., & Wehrly, K., (1991). Identification of human immunodeficiency virus envelope gene sequences influencing viral entry in CD4 positive HeLa cells, Tleukemia cells, and macrophages. Journal of Virology 65, 5782–5789.CrossRefGoogle Scholar
Doi, H., (1991). Importance of purine and pyrimidine content of local nucleotide sequences (6 bases long) for evolution of the human immunodeficiency virus type 1. Proceedings of the National Academy of Sciences U.S.A. 88, 9282–9286.CrossRefGoogle ScholarPubMed
Fisher, A. G., Ensoli, B., Looney, D., Rose, A., Gallo, R. C., Saag, M. S., Shaw, G. M., Hahn, B. H., & Staal, F. Wong, (1988). Biologically diverse molecular variants within a single HIV-1 isolate. Nature 334, 444–447.CrossRefGoogle ScholarPubMed
Fouchier, R. A. M., Groenink, M., Kootstra, N. A., Tersmette, M., Huisman, G. H., Miedema, F., & Schuitemaker, H., (1992). Phenotype associated sequence variation in the third variable domain of the human immunodeficiency type 1 gp120 molecule. Journal of Virology 66, 3138.CrossRefGoogle ScholarPubMed
Hahn, B. H., Shaw, G. M., Taylor, M. E., Redfield, R. R., Markham, P. D., Salahuddin, S. Z., Wong-Stall, F., Gallo, R. C., Parks, E. S., & Parks, W., (1986). Genetic variation in HTLV-III/LAV over time in patients with AIDS or at risk for AIDS. Science 232, 1548–1553.CrossRefGoogle ScholarPubMed
Hill, W. G., & Robertson, A., (1966). The effects of linkage on the limits to artificial selection. Genetic Research 8, 269–294.CrossRefGoogle ScholarPubMed
Holmes, E. C., Zhang, L. Q., Simmonds, P., Ludlam, C. A., & Brown, A. J. L., (1992). Convergent and divergent sequence evolution in the surface envelope glycoprotein of human immunodeficiency virus type 1 within a single infected patient. Proceedings of the National Academy of Sciences U.S.A. 89, 4835–4839.CrossRefGoogle ScholarPubMed
Hwang, S. S., Boyle, T. J., Lyerly, H. K., & Cullen, B. R., (1991). Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 253, 71–74.CrossRefGoogle ScholarPubMed
Ji, J., & Loeb, L. A., (1992). Fidelity of HIV-1 reverse transcriptase in copying RNA in vitro. Biochemistry 31, 954–958.CrossRefGoogle ScholarPubMed
Kimura, M., (1969). The Number of Heterozygous Nucleotide Sites Maintained in a Finite Population due to Steady Flux of Mutations. Genetics 61, 893–903.CrossRefGoogle Scholar
Kreitman, M., (1991). Detecting selection at the level of DNA. In Evolution at the Molecular Level (ed. Selander, R. K., Clark, A. G., and Whittam, T. S.).Google Scholar
Looney, D. J., Fisher, A. G., Putney, S. D., Rusche, J. R., Redfield, R. R., Burke, S. D., Gallo, R. C., & Staal, F. Wong, (1988). Type restricted neutralization of molecular clones of HIV. Science 241, 357–359.CrossRefGoogle Scholar
MacKeating, J. A., Gow, J., Goudsmit, J., Pearl, L. H., Mulder, C., & Weiss, R., (1989). Characterisation of HIV- 1 neutralization escape mutants. AIDS 3, 777–784.CrossRefGoogle Scholar
Nowak, M. A., Anderson, R. M., & May, R. M., (1990). The evolutionary dynamics of HIV-1 quasispecies and the development of immunodeficiency disease. AIDS 4, 1095–1103.CrossRefGoogle ScholarPubMed
Nowak, M. A., Anderson, R. M., McLean, A. R., Wolfs, T. F. W., Goudsmit, J., & May, R. M., (1991). Antigenic diversity thresholds and the development of AIDS. Science 254, 963–969.CrossRefGoogle ScholarPubMed
Preston, B. D., Poiesz, B. J., & Loeb, L. A., (1988). Fidelity of HIV reverse transcriptase. Science 242, 1168–1171.CrossRefGoogle Scholar
Ricchetti, M., & Buc, H., (1990). Reverse transcriptases and genomic variability: the accuracy of DNA replication is enzyme specific and sequence dependent. EMBO Journal 9, 1583–1593.CrossRefGoogle ScholarPubMed
Roberts, J. D., Bebenek, K., & Kunkel, T. A., (1988). The accuracy of reverse transcriptase from HIV-1. Science 242, 1171–1173.CrossRefGoogle ScholarPubMed
Simmonds, P., Balfe, P., Ludlam, C. A., Bishop, J. O., & Brown, A. J. L., (1990). Analysis of sequence diversity in the hypervariable regions of the external glycoprotein of human immunodeficiency virus type 1. Journal of Virology 64, 5840–5850.CrossRefGoogle ScholarPubMed
Simmonds, P., Zhang, L. Q., McOmish, F., Balfe, P., Ludlam, C. A., & Brown, A. J. L., (1991). Discontinuous sequence change of human immunodeficiency virus (HIV) type 1 env sequences in plasma viral and lymphocyteassociated proviral populations in vivo: implications for models of HIV pathogenesis. Journal of Virology 65, 6266–6276.CrossRefGoogle ScholarPubMed
Tersmette, M., Gruers, R. A., de Wolf, F., de Groede, R. E., Lange, J. M., Schellekens, P. T., Goudsmit, J., Huisman, H. G., & Miedema, F., (1988). Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. Journal of Virology 63, 2118–2125.CrossRefGoogle Scholar
Weber, H., & Grosse, F., (1989). Fidelity of human immunodeficiency virus type 1 reverse transcriptase in copying natural RNA. Nucleic Acid Research 17, 1379–1393.CrossRefGoogle Scholar
Westervelt, P., Trowbridge, D. B., Epstein, L. G., Blumberg, B. M., Li, Y., Hahn, B. H., Shaw, G. M., Price, R. W., & Ratner, L., (1992). Macrophage tropism determinants of human immunodeficiency virus type 1 in vivo. Journal of Virology 66, 2577–2582.CrossRefGoogle Scholar
Wolfs, T. F. W., Zwart, G., Valk, M., Kuiken, C. L., & Goudsmit, J., (1991). Naturally occurring mutations Population genetics of HIV within HIV-1 V3 genomic RNA lead to antigenic variation dependent on a single amino acid substitution. Virology 185, 195–205.CrossRefGoogle ScholarPubMed
Wolinsky, S. M., Wike, C. M., Korber, B. T. M., Hutto, C., Parks, W. P., Rosenblum, L. A., Kunstman, K. J., Furtado, R., & Munoz, J. L., (1992). Selective transmission of human immunodeficiency virus type 1 variants from mothers to infants. Science 255, 1134–1137.CrossRefGoogle ScholarPubMed
Yu, H., & Goodman, M. F., (1992). Comparison of HIV-1 and avian myeloblastosis virus reverse transcriptase fidelity on RNA and DNA templates. Journal of Biological Chemistry 267, 10888–10896.CrossRefGoogle ScholarPubMed
Zhang, L. Q., MacKenzie, P., Cleland, A., Holmes, E. C., Brown, A. J. L., & Simmonds, P., (1993). Selection for specific sequences in the external envelope protein of human immunodeficiency virus type 1 upon primary infection. Journal of Virology 67, 3345–3356.CrossRefGoogle ScholarPubMed