On the origin and evolution of the human immunodeficiency virus (HIV)

Biological Reviews of the Cambridge Philosophical Society

Volumn 76, Issue 2, 2001, Pages 239-254

  Holmes, Edward C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

AIDS; Epidemiology; Evolution; HIV; Phylogeny; Primates; Tropism; Virulence; Zoonosis

Indexed keywords

CHIMPANZEE; EVOLUTION; GENETIC DRIFT; GENETIC VARIABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; NONHUMAN; PRIMATE; REVIEW; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIES DIFFERENTIATION; STRAIN DIFFERENCE; VIRUS CHARACTERIZATION; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANIMALS; EVOLUTION, MOLECULAR; HIV INFECTIONS; HIV-1; HIV-2; HUMANS; PHYLOGENY; PRIMATES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRULENCE; ZOONOSES;

AIDS VIRUS; ANIMALIA; CERCOCEBUS TORQUATUS ATYS; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; PAN TROGLODYTES; PRIMATES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0035007987     PISSN: 14647931     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1464793101005668     Document Type: Review

References (97)

1. ANDERSON, J. P., Rodrigo, A. G., LEARN, G. H., MADAN, A., DELAHUNTY, C., COON, M., GIRARD, M., OSMANOV, S., HOOD, L. & MULLINS, J. I. (2000). Testing the hypothesis of a recombinant origin of human immunodeficiency virus type 1 subtype E. Journal of Virology 74, 10752-10765.
2. ANDERSON, R. M. & MAY, R. M. (1991). Infectious Diseases of Humans. Oxford University Press, Oxford, U.K.
3. ANDERSON, R. M. & MAY, R. M. (1996). The population biology of the interaction between HIV-1 and HIV-2: coexistence or competitive exclusion? AIDS 10, 1663-1673.
4. BAIER, M., DITTMAR, M. T., CICHUTEK, K. & KURTH, R. (1991). Development in vivo of genetic variability of simian immunodeficiency virus. Proceedings of the National Academy of Sciences USA 88, 8126-8130.
5. BARRÉ-SINOUSSI, F., CHERMANN, J. C., REY, F., NUGEYTRE, M. T., CHAMARET, S., GRUEST, J., DAUGUET, C., AXLER-BLUE, C., VEZINET-BRUN, F., ROUZIOUX, C., ROZENBAUM, W. & MONTAGNIER, L. (1983). Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220, 868-871.
6. BEER, B. E., BAILES, E., GOEKEN, R., DAPOLITO, G., COULIBALY, C., NORLEY, S. G., KURTH, B., GAUTIER, J.-P., GAUTIER-HION, A., VALLET, D., SHARP, P. M. & HIRSCH, V. M. (1999). Simian immunodeficiency virus (SIV) from sun-tailed monkeys (Ceropithecus solatus): evidence for host-dependent evolution of SIV within the C. Ihoesti supersperies. Journal of Virology 73, 7734-7744.
7. BIBOLLET-RUCHE, F., GALAT-LUONG, A., CUNY, G., SARNI-MANCHADO, P., GALAT, G., DURAND, J. P., POURRUT, X. & VEAS, F. (1996). Simian immunodeficiency virus infection in a patas monkey (Erythrocebus patas): evidence for cross-species transmission from African green monkeys (Cercopithecus aethiops sabaeus) in the wild. Journal of General Virology 77, 773-781.
8. BJORNDAL, A., DENG, H., JANSSON, M., FIORE , J. R., COLOGNESI, C., KARLSSON, A., ALBERT, J., SCARLATTI, G., LITTMAN, D. R. & FENYO, E. M. (1997). Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. Journal of Virology 71, 7478-7487.
9. BLATTNER, W. A., O'BRIEN, T. R. & MUELLER, N. E. (1997). Retroviruses - Human Immunodeficiency Virus. In Viral Infections of Humans: Epidemiology and Control 4th Edition (ed. A. S. Evans & R. A. Kaslowi), pp. 713-783. Plenum Medical Book Company, New York.
10. BONHOEFFER, S., HOLMES, E. C. & NOWAK, M. A. (1995). Causes of HIV diversity, Nature 376, 125.
11. BONHOEFFER, S. & NOWAK, M. A. (1994). Intra-host versus inter-host selection: viral strategies of immune function impairment. Proceedings of the National Academy of Sciences USA 91, 8062-8066.
12. BORROW, P., LEWIKI, H., WEI, X., HORWITZ, M. S., PEFFER, N., MEYERS, H., NELSON, J. A., GAIRIN, J. E., HAHN, B. H., OLDSTONE, M. B. A. & SHAW, G. M. (1997). Antiviral pressure exerted by HIV-1 specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nature Medicine 3, 205-211.
13. CALLAWAY, D.S., RIBEIRO, R. M. & NOWAK, M. A. (1999). Virus phenotype switching and disease progression in HIV-1 infection. Proceedings of the Royal Society of London series B 266, 2523-2530.
14. CHEN, Z., GETTIE, A., HO, D. D. & MARX, P.A. (1998). Primary SIVsm isolates use the CCR5 coreceptor from sooty mangabeys naturally infected in west Africa: a comparison of coreceptor usage of primary SIVsm, HIV-2, and SIVmac. Virology 246, 113-124.
15. CHEN, Z., TELFIER, P., GETTIE, A., REED, P., ZHANG, E. Q., HO, D. D. & MARX, P. A. (1996). Genetic characterization of new West African simian immunodeficiency virus SIVsm: geographic clustering of household-derived SIV strains with human immunodeficiency virus type 2 subtypes and genetically diverse viruses from a single feral sooty mangabey troop. Journal of Virology 70, 3617-3627.
16. CHESEBRO, B., WEHRLY, K., NISHIO, J. & PERRYMAN, S. (1992). Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual Y3 envelope sequence homogeneity in comparison with T-cell tropic isolates: definition of critical amino acids involved in cell tropism. Journal of Virology 66, 6547-6554.
17. CORBET, S., MÜLLER-TRUTWIN, M. C., VERSMISSE, P., DELARUE, S., AYOUBA, A., LEWIS, J., BRUNAK, S., MARTIN, P., BRUN-VEZINET, F., SIMON, F., BARRÉ-SINOUSSI, F. & MAUCLERE, P. (2000). env sequences of simian immunodeficiency viruses from chimpanzees in Cameroon are strongly related to those of human immunodeficiency virus group N from the same geographic area. Journal of Virology 74, 529-534.
18. COURGNAUD, V., SAURIN, W., VILLINGER, F. & SONIGO, P. (1998). Different evolution of simian immunodeficiency virus in a natural host and a new host. Virology 247, 41-50.
19. DEAN, M., CARRINGTON, M., WINKLER, C., HUTTLEY, G. A., SMITH, M. W., ALLIKMETS, R., GOEDERT, J. J., BUCHBINDER, S. P., VITTINGHOFF, E., GOMPERTS, E., DONFIELD, S., VLAHOV, D., KASLOW, R., SAAH, A., RINALDO, C., DETELS, R., HEMOPHILIA GROWTH AND DEVELOPMENT STUDY, MULTICENTER AIDS COHORT STUDY, MULTICENTER HEMOPHILIA COHORT STUDY, SAN FRANCISCO CITY COHORT, ALIVE STUDY & O'BRIEN, S. J. (1996). Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science 273, 1856-1862.
20. DELWART, E. L., PAN, H., SHEPPARD, H. W., WOLPERT, D., NEUMANN, A. U., KORBER, B. & MULLINS J. I. (1997). Slower evolution of human immunodeficiency virus type 1 quasispecies during progression to AIDS. Journal of Virology 71, 7498-7508.
21. DIAZ, R. S., SABINO, E. C., MAYER, A., MOSLEY., J. W. & BUSCH, M. P. (1995). Dual human immunodeficiency virus type 1 infection in a dually exposed transfusion recipient. Journal of Virology 69, 3273-3281.
22. DRAKE, J. W. (1993). Rates of spontaneous mutation among RNA viruses. Proceedings of the National Academy of Sciences USA 90, 4171-4175.
23. EDINGER, A. L., AMEDEE, A., MILLER, K., DORANZ, B. J., ENDRES, M., SHARRON, M., SAMSON, M., LU, Z.-H., CLEMENTS, J. E., MURPHEY-CORB, M., PEIPER, S. C., PARMENTIER, M., BRODER, C. C. & DOMS, R. W. (1997). Differential utilization of CCR5 by macrophage and T cell tropic simian immunodeficiency virus strains. Proceedings of the National Academy of Sciences USA 94, 4005-4010.
24. EICKBUSH, T. H. (1994). Origin and evolutionary relationships of retroelements. In The Evolutionary Biology of Viruses (ed. S. S. Morse), pp. 121-157. Raven Press, New York.
25. EWALD, P. W. (1999). Evolutionary control of HIV and other sexually transmitted diseases. In Evolutionary Medicine (ed. W. R. Trevathan, E. O. Smith & J. J. McKenna), pp. 271-311. Oxford University Press, New York.
26. FELSENSTEIN, J. (1993). PHYLIP (Phylogeny Inference Package) Version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle.
27. GAGNEUX, P., WILLS, C., GERLOFF, U., TAUTZ, D., MORIN, P. A., BOESCH, C., FRUTH, B., HOHMANN, G., RYDER, O. A. & WOODRUFF, D. S. (1999). Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proceedings of the National Academy of Sciences USA 96, 5077-5082.
28. GAO, F., BAILES, E., ROBERTSON, D. L., CHEN, Y., RODENBURG, C. M., MICHAEL, S. F., CUMMINS, L. B., ARTHUR, L. O., PEETERS, M., SHAW, G. M., SHARP, P. M. & HAHN, B. H. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397, 436-441.
29. GAO, F., ROBERTSON, D. L., CARRUTHERS, C. D., LI, Y. Y., BAILES, E., KOSTRIKIS, L. G., SALMINEN, M. O., BIBOLLET-RUCHE, F., PEETERS, M., HO, D. D., SHAW, G. M., SHARP, P. M. & HAHN, B. H. (1998). An isolate of human immunodeficiency virus type 1 originally classified as subtype I represents a complex mosaic comprising three different group M subtypes (A, G and I). Journal of Virology 72, 10234-10241.
30. GEORGES-COURBOT, M. C., MOISSON, P., LEROY, E., PINGARD, A. M., NERRIENET, E., DUBREUIL, G., WICKINGS, E. J., DEBELS, F., BEDJABAGA, I., POATY-MAVOUNGOU, V., HAHN, N. T. & GEORGES, A. J. (1996). Occurrence and frequency of transmission of naturally occurring simian retroviral infections (SIV, STLV, and SRV) at the CIRMF Primate Center, Gabon. Journal of Medical Primatology 25, 313-326.
31. GOUDSMIT, J., DE RONDE, A., HO, D. D. & PERELSON, A. S. (1996). Human immunodeficiency virus in vivo: calculations based on a single zidovudine resistance mutation at codon 215 of reverse transcriptase. Journal of Virology 70, 5662-5664.
32. GOULDER, P. J. R., PHILLIPS, R. E., COLBERT, R. A., MCADAM, S., OGG, G., NOWAK, M. A., GIANGRANDE, P., LUZZI, G., MORGAN, B., EDWARDS, A., MCMICHAEL, A. J. & ROWLAND-JONES, S. (1997). Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nature Medicine 3, 212-217.
33. HAHN, B. H., SHAW, G. M., DE COCK, K. M. & SHARP, P. M. (2000). AIDS as a zoonosis: scientific and public health implications. Science 287, 607-614.
34. HALAPI, E., LEITNER, T., JANSSON, M., SCARLATTI, G., ORLANDI, P., PLEBANI, A., ROMITI, L., ALBERT, J., WIGZELL, H. & ROSSI, P. (1997). Correlation between HIV sequence evolution, specific immune response and clinical outcome in vertically infected infants. AIDS 11, 1709-1717.
35. HEYNDRICKX, L., JANSSENS, W., ZEKENG, L., MUSONDA, R., ANAGONOU, S., YAN DER AUWERA, G., COPPENS, S., VEREECKEN, K., DE WITTE, K., VAN RAMPELBERGH, R., KAHINDO, M., MORISON, L., MCCUTCHAN, F. E., CARR, J. K., ALBERT, J., ESSEX, M., GOUDSMIT, J., ASJO, B., SALMINEN, M., BUVE, A. & VAN DER GROEN, G. (2000). Simplified strategy for detection of recombinant human immunodeficiency virus type 1 group M isolates by gag/env heteroduplex mobility assay. Journal of Virology, 74, 363-370.
36. HIRSCH, V. M., DAPOLITO, G., JOHNSON, P. R., ELKINS, W. R., LONDON, W. T., MONTALI, R. J., GOLDSTEIN, S. & BROWN, C. (1995). Induction of AIDS by simian immunodeficiency virus from an African green monkey: species-specific variation in pathogenicity correlates with the extent of in vivo replication. Journal of Virologry 69, 955-967.
37. HO, D. D. (1998). Toward HIV eradication or remission: the tasks ahead. Science 280, 1866-1867.
38. HOLMES, E. C., ZHANG, L. Q., SIMMONDS, P., LUDLAM, C. A. & LEIGH BROWN, A.J. (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 USA 89, 4835-4839.
39. HOOPER, E. (1999). The River. A Journey Back to the Source of HIV and AIDS. Allen Lane, The Penguin Press, U.K.
40. HU, W. S. & TEMIN, H. M. (1990). Genetic consequences of packing two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proceedings of the National Academy of Sciences USA 87, 1556-1560.
41. HU, X., MARGOLIS, H. S., PURCELL, R. H., EBERT, J. & ROBERTSON, B. H. (2000). Identification of hepatitis B virus indigenous to chimpanzees. Proceedings of the National Academy of Sciences USA 97, 1661-1664.
42. HUANG, Y., PAXTON, W. A., WOLINSKY, S. M., NEUMANN, A. U., ZHANG, L. Q., HE, T., KANG, S., CERADINI, D., JIN, Z., YAZDANBAKHSH, K., KUNSTMAN, K., ERICKSON, D., DRAGON, E., LANDAU, N. R., PHAIR, J., HO, D. D. & KOUP, R. A. (1996). The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nature Medicine 2, 1240-1247.
43. JACQUEZ, J. A., KOOPMAN, J. S., SIMON, C. P. & LONGINI, I. M. JNR. (1994). Role of the primary infection in epidemics of HIV infection in gay cohorts. Journal of Acquired Immunodeficiency Syndromes 7, 1169-1184.
44. JETZT, A. E., YU, H., KLARMANN, G. J., RON, Y., PRESTON, B. D. & DOUGHERTY, J. P. (2000). High rate of recombination throughout the human immunodeficiency virus type 1 genome. Journal of Virology 74, 1234-1240.
45. JIN, M. J., HUI, H., ROBERTSON, D. L., MÜLLER, M. C., BARRÉ-SINOUSSI, F., HIRSCH, V. M., ALLAN, J. S., SHAW, G. M., SHARP, P.M. & HAHN, B. H. (1994a). Mosaic genome structure of simian immunodeficiency virus from West African green monkeys. EMBO Journal 13, 2935-2947.
46. JIN, M. J., ROGERS, J., PHILLIPS-CONROY, J. E., ALLAN, J. S., DESROSIERS, R. C., SHAW, G. M., SHARP, P. M. & HAHN, B. H. (1994b). Infection of a yellow baboon with simian immunodeficiency virus from African green monkeys: evidence for cross-species transmission in the wild. Journal of Virology 68, 8454-8460.
47. JONASSEN, T. Ø., STENE-JOHANSON, K., BERG, E. S., HUNGES, O., LINDBOE, C. F., FRøLAND, S. S. & GRINDE, B. (1997). Sequence analysis of HIV-1 group O from Norwegian patients infected in the 1960s. Virology 231, 43-47.
48. KANKI, P.J., TRAVERS, K. U., M'BOUP, S., HSIEH, C. C., MARLINK, R. G., GUEYE-NDIAYE, A., SIBY, T., THIOR, I., HERNANDEZ-AVILA, M., SANKALÉ, J. L., NDOYE, I. & ESSEX, M. (1994). Slower heterosexual spread of HIV-2 than HIV-1. Lancet 343, 943-946.
49. KIRCHHOFF, F., GREENOUGH, T. C., BRETTLER, D. B., SULLIVAN, J. E. & DESROSIERS, R. G. (1995). Absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. New England Journal of Medicine 332, 228-232.
50. KORBER, B., MULDOON, M., THEILER, J., GAO, F., GUPTA, R., LAPEDES, A., HAHN, B. H., WOLINKSY, S. & BHATTACHARYA, T. (2000). Timing the ancestor of the HIV-1 pandemic strains. Science 288, 1789-1796.
51. KORBER, B. T., SHARP, P. M. & HO, D. D. (1999). Dating the origin of HIY-1 subtypes. Nature 400, 326.
52. KOSTRIKIS, L. G., HUANG, Y., MOORE, J. P., WOLINSKY, S. M., ZHANG, L. Q., GUO, Y., DEUTSCH, L., PHAIR, J., NEUMANN, A. U. & HO, D. D. (1998). A chemokine receptor CCR2 allele delays HIV-1 disease progression and is associated with a CCR5 promoter mutation. Nature Medicine 4, 350-353.
53. KROODSMA, K. E., KOZAL, M. J., HAMED, K. A., WINTERS, M. A. & MERIGAN, T. C. (1994). Detection of drug resistance mutations in the human immunodeficiency virus type 1 (HIV-1) pol gene: differences in semen and blood HIV-1 RNA and proviral DNA. Journal of Infectious Diseases 170, 1292-1295.
54. LARDER, B. A. & KEMP, S. D. (1989). Multiple mutations in HIY-1 reverse transcriptase confer high-level resistance to Zidovudine (AZT). Science 246, 1155-1158.
55. LEIGH BROWN, A. J. (1997). Analysis of HIY-1 env gene sequences reveals evidence for a low effective number in the viral population. Proceedings National Academy of Sciences USA 94, 1862-1865.
56. LEIGH BROWN, A.J. & RICHMAN, D.D. (1997). HIY-1: Gambling on the evolution of drug resistance? Nature Medicine 3, 268-271.
57. LEVIN, B. R. & BULL, J. J. (1994). Short-sighted evolution and the virulence of pathogenic micro-organisms. Trends in Microbiology 2, 76-81.
58. LEVIN, B. R., LIPSITCH, M. & BONHOEFFER, S. (1999). Evolution and disease - population biology, evolution, and infectious disease: convergence and synthesis. Science 283, 806-809.
59. LI, W.-H., TANIMURA, M. & SHARP, P. M. (1988). Rates and dates of divergence between AIDS virus nucleotide sequences. Molecular Biology and Evolution 5, 313-330.
60. LIU, S.-L., SCHACKER, T., MUSEY, L., SHRINER, D., MCELRATH, M. J., COREY, L. & MULLINS, J. I. (1997). Divergent patterns of progression to AIDS after infection from the same source: human immunodeficiency virus type 1 evolution and antiviral responses. Journal of Virology 71, 4284-4295.
61. MACDONALD, D. M., HOLMES, E. C., LEWIS, J. C. M. & SIMMONDS, P. (2000). Detection of hepatitis B virus infection in wild caught chimpanzees (Pan troglodytes verus); phylogenetic relationships with human and other primate genotypes. Journal of Virology 74, 4253-4257.
62. MARKHAM, R. B., WANG, W.-C., WEISSTEIN, A. E., WANG, Z., MUNOZ, A., TEMPLETON, A., MARGOLICK, J., VLAHOV, D., QUINN, T., FARZADEGAN, H. & YU, X.-F. (1998). Patterns of HIY-1 evolution in individuals with differing rates of CD4 T cell decline. Proceedings National Academy of Sciences USA 95, 12568-12573.
63. MCMICHAEL, A. J. & PHILLIPS, R. E. (1997). Escape of human immunodeficiency virus from immune control. Annual Reviews of Immunology 15, 271-296.
64. MELLORS, J. W., RINALDO, C. R. JNR., GUPTA, P., WHITE, R. M., TODD, J. A. & KINGSLEY, L. A. (1996). Prognosis of HIV-1 infection predicted by the quantity of virus in plasma. Science 272, 1167-1170.
65. MOUTOUH, L., GORBEIL, J. & RICHMAN, D. D. (1996). Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure. Proceedings National Academy of Sciences USA 93, 6106-6111.
66. MULDER, D. W., NUNN, A. J., KAMALI, A., NAKIYINGI, J., WAGNER, H. U. & KENGEYA-KAYONDO, J. F. (1994). Two-year HIV-1 associated mortality in a Ugandan rural population. Lancet 343, 1021-1023.
67. MÜLLER-TRUTWIN, M. C., GORBET, S., DIAS TAVARES, M., HERVÉ, V. M. A., NERRIENET, E., GEORGES-COURBOT, M.-C., SAURIN, W., SONIGO, P. & BARRÉ-SINOUSSI, F. (1996). The evolutionary rate of nonpathogenic simian immunodeficiency virus (SIVagm) is in agreement with a rapid and continuous replication in vivo. Virology 223, 89-102.
68. MUSEY, L., HU, Y., ECKERT L., CHRISTENSEN, M., KARCHMER, T. & MCELRATH, M. J. (1997). HIV-1 induces cytotoxic T lymphocytes in the cervix of infected women. Journal of Experimental Medicine 185, 293-303.
69. NIJHUIS, M., BOUCHER, C. A. B., SCHIPPER, P., LEITNER, T., SCHUURMAN, R. & ALBERT, J. (1998). Stochastic processes strongly influence protease-inhibitor therapy. Proceedings National Academy of Sciences USA 95, 14441-14446.
70. NOWAK, M. & BANGHAM, C. R. M. (1996). Population dynamics of immune responses to persistent viruses. Science 272, 74-79.
71. OGG, G. S., JIN, X., BONHOEFFER, S., DUNBAR, P. R., NOWAK, M. A., MONARD, S., SEGAL, J. P., CAO, Y., ROWLAND-JONES, S. L., CERUNDOLO, V., HURLEY, A., MARKOWITZ, A., HO, D. D., NIXON, D. F. & MCMICHAEL, A. J. (1998). Quantitation of HIV-1 specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279, 2103-2106.
72. PERELSON, A. S., NEUMANN, A. U., MARKOWITZ, M., LEONARD, J. M. & HO, D. D. (1996). HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271, 1582-1586.
73. PEETERS, M., VINCENT, R., PERRET, J. L., LASKY, M., PATREL, D., LIEGEOIS, F., COURGNAUD, V., SENG, R., MATTON, T., MOLINIER, S. & DELAPORTE, E. (1999). Evidence for differences in MT2 cell tropism according to genetic subtypes of HIV-1: syncytium-inducing variants seem rare among subtype C HIV-1 viruses. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology 20, 115-121.
74. PRICE, D. A., GOULDER, P. J. R., KLENERMAN, P., SEWELL, A. K., EASTERBROOK, P. J., TROOP, M., BANGHAM, C. R. M., PHILLIPS, R. E. (1997). Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proceedings National Academy of Sciences USA 94, 1890-1895.
75. PYBUS, O. G., HOLMES, E. C. & HARVEY, P. H. (1999). The mid-depth method and HIV-1: a practical approach to testing hypotheses of viral epidemic history. Molecular Biology & Evolution 16, 953-959.
76. REY-CUILLÉ, M.-A., BERTHIER, J.-L., BOMSEL-DEMONTOY, M.-C., CHADUC, V., MONTAGNIER, L., HOVANESSIAN, A. G. & CHAKRABARTI, L. A. (1998). Simian immunodeficiency virus replicates to high levels in sooty mangabeys without inducing disease. Journal of Virology 72, 3872-3886.
77. ROBERTSON, D. L., SHARP, P. M., MCCUTHAN, F. E. & HAHN, B. H. (1995). Recombination in HIV-1. Nature 374, 124-126.
78. ROWLAND-JONES, S. L. (1998). Survival with HIV infection: good luck or good breeding? Trends in Genetics 14, 343-345.
79. ROWLAND-JONES, S. L., SUTTON, J., ARIYOSHI, K., DONG, T., GOTCH, F., MCADAM, S., WHITBY, D., SABALLY, S., GALLIMORE, A., CORRAH, T., TAKIGUCHI, M., SCHULTZ, T., MCMICHAEL, A. & WHITTLE, H. (1995). HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nature Medicine 1, 59-64.
80. SCARLATTI, G., TRESOLDI, E., BJORNDAL, A., FREDRIKSSON, R., COLOGNESI, C., DENG, H. K., MALNATI, M. S., PLEBANI, A., SICCARDI, A. G., LITTMAN, D. R., FENYO, E. M. & LUSSO, P. (1997). In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nature Medicine 3, 1259-1265.
81. SCHIERUP, M. H. & HEIN, J. (2000). Consequences of recombination on traditional phylogenetic analysis. Genetics 156, 879-891.
82. SCHMITZ, J. E., KURODA, M. J., SANTRA, S., SASSEVILLE, V. G., SIMON, M. A., LIFTON, M. A., RACZ, P., TENNER-RACZ, K., DELESANDRO, M., SCALLON, B. J., GHRAYEB, J., FROMAN, M. A., MONTEFIORI, D. C., RIEBER, E. P., LETVIN, N. L. & REIMANN, K. A. (1999). Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283, 857-860.
83. SCHUITEMAKER, H., MEYAARD, L., KOOTSTRA, N. A., DUBBES, R., OTTO, S. A., TERSMETTE, M., HEENY, J. L. & MIEDEMA, F. (1993). Lack of T-cell dysfunction and programmed cell death in human immunodeficiency virus type-1 infected chimpanzees correlates with absence of monocytotropic variants. Journal of Infectious Diseases 168, 1140-1147.
84. SHANKARAPPA, R., MARGOLICK, J. B., GANGE, S. J., RODRIGO, A. G., UPCHURCH, D., FARZADEGAN, H., GUPTA, P., RINALDO, C. R., LEARN, G. H., HE, X., HUANG, X. L. & MULLINS, J. I. (1999). Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. Journal of Virology 73, 10489-10502.
85. SHARP, P. M., BAILES, E., GAO, F., BEER, B. E., HIRSCH, V. M. & HAHN, B. H. (2000). Origins and evolution of AIDS viruses: estimating the time-scale. Biochemical Society Transactions 28, 275-282.
86. SHPAER, E. G. & MULLINS, J. I. (1993). Rates of amino acid change in the envelope protein correlate with pathogenicity of primate lentiviruses. Journal of Molecular Evolution 37, 57-65.
87. STRIMMER, K. & VON HAESELER, A. (1996). Quartet puzzling: A quartet maximum-likelihood method for reconstructing tree topologies. Molecular Biology & Evolution 13, 964-969.
88. TAO, B. & FULTZ, P. N. (1999). Pathogenicity and comparative evolution in vivo of the transitional quasispecies SIVsmmPBj8. Virology 259, 166-175.
89. VAN RENSBURG, E. J., ENGELBRECHT, S., MWENDA, J., LATEN, J. D., ROBSON, B. A., STANDER, T. & CHEGE, G. K. (1998). Simian immunodeficiency viruses (SIVs) from eastern and southern Africa: detection of a SIVagm variant from a charma baboon. Journal of General Virology 79, 1809-1814.
90. WOLINKSY, S. M., KORBER, B. T. M., NEUMANN, A. U., DANIELS, M., KUNSTMAN K. J., WHETSELL, A. J., FURTADO, M. R., CAO, Y., HO, D. D., SAFRIT, J. T. & KOUP, R. A. (1996). Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 272, 537-542.
91. YAMAGUCHI-KABATA, Y. & GOJOBORI, T. (2000). Reevaluation of amino acid variability of the human immunodeficiency virus type 1 gp120 envelope glycoprotein and prediction of new discontinuous epitopes. Journal of Virology 74, 4335-4350.
92. ZANOTTO, P. M. DE A., KALLAS, E. G., DE SOUZA, R. F. & HOLMES, E. C. (1999). Genealogical evidence for positive selection in the nef gene of HIV-1. Genetics 153, 1077-1089.
93. ZHANG, L. Q., DAILEY, P. J., HE, T., GETTIE, A., BONHOEFFER, S., PERELSON, A. S. & HO, D. D. (1999). Rapid clearance of simian immunodeficiency virus particles from plasma of rhesus macaques. Journal of Virology 73, 855-860.
94. ZHANG, L. Q., HE, T., HUANG, Y., CHEN, Z., GUO, Y., WU, S., KUNSTMAN, K. J., BROWN, R. C., PHAIR J. P., NEUMANN, A. U., HO, D. D. & WOLINKSY, S. M. (1998). Chemokine coreceptor usage by diverse primary isolates of human immunodeficiency virus type 1. Journal of Virology 72, 9301-9312.
95. ZHANG, L. Q., MACKENZIE, P., CLELAND, A., HOLMES, E. C., LEIGH BROWN A. J., SIMMONDS, P. (1993). Selection for specific sequences in the external envelope protein of HIV-1 upon primary infection. Journal of Virology 67, 3345-3356.
96. ZHU, T. F., KORBER, B. T., NAHMIAS, A. J., HOOPER, E., SHARP, P. M. & HO, D. D. (1998). An African HIY-1 sequence from 1959 and implications for the origin of the epidemic. Nature 391, 594-597.
97. ZHU, T. F., MO, H. M., WANG, N., NAM, D. S., CAO, Y. Z., KOUP, R. A. & HO, D. D. (1993). Genotypic and phenotypic characterization of HIV-1 in patients with primary infection. Science 261, 1179-1181.