Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection

Journal of Virology

Volumn 73, Issue 12, 1999, Pages 10489-10502

  Shankarappa, Raj ^a   Margolick, Joseph B ^b   Gange, Stephen J ^b   Rodrigo, Allen G ^a   Upchurch, David ^a   Farzadegan, Homayoon ^b   Gupta, Phalguni ^c   Rinaldo, Charles R ^c   Learn, Gerald H ^a   He, Xi ^a   Huang, Xiao Li ^c   Mullins, James I ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; VIRUS ENVELOPE PROTEIN;

ADULT; ARTICLE; BIODIVERSITY; CLINICAL ARTICLE; DISEASE COURSE; EVOLUTION; FOUNDER EFFECT; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEROCONVERSION; T LYMPHOCYTE SUBPOPULATION; UNINDEXED SEQUENCE;

EID: 0032710838     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.12.10489-10502.1999     Document Type: Article

References (86)

1. Autran, B., G. Carcelain, T. S. Li, C. Blanc, D. Mathez, R. Tubiana, C. Katlama, P. Debré, and J. Leibowitch. 1997. Positive effects of combined antiretroviral therapy on CD4+ T cell homeostasis and function in advanced HIV disease. Science 277:112-116.
2. Bagnarelli, P., F. Mazzola, S. Menzo, M. Montroni, L. Butini, and M. Clementi. 1999. Host-specific modulation of the selective constraints driving human immunodeficiency virus type 1 env gene evolution. J. Virol. 73:3764-3777.
3. Berger, E., R. Doms, E. Fenyo, B. Korber, D. Littman, J. Moore, Q. Sattentau, H. Schuitemaker, J. Sodroski, and R. Weiss. 1998. A new classification for HIV-1. Nature 391:240.
4. Berger, E. A. 1997. HIV entry and tropism: the chemokine receptor connection. AIDS 11(Suppl. A):S3-S16.
5. Berkowitz, R. D., S. Alexander, C. Bare, V. Linquist-Steppes, M. Bogan, M. E. Moreno, L. Gibson, E. Wieder, J. Kosek, C. Stoddart, and J. M. McCune. 1998. CCR5- and CXCR4-utilizing strains of human immunodeficiency virus type 1 exhibit differential tropism and pathogenesis in vitro. J. Virol. 72:10108-10117.
6. Berkowitz, R. D., K. P. Beckerman, T. J. Schall, and J. M. McCune. 1998. CXCR4 and CCR5 expression delineates targets for HIV-1 disruption of T cell differentiation. J. Immunol. 161:3702-3710.
7. Bjorndal, A., H. Deng, M. Jansson, J. R. Fiore, C. Colognesi, A. Karlsson, J. Albert, G. Scarlatti, D. R. Littman, and E. M. Fenyo. 1997. Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J. Virol. 71:7478-7487.
8. Bleul, C. C., M. Farzan, H. Choe, C. Parolin, I. Clark-Lewis, J. Sodroski, and T. A. Springer. 1996. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382:829-832.
9. Bleul, C. C., L. Wu, J. A. Hoxie, T. A. Springer, and C. R. Mackay. 1997. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. USA 94:1925-1930.
10. Carr, A., K. Samaras, D. J. Chisholm, and D. A. Cooper. 1998. Pathogenesis of HIV-1-protease inhibitor-associated peripheral lipodystrophy, hyperlipidaemia, and insulin resistance. Lancet 351:1881-1883.
11. Centers for Disease Control and Prevention. 1992. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. Morbid. Mortal. Weekly Rep. 41:1-19.
12. Chun, T.-W., D. Finzi, J. Margolick, K. Chadwick, D. Schwartz, and R. F. Siliciano. 1995. In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nat. Med. 1:1284-1290.
13. de Jong, J. J., A. de Ronde, W. Keulen, M. Tersmette, and J. Goudsmit. 1992. Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. J. Virol. 66:6777-6780.
14. Delwart, E. L., M. P. Busch, M. L. Kalish, J. W. Mosley, and J. I. Mullins. 1995. Rapid molecular epidemiology of HIV transmission. AIDS Res. Hum. Retrovir. 11:1181-1193.
15. Delwart, E. L., H. Pan, H. W. Sheppard, D. Wolpert, A. U. Neumann, B. Korber, and J. I. Mullins. 1997. Slower evolution of human immunodeficiency virus type 1 quasispecies during progression to AIDS. J. Virol. 71: 7498-7508.
16. Delwart, E. L., H. W. Sheppard, B. D. Walker, J. Goudsmit, and J. I. Mullins. 1994. Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J. Virol. 68:6672-6683.
17. Delwart, E. L., E. G. Shpaer, F. E. McCutchan, J. Louwagie, M. Grez, H. Rübsamen-Waigmann, and J. I. Mullins. 1993. Genetic relationships determined by a DNA heteroduplex mobility assay: analysis of HIV-1 env genes. Science 262:1257-1261.
18. De Wolf, F., E. Hogervorst, J. Goudsmit, E. M. Fenyo, H. Rubsamen-Waigmann, H. Holmes, B. Galvao-Castro, E. Karita, C. Wasi, S. D. K. Sempala, E. Baan, F. Zorgdrager, V. Lukashov, S. Osmanov, C. Kuiken, M. Cornelissen, and WHO Network for HIV Isolation and Characterization. 1994. Syncytium-inducing and non-syncytium-inducing capacity of HIV-1 subtypes other than B: phenotypic and genotypic characteristics. AIDS Res. Hum. Retrovir. 10:1387-1401.
19. Erlich, H. A., D. Gelfand, and J. J. Sninsky. 1991. Recent advances in the polymerase chain reaction. Science 252:1643-1651.
20. Felsenstein, J. 1989. PHYLIP-Phylogeny inference package, version 3.2. Cladistics 5:164-166.
21. Folks, T. M., D. Powell, M. Lightfoote, S. Koenig, A. S. Fauci, S. Benn, A. Rabson, D. Daugherty, H. E. Gendelman, M. D. Hoggan, et al. 1986. Biological and biochemical characterization of a cloned Leu-3- cell surviving infection with the acquired immune deficiency syndrome retrovirus. J. Exp. Med. 164:280-290.
22. Fouchier, R. A. M., M. Groenink, N. A. Kootstra, M. Tersmette, H. G. Huisman, F. Miedema, and H. Schuitemaker. 1992. Phenotype-associated sequence variation in the third variable domain (V3) of the human immunodeficiency virus type 1 gp120 molecule. J. Virol. 66:3183-3187.
23. Ganeshan, S., R. E. Dickover, B. T. Korber, Y. J. Bryson, and S. M. Wolinsky. 1997. Human immunodeficiency virus type 1 genetic evolution in children with different rates of development of disease. J. Virol. 71:663-677.
24. Gange, S. J., A. Muñoz, J. S. Chmiel, A. D. Donnenberg, L. M. Kirstein, R. Detels, and J. B. Margolick. 1998. Identification of inflections in T-cell counts among HIV-1-infected individuals and relationship with progression to clinical AIDS. Proc. Natl. Acad. Sci. USA 95:10848-10853.
25. Giorgi, J. V., H. L. Cheng, J. B. Margolick, K. D. Bauer, J. Ferbas, M. Waxdal, I. Schmid, L. E. Hultin, A. L. Jackson, L. Park, et al. 1990. Quality control in the flow cytometric measurement of T-lymphocyte subsets: the Multicenter AIDS Cohort Study experience. The Multicenter AIDS Cohort Study Group. Clin. Immunol. Immunopathol. 55:173-186.
26. Goodenow, M., T. Huet, W. Saurin, S. Kwok, J. Sninsky, and S. Wain-Hobson. 1989. HIV-1 isolates are rapidly evolving quasispecies: evidence for viral mixtures and preferred nucleotide substitutions. J. Acquir. Immun. Defic. Syndr. 2:344-352.
27. Haynes, B. F., G. Pantaleo, and A. S. Fauci. 1996. Toward an understanding of the correlates of protective immunity to HIV infection. Science 271:324-328.
28. Henry, K., H. Melroe, J. Huebsch, J. Hermundson, C. Levine, L. Swensen, and J. Daley. 1998. Severe premature coronary artery disease with protease inhibitors. Lancet 351:1328. (Letter.)
29. Herbein, G., V. Mahlknecht, F. Batliwalla, P. Gregersen, T. Pappas, J. Butler, W. A. O'Brien, and E. Verdin. 1998. Apoptosis of CD8+ T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 395:189-194.
30. Ida, S., H. Gatanaga, T. Shioda, Y. Nagai, N. Kobayashi, K. Shimada, S. Kimura, A. Iwamoto, and S. Oka. 1997. HIV type 1 V3 variation dynamics in vivo: long-term persistence of non-syncytium-inducing genotypes and transient presence of syncytium-inducing genotypes during the course of progressive AIDS. AIDS Res. Hum. Retrovir. 13:1597-1609.
31. Japour, A. J., S. A. Fiscus, J. M. Arduino, D. L. Mayers, P. S. Reichelderfer, and D. R. Kurizkes. 1994. Standardized microtiter assay for determination of syncytium-inducing phenotypes of clinical human immunodeficiency virus type 1 isolates. J. Clin. Microbiol. 32:2291-2294.
32. Jurriaans, S., B. Van Gemen, G. J. Weverling, D. Van Strijp, P. Nara, R. Coutinho, M. Koot, H. Schuitemaker, and J. Goudsmit. 1994. The natural history of HIV-1 infection: virus load and virus phenotype independent determinants of clinical course? Virology 204:223-233.
33. Kaneshima, H., L. Su, M. L. Bonyhadi, R. I. Connor, D. D. Ho, and J. M. McCune. 1994. Rapid-high, syncytium-inducing isolates of human immunodeficiency virus type 1 induce cytopathicity in the human thymus of the SCID-hu mouse. J. Virol. 68:8188-8192.
34. Kaslow, R. A., D. G. Ostrow, R. Detels, J. P. Phair, B. F. Polk, and C. R. Rinaldo, Jr. 1987. The Multicenter AIDS Cohort Study: rationale, organization, and selected characteristics of the participants. Am. J. Epidemiol. 126:310-318.
35. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
36. Koot, M., I. Keet, A. Vos, R. deGoede, M. Roos, R. Coutinho, F. Miedema, P. Schellekens, and M. Tersmette. 1993. Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. Ann. Intern. Med. 118:681-688.
37. Korber, B., M. Hoelscher, F. McCutchan, C. Williamson, F. von Sonnenburg, J. Mullins, M. Pletschette, J. Weber, G. van der Groen, S. Osmanov, and Workshop Report from the European Commission and the Joint United Nations Programme on HIV/AIDS. 1997. HIV-1 subtypes: implications for epidemiology, pathogenicity, vaccines and diagnostics. AIDS 11:UNAIDS17-UNAIDS36.
38. Koup, R. A., J. T. Safrit, Y. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
39. Kuiken, C. L., and B. Korber. 1994. Epidemiological significance of intra- and inter-person variation of HIV-1. AIDS 8:S73-S83.
40. Kumar, S., K. Tamura, and M. Nei. 1994. MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput. Appl. Biosci. 10: 189-191.
41. Laco, G., et al. Unpublished data.
42. Leitner, T., S. Kumar, and J. Albert. 1997. Tempo and mode of nucleotide substitutions in gag and env gene fragments in human immunodeficiency virus type 1 populations with a known transmission history. J. Virol. 71:4761-4770.
43. Levy, J. A. 1993. Pathogenesis of human immunodeficiency virus infection. Microbiol. Rev. 57:183-289.
44. Liu, S.-L., T. Mulvania, A. Rodrigo, B. Kosloff, X. He, D. Shriner, L. Corey, and J. I. Mullins. Emergence, evolutionary dynamics and selective advantage of human immunodeficiency virus type-1 chimeras in vivo. Submitted for publication.
45. Liu, S.-L., A. G. Rodrigo, R. Shankarappa, G. H. Learn, L. Hsu, O. Davidov, L. P. Zhao, and J. I. Mullins. 1996. HIV quasispecies and resampling. Science 273:415-416.
46. Liu, S. L., T. Schacker, L. Musey, D. Shriner, M. J. McElrath, L. Corey, and J. I. Mullins. 1997. Divergent patterns of progression to AIDS after infection from the same source: human immunodeficiency virus type 1 evolution and antiviral responses. J. Virol. 71:4284-4295.
47. Lukashov, V. V., C. L. Kuiken, and J. Goudsmit. 1995. Intrahost human immunodeficiency virus type 1 evolution is related to length of the immunocompetent period. J. Virol. 69:6911-6916.
48. Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Res. 27:209-220.
49. Margolick, J. B., A. Muñoz, A. D. Donnenberg, L. P. Park, N. Galai, J. V. Giorgi, R. G. O'Gorman, and J. Ferbas, for the Multicenter AIDS Cohort Study. 1995. Failure of T-cell homeostasis preceding AIDS in HIV-1 infection. Nat. Med. 1:674-680.
50. Markham, R. B., W. C. Wang, A. E. Weisstein, Z. Wang, A. Munoz, A. Templeton, J. Margolick, D. Vlahov, T. Quinn, H. Farzadegan, and X. F. Yu. 1998. Patterns of HIV-1 evolution in individuals with differing rates of CD4 T cell decline. Proc. Natl. Acad. Sci. USA 95:12568-12573.
51. McCune, J. M., R. Loftus, D. K. Schmidt, P. Carroll, D. Webster, Y.-L. B. Swor, I. R. Francis, B. H. Gross, and R. M. Grant. 1998. High prevalence of thymic tissue in adults with human immunodeficiency virus-1 infection. J. Clin. Investig. 101:2301-2308.
52. McDonald, R. A., D. L. Mayers, R. C-Y. Chung, K. F. Wagner, S. Ratto-Kim, D. L. Birx, and N. L. Michael. 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.
53. McNearney, T., Z. Hornickova, R. Markham, A. Birdwell, M. Arens, A. Saah, and L. Ratner. 1992. Relationship of human immunodeficiency virus type 1 sequence heterogeneity to stage of disease. Proc. Natl. Acad. Sci. USA 89:10247-10251.
54. Mellors, J. W., L. A. Kingsley, C. R. J. Rinaldo, J. A. Todd, B. S. Hoo, R. P. Kokka, and P. Gupta. 1995. Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann. Intern. Med. 122:573-579.
55. Mellors, J. W., A. Muñoz, J. V. Giorgi, J. B. Margolick, C. J. Tassoni, P. Gupta, L. A. Kingsley, J. A. Todd, A. J. Saah, R. Detels, J. P. Phair, and C. R. Rinaldo, Jr. 1997. Plasma viral load and CD4+ lymphocytes as prognostic markers of HIV-1 infection. Ann. Intern. Med. 126:946-954.
56. Mellors, J. W., C. R. Rinaldo, Jr., P. Gupta, R. M. White, J. A. Todd, and L. A. Kingsley. 1996. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272:1167-1170.
57. Muñoz, A., C. A. Sabin, and A. N. Phillips. 1997. The incubation period of AIDS. AIDS 11:S69-S76.
58. Nelson, J. A. E., S. A. Fiscus, and R. Swanstrom. 1997. Evolutionary variants of the human immunodeficiency virus type 1 V3 region characterized by using a heteroduplex tracking assay. J. Virol. 71:8750-8758.
59. Nowak, M. A., R. M. Anderson, A. R. McLean, T. F. Wolfs, J. Goudsmit, and R. M. May. 1991. Antigenic diversity thresholds and the development of AIDS. Science 254:963-969.
60. Peeters, M., R. Vincent, J. L. Perret, M. Lasky, D. Patrel, F. Liegeois, V. Courgnaud, R. Seng, T. Matton, S. Molinier, and E. Delaporte. 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. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 20:115-121.
61. Pelletier, E., and S. Wain-Hobson. 1996. AIDS is not caused by the extreme genetic variability of HIV. J. NIH Res. 8:45-48.
62. Perelson, A. S., P. Essunger, Y. Cao, M. Vesanen, A. Hurley, K. Saksela, M. Markowitz, and D. D. Ho. 1997. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387:188-191.
63. Poss, M., A. G. Rodrigo, J. J. Gosink, G. H. Learn, D. de Vange Panteleeff, H. L. Martin, Jr., J. Bwayo, J. K. Kreiss, and J. Overbaugh. 1998. Evolution of envelope sequences from the genital tract and peripheral blood of women infected with clade A human immunodeficiency virus type 1. J. Virol. 72: 8240-8251.
64. Psallidopoulos, M. C., S. M. Schnittman, L. M. Thompson III, M. Baseler, A. S. Fauci, H. C. Lane, and N. P. Salzman. 1989. Integrated proviral human immunodeficiency virus type 1 is present in CD4+ peripheral blood lymphocytes in healthy seropositive individuals. J. Virol. 63:4626-4631.
65. Richman, D. D., and S. A. Bozzette. 1994. The impact of the syncytium-inducing phenotype of human immunodeficiency virus on disease progression. J. Infect. Dis. 169:968-974.
66. Rinaldo, C. R., Jr., P. Gupta, X. Huang, Z. Fan, J. I. Mullins, S. Gange, H. Farzadegan, R. Shankarappa, A. Muñoz, and J. B. Margolick. 1998. Anti-HIV-1 memory cytotoxic T lymphocyte responses associated with changes in CD4+ T cell numbers in the progression of HIV-1 infection. AIDS Res. Hum. Retrovir. 14:1423-1433.
67. Rodrigo, A. G., P. C. Goracke, K. Rowhanian, and J. I. Mullins. 1997. Quantitation of target molecules from polymerase chain reaction-based limiting dilution assays. AIDS Res. Hum. Retrovir. 13:737-742.
68. Salvatori, F., S. Masiero, C. Giaquinto, C. M. Wade, A. J. Leigh Brown, L. Chieco-Bianchi, and A. De Rossi. 1997. Evolution of human immunodeficiency virus type 1 in perinatally infected infants with rapid and slow progression to disease. J. Virol. 71:4694-4706.
69. Schenker, E. L., L. E. Hultin, K. D. Bauer, J. Ferbas, J. B. Margolick, and J. V. Giorgi. 1993. Evaluation of a dual-color flow cytometry immunophenotyping panel in a multicenter quality assurance program. Cytometry 14: 307-317.
70. Schnittman, S. M., M. C. Psallidopoulos, H. C. Lane, L. Thompson, M. Baseler, F. Massari, C. H. Fox, N. P. Salzman, and A. S. Fauci. 1989. The reservoir for HIV-1 in human peripheral blood is a T cell that maintains expression of CD4. Science 245:305-308. (Erratum, 245: before 694, 1989.)
71. Schuitemaker, H., M. Koot, N. A. Kootstra, M. W. Dercksen, R. E. de Goede, R. P. van Steenwijk, J. M. Lange, J. K. Schattenkerk, F. Miedema, and M. Tersmette. 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.
72. Shankarappa, R., P. Gupta, G. H. Learn, A. G. Rodrigo, C. R. Rinaldo, M. C. Gorry, J. I. Mullins, P. L. Nara, and G. D. Ehrlich. 1998. Evolution of human immunodeficiency virus type 1 envelope sequences in infected individuals with differing disease progression profiles. Virology 241:251-259.
73. Shankarappa, R., A. G. Rodrigo, D. Upchurch, G. H. Learn, and J. I. Mullins. 20 September 1999, posting date. Mullins Molecular Retrovirology Lab. [Online.] http://ubik.microbiol.washington.edu/HIV/evolution1/. [15 October 1999, last date accessed.]
74. Shearer, W. T., T. C. Quinn, P. LaRussa, J. F. Lew, L. Mofenson, S. Almy, K. Rich, E. Handelsman, C. Diaz, M. Pagano, V. Smeriglio, L. A. Kalish, and the Women and Infants Transmission Study Group. 1997. Viral load and disease progression in infants infected with human immunodeficiency virus type 1. New Engl. J. Med. 336:1337-1342.
75. Shioda, T., S. Oka, X. Xin, H. Liu, R. Harukuni, A. Kurotani, M. Fukushima, M. K. Hasan, T. Shiino, Y. Takebe, A. Iwamoto, and Y. Nagai. 1997. In vivo sequence variability of human immunodeficiency virus type 1 envelope gp120: association of V2 extension with slow disease progression. J. Virol. 71:4871-4881.
76. Smouse, P., J. C. Jong, and R. R. Sokal. 1986. Multiple regression and correlation extensions of the Mantel's test of matrix correspondence. Syst. Zool. 35:627-632.
77. Spina, C. A, H. E. Prince, and D. D. Richman. 1997. Preferential replication of HIV-1 in the CD45RO memory cell subset of primary CD4 lymphocytes in vitro. J. Clin. Investig. 99:1774-1785.
78. Strunnikova, N., S. C. Ray, R. A. Livingson, E. Rubalcaba, and R. P. Viscidi. 1995. Convergent evolution within the V3 loop domain of human immunodeficiency virus type 1 in association with disease progression. J. Virol. 69:7548-7558.
79. Swofford, D. L., G. J. Olsen, P. J. Waddell, and D. M. Hillis. 1996. Phylogenetic inference, p. 407-514. In D. M. Hillis, C. Moritz, and B. K. Mable (ed.), Molecular systematics, 2nd ed. Sinauer Associates, Sunderland, Mass.
80. Tersmette, M., R. A. Gruters, F. de Wolf, R. E. Y. de Goede, J. M. A. Lange, P. T. A. Schellekens, J. Goudsmit, H. G. Huisman, and F. Miedema. 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.
81. Tien, P. C. T. Chiu, A. Latif, S. Ray, M. Batra, C. H. Contag, L. Zejena, M. Mbizvo, E. L. Delwart, J. I. Mullins, and D. A. Katzenstein. 1999. Primary subtype C HIV-1 infection in Harare, Zimbabwe. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 20:147-153.
82. Waddle, D. M. 1994. Matrix correlation tests support a single origin for modern humans. Nature 368:452-454.
83. Winkler, C., W. Modi, M. W. Smith, G. W. Nelson, X. Wu, M. Carrington, M. Dean, T. Honjo, K. Tashiro, D. Yabe, S. Buchbinder, E. Vittinghoff, J. J. Goedert, T. R. O'Brien, L. P. Jacobson, R. Detels, S. Donfield, A. Willoughby, E. Gomperts, D. Vlahov, J. Phair, ALIVE Study, Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, San Francisco City Cohort, and S. J. O'Brien. 1998. Genetic restriction of AIDS pathogenesis by an SDF-1 chemokine gene variant. Science 279:389-393.
84. Wolfs, T. F. W., J. J. de Jong, H. van den Berg, J. M. G. H. Tijnagel, W. J. A. Krone, and J. Goudsmit. 1990. Evolution of sequences encoding the principal neutralization epitope of human immunodeficiency virus 1 is host dependent, rapid, and continuous. Proc. Natl. Acad. Sci. USA 87:9938-9942.
85. Wolinsky, S. M., B. T. M. Korber, A. U. Neumann, M. Daniels, K. J. Kuntsman, A. J. Whetsell, M. R. Furtado, Y. Cao, D. D. Ho, J. T. Safrit, and R. A. Koup. 1996. Adaptive evolution of HIV-1 during the natural course of infection. Science 272:537-542.
86. Zhang, L., R. S. Diaz, D. D. Ho, J. W. Mosley, M. P. Busch, and A. Mayer. 1997. Host-specific driving force in human immunodeficiency virus type 1 evolution in vivo. J. Virol. 71:2555-2561.