Impact of clade diversity on HIV-1 virulence, antiretroviral drug sensitivity and drug resistance

Journal of Antimicrobial Chemotherapy

Volumn 51, Issue 2, 2003, Pages 229-240

  Spira, Shalom ^a   Wainberg, Mark A ^a   Loemba, Hugues ^a   Turner, Dan ^a   Brenner, Bluma G ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Clade; HIV; Resistance

Indexed keywords

ANTIRETROVIRUS AGENT; DIDANOSINE; EFAVIRENZ; LAMIVUDINE; NEVIRAPINE; NUCLEOSIDE DERIVATIVE; PROTEINASE INHIBITOR; RITONAVIR; RNA DIRECTED DNA POLYMERASE INHIBITOR; SAQUINAVIR; ZALCITABINE; ZIDOVUDINE;

CLADISTICS; CLINICAL TRIAL; EPIDEMIOLOGICAL DATA; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GEOGRAPHY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; MOLECULAR EVOLUTION; NONHUMAN; REVIEW; STRAIN DIFFERENCE; VIRUS MUTATION; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANIMALS; ANTI-HIV AGENTS; DRUG RESISTANCE, VIRAL; EPITOPES; GEOGRAPHY; HIV-1; HUMANS; VARIATION (GENETICS);

EID: 0037326239     PISSN: 03057453     EISSN: None     Source Type: Journal    
DOI: 10.1093/jac/dkg079     Document Type: Review

References (122)

1. Joint United Nations Programme on HIV/AIDS. AIDS epidemic update. [Online.] http://www.unaids.org (June 2002, date last accessed).
2. Renjifo, B. & Essex, M. (2002). HIV-1 subtypes and recombinants. In AIDS in Africa, 2nd edn (Essex, M., Mboup, S., Kanki, P. J., Marlink, P. J. & Tlou, S. D., Eds), pp. 138-57. Kluwer Academic/Plenum Publishers, New York, NY, USA.
3. Simon, F., Mauclere, P., Roques, P., Loussert-Ajaka, I., Muller-Trutwin, M. C., Saragosti, S. et al. (1998). Identification of a new human immunodeficiency virus type 1 distinct from group M and group O. Nature Medicine 4, 1032-7.
4. Quinones-Mateu, M. E. & Arts, E. J. (1999). Recombination in HIV-1: update and implications. AIDS Reviews 1, 89-100.
5. Triques, K., Bourgeois, A., Vidal, N., Mpoudi-Ngole, E., Mulanga-Kabeya, C., Nzilambi, N. et al. (2000). Near-full-length genome sequencing of divergent African HIV type 1 subtype F viruses leads to the identification of a new HIV type 1 subtype designated K. AIDS Research and Human Retroviruses 16, 139-51.
6. Piot, P. & Bartos, M. (2002). The epidemiology of HIV and AIDS. In AIDS in Africa, 2nd edn (Essex, M., Mboup, S., Kanki, P. J., Marlink, P. J. & Tlou, S. D., Eds), pp. 200-17. Kluwer Academic/Plenum Publishers, New York, NY, USA.
7. Janssens, W., Buve, A. & Nkengasong, J. N. (1997). The puzzle of HIV-1 subtypes in Africa. AIDS 11, 705-12.
8. Takehisa, J., Zekeng, L., Ido, E., Mboudjeka, I., Moriyama, H., Miura, T. et al. (1998). Various types of HIV mixed infections in Cameroon. Virology 245, 1-10.
9. Delaporte, E., Janssens, W., Peeters, M., Buve, A., Dibanga, G., Perret, J. L. et al. (1996). Epidemiological and molecular characteristics of HIV infection in Gabon, 1986-1994. AIDS 10, 903-10.
10. Bikandou, B., Takehisa, J., Mboudjeka, I., Ido, E., Kuwata, T., Miyazaki, Y. et al. (2000). Genetic subtypes of HIV type 1 in Republic of Congo. AIDS Research and Human Retroviruses 16, 613-9.
11. Essex, M. (1998). State of the HIV pandemic. Journal of Human Virology 1, 427-9.
12. Novitsky, V. A., Montano, M. A., McLane, M. F., Renjifo, B., Vannberg, F., Foley, B. T. et al. (1999). Molecular cloning and phylogenetic analysis of human immunodeficiency virus type 1 subtype C: a set of 23 full-length clones from Botswana. Journal of Virology 73, 4427-32.
13. Oelrichs, R. B., Shrestha, I. L., Anderson, D. A. & Deacon, N. J. (2000). The explosive human immunodeficiency virus type 1 epidemic among injecting drug users of Kathmandu, Nepal, is caused by a subtype C virus of restricted genetic diversity. Journal of Virology 74, 1149-57.
14. Weniger, B. G., Takebe, Y., Ou, C. Y. & Yamazaki, S. (1994). The molecular epidemiology of HIV in Asia. AIDS 8, Suppl. 2, S13-28.
15. Chen, Z., Huang, Y., Zhao, X., Skulsky, E., Lin, D., Ip, J. et al. (2000). Enhanced infectivity of an R5-tropic simian/human immunodeficiency virus carrying human immunodeficiency virus type 1 subtype C envelope after serial passages in pig-tailed macaques (Macaca nemestrina). Journal of Virology 74, 6501-10.
16. Toure-Kane, C., Montavon, C., Awa Faye, M., Gueye, P. M., Sow, P. S., Ndoye, I. et al. (2000). Identification of all HIV type 1 group M subtypes in Senegal, a country with low and stable seroprevalence. AIDS Research and Human Retroviruses 16, 603-9.
17. Janssens, W., Heyndrickx, L., Van de Peer, Y., Bouckaert, A., Fransen, K., Motte, J. et al. (1994). Molecular phylogeny of part of the env gene of HIV-1 strains isolated in Cote d'Ivoire. AIDS 8, 21-6.
18. Artenstein, A. W., Coppola, J., Brown, A. E., Carr, J. K., Sanders-Buell, E., Galbarini, E. et al. (1995). Multiple introductions of HIV-1 subtype E into the western hemisphere. Lancet 346, 1197-8.
19. Paladin, F. J., Monzon, O. T., Tsuchie, H., Aplasca, M. R., Learn, G. H., Jr & Kurimura, T. (1998). Genetic subtypes of HIV-1 in the Philippines. AIDS 12, 291-300.
20. Kalish, M. L., Baldwin, A., Raktham, S., Wasi, C., Luo, C. C., Schochetman, G. et al. (1995). The evolving molecular epidemiology of HIV-1 envelope subtypes in injecting drug users in Bangkok, Thailand: implications for HIV vaccine trials. AIDS 9, 851-7.
21. Triques, K., Bourgeois, A., Saragosti, S., Vidal, N., Mpoudi-Ngole, E., Nzilambi, N. et al. (1999). High diversity of HIV-1 subtype F strains in Central Africa. Virology 259, 99-109.
22. Irwin, K. L., Pau, C. P., Lupo, D., Pienazek, D., Luo, C. C., Olivo, N. et al. (1997). Presence of human immunodeficiency virus (HIV) type 1 subtype A infection in a New York community with high HIV prevalence: a sentinel site for monitoring HIV genetic diversity in North America. Centers for Disease Control and Prevention-Bronx Lebanon HIV Serosurvey Team. Journal of Infectious Diseases 176, 1629-33.
23. Gurtler, L. G., Hauser, P. H., Eberle, J., von Brunn, A., Knapp, S., Zekeng, L. et al. (1994). A new subtype of human immunodeficiency virus type 1 (MVP-5180) from Cameroon. Journal of Virology 68, 1581-5.
24. Gao, F., Yue, L., Robertson, D. L., Hill, S. C., Hui, H., Biggar, R. J. et al. (1994). Genetic diversity of human immunodeficiency virus type 2: evidence for distinct sequence subtypes with differences in virus biology. Journal of Virology 68, 7433-47.
25. Korber, B., Gifford, A. & Myers, G. (1993). Patterns of variation among international isolates in the highly immunogenic V3 region of the HIV-1 envelope protein. AIDS Research and Human Retroviruses 9, Suppl. 1, S98.
26. Myers, G., Korber, B. & Wain-Hobson, S. (1995). Human Retroviruses and AIDS 1995. Los Alamos National Laboratory, Los Alamos, NM, USA.
27. Gao, F., Robertson, D. L., Carruthers, C. D., Morrison, S. G., Jian, B., Chen, Y. et al. (1998). A comprehensive panel of near-full-length clones and reference sequences for non-subtype B isolates of human immunodeficiency virus type 1. Journal of Virology 72, 5680-98.
28. Loemba, H., Brenner, B., Parniak, M. A., Ma'ayan, S., Spira, B., Moisi, D. et al. (2002). Genetic divergence of human immunodeficiency virus type 1 (HIV-1) Ethiopian clade C reverse transcriptase (RT) and rapid development of resistance against non-nucleoside inhibitors of RT. Antimicrobial Agents and Chemotherapy 46, 2087-94.
29. Loemba, H., Brenner, B., Parniak, M. A., Ma'ayan, S., Spira, B., Moisi, D. et al. (2002). Co-receptor usage and HIV-1 inter-clade C polymorphisms in the protease and reverse transcriptase genes of HIV-1 isolates from Ethiopia and Botswana. Antiviral Therapy 7, 141-8.
30. Loemba, H., Brenner, B., Parniak, M. A., Ma'ayan, S., Spira, B., Moisi, D. et al. (2002). Polymorphisms of cytotoxic T-lymphocyte (CTL) and T-helper epitopes within reverse transcriptase (RT) of HIV-1 subtype C from Ethiopia and Botswana following selection of antiretroviral drug resistance. Antiviral Research 56, 129-42.
31. Montano, M. A., Novitsky, V. A., Blackard, J. T., Cho, N. L., Katzenstein, D. A. & Essex, M. (1997). Divergent transcriptional regulation among expanding human immunodeficiency virus type 1 subtypes. Journal of Virology 71, 8657-65.
32. Jeeninga, R. E., Hoogenkamp, M., Armand-Ugon, M., de Baar, M., Verhoef, K. & Berkhout, B. (2000). Functional differences between the long terminal repeat transcriptional promoters of human immunodeficiency virus type 1 subtypes A through G. Journal of Virology 74, 3740-51.
33. Zacharova, V., Becker, M. L. B., Zachar, V., Ebbesen, P. & Goustin, A. S. (1997). DNA sequence analysis of the long terminal repeat of the C subtype of human immunodeficiency virus type 1 from Southern Africa reveals a dichotomy between B subtype and African subtypes on the basis of upstream NF-IL6 motif. AIDS Research and Human Retroviruses 13, 719-24.
34. Naghavi, M. H., Schwartz, S., Sonnerborg, A. & Vahlne, A. (1999). Long terminal repeat promoter/enhancer activity of different subtypes of HIV type 1. AIDS Research and Human Retroviruses 15, 1293-303.
35. Henderson, A. J., Zou, X. & Calame, K. L. (1995). C/EBP proteins activate transcription from the human immunodeficiency virus type 1 long terminal repeat in macrophages/monocytes. Journal of Virology 69, 5337-44.
36. Rosen, C. A., Haseltine, W. A., Lenz, J., Ruprecht, R. & Cloyd, M. W. (1985). Tissue selectivity of murine leukemia virus infection is determined by long terminal repeat sequences. Journal of Virology 55, 862-6.
37. Jubier-Maurin, V., Saragosti, S., Perret, J. L., Mpoudi, E., Esu-Williams, E., Mulanga C. et al. (1999). Genetic characterization of the nef gene from human immunodeficiency virus type 1 group M strains representing genetic subtypes A, B, C, E, F, G, and H. AIDS Research and Human Retroviruses 15, 23-32.
38. Kirchhoff, F., Easterbrook, P. J., Douglas, N., Troop, M., Greenough, T. C., Weber, J. et al. (1999). Sequence variations in human immunodeficiency virus type 1 Nef are associated with different stages of disease. Journal of Virology 73, 5497-508.
39. Kawano, Y., Tanaka, Y., Misawa, N., Tanaka, R., Kira, J. I., Kimura, T. et al. (1997). Mutational analysis of human immunodeficiency virus type 1 (HIV-1) accessory genes: requirement of a site in the nef gene for HIV-1 replication in activated CD4+ T cells in vitro and in vivo. Journal of Virology 71, 8456-66.
40. Worgall, S., Connor, R., Kaner, R. J., Fenamore, E., Sheridan, K., Singh, R. et al. (1999). Expression and use of human immunodeficiency virus type 1 coreceptors by human alveolar macrophages. Journal of Virology 73, 5865-74.
41. Fenyo, E. M., Morfeldt-Manson, L., Chiodi, F., Lind, B., von Gegerfelt, A., Albert, J. et al. (1998). Distinct replicative and cytopathic characteristics of human immunodeficiency virus isolates. Journal of Virology 62, 4414-9.
42. Tersmette, M., De Goede, R. E. Y., Al, B. J., Winkel, I. N., Gruters, R. A., Cuypers, H. T. et al. (1998). Differential syncytium-inducing capacity of human immunodeficiency virus isolates: frequent detection of syncytium-inducing isolates in patients with acquired immunodeficiency syndrome (AIDS) and AIDS-related complex. Journal of Virology 62, 2026-32.
43. Choe, H., Farzan, M., Sun, Y., Sullivan, N., Rollins, B., Ponath, P. D. et al. (1996). The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85, 1135-48.
44. Cocchi, F., DeVico, A. L., Garzino-Demo, A., Arya, S. K., Gallo, R. C. & Lusso, P. (1995). Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 270, 1811-5.
45. Deng, H., Liu, R., Ellmeier, W., Choe, S., Unutmaz, D., Burkhart, M. et al. (1996). Identification of a major co-receptor for primary isolates of HIV-1. Nature 381, 661-6.
46. Doranz, B. J., Rucker, J., Yi, Y., Smyth, R. J., Samson, M., Peiper, S. C. et al. (1996). A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85, 1149-58.
47. Comelissen, M., Mulder-Kampinga, G., Veenstra, J., Zorgdrager, F., Kuiken, C., Hartman, S. et al. (1995). Syncytium-inducing (SI) phenotype suppression at seroconversion after intramuscular inoculation of a non-syncytium-inducing/SI phenotypically mixed human immunodeficiency virus population. Journal of Virology 69, 1810-8.
48. Keet, I. P. M., Krijnen, P., Koot, M., Lange, J. M., Miedema, F., Goudsmit, J. et al. (1993). Predictors of rapid progression to AIDS in HIV-1 seroconverters. AIDS 7, 51-7.
49. Nielsen, C., Pederson, C., Lundgren, J. D. & Gerstoft, J. (1993). Biological properties of HIV isolates in primary HIV infection: consequences for the subsequent course of infection. AIDS 7, 1035-40.
50. Tscherning, C., Alaeus, A., Fredriksson, R., Bjorndal, A., Deng, H., Littman, D. R. et al. (1998). Differences in chemokine coreceptor usage between genetic subtypes of HIV-1. Virology 241, 181-8.
51. Abebe, A., Demissie, D., Goudsmit, J., Brouwer, M., Kuiken, C. L., Pollakis, G. et al. (1999). HIV-1 subtype C syncytium- and non-syncytium-inducing phenotypes and coreceptor usage among Ethiopian patients with AIDS. AIDS 13, 1305-11.
52. Zhang, L., Huang, Y., He, T., Cao, Y. & Ho, D. D. (1996). HIV-1 subtype and second-receptor use. Nature 383, 768.
53. Peeters, M., Vincent, R., Perret, J. L., Lasky, M., Patrel, D. & Liegeois, F. (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, 115-21.
54. Bleul, C. C., Wu, L., Hoxie, J. A., Springer, T. A. & Mackay, C. R. (1997). The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proceedings of the National Academy of Sciences, USA 94, 1925-30.
55. Bentwich, Z., Kalinkovich, A., Weisman, Z. & Grossman, Z. (1998). Immune activation in the context of HIV infection. Clinical and Experimental Immunology 111, 1-2.
56. Bentwich, Z., Maartens, G., Torten, D., Lal, A. A. & Lal, R. B. (2000). Concurrent infections and HIV pathogenesis. AIDS 14, 2071-81.
57. Hu, D. J., Buve, A., Baggs, J., van der Groen, G. & Dondero, T. J. (1999). What role does HIV-1 subtype play in transmission and pathogenesis? An epidemiological perspective. AIDS 13, 873-81.
58. Soto-Ramirez, L. E., Renjifo, B., McLane, M. F., Marlink, R., O'Hara, C., Sutthent, R. et al. (1996). HIV-1 Langerhans' cell tropism associated with heterosexual transmission of HIV. Science 271, 1291-3.
59. Dittmar, M. T., Simmons, G., Hibbitts, S., O'Hare, M., Louisirirotchanakul, S., Beddows, S. et al. (1997). Langerhans cell tropism of human immunodeficiency virus type 1 subtype A through F isolates derived from different transmission groups. Journal of Virology 71, 8008-13.
60. Kato, K., Sato, H. & Takebe, Y. (1999). Role of naturally occurring basic amino acid substitutions in the human immunodeficiency virus type 1 subtype E envelope V3 loop on viral coreceptor usage and cell tropism. Journal of Virology 73, 5520-6.
61. 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, 71-4.
62. de Jong, J. J., de Ronde, A., Keulen, W., Tersmette, M. & Goudsmit, J. (1992). Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. Journal of Virology 66, 6777-80.
63. 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. Journal of Virology 74, 1069-78.
64. Dighe, P. K., Korber, B. & Foley, B. T. (1997). Human Retrovirus and AIDS, vol. III, Los Alamos National Laboratory, Los Alamos, NM, USA.
65. Orloff, G. M., Kalish, M. L., Chiphangwi, J., Potts, K. E., Ou, C. Y., Schochetman, G. et al. (1993). V3 loops of HIV-1 specimens from pregnant women in Malawi uniformly lack a potential N-linked glycosylation site. AIDS Research and Human Retroviruses 9, 705-6.
66. Wolinsky, S. M., Wike, A. M., Korber, B. T. M., Hutto, C., Parks, W. P., Rosenblum, L. L. et al. (1992). Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science 255, 1134-7.
67. van Harmelen, J., Wood, R., Lambrick, M., Rybicki, E. P., Williamson, A. L. & Williamson, C. (1997). An association between HIV-1 subtypes and mode of transmission in Cape Town, South Africa. AIDS 11, 81-7.
68. Neilson, J. R., John, G. C., Carr, J. K., Lewis, P., Kreiss, J. K., Jackson, S. et al. (1999). Subtypes of human immunodeficiency virus type 1 and disease stage among women in Nairobi, Kenya. Journal of Virology 73, 4393-403.
69. Kaleebu, P., French, N., Mahe, C., Yirrell, D., Watera, C., Lyagoba, F. et al. (2002). Effect of human immunodeficiency virus (HIV) type 1 envelope subtypes A and D on disease progression in a large cohort of HIV-1-positive persons in Uganda. Journal of Infectious Diseases 185, 1244-50.
70. Kanki, P. J., Hamel, D. J., Sankale, J. L., Hsieh, C., Thior, I., Barin, F. et al. (1999). Human immunodeficiency virus type 1 subtypes differ in disease progression. Journal of Infectious Diseases 179, 68-73.
71. Hirsch, M. S., Conway, B., D'Aquila, R. T., Johnson, V. A., Brun-Vezinet, F., Clotet, B. et al. (1998). Antiretroviral drug resistance testing in adults with HIV infection: implications for clinical management. International AIDS Society-USA Panel. Journal of the American Medical Association 279, 1984-91.
72. Wainberg, M. A. & Friedland, G. (1999). Public health implications of antiretroviral therapy and HIV drug resistance. Journal of the American Medical Association 279, 1977-83.
73. Schinazi, R. F., Larder, B. A. & Mellors, J. W. (1997). Mutations in retroviral genes associated with drug resistance. International Antiviral News 5, 2-14.
74. Condra, J. (1998). Virological and clinical implications of resistance to HIV-1 protease inhibitors. Drug Resistance Updates 1, 292-9.
75. Haesevelde, M. V., Decourt, J. L., De Leys, R. J., Vanderborght, B., van der Groen, G., van Heuverswijn, H. et al. (1994). Genomic cloning and complete sequence analysis of a highly divergent African human immunodeficiency virus isolate. Journal of Virology 68, 1586-96.
76. Cornelissen, M., van den Burg, R., Zorgdrager, F., Lukashov, V. & Goudsmit, J. (1997). pol gene diversity of five human immunodeficiency virus type 1 subtypes: evidence for naturally occurring mutations that contribute to drug resistance, limited recombination patterns, and common ancestry for subtypes B and D. Journal of Virology 71, 6348-58.
77. Gao, Q., Gu, Z., Salomon, H., Nagai, K., Parniak, M. A. & Wainberg, M. A. (1994). Generation of multiple drug resistance by sequential in vitro passage of the human immunodeficiency virus type 1. Archives of Virology 136, 111-22.
78. Shafer, R. W., Winters, M. A., Palmer, S. & Merigan, T. C. (1998). Multiple concurrent reverse transcriptase and protease mutations and multidrug resistance of HIV-1 isolates from heavily treated patients. Annals of Internal Medicine 128, 906-11.
79. Becker-Pergola, G., Kataaha, P., Johnston-Dow, L., Fung, S., Jackson, J. B. & Eshleman, S. H. (2000). Analysis of HIV type 1 protease and reverse transcriptase in antiretroviral drug-naive Ugandan adults. AIDS Research and Human Retroviruses 16, 807-13.
80. Quinones-Mateu, M. E., Albright, J. L., Mas, A., Soriano, V. & Arts, E. J. (1998). Analysis of pol gene heterogeneity, viral quasi-species, and drug resistance in individuals infected with group O strains of human immunodeficiency virus type 1. Journal of Virology 72, 9002-15.
81. Descamps, D., Collin, G., Loussert-Ajaka, I., Saragosti, S., Simon, F. & Brun-Vezinet, F. (1995). HIV-1 group O sensitivity to antiretroviral drugs. AIDS 9, 977-8.
82. Descamps, D., Collin, G., Letourneur, F., Apetrei, C., Damond, F., Loussert-Ajaka, I. et al. (1997). Susceptibility of human immunodeficiency virus type 1 group O isolates to antiretroviral agents: in vitro phenotypic and genotypic analyses. Journal of Virology 71, 8893-8.
83. Tantillo, C., Ding, J., Jacobo-Molina, R., Nanni, R. G., Boyer, P. L., Hughes, S. H. et al. (1994). Locations of anti-AIDS drug binding sites and resistance mutations in the three-dimensional structure of HIV-1 reverse transcriptase. Implications for mechanisms of drug inhibition and resistance. Journal of Molecular Biology 243, 369-87.
84. Apetrei, C., Descamps, D., Collin, G., Loussert-Ajaka, I., Damond, F., Duca, M. et al. (1998). Human immunodeficiency virus type 1 subtype F reverse transcriptase sequence and drug susceptibility. Journal of Virology 72, 3534-38.
85. Shafer, R. W., Eisen, J. A., Merigan, T. C. & Katzenstein, D. A. (1997). Sequence and drug susceptibility of subtype C reverse transcriptase from human immunodeficiency virus type 1 seroconverters in Zimbabwe. Journal of Virology 71, 5441-8.
86. Birk, M. & Sonnerborg, A. (1998). Variations in HIV-1 pol gene associated with reduced sensitivity to antiretroviral drugs in treatment-naive patients. AIDS 12, 2369-75.
87. Palmer, S., Alaeus, A., Albert, J. & Cox, S. (1998). Drug susceptibility of subtypes A, B, C, D, and E human immunodeficiency virus type 1 primary isolates. AIDS Research and Human Retroviruses 14, 157-62.
88. Pillay, D., Walker, S., Gibb, D. M., de Rossi, A., Kaye, S., Ait-Khaleb, M. et al. (2002). Impact of human immunodeficiency virus type 1 subtypes on virologic response and emergence of drug resistance among children in the Paediatric European Network for Treatment of AIDS (PENTA) 5 trial. Journal of Infectious Diseases 186, 617-25.
89. Salminen, M. O., Johansson, B. O., Sonnerborg, A., Ayehunie, S., Gotte, D., Leinikki, P. et al. (1996). Full-length sequence of Ethiopian human immunodeficiency virus type 1 (HIV-1) isolate of genetic subtype C. AIDS Research and Human Retroviruses 12, 1329-39.
90. Ayenie, S., Johansson, B. O., Salminen, M. O., Leinikki, P., Sonnerborg, A., Work-Zewdie, D. et al. (1991). HIV-1 in Ethiopia: phylogenetic divergence from other HIV-1 strains. Virus Genes 5, 359-66.
91. Dietrich, U., Grez, M., von Briesen, H., Panhans, B., Geissendorfer, M., Kuhnel, H. et al. (1993). HIV-1 strains from India are highly divergent from prototypic African and US/European strains, but are linked to a South African isolate. AIDS 7, 23-7.
92. Robertson, D., Sharp, P., McCutchan, F. & Hahn, B. H. (1995). Recombination in HIV-1. Nature 374, 124-6.
93. Zhu, T., Wang, N., Carr, A., Wolinsky, S. & Ho, D. (1995). Evidence for coinfection by multiple strains of human immunodeficiency virus type 1 subtype B in an acute seroconvertor. Journal of Virology 69, 1324-7.
94. Xin, K. Q., Ma, X. H., Crandall, K. A., Bukawa, H., Ishigatsubo, Y., Kawamoto, S. et al. (1995). Dual infection with HIV-1 Thai subtype B and E. Lancet 346, 1372-3.
95. Janini, L. M., Tanuri, A., Schechter, M., Peralta, J. M., Vicente, A. C., dela Torre, N. et al. (1998). Horizontal and vertical transmission of human immunodeficiency virus type 1 dual infections caused by viruses of subtypes B and C. Journal of Infectious Diseases 177, 227-31.
96. Adje, C., Cheingsong, R., Roels, T. H., Maurice, C., Djomand, G., Verbiest, W. et al. (2001). High prevalence of genotypic HIV-1 drug-resistant strains among patients receiving antiretroviral therapy in Abidjan, Côte d'Ivoire. Journal of Acquired Immune Deficiency Syndromes 26, 501-6.
97. Fatkenheuer, G., Theisen, A., Rockstroh, J., Grabow, T., Wicke, C., Becker, K. et al. (1997). Virological treatment failure of protease inhibitor therapy in an unselected cohort of HIV-infected patients. AIDS 11, F113-6.
98. Deeks, S. G., Hecht, F. M., Swanson, M., Elbeik, T., Loftus, R., Cohen, P. T. et al. (1999). HIV RNA and CD4 cell count response to protease inhibitor therapy in an urban AIDS clinic: response to both initial and salvage therapy. AIDS 13, F35-43.
99. Dabis, F., Msellati, P., Meda, N., Welffens-Ekra, C., You, B., Manigart, O. et al. (1999). 6 month efficacy, tolerance, and acceptability of a short regimen of oral zidovudine to reduce vertical transmission of HIV in breastfed children in Cote d'Ivoire and Burkina Faso: a double-blind placebo-controlled multicentre trial. Lancet 353, 786-92.
100. Bacheler, L., Jeffrey, S., Hanna, G., D'Aquila, R., Wallace, L., Logue, K. et al. (2001). Genotypic correlates of phenotypic resistance to efavirenz in virus isolates from patients failing nonnucleoside reverse transcriptase inhibitor therapy. Journal of Virology 75, 4999-5008.
101. Caride, E., Hertogs, K., Larder, B., Dehertogh, P., Brindeiro, R., Machado, E. et al. (2000). Genotyping and phenotyping analysis of B and non-B HIV-1 subtypes from Brazilian patients under HAART. Antiviral Therapy 5, Suppl. 3, 128 (abstract 164).
102. Pillay, D., Sinka, K., Rice, P., Peters, B., Clarke, J., Workman, J. et al. (2000). Impact of HIV-1 subtype on NNRTI resistance mutations. Antiviral Therapy 5, Suppl. 3, 128 (abstract 163).
103. Richman, D. D., Havlir, D., Corbeil, J., Looney, D., Ignacio, C., Spector, S. A. et al. (1994). Nevirapine resistance mutations of human immunodeficiency virus type 1 selected during therapy. Journal of Virology. 68, 1660-6.
104. Wainberg, M. A. (1999). HIV resistance to antagonists of viral reverse transcriptase. In AIDS and the New Viruses, 2nd edn (Dalgleish, A. & Weiss, R., Eds), pp. 223-49. Academic Press, London, UK.
105. Jackson, J. B., Becker-Pergola, G., Guay, L. A., Musoke, P., Mracna, M., Fowler, M. G. et al. (2000). Identification of the K103N resistance mutation in Ugandan women receiving nevirapine to prevent HIV-1 vertical transmission. AIDS 14, F111-5.
106. gag protein. Journal of Virology 67, 694-702.
107. Kelleher, A. D., Long, C., Holmes, E. C., Allen, R. L., Wilson, J., Conlon, C. et al. (2001). Clustered mutations in HIV-1 Gag are consistently required for escape from HLA-B27-restricted CTL responses. Journal of Experimental Medicine 193, 375-86.
108. Ridge, J. P., Di Rosa, F. & Matzinger, P. A. (1998). A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 393, 474-8.
109. McMichael, A. J. & Rowland-Jones, S. L. (2001). Cellular immune responses to HIV. Nature 410, 980-7.
110. Dalod, M., Harzic, M., Pellegrin, I., Dumon, B., Hoen, B., Sereni, D. et al. (1998). Evolution of cytotoxic T lymphocyte responses to human immunodeficiency virus type 1 in patients with symptomatic primary infection receiving antiretroviral triple therapy. Journal of Infectious Diseases 178, 61-9.
111. Gray, C. M., Lawrence, J., Schapiro, J. M., Altman, J. M., Winters, M. A., Crompton, M. et al. (1999). Frequency of class 1 HLA-restricted anti-HIV CD8+ T cells in individuals receiving highly active antiretroviral therapy (HAART). Journal of Immunology 162, 1780-9.
112. Samri, A., Haas, G., Duntze, J., Bouley, J. M., Calvez, V., Katlama, C. et al. (2000). Immunogenicity of mutations induced by nucleoside reverse transcriptase inhibitors for human immunodeficiency virus type 1-specific cytotoxic T cells. Journal of Virology 74, 9306-12.
113. Wainberg, M. A. & Cameron, D. W. (1998). HIV resistance to antiviral drugs: public health implications. Drug Resistance Updates 1, 104-8.
114. Walker, B. D., Flexner, C., Paradis, T. J., Fuller, T. C., Hirsch, M. S., Schooley, R. T. et al. (1988). HIV-1 reverse transcriptase is a target for cytotoxic T lymphocytes in infected individuals. Science 240, 64-6.
115. van der Burg, S. H., Klein, M. R., van de Velde, C. J. H., Kast, W. M., Miedema, F. & Melief, J. M. (1995). Induction of a primary human cytotoxic T-lymphocyte response against a novel conserved epitope in a functional sequence of HIV-1 reverse transcriptase. AIDS 9, 121-7.
116. Haas, G., Samri, A., Gomard, E., Hosmalin, A., Duntze, J. & Bouley, J. M. (1998). Cytotoxic T-cell responses to HIV-1 reverse transcriptase, integrase and protease. AIDS 12, 1427-36.
117. Day, C. L., Shea, A. K., Altfeld, M. A., Olson, D. P., Buchbinder, S. P. & Hecht, F. M. (2001). Relative dominance of epitope-specific cytotoxic T-lymphocyte responses in human immunodeficiency virus type 1-infected persons with shared HLA alleles. Journal of Virology 75, 6279-91.
118. Del Val, M., Schlicht, H. J., Ruppert, T., Reddehase, M. J. & Koszinowski, U. H. (1991). Efficient processing of an antigenic sequence for presentation by MHC class 1 molecules depends on its neighboring residues in the protein. Cell 66, 1145-53.
119. Ossendorp, F., Eggers, M., Neisig, A., Ruppert, T., Groettrup, M., Sijts, A. et al. (1996). A single residue exchange within a viral CTL epitope alters proteasome-mediated degradation resulting in lack of antigen presentation. Immunity 5, 115-24.
120. Goulder, P. J., Phillips, R. E., Colbert, R. A., McAdam, S., Ogg, G., Nowak, M. A. et al. (1997). Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nature Medicine 3, 212-7.
121. Koup, R. A., Safrit, J. T., Cao, Y., Andrews, C. A., McLeod, G., Borkowsky, W. et al. (1994). Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. Journal of Virology 68, 4650-5.
122. Brenner, B. G. & Wainberg, M. A. (2000). The role of antiretrovirals and drug resistance in vertical transmission of HIV-1 infection. Annals of the New York Academy of Sciences 918, 9-15.