1887

Abstract

A small subset of human immunodeficiency virus type 1 (HIV-1)-infected, therapy-naive individuals – referred to as long-term non-progressors (LTNPs) – maintain a favourable course of infection, often being asymptomatic for many years with high CD4 and CD8 T-cell counts (>500 cells μl) and low plasma HIV-RNA levels (<10 000 copies ml). Research in the field has undergone considerable development in recent years and LTNPs offer a piece of the puzzle in understanding the ways that persons can naturally control HIV-1 infection. Their method of control is based on viral, genetic and immunological components. With respect to virological features, genomic sequencing has shown that some LTNPs are infected with attenuated strains of HIV-1 and harbour mutant , , or genes that contain single nuclear polymorphisms, or less frequently, large deletions, in conserved domains. Studies have also shown that some LTNPs have unique genetic advantages, including heterozygosity for the polymorphism, and have been found with excitatory mutations that upregulate the production of the chemokines that competitively inhibit HIV-1 binding to CCR5 or CXCR4. Lastly, immunological factors are crucial for providing LTNPs with a natural form of control, the most important being robust HIV-specific CD4 and CD8 T-cell responses that correlate with lower viral loads. Many LTNPs carry the allele that enhances presentation of antigenic peptides on the surface of infected CD4 cells to cytotoxic CD8 T cells. For these reasons, LTNPs serve as an ideal model for HIV-1 vaccine development due to their natural control of HIV-1 infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.027102-0
2011-02-01
2019-08-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/2/247.html?itemId=/content/journal/jgv/10.1099/vir.0.027102-0&mimeType=html&fmt=ahah

References

  1. Alexander, L., Weiskopf, E., Greenough, T. C., Gaddis, N. C., Auerbach, M. R., Malim, M. H., O'Brien, S. J., Walker, B. D., Sullivan, J. L. & other authors ( 2000; ). Unusual polymorphisms in human immunodeficiency virus type 1 associated with nonprogressive infection. J Virol 74, 4361–4376.[CrossRef]
    [Google Scholar]
  2. Alexander, L., Aquino-DeJesus, M. J., Chan, M. & Andiman, W. A. ( 2002; ). Inhibition of human immunodeficiency virus type 1 (HIV-1) replication by a two-amino-acid insertion in HIV-1 Vif from a nonprogressing mother and child. J Virol 76, 10533–10539.[CrossRef]
    [Google Scholar]
  3. Alter, G. & Altfeld, M. ( 2009; ). NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med 265, 29–42.[CrossRef]
    [Google Scholar]
  4. An, P., Martin, M. P., Nelson, G. W., Carrington, M., Smith, M. W., Gong, K., Vlahov, D., O'Brien, S. J. & Winkler, C. A. ( 2000; ). Influence of CCR5 promoter haplotypes on AIDS progression in African-Americans. AIDS 14, 2117–2122.[CrossRef]
    [Google Scholar]
  5. An, P., Bleiber, G., Duggal, P., Nelson, G., May, M., Mangeat, B., Alobwede, I., Trono, D., Viahov, D. & other authors ( 2004; ). APOBEC3G genetic variants and their influence on progression to AIDS. J Virol 78, 11070–11076.[CrossRef]
    [Google Scholar]
  6. Anzala, A. O., Ball, T. B., Rostron, T., O'Brien, S. J., Plummer, F. A. & Rowland-Jones, S. L. ( 1998; ). CCR2–64I allele and genotype association with delayed AIDS progression in African women. University of Nairobi Collaboration for HIV Research. Lancet 351, 1632–1633.[CrossRef]
    [Google Scholar]
  7. Bailey, J. R., Zhang, H., Wegweiser, B. W., Yang, H. C., Herrera, L., Ahonkhai, A., Williams, T. M., Siliciano, R. F. & Blankson, J. N. ( 2007; ). Evolution of HIV-1 in an HLA-B*57-positive patient during virologic escape. J Infect Dis 196, 50–55.[CrossRef]
    [Google Scholar]
  8. Baker, B. M., Block, B. L., Rothchild, A. C. & Walker, B. D. ( 2009; ). Elite control of HIV infection: implications for vaccine design. Expert Opin Biol Ther 9, 55–69.[CrossRef]
    [Google Scholar]
  9. Bello, G., Casado, C., Sandonis, V., Alonso-Nieto, M., Vicario, J. L., García, S., Hernando, V., Rodríguez, C., del Romero, J. & other authors ( 2005; ). A subset of human immunodeficiency virus type I long-term non-progressors is characterized by the unique presence of ancestral sequences in the viral population. J Gen Virol 86, 355–364.[CrossRef]
    [Google Scholar]
  10. Bello, G., Velasco-de-Castro, C. A., Bongertz, V., Santos Rodrigues, C. A., Giacoia-Gripp, C. B. W., Pilotto, J. H., Grinsztejn, B., Veloso, V. G. & Morgado, M. G. ( 2009; ). Immune activation and antibody responses in non-progressing elite controller individuals infected with HIV-1. J Med Virol 81, 1681–1690.[CrossRef]
    [Google Scholar]
  11. Benlahrech, A., Harris, J., Meiser, A., Papagatsias, T., Hornig, J., Hayes, P., Lieber, A., Athanasopoulos, T., Bachy, V. & other authors ( 2009; ). Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1. Proc Natl Acad Sci U S A 106, 19940–19945.[CrossRef]
    [Google Scholar]
  12. Betts, M. R., Krowka, J. F., Kepler, T. B., Davidian, M., Christopherson, C., Kwok, S., Louie, L., Eron, J., Sheppard, H. & other authors ( 1999; ). Human immunodeficiency virus type 1-specific cytotoxic T lymphocyte activity is inversely correlated with HIV type 1 viral load in HIV type 1-infected long-term survivors. AIDS Res Hum Retroviruses 15, 1219–1228.[CrossRef]
    [Google Scholar]
  13. Betts, M. R., Nason, M. C., West, S. M., De Rosa, S. C., Migueles, S. A., Abraham, J., Lederman, M. M., Benito, J. M., Goepfert, P. A. & other authors ( 2006; ). HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107, 4781–4789.[CrossRef]
    [Google Scholar]
  14. Blankson, J. N., Bailey, J. R., Thayil, S., Yang, H. C., Lassen, K., Lai, J., Gandhi, S. K., Siliciano, J. D., Williams, T. M. & other authors ( 2007; ). Isolation and characterization of replication-competent human immunodeficiency virus type 1 from a subset of elite suppressors. J Virol 81, 2508–2518.[CrossRef]
    [Google Scholar]
  15. Boaz, M. J., Waters, A., Murad, S., Easterbrook, P. J. & Vyakarnam, A. ( 2002; ). Presence of HIV-1 Gag-specific IFN-γ+IL-2+ and CD28+IL-2+ CD4 T cell responses is associated with nonprogression in HIV-1 infection. J Immunol 169, 6376–6385.[CrossRef]
    [Google Scholar]
  16. Bochud, P. Y., Hersberger, M., Taffe, P., Bochud, M., Stein, C. M., Rodrigues, S. D., Calandra, T., Francioli, P., Telenti, A. & other authors ( 2007; ). Polymorphisms in Toll-like receptor 9 influence the clinical course of HIV-1 infection. AIDS 21, 441–446.[CrossRef]
    [Google Scholar]
  17. Braibant, M., Agut, H., Rouzioux, C., Costagliola, D., Autran, B. & Barin, F. ( 2008; ). Characteristics of the env genes of HIV type 1 quasispecies in long-term nonprogressors with broadly neutralizing antibodies. J Acquir Immune Defic Syndr 47, 274–284.[CrossRef]
    [Google Scholar]
  18. Brambilla, A., Turchetto, L., Gatti, A., Bovolenta, C., Veglia, F., Santagostino, E., Gringeri, A., Clementi, M., Poli, G. & other authors ( 1999; ). Defective nef alleles in a cohort of hemophiliacs with progressing and nonprogressing HIV-1 infection. Virology 259, 349–368.[CrossRef]
    [Google Scholar]
  19. Buchbinder, S. P., Mehrotra, D. V., Duerr, A., Fitzgerald, D. W., Mogg, R., Li, D., Gilbert, P. B., Lama, J. R., Marmor, M. & other authors ( 2008; ). Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomized, placebo-controlled, test-of-concept trial. Lancet 372, 1881–1893.[CrossRef]
    [Google Scholar]
  20. Burton, D. R. & Weiss, R. A. ( 2010; ). A boost for HIV vaccine design. Science 329, 770–773.[CrossRef]
    [Google Scholar]
  21. Calugi, G., Montella, F., Favalli, C. & Benedetto, A. ( 2006; ). Entire genome of a strain of human immunodeficiency virus type 1 with a deletion of nef that was recovered 20 years after primary infection: large pool of proviruses with deletions of env. J Virol 80, 11892–11896.[CrossRef]
    [Google Scholar]
  22. Caly, L., Saksena, N. K., Piller, S. C. & Jans, D. A. ( 2008; ). Impaired nuclear import and viral incorporation of Vpr derived from a HIV long-term non-progressor. Retrovirology 5, 67.[CrossRef]
    [Google Scholar]
  23. Carrington, M. & O'Brien, S. J. ( 2003; ). The influence of HLA genotype on AIDS. Annu Rev Med 54, 535–551.[CrossRef]
    [Google Scholar]
  24. Carrington, M., Nelson, G. W., Martin, M. P., Kissner, T., Vlahov, D., Goedert, J. J., Kaslow, R., Buchbinder, S., Hoots, K. & other authors ( 1999; ). HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283, 1748–1752.[CrossRef]
    [Google Scholar]
  25. Casartelli, N., Di Matteo, G., Potesta, M., Rossi, P. & Doria, M. ( 2003; ). CD4 and major histocompatibility complex class I downregulation by the human immunodeficiency virus type 1 nef protein in pediatric AIDS progression. J Virol 77, 11536–11545.[CrossRef]
    [Google Scholar]
  26. Cecilia, D., Kleeberger, C., Munoz, A., Giorgi, J. V. & Zolla-Pazner, S. ( 1999; ). A longitudinal study of neutralizing antibodies and disease progression in HIV-1-infected subjects. J Infect Dis 179, 1365–1374.[CrossRef]
    [Google Scholar]
  27. Chakraborty, R., Reinis, M., Rostron, T., Philpott, S., Dong, T., D'Agostino, A., Musoke, R., de Silva, E., Stumpf, M. & other authors ( 2006; ). nef gene sequence variation among HIV-1-infected African children. HIV Med 7, 75–84.[CrossRef]
    [Google Scholar]
  28. Choudhary, S. K., Choudhary, N. R., Kimbrell, K. C., Colasanti, J., Ziogas, A., Kwa, D., Schuitemaker, H. & Camerini, D. ( 2005; ). R5 human immunodeficiency virus type 1 infection of fetal thymic organ culture induces cytokine and CCR5 expression. J Virol 79, 458–471.[CrossRef]
    [Google Scholar]
  29. Cohen, O. J., Vaccarezza, M., Lam, G. K., Baird, B. F., Wildt, K., Murphy, P. M., Zimmerman, P. A., Nutman, T. B., Fox, C. H. & other authors ( 1997; ). Heterozygosity for a defective gene for CC chemokine receptor 5 is not the sole determinant for the immunologic and virologic phenotype of HIV-infected long-term nonprogressors. J Clin Invest 100, 1581–1589.[CrossRef]
    [Google Scholar]
  30. Crotti, A., Neri, F., Corti, D., Ghezzi, S., Heltai, S., Baur, A., Poli, G., Santagostino, E. & Vicenzi, E. ( 2006; ). Nef alleles from human immunodeficiency virus type 1-infected long-term-nonprogressor hemophiliacs with or without late disease progression are defective in enhancing virus replication and CD4 down-regulation. J Virol 80, 10663–10674.[CrossRef]
    [Google Scholar]
  31. Deacon, N. J., Tsykin, A., Solomon, A., Smith, K., Ludford-Menting, M., Hooker, D. J., McPhee, D. A., Greenway, A. L., Ellett, A. & other authors ( 1995; ). Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270, 988–991.[CrossRef]
    [Google Scholar]
  32. Dean, M., Carrington, M., Winkler, C., Huttley, G. A., Smith, M. W., Allikmets, R., Goedert, J. J., Buchbinder, S. P., Vittinghoff, E. & other authors ( 1996; ). Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science 273, 1856–1862.[CrossRef]
    [Google Scholar]
  33. Deeks, S. G., Schweighardt, B., Wrin, T., Galovich, J., Hoh, R., Sinclair, E., Hunt, P., McCune, J. M., Martin, J. N. & other authors ( 2006; ). Neutralizing antibody response against autologous and heterologous viruses in acute versus chronic human immunodeficiency virus (HIV) infection: evidence for a constraint on the ability of HIV to completely evade neutralizing antibody responses. J Virol 80, 6155–6164.[CrossRef]
    [Google Scholar]
  34. Di Lorenzo, A. L. ( 2008; ). “HLA-B27 Syndromes.” eMedicine. WebMD, http://emedicine.medscape.com/article/1201027-overview.
  35. Dolan, M. J., Kulkarni, H., Camargo, J. F., He, W., Smith, A., Anaya, J. M., Miura, T., Hecht, F. M., Mamtani, M. & other authors ( 2007; ). CCL3L1 and CCR5 influence cell-mediated immunity and affect HIV-AIDS pathogenesis via viral entry-independent mechanisms. Nat Immunol 8, 1324–1336.[CrossRef]
    [Google Scholar]
  36. Doria-Rose, N. A., Klein, R. M., Daniels, M. G., O'Dell, S., Nason, M., Lapedes, A., Bhattacharya, T., Migueles, S. M., Wyatt, R. T. & other authors ( 2010; ). Breadth of human immunodeficiency virus-specific neutralizing activity in sera: clustering analysis and association with clinical variables. J Virol 84, 1631–1636.[CrossRef]
    [Google Scholar]
  37. Emu, B., Sinclair, E., Hatano, H., Ferre, A., Shacklett, B., Martin, J. N., McCune, J. M. & Deeks, S. G. ( 2008; ). HLA class I-restricted T-cell responses may contribute to the control of human immunodeficiency virus infection, but such responses are not always necessary for long-term virus control. J Virol 82, 5398–5407.[CrossRef]
    [Google Scholar]
  38. Estes, J. D., Gordon, S. N., Zeng, M., Chahroudi, A. M., Dunham, R. M., Staprans, S. I., Reilly, C. S., Silvestri, G. & Haase, A. T. ( 2008; ). Early resolution of acute immune activation and induction of PD-1 in SIV-infected sooty mangabeys distinguishes nonpathogenic from pathogenic infection in rhesus macaques. J Immunol 180, 6798–6807.[CrossRef]
    [Google Scholar]
  39. Eugen-Olsen, J., Iversen, A. K., Garred, P., Koppelhus, U., Pedersen, C., Benfield, T. L., Sorensen, A. M., Katzenstein, T., Dickmeiss, E. & other authors ( 1997; ). Heterozygosity for a deletion in the CKR-5 gene leads to prolonged AIDS-free survival and slower CD4 T-cell decline in a cohort of HIV-seropositive individuals. AIDS 11, 305–310.[CrossRef]
    [Google Scholar]
  40. Ferre, A. L., Lemongello, D., Hunt, P. W., Morris, M. M., Garcia, J. C., Pollard, R. B., Yee, H. F., Martin, J. N., Deeks, S. G. & other authors ( 2010; ). Immunodominant HIV-specific CD8+ T-cell responses are common to blood and gastrointestinal mucosa, and gag-specific responses dominate in rectal mucosa of HIV controllers. J Virol 84, 10354–10365.[CrossRef]
    [Google Scholar]
  41. Garred, P., Madsen, H. O., Balslev, U., Hofmann, B., Pedersen, C., Gerstoft, J. & Svejgaard, A. ( 1997; ). Susceptibility to HIV infection and progression of AIDS in relation to variant alleles of mannose-binding lectin. Lancet 349, 236–240.[CrossRef]
    [Google Scholar]
  42. Geffin, R., Wolf, D., Muller, R., Hill, M. D., Stellwag, E., Freitag, M., Sass, G., Scott, G. B. & Baur, A. S. ( 2000; ). Functional and structural defects in HIV type 1 nef genes derived from pediatric long-term survivors. AIDS Res Hum Retroviruses 16, 1855–1868.[CrossRef]
    [Google Scholar]
  43. Geldmacher, C., Currier, J. R., Herrmann, E., Haule, A., Kuta, E., McCutchan, F., Njovu, L., Geis, S., Hoffmann, O. & other authors ( 2007; ). CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J Virol 81, 2440–2448.[CrossRef]
    [Google Scholar]
  44. Goicoechea, M., Smith, D., May, S., Mathews, C. & Spina, C. ( 2009; ). Prevalence and T cell phenotype of slow HIV disease progressors with robust HIV replication. J Acquir Immune Defic Syndr 52, 299.[CrossRef]
    [Google Scholar]
  45. Gonzalez, E., Kulkarni, H., Bolivar, H., Mangano, A., Sanchez, R., Catano, G., Nibbs, R. J., Freedman, B. I., Quinones, M. P. & other authors ( 2005; ). The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307, 1434–1440.[CrossRef]
    [Google Scholar]
  46. Goulder, P. J., Bunce, M., Krausa, P., McIntyre, K., Crowley, S., Morgan, B., Edwards, A., Giangrande, P., Phillips, R. E. & other authors ( 1996; ). Novel, cross-restricted, conserved, and immunodominant cytotoxic T lymphocyte epitopes in slow progressors in HIV type 1 infection. AIDS Res Hum Retroviruses 12, 1691–1698.[CrossRef]
    [Google Scholar]
  47. Gulzar, N. & Copeland, K. F. ( 2004; ). CD8+ T-cells: function and response to HIV infection. Curr HIV Res 2, 23–37.[CrossRef]
    [Google Scholar]
  48. Gupta, S. B., Jacobson, L. P., Margolick, J. B., Rinaldo, C. R., Phair, J. P., Jamieson, B. D., Mehrotra, D. V., Robertson, M. N. & Straus, W. L. ( 2007; ). Estimating the benefit of an HIV-1 vaccine that reduces viral load set point. J Infect Dis 195, 546–550.[CrossRef]
    [Google Scholar]
  49. He, W., Neil, S., Kulkarni, H., Wright, E., Agan, B. K., Marconi, V. C., Dolan, M. J., Weiss, R. A. & Ahuja, S. K. ( 2008; ). Duffy antigen receptor for chemokines mediates trans-infection of HIV-1 from red blood cells to target cells and affects HIV-AIDS susceptibility. Cell Host Microbe 4, 52–62.[CrossRef]
    [Google Scholar]
  50. Hendel, H., Henon, N., Lebuanec, H., Lachgar, A., Poncelet, H., Caillat-Zucman, S., Winkler, C. A., Smith, M. W., Kenefic, L. & other authors ( 1998; ). Distinctive effects of CCR5, CCR2, and SDF1 genetic polymorphisms in AIDS progression. J Acquir Immune Defic Syndr Hum Retrovirol 19, 381–386.[CrossRef]
    [Google Scholar]
  51. Hendel, H., Caillat-Zucman, S., Lebuanec, H., Carrington, M., O'Brien, S., Andrieu, J. M., Schachter, F., Zagury, D., Rappaport, J. & other authors ( 1999; ). New class I and II HLA alleles strongly associated with opposite patterns of progression to AIDS. J Immunol 162, 6942–6946.
    [Google Scholar]
  52. Huang, Y., Paxton, W. A., Wolinsky, S. M., Neumann, A. U., Zhang, L., He, T., Kang, S., Ceradini, D., Jin, Z. & other authors ( 1996; ). The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat Med 2, 1240–1243.[CrossRef]
    [Google Scholar]
  53. Huang, Y., Zhang, L. & Ho, D. D. ( 1998; ). Characterization of gag and pol sequences from long-term survivors of human immunodeficiency virus type 1 infection. Virology 240, 36–49.[CrossRef]
    [Google Scholar]
  54. Hunt, P. W. ( 2009; ). Natural control of HIV-1 replication and long-term nonprogression: overlapping but distinct phenotypes. J Infect Dis 200, 1636–1638.[CrossRef]
    [Google Scholar]
  55. Hunt, P. W., Brenchley, J., Sinclair, E., McCune, J. M., Roland, M., Page-Shafer, K., Hsue, P., Emu, B., Krone, M. & other authors ( 2008; ). Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 197, 126–133.[CrossRef]
    [Google Scholar]
  56. Ioannidis, J. P., Rosenberg, P. S., Goedert, J. J., Ashton, L. J., Benfield, T. L., Buchbinder, S. P., Coutinho, R. A., Eugen-Olsen, J., Gallart, T. & other authors ( 2001; ). Effects of CCR5-Delta32, CCR2–64I, and SDF-1 3′A alleles on HIV-1 disease progression: an international meta-analysis of individual-patient data. Ann Intern Med 135, 782–795.[CrossRef]
    [Google Scholar]
  57. Iversen, A. K., Shpaer, E. G., Rodrigo, A. G., Hirsch, M. S., Walker, B. D., Sheppard, H. W., Merigan, T. C. & Mullins, J. I. ( 1995; ). Persistence of attenuated rev genes in a human immunodeficiency virus type 1-infected asymptomatic individual. J Virol 69, 5743–5753.
    [Google Scholar]
  58. Jagannathan, P., Osborne, C. M., Royce, C., Manion, M. M., Tilton, J. C., Li, L., Fischer, S., Hallahan, C. W., Metcalf, J. A. & other authors ( 2009; ). Comparisons of CD8+ T cells specific for human immunodeficiency virus, hepatitis C virus, and cytomegalovirus reveal differences in frequency, immunodominance, phenotype, and interleukin-2 responsiveness. J Virol 83, 2728–2742.[CrossRef]
    [Google Scholar]
  59. Jang, D. H., Choi, B. S. & Kim, S. S. ( 2008; ). The effects of RANTES/CCR5 promoter polymorphisms on HIV disease progression in HIV-infected Koreans. Int J Immunogenet 35, 101–105.[CrossRef]
    [Google Scholar]
  60. Javanbakht, H., An, P., Gold, B., Petersen, D. C., O'Huigin, C., Nelson, G. W., O'Brien, S. J., Kirk, G. D., Detels, R. & other authors ( 2006; ). Effects of human TRIM5α polymorphisms on antiretroviral function and susceptibility to human immunodeficiency virus infection. Virology 354, 15–27.[CrossRef]
    [Google Scholar]
  61. Jin, X., Wu, H. & Smith, H. ( 2007; ). APOBEC3G levels predict rates of progression to AIDS. Retrovirology 4, 20.[CrossRef]
    [Google Scholar]
  62. Kalinkovich, A., Weisman, Z. & Bentwich, Z. ( 1999; ). Chemokines and chemokine receptors: role in HIV infection. Immunol Lett 68, 281–287.[CrossRef]
    [Google Scholar]
  63. Kirchhoff, F., Easterbrook, P. J., Douglas, N., Troop, M., Greenough, T. C., Weber, J., Carl, S., Sullivan, J. L. & Daniels, R. S. ( 1999; ). Sequence variations in human immunodeficiency virus type 1 Nef are associated with different stages of disease. J Virol 73, 5497–5508.
    [Google Scholar]
  64. Klein, M. R., van der Burg, S. H., Hovenkamp, E., Holwerda, A. M., Drijfhout, J. W., Melief, C. J. & Miedema, F. ( 1998; ). Characterization of HLA-B57-restricted human immunodeficiency virus type 1 Gag- and RT-specific cytotoxic T lymphocyte responses. J Gen Virol 79, 2191–2201.
    [Google Scholar]
  65. Koning, F. A., Kwa, D., Boeser-Nunnink, B., Dekker, J., Vingerhoed, J., Hiemstra, H. & Schuitemaker, H. ( 2003; ). Decreasing sensitivity to RANTES (regulated on activation, normally T cell-expressed and -secreted) neutralization of CC chemokine receptor 5-using, non-syncytium-inducing virus variants in the course of human immunodeficiency virus type 1 infection. J Infect Dis 188, 864–872.[CrossRef]
    [Google Scholar]
  66. Lai, M. & Chen, J. ( 2006; ). The role of Vpr in HIV-1 disease progression is independent of its G2 arrest induction function. Cell Cycle 5, 2275–2280.[CrossRef]
    [Google Scholar]
  67. Land, A. M., Ball, B. T., Luo, M., Pilon, R., Sandstrom, P., Embree, J. E., Wachihi, C., Kimani, J. & Plummer, F. A. ( 2008; ). Human immunodeficiency virus (HIV) type 1 proviral hypermutation correlates with CD4 count in HIV-infected women from Kenya. J Virol 82, 8172–8182.[CrossRef]
    [Google Scholar]
  68. Lassen, K. G., Lobritz, M. A., Bailey, J. R., Johnston, S., Nguyen, S., Lee, B., Chou, T., Siliciano, R. F., Markowitz, M. & other authors ( 2009; ). Elite suppressor-derived HIV-1 envelope glycoprotein's exhibit reduced entry efficiency and kinetics. PLoS Pathog 5, e1000377.[CrossRef]
    [Google Scholar]
  69. Learmont, J. C., Geczy, A. F., Mills, J., Ashton, L. J., Raynes-Greenow, C. H., Garsia, R. J., Dyer, W. B., McIntyre, L., Oelrichs, R. B. & other authors ( 1999; ). Immunologic and virologic status after 14 to 18 years of infection with an attenuated strain of HIV-1. A report from the Sydney Blood Bank Cohort. N Engl J Med 340, 1715–1722.[CrossRef]
    [Google Scholar]
  70. Lee, E. Y., Yue, F. Y., Jones, R. B., Lo, C., Sheth, P., Hyrcza, M. D., Kovacs, C., Benko, E., Kaul, R. & other authors ( 2010; ). The impact of CCL3L1 copy number in an HIV-1-infected white population. AIDS 24, 1589–1591.[CrossRef]
    [Google Scholar]
  71. Leligdowicz, A. & Rowland-Jones, S. ( 2008; ). Tenets of protection from progression to AIDS: lessons from the immune responses to HIV-2 infection. Expert Rev Vaccines 7, 319–331.[CrossRef]
    [Google Scholar]
  72. Leslie, A., Matthews, P. C., Listgarten, J., Carlson, J. M., Kadie, C., Ndung'u, T., Brander, C., Coovadia, H., Walker, B. D. & other authors ( 2010; ). Additive contribution of HLA class I alleles in the immune control of HIV-1 infection. J Virol 84, 9879–9888.[CrossRef]
    [Google Scholar]
  73. Levy, J. A. ( 2009; ). HIV pathogenesis: 25 years of progress and persistent challenges. AIDS 23, 147–160.[CrossRef]
    [Google Scholar]
  74. Limou, S., Coulonges, C., Herbec, J. T., van Manen, D., An, P., Le Clerc, S., Delaneau, O., Diop, G., Taing, L. & other authors ( 2010; ). Multiple-cohort genetic association study reveals CXCR6 as a new chemokine receptor involved in long-term nonprogression to AIDS. J Infect Dis 202, 908–915.[CrossRef]
    [Google Scholar]
  75. Liu, H., Chao, D., Nakayama, E. E., Taguchi, H., Goto, M., Xin, X., Takamatsu, J. K., Saito, H., Ishikawa, Y. & other authors ( 1999; ). Polymorphism in RANTES chemokine promoter affects HIV-1 disease progression. Proc Natl Acad Sci U S A 96, 4581–4585.[CrossRef]
    [Google Scholar]
  76. Loffredo, J. T., Sidney, J., Bean, A. T., Beal, D. R., Bardet, W., Wahl, A., Hawkins, O. E., Piaskowski, S., Wilson, N. A. & other authors ( 2009; ). Two MHC class I molecules associated with elite control of immunodeficiency virus replication, Mamu-B*08 and HLA-B*2705, bind peptides with sequences similarity. J Immunol 182, 7763–7775.[CrossRef]
    [Google Scholar]
  77. Lopalco, L. ( 2004; ). Humoral immunity in HIV-1 exposure: cause or effect of HIV resistance? Curr HIV Res 2, 127–139.[CrossRef]
    [Google Scholar]
  78. Lopez-Larrea, C., Njobvu, P. D., Gonzalez, S., Blanco-Gelaz, M. A., Martinez-Borra, J. & Lopez-Vazquez, A. ( 2005; ). The HLA-B*5703 allele confers susceptibility to the development of spondylarthropathies in Zambian human immunodeficiency virus-infected patients with slow progression to acquired immunodeficiency syndrome. Arthritis Rheum 52, 275–279.[CrossRef]
    [Google Scholar]
  79. Lucotte, G. & Mercier, G. ( 1998; ). Distribution of the CCR5 gene 32-bp deletion in Europe. J Acquir Immune Defic Syndr Hum Retrovirol 19, 174–177.[CrossRef]
    [Google Scholar]
  80. Lum, J. J., Cohen, O. J., Nie, Z., Weaver, J. G., Gomez, T. S., Yao, X. J., Lynch, D., Pilon, A. A., Hawley, N. & other authors ( 2003; ). Vpr R77Q is associated with long-term nonprogressive HIV infection and impaired induction of apoptosis. J Clin Invest 111, 1547–1554.[CrossRef]
    [Google Scholar]
  81. Maas, J., de Roda Husman, A. M., Brouwer, M., Krol, A., Coutinho, R., Keet, I., van Leeuwen, R. & Schuitemaker, H. ( 1998; ). Presence of the variant mannose-binding lectin alleles associated with slower progression to AIDS. Amsterdam Cohort Study. AIDS 12, 2275–2280.[CrossRef]
    [Google Scholar]
  82. Macreadie, I. G., Castelli, L. A., Hewish, D. R., Kirkpatrick, A., Ward, A. C. & Azad, A. A. ( 1995; ). A domain of human immunodeficiency virus type 1 Vpr containing repeated H(S/F)RIG amino acid motifs causes cell growth arrest and structural defects. Proc Natl Acad Sci U S A 92, 2770–2774.[CrossRef]
    [Google Scholar]
  83. Madec, Y., Boufassa, F., Porter, K. & Meyer, L. ( 2005; ). Spontaneous control of viral load and CD4 cell count progression among HIV-1 seroconverters. AIDS 19, 2001–2007.[CrossRef]
    [Google Scholar]
  84. Magierowska, M., Theodorou, I., Debré, P., Sanson, F., Autran, B., Riviére, Y., Charron, D. & Costagliola, D. ( 1999; ). Combined genotypes of CCR5, CCR2, SDF1, and HLA genes can predict the long-term nonprogressor status in human immunodeficiency virus-1-infected individuals. Blood 93, 936–941.
    [Google Scholar]
  85. Mahalanabis, M., Jayaraman, P., Miura, T., Pereyra, F., Chester, E. M., Richardson, B., Walker, B. & Haigwood, N. L. ( 2009; ). Continuous viral escape and selection by autologous neutralizing antibodies in drug-naive human immunodeficiency virus controllers. J Virol 83, 662–672.[CrossRef]
    [Google Scholar]
  86. Malim, M. H., McCarn, D. F., Tiley, L. S. & Cullen, B. R. ( 1991; ). Mutational definition of the human immunodeficiency virus type 1 Rev activation domain. J Virol 65, 4248–4254.
    [Google Scholar]
  87. Mansfield, K., Lang, S. M., Gauduin, M., Sanford, H. B., Lifson, J. D., Johnson, R. P. & Desrosiers, R. C. ( 2008; ). Vaccine protection by live, attenuated simian immunodeficiency virus in the absence of high-titer antibody responses and high-frequency cellular immune responses measurable in the periphery. J Virol 82, 4135–4148.[CrossRef]
    [Google Scholar]
  88. Marchetti, G., Riva, A., Cesari, M., Bellistri, G. M., Gianelli, E., Casabianca, A., Orlandi, C., Magnani, M., Meroni, L. & other authors ( 2009; ). HIV-infected long-term nonprogressors display a unique correlative pattern between the interleukin-7/interleukin-7 receptor circuit and T-cell homeostasis. HIV Med 10, 422–431.[CrossRef]
    [Google Scholar]
  89. Martin, M. P., Dean, M., Smith, M. W., Winkler, C., Gerrard, B., Michael, N. L., Lee, B., Doms, R. W., Margolick, J. & other authors ( 1998; ). Genetic acceleration of AIDS progression by a promoter variant of CCR5. Science 282, 1907–1911.[CrossRef]
    [Google Scholar]
  90. Martin, M. P., Gao, X., Lee, J., Nelson, G. W., Detels, R., Goedert, J. J., Buchbinder, S., Hoots, K., Vlahov, D. & other authors ( 2002; ). Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 31, 429–434.
    [Google Scholar]
  91. Martin, M. P., Qi, Y., Gao, X., Yamada, E., Martin, J. N., Pereyra, F., Colombo, S., Brown, E. E., Shupert, L. W. & other authors ( 2007; ). Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 39, 733–740.[CrossRef]
    [Google Scholar]
  92. McDermott, D. H., Beecroft, M. J., Kleeberger, C. A., Al-Sharif, F. M., Ollier, W. E., Zimmerman, P. A., Boatin, B. A., Leitman, S. F., Detels, R. & other authors ( 2000; ). Chemokine RANTES promoter polymorphism affects risk of both HIV infection and disease progression in the Multicenter AIDS Cohort Study. AIDS 14, 2671–2678.[CrossRef]
    [Google Scholar]
  93. Meyer, L., Magierowska, M., Hubert, J. B., Mayaux, M. J., Misrahi, M., Le Chenadec, J., Debre, P., Rouzioux, C., Delfraissy, J. F. & other authors ( 1999; ). CCR5 Δ32 deletion and reduced risk of toxoplasmosis in persons infected with human immunodeficiency virus type 1. The SEROCO-HEMOCO-SEROGEST Study Groups. J Infect Dis 180, 920–924.[CrossRef]
    [Google Scholar]
  94. Michael, N. L., Louie, L. G., Rohrbaugh, A. L., Schultz, K. A., Dayhoff, D. E., Wang, C. E. & Sheppard, H. W. ( 1997; ). The role of CCR5 and CCR2 polymorphisms in HIV-1 transmission and disease progression. Nat Med 3, 1160–1162.[CrossRef]
    [Google Scholar]
  95. Middleton, D., Menchaca, L., Rood, H. & Komerofsky, R. ( 2003; ). New Allele Frequency Database: http://www.allelefrequencies.net. Tissue Antigens 61, 403–407.[CrossRef]
    [Google Scholar]
  96. Migueles, S. A. & Connors, M. ( 2001; ). Frequency and function of HIV-specific CD8+ T cells. Immunol Lett 79, 141–150.[CrossRef]
    [Google Scholar]
  97. Migueles, S. A. & Connors, M. ( 2010; ). Long-term nonprogressive disease among untreated HIV-infected individuals: clinical implications of understanding immune control of HIV. JAMA 304, 194–201.[CrossRef]
    [Google Scholar]
  98. Migueles, S. A., Sabbaghian, M. S., Shupert, W. L., Bettinotti, M. P., Marincola, F. M., Martino, L., Hallahan, C. W., Selig, S. M., Schwartz, D. & other authors ( 2000; ). HLA B*5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc Natl Acad Sci U S A 97, 2709–2714.[CrossRef]
    [Google Scholar]
  99. Migueles, S. A., Laborico, A. C., Shupert, W. L., Sabbaghian, M. S., Rabin, R., Hallahan, C. W., Van Baarle, D., Kostense, S., Miedema, F. & other authors ( 2002; ). HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat Immunol 3, 1061–1068.[CrossRef]
    [Google Scholar]
  100. Migueles, S. A., Osborne, C. M., Royce, C., Compton, A. A., Joshi, R. P., Weeks, K. A., Rood, J. E., Berkley, A. M. & Sacha, J. B. ( 2008; ). Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29, 1009–1021.[CrossRef]
    [Google Scholar]
  101. Mikhail, M., Wang, B. & Saksena, N. K. ( 2003; ). Mechanisms involved in non-progressive HIV disease. AIDS Rev 5, 230–244.
    [Google Scholar]
  102. Misrahi, M., Teglas, J. P., N'Go, N., Burgard, M., Mayaux, M. J., Rouzioux, C., Delfraissy, J. F. & Blanche, S. ( 1998; ). CCR5 chemokine receptor variant in HIV-1 mother-to-child transmission and disease progression in children. French Pediatric HIV Infection Study Group. JAMA 279, 277–280.[CrossRef]
    [Google Scholar]
  103. Miura, T., Brockman, M. A., Brumme, C. J., Brumme, Z. L., Carlson, J. M., Pereyra, F., Trocha, A., Addo, M. M., Block, B. L. & other authors ( 2008; ). Genetic characterization of human immunodeficiency virus type 1 in elite controllers: lack of gross genetic defects or common amino acid changes. J Virol 82, 8422–8430.[CrossRef]
    [Google Scholar]
  104. Miura, T., Brumme, Z. L., Brockman, M. A., Rosato, P., Sela, J., Brumme, C. J., Pereyra, F., Kaufmann, D. E., Trocha, A. & other authors ( 2010; ). Impaired replication capacity of acute/early viruses in persons who become HIV controllers. J Virol 84, 7581–7591.[CrossRef]
    [Google Scholar]
  105. Mologni, D., Citterio, P., Menzaghi, B., Zanone Poma, B., Riva, C., Broggini, V., Sinicco, A., Milazzo, L., Adorni, F. & other authors ( 2006; ). Vpr and HIV-1 disease progression: R77Q mutation is associated with long-term control of HIV-1 infection in different groups of patients. AIDS 20, 567–574.[CrossRef]
    [Google Scholar]
  106. Morawetz, R. A., Rizzardi, G. P., Glauser, D., Rutschmann, O., Hirschel, B., Perrin, L., Opravil, M., Flepp, M., von Overbeck, J. & other authors ( 1997; ). Genetic polymorphism of CCR5 gene and HIV disease: the heterozygous (CCR5/delta ccr5) genotype is neither essential nor sufficient for protection against disease progression. Swiss HIV Cohort. Eur J Immunol 27, 3223–3227.[CrossRef]
    [Google Scholar]
  107. Munkanta, M., Terunuma, H., Takahashi, M., Hanabusa, H., Miura, T., Ikeda, S., Sakai, M., Fuji, T., Takahashi, Y. & other authors ( 2005; ). HLA-B polymorphisms in Japanese HIV-1-infected long-term surviving hemophiliacs. Viral Immunol 2005, 500–505.
    [Google Scholar]
  108. Nakajima, T., Ohtani, H., Naruse, T., Shibata, H., Mimaya, J. I., Terunuma, H. & Kimura, A. ( 2007; ). Copy number variations of CCL3L1 and long-term prognosis of HIV-1 infection in asymptomatic HIV-infected Japanese with hemophilia. Immunogenetics 59, 793–798.[CrossRef]
    [Google Scholar]
  109. Nou, E., Zhou, Y., Nou, D. D. & Blankson, J. N. ( 2009; ). Effective downregulation of HLA-A*2 and HLA-B*57 by primary human immunodeficiency virus type 1 isolates cultured from elite suppressors. J Virol 83, 6941–6946.[CrossRef]
    [Google Scholar]
  110. O'Brien, K. L., Liu, J., King, S. L., Sun, Y., Schmitz, J. E., Lifton, M. A., Hutnick, N. A., Betts, M. R., Dubey, S. A. & other authors ( 2009; ). Adenovirus-specific immunity following immunization with an Ad5 HIV-1 vaccine candidate in humans. Nat Med 15, 873–875.[CrossRef]
    [Google Scholar]
  111. O'Connell, K. A., Han, Y., Williams, T. M., Siliciano, R. F. & Blankson, J. N. ( 2009; ). Role of natural killer cells in a cohort of elite suppressors: low frequency of the protective KIR3DS1 allele and limited inhibition of human immunodeficiency virus type 1 replication in vitro. J Virol 83, 5028–5034.[CrossRef]
    [Google Scholar]
  112. O'Connell, K. A., Brennan, T. P., Bailey, J. R., Ray, S. C., Siliciano, R. F. & Blankson, J. N. ( 2010; ). Control of HIV-1 in elite suppressors despite ongoing replication and evolution in plasma virus. J Virol 84, 7018–7028.[CrossRef]
    [Google Scholar]
  113. O'Connor, G. M., Holmes, A., Mulcahy, F. & Gardiner, C. M. ( 2007; ). Natural killer cells from long-term non-progressor HIV patients are characterized by altered phenotype and function. Clin Immunol 124, 277–283.[CrossRef]
    [Google Scholar]
  114. Okulicz, J. F., Marconi, V. C., Landrum, M. L., Wegner, S., Weintrob, A., Ganesan, A., Hale, B., Crum-Cianfione, N., Delmar, J. & other authors ( 2009; ). Clinical outcomes of elite controllers, viremic controllers, and long-term nonprogressors in the US Department of Defense HIV Natural History Study. J Infect Dis 200, 1714–1723.[CrossRef]
    [Google Scholar]
  115. Oelrichs, R., Tsykin, A., Rhodes, D., Solomon, A., Ellett, A., McPhee, D. & Deacon, N. ( 1998; ). Genomic sequence of HIV type 1 from four members of the Sydney Blood Bank Cohort of long-term nonprogressors. AIDS Res Hum Retroviruses 10, 811–814.
    [Google Scholar]
  116. Pantaleo, G. & Fauci, A. S. ( 1996; ). Immunopathogenesis of HIV infection. Annu Rev Microbiol 50, 825–854.[CrossRef]
    [Google Scholar]
  117. Papathanasopoulos, M. A., Patience, T., Meyers, T. M., McCutchan, F. E. & Morris, L. ( 2003; ). Full-length genome characterization of HIV type 1 subtype C isolates from two slow-progressing perinatally infected siblings in South Africa. AIDS Res Hum Retroviruses 19, 1033–1037.[CrossRef]
    [Google Scholar]
  118. Pereyra, F., Addo, M. M., Kaufmann, D. E., Liu, Y., Miura, T., Rathod, A., Baker, B., Trocha, A., Rosenberg, R. & other authors ( 2008; ). Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J Infect Dis 197, 563–571.[CrossRef]
    [Google Scholar]
  119. Piacentini, L., Biasin, M., Fenizia, C. & Clerici, M. ( 2009; ). Genetic correlates of protection against HIV infection: the ally within. J Intern Med 265, 110–124.[CrossRef]
    [Google Scholar]
  120. Pilgrim, A. K., Pantaleo, G., Cohen, O. J., Fink, L. M., Zhou, J. Y., Zhou, J. T., Bolognesi, D. P., Fauci, A. S. & Montefiori, D. C. ( 1997; ). Neutralizing antibody responses to human immunodeficiency virus type 1 in primary infection and long-term-nonprogressive infection. J Infect Dis 176, 924–932.[CrossRef]
    [Google Scholar]
  121. Potter, S. J., Lacabaratz, C., Lambotte, O., Perez-Patrigeon, S., Vingert, B., Sinet, M., Colle, J. H., Urrutia, A., Scott-Algara, D. & other authors ( 2007; ). Preserved central memory and activated effector memory CD4+ T-cell subsets in human immunodeficiency virus controllers: an ANRS EP36 study. J Virol 81, 13904–13915.[CrossRef]
    [Google Scholar]
  122. Premkumar, D. R., Ma, X. Z., Maitra, R. K., Chakrabarti, B. K., Salkowitz, J., Yen-Lieberman, B., Hirsch, M. S. & Kestler, H. W. ( 1996; ). The nef gene from a long-term HIV type 1 nonprogressor. AIDS Res Hum Retroviruses 12, 337–345.[CrossRef]
    [Google Scholar]
  123. Rangel, H. R., Garzaro, D., Rodríguez, A. K., Ramírez, A. H., Ameli, G., del Rosario Gutiérrez, C. & Pujol, F. H. ( 2009; ). Deletion, insertion and stop codon mutations in vif genes of HIV-1 infecting slow progressor patients. J Infect Dev Ctries 3, 531–538.
    [Google Scholar]
  124. Rappaport, J., Cho, Y. Y., Hendel, H., Schwartz, E. J., Schachter, F. & Zagury, J. F. ( 1997; ). 32 bp CCR-5 gene deletion and resistance to fast progression in HIV-1 infected heterozygotes. Lancet 349, 922–923.[CrossRef]
    [Google Scholar]
  125. Romiti, M. L., Colognesi, C., Cancrini, C., Mas, A., Berrino, M., Salvatori, F., Orlandi, P., Jansson, M., Palomba, E. & other authors ( 2000; ). Prognostic value of a CCR5 defective allele in pediatric HIV-1 infection. Mol Med 6, 28–36.
    [Google Scholar]
  126. Ronquillo, R. E., Desai, S. N., Norris, P. J., Golub, E. T., Greenblatt, R. M., Gange, S. J. & Landay, A. L. ( 2010; ). Elevated caspase-3 expression and T-cell activation in elite suppressors. J Acquir Immune Defic Syndr 54, 110–111.[CrossRef]
    [Google Scholar]
  127. Rosenberg, E. S., Billingsley, J. M., Caliendo, A. M., Boswell, S. L., Sax, P. E., Kalams, S. A. & Walker, B. D. ( 1997; ). Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278, 1447–1450.[CrossRef]
    [Google Scholar]
  128. Saha, K., Bentsman, G., Chess, L. & Volsky, D. J. ( 1998; ). Endogenous production of beta-chemokines by CD4+, but not CD8+, T-cell clones correlates with the clinical state of human immunodeficiency virus type 1 (HIV-1)-infected individuals and may be responsible for blocking infection with non-syncytium-inducing HIV-1 in vitro. J Virol 72, 876–881.
    [Google Scholar]
  129. Saksena, N. K., Rodes, B., Wang, B. & Soriano, V. ( 2007; ). Elite HIV controllers: myth or reality? AIDS Rev 9, 195–207.
    [Google Scholar]
  130. Sandonís, V., Casado, C., Alvaro, T., Pernas, M., Olivares, I., García, S., Rodríguez, C., del Romero, J. & López-Galíndez, C. ( 2009; ). A combination of defective DNA and protective host factors are found in a set of HIV-1 ancestral LTNPs. Virology 391, 73–82.[CrossRef]
    [Google Scholar]
  131. Schinkel, J., Langendam, M. W., Coutinho, R. A., Krol, A., Brouwer, M. & Schuitemaker, H. ( 1999; ). No evidence for an effect of the CCR5 Δ32/+ and CCR2b 64I/+ mutations on human immunodeficiency virus (HIV)-1 disease progression among HIV-1-infected injecting drug users. J Infect Dis 179, 825–831.[CrossRef]
    [Google Scholar]
  132. Shen, C., Gupta, P., Wu, H., Chen, X., Huang, X., Zhou, Y. & Chen, Y. ( 2008; ). Molecular characterization of the HIV type 1 vpr gene in infected Chinese former blood/plasma donors at different stages of diseases. AIDS Res Hum Retroviruses 24, 661–666.[CrossRef]
    [Google Scholar]
  133. Simek, M. D., Rida, W., Priddy, F. H., Pung, P., Carrow, E., Laufer, D. S., Lehrman, J. K., Boaz, M., Tarragona-Fiol, T. & other authors ( 2009; ). Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J Virol 83, 7337–7348.[CrossRef]
    [Google Scholar]
  134. Soriano-Sarabia, N., Vallejo, A., Ramírez-Lorca, R., del Mar Rodríguez, M., Salinas, A., Pulido, I., Sáez, M. I. & Leal, M. ( 2008; ). Influence of the Toll-like receptor 9 1635A/G polymorphism on the CD4 count, HIV viral load, and clinical progression. J Acquir Immune Defic Syndr 49, 128–135.[CrossRef]
    [Google Scholar]
  135. Sreepian, A., Srisurapanon, S., Horthongkham, N., Tunsupasawasdikul, S., Kaoriangudom, S., Khusmith, S. & Sutthent, R. ( 2004; ). Conserved neutralizing epitopes of HIV type 1 CRF01_AE against primary isolates in long-term nonprogressors. AIDS Res Hum Retroviruses 20, 531–542.[CrossRef]
    [Google Scholar]
  136. Stephens, J. C., Reich, D. E., Goldstein, D. B., Shin, H. D., Smith, M. W., Carrington, M., Winkler, C., Huttley, G. A., Allikmets, R. & other authors ( 1998; ). Dating the origin of the CCR5-Δ32 AIDS-resistance allele by the coalescence of haplotypes. Am J Hum Genet 62, 1507–1515.[CrossRef]
    [Google Scholar]
  137. Stewart, G. J., Ashton, L. J., Biti, R. A., French, R. A., Bennetts, B. H., Newcombe, N. R., Benson, E. M., Carr, A., Cooper, D. A. & other authors ( 1997; ). Increased frequency of CCR-5 delta 32 heterozygotes among long-term non-progressors with HIV-1 infection. The Australian long-term non-progressor study group. AIDS 11, 1833–1838.[CrossRef]
    [Google Scholar]
  138. Tolstrup, M., Laursen, A. L., Gerstoft, J., Pedersen, F. S., Ostergaard, L. & Duch, M. ( 2006; ). Cysteine 138 mutation in HIV-1 Nef from patients with delayed disease progression. Sex Health 3, 281–286.[CrossRef]
    [Google Scholar]
  139. Tresoldi, E., Romiti, M. L., Boniotto, M., Crovella, S., Salvatori, F., Palomba, E., Pastore, A., Cancrini, C., de Martino, M. & other authors ( 2002; ). Prognostic value of the stromal cell-derived factor 1 3′A mutation in pediatric human immunodeficiency virus type 1 infection. J Infect Dis 185, 696–700.[CrossRef]
    [Google Scholar]
  140. Urban, T. J., Weintrob, A. C., Fellay, J., Colombo, S., Shianna, K. V., Gumbs, C., Rotger, M., Pelak, K. & Dang, K. K. ( 2009; ). CCL3L1 and HIV/AIDS susceptibility. Nat Med 15, 1110–1112.[CrossRef]
    [Google Scholar]
  141. Valdez, H., Carlson, N. L., Post, A. B., Asaad, R., Heeger, P. S., Lederman, M. M., Lehmann, P. V. & Anthony, D. D. ( 2002; ). HIV long-term non-progressors maintain brisk CD8 T cell responses to other viral antigens. AIDS 16, 1113–1118.[CrossRef]
    [Google Scholar]
  142. van Manen, D., Rits, M. A., Beugeling, C., van Dort, K., Schuitemaker, H. & Kootstra, N. A. ( 2008; ). The effect of Trim5 polymorphisms on the clinical course of HIV-1 infection. PLoS Pathog 4, e18.[CrossRef]
    [Google Scholar]
  143. Varela-Rohena, A., Carpenito, C., Perez, E. E., Richardson, M., Parry, R. V., Milone, M., Scholler, J., Hao, X., Mexas, A. & other authors ( 2008; ). Genetic engineering of T cells for adoptive immunotherapy. Immunol Res 42, 166–181.[CrossRef]
    [Google Scholar]
  144. Vázquez-Pérez, J. A., Ormsby, C. E., Hernández-Juan, R., Torres, K. J. & Reyes-Terán, G. ( 2009; ). APOBEC3G mRNA expression in exposed seronegative and early stage HIV infected individuals decreases with removal of exposure and with disease progression. Retrovirology 6, 23.[CrossRef]
    [Google Scholar]
  145. Vidal, F., Peraire, J., Domingo, P., Broch, M., Knobel, H., Pedrol, E., Dalmau, D., Vilades, C. & Sambeat, M. A. ( 2005a; ). Lack of association of SDF-1 3′A variant allele with long-term nonprogressive HIV-1 infection is extended beyond 16 years. J Acquir Immune Defic Syndr 40, 276–279.[CrossRef]
    [Google Scholar]
  146. Vidal, F., Vilades, C., Domingo, P., Broch, M., Pedrol, E., Dalmau, D., Knobel, H., Peraire, J., Gutierrez, C. & other authors ( 2005b; ). Spanish HIV-1-infected long-term nonprogressors of more than 15 years have an increased frequency of the CX3CR1 249I variant allele. J Acquir Immune Defic Syndr 40, 527–531.[CrossRef]
    [Google Scholar]
  147. Vieillard, V., Fausther-Bovendo, H., Samri, A. & Debré, P., French Asymptomatiques à Long Terme (ALT) ANRS-CO15 Study Group ( 2010; ). Specific phenotypic and functional features of natural killer cells from HIV-infected long-term nonprogressors and HIV controllers. J Acquir Immune Defic Syndr 53, 564–573.
    [Google Scholar]
  148. Walker, B. D. ( 2007; ). Elite control of HIV infection: implications for vaccines and treatment. Top HIV Med 15, 134–136.
    [Google Scholar]
  149. Wang, B., Mikhail, M., Dyer, W. B., Zaunders, J. J., Kelleher, A. D. & Saksena, N. K. ( 2003; ). First demonstration of a lack of viral sequence evolution in a nonprogressor, defining replication-incompetent HIV-1 infection. Virology 312, 135–150.[CrossRef]
    [Google Scholar]
  150. Wichukchinda, N., Nakayama, E. E., Rojanawiwat, A., Pathipvanich, P., Auwanit, W., Vongsheree, S., Ariyoshi, K., Sawanpanyalert, P. & Shioda, T. ( 2006; ). Protective effects of IL4–589T and RANTES-28G on HIV-1 disease progression in infected Thai females. AIDS 20, 189–196.[CrossRef]
    [Google Scholar]
  151. Wilkinson, D. A., Operskalski, E. A., Busch, M. P., Mosley, J. W. & Koup, R. A. ( 1998; ). A 32-bp deletion within the CCR5 locus protects against transmission of parenterally acquired human immunodeficiency virus but does not affect progression to AIDS-defining illness. J Infect Dis 178, 1163–1166.[CrossRef]
    [Google Scholar]
  152. Winkler, C., Modi, W., Smith, M. W., Nelson, G. W., Wu, X., Carrington, M., Dean, M., Honjo, T., Tashiro, K. & other authors ( 1998; ). Genetic restriction of AIDS pathogenesis by an SDF-1 chemokine gene variant. ALIVE Study, Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort (SFCC). Science 279, 389–393.[CrossRef]
    [Google Scholar]
  153. Wu, J. Q., Wang, B., Belov, L., Chrisp, J., Learmont, J., Dyer, W. B., Zaunders, J., Cunningham, A. L., Dwyer, D. E. & other authors ( 2007; ). Antibody microarray analysis of cell surface antigens on CD4+ and CD8+ T cells from HIV+ individuals correlates with disease stages. Retrovirology 4, 83.[CrossRef]
    [Google Scholar]
  154. Wu, X., Yang, Z., Li, Y., Hogerkorp, C., Schief, W. R., Seaman, M. S., Zhou, T., Schmidt, S. D., Wu, L. & other authors ( 2010; ). Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856–861.[CrossRef]
    [Google Scholar]
  155. Zhang, W., Chen, G., Niewiadomska, A. M., Xu, R. & Yu, Z. F. ( 2008; ). Distinct determinants in HIV-1 Vif and human APOBEC3 proteins are required for the suppression of diverse host anti-viral proteins. PLoS ONE 3, e3963.[CrossRef]
    [Google Scholar]
  156. Zimmerman, P. A., Buckler-White, A., Alkhatib, G., Spalding, T., Kubofcik, J., Combadiere, C., Weissman, D., Cohen, O., Rubbert, A. & other authors ( 1997; ). Inherited resistance to HIV-1 conferred by an inactivating mutation in CC chemokine receptor 5: studies in populations with contrasting clinical phenotypes, defined racial background, and quantified risk. Mol Med 3, 23–36.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.027102-0
Loading
/content/journal/jgv/10.1099/vir.0.027102-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error