Human leukocyte antigen variants B*44 and B*57 are consistently favorable during two distinct phases of primary HIV-1 infection in sub-Saharan Africans with several viral subtypes

Journal of Virology

Volumn 85, Issue 17, 2011, Pages 8894-8902

  Tang, Jianming ^a   Cormier, Emmanuel ^b   Gilmour, Jill ^b   Price, Matthew A ^c   Prentice, Heather A ^d   Song, Wei ^d   Kamali, Anatoli ^e   Karita, Etienne ^f   Lakhi, Shabir ^g   Sanders, Eduard J ^h,i   Anzala, Omu ^j   Amornkul, Pauli N ^c   Allen, Susan ^g,k   Hunter, Eric ^l   Kaslow, Richard A ^d  

^a University of Alabama at Birmingham   (United States)

^b CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^c INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e MRC/UVRI Uganda Virus Research Unit on AIDS   (Uganda)

^f Projet San Francisco   (Rwanda)

^g Zambia Emory HIV Research Project   (Zambia)

^h KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

^j Kenya AIDS Vaccine Initiative (KAVI)   (Kenya)

^k EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l EMORY UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HLA B44 ANTIGEN; HLA B57 ANTIGEN;

ADULT; ARTICLE; CD4 LYMPHOCYTE COUNT; CONTROLLED STUDY; DISEASE DURATION; DISEASE SEVERITY; ETHNIC GROUP; FEMALE; GEOGRAPHIC ORIGIN; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MAJOR CLINICAL STUDY; MALE; NONHUMAN; ONSET AGE; PRIMARY INFECTION; PRIORITY JOURNAL; SEROCONVERSION; SUB SAHARAN AFRICAN; VIREMIA; VIRUS IDENTIFICATION; VIRUS LOAD; VIRUS TYPING;

ADULT; AFRICA SOUTH OF THE SAHARA; CD4 LYMPHOCYTE COUNT; FEMALE; HIV INFECTIONS; HIV-1; HLA-B ANTIGENS; HUMANS; IMMUNITY, INNATE; MALE; MIDDLE AGED; VIRAL LOAD;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 80052285180     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00439-11     Document Type: Article

References (95)

1. Allen, T. M., and M. Altfeld. 2008. Crippling HIV one mutation at a time. J. Exp. Med. 205:1003-1007.
2. Altfeld, M., et al. 2003. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17:2581-2591.
3. + T cell response against HIV-1. PLoS Med. 3:e403.
4. Baeten, J. M., et al. 2007. HIV-1 subtype D infection is associated with faster disease progression than subtype A in spite of similar plasma HIV-1 loads. J. Infect. Dis. 195:1177-1180.
5. Bansal, A., et al. 2007. Immunological control of chronic HIV-1 infection: HLA-mediated immune function and viral evolution in adolescents. AIDS 21:2387-2397.
6. Brenchley, J. M., D. A. Price, and D. C. Douek. 2006. HIV disease: fallout from a mucosal catastrophe? Nat. Immunol. 7:235-239.
7. Cano, P., et al. 2007. Common and well-documented HLA alleles: report of the ad-hoc committee of the American Society for Histocompatibility and Immunogenetics. Hum. Immunol. 68:392-417.
8. Cao, J., J. McNevin, U. Malhotra, and M. J. McElrath. 2003. Evolution of CD8+ T cell immunity and viral escape following acute HIV-1 infection. J. Immunol. 171:3837-3846.
9. Carrington, M., and S. J. O'Brien. 2003. The influence of HLA genotype on AIDS. Annu. Rev. Med. 54:535-551.
10. Centlivre, M., M. Sala, S. Wain-Hobson, and B. Berkhout. 2007. In HIV-1 pathogenesis the die is cast during primary infection. AIDS 21:1-11.
11. Costello, C., et al. 1999. HLA-B*5703 independently associated with slower HIV-1 disease progression in Rwandan women. AIDS 13:1990-1991.
12. Crawford, H., et al. 2009. Evolution of HLA-B*5703 HIV-1 escape mutations in HLA-B*5703-positive individuals and their transmission recipients. J. Exp. Med. 206:909-921.
13. Currier, J. R., et al. 2002. A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J. Immunol. Methods 260:157-172.
14. Dalmasso, C., et al. 2008. Distinct genetic loci control plasma HIV-RNA and cellular HIV-DNA levels in HIV-1 infection: the ANRS Genome Wide Association 01 study. PLoS One 3:e3907.
15. Derdeyn, C. A., et al. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019-2022.
16. Fellay, J., et al. 2009. Common genetic variation and the control of HIV-1 in humans. PLoS Genet. 5:e1000791.
17. Fellay, J., et al. 2007. A whole-genome association study of major determinants for host control of HIV-1. Science 317:944-947.
18. Fideli, U. S., et al. 2001. Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 (HIV-1) in Africa. AIDS Res. Hum. Retroviruses 17:901-910.
19. Fiebig, E. W., et al. 2003. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 17:1871-1879.
20. Fischer, W., et al. 2010. Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One 5:e12303.
21. Gao, X., et al. 2010. HLA-B alleles associate consistently with HIV heterosexual transmission, viral load, and progression to AIDS, but not susceptibility to infection. AIDS 24:1835-1840.
22. Gill, D. K., et al. 2010. Equivalence of ELISpot assays demonstrated between major HIV network laboratories. PLoS One 5:e14330.
23. Goepfert, P. A., et al. 2008. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J. Exp. Med. 205:1009-1017.
24. Gonzalez, E., et al. 1999. Race-specific HIV-1 disease modifying effects associated with CCR5 haplotypes. Proc. Natl. Acad. Sci. U. S. A. 96:12004-12009.
25. Goonetilleke, N., et al. 2009. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J. Exp. Med. 206:1253-1272.
26. Hecht, F. M., et al. 2010. HIV RNA level in early infection is predicted by viral load in the transmission source. AIDS 24:941-945.
27. Hollingsworth, T. D., et al. 2010. HIV-1 transmitting couples have similar viral load set-points in Rakai, Uganda. PLoS Pathog. 6:e1000876.
28. Honeyborne, I., et al. 2010. HLA-Cw*03-restricted CD8+ T-cell responses targeting the HIV-1 Gag major homology region drive virus immune escape and fitness constraints compensated by intra-codon variation. J. Virol. 84:11279-11288.
29. Honeyborne, I., et al. 2007. Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple gag-specific CD8+ T-cell epitopes. J. Virol. 81:3667-3672.
30. John, G. C., et al. 2001. Correlates of mother-to-child human immunodeficiency virus type 1 (HIV-1) transmission: association with maternal plasma HIV-1 RNA load, genital HIV-1 DNA shedding, and breast infections. J. Infect. Dis. 183:206-212.
31. Jones, N. A., et al. 2004. Determinants of human immunodeficiency virus type 1 escape from the primary CD8+ cytotoxic T lymphocyte response. J. Exp. Med. 200:1243-1256.
32. Kaleebu, P., 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. J. Infect. Dis. 185:1244-1250.
33. Kanki, P. J., et al. 1999. Human immunodeficiency virus type 1 subtypes differ in disease progression. J. Infect. Dis. 179:68-73.
34. Karita, E., et al. 2009. CLSI-derived hematology and biochemistry reference intervals for healthy adults in eastern and southern Africa. PLoS One 4:e4401.
35. Karita, E., et al. 2007. Investigating the utility of the HIV-1 BED capture enzyme immunoassay using cross-sectional and longitudinal seroconverter specimens from Africa. AIDS 21:403-408.
36. Kaslow, R. A., et al. 1996. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 2:405-411.
37. Kaslow, R. A., et al. 2001. Polymorphisms in HLA class I genes associated with both favorable prognosis of human immunodeficiency virus (HIV) type 1 infection and positive cytotoxic T-lymphocyte responses to ALVAC-HIV recombinant canarypox vaccines. J. Virol. 75:8681-8689.
38. Kebba, A., et al. 2007. Recent HIV-1 infection in a high-risk Ugandan cohort: implications for phase IIB test-of-concept HIV vaccine trials. Pharmacogenomics 8:409-414.
39. Kiepiela, P., et al. 2007. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
40. Kiwanuka, N., et al. 2008. Effect of human immunodeficiency virus Type 1 (HIV-1) subtype on disease progression in persons from Rakai, Uganda, with incident HIV-1 infection. J. Infect. Dis. 197:707-713.
41. Koehler, R. N., et al. 2010. Class I HLA-A*7401 is associated with protection from HIV-1 acquisition and disease progression in Mbeya, Tanzania. J. Infect. Dis. 202:1562-1566.
42. Korber, B. T., N. L. Letvin, and B. F. Haynes. 2009. T-cell vaccine strategies for human immunodeficiency virus, the virus with a thousand faces. J. Virol. 83:8300-8314.
43. Koup, R. A. 1994. Virus escape from CTL recognition. J. Exp. Med. 180:779-782.
44. Koup, R. A., B. S. Graham, and D. C. Douek. 2011. The quest for a T cell-based immune correlate of protection against HIV: a story of trials and errors. Nat. Rev. Immunol. 11:65-70.
45. Kulkarni, S., et al. 2008. Neutralizing antibody responses in recent seroconverters with HIV-1 subtype C infections in India. AIDS Res. Hum. Retroviruses 24:1159-1166.
46. Larkin, M. A., et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
47. Lazaryan, A., et al. 2010. Human leukocyte antigen class I supertypes and HIV-1 control in African Americans. J. Virol. 84:2610-2617.
48. Lazaryan, A., et al. 2011. The influence of human leukocyte antigen class I alleles and their population frequencies on human immunodeficiency virus type 1 control among African Americans. Hum. Immunol. 72:312-318.
49. Leslie, A., et al. 2010. Additive contribution of HLA class I alleles in the immune control of HIV-1 infection. J. Virol. 84:9879-9888.
50. Liu, R., et al. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-377.
51. Liu, Y., et al. 2006. Selection on the human immunodeficiency virus type 1 proteome following primary infection. J. Virol. 80:9519-9529.
52. Los Alamos National Laboratory. 2010. HIV Molecular Immunology Database. http://www.hiv.lanl.gov/content/immunology/index.html. Last accessed April 2011.
53. Maiers, M., L. Gragert, and W. Klitz. 2007. High-resolution HLA alleles and haplotypes in the United States population. Hum. Immunol. 68:779-788.
54. Mann, D. L., et al. 1998. Major histocompatibility complex genotype is associated with disease progression and virus load levels in a cohort of human immunodeficiency virus type 1-infected Caucasians and African Americans. J. Infect. Dis. 178:1799-1802.
55. Marsh, S. G., et al. 2010. Nomenclature for factors of the HLA system, 2010. Tissue Antigens 75:291-455.
56. Matthews, P. C., et al. 2008. Central role of reverting mutations in HLA associations with human immunodeficiency virus set point. J. Virol. 82:8548-8559.
57. McMichael, A., M. Mwau, and T. Hanke. 2002. HIV T cell vaccines, the importance of clades. Vaccine 20:1918-1921.
58. Mellors, J. W., et al. 1995. Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann. Intern. Med. 122:573-579.
59. Mellors, J. W., et al. 2007. Prognostic value of HIV-1 RNA, CD4 cell count, and CD4 cell count slope for progression to AIDS and death in untreated HIV-1 infection. JAMA 297:2349-2350.
60. Migueles, S. A., et al. 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.
61. Modjarrad, K., E. Chamot, and S. H. Vermund. 2008. Impact of small reductions in plasma HIV RNA levels on the risk of heterosexual transmission and disease progression. AIDS 22:2179-2185.
62. Neilson, J. R., et al. 1999. Subtypes of human immunodeficiency virus type 1 and disease stage among women in Nairobi, Kenya. J. Virol. 73:4393-4403.
63. Novitsky, V., et al. 2001. Identification of most frequent HLA class I antigen specificities in Botswana: relevance for HIV vaccine design. Hum. Immunol. 62:146-156.
64. Novitsky, V., et al. 2009. Timing constraints of in vivo Gag mutations during primary HIV-1 subtype C infection. PLoS One 4:e7727.
65. Paris, R., et al. 2004. HLA class I serotypes and cytotoxic T-lymphocyte responses among human immunodeficiency virus-1-uninfected Thai volunteers immunized with ALVAC-HIV in combination with monomeric gp120 or oligomeric gp160 protein boosting. Tissue Antigens 64:251-256.
66. Pelak, K., et al. 2010. Host determinants of HIV-1 control in African Americans. J. Infect. Dis. 201:1141-1149.
67. Pellegrin, I., et al. 1996. Kinetics of appearance of neutralizing antibodies in 12 patients with primary or recent HIV-1 infection and relationship with plasma and cellular viral loads. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 11:438-447.
68. Pinkerton, S. D. 2007. How many sexually-acquired HIV infections in the U. S. A. are due to acute-phase HIV transmission? AIDS 21:1625-1629.
69. Prado, J. G., et al. 2010. Replicative capacity of human immunodeficiency virus type 1 transmitted from mother to child is associated with pediatric disease progression rate. J. Virol. 84:492-502.
70. Price, M. A., et al. 2011. Transmitted HIV type 1 drug resistance among individuals with recent HIV infection in East and Southern Africa. AIDS Res. Hum. Retroviruses 27:5-12.
71. Quinn, T. C., et al. 2000. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N. Engl. J. Med. 342:921-929.
72. Rolland, M., et al. 2010. Amino-acid co-variation in HIV-1 Gag subtype C: HLA-mediated selection pressure and compensatory dynamics. PLoS One 5:e12463.
73. Rousseau, C. M., et al. 2008. HLA class I-driven evolution of human immunodeficiency virus type 1 subtype C proteome: immune escape and viral load. J. Virol. 82:6434-6446.
74. Saag, M. S., et al. 1996. HIV viral load markers in clinical practice. Nat. Med. 2:625-629.
75. Saah, A. J., et al. 1998. Association of HLA profiles with early plasma viral load, CD4+ cell count and rate of progression to AIDS following acute HIV-1 infection. Multicenter AIDS Cohort Study. AIDS 12:2107-2113.
76. Salazar-Gonzalez, J. F., et al. 2009. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J. Exp. Med. 206:1273-1289.
77. Shrestha, S., et al. 2009. Host genetics and HIV-1 viral load set-point in African-Americans. AIDS 23:673-677.
78. Stacey, A. R., et al. 2009. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J. Virol. 83:3719-3733.
79. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
80. Tang, J., and R. A. Kaslow. 2003. The impact of host genetics on HIV infection and disease progression in the era of highly active antiretroviral therapy. AIDS 17:S51-S60.
81. Tang, J., et al. 2010. Human leukocyte antigens and HIV type 1 viral load in early and chronic infection: predominance of evolving relationships. PLoS One 5:e9629.
82. Tang, J., et al. 2008. Human leukocyte antigen class I genotypes in relation to heterosexual HIV type 1 transmission within discordant couples. J. Immunol. 181:2626-2635.
83. Tang, J., et al. 2002. Distribution of chemokine receptor CCR2 and CCR5 genotypes and their relative contribution to human immunodeficiency virus type 1 (HIV-1) seroconversion, early HIV-1 RNA concentration in plasma, and later disease progression. J. Virol. 76:662-672.
84. Tang, J., et al. 2002. Favorable and unfavorable HLA class I alleles and haplotypes in Zambians predominantly infected with clade C human immunodeficiency virus type 1. J. Virol. 76:8276-8284.
85. Tang, J., et al. 2004. HLA allele sharing and HIV type 1 viremia in seroconverting Zambians with known transmitting partners. AIDS Res. Hum. Retroviruses 20:19-26.
86. Tang, J., et al. 2002. Host genetic profiles predict virological and immunological control of HIV-1 infection in adolescents. AIDS 16:2275-2284.
87. Tang, J., et al. 2011. HIV-1 viral load during acute infection in sub-Saharan Africans: deciphering the impact of host and viral factors, poster abstr. 510. Abstr. 18th Conf. Retrovir. Opportun. Infect., Boston, MA, 27 February to 2 March 2011.
88. Tebit, D. M., and E. J. Arts. 2011. Tracking a century of global expansion and evolution of HIV to drive understanding and to combat disease. Lancet Infect. Dis. 11:45-56.
89. The International HIV Controllers Study. 2010. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330:1551-1557.
90. Treurnicht, F. K., et al. 2010. Adaptive changes in HIV-1 subtype C proteins during early infection are driven by changes in HLA-associated immune pressure. Virology 396:213-225.
91. Vasan, A., et al. 2006. Different rates of disease progression of HIV type 1 infection in Tanzania based on infecting subtype. Clin. Infect. Dis. 42:843-852.
92. Walker, L. E., et al. 2009. Design and preclinical development of a recombinant protein and DNA plasmid mixed format vaccine to deliver HIVderived T-lymphocyte epitopes. Vaccine 27:7087-7095.
93. + T-cell responses are associated with viral escape mutations located in highly conserved regions of human immunodeficiency virus type 1. J. Virol. 83:1845-1855.
94. Wawer, M. J., et al. 2005. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J. Infect. Dis. 191:1403-1409.
95. Zhang, M., et al. 2010. The role of recombination in the emergence of a complex and dynamic HIV epidemic. Retrovirology 7:25.