Cumulative impact of host and viral factors on HIV-1 viral-load control during early infection

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 708-715

  Yue, Ling ^a   Prentice, Heather A ^b   Farmer, Paul ^a   Song, Wei ^b   He, Dongning ^b   Lakhi, Shabir ^c   Goepfert, Paul ^d   Gilmour, Jill ^e   Allen, Susan ^f   Tang, Jianming ^d   Kaslow, Richard A ^b   Hunte, Eric ^a,f  

^a EMORY UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c Zambia Emory HIV Research Project   (Zambia)

^d and Clinical Center   (United States)

^e INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

^f EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE DISTRIBUTION; ALLELE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ANALYSIS; HEREDITY; HETEROSEXUALITY; HLA SYSTEM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGENETICS; INFECTION CONTROL; INFECTION RISK; MAJOR CLINICAL STUDY; MALE; PHENOTYPE; PHYLOGENY; POPULATION RESEARCH; PRIORITY JOURNAL; RISK ASSESSMENT; SEX DIFFERENCE; VIRUS LOAD; VIRUS TRANSMISSION; ZAMBIA;

ADULT; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MALE; MIDDLE AGED; SEX FACTORS; VIRAL LOAD; ZAMBIA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84871983347     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02118-12     Document Type: Article

References (54)

1. Fideli US, Allen SA, Musonda R, Trask S, Hahn BH, Weiss H, Mulenga J, Kasolo F, Vermund SH, Aldrovandi GM. 2001. Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa. AIDS Res. Hum. Retroviruses 17:901-910.
2. Fraser C, Hollingsworth TD, Chapman R, de Wolf F, Hanage WP. 2007. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl. Acad. Sci. U. S. A. 104:17441-17446.
3. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, Meehan MO, Lutalo T, Gray RH. 2000. Viral load and heterosexual transmission of human immunodeficiency virus type 1. N. Engl. J. Med. 342:921-929.
4. Jurriaans S, Van Gemen B, Weverling GJ, Van Strijp D, Nara P, Coutinho R, Koot M, Schuitemaker H, Goudsmit J. 1994. The natural history of HIV-1 infection: virus load and virus phenotype independent determinants of clinical course? Virology 204:223-233.
5. Mellors JW, Kingsley LA, Rinaldo CR, Jr, Todd JA, Hoo BS, Kokka RP, Gupta P. 1995. Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann. Intern. Med. 122:573-579.
6. Streeck H, Nixon DF. 2010. T cell immunity in acute HIV-1 infection. J. Infect. Dis. 202(Suppl 2):S302-S308.
7. Gras L, Jurriaans S, Bakker M, van Sighem A, Bezemer D, Fraser C, Lange J, Prins JM, Berkhout B, de Wolf F. 2009. Viral load levels measured at set-point have risen over the last decade of the HIV epidemic in the Netherlands. PLoS One 4:e7365. doi:10.1371/journal.pone.0007365.
8. Herbeck JT, Muller V, Maust BS, Ledergerber B, Torti C, Di Giambenedetto S, Gras L, Gunthard HF, Jacobson LP, Mullins JI, Gottlieb GS. 2012. Is the virulence of HIV changing? A meta-analysis of trends in prognostic markers of HIV disease progression and transmission. AIDS 26:193-205.
9. Kawashima Y, Pfafferott K, Frater J, Matthews P, Payne R, Addo M, Gatanaga H, Fujiwara M, Hachiya A, Koizumi H, Kuse N, Oka S, Duda A, Prendergast A, Crawford H, Leslie A, Brumme Z, Brumme C, Allen T, Brander C, Kaslow R, Tang J, Hunter E, Allen S, Mulenga J, Branch S, Roach T, John M, Mallal S, Ogwu A, Shapiro R, Prado JG, Fidler S, Weber J, Pybus OG, Klenerman P, Ndung'u T, Phillips R, Heckerman D, Harrigan PR, Walker BD, Takiguchi M, Goulder P. 2009. Adaptation of HIV-1 to human leukocyte antigen class I. Nature 458:641-645.
10. Payne RP, Matthews PC, Prado JG, Goulder PJ. 2009. HLA-mediated control of HIV and HIV adaptation to HLA. Adv. Parasitol. 68:1-20.
11. Crawford H, Lumm W, Leslie A, Schaefer M, Boeras D, Prado JG, Tang J, Farmer P, Ndung'u T, Lakhi S, Gilmour J, Goepfert P, Walker BD, Kaslow R, Mulenga J, Allen S, Goulder PJ, Hunter E. 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.
12. Goulder PJ, Brander C, Tang Y, Tremblay C, Colbert RA, Addo MM, Rosenberg ES, Nguyen T, Allen R, Trocha A, Altfeld M, He S, Bunce M, Funkhouser R, Pelton SI, Burchett SK, McIntosh K, Korber BT, Walker BD. 2001. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412:334-338.
13. Wright JK, Novitsky V, Brockman MA, Brumme ZL, Brumme CJ, Carlson JM, Heckerman D, Wang B, Losina E, Leshwedi M, van der Stok M, Maphumulo L, Mkhwanazi N, Chonco F, Goulder PJ, Essex M, Walker BD, Ndung'u T. 2011. Influence of Gag-protease-mediated replication capacity on disease progression in individuals recently infected with HIV-1 subtype C. J. Virol. 85:3996-4006.
14. Fellay J, Ge D, Shianna KV, Colombo S, Ledergerber B, Cirulli ET, Urban TJ, Zhang K, Gumbs CE, Smith JP, Castagna A, Cozzi-Lepri A, De Luca A, Easterbrook P, Gunthard HF, Mallal S, Mussini C, Dalmau J, Martinez-Picado J, Miro JM, Obel N, Wolinsky SM, Martinson JJ, Detels R, Margolick JB, Jacobson LP, Descombes P, Antonarakis SE, Beckmann JS, O'Brien SJ, Letvin NL, McMichael AJ, Haynes BF, Carrington M, Feng S, Telenti A, Goldstein DB. 2009. Common genetic variation and the control of HIV-1 in humans. PLoS Genet. 5:e1000791. doi:10.1371/journal.pgen.1000791.
15. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, Weale M, Zhang K, Gumbs C, Castagna A, Cossarizza A, Cozzi-Lepri A, De Luca A, Easterbrook P, Francioli P, Mallal S, Martinez-Picado J, Miro JM, Obel N, Smith JP, Wyniger J, Descombes P, Antonarakis SE, Letvin NL, McMichael AJ, Haynes BF, Telenti A, Goldstein DB. 2007. A wholegenome association study of major determinants for host control of HIV-1. Science 317:944-947.
16. International HIV Controllers Study. 2010. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330:1551-1557.
17. Goepfert PA, Lumm W, Farmer P, Matthews P, Prendergast A, Carlson JM, Derdeyn CA, Tang J, Kaslow RA, Bansal A, Yusim K, Heckerman D, Mulenga J, Allen S, Goulder PJ, Hunter E. 2008. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J. Exp. Med. 205:1009-1017.
18. Hollingsworth TD, Laeyendecker O, Shirreff G, Donnelly CA, Serwadda D, Wawer MJ, Kiwanuka N, Nalugoda F, Collinson-Streng A, Ssempijja V. 2010. HIV-1 transmitting couples have similar viral load set-points in Rakai, Uganda. PLoS Pathog. 6:e1000876. doi:10.1371/ journal.ppat.1000876.
19. Tang J, Tang S, Lobashevsky E, Zulu I, Aldrovandi G, Allen S, Kaslow RA. 2004. HLA allele sharing and HIV type 1 viremia in seroconverting Zambians with known transmitting partners. AIDS Res. Hum. Retroviruses 20:19-25.
20. van der Kuyl AC, Jurriaans S, Pollakis G, Bakker M, Cornelissen M. 2010. HIV RNA levels in transmission sources only weakly predict plasma viral load in recipients. AIDS 24:1607-1608.
21. Hecht FM, Hartogensis W, Bragg L, Bacchetti P, Atchison R, Grant R, Barbour J, Deeks SG. 2010. HIV RNA level in early infection is predicted by viral load in the transmission source. AIDS 24:941-945.
22. Alizon S, von Wyl V, Stadler T, Kouyos RD, Yerly S, Hirschel B, Boni J, Shah C, Klimkait T, Furrer H, Rauch A, Vernazza PL, Bernasconi E, Battegay M, Burgisser P, Telenti A, Gunthard HF, Bonhoeffer S. 2010. Phylogenetic approach reveals that virus genotype largely determines HIV set-point viral load. PLoS Pathog. 6:e1001123. doi:10.1371/journal. ppat.1001123.
23. Frater AJ, Brown H, Oxenius A, Gunthard HF, Hirschel B, Robinson N, Leslie AJ, Payne R, Crawford H, Prendergast A, Brander C, Kiepiela P, Walker BD, Goulder PJ, McLean A, Phillips RE. 2007. Effective T-cell responses select human immunodeficiency virus mutants and slow disease progression. J. Virol. 81:6742-6751.
24. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13 46-53
25. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. 2010. The immune response during acute HIV-1 infection: clues for vaccine development. Nat. Rev. Immunol. 10:11-23.
26. Lazaryan A, Song W, Lobashevsky E, Tang J, Shrestha S, Zhang K, McNicholl JM, Gardner LI, Wilson CM, Klein RS, Rompalo A, Mayer K, Sobel J, Kaslow RA. 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.
27. Tang J, Malhotra R, Song W, Brill I, Hu L, Farmer PK, Mulenga J, Allen S, Hunter E, Kaslow RA. 2010. Human leukocyte antigens and HIV type 1 viral load in early and chronic infection: predominance of evolving relationships. PLoS One 5:e9629. doi:10.1371/journal.pone.0009629.
28. Leslie A, Matthews PC, Listgarten J, Carlson JM, Kadie C, Ndung'u T, Brander C, Coovadia H, Walker BD, Heckerman D, Goulder PJ. 2010. Additive contribution of HLA class I alleles in the immune control of HIV-1 infection. J. Virol. 84:9879-9888.
29. Anastos K, Gange SJ, Lau B, Weiser B, Detels R, Giorgi JV, Margolick JB, Cohen M, Phair J, Melnick S, Rinaldo CR, Kovacs A, Levine A, Landesman S, Young M, Munoz A, Greenblatt RM. 2000. Association of race and gender with HIV-1 RNA levels and immunologic progression. J. Acquir. Immune Defic. Syndr. 24:218-226.
30. Collazos J, Asensi V, Carton JA. 2007. Sex differences in the clinical, immunological and virological parameters of HIV-infected patients treated with HAART. AIDS 21:835-843.
31. Napravnik S, Poole C, Thomas JC, Eron JJ, Jr. 2002. Gender difference in HIV RNA levels: a meta-analysis of published studies. J. Acquir. Immune Defic. Syndr. 31:11-19.
32. Meier A, Chang JJ, Chan ES, Pollard RB, Sidhu HK, Kulkarni S, Wen TF, Lindsay RJ, Orellana L, Mildvan D, Bazner S, Streeck H, Alter G, Lifson JD, Carrington M, Bosch RJ, Robbins GK, Altfeld M. 2009. Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat. Med. 15:955-959.
33. Thobakgale CF, Prendergast A, Crawford H, Mkhwanazi N, Ramduth D, Reddy S, Molina C, Mncube Z, Leslie A, Prado J, Chonco F, Mphatshwe W, Tudor-Williams G, Jeena P, Blanckenberg N, Dong K, Kiepiela P, Coovadia H, Ndung'u T, Walker BD, Goulder PJ. 2009. Impact of HLA in mother and child on disease progression of pediatric human immunodeficiency virus type 1 infection. J. Virol. 83:10234-10244.
34. Trask SA, Derdeyn CA, Fideli U, Chen Y, Meleth S, Kasolo F, Musonda R, Hunter E, Gao F, Allen S, Hahn BH. 2002. Molecular epidemiology of human immunodeficiency virus type 1 transmission in a heterosexual cohort of discordant couples in Zambia. J. Virol. 76:397-405.
35. Tang J, Tang S, Lobashevsky E, Myracle AD, Fideli U, Aldrovandi G, Allen S, Musonda R, Kaslow RA. 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.
36. Matthews PC, Adland E, Listgarten J, Leslie A, Mkhwanazi N, Carlson JM, Harndahl M, Stryhn A, Payne RP, Ogwu A, Huang KH, Frater J, Paioni P, Kloverpris H, Jooste P, Goedhals D, van Vuuren C, Steyn D, Riddell L, Chen F, Luzzi G, Balachandran T, Ndung'u T, Buus S, Carrington M, Shapiro R, Heckerman D, Goulder PJ. 2011. HLAA* 7401-mediated control of HIV viremia is independent of its linkage disequilibrium with HLA-B*5703. J. Immunol. 186:5675-5686.
37. Altfeld M, Addo MM, Rosenberg ES, Hecht FM, Lee PK, Vogel M, Yu XG, Draenert R, Johnston MN, Strick D, Allen TM, Feeney ME, Kahn JO, Sekaly RP, Levy JA, Rockstroh JK, Goulder PJ, Walker BD. 2003. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17:2581-2591.
38. Altfeld M, Kalife ET, Qi Y, Streeck H, Lichterfeld M, Johnston MN, Burgett N, Swartz ME, Yang A, Alter G, Yu XG, Meier A, Rockstroh JK, Allen TM, Jessen H, Rosenberg ES, Carrington M, Walker BD. 2006. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med. 3:e403. doi:10.1371/journal.pmed.0030403.
39. Ngumbela KC, Day CL, Mncube Z, Nair K, Ramduth D, Thobakgale C, Moodley E, Reddy S, de Pierres C, Mkhwanazi N, Bishop K, van der Stok M, Ismail N, Honeyborne I, Crawford H, Kavanagh DG, Rousseau C, Nickle D, Mullins J, Heckerman D, Korber B, Coovadia H, Kiepiela P, Goulder PJ, Walker BD. 2008. Targeting of a CD8 T cell env epitope presented by HLA-B*5802 is associated with markers of HIV disease progression and lack of selection pressure. AIDS Res. Hum. Retroviruses 24: 72-82.
40. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, Goedert JJ, Winkler C, O'Brien SJ, Rinaldo C, Detels R, Blattner W, Phair J, Erlich H, Mann DL. 1996. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 2:405-411.
41. Scherer A, Frater J, Oxenius A, Agudelo J, Price DA, Gunthard HF, Barnardo M, Perrin L, Hirschel B, Phillips RE, Mclean AR. 2004. Quantifiable cytotoxic T lymphocyte responses and HLA-related risk of progression to AIDS. Proc. Natl. Acad. Sci. U. S. A. 101:12266-12270.
42. Boeras DI, Hraber PT, Hurlston M, Evans-Strickfaden T, Bhattacharya T, Giorgi EE, Mulenga J, Karita E, Korber BT, Allen S, Hart CE, Derdeyn CA, Hunter E. 2011. Role of donor genital tract HIV-1 diversity in the transmission bottleneck. Proc. Natl. Acad. Sci. U. S. A. 108:E1156-E1163.
43. Derdeyn CA, Decker JM, Bibollet-Ruche F, Mokili JL, Muldoon M, Denham SA, Heil ML, Kasolo F, Musonda R, Hahn BH, Shaw GM, Korber BT, Allen S, Hunter E. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019-2022.
44. Haaland RE, Hawkins PA, Salazar-Gonzalez J, Johnson A, Tichacek A, Karita E, Manigart O, Mulenga J, Keele BF, Shaw GM, Hahn BH, Allen SA, Derdeyn CA, Hunter E. 2009. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog. 5:e1000274. doi:10.1371/journal.ppat.1000274.
45. Frost SD, Liu Y, Pond SL, Chappey C, Wrin T, Petropoulos CJ, Little SJ, Richman DD. 2005. Characterization of human immunodeficiency virus type 1 (HIV-1) envelope variation and neutralizing antibody responses during transmission of HIV-1 subtype B. J. Virol. 79:6523-6527
46. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. 1994. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68:6103-6110.
47. Brockman MA, Brumme ZL, Brumme CJ, Miura T, Sela J, Rosato PC, Kadie CM, Carlson JM, Markle TJ, Streeck H, Kelleher AD, Markowitz M, Jessen H, Rosenberg E, Altfeld M, Harrigan PR, Heckerman D, Walker BD, Allen TM. 2010. Early selection in Gag by protective HLA alleles contributes to reduced HIV-1 replication capacity that may be largely compensated for in chronic infection. J. Virol. 84:11937-11949.
48. Goulder PJ, Watkins DI. 2008. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 8:619-630.
49. Matthews PC, Prendergast A, Leslie A, Crawford H, Payne R, Rousseau C, Rolland M, Honeyborne I, Carlson J, Kadie C, Brander C, Bishop K, Mlotshwa N, Mullins JI, Coovadia H, Ndung'u T, Walker BD, Heckerman D, Goulder PJ. 2008. Central role of reverting mutations in HLA associations with human immunodeficiency virus set point. J. Virol. 82: 8548-8559.
50. Rousseau CM, Daniels MG, Carlson JM, Kadie C, Crawford H, Prendergast A, Matthews P, Payne R, Rolland M, Raugi DN, Maust BS, Learn GH, Nickle DC, Coovadia H, Ndung'u T, Frahm N, Brander C, Walker BD, Goulder PJ, Bhattacharya T, Heckerman DE, Korber BT, Mullins JI. 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.
51. Prentice HA, Tang J. 2012. HIV-1 dynamics: a reappraisal of host and viral factors, as well as methodological issues. Viruses 4:2080-2096.
52. Allen TM, Altfeld M. 2008. Crippling HIV one mutation at a time. J. Exp. Med. 205:1003-1007.
53. Prince JL, Claiborne DT, Carlson JM, Schaefer M, Yu T, Lahki S, Prentice HA, Yue L, Kilembe SAVW, Goepfert P, Price MA, Gilmour J, Mulenga J, Farmer P, Derdeyn CA, Tang J, Heckerman D, Kaslow RA, Allen SA, Hunter E. 2012. Role of transmitted Gag CTL polymorphisms in defining replicative capacity and early HIV-1 pathogenesis. PLoS Pathog. 8:e1003041. doi:10.1371/journal.ppat.1003041.
54. Wright JK, Brumme ZL, Carlson JM, Heckerman D, Kadie CM, Brumme CJ, Wang B, Losina E, Miura T, Chonco F, van der Stok M, Mncube Z, Bishop K, Goulder PJ, Walker BD, Brockman MA, Ndung'u T. 2010. Gag-protease-mediated replication capacity in HIV-1 subtype C chronic infection: associations with HLA type and clinical parameters. J. Virol. 84:10820-10831.