Emergence of individual HIV-specific CD8 T cell responses during primary HIV-1 infection can determine long-term disease outcome

Journal of Virology

Volumn 88, Issue 21, 2014, Pages 12793-12801

  Streeck, Hendrik ^a,b,c   Lu, Richard ^a,b   Beckwith, Noor ^d   Milazzo, Mark ^a,b   Liu, Michelle ^a,b   Routy, Jean Pierre ^e   Little, Susan ^f   Jessen, Heiko ^g   Kelleher, Anthony D ^h   Hecht, Frederick ⁱ   Sekaly, Rafick Pierre ^j   Alter, Galit ^c   Heckerman, David ^k   Carrington, Mary ^c,l   Rosenberg, Eric S ^m   Altfeldc, Marcus ⁿ  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e ROYAL VICTORIA HOSPITAL   (Canada)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^g HIV Clinic Praxis Jessen   (Germany)

^h UNIVERSITY OF NEW SOUTH WALES   (Australia)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j Cancer Vaccines and Immune Therapies Program   (United States)

^k MICROSOFT RESEARCH   (United States)

^l FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^m MASSACHUSETTS GENERAL HOSPITAL   (United States)

ⁿ LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; EPITOPE; GAG PROTEIN; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; HLA B57 ANTIGEN; HLA B8 ANTIGEN; VIRUS RNA;

ACUTE DISEASE; ALLELE; ARTICLE; CAUCASIAN; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELL SPECIFICITY; CELLULAR IMMUNITY; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE CONTROL; DISEASE DURATION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSPOT ASSAY; EVOLUTION; FEMALE; GENOTYPE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NONHUMAN; OUTCOME ASSESSMENT; SPECIES DIFFERENCE; VIREMIA; VIRUS INHIBITION; VIRUS LOAD; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; SECRETION (PROCESS); TIME; TREATMENT OUTCOME; VIROLOGY;

CD4 LYMPHOCYTE COUNT; CD8-POSITIVE T-LYMPHOCYTES; ENZYME-LINKED IMMUNOSPOT ASSAY; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-GAMMA; LONGITUDINAL STUDIES; MALE; TIME FACTORS; TREATMENT OUTCOME; VIRAL LOAD;

EID: 84907967547     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02016-14     Document Type: Article

References (31)

1. Sinicco A, Fora R, Sciandra M, Lucchini A, Caramello P, Gioannini P. 1993 Risk of developing AIDS after primary acute HIV-1 infection. J. Acquir. Immune Defic. Syndr. 6:575-581.
2. Pedersen C, Lindhardt BO, Jensen BL, Lauritzen E, Gerstoft J, Dickmeiss E, Gaub J, Scheibel E, Karlsmark T. 1989. Clinical course of primary HIV infection: consequences for subsequent course of infection. BMJ 299:154-157. http://dx.doi.org/10.1136/bmj.299.6692.154.
3. Vanhems P, Hirschel B, Phillips AN, Cooper DA, Vizzard J, Brassard J, Perrin L. 2000. Incubation time of acute human immunodeficiency virus (HIV) infection and duration of acute HIV infection are independent prognostic factors of progression to AIDS. J. Infect. Dis. 182:334-337. http://dx.doi.org/10.1086/315687.
4. Vanhems P, Lambert J, Cooper DA, Perrin L, Carr A, Hirschel B, Vizzard J, Kinloch-de Loes S, Allard R. 1998. Severity and prognosis of acute human immunodeficiency virus type 1 illness: a dose-response relationship. Clin. Infect. Dis. 26:323-329. http://dx.doi.org/10.1086 /516289.
5. Vanhems P, Voirin N, Hirschel B, Cooper DA, Vizzard J, Carr A, Perrin L. 2003. Brief report: incubation and duration of specific symptoms at acute retroviral syndrome as independent predictors of progression to AIDS. J. Acquir. Immune Defic. Syndr. 32:542-544. http://dx.doi.org/10.1097/00126334-200304150-00012.
6. Saez-Cirion A, Bacchus C, Hocqueloux L, Avettand-Fenoel V, Girault I, Lecuroux C, Potard V, Versmisse P, Melard A, Prazuck T, Descours B, Guergnon J, Viard JP, Boufassa F, Lambotte O, Goujard C, Meyer L, Costagliola D, Venet A, Pancino G, Autran B, Rouzioux C. 2013. Post-treatment HIV-1 controllers with a long-term virological remission after the interruption of early initiated antiretroviral therapy ANRS VISCONTI Study. PLoS Pathog. 9:e1003211. http://dx.doi.org/10.1371/journal.ppat.1003211.
7. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W, Farthing C, Ho DD. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
8. 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.
9. Soghoian DZ, Jessen H, Flanders M, Sierra-Davidson K, Cutler S, Pertel T, Ranasinghe S, Lindqvist M, Davis I, Lane K, Rychert J, Rosenberg ES, Piechocka-Trocha A, Brass AL, Brenchley JM, Walker BD, Streeck H. 2012. HIV-specific cytolytic CD4 T cell responses during acute HIV infection predict disease outcome. Sci. Transl. Med. 4:123ra125. http://dx.doi.org/10.1126/scitranslmed.3003165.
10. Schieffer M, Jessen H, Oster A, Pissani F, Soghoian DZ, Lu R, Jessen A, Zedlack C, Schultz B, Davis I, Ranasinghe S, Rosenberg ES, Alter G, Schumann R, Streeck H. 2014. Induction of Gag-specific CD4 T cell responses during acute HIV infection is associated with improved viral control. J. Virol. 88:7357-7366. http://dx.doi.org/10.1128/JVI.00728-14.
11. Lyles RH, Munoz A, Yamashita TE, Bazmi H, Detels R, Rinaldo CR, Margolick JB, Phair JP, Mellors JW. 2000. Natural history of human immunodeficiency virus type 1 viremia after seroconversion and proximal to AIDS in a large cohort of homosexual men. Multicenter AIDS Cohort Study. J. Infect. Dis. 181:872-880.
12. Streeck H, Jolin JS, Qi Y, Yassine-Diab B, Johnson RC, Kwon DS, Addo MM, Brumme C, Routy JP, Little S, Jessen HK, Kelleher AD, Hecht FM, Sekaly RP, Rosenberg ES, Walker BD, Carrington M, Altfeld M. 2009. HIV-1-specific CD8+T cell responses during primary infection are major determinants of the viral set point and loss of CD4+ T cells. J. Virol. 83:7641-7648. http://dx.doi.org/10.1128/JVI.00182-09.
13. Mudd PA, Martins MA, Ericsen AJ, Tully DC, Power KA, Bean AT, Piaskowski SM, Duan L, Seese A, Gladden AD, Weisgrau KL, Furlott JR, Kim YI, Veloso de Santana MG, Rakasz E, Capuano S, III, Wilson NA, Bonaldo MC, Galler R, Allison DB, Piatak M, Jr, Haase AT, Lifson JD, Allen TM, Watkins DI. 2012. Vaccine-induced CD8+ T cells control AIDS virus replication. Nature 491:129-133. http://dx.doi.org/10.1038 /nature11443.
14. O' Connor DH, Allen TM, Vogel TU, Jing P, DeSouza IP, Dodds E, Dunphy EJ, Melsaether C, Mothe B, Yamamoto H, Horton H, Wilson N, Hughes AL, Watkins DI. 2002. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat. Med. 8:493-499. http://dx.doi.org/10.1038/nm0502-493.
15. Allen TM, Altfeld M, Yu XG, O' Sullivan KM, Lichterfeld M, Le Gall S, John M, Mothe BR, Lee PK, Kalife ET, Cohen DE, Freedberg KA, Strick DA, Johnston MN, Sette A, Rosenberg ES, Mallal SA, Goulder PJ, Brander C, Walker BD. 2004. Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J. Virol. 78:7069-7078. http: //dx.doi.org/10.1128/JVI.78.13.7069-7078.2004.
16. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, Nowak MA, Giangrande P, Luzzi G, Morgan B, Edwards A, McMichael AJ, Rowland-Jones S. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217. http://dx.doi.org/10.1038/nm0297-212.
17. Carrington M, O' Brien SJ. 2003. The influence of HLA genotype on AIDS. Annu. Rev. Med. 54:535-551. http://dx.doi.org/10.1146/annurev.med.54.101601.152346.
18. Addo MM, Yu XG, Rathod A, Cohen D, Eldridge RL, Strick D, Johnston MN, Corcoran C, Wurcel AG, Fitzpatrick CA, Feeney ME, Rodriguez WR, Basgoz N, Draenert R, Stone DR, Brander C, Goulder PJ, Rosenberg ES, Altfeld M, Walker BD. 2003. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J. Virol. 77:2081-2092. http://dx.doi.org/10.1128/JVI.77.3.2081-2092.2003.
19. Frahm N, Korber BT, Adams CM, Szinger JJ, Draenert R, Addo MM, Feeney ME, Yusim K, Sango K, Brown NV, SenGupta D, Piechocka-Trocha A, Simonis T, Marincola FM, Wurcel AG, Stone DR, Russell CJ, Adolf P, Cohen D, Roach T, StJohn A, Khatri A, Davis K, Mullins J, Goulder PJ, Walker BD, Brander C. 2004. Consistent cytotoxic-Tlymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J. Virol. 78:2187-2200. http: //dx.doi.org/10.1128/JVI.78.5.2187-2200.2004.
20. Betts MR, Ambrozak DR, Douek DC, Bonhoeffer S, Brenchley JM, Casazza JP, Koup RA, Picker LJ. 2001. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75:11983-11991 http://dx.doi.org/10.1128/JVI.75.24.11983-11991.2001.
21. Streeck H, Brumme ZL, Anastario M, Cohen KW, Jolin JS, Meier A, Brumme CJ, Rosenberg ES, Alter G, Allen TM, Walker BD, Altfeld M. 2008 Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8+T cells. PLoS Med. 5:e100. http://dx.doi.org/10.1371/journal.pmed.0050100.
22. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, Peddada L, Heldebrant C, Smith R, Conrad A, Kleinman SH, Busch MP. 2003. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 17:1871-1879 http://dx.doi.org/10.1097/00002030-200309050-00005.
23. Streeck H, Frahm N, Walker BD. 2009. The role of IFN-gamma Elispot assay in HIV vaccine research. Nat. Protoc. 4:461-469. http://dx.doi.org /10.1038/nprot.2009.7.
24. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U. S. A. 100:9440-9445. http://dx.doi.org /10.1073/pnas.1530509100.
25. Kelley CF, Barbour JD, Hecht FM. 2007. The relation between symptoms, viral load, and viral load set point in primary HIV infection. J. Acquir. Immune Defic. Syndr. 45:445-448. http://dx.doi.org/10.1097 /QAI.0b013e318074ef6e.
26. Brockman MA, Schneidewind A, Lahaie M, Schmidt A, Miura T, Desouza I, Ryvkin F, Derdeyn CA, Allen S, Hunter E, Mulenga J, Goepfert PA, Walker BD, Allen TM. 2007. Escape and compensation from early HLAB57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J. Virol. 81:12608-12618. http://dx.doi.org/10.1128/JVI.01369-07.
27. Altfeld M, Allen TM, Kalife ET, Frahm N, Addo MM, Mothe BR, Rathod A, Reyor LL, Harlow J, Yu XG, Perkins B, Robinson LK, Sidney J, Alter G, Lichterfeld M, Sette A, Rosenberg ES, Goulder PJ, Brander C, Walker BD. 2005. The majority of currently circulating human immunodeficiency virus type 1 clade B viruses fail to prime cytotoxic T-lymphocyte responses against an otherwise immunodominant HLA-A2-restricted epitope: implications for vaccine design. J. Virol. 79:5000-5005. http://dx.doi.org/10.1128/JVI.79.8.5000-5005.2005.
28. Mellors JW, Margolick JB, Phair JP, Rinaldo CR, Detels R, Jacobson LP, Munoz A. 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. http://dx.doi.org/10.1001/jama.297.21.2349.
29. Mellors JW, Rinaldo CR, Jr, Gupta P, White RM, Todd JA, Kingsley LA. 1996 Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272:1167-1170. http://dx.doi.org/10.1126/science.272.5265.1167.
30. Raposo RA, Abdel-Mohsen M, Holditch SJ, Kuebler PJ, Cheng RG, Eriksson EM, Liao W, Pillai SK, Nixon DF. 2013. Increased expression of intrinsic antiviral genes in HLA-B*57-positive individuals. J. Leukoc. Biol. 94:1051-1059. http://dx.doi.org/10.1189/jlb.0313150.
31. Brumme ZL, Brumme CJ, Carlson J, Streeck H, John M, Eichbaum Q, Block BL, Baker B, Kadie C, Markowitz M, Jessen H, Kelleher AD, Rosenberg E, Kaldor J, Yuki Y, Carrington M, Allen TM, Mallal S, Altfeld M, Heckerman D, Walker BD. 2008. Marked epitope-and allelespecific differences in rates of mutation in human immunodeficiency type 1 (HIV-1) Gag, Pol, and Nef cytotoxic T-lymphocyte epitopes in acute/ early HIV-1 infection. J. Virol. 82:9216-9227. http://dx.doi.org/10.1128 /JVI.01041-08.