Magnitude and Kinetics of CD8+ T Cell Activation during Hyperacute HIV Infection Impact Viral Set Point

Immunity

Volumn 43, Issue 3, 2015, Pages 591-604

  Ndhlovu, Zaza M ^a,b   Kamya, Philomena ^a,b   Mewalal, Nikoshia ^a   Kløverpris, Henrik N ^a,g   Nkosi, Thandeka ^a   Pretorius, Karyn ^a   Laher, Faatima ^a   Ogunshola, Funsho ^a   Chopera, Denis ^a   Shekhar, Karthik ^e   Ghebremichael, Musie ^b   Ismail, Nasreen ^a   Moodley, Amber ^a,b   Malik, Amna ^f   Leslie, Alasdair ^a,b   Goulder, Philip J R ^a,f   Buus, Søren ^g   Chakraborty, Arup ^b,e   Dong, Krista ^b   Ndung'u, Thumbi ^a,b,c   Walker, Bruce D ^a,b,d   more..

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

^b HARVARD UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e Massachusetts Institute of Technology Cambridge   (United States)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; TETRAMER; TUMOR NECROSIS FACTOR ALPHA; FAS ANTIGEN; PROTEIN BCL 2; VIRUS RNA;

ADULT; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; BASIC REPRODUCTION NUMBER; BLOOD DONOR; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOPHENOTYPING; KINETICS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TARGET CELL; VIREMIA; VIRUS LOAD; YOUNG ADULT; ADOLESCENT; BLOOD; FLOW CYTOMETRY; GENETICS; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; TIME FACTOR; VIROLOGY;

ADOLESCENT; ANTIGENS, CD95; APOPTOSIS; CD4 LYMPHOCYTE COUNT; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HIV-1; HUMANS; KINETICS; LYMPHOCYTE ACTIVATION; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, VIRAL; TIME FACTORS; VIRAL LOAD; VIREMIA; YOUNG ADULT;

EID: 84941745031     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.08.012     Document Type: Article

References (52)

1. Anahtar M.N., Byrne E.H., Doherty K.E., Bowman B.A., Yamamoto H.S., Soumillon M., Padavattan N., Ismail N., Moodley A., Sabatini M.E., et al. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity 2015, 42:965-976.
2. Appay V., Papagno L., Spina C.A., Hansasuta P., King A., Jones L., Ogg G.S., Little S., McMichael A.J., Richman D.D., Rowland-Jones S.L. Dynamics of T cell responses in HIV infection. J. Immunol. 2002, 168:3660-3666.
3. Badovinac V.P., Porter B.B., Harty J.T. Programmed contraction of CD8(+) T cells after infection. Nat. Immunol. 2002, 3:619-626.
4. Bangs S.C., McMichael A.J., Xu X.N. Bystander T cell activation--implications for HIV infection and other diseases. Trends Immunol. 2006, 27:518-524.
5. Borrow P., Lewicki H., Hahn B.H., Shaw G.M., Oldstone M.B. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 1994, 68:6103-6110.
6. Borrow P., Lewicki H., Wei X., Horwitz M.S., Peffer N., Meyers H., Nelson J.A., Gairin J.E., Hahn B.H., Oldstone M.B., Shaw G.M. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 1997, 3:205-211.
7. Brumme Z.L., Brumme C.J., Carlson J., Streeck H., John M., Eichbaum Q., Block B.L., Baker B., Kadie C., Markowitz M., et al. Marked epitope- and allele-specific 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. 2008, 82:9216-9227.
8. Butz E.A., Bevan M.J. Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity 1998, 8:167-175.
9. Chen H., Ndhlovu Z.M., Liu D., Porter L.C., Fang J.W., Darko S., Brockman M.A., Miura T., Brumme Z.L., Schneidewind A., et al. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat. Immunol. 2012, 13:691-700.
10. Cossarizza A., Bertoncelli L., Nemes E., Lugli E., Pinti M., Nasi M., De Biasi S., Gibellini L., Montagna J.P., Vecchia M., et al. T cell activation but not polyfunctionality after primary HIV infection predicts control of viral load and length of the time without therapy. PLoS ONE 2012, 7:e50728.
11. Dalod M., Dupuis M., Deschemin J.C., Goujard C., Deveau C., Meyer L., Ngo N., Rouzioux C., Guillet J.G., Delfraissy J.F., et al. Weak anti-HIV CD8(+) T-cell effector activity in HIV primary infection. J. Clin. Invest. 1999, 104:1431-1439.
12. Delva W., Abdool Karim Q. The HIV epidemic in Southern Africa - Is an AIDS-free generation possible?. Curr. HIV/AIDS Rep. 2014, 11:99-108.
13. Doisne J.M., Urrutia A., Lacabaratz-Porret C., Goujard C., Meyer L., Chaix M.L., Sinet M., Venet A. CD8+ T cells specific for EBV, cytomegalovirus, and influenza virus are activated during primary HIV infection. J. Immunol. 2004, 173:2410-2418.
14. Fiebig E.W., Wright D.J., Rawal B.D., Garrett P.E., Schumacher R.T., Peddada L., Heldebrant C., Smith R., Conrad A., Kleinman S.H., Busch M.P. Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. AIDS 2003, 17:1871-1879.
15. Freel S.A., Lamoreaux L., Chattopadhyay P.K., Saunders K., Zarkowsky D., Overman R.G., Ochsenbauer C., Edmonds T.G., Kappes J.C., Cunningham C.K., et al. Phenotypic and functional profile of HIV-inhibitory CD8 T cells elicited by natural infection and heterologous prime/boost vaccination. J. Virol. 2010, 84:4998-5006.
16. Gerdes J., Lemke H., Baisch H., Wacker H.H., Schwab U., Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 1984, 133:1710-1715.
17. Goonetilleke N., Liu M.K., Salazar-Gonzalez J.F., Ferrari G., Giorgi E., Ganusov V.V., Keele B.F., Learn G.H., Turnbull E.L., Salazar M.G., et al. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J. Exp. Med. 2009, 206:1253-1272. CHAVI Clinical Core B.
18. Grayson J.M., Zajac A.J., Altman J.D., Ahmed R. Cutting edge: increased expression of Bcl-2 in antigen-specific memory CD8+ T cells. J. Immunol. 2000, 164:3950-3954.
19. Hansen S.G., Ford J.C., Lewis M.S., Ventura A.B., Hughes C.M., Coyne-Johnson L., Whizin N., Oswald K., Shoemaker R., Swanson T., et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 2011, 473:523-527.
20. Hazenberg M.D., Stuart J.W., Otto S.A., Borleffs J.C., Boucher C.A., de Boer R.J., Miedema F., Hamann D. T-cell division in human immunodeficiency virus (HIV)-1 infection is mainly due to immune activation: a longitudinal analysis in patients before and during highly active antiretroviral therapy (HAART). Blood 2000, 95:249-255.
21. Hel Z., Nacsa J., Tryniszewska E., Tsai W.P., Parks R.W., Montefiori D.C., Felber B.K., Tartaglia J., Pavlakis G.N., Franchini G. Containment of simian immunodeficiency virus infection in vaccinated macaques: correlation with the magnitude of virus-specific pre- and postchallenge CD4+ and CD8+ T cell responses. J. Immunol. 2002, 169:4778-4787.
22. Huang J., Ofek G., Laub L., Louder M.K., Doria-Rose N.A., Longo N.S., Imamichi H., Bailer R.T., Chakrabarti B., Sharma S.K., et al. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 2012, 491:406-412.
23. Jin X., Bauer D.E., Tuttleton S.E., Lewin S., Gettie A., Blanchard J., Irwin C.E., Safrit J.T., Mittler J., Weinberger L., et al. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 1999, 189:991-998.
24. Kaech S.M., Tan J.T., Wherry E.J., Konieczny B.T., Surh C.D., Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 2003, 4:1191-1198.
25. Kägi D., Vignaux F., Ledermann B., Bürki K., Depraetere V., Nagata S., Hengartner H., Golstein P. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994, 265:528-530.
26. Kalichman S.C., Simbayi L.C., Kagee A., Toefy Y., Jooste S., Cain D., Cherry C. Associations of poverty, substance use, and HIV transmission risk behaviors in three South African communities. Soc. Sci. Med. 2006, 62:1641-1649.
27. Kiepiela P., Ngumbela K., Thobakgale C., Ramduth D., Honeyborne I., Moodley E., Reddy S., de Pierres C., Mncube Z., Mkhwanazi N., et al. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 2007, 13:46-53.
28. Kostense S., Vandenberghe K., Joling J., Van Baarle D., Nanlohy N., Manting E., Miedema F. Persistent numbers of tetramer+ CD8(+) T cells, but loss of interferon-gamma+ HIV-specific T cells during progression to AIDS. Blood 2002, 99:2505-2511.
29. Koup R.A., Safrit J.T., Cao Y., Andrews C.A., McLeod G., Borkowsky W., Farthing C., Ho D.D. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 1994, 68:4650-4655.
30. Liu M.K., Hawkins N., Ritchie A.J., Ganusov V.V., Whale V., Brackenridge S., Li H., Pavlicek J.W., Cai F., Rose-Abrahams M., et al. Vertical T cell immunodominance and epitope entropy determine HIV-1 escape. J. Clin. Invest. 2013, 123:380-393. CHAVI Core B.
31. Lyles R.H., Muñoz A., Yamashita T.E., Bazmi H., Detels R., Rinaldo C.R., Margolick J.B., Phair J.P., Mellors J.W. 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. 2000, 181:872-880.
32. MacPherson P.A., Fex C., Sanchez-Dardon J., Hawley-Foss N., Angel J.B. Interleukin-7 receptor expression on CD8(+) T cells is reduced in HIV infection and partially restored with effective antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 2001, 28:454-457.
33. Migueles S.A., Connors M. Success and failure of the cellular immune response against HIV-1. Nat. Immunol. 2015, 16:563-570.
34. Migueles S.A., Laborico A.C., Shupert W.L., Sabbaghian M.S., Rabin R., Hallahan C.W., Van Baarle D., Kostense S., Miedema F., McLaughlin M., et al. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 2002, 3:1061-1068.
35. Miller J.D., van der Most R.G., Akondy R.S., Glidewell J.T., Albott S., Masopust D., Murali-Krishna K., Mahar P.L., Edupuganti S., Lalor S., et al. Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity 2008, 28:710-722.
36. Mueller S.N., Hosiawa-Meagher K.A., Konieczny B.T., Sullivan B.M., Bachmann M.F., Locksley R.M., Ahmed R., Matloubian M. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 2007, (New York, N.Y 317, 670-674.
37. Murali-Krishna K., Altman J.D., Suresh M., Sourdive D.J., Zajac A.J., Miller J.D., Slansky J., Ahmed R. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 1998, 8:177-187.
38. Ndhlovu Z.M., Chibnik L.B., Proudfoot J., Vine S., McMullen A., Cesa K., Porichis F., Jones R.B., Alvino D.M., Hart M.G., et al. High-dimensional immunomonitoring models of HIV-1-specific CD8 T-cell responses accurately identify subjects achieving spontaneous viral control. Blood 2013, 121:801-811.
39. Ndung'u T., Sepako E., McLane M.F., Chand F., Bedi K., Gaseitsiwe S., Doualla-Bell F., Peter T., Thior I., Moyo S.M., et al. HIV-1 subtype C in vitro growth and coreceptor utilization. Virology 2006, 347:247-260.
40. Pantaleo G., Demarest J.F., Soudeyns H., Graziosi C., Denis F., Adelsberger J.W., Borrow P., Saag M.S., Shaw G.M., Sekaly R.P., et al. Major expansion of CD8+ T cells with a predominant V beta usage during the primary immune response to HIV. Nature 1994, 370:463-467.
41. Phillips A.N., Lundgren J.D. The CD4 lymphocyte count and risk of clinical progression. Curr. Opin. HIV AIDS 2006, 1:43-49.
42. Radebe M., Nair K., Chonco F., Bishop K., Wright J.K., van der Stok M., Bassett I.V., Mncube Z., Altfeld M., Walker B.D., Ndung'u T. Limited immunogenicity of HIV CD8+ T-cell epitopes in acute Clade C virus infection. J. Infect. Dis. 2011, 204:768-776.
43. Radebe M., Gounder K., Mokgoro M., Ndhlovu Z.M., Mncube Z., Mkhize L., van der Stok M., Jaggernath M., Walker B.D., Ndung'u T. Broad and persistent Gag-specific CD8+ T-cell responses are associated with viral control but rarely drive viral escape during primary HIV-1 infection. AIDS 2015, 29:23-33.
44. Ribeiro R.M., Qin L., Chavez L.L., Li D., Self S.G., Perelson A.S. Estimation of the initial viral growth rate and basic reproductive number during acute HIV-1 infection. J. Virol. 2010, 84:6096-6102.
45. Schmitz J.E., Kuroda M.J., Santra S., Sasseville V.G., Simon M.A., Lifton M.A., Racz P., Tenner-Racz K., Dalesandro M., Scallon B.J., et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999, (New York, N.Y 283, 857-860.
46. Streeck H., Jolin J.S., Qi Y., Yassine-Diab B., Johnson R.C., Kwon D.S., Addo M.M., Brumme C., Routy J.P., Little S., et al. Human immunodeficiency virus type 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. 2009, 83:7641-7648.
47. Streeck H., Lu R., Beckwith N., Milazzo M., Liu M., Routy J.P., Little S., Jessen H., Kelleher A.D., Hecht F., et al. Emergence of individual HIV-specific CD8 T cell responses during primary HIV-1 infection can determine long-term disease outcome. J. Virol. 2014, 88:12793-12801.
48. Trautmann L., Mbitikon-Kobo F.M., Goulet J.P., Peretz Y., Shi Y., Van Grevenynghe J., Procopio F.A., Boulassel M.R., Routy J.P., Chomont N., et al. Profound metabolic, functional, and cytolytic differences characterize HIV-specific CD8 T cells in primary and chronic HIV infection. Blood 2012, 120:3466-3477.
49. Turnbull E.L., Wong M., Wang S., Wei X., Jones N.A., Conrod K.E., Aldam D., Turner J., Pellegrino P., Keele B.F., et al. Kinetics of expansion of epitope-specific T cell responses during primary HIV-1 infection. J. Immunol. 2009, 182:7131-7145.
50. + T cell functions reveals discordance for cytokine secretion and cytolysis. J. Clin. Invest. 2011, 121:4322-4331.
51. Walker B., McMichael A. The T-cell response to HIV. Cold Spring Harb. Perspect. Med. 2012, 2:a007054.
52. Wilson J.D., Ogg G.S., Allen R.L., Goulder P.J., Kelleher A., Sewell A.K., O'Callaghan C.A., Rowland-Jones S.L., Callan M.F., McMichael A.J. Oligoclonal expansions of CD8(+) T cells in chronic HIV infection are antigen specific. J. Exp. Med. 1998, 188:785-790.