248
Views
5
CrossRef citations to date
0
Altmetric
Review

HIV Susceptibility of human antigen-specific CD4 T cells in AIDS pathogenesis and vaccine response

, , &
Pages 709-717 | Received 10 Dec 2015, Accepted 25 Jan 2016, Published online: 17 Feb 2016

References

  • Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood. 2008;112(5):1557–1569.
  • Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations (*). Annu Rev Immunol. 2010;28:445–489.
  • Moir S, Chun TW, Fauci AS. Pathogenic mechanisms of HIV disease. Annu Rev Pathol. 2011;6:223–248.
  • Maartens G, Celum C, Lewin SR. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet. 2014;384(9939):258–271.
  • Stevenson M. HIV-1 pathogenesis. Nat Med. 2003;9(7):853–860.
  • Okoye AA, Picker LJ. CD4(+) T-cell depletion in HIV infection: mechanisms of immunological failure. Immunol Rev. 2013;254(1):54–64.
  • Lane HC, Fauci AS. Immunologic abnormalities in the acquired immunodeficiency syndrome. Annu Rev Immunol. 1985;3:477–500.
  • Schnittman SM, Lane HC, Greenhouse J, et al. Preferential infection of CD4+ memory T cells by human immunodeficiency virus type 1: evidence for a role in the selective T-cell functional defects observed in infected individuals. Proc Natl Acad Sci U S A. 1990;87(16):6058–6062.
  • Munoz A, Schrager LK, Bacellar H, et al. Trends in the incidence of outcomes defining acquired immunodeficiency syndrome (AIDS) in the multicenter AIDS cohort study: 1985-1991. Am J Epidemiol. 1993;137(4):423–438.
  • Mocroft A, Youle M, Phillips AN, et al. The incidence of AIDS-defining illnesses in 4883 patients with human immunodeficiency virus infection. Royal free/chelsea and westminster hospitals collaborative group. Arch Intern Med. 1998;158(5):491–497.
  • Hu H, Eller MA, Zafar S, et al. Preferential infection of human Ad5-specific CD4 T cells by HIV in Ad5 naturally exposed and recombinant Ad5-HIV vaccinated individuals. Proc Natl Acad Sci U S A. 2014;111(37):13439–13444.
  • Hu H, Nau M, Ehrenberg P, et al. Distinct gene-expression profiles associated with the susceptibility of pathogen-specific CD4 T cells to HIV-1 infection. Blood. 2013;121(7):1136–1144.
  • Douek DC, Brenchley JM, Betts MR, et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature. 2002;417(6884):95–98.
  • Geldmacher C, Ngwenyama N, Schuetz A, et al. Preferential infection and depletion of mycobacterium tuberculosis-specific CD4 T cells after HIV-1 infection. J Exp Med. 2010;207(13):2869–2881.
  • Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med. 2009;361(23):2209–2220.
  • Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med. 2012;366(14):1275–1286.
  • Rosenberg ES, Billingsley JM, Caliendo AM, et al. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science. 1997;278(5342):1447–1450.
  • Wilson JD, Imami N, Watkins A, et al. Loss of CD4+ T cell proliferative ability but not loss of human immunodeficiency virus type 1 specificity equates with progression to disease. J Infect Dis. 2000;182(3):792–798.
  • Streeck H, D’Souza MP, Littman DR, et al. Harnessing CD4(+) T cell responses in HIV vaccine development. Nat Med. 2013;19(2):143–149.
  • Huang Y, Follmann D, Nason M, et al. Effect of rAd5-vector HIV-1 preventive vaccines on HIV-1 acquisition: a participant-level meta-analysis of randomized trials. PLoS One. 2015;10(9):e0136626.
  • Buchbinder SP, Mehrotra DV, Duerr A, et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet. 2008;372(9653):1881–1893.
  • Duerr A, Huang Y, Buchbinder S, et al. Extended follow-up confirms early vaccine-enhanced risk of HIV acquisition and demonstrates waning effect over time among participants in a randomized trial of recombinant adenovirus HIV vaccine (Step Study). J Infect Dis. 2012;206(2):258–266.
  • Gray GE, Allen M, Moodie Z, et al. Safety and efficacy of the HVTN 503/phambili study of a clade-B-based HIV-1 vaccine in South Africa: a double-blind, randomised, placebo-controlled test-of-concept phase 2b study. Lancet Infect Dis. 2011;11(7):507–515.
  • Gray GE, Moodie Z, Metch B, et al. Recombinant adenovirus type 5 HIV gag/pol/nef vaccine in South Africa: unblinded, long-term follow-up of the phase 2b HVTN 503/phambili study. Lancet Infect Dis. 2014;14(5):388–396.
  • Hammer SM, Sobieszczyk ME, Janes H, et al. Efficacy trial of a DNA/rAd5 HIV-1 preventive vaccine. N Engl J Med. 2013;369(22):2083–2092.
  • McElrath MJ, De Rosa SC, Moodie Z, et al. HIV-1 vaccine-induced immunity in the test-of-concept step study: a case-cohort analysis. Lancet. 2008;372(9653):1894–1905.
  • Frahm N, DeCamp AC, Friedrich DP, et al. Human adenovirus-specific T cells modulate HIV-specific T cell responses to an Ad5-vectored HIV-1 vaccine. J Clin Invest. 2012;122(1):359–367.
  • Huang Y, Duerr A, Frahm N, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial reveals an association of nonspecific interferon-gamma secretion with increased HIV-1 infection risk: a cohort-based modeling study. PLoS One. 2014;9(11):e108631.
  • Pandey JP, Namboodiri AM, Bu S, et al. Immunoglobulin genes and the acquisition of HIV infection in a randomized trial of recombinant adenovirus HIV vaccine. Virology. 2013;441(1):70–74.
  • Fellay J, Frahm N, Shianna KV, et al. Host genetic determinants of T cell responses to the MRKAd5 HIV-1 gag/pol/nef vaccine in the step trial. J Infect Dis. 2011;203(6):773–779.
  • Zack JA, Arrigo SJ, Weitsman SR, et al. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell. 1990;61(2):213–222.
  • Zack JA, Cann AJ, Lugo JP, et al. HIV-1 production from infected peripheral blood T cells after HTLV-I induced mitogenic stimulation. Science. 1988;240(4855):1026–1029.
  • Chomont N, El-Far M, Ancuta P, et al. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med. 2009;15(8):893–900.
  • Chun TW, Chadwick K, Margolick J, et al. Differential susceptibility of naive and memory CD4+ T cells to the cytopathic effects of infection with human immunodeficiency virus type 1 strain LAI. J Virol. 1997;71(6):4436–4444.
  • Geldmacher C, Koup RA. Pathogen-specific T cell depletion and reactivation of opportunistic pathogens in HIV infection. Trends Immunol. 2012;33(5):207–214.
  • Geldmacher C, Schuetz A, Ngwenyama N, et al. Early depletion of mycobacterium tuberculosis-specific T helper 1 cell responses after HIV-1 infection. J Infect Dis. 2008;198(11):1590–1598.
  • Casazza JP, Brenchley JM, Hill BJ, et al. Autocrine production of beta-chemokines protects CMV-specific CD4 T cells from HIV infection. PLoS Pathog. 2009;5(10):e1000646.
  • Casazza JP, Betts MR, Price DA, et al. Acquisition of direct antiviral effector functions by CMV-specific CD4+ T lymphocytes with cellular maturation. J Exp Med. 2006;203(13):2865–2877.
  • Flynn NM, Forthal DN, Harro CD, et al. Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J Infect Dis. 2005;191(5):654–665.
  • Pitisuttithum P, Gilbert P, Gurwith M, et al. Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J Infect Dis. 2006;194(12):1661–1671.
  • Klein F, Mouquet H, Dosenovic P, et al. Antibodies in HIV-1 vaccine development and therapy. Science. 2013;341(6151):1199–1204.
  • Koup RA, Douek DC. Vaccine design for CD8 T lymphocyte responses. Cold Spring Harb Perspect Med. 2011;1(1):a007252.
  • Kwong PD, Mascola JR, Nabel GJ. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat Rev Immunol. 2013;13(9):693–701.
  • Porichis F, Kaufmann DE. HIV-specific CD4 T cells and immune control of viral replication. Curr Opin HIV AIDS. 2011;6(3):174–180.
  • McCune JM. The dynamics of CD4+ T-cell depletion in HIV disease. Nature. 2001;410(6831):974–979.
  • Rowland-Jones S. HIV infection: where have all the T cells gone? Lancet. 1999;354(9172):5–7.
  • Chou CS, Ramilo O, Vitetta ES. Highly purified CD25- resting T cells cannot be infected de novo with HIV-1. Proc Natl Acad Sci U S A. 1997;94(4):1361–1365.
  • Benlahrech A, Harris J, Meiser A, et al. 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. 2009;106(47):19940–19945.
  • Perreau M, Pantaleo G, Kremer EJ. Activation of a dendritic cell-T cell axis by Ad5 immune complexes creates an improved environment for replication of HIV in T cells. J Exp Med. 2008;205(12):2717–2725.
  • Eller MA, Eller LA, Opollo MS, et al. Induction of HIV-specific functional immune responses by a multiclade HIV-1 DNA vaccine candidate in healthy Ugandans. Vaccine. 2007;25(45):7737–7742.
  • Pantaleo G, Esteban M, Jacobs B, et al. Poxvirus vector-based HIV vaccines. Curr Opin HIV AIDS. 2010;5(5):391–396.
  • Franchini G, Gurunathan S, Baglyos L, et al. Poxvirus-based vaccine candidates for HIV: two decades of experience with special emphasis on canarypox vectors. Expert Rev Vaccines. 2004;3(4 Suppl):S75–S88.
  • Marovich MA. ALVAC-HIV vaccines: clinical trial experience focusing on progress in vaccine development. Expert Rev Vaccines. 2004;3(4 Suppl):S99–S104.
  • de Bruyn G, Rossini AJ, Chiu YL, et al. Safety profile of recombinant canarypox HIV vaccines. Vaccine. 2004;22(5–6):704–713.
  • Hansen SG, Ford JC, Lewis MS, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature. 2011;473(7348):523–527.
  • Hansen SG, Piatak M Jr., Ventura AB, et al. Immune clearance of highly pathogenic SIV infection. Nature. 2013;502(7469):100–104.
  • Hansen SG, Sacha JB, Hughes CM, et al. Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms. Science. 2013;340(6135):1237874.
  • Hansen SG, Vieville C, Whizin N, et al. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med. 2009;15(3):293–299.
  • Staprans SI, Barry AP, Silvestri G, et al. Enhanced SIV replication and accelerated progression to AIDS in macaques primed to mount a CD4 T cell response to the SIV envelope protein. Proc Natl Acad Sci U S A. 2004;101(35):13026–13031.
  • Vogels R, Zuijdgeest D, van Rijnsoever R, et al. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J Virol. 2003;77(15):8263–8271.
  • Abbink P, Lemckert AA, Ewald BA, et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol. 2007;81(9):4654–4663.
  • McFadden G. Poxvirus tropism. Nat Rev Microbiol. 2005;3(3):201–213.
  • Lore K, Adams WC, Havenga MJ, et al. Myeloid and plasmacytoid dendritic cells are susceptible to recombinant adenovirus vectors and stimulate polyfunctional memory T cell responses. J Immunol. 2007;179(3):1721–1729.
  • Teigler JE, Iampietro MJ, Barouch DH. Vaccination with adenovirus serotypes 35, 26, and 48 elicits higher levels of innate cytokine responses than adenovirus serotype 5 in rhesus monkeys. J Virol. 2012;86(18):9590–9598.
  • Teigler JE, Phogat S, Franchini G, et al. The canarypox virus vector ALVAC induces distinct cytokine responses compared to the vaccinia virus-based vectors MVA and NYVAC in rhesus monkeys. J Virol. 2014;88(3):1809–1814.
  • Teigler JE, Kagan JC, Barouch DH. Late endosomal trafficking of alternative serotype adenovirus vaccine vectors augments antiviral innate immunity. J Virol. 2014;88(18):10354–10363.
  • Barouch DH, Picker LJ. Novel vaccine vectors for HIV-1. Nat Rev Microbiol. 2014;12(11):765–771.
  • Haase AT. Targeting early infection to prevent HIV-1 mucosal transmission. Nature. 2010;464(7286):217–223.
  • Wu L, KewalRamani VN. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol. 2006;6(11):859–868.
  • Garnett CT, Erdman D, Xu W, et al. Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J Virol. 2002;76(21):10608–10616.
  • NIAID. Mini-summit on adenovirus platforms for HIV vaccines. Bethesda (MD): National Institutes of Health; 2013.
  • Carnathan DG, Wetzel KS, Yu J, et al. Activated CD4+CCR5+ T cells in the rectum predict increased SIV acquisition in SIVGag/tat-vaccinated rhesus macaques. Proc Natl Acad Sci U S A. 2015;112(2):518–523.
  • Vaccari M, Gordon SN, Fourati S, et al. Adjuvant dependent mucosal V2 responses and RAS activation in vaccine induced protection from SIV(mac251) acquisition. AIDS Res Hum Retroviruses. 2014;30(Suppl 1):A64–A65.
  • Qureshi H, Ma ZM, Huang Y, et al. Low-dose penile SIVmac251 exposure of rhesus macaques infected with adenovirus type 5 (Ad5) and then immunized with a replication-defective Ad5-based SIV gag/pol/nef vaccine recapitulates the results of the phase IIb step trial of a similar HIV-1 vaccine. J Virol. 2012;86(4):2239–2250.
  • Chattopadhyay PK, Yu J, Roederer M. Live-cell assay to detect antigen-specific CD4+ T-cell responses by CD154 expression. Nat Protoc. 2006;1(1):1–6.
  • Zaunders JJ, Munier ML, Seddiki N, et al. High levels of human antigen-specific CD4+ T cells in peripheral blood revealed by stimulated coexpression of CD25 and CD134 (OX40). J Immunol. 2009;183(4):2827–2836.
  • Nepom GT. MHC class II tetramers. J Immunol. 2012;188(6):2477–2482.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.