Decreased HIV-Specific T-Regulatory Responses Are Associated with Effective DC-Vaccine Induced Immunity

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-19

  Brezar, Vedran ^a,b,c   Ruffin, Nicolas ^a,b,c   Richert, Laura ^c,d,e,f,g   Surenaud, Mathieu ^a,b,c   Lacabaratz, Christine ^a,b,c   Palucka, Karolina ^h,i   Thiébaut, Rodolphe ^c,d,e,f,g   Banchereau, Jacques ^a,b,c,h,i   Levy, Yves ^a,b,c,j   Seddiki, Nabila ^a,b,c  

^a INSERM U955   (France)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^c Vaccine Research Institute   (France)

^d UNIVERSITÉ DE BORDEAUX   (France)

^e INSERM   (France)

^f BORDEAUX UNIVERSITY HOSPITAL   (France)

^g INRIA SISTM   (France)

^h BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

ⁱ JACKSON LABORATORY   (United States)

^j HENRI MONDOR HOSPITAL   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD134 ANTIGEN; CD39 ANTIGEN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17F; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 21; INTERLEUKIN 27; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 9; LIPO 5 VACCINE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; PROTEIN BCL 6; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; IFNG PROTEIN, HUMAN;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; MALE; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; VACCINATION; VIRUS LOAD; VIRUS REPLICATION; CLINICAL TRIAL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; MIDDLE AGED; MULTICENTER STUDY; PHASE 1 CLINICAL TRIAL;

ADULT; AIDS VACCINES; DENDRITIC CELLS; FEMALE; HIV-1; HUMANS; INTERFERON-GAMMA; MALE; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY; VIRAL LOAD;

EID: 84926471944     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004752     Document Type: Article

References (46)

1. Friis-Møller N, Reiss P, Sabin CA, Weber R, DAD Study Group, et al. (2007) Class of antiretroviral drugs and the risk of myocardial infarction. N Engl J Med 356: 1723–1735. doi: 10.1056/NEJMoa062744 17460226
2. Cazanave C, Dupon M, Lavignolle-Aurillac V, Barthe N, Lawson-Ayayi S, et al. (2008) Reduced bone mineral density in HIV-infected patients: prevalence and associated factors. AIDS 22: 395–402. doi: 10.1097/QAD.0b013e3282f423dd 18195566
3. Bonnet F, Amieva H, Marquant F, Bernard C, Bruyand M, et al. (2013) Cognitive disorders in HIV-infected patients: are they HIV-related? AIDS 27: 391–400. doi: 10.1097/QAD.0b013e32835b1019 23079813
4. McMichael AJ, (2006) HIV vaccines. Annu Rev Immunol 24: 227–255. doi: 10.1146/annurev.immunol.24.021605.090605 16551249
5. Fauci AS, Johnston MI, Dieffenbach CW, Burton DR, Hammer SM, et al. (2008) HIV vaccine research: the way forward. Science 321: 530–532. doi: 10.1126/science.1161000 18653883
6. Appay V, (2009) 25 years of HIV research!… and what about a vaccine? Eur J Immunol 39: 1999–2003. doi: 10.1002/eji.200939551 19672891
7. Lévy Y, Gahéry-Ségard H, Durier C, Lascaux A-S, Goujard C, et al. (2005) Immunological and virological efficacy of a therapeutic immunization combined with interleukin-2 in chronically HIV-1 infected patients. AIDS 19: 279–286. 15718838
8. Lévy Y, Durier C, Lascaux A-S, Meiffrédy V, Gahéry-Ségard H, et al. (2006) Sustained control of viremia following therapeutic immunization in chronically HIV-1-infected individuals. AIDS 20: 405–413. doi: 10.1097/01.aids.0000206504.09159.d3 16439874
9. Hansen SG, Vieville C, Whizin N, Coyne-Johnson L, Siess DC, et al. (2009) Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med 15: 293–299. doi: 10.1038/nm.1935 19219024
10. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, et al. (2011) Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473: 523–527. doi: 10.1038/nature10003 21562493
11. Banchereau J, Steinman RM, (1998) Dendritic cells and the control of immunity. Nature 392: 245–252. doi: 10.1038/32588 9521319
12. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767–811. doi: 10.1146/annurev.immunol.18.1.767 10837075
13. Palucka K, Banchereau J, (2013) Human dendritic cell subsets in vaccination. Curr Opin Immunol 25: 396–402. doi: 10.1016/j.coi.2013.05.001 23725656
14. García F, Routy J-P, (2011) Challenges in dendritic cells-based therapeutic vaccination in HIV-1 infection Workshop in dendritic cell-based vaccine clinical trials in HIV-1. Vaccine 29: 6454–6463. doi: 10.1016/j.vaccine.2011.07.043 21791232
15. Lu W, Arraes LC, Ferreira WT, Andrieu J-M, (2004) Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat Med 10: 1359–1365. doi: 10.1038/nm1147 15568033
16. Van Gulck E, Vlieghe E, Vekemans M, Van Tendeloo VFI, Van De Velde A, et al. (2012) mRNA-based dendritic cell vaccination induces potent antiviral T-cell responses in HIV-1-infected patients. AIDS 26: F1–12. doi: 10.1097/QAD.0b013e32834f33e8 22156965
17. García F, Climent N, Guardo AC, Gil C, León A, et al. (2013) A dendritic cell-based vaccine elicits T cell responses associated with control of HIV-1 replication. Sci Transl Med 5: 166ra2. doi: 10.1126/scitranslmed.3004682 23283367
18. Lévy Y, Thiébaut R, Montes M, Lacabaratz C, Sloan L, et al. (2014) Dendritic cell-based therapeutic vaccine elicits polyfunctional HIV-specific T-cell immunity associated with control of viral load. Eur J Immunol 44: 2802–2810. doi: 10.1002/eji.201344433 25042008
19. Weiss L, Donkova-Petrini V, Caccavelli L, Balbo M, Carbonneil C, et al. (2004) Human immunodeficiency virus-driven expansion of CD4+CD25+ regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 104: 3249–3256. doi: 10.1182/blood-2004-01-0365 15271794
20. Takahashi T, Kuniyasu Y, Toda M, Sakaguchi N, Itoh M, et al. (1998) Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int Immunol 10: 1969–1980. 9885918
21. Zaunders JJ, Munier ML, Seddiki N, Pett S, Ip S, et al. (2009) High levels of human antigen-specific CD4+ T cells in peripheral blood revealed by stimulated coexpression of CD25 and CD134 (OX40). J Immunol 183: 2827–2836. doi: 10.4049/jimmunol.0803548 19635903
22. Seddiki N, Cook L, Hsu DC, Phetsouphanh C, Brown K, et al. (2014) Human antigen-specific CD4+CD25+CD134+CD39+ T cells are enriched for regulatory T cells and comprise a substantial proportion of recall responses. Eur J Immunol: n/a–n/a. doi: 10.1002/eji.201344102
23. Croft M, (2010) Control of Immunity by the TNFR-Related Molecule OX40 (CD134). Annu Rev Immunol 28: 57–78. doi: 10.1146/annurev-immunol-030409-101243 20307208
24. Chattopadhyay PK, Yu J, Roederer M, (2006) Live-cell assay to detect antigen-specific CD4+ T-cell responses by CD154 expression. Nat Protocols 1: 1–6. doi: 10.1038/nprot.2006.1
25. Phetsouphanh C, Xu Y, Amin J, Seddiki N, Procopio F, et al. (2013) Characterization of transcription factor phenotypes within antigen-specific CD4+ T cells using qualitative multiplex single-cell RT-PCR. PLoS ONE 8: e74946. doi: 10.1371/journal.pone.0074946 24124462
26. Thornton AM, Korty PE, Tran DQ, Wohlfert EA, Murray PE, et al. (2010) Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J Immunol 184: 3433–3441. doi: 10.4049/jimmunol.0904028 20181882
27. Himmel ME, MacDonald KG, Garcia RV, Steiner TS, Levings MK, (2013) Helios+ and Helios- cells coexist within the natural FOXP3+ T regulatory cell subset in humans. J Immunol 190: 2001–2008. doi: 10.4049/jimmunol.1201379 23359504
28. Allan SE, Crome SQ, Crellin NK, Passerini L, Steiner TS, et al. (2007) Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 19: 345–354. doi: 10.1093/intimm/dxm014 17329235
29. Miyara M, Yoshioka Y, Kitoh A, Shima T, Wing K, et al. (2009) Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 30: 899–911. doi: 10.1016/j.immuni.2009.03.019 19464196
30. McMurchy AN, Levings MK, (2012) Suppression assays with human T regulatory cells: a technical guide. Eur J Immunol 42: 27–34. doi: 10.1002/eji.201141651 22161814
31. Brezar V, Ruffin N, Lévy Y, Seddiki N, (2014) A highly relevant and efficient single step method for simultaneous depletion and isolation of human regulatory T cells in a clinical setting. J Immunol Methods. doi: 10.1016/j.jim.2014.06.003
32. Maeda Y, Nishikawa H, Sugiyama D, Ha D, Hamaguchi M, et al. (2014) Detection of self-reactive CD8+ T cells with an anergic phenotype in healthy individuals. Science 346: 1536–1540. doi: 10.1126/science.aaa1292 25525252
33. Chevalier MF, Jülg B, Pyo A, Flanders M, Ranasinghe S, et al. (2011) HIV-1-specific interleukin-21+ CD4+ T cell responses contribute to durable viral control through the modulation of HIV-specific CD8+ T cell function. J Virol 85: 733–741. doi: 10.1128/JVI.02030-10 21047960
34. Norris PJ, Moffett HF, Yang OO, Kaufmann DE, Clark MJ, et al. (2004) Beyond help: direct effector functions of human immunodeficiency virus type 1-specific CD4(+) T cells. J Virol 78: 8844–8851. doi: 10.1128/JVI.78.16.8844-8851.2004 15280492
35. Stockinger B, Bourgeois C, Kassiotis G, (2006) CD4+ memory T cells: functional differentiation and homeostasis. Immunol Rev 211: 39–48. doi: 10.1111/j.0105-2896.2006.00381 16824115
36. Seddiki N, Brezar V, Draenert R, (2014) Cell exhaustion in HIV-1 infection: role of suppressor cells. Curr Opin HIV AIDS. doi: 10.1097/COH.0000000000000087
37. Welters MJP, Kenter GG, De Vos van Steenwijk PJ, Löwik MJG, Berends-van der Meer DMA, et al. (2010) Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses. Proc Natl Acad Sci USA 107: 11895–11899. doi: 10.1073/pnas.1006500107 20547850
38. Sugiyama D, Nishikawa H, Maeda Y, Nishioka M, Tanemura A, et al. (2013) Anti-CCR4 mAb selectively depletes effector-type FoxP3+CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc Natl Acad Sci USA 110: 17945–17950. doi: 10.1073/pnas.1316796110 24127572
39. Macatangay BJC, Szajnik ME, Whiteside TL, Riddler SA, Rinaldo CR, (2010) Regulatory T cell suppression of Gag-specific CD8 T cell polyfunctional response after therapeutic vaccination of HIV-1-infected patients on ART. PLoS ONE 5: e9852. doi: 10.1371/journal.pone.0009852 20352042
40. Angin M, King M, Altfeld M, Walker BD, Wucherpfennig KW, et al. (2012) Identification of HIV-1-specific regulatory T-cells using HLA class II tetramers. AIDS 26: 2112–2115. doi: 10.1097/QAD.0b013e328358cc75 22874519
41. Sutmuller RPM, Den Brok MHMGM, Kramer M, Bennink EJ, Toonen LWJ, et al. (2006) Toll-like receptor 2 controls expansion and function of regulatory T cells. J Clin Invest 116: 485–494. doi: 10.1172/JCI25439 16424940
42. Liu H, Komai-Koma M, Xu D, Liew FY, (2006) Toll-like receptor 2 signaling modulates the functions of CD4+ CD25+ regulatory T cells. Proc Natl Acad Sci USA 103: 7048–7053. doi: 10.1073/pnas.0601554103 16632602
43. Sierro SR, Donda A, Perret R, Guillaume P, Yagita H, et al. (2011) Combination of lentivector immunization and low-dose chemotherapy or PD-1/PD-L1 blocking primes self-reactive T cells and induces anti-tumor immunity. Eur J Immunol 41: 2217–2228. doi: 10.1002/eji.201041235 21538347
44. Pen JJ, Keersmaecker BD, Heirman C, Corthals J, Liechtenstein T, et al. (2014) Interference with PD-L1/PD-1 co-stimulation during antigen presentation enhances the multifunctionality of antigen-specific T cells. Gene Ther 21: 262–271. doi: 10.1038/gt.2013.80 24401835
45. Cobb A, Roberts LK, Palucka AK, Mead H, Montes M, et al. (2011) Development of a HIV-1 lipopeptide antigen pulsed therapeutic dendritic cell vaccine. J Immunol Methods 365: 27–37. doi: 10.1016/j.jim.2010.11.002 21093448
46. Wittkowski KM, Lee E, Nussbaum R, Chamian FN, Krueger JG, (2004) Combining several ordinal measures in clinical studies. Stat Med 23: 1579–1592. doi: 10.1002/sim.1778 15122738