Regulatory T cells modulate DNA vaccine immunogenicity at early time via functional CD4+ T cells and antigen duration

Frontiers in Immunology

Volumn 6, Issue SEP, 2015, Pages

  Qin, Lizeng ^a,b   Jiang, Guosheng ^a   Han, Jinxiang ^a   Letvin, Norman L ^b  

^a SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG FIRST MEDICAL UNIVERSITY   (China)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Antigen; DNA vaccine; Immunogenicity; Mice; Regulatory T cells

Indexed keywords

DNA VACCINE; GAMMA INTERFERON; GLYCOPROTEIN GP 120; INTERLEUKIN 2; L SELECTIN; NEUTRALIZING ANTIBODY; TRANSCRIPTION FACTOR FOXP3;

ANTIGENIC MODULATION; ARTICLE; BIOLUMINESCENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T CELL DEPLETION;

EID: 84946571774     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00510     Document Type: Article

References (55)

1. Qin L, Greenland JR, Moriya C, Cayabyab MJ, Letvin NL. Effects of type I interferons on the adjuvant properties of plasmid granulocyte-macrophage colony-stimulating factor in vivo. J Virol (2007) 81:10606-13. doi:10.1128/JVI.01000-07.
2. Chen TC, Cobbold SP, Fairchild PJ, Waldmann H. Generation of anergic and regulatory T cells following prolonged exposure to a harmless antigen. J Immunol (2004) 172:5900-7. doi:10.4049/jimmunol.172.10.5900.
3. Boyer JD, Robinson TM, Kutzler MA, Vansant G, Hokey DA, Kumar S, et al. Protection against simian/human immunodeficiency virus (SHIV) 89.6P in Macaques after coimmunization with SHIV antigen and IL-15 plasmid. Proc Natl Acad Sci USA (2007) 104:18648-53. doi:10.1073/pnas.0709198104.
4. Sakaguchi S, Vignali DA, Rudensky AY, Niec RE, Waldmann H. The plasticity and stability of regulatory T cells. Nat Rev Immunol (2013) 13:461-7. doi:10.1038/nri3464.
5. Jelley-Gibbs DM, Dibble JP, Filipson S, Haynes L, Kemp RA, Swain SL. Repeated stimulation of CD4 effector T cells can limit their protective function. J Exp Med (2005) 201:1101-12. doi:10.1084/jem.20041852.
6. Kaech SM, Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol (2001) 2:415-22. doi:10.1038/87720.
7. Prlic M, Blazar BR, Khoruts A, Zell T, Jameson SC. Homeostatic expansion occurs independently of costimulatory signals. J Immunol (2001) 167:5664-8. doi:10.4049/jimmunol.167.10.5664.
8. Radcliffe JN, Roddick JS, Stevenson FK, Thirdborough SM. Prolonged antigen expression following DNA vaccination impairs effector CD8+ T cell function and memory development. J Immunol (2007) 179:8313-21. doi:10.4049/jimmunol.179.12.8313.
9. Swain SL, Agrewala JN, Brown DM, Jelley-Gibbs DM, Golech S, Huston G, et al. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol Rev (2006) 211:8-22. doi:10.1111/j.0105-2896.2006.00388.x.
10. van Stipdonk MJ, Lemmens EE, Schoenberger SP. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol (2001) 2:423-9. doi:10.1038/87730.
11. Aandahl EM, Michaelsson J, Moretto WJ, Hecht FM, Nixon DF. Human CD4+ CD25+ regulatory T cells control T-cell responses to human immunodeficiency virus and Cytomegalovirus antigens. J Virol (2004) 78:2454-9. doi:10.1128/JVI.78.5.2454-2459.2004.
12. Cabrera R, Tu Z, Xu Y, Firpi RJ, Rosen HR, Liu C, et al. An immunomodulatory role for CD4(+)CD25(+) regulatory T lymphocytes in hepatitis C virus infection. Hepatology (2004) 40:1062-71. doi:10.1002/hep.20454.
13. Kinter AL, Hennessey M, Bell A, Kern S, Lin Y, Daucher M, et al. CD25(+)CD4(+) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(+) and CD8(+) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status. J Exp Med (2004) 200:331-43. doi:10.1084/jem.20032069.
14. Scott-Browne JP, Shafiani S, Tucker-Heard G, Ishida-Tsubota K, Fontenot JD, Rudensky AY, et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J Exp Med (2007) 204:2159-69. doi:10.1084/jem.20062105.
15. Weiss L, Donkova-Petrini V, Caccavelli L, Balbo M, Carbonneil C, Levy Y. Human immunodeficiency virus-driven expansion of CD4+CD25+ regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood (2004) 104:3249-56. doi:10.1182/blood-2004-01-0365.
16. Andersson J, Boasso A, Nilsson J, Zhang R, Shire NJ, Lindback S, et al. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J Immunol (2005) 174:3143-7. doi:10.4049/jimmunol.174.6.3143.
17. Suvas S, Rouse BT. Treg control of antimicrobial T cell responses. Curr Opin Immunol (2006) 18:344-8. doi:10.1016/j.coi.2006.03.005.
18. Davis HL, Millan CL, Watkins SC. Immune-mediated destruction of transfected muscle fibers after direct gene transfer with antigen-expressing plasmid DNA. Gene Ther (1997) 4:181-8. doi:10.1038/sj.gt.3300380.
19. Greenland JR, Geiben R, Ghosh S, Pastor WA, Letvin NL. Plasmid DNA vaccine-elicited cellular immune responses limit in vivo vaccine antigen expression through Fas-mediated apoptosis. J Immunol (2007) 178:5652-8. doi:10.4049/jimmunol.178.9.5652.
20. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol (2003) 4:330-6. doi:10.1038/ni904.
21. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science (2003) 299:1057-61. doi:10.1126/science.1079490.
22. Kedzierska K, Stambas J, Jenkins MR, Keating R, Turner SJ, Doherty PC. Location rather than CD62L phenotype is critical in the early establishment of influenza-specific CD8+ T cell memory. Proc Natl Acad Sci USA (2007) 104:9782-7. doi:10.1073/pnas.0703699104.
23. Janssen EM, Lemmens EE, Wolfe T, Christen U, von Herrath MG, Schoenberger SP. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature (2003) 421:852-6. doi:10.1038/nature01441.
24. Fehervari Z, Yamaguchi T, Sakaguchi S. The dichotomous role of IL-2: tolerance versus immunity. Trends Immunol (2006) 27:109-11. doi:10.1016/j.it.2006.01.005.
25. Obst R, van Santen HM, Mathis D, Benoist C. Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J Exp Med (2005) 201:1555-65. doi:10.1084/jem.20042521.
26. Sugimoto K, Ikeda F, Stadanlick J, Nunes FA, Alter HJ, Chang KM. Suppression of HCV-specific T cells without differential hierarchy demonstrated ex vivo in persistent HCV infection. Hepatology (2003) 38:1437-48. doi:10.1016/j.hep.2003.09.026.
27. Rech AJ, Mick R, Martin S, Recio A, Aqui NA, Powell DJ Jr, et al. CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients. Sci Transl Med (2012) 4:134ra62. doi:10.1126/scitranslmed.3003330.
28. Jacobs JF, Punt CJ, Lesterhuis WJ, Sutmuller RP, Brouwer HM, Scharenborg NM, et al. Dendritic cell vaccination in combination with anti-CD25 monoclonal antibody treatment: a phase I/II study in metastatic melanoma patients. Clin Cancer Res (2010) 16:5067-78. doi:10.1158/1078-0432.CCR-10-1757.
29. Bayry J, Tartour E, Tough DF. Targeting CCR4 as an emerging strategy for cancer therapy and vaccines. Trends Pharmacol Sci (2014) 35:163-5. doi:10.1016/j.tips.2014.02.003.
30. Dittmer U, He H, Messer RJ, Schimmer S, Olbrich AR, Ohlen C, et al. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity (2004) 20:293-303. doi:10.1016/S1074-7613(04)00115-3.
31. Toka FN, Suvas S, Rouse BT. CD4+ CD25+ T cells regulate vaccine-generated primary and memory CD8+ T-cell responses against herpes simplex virus type 1. J Virol (2004) 78:13082-9. doi:10.1128/JVI.78.23.13082-13089.2004.
32. Kursar M, Bonhagen K, Fensterle J, Kohler A, Hurwitz R, Kamradt T, et al. Regulatory CD4+CD25+ T cells restrict memory CD8+ T cell responses. J Exp Med (2002) 196:1585-92. doi:10.1084/jem.20011347.
33. Mendez S, Reckling SK, Piccirillo CA, Sacks D, Belkaid Y. Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J Exp Med (2004) 200:201-10. doi:10.1084/jem.20040298.
34. Suvas S, Kumaraguru U, Pack CD, Lee S, Rouse BT. CD4+CD25+ T cells regulate virus-specific primary and memory CD8+ T cell responses. J Exp Med (2003) 198:889-901. doi:10.1084/jem.20030171.
35. Badovinac VP, Harty JT. Programming, demarcating, and manipulating CD8+ T-cell memory. Immunol Rev (2006) 211:67-80. doi:10.1111/j.0105-2896.2006.00384.x.
36. Wong P, Lara-Tejero M, Ploss A, Leiner I, Pamer EG. Rapid development of T cell memory. J Immunol (2004) 172:7239-45. doi:10.4049/jimmunol.172.12.7239.
37. Buchholz VR, Flossdorf M, Hensel I, Kretschmer L, Weissbrich B, Graf P, et al. Disparate individual fates compose robust CD8+ T cell immunity. Science (2013) 340:630-5. doi:10.1126/science.1235454.
38. Gett AV, Sallusto F, Lanzavecchia A, Geginat J. T cell fitness determined by signal strength. Nat Immunol (2003) 4:355-60. doi:10.1038/ni908.
39. Masopust D, Kaech SM, Wherry EJ, Ahmed R. The role of programming in memory T-cell development. Curr Opin Immunol (2004) 16:217-25. doi:10.1016/j.coi.2004.02.005.
40. Klenerman P, Hill A. T cells and viral persistence: lessons from diverse infections. Nat Immunol (2005) 6:873-9. doi:10.1038/ni1241.
41. Wherry EJ, Ahmed R. Memory CD8 T-cell differentiation during viral infection. J Virol (2004) 78:5535-45. doi:10.1128/JVI.78.11.5535-5545.2004.
42. Hovav AH, Panas MW, Rahman S, Sircar P, Gillard G, Cayabyab MJ, et al. Duration of antigen expression in vivo following DNA immunization modifies the magnitude, contraction, and secondary responses of CD8+ T lymphocytes. J Immunol (2007) 179:6725-33. doi:10.4049/jimmunol.179.10.6725.
43. Altfeld M, Rosenberg ES. The role of CD4(+) T helper cells in the cytotoxic T lymphocyte response to HIV-1. Curr Opin Immunol (2000) 12:375-80. doi:10.1016/S0952-7915(00)00103-5.
44. Sun JC, Williams MA, Bevan MJ. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol (2004) 5:927-33. doi:10.1038/ni1105.
45. Northrop JK, Shen H. CD8+ T-cell memory: only the good ones last. Curr Opin Immunol (2004) 16:451-5. doi:10.1016/j.coi.2004.05.004.
46. Bourgeois C, Rocha B, Tanchot C. A role for CD40 expression on CD8+ T cells in the generation of CD8+ T cell memory. Science (2002) 297:2060-3. doi:10.1126/science.1072615.
47. Sercan O, Hammerling GJ, Arnold B, Schuler T. Innate immune cells contribute to the IFN-gamma-dependent regulation of antigen-specific CD8+ T cell homeostasis. J Immunol (2006) 176:735-9. doi:10.4049/jimmunol.176.2.735.
48. Whitmire JK, Benning N, Whitton JL. Cutting edge: early IFN-gamma signaling directly enhances primary antiviral CD4+ T cell responses. J Immunol (2005) 175:5624-8. doi:10.4049/jimmunol.175.9.5624.
49. Whitmire JK, Tan JT, Whitton JL. Interferon-gamma acts directly on CD8+ T cells to increase their abundance during virus infection. J Exp Med (2005) 201:1053-9. doi:10.1084/jem.20041463.
50. D'Souza WN, Schluns KS, Masopust D, Lefrancois L. Essential role for IL-2 in the regulation of antiviral extralymphoid CD8 T cell responses. J Immunol (2002) 168:5566-72. doi:10.4049/jimmunol.168.11.5566.
51. Schoenberger SP, Janssen EM. IL-2 gets with the program. Nat Immunol (2006) 7:798-800. doi:10.1038/ni0806-798.
52. Williams MA, Tyznik AJ, Bevan MJ. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature (2006) 441:890-3. doi:10.1038/nature04790.
53. Barouch DH, Santra S, Tenner-Racz K, Racz P, Kuroda MJ, Schmitz JE, et al. Potent CD4+ T cell responses elicited by a bicistronic HIV-1 DNA vaccine expressing gp120 and GM-CSF. J Immunol (2002) 168:562-8. doi:10.4049/jimmunol.168.2.562.
54. Seaman MS, Peyerl FW, Jackson SS, Lifton MA, Gorgone DA, Schmitz JE, et al. Subsets of memory cytotoxic T lymphocytes elicited by vaccination influence the efficiency of secondary expansion in vivo. J Virol (2004) 78:206-15. doi:10.1128/JVI.78.1.206-215.2004.
55. Takahashi H, Nakagawa Y, Pendleton CD, Houghten RA, Yokomuro K, Germain RN, et al. Induction of broadly cross-reactive cytotoxic T cells recognizing an HIV-1 envelope determinant. Science (1992) 255:333-6. doi:10.1126/science.1372448.