Shaping the CD4+ memory immune response against tuberculosis: The role of antigen persistence, location and multi-functionality

Biomolecular Concepts

Volumn 3, Issue 1, 2012, Pages 13-20

  Ancelet, Lindsay ^a   Kirman, Joanna ^a  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

Author keywords

CD4; intracellular pathogen; T cell memory; tuberculosis; vaccine

Indexed keywords

EID: 84865469321     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc.2011.051     Document Type: Review

References (81)

1. Whitmire JK, Benning N, Whitton JL. Precursor frequency, nonlinear proliferation, and functional maturation of virus-specific CD4 + T cells. J Immunol 2006; 176: 3028-36.
2. Swain SL, Croft M, Dubey C, Haynes L, Rogers P, Zhang X, Bradley LM. From naive to memory T cells. Immunol Rev 1996; 150: 143-67.
3. Uehara T, Miyawaki T, Ohta K, Tamaru Y, Yokoi T, Nakamura S, Taniguchi N. Apoptotic cell death of primed CD45RO + T lymphocytes in Epstein-Barr virus-induced infectious mononucleosis. Blood 1992; 80: 452-8.
4. Ahmed R, Gray D. Immunological memory and protective immunity: understanding their relation. Science 1996; 272: 54-60.
5. Rogers PR, Dubey C, Swain SL. Qualitative changes accompany memory T cell generation: faster, more effective responses at lower doses of antigen. J Immunol 2000; 164: 2338-46.
6. Seder RA, Hill AV. Vaccines against intracellular infections requiring cellular immunity. Nature 2000; 406: 793-8.
7. Glaziou P, Floyd K, Raviglione M. Global burden and epidemiology of tuberculosis. Clin Chest Med 2009; 30: 621-36.
8. Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 1999; 282: 677-86.
9. Fine PE. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 1995; 346: 1339-45.
10. Colditz GA, Brewer TF, Berkey CS, Wilson ME, Burdick E, Fineberg HV, Mosteller F. Efficacy of BCG vaccine in the prevention of tuberculosis. Meta-analysis of the published literature. JAMA 1994; 271: 698-702.
11. Weir RE, Gorak-Stolinska P, Floyd S, Lalor MK, Stenson S, Branson K, Blitz R, Ben-Smith A, Fine PE, Dockrell HM. Persistence of the immune response induced by BCG vaccination. BMC Infect Dis 2008; 8: 9.
12. Ozeki Y, Hirayama Y, Takii T, Yamamoto S, Kobayashi K, Matsumoto S. Loss of anti-mycobacterial efficacy in mice over time following vaccination with Mycobacterium bovis bacillus Calmette-Guerin. Vaccine 2011; 29: 6881-7.
13. Nunn P, Williams B, Floyd K, Dye C, Elzinga G, Raviglione M. Tuberculosis control in the era of HIV. Nat Rev Immunol 2005; 5: 819-26.
14. Jassal M, Bishai WR. Extensively drug-resistant tuberculosis. Lancet Infect Dis 2009; 9: 19-30.
15. Kaufmann SH. Protection against tuberculosis: cytokines, T cells, and macrophages. Ann Rheum Dis 2002; 61 Suppl 2: ii 54-8.
16. Cooper AM. Cell-mediated immune responses in tuberculosis. Annu Rev Immunol 2009; 27: 393-422.
17. Havlir DV, Barnes PF. Tuberculosis in patients with human immunodeficiency virus infection. N Engl J Med 1999; 340: 367-73.
18. Scanga CA, Mohan VP, Yu K, Joseph H, Tanaka K, Chan J, Flynn JL. Depletion of CD4 + T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon-γ and nitric oxide synthase 2. J Exp Med 2000; 192: 347-58.
19. Mogues T, Goodrich ME, Ryan L, LaCourse R, North RJ. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J Exp Med 2001; 193: 271-80.
20. Cooper AM, Magram J, Ferrante J, Orme IM. Interleukin 12 (IL-12) is crucial to the development of protective immunity in mice intravenously infected with mycobacterium tuberculosis. J Exp Med 1997; 186: 39-45.
21. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon-γ genedisrupted mice. J Exp Med 1993; 178: 2243-7.
22. Caruso AM, Serbina N, Klein E, Triebold K, Bloom BR, Flynn JL. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-γ , yet succumb to tuberculosis. J Immunol 1999; 162: 5407-16.
23. Ladel CH, Daugelat S, Kaufmann SH. Immune response to Mycobacterium bovis bacille Calmette Guerin infection in major histocompatibility complex class I-and II-deficient knock-out mice: contribution of CD4 and CD8 T cells to acquired resistance. Eur J Immunol 1995; 25: 377-84.
24. Flynn J, Chan C. Immunology of tuberculosis. Annu Rev Immunol 2001; 19: 93-129.
25. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999; 401: 708-12.
26. Andersen P, Smedegaard B. CD4 + T-cell subsets that mediate immunological memory to Mycobacterium tuberculosis infection in mice. Infect Immun 2001; 68: 621-9.
27. Dharmadhikari AS, Nardell EA. What animal models teach humans about tuberculosis. Am J Respir Cell Mol Biol 2008; 39: 503-8.
28. Jung Y, Ryan L, LaCourse R, North RJ. Properties and protective value of the secondary versus primary T helper type 1 response to airborne Mycobacterium tuberculosis infection in mice. J Exp Med 2005; 201: 1915-24.
29. McKinstry KK, Strutt TM, Swain SL. The potential of CD4 T-cell memory. Immunology 2010; 130: 1-9.
30. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004; 22: 745-63.
31. Henao-Tamayo MI, Ordway DJ, Irwin SM, Shang S, Shanley C, Orme IM. Phenotypic definition of effector and memory T-lymphocyte subsets in mice chronically infected with Mycobacterium tuberculosis . Clin Vaccine Immunol 2010; 17: 618-25.
32. Zielinski CE, Corti D, Mele F, Pinto D, Lanzavecchia A, Sallusto F. Dissecting the human immunologic memory for pathogens. Immunol Rev 2011; 240: 40-51.
33. Sallusto F, Lanzavecchia A. Heterogeneity of CD4 + memory T cells: functional modules for tailored immunity. Eur J Immunol 2009; 39: 2076-82.
34. Masopust D, Kaech SM, Wherry EJ, Ahmed R. The role of programming in memory T-cell development. Curr Opin Immunol 2004; 16: 217-25.
35. Ulrichs T, Kaufmann SH. Mycobacterial persistence and immunity. Front Biosci 2002; 7: d458-69.
36. Trevenen CL, Pagtakhan RD. Disseminated tuberculoid lesions in infants following BCG vaccination. Can Med Assoc J 1982; 127: 502-4.
37. Orme IM. The Achilles heel of BCG. Tuberculosis (Edinb) 2010; 90: 329-32.
38. Lanzavecchia A, Sallusto F. Understanding the generation and function of memory T cell subsets. Curr Opin Immunol 2005; 17: 326-32.
39. Lanzavecchia A, Sallusto F. Progressive differentiation and selection of the fittest in the immune response. Nat Rev Immunol 2002; 2: 982-7.
40. Reiley WW, Shafiani S, Wittmer ST, Tucker-Heard G, Moon JJ, Jenkins MK, Urdahl KB, Winslow GM, Woodland DL. Distinct functions of antigen-specific CD4 T cells during murine Mycobacterium tuberculosis infection. Proc Natl Acad Sci USA 2010; 107: 19408-13.
41. Albrecht I, Niesner U, Janke M, Menning A, Loddenkemper C, Kuhl AA, Lepenies I, Lexberg MH, Westendorf K, Hradilkova K, Grun J, Hamann A, Epstein JA, Chang HD, Tokoyoda K, Radbruch A. Persistence of effector memory Th1 cells is regulated by Hopx. Eur J Immunol 2010; 40: 2993-3006.
42. Orme IM. Characteristics and specificity of acquired immunologic memory to Mycobacterium tuberculosis infection. J Immunol 1988; 140: 3589-93.
43. Harbertson J, Biederman E, Bennett KE, Kondrack RM, Bradley LM. Withdrawal of stimulation may initiate the transition of effector to memory CD4 cells. J Immunol 2002; 168: 1095-102.
44. Zaph C, Uzonna J, Beverley SM, Scott P. Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat Med 2004; 10: 1104-10.
45. Dalai SK, Khoruzhenko S, Drake CG, Jie CC, Sadegh-Nasseri S. Resolution of infection promotes a state of dormancy and long survival of CD4 memory T cells. Immunol Cell Biol 2011; 107: 19408-13.
46. Williams MA, Ravkov EV, Bevan MJ. Rapid culling of the CD4 + T cell repertoire in the transition from effector to memory. Immunity 2008; 28: 533-45.
47. Ochsenbein AF, Karrer U, Klenerman P, Althage A, Ciurea A, Shen H, Miller JF, Whitton JL, Hengartner H, Zinkernagel RM. A comparison of T cell memory against the same antigen induced by virus versus intracellular bacteria. Proc Natl Acad Sci USA 1999; 96: 9293-8.
48. Triccas JA, Nambiar JK. Challenge of developing new tuberculosis vaccines to generate life-long protective immunity. Expert Rev Vaccines 2009; 8: 823-5.
49. Martin C, Williams A, Hernandez-Pando R, Cardona PJ, Gormley E, Bordat Y, Soto CY, Clark SO, Hatch GJ, Aguilar D, Ausina V, Gicquel B. The live Mycobacterium tuberculosis phoP mutant strain is more attenuated than BCG and confers protective immunity against tuberculosis in mice and guinea pigs. Vaccine 2006; 24: 3408-19.
50. Pinto R, Saunders BM, Camacho LR, Britton WJ, Gicquel B, Triccas JA. Mycobacterium tuberculosis defective in phthiocerol dimycocerosate translocation provides greater protective immunity against tuberculosis than the existing bacille Calmette-Guerin vaccine. J Infect Dis 2004; 189: 105-12.
51. Duffy D, Dawoodji A, Agger EM, Andersen P, Westermann J, Bell EB. Immunological memory transferred with CD4 T cells specific for tuberculosis antigens Ag85B-TB10.4: persisting antigen enhances protection. PLoS One 2009; 4: e8272.
52. Orme IM. Induction of nonspecific acquired resistance and delayed-type hypersensitivity, but not specific acquired resistance in mice inoculated with killed mycobacterial vaccines. Infect Immun 1988; 56: 3310-2.
53. Haile M, Schroder U, Hamasur B, Pawlowski A, Jaxmar T, Kallenius G, Svenson SB. Immunization with heat-killed Mycobacterium bovis bacille Calmette-Guerin (BCG) in Eurocine L3 adjuvant protects against tuberculosis. Vaccine 2004; 22: 1498-508.
54. Sambandamurthy VK, Derrick SC, Jalapathy KV, Chen B, Russell RG, Morris SL, Jacobs WR Jr. Long-term protection against tuberculosis following vaccination with a severely attenuated double lysine and pantothenate auxotroph of Mycobacterium tuberculosis . Infect Immun 2005; 73: 1196-203.
55. Wolf AJ, Desvignes L, Linas B, Banaiee N, Tamura T, Takatsu K, Ernst JD. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 2008; 205: 105-15.
56. Reiley WW, Calayag MD, Wittmer ST, Huntington JL, Pearl JE, Fountain JJ, Martino CA, Roberts AD, Cooper AM, Winslow GM, Woodland DL. ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc Natl Acad Sci USA 2008; 105: 10961-6.
57. Price PW, Cerny J. Characterization of CD4 + T cells in mouse bone marrow. I. Increased activated/memory phenotype and altered TCR V β repertoire. Eur J Immunol 1999; 29: 1051-6.
58. Tokoyoda K, Zehentmeier S, Hegazy AN, Albrecht I, Grun JR, Lohning M, Radbruch A. Professional memory CD4 + T lymphocytes preferentially reside and rest in the bone marrow. Immunity 2009; 30: 721-30.
59. Li J, Huston G, Swain SL. IL-7 promotes the transition of CD4 effectors to persistent memory cells. J Exp Med 2003; 198: 1807-15.
60. Kondrack RM, Harbertson J, Tan JT, McBreen ME, Surh CD, Bradley LM. Interleukin 7 regulates the survival and generation of memory CD4 cells. J Exp Med 2003; 198: 1797-806.
61. Pepper M, Linehan JL, Pagan AJ, Zell T, Dileepan T, Cleary PP, Jenkins MK. Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat Immunol 2010; 11: 83-9.
62. DeNucci CC, Shimizu Y. Beta1 integrin is critical for the maintenance of antigen-specific CD4 T cells in the bone marrow but not long-term immunological memory. J Immunol 2011; 186: 4019-26.
63. Hofmann M, Brinkmann V, Zerwes HG. FTY720 preferentially depletes naive T cells from peripheral and lymphoid organs. Int Immunopharmacol 2006; 6: 1902-10.
64. Maeda Y, Seki N, Sato N, Sugahara K, Chiba K. Sphingosine 1-phosphate receptor type 1 regulates egress of mature T cells from mouse bone marrow. Int Immunol 2010; 22: 515-25.
65. Connor LM, Harvie MC, Rich FJ, Quinn KM, Brinkmann V, Le Gros G, Kirman JR. A key role for lung-resident memory lymphocytes in protective immune responses after BCG vaccination. Eur J Immunol 2010; 40: 2482-92.
66. Santosuosso M, Zhang X, McCormick S, Wang J, Hitt M, Xing Z. Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J Immunol 2005; 174: 7986-94.
67. Day TA, Koch M, Nouailles G, Jacobsen M, Kosmiadi GA, Miekley D, Kuhlmann S, Jorg S, Gamradt P, Mollenkopf H-J, Hurwitz R, Reece ST, Kaufmann SH, Kursar M. Secondary lymphoid organs are dispensable for the development of Tcell-mediated immunity during tuberculosis. Eur J Immunol 2010; 40: 1663-73.
68. Chackerian AA, Alt JM, Perera TV, Dascher CC, Behar SM. Dissemination of Mycobacterium tuberculosis is influenced by host factors and precedes the initiation of T-cell immunity. Infect Immun 2002; 70: 4501-9.
69. Feuerer M, Beckhove P, Garbi N, Mahnke Y, Limmer A, Hommel M, Hammerling GJ, Kyewski B, Hamann A, Umansky V, Schirrmacher V. Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat Med 2003; 9: 1151-7.
70. Mittrucker H-W, Steinhoff U, Kohler A, Krause M, Lazar D, Mex P, Miekley D, Kaufmann SH. Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. Proc Natl Acad Sci USA 2007; 104: 12434-9.
71. Goldsack L, Kirman JR. Half-truths and selective memory: interferon-γ , CD4 + T cells and protective memory against tuberculosis. Tuberculosis (Edinb) 2007; 87: 465-73.
72. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, Hoff ST, Andersen P, Reed SG, Morris SL, Roederer M, Seder RA. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major . Nat Med 2007; 13: 843-50.
73. Lindenstrom T, Agger EM, Korsholm KS, Darrah PA, Aagaard C, Seder RA, Rosenkrands I, Andersen P. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J Immunol 2009; 182: 8047-55.
74. Derrick SC, Yabe IM, Yang A, Morris SL. Vaccine-induced antituberculosis protective immunity in mice correlates with the magnitude and quality of multifunctional CD4 T cells. Vaccine 2011; 29: 2902-9.
75. Forbes EK, Sander C, Ronan EO, McShane H, Hill AV, Beverley PC, Tchilian EZ. Multifunctional, high-level cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J Immunol 2008; 181: 4955-64.
76. Caccamo N, Guggino G, Joosten SA, Gelsomino G, Di Carlo P, Titone L, Galati D, Bocchino M, Matarese A, Salerno A, Sanduzzi A, Franken WP, Ottenhoff TH, Dieli F. Multifunctional CD4 + T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol 2010; 40: 2211-20.
77. Sutherland JS, Adetifa IM, Hill PC, Adegbola RA, Ota MO. Pattern and diversity of cytokine production differentiates between Mycobacterium tuberculosis infection and disease. Eur J Immunol 2009; 39: 723-9.
78. Harari A, Rozot V, Enders FB, Perreau M, Stalder JM, Nicod LP, Cavassini M, Calandra T, Blanchet CL, Jaton K, Faouzi M, Day CL, Hanekom WA, Bart P-A, Pantaleo G. Dominant TNF-α + Mycobacterium tuberculosis-specific CD4 + T cell responses discriminate between latent infection and active disease. Nat Med 2011; 17: 372-6.
79. Day CL, Abrahams DA, Lerumo L, Janse van Rensburg E, Stone L, O Rie T, Pienaar B, de Kock M, Kaplan G, Mahomed H, Dheda K, Hanekom WA. Functional capacity of Mycobacterium tuberculosis-specific T cell responses in humans is associated with mycobacterial load. J Immunol 2011: epublished ahead of print.
80. Kagina BM, Abel B, Scriba TJ, Hughes EJ, Keyser A, Soares A, Gamieldien H, Sidibana M, Hatherill M, Gelderbloem S, Mahomed H, Hawkridge A, Hussey G, Kaplan G, Hanekom WA, other members of the South African Tuberculosis Vaccine Initiative. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after bacillus Calmette-Guerin vaccination of newborns. Am J Respir Crit Care Med 2010; 182: 1073-9.
81. MacLeod MK, Kappler JW, Marrack P. Memory CD4 T cells: generation, reactivation and reassignment. Immunology 2010; 130: 10-5.