Functional profile of CD4+ and CD8+ T cells in latently infected individuals and patients with active TB

Tuberculosis

Volumn 93, Issue 2, 2013, Pages 155-166

  Marín, Nancy D ^a,c   París, Sara C ^a   Rojas, Mauricio ^a,b   García, Luis F ^a  

^a Instituto de Biología   (Colombia)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^c NDM Is the Recipient of A Predoctoral Scholarship from Colciencias   (Colombia)

Author keywords

CD4+; CD8+; Polyfunctional T cells; Th1; Th17; Tuberculosis

Indexed keywords

BCG VACCINE; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 2; MYCOBACTERIUM ANTIGEN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; LATENT PERIOD; MAJOR CLINICAL STUDY; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; TUBERCULOSIS;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; HUMANS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; LATENT TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; TH1 CELLS; TH17 CELLS; TIME FACTORS; TUBERCULIN; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84875225016     PISSN: 14729792     EISSN: 1873281X     Source Type: Journal    
DOI: 10.1016/j.tube.2012.12.002     Document Type: Article

References (66)

1. WHO Global tuberculosis report 2012 2012 World Health Organization p. 282
2. G. Walzl, K. Ronacher, W. Hanekom, T.J. Scriba, and A. Zumla Immunological biomarkers of tuberculosis Nat Rev Immunol 11 2011 343 354
3. A. Lalvani, A.A. Pathan, H. McShane, R.J. Wilkinson, M. Latif, C.P. Conlon, G. Pasvol, and A.V. Hill Rapid detection of Mycobacterium tuberculosis infection by enumeration of antigen-specific T cells Am J Respir Crit Care Med 163 2001 824 828
4. T. Mori, M. Sakatani, F. Yamagishi, T. Takashima, Y. Kawabe, K. Nagao, E. Shigeto, N. Harada, S. Mitarai, M. Okada, K. Suzuki, Y. Inoue, K. Tsuyuguchi, Y. Sasaki, G.H. Mazurek, and I. Tsuyuguchi Specific detection of tuberculosis infection: an interferon-gamma-based assay using new antigens Am J Respir Crit Care Med 170 2004 59 64
5. M. Pai, A. Zwerling, and D. Menzies Systematic review: T-cell-based assays for the diagnosis of latent tuberculosis infection: an update Ann Intern Med 149 2008 177 184
6. D. Goletti, S. Carrara, O. Butera, M. Amicosante, M. Ernst, I. Sauzullo, V. Vullo, D. Cirillo, E. Borroni, R. Markova, R. Drenska, J. Dominguez, I. Latorre, C. Angeletti, A. Navarra, N. Petrosillo, F.N. Lauria, G. Ippolito, G.B. Migliori, C. Lange, and E. Girardi Accuracy of immunodiagnostic tests for active tuberculosis using single and combined results: a multicenter TBNET-Study PLoS One 3 2008 e3417
7. J.L. Flynn, J. Chan, K.J. Triebold, D.K. Dalton, T.A. Stewart, and B.R. Bloom An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection J Exp Med 178 1993 2249 2254
8. A.A. Chackerian, T.V. Perera, and S.M. Behar Gamma interferon-producing CD4+ T lymphocytes in the lung correlate with resistance to infection with Mycobacterium tuberculosis Infect Immun 69 2001 2666 2674
9. I.M. Orme, and A.M. Cooper Cytokine/chemokine cascades in immunity to tuberculosis Immunol Today 20 1999 307 312
10. B.M. Kagina, B. Abel, T.J. Scriba, E.J. Hughes, A. Keyser, A. Soares, H. Gamieldien, M. Sidibana, M. Hatherill, S. Gelderbloem, H. Mahomed, A. Hawkridge, G. Hussey, G. Kaplan, and W.A. Hanekom 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 182 2010 1073 1079
11. N. Caccamo, G. Guggino, S.A. Joosten, G. Gelsomino, P. Di Carlo, L. Titone, D. Galati, M. Bocchino, A. Matarese, A. Salerno, A. Sanduzzi, W.P. Franken, T.H. Ottenhoff, and F. Dieli Multifunctional CD4(+) T cells correlate with active Mycobacterium tuberculosis infection Eur J Immunol 40 2010 2211 2220
12. J.W. Gratama, F. Kern, F. Manca, and M. Roederer Measuring antigen-specific immune responses, 2008 update Cytometry A 73 2008 971 974
13. H.M. Algood, P.L. Lin, and J.L. Flynn Tumor necrosis factor and chemokine interactions in the formation and maintenance of granulomas in tuberculosis Clin Infect Dis 41 Suppl. 3 2005 S189 S193
14. M. Jacobs, D. Togbe, C. Fremond, A. Samarina, N. Allie, T. Botha, D. Carlos, S.K. Parida, S. Grivennikov, S. Nedospasov, A. Monteiro, M. Le Bert, V. Quesniaux, and B. Ryffel Tumor necrosis factor is critical to control tuberculosis infection Microb Infect 9 2007 623 628
15. J. Keane, S. Gershon, R.P. Wise, E. Mirabile-Levens, J. Kasznica, W.D. Schwieterman, J.N. Siegel, and M.M. Braun Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent N Engl J Med 345 2001 1098 1104
16. K.K. Hoyer, H. Dooms, L. Barron, and A.K. Abbas Interleukin-2 in the development and control of inflammatory disease Immunol Rev 226 2008 19 28
17. E. Zorn, E.A. Nelson, M. Mohseni, F. Porcheray, H. Kim, D. Litsa, R. Bellucci, E. Raderschall, C. Canning, R.J. Soiffer, D.A. Frank, and J. Ritz IL-2 regulates FOXP3 expression in human CD4+CD25+ regulatory T cells through a STAT-dependent mechanism and induces the expansion of these cells in vivo Blood 108 2006 1571 1579
18. T.R. Malek, and A.L. Bayer Tolerance, not immunity, crucially depends on IL-2 Nat Rev Immunol 4 2004 665 674
19. M. Zhang, Y. Lin, D.V. Iyer, J. Gong, J.S. Abrams, and P.F. Barnes T-cell cytokine responses in human infection with Mycobacterium tuberculosis Infect Immun 63 1995 3231 3234
20. V. Sargentini, S. Mariotti, S. Carrara, M.C. Gagliardi, R. Teloni, D. Goletti, and R. Nisini Cytometric detection of antigen-specific IFN-gamma/IL-2 secreting cells in the diagnosis of tuberculosis BMC Infect Dis 9 2009 99
21. K.A. Millington, J.A. Innes, S. Hackforth, T.S. Hinks, J.J. Deeks, D.P. Dosanjh, V. Guyot-Revol, R. Gunatheesan, P. Klenerman, and A. Lalvani Dynamic relationship between IFN-gamma and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load J Immunol 178 2007 5217 5226
22. Y. Okamoto Yoshida, M. Umemura, A. Yahagi, R.L. O'Brien, K. Ikuta, K. Kishihara, H. Hara, S. Nakae, Y. Iwakura, and G. Matsuzaki Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung J Immunol 184 2010 4414 4422
23. S.A. Khader, G.K. Bell, J.E. Pearl, J.J. Fountain, J. Rangel-Moreno, G.E. Cilley, F. Shen, S.M. Eaton, S.L. Gaffen, S.L. Swain, R.M. Locksley, L. Haynes, T.D. Randall, and A.M. Cooper IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge Nat Immunol 8 2007 369 377
24. B. Nandi, and S.M. Behar Regulation of neutrophils by interferon-{gamma} limits lung inflammation during tuberculosis infection J Exp Med 208 2011 2251 2262
25. J.K. Kolls, and A. Linden Interleukin-17 family members and inflammation Immunity 21 2004 467 476
26. B.S. McKenzie, R.A. Kastelein, and D.J. Cua Understanding the IL-23-IL-17 immune pathway Trends Immunol 27 2006 17 23
27. S.Y. Eum, J.H. Kong, M.S. Hong, Y.J. Lee, J.H. Kim, S.H. Hwang, S.N. Cho, L.E. Via, and C.E. Barry 3rd Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB Chest 137 2010 122 128
28. E. Torrado, and A.M. Cooper IL-17 and Th17 cells in tuberculosis Cytokine Growth Factor Rev 21 2010 455 462
29. R.A. Seder, P.A. Darrah, and M. Roederer T-cell quality in memory and protection: implications for vaccine design Nat Rev Immunol 8 2008 247 258
30. J.R. Almeida, D.A. Price, L. Papagno, Z.A. Arkoub, D. Sauce, E. Bornstein, T.E. Asher, A. Samri, A. Schnuriger, I. Theodorou, D. Costagliola, C. Rouzioux, H. Agut, A.G. Marcelin, D. Douek, B. Autran, and V. Appay Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover J Exp Med 204 2007 2473 2485
31. P.A. Darrah, D.T. Patel, P.M. De Luca, R.W. Lindsay, D.F. Davey, B.J. Flynn, S.T. Hoff, P. Andersen, S.G. Reed, S.L. Morris, M. Roederer, and R.A. Seder Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major Nat Med 13 2007 843 850
32. T.J. Scriba, M. Tameris, N. Mansoor, E. Smit, L. van der Merwe, F. Isaacs, A. Keyser, S. Moyo, N. Brittain, A. Lawrie, S. Gelderbloem, A. Veldsman, M. Hatherill, A. Hawkridge, A.V. Hill, G.D. Hussey, H. Mahomed, H. McShane, and W.A. Hanekom Modified vaccinia Ankara-expressing Ag85A, a novel tuberculosis vaccine, is safe in adolescents and children, and induces polyfunctional CD4+ T cells Eur J Immunol 40 2010 279 290
33. B. Abel, M. Tameris, N. Mansoor, S. Gelderbloem, J. Hughes, D. Abrahams, L. Makhethe, M. Erasmus, M. de Kock, L. van der Merwe, A. Hawkridge, A. Veldsman, M. Hatherill, G. Schirru, M.G. Pau, J. Hendriks, G.J. Weverling, J. Goudsmit, D. Sizemore, J.B. McClain, M. Goetz, J. Gearhart, H. Mahomed, G.D. Hussey, J.C. Sadoff, and W.A. Hanekom The novel tuberculosis vaccine, AERAS-402, induces robust and polyfunctional CD4+ and CD8+ T cells in adults Am J Respir Crit Care Med 181 2010 1407 1417
34. A.P. Soares, T.J. Scriba, S. Joseph, R. Harbacheuski, R.A. Murray, S.J. Gelderbloem, A. Hawkridge, G.D. Hussey, H. Maecker, G. Kaplan, and W.A. Hanekom Bacillus Calmette-Guerin vaccination of human newborns induces T cells with complex cytokine and phenotypic profiles J Immunol 180 2008 3569 3577
35. N.E. Beveridge, D.A. Price, J.P. Casazza, A.A. Pathan, C.R. Sander, T.E. Asher, D.R. Ambrozak, M.L. Precopio, P. Scheinberg, N.C. Alder, M. Roederer, R.A. Koup, D.C. Douek, A.V. Hill, and H. McShane Immunisation with BCG and recombinant MVA85A induces long-lasting, polyfunctional Mycobacterium tuberculosis-specific CD4+ memory T lymphocyte populations Eur J Immunol 37 2007 3089 3100
36. D. Ciuffreda, D. Comte, M. Cavassini, E. Giostra, L. Buhler, M. Perruchoud, M.H. Heim, M. Battegay, D. Genne, B. Mulhaupt, R. Malinverni, C. Oneta, E. Bernasconi, M. Monnat, A. Cerny, C. Chuard, J. Borovicka, G. Mentha, M. Pascual, J.J. Gonvers, G. Pantaleo, and V. Dutoit Polyfunctional HCV-specific T-cell responses are associated with effective control of HCV replication Eur J Immunol 38 2008 2665 2677
37. J.M. Young, I.M. Adetifa, M.O. Ota, and J.S. Sutherland Expanded polyfunctional T cell response to mycobacterial antigens in TB disease and contraction post-treatment PLoS One 5 2010 e11237
38. J.S. Sutherland, I.M. Adetifa, P.C. Hill, R.A. Adegbola, and M.O. Ota Pattern and diversity of cytokine production differentiates between Mycobacterium tuberculosis infection and disease Eur J Immunol 39 2009 723 729
39. A. Harari, V. Rozot, F.B. Enders, M. Perreau, J.M. Stalder, L.P. Nicod, M. Cavassini, T. Calandra, C.L. Blanchet, K. Jaton, M. Faouzi, C.L. Day, W.A. Hanekom, P.A. Bart, and G. Pantaleo Dominant TNF-alpha+ Mycobacterium tuberculosis-specific CD4+ T cell responses discriminate between latent infection and active disease Nat Med 17 2011 372 376
40. C.L. Day, D.A. Abrahams, L. Lerumo, E. Janse van Rensburg, L. Stone, T. O'Rie, B. Pienaar, M. de Kock, G. Kaplan, H. Mahomed, K. Dheda, and W.A. Hanekom Functional capacity of Mycobacterium tuberculosis-specific T cell responses in humans is associated with mycobacterial load J Immunol 187 2011 2222 2232
41. R. Casey, D. Blumenkrantz, K. Millington, D. Montamat-Sicotte, O.M. Kon, M. Wickremasinghe, S. Bremang, M. Magtoto, S. Sridhar, D. Connell, and A. Lalvani Enumeration of functional T-cell subsets by fluorescence-immunospot defines signatures of pathogen burden in tuberculosis PLoS One 5 2010 e15619
42. E.K. Forbes, C. Sander, E.O. Ronan, H. McShane, A.V. Hill, P.C. Beverley, and E.Z. Tchilian 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 181 2008 4955 4964
43. H. del Corral, S.C. Paris, N.D. Marin, D.M. Marin, L. Lopez, H.M. Henao, T. Martinez, L. Villa, L.F. Barrera, B.L. Ortiz, M.E. Ramirez, C.J. Montes, M.C. Oquendo, L.M. Arango, F. Riano, C. Aguirre, A. Bustamante, J.T. Belisle, K. Dobos, G.I. Mejia, M.R. Giraldo, P.J. Brennan, J. Robledo, M.P. Arbelaez, C.A. Rojas, and L.F. Garcia IFNgamma response to Mycobacterium tuberculosis, risk of infection and disease in household contacts of tuberculosis patients in Colombia PLoS One 4 2009 e8257
44. N.D. Marin, S.C. Paris, V.M. Velez, C.A. Rojas, M. Rojas, and L.F. Garcia Regulatory T cell frequency and modulation of IFN-gamma and IL-17 in active and latent tuberculosis Tuberculosis (Edinb) 90 2010 252 261
45. N.D. Marin, S.C. Paris, M. Rojas, and L.F. Garcia Reduced frequency of memory T cells and increased Th17 responses in patients with active tuberculosis Clin Vaccine Immunol 2012
46. W.A. Hanekom, H.M. Dockrell, T.H. Ottenhoff, T.M. Doherty, H. Fletcher, H. McShane, F.F. Weichold, D.F. Hoft, S.K. Parida, and U.J. Fruth Immunological outcomes of new tuberculosis vaccine trials: WHO panel recommendations PLoS Med 5 2008 e145
47. C.B. Chee, T.M. Barkham, K.W. Khinmar, S.H. Gan, and Y.T. Wang Quantitative T-cell interferon-gamma responses to Mycobacterium tuberculosis-specific antigens in active and latent tuberculosis Eur J Clin Microbiol Infect Dis 28 2009 667 670
48. J.P. Janssens, P. Roux-Lombard, T. Perneger, M. Metzger, R. Vivien, and T. Rochat Quantitative scoring of an interferon-gamma assay for differentiating active from latent tuberculosis Eur Respir J 30 2007 722 728
49. Y.S. Cho, K.M. Dobos, J. Prenni, H. Yang, A. Hess, I. Rosenkrands, P. Andersen, S.W. Ryoo, G.H. Bai, M.J. Brennan, A. Izzo, H. Bielefeldt-Ohmann, and J.T. Belisle Deciphering the proteome of the in vivo diagnostic reagent "purified protein derivative" from Mycobacterium tuberculosis Proteomics 12 2012 979 991
50. C. Jafari, M. Ernst, B. Kalsdorf, U. Greinert, R. Diel, D. Kirsten, K. Marienfeld, A. Lalvani, and C. Lange Rapid diagnosis of smear-negative tuberculosis by bronchoalveolar lavage enzyme-linked immunospot Am J Respir Crit Care Med 174 2006 1048 1054
51. W.A. Hanekom, J. Hughes, M. Mavinkurve, M. Mendillo, M. Watkins, H. Gamieldien, S.J. Gelderbloem, M. Sidibana, N. Mansoor, V. Davids, R.A. Murray, A. Hawkridge, P.A. Haslett, S. Ress, G.D. Hussey, and G. Kaplan Novel application of a whole blood intracellular cytokine detection assay to quantitate specific T-cell frequency in field studies J Immunol Meth 291 2004 185 195
52. C.M. Rueda, N.D. Marin, L.F. Garcia, and M. Rojas Characterization of CD4 and CD8 T cells producing IFN-gamma in human latent and active tuberculosis Tuberculosis (Edinb) 90 2010 346 353
53. N. Caccamo, G. Guggino, S. Meraviglia, G. Gelsomino, P. Di Carlo, L. Titone, M. Bocchino, D. Galati, A. Matarese, J. Nouta, M.R. Klein, A. Salerno, A. Sanduzzi, F. Dieli, and T.H. Ottenhoff Analysis of Mycobacterium tuberculosis-specific CD8 T-cells in patients with active tuberculosis and in individuals with latent infection PLoS One 4 2009 e5528
54. S. Rahman, B. Gudetta, J. Fink, A. Granath, S. Ashenafi, A. Aseffa, M. Derbew, M. Svensson, J. Andersson, and S.G. Brighenti Compartmentalization of immune responses in human tuberculosis: few CD8+ effector T cells but elevated levels of FoxP3+ regulatory t cells in the granulomatous lesions Am J Pathol 174 2009 2211 2224
55. A.M. Cooper Editorial: be careful what you ask for: is the presence of IL-17 indicative of immunity? J Leukoc Biol 88 2010 221 223
56. M. Umemura, A. Yahagi, S. Hamada, M.D. Begum, H. Watanabe, K. Kawakami, T. Suda, K. Sudo, S. Nakae, Y. Iwakura, and G. Matsuzaki IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection J Immunol 178 2007 3786 3796
57. Q. Han, N. Bagheri, E.M. Bradshaw, D.A. Hafler, D.A. Lauffenburger, and J.C. Love Polyfunctional responses by human T cells result from sequential release of cytokines Proc Natl Acad Sci U S A 109 2012 1607 1612
58. E.M. Leyten, S.M. Arend, C. Prins, F.G. Cobelens, T.H. Ottenhoff, and J.T. van Dissel Discrepancy between Mycobacterium tuberculosis-specific gamma interferon release assays using short and prolonged in vitro incubation Clin Vaccine Immunol 14 2007 880 885
59. A. Cehovin, J.M. Cliff, P.C. Hill, R.H. Brookes, and H.M. Dockrell Extended culture enhances sensitivity of a gamma interferon assay for latent Mycobacterium tuberculosis infection Clin Vaccine Immunol 14 2007 796 798
60. O. Butera, T. Chiacchio, S. Carrara, R. Casetti, V. Vanini, S. Meraviglia, G. Guggino, F. Dieli, M. Vecchi, F.N. Lauria, A. Marruchella, P. Laurenti, M. Singh, N. Caccamo, E. Girardi, and D. Goletti New tools for detecting latent tuberculosis infection: evaluation of RD1-specific long-term response BMC Infect Dis 9 2009 182
61. K. Pfeffer Biological functions of tumor necrosis factor cytokines and their receptors Cytokine Growth Factor Rev 14 2003 185 191
62. J.L. Flynn, M.M. Goldstein, J. Chan, K.J. Triebold, K. Pfeffer, C.J. Lowenstein, R. Schreiber, T.W. Mak, and B.R. Bloom Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice Immunity 2 1995 561 572
63. L.G. Bekker, A.L. Moreira, A. Bergtold, S. Freeman, B. Ryffel, and G. Kaplan Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent Infect Immun 68 2000 6954 6961
64. M. Denis Killing of Mycobacterium tuberculosis within human monocytes: activation by cytokines and calcitriol Clin Exp Immunol 84 1991 200 206
65. F. Riano, L. Arroyo, S. Paris, M. Rojas, A.H. Friggen, K.E. van Meijgaarden, K.L. Franken, T.H. Ottenhoff, L.F. Garcia, and L.F. Barrera T cell responses to DosR and Rpf proteins in actively and latently infected individuals from Colombia Tuberculosis (Edinb) 92 2012 148 159
66. F.O. Sanchez, J.I. Rodriguez, G. Agudelo, and L.F. Garcia Immune responsiveness and lymphokine production in patients with tuberculosis and healthy controls Infect Immun 62 1994 5673 5678