Functional signatures of human CD4 and CD8 T cell responses to Mycobacterium tuberculosis

Frontiers in Immunology

Volumn 5, Issue APR, 2014, Pages

  Prezzemolo, Teresa ^a   Guggino, Giuliana ^a   La Manna, Marco Pio ^a   Di Liberto, Diana Di ^a   Dieli, Francesco ^a   Caccamo, Nadia ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Cytokines; Disease; Human memory T cells; Infection; M. tuberculosis

Indexed keywords

CD27 ANTIGEN; CD28 ANTIGEN; GAMMA INTERFERON; GRANZYME A; GRANZYME B; INTERLEUKIN 17; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PERFORIN; TUMOR NECROSIS FACTOR ALPHA;

AUTOPHAGY; BACTERIAL LOAD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INFECTION CONTROL; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; REVIEW;

EID: 84900853654     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00180     Document Type: Review

References (146)

1. WHO. Global Tuberculosis Report 2011. Geneva: WHO Press (2011). Available from: http://whqlibdoc.who.int/publications/2011/9789241564380_eng.pdf.
2. Raviglione M, Marais B, Floyd K, Lönnroth K, Getahun H, Migliori GB, et al. Scaling up interventions to achieve global tuberculosis control: progress and new developments. Lancet (2012) 379:1902-13. doi: 10.1016/S0140-6736(12)60727-2.
3. Whitworth HS, Scott M, Connell DW, Dongés B, Lalvani A. IGRAs-the gateway to T cell based TB diagnosis. Methods (2013) 15:52-62. doi:10.1016/j.ymeth.2012.12.012.
4. McNerney R, Maeurer M, Abubakar I, Marais B, McHugh TD, Ford N, et al. Tuberculosis diagnostics and biomarkers: needs, challenges, recent advances, and opportunities. J Infect Dis (2012) 15:S147-58. doi:10.1093/infdis/jir860.
5. Zumla A, Atun R, Maeurer M, Mwaba P, Ma Z, O'Grady J, et al. Viewpoint: scientific dogmas, paradoxes and mysteries of latent Mycobacterium tuberculosis infection. Trop Med Int Health (2011) 16:79-83. doi:10.1111/j.1365-3156.2010.02665.x.
6. Lillebaek T, Andersen AB, Dirksen A, Smith E, Skovgaard LT, Kok-Jensen A. Persistent high incidence of tuberculosis in immigrants in a low-incidence country. Emerg Infect Dis (2002) 8:679-84. doi:10.3201/eid0807.010482.
7. Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med (2001) 345:1098-104. doi:10.1056/NEJMoa011110.
8. National Collaborating Centre for Chronic Conditions (UK), Centre for Clinical Practice at NICE (UK). Tuberculosis: Clinical Diagnosis and Management of Tuberculosis, and Measures for Its Prevention and Control. London: National Institute for Health and Clinical Excellence (2011). Available from: http://www.nice.org.uk/nicemedia/live/13422/53642/53642.pdf.
9. Broekmans JF, Migliori GB, Rieder HL, Lees J, Ruutu P, Loddenkemper R, et al. European framework for tuberculosis control and elimination in countries with a low incidence. Recommendations of the World Health Organization (WHO), International Union Against Tuberculosis and Lung Disease (IUATLD) and Royal Netherlands Tuberculosis Association (KNCV) Working Group. Eur Respir J (2002) 19:765-75.
10. Pareek M, Abubakar I, White PJ, Garnett GP, Lalvani A. Tuberculosis screening of migrants to low-burden nations: insights from evaluation of UK practice. Eur Respir J (2011) 37:1175-82. doi:10.1183/09031936.00105810.
11. Abubakar I, Lipman M, Anderson C, Davies P, Zumla A. Tuberculosis in the UK-time to regain control. BMJ (2011) 343:d4281. doi:10.1136/bmj.d4281.
12. Parida SK, Kaufmann SH. The quest for biomarkers in tuberculosis. Drug Discov Today (2010) 15:148-57. doi:10.1016/j.drudis.2009.10.005.
13. Mittrücker HW, Steinhoff U, Köhler A, Krause M, Lazar D, Mex P, et al. Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. Proc Natl Acad Sci U S A (2007) 104:12434-9. doi:10.1073/pnas.0703510104.
14. Kaufmann SH. Tuberculosis vaccines: time to think about the next generation. Semin Immunol (2013) 25:172-81. doi:10.1016/j.smim.2013.04.006.
15. + T cells inactive disease. Eur J Immunol (2013) 43:939-48. doi:10.1002/eji.201243090.
16. Ottenhoff TH. New pathways of protective and pathological host defense to mycobacteria. Trends Microbiol (2012) 20:419-28. doi:10.1016/j.tim.2012.06.002.
17. Jurado JO, Pasquinelli V, Alvarez IB, Peña D, Rovetta AI, Tateosian NL, et al. IL-17 and IFN-γ expression in lymphocytes from patients with active tuberculosis correlates with the severity of the disease. J Leukoc Biol (2012) 91:991-1002. doi:10.1189/jlb.1211619.
18. Auffray C, Sieweke MH, Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol (2009) 27:669-92. doi:10.1146/annurev.immunol.021908.132557.
19. Chowdhury D, Lieberman J. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu Rev Immunol (2008) 26:389-420. doi:10.1146/annurev.immunol.26.021607.090404.
20. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol (2006) 6:173-82. doi:10.1038/nri1785.
21. Dorhoi A, Reece ST, Kaufmann SHE. Fundamental immunology. 7th ed. In: Paul WE editor. Immunity to Intracellular Bacteria. Philadelphia: Wolters KluwerHealth, Lippincott Williams & Wilkins (2012). p. 973-1000.
22. Harding CV, Boom WH. Regulation of antigen presentation by Mycobacterium tuberculosis: a role for Toll-like receptors. Nat Rev Microbiol (2010) 8:296-307. doi:10.1038/nrmicro2321.
23. Kaufmann SHE. Fundamental immunology. 5th ed. In: Paul WE editor. Immunityto Intracellular Bacteria. Philadelphia, NY: Lippincott-Raven (2003). p. 1229-61.
24. Cooper AM. Cell-mediated immune responses in tuberculosis. Annu Rev Immunol (2009) 27:393-422. doi:10.1146/annurev.immunol.021908.132703.
25. Stenger S, Hanson DA, Teitelbaum R, Dewan P, Niazi KR, Froelich CJ, et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science (1998) 282:121-5. doi:10.1126/science.282.5386.121.
26. Van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell (2007) 129:1287-98. doi:10.1016/j.cell.2007.05.059.
27. Schaible UE, Winau F, Sieling PA, Fischer K, Collins HL, Hagens K, et al. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med (2003) 9:1039-46. doi:10.1038/nm906.
28. Winau F, Weber S, Sad S, de Diego J, Hoops SL, Breiden B, et al. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity (2006) 24:105-17. doi:10.1016/j.immuni.2005.12.001.
29. Lin MY, Ottenhoff TH. Host-pathogen interactions in latent Mycobacterium tuberculosis infection: identification of new targets for tuberculosis intervention. Endocr Metab Immune Disord Drug Targets (2008) 8:15-29. doi:10.2174/187153008783928398.
30. Mosmann TR, Coffman RL. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol (1989) 7:145-73. doi:10.1146/annurev.iy.07.040189.001045.
31. Romagnani S. "Immunology. 10th ed. In: Kaufmann SHE, Steward MW editors. Cytokines. London: Hodder Arnold/ASM Press (2005). p. 273-99.
32. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol (2008) 26:677-704. doi:10.1146/annurev.immunol.26.021607.090331.
33. De Libero G, Mori L. Recognition of lipid antigens by T cells. Nat Rev Immunol (2005) 5:485-96. doi:10.1038/nri1631.
34. Gold MC, Cerri S, Smyk-Pearson S, Cansler ME, Vogt TM, Delepine J, et al. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol (2010) 8:e1000407. doi:10.1371/journal.pbio.1000407.
35. Scotet E, Nedellec S, Devilder MC, Allain S, Bonneville M. Bridging innate and adaptive immunity through gammadelta T-dendritic cell crosstalk. Front Biosci (2008) 13:6872-85. doi:10.2741/3195.
36. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med (2007) 13:843-50. doi:10.1038/nm1592.
37. Derrick SC, Yabe IM, Yang A, Morris SL. Vaccine-induced anti-tuberculosis protective immunity in mice correlates with the magnitude and quality of multifunctional CD4 T cells. Vaccine (2011) 29:2902-9. doi:10.1016/j.vaccine.2011.02.010.
38. Joosten SA, Ottenhoff TH. Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination. Hum Immunol (2008) 69:760-70. doi:10.1016/j.humimm.2008.07.017.
39. Urdahl KB, Shafiani S, Ernst JD. Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol (2011) 4:288-93. doi:10.1038/mi.2011.10.
40. Caccamo N, Dieli F. Are Polyfunctional Cells Protective in M. tuberculosis Infection? Understanding Tuberculosis-Analyzing the Origin of Mycobacterium tuberculosis Pathogenicity. Available from: http://www.intechopen.com/books/understanding-tuberculosis-analyzing-the-origin-of-mycobacterium-tuberculosis-pathogenicity/are-polyfunctional-cells-protective-in-m-tuberculosis-infection.
41. Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature (1999) 401:708-12. doi:10.1038/44385.
42. Lanzavecchia A, Sallusto F. Understanding the generation and function of memory T cell subsets. Curr Opin Immunol (2005) 17:326-32. doi:10.1016/j.coi.2005.04.010.
43. Zanetti M, Franchini G. T cell memory and protective immunity by vaccination: is more better? Trends Immunol (2006) 27:511-7. doi:10.1016/j.it.2006.09.004.
44. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E. The who's who of T-cell differentiation: human memory T-cell subsets. Eur J Immunol (2013) 43:2797-809. doi:10.1002/eji.201343751.
45. Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science (1996) 272:60-6. doi:10.1126/science.272.5258.60.
46. Sallusto F, Mackay CR, Lanzavecchia A. The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol (2000) 18:593-620. doi:10.1146/annurev.immunol.18.1.593.
47. Appay V, van Lier RA, Sallusto F, Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A (2008) 73:975-83. doi:10.1002/cyto.a.20643.
48. Picker LJ, Treer JR, Ferguson-Darnell B, Collins PA, Buck D, Terstappen LW. Control of lymphocyte recirculation in man. I. Differential regulation of the peripheral lymph node homing receptor L-selectin on T cells during the virgin to memory cell transition. J Immunol (1993) 150:1105-21.
49. Picker LJ, Treer JR, Ferguson-Darnell B, Collins PA, Bergstresser PR, Terstappen LW. Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyte-associated antigen, a tissue-selective homing receptor for skin-homing T cells. J Immunol (1993) 150:1122-36.
50. Picker LJ, Singh MK, Zdraveski Z, Treer JR, Waldrop SL, Bergstresser PR, et al. Direct demonstration of cytokine synthesis heterogeneity among human memory/effector T cells by flow cytometry. Blood (1995) 86:1408-19.
51. Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, et al. A human memory T cell subset with stem cell-like properties. Nat Med (2011) 17:1290-7. doi:10.1038/nm.2446.
52. Lugli E, Dominguez MH, Gattinoni L, Chattopadhyay PK, Bolton DL, Song K, et al. Superior T memory stem cell persistence supports long-lived T cell memory. J Clin Invest (2013) 123:594-9. doi:10.1172/JCI66327.
53. +) T cells provides new insights on immunodeficiency in aging. Blood (2000) 95:2860-8.
54. Lugli E, Pinti M, Nasi M, Troiano L, Ferraresi R, Mussi C, et al. Subject classification obtained by cluster analysis and principal component analysis applied to flow cytometric data. Cytometry A (2007) 71:334-44. doi:10.1002/cyto.a.20387.
55. Fritsch RD, Shen X, Sims GP, Hathcock KS, Hodes RJ, Lipsky PE. Stepwise differentiation of CD4 memory T cells defined by expression of CCR7 and CD27. J Immunol (2005) 175:6489-97.
56. + T cell subsets and their differentiation. Int Immunol (2008) 20:1189-99. doi:10.1093/intimm/dxn075.
57. Picker LJ, Reed-Inderbitzin EF, Hagen SI, Edgar JB, Hansen SG, Legasse A, et al. IL-15 induces CD4 effector memory T cell production and tissue emigration in nonhuman primates. J Clin Invest (2006) 116:1514-24. doi:10.1172/JCI27564.
58. Lugli E, Goldman CK, Perera LP, Smedley J, Pung R, Yovandich JL, et al. Transient and persistent effects of IL-15 on lymphocyte homeostasis in nonhuman primates. Blood (2010) 116:3238-48. doi:10.1182/blood-2010-03-275438.
59. Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol (2008) 8:247-58. doi:10.1038/nri2274.
60. Bird JJ, Brown DR, Mullen AC, Moskowitz NH, Mahowald MA, Sider JR, et al. Helper T cell differentiation is controlled by the cell cycle. Immunity (1998) 9:229-37. doi:10.1016/S1074-7613(00)80605-6.
61. + T lymphocytes. J Immunol (2007) 178:4112-9.
62. + T cells differently expressing three cytolytic effector molecules. J Immunol (2006) 177:4330-40.
63. Chattopadhyay PK, Betts MR, Price DA, Gostick E, Horton H, Roederer M, et al. The cytolytic enzymes granyzme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression. J Leukoc Biol (2009) 85:88-97. doi:10.1189/jlb.0208107.
64. + T cells reflecting their function: inverse correlation between quantitative expression of CD27 and cytotoxic effector function. Eur J Immunol (2004) 34:999-1010. doi:10.1002/eji.200324478.
65. Harari A, Petitpierre S, Vallelian F, Pantaleo G. Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood (2004) 103:966-72. doi:10.1182/blood-2003-04-1203.
66. + T cells endowed with proliferative capacity. J Exp Med (2003) 198:1909-22. doi:10.1084/jem.20031598.
67. + T helper cells in chronic HCV infection. Hepatology (2005) 41:1019-28. doi:10.1002/hep.20669.
68. 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. doi:10.1111/j.1600-065X.2010.01000.x.
69. Millington KA, Innes JA, Hackforth S, Hinks TS, Deeks JJ, Dosanjh DP, et al. Dynamic relationship between IFN-gamma and IL-2 profile of Mycobacterium tuberculosis-specific T cells and antigen load. J Immunol (2007) 178:5217-26.
70. Unutmaz D, Pileri P, Abrignani S. Antigen-independent activation of naive and memory resting T cells by a cytokine combination. J Exp Med (1994) 180:1159-64. doi:10.1084/jem.180.3.1159.
71. + memory T-cell subsets in response to antigen or homeostatic cytokines. Blood (2003) 101:4260-6. doi:10.1182/blood-2002-11-3577.
72. +) T cells. J Exp Med (2001) 194:1711-9. doi:10.1084/jem.194.12.1711.
73. Walzl G, Ronacher K, Hanekom W, Scriba TJ, Zumla A. Immunological biomarkers of tuberculosis. Nat Rev Immunol (2011) 11:343-54. doi:10.1038/nri2960.
74. + T cells are functionally and phenotypically different between latent infection and active disease. Eur J Immunol (2013) 43:1568-77. doi:10.1002/eji.201243262.
75. + T cells in latently infected individuals and patients with active TB. Tuberculosis (Edinb) (2013) 93:155-66. doi:10.1016/j.tube.2012.12.002.
76. Flynn JL, Chan J. Tuberculosis: latency and reactivation. Infect Immun (2001) 69:4195-201. doi:10.1128/IAI.69.7.4195-4201.2001.
77. + T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med (2007) 204:2473-85. doi:10.1084/jem.20070784.
78. + T cells. Eur J Immunol (2010) 40:279-90. doi:10.1002/eji.200939754.
79. + T cells in adults. Am J Respir Crit Care Med (2010) 181:1407-17. doi:10.1164/rccm.200910-1484OC.
80. Soares AP, Scriba TJ, Joseph S, Harbacheuski R, Murray RA, Gelderbloem SJ, et al. Bacillus Calmette-Guérin vaccination of human newborns induces T cells with complex cytokine and phenotypic profiles. J Immunol (2008) 180:3569-77.
81. + memory T lymphocyte populations. Eur J Immunol (2007) 37:3089-100. doi:10.1002/eji.200737504.
82. Petruccioli E, Petrone L, Vanini V, Sampaolesi A, Gualano G, Girardi E, et al. γ/TNFα specific-cells and effector memory phenotype associate with active tuberculosis. J Infect (2013) 66:475-86. doi:10.1016/j.jinf.2013.02.004.
83. Ciuffreda D, Comte D, Cavassini M, Giostra E, Bühler L, Perruchoud M, et al. Polyfunctional HCV-specific T-cell responses are associated with effective control of HCV replication. Eur J Immunol (2008) 38:2665-77. doi:10.1002/eji.200838336.
84. Chiacchio T, Petruccioli E, Vanini V, Butera O, Cuzzi G, Petrone L, et al. Higher frequency of T-cell response to M. tuberculosis latency antigen Rv2628 at the site of active tuberculosis disease than in peripheral blood. PLoS One (2011) 6:e27539. doi:10.1371/journal.pone.0027539.
85. + T cells at sites of pleural TB. Tuberculosis (Edinb) (2011) 91:224-30. doi:10.1016/j.tube.2010.12.005.
86. Sargentini V, Mariotti S, Carrara S, Gagliardi MC, Teloni R, Goletti D, et al. Cytometric detection of antigen-specific IFN-gamma/IL-2 secreting cells in the diagnosis of tuberculosis. BMC Infect Dis (2009) 9:99. doi:10.1186/1471-2334-9-99.
87. Caccamo N, Guggino G, Meraviglia S, Gelsomino G, Di Carlo P, Titone L, et al. Analysis of Mycobacterium tuberculosis-specific CD8 T-cells in patients with active tuberculosis and in individuals with latent infection. PLoS One (2009) 4:e5528. doi:10.1371/journal.pone.0005528.
88. Sester U, Fousse M, Dirks J, Mack U, Prasse A, Singh M, et al. Whole-blood flow-cytometric analysis of antigen-specific CD4 T-cell cytokine profiles distinguishes active tuberculosis from non-active states. PLoS One (2011) 6:e17813. doi:10.1371/journal.pone.0017813.
89. Young JM, Adetifa IM, Ota MO, Sutherland JS. Expanded polyfunctional T cell response to mycobacterial antigens in TB disease and contraction post-treatment. PLoS One (2010) 5:e11237. doi:10.1371/journal.pone.0011237.
90. 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. doi:10.1002/eji.200838693.
91. +) T cells correlate with active Mycobacterium tuberculosis infection. Eur J Immunol (2010) 40:2211-20. doi:10.1002/eji.201040455.
92. + T cell responses discriminate between latent infection and active disease. Nat Med (2011) 17:372-6. doi:10.1038/nm.2299.
93. Day CL, Abrahams DA, Lerumo L, Janse van Rensburg E, Stone L, O'Rie T, et al. Functional capacity of Mycobacterium tuberculosis-specific T cell responses in humans is associated with mycobacterial load. J Immunol (2011) 187:2222-32. doi:10.4049/jimmunol.1101122.
94. + multifunctional memory T cells coexpress GM-CSF. Cytokine (2008) 43:143-8. doi:10.1016/j.cyto.2008.05.002.
95. Casey R, Blumenkrantz D, Millington K, Montamat-Sicotte D, Kon OM, Wickremasinghe M, et al. Enumeration of functional T-cell subsets by fluorescence-immunospot defines signatures of pathogen burden in tuberculosis. PLoS One (2010) 5:e15619. doi:10.1371/journal.pone.0015619.
96. +) memory T cell subsets with outcome of pulmonary tuberculosis. J Infect (2010) 60:133-9. doi:10.1016/j.jinf.2009.10.048.
97. Schuetz A, Haule A, Reither K, Ngwenyama N, Rachow A, Meyerhans A, et al. Monitoring CD27 expression to evaluate Mycobacterium tuberculosis activity in HIV-1 infected individuals in vivo. PLoS One (2011) 6:e27284. doi:10.1371/journal.pone.0027284.
98. Pollock KM, Whitworth HS, Montamat-Sicotte DJ, Grass L, Cooke GS, Kapembwa MS, et al. T-cell immunophenotyping distinguishes active from latent tuberculosis. J Infect Dis (2013) 208:952-68. doi:10.1093/infdis/jit265.
99. + T lymphocytes specific for Mycobacterium tuberculosis. Proc Natl Acad Sci U S A (1998) 95:270-5. doi:10.1073/pnas.95.1.270.
100. Ladel CH, Daugelat S, Kaufmann SH. Immune response to Mycobacterium bovis bacille Calmette Guérin 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. doi:10.1002/eji.1830250211.
101. Ottenhoff TH, Lewinsohn DA, Lewinsohn DM. Human CD4 and CD8 T cell responses to Mycobacterium tuberculosis: antigen specificity, function, implications and applications. In: Handbook of Tuberculosis: Immunology and Cell Biology. Weinheim: Wiley-VCH (2008). p. 119-56.
102. + cytolytic T cells in human tuberculosis and HIV infection. Biochem Biophys Res Commun (2010) 396:50-7. doi:10.1016/j.bbrc.2010.02.141.
103. Chen CY, Huang D, Wang RC, Shen L, Zeng G, Yao S, et al. A critical role for CD8 T cells in a nonhuman primate model of tuberculosis. PLoS Pathog (2009) 5:e1000392. doi:10.1371/journal.ppat.1000392.
104. Mazzaccaro RJ, Stenger S, Rock KL, Porcelli SA, Brenner MB, Modlin RL, et al. Cytotoxic T lymphocytes in resistance to tuberculosis. Adv Exp Med Biol (1998) 452:85-101. doi:10.1007/978-1-4615-5355-7_11.
105. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature (2011) 469:323-35. doi:10.1038/nature09782.
106. Deretic V. Autophagy in infection. Curr Opin Cell Biol (2010) 22:252-62. doi:10.1016/j.ceb.2009.12.009.
107. Joosten SA, van Meijgaarden KE, van Weeren PC, Kazi F, Geluk A, Savage ND, et al. Mycobacterium tuberculosis peptides presented by HLA-E molecules are targets for human CD8 T-cells with cytotoxic as well as regulatory activity. PLoS Pathog (2010) 6:e1000782. doi:10.1371/journal.ppat.1000782.
108. + T cells. J Exp Med (2002) 196:1473-81. doi:10.1084/jem.20020609.
109. Cohen NR, Garg S, Brenner MB. Antigen presentation by CD1 lipids, T cells, and NKT cells in microbial immunity. Adv Immunol (2009) 102:1-94. doi:10.1016/S0065-2776(09)01201-2.
110. + T cell-mediated antimicrobial activity against Mycobacterium tuberculosis in humans. J Clin Invest (2009) 119:1167-77. doi:10.1172/JCI38482.
111. Stenger S, Mazzaccaro RJ, Uyemura K, Cho S, Barnes PF, Rosat JP, et al. Differential effects of cytolytic T cell subsets on intracellular infection. Science (1997) 276:1684-7. doi:10.1126/science.276.5319.1684.
112. Semple PL, Watkins M, Davids V, Krensky AM, Hanekom WA, Kaplan G, et al. Induction of granulysin and perforin cytolytic mediator expression in 10-week-old infants vaccinated with BCG at birth. Clin Dev Immunol (2011) 2011:438463. doi:10.1155/2011/438463.
113. + effector T cells but elevated levels of FoxP3+ regulatory t cells in the granulomatous lesions. Am J Pathol (2009) 174:2211-24. doi:10.2353/ajpath.2009.080941.
114. + T cells at the site of infection in human chronic pulmonary tuberculosis. Infect Immun (2007) 75:5210-22. doi:10.1128/IAI.00624-07.
115. Kagina BM, Abel B, Scriba TJ, Hughes EJ, Keyser A, Soares A, et al. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after Bacillus Calmette-Guérin vaccination of newborns. Am J Respir Crit Care Med (2010) 182:1073-9. doi:10.1164/rccm.201003-0334OC.
116. Smith SG, Lalor MK, Gorak-Stolinska P, Blitz R, Beveridge NE, Worth A, et al. Mycobacterium tuberculosis PPD-induced immune biomarkers measurable in vitro following BCG vaccination of UK adolescents by multiplex bead array and intracellular cytokine staining. BMC Immunol (2010) 11:35. doi:10.1186/1471-2172-11-35.
117. Caccamo N, Meraviglia S, La Mendola C, Guggino G, Dieli F, Salerno A. Phenotypical and functional analysis of memory and effector human CD8 T cells specific for mycobacterial antigens. J Immunol (2006) 177:1780-5.
118. Leyten EM, Lin MY, Franken KL, Friggen AH, Prins C, van Meijgaarden KE, et al. Human T-cell responses to 25 novel antigens encoded by genes of the dormancy regulon of Mycobacterium tuberculosis. Microbes Infect (2006) 8:2052-60. doi:10.1016/j.micinf.2006.03.018.
119. Roupie V, Romano M, Zhang L, Korf H, Lin MY, Franken KL, et al. Immunogenicity of eight dormancy regulon-encoded proteins of Mycobacterium tuberculosis in DNA-vaccinated and tuberculosis-infected mice. Infect Immun (2007) 75:941-9. doi:10.1128/IAI.01137-06.
120. Schuck SD, Mueller H, Kunitz F, Neher A, Hoffmann H, Franken KL, et al. Identification of T-cell antigens specific for latent mycobacterium tuberculosis infection. PLoS One (2009) 4:e5590. doi:10.1371/journal.pone.0005590.
121. Flynn JL, Goldstein MM, Triebold KJ, Koller B, Bloom BR. Major histocompatibility complex class I-restricted T cells are required for resistance to Mycobacterium tuberculosis infection. Proc Natl Acad Sci U S A (1992) 89:12013-7. doi:10.1073/pnas.89.24.12013.
122. + T-cell responses to Mycobacterium tuberculosis DosR antigens and peptides in long-term latently infected individuals. Eur J Immunol (2011) 41:2925-36. doi:10.1002/eji.201141602.
123. +) T cells rapidly decline with antituberculosis treatment. PLoS One (2013) 8:e81564. doi:10.1371/journal.pone.0081564.
124. Kunnath-Velayudhan S, Davidow AL, Wang HY, Molina DM, Huynh VT, Salamon H, et al. Proteome-scale antibody responses and outcome of Mycobacterium tuberculosis infection in nonhuman primates and in tuberculosis patients. J Infect Dis (2012) 206:697-705. doi:10.1093/infdis/jis421.
125. Harari A, Dutoit V, Cellerai C, Bart PA, Du Pasquier RA, Pantaleo G. Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol Rev (2006) 211:236-54. doi:10.1111/j.0105-2896.2006.00395.x.
126. + T cells preferentially recognize heavily infected cells. Am J Respir Crit Care Med (2003) 168:1346-52. doi:10.1164/rccm.200306-837OC.
127. + T cells provide an immunologic signature of tuberculosis in young children. Am J Respir Crit Care Med (2012) 185:206-12. doi:10.1164/rccm.201107-1355OC.
128. Flynn Diedrich CR, Flynn JL. HIV-1/Mycobacterium tuberculosis coinfection immunology: how does HIV-1 exacerbate tuberculosis? Infect Immun (2011) 79:1407-17. doi:10.1128/IAI.01126-10.
129. Nambuya A, Sewankambo N, Mugerwa J, Goodgame R, Lucas S. Tuberculous lymphadenitis associated with human immunodeficiency virus (HIV) in Uganda. J Clin Pathol (1988) 41:93-6. doi:10.1136/jcp.41.1.93.
130. Pitchenik AE, Burr J, Suarez M, Fertel D, Gonzalez G, Moas C. Human T-cell lymphotropic virus-III (HTLV-III) seropositivity and related disease among 71 consecutive patients in whom tuberculosis was diagnosed. A prospective study. Am Rev Respir Dis (1987) 135:875-9.
131. Selwyn PA, Sckell BM, Alcabes P, Friedland GH, Klein RS, Schoenbaum EE. High risk of active tuberculosis in HIV-infected drug users with cutaneous anergy. JAMA (1992) 268:504-9. doi:10.1001/jama.1992.03490040080029.
132. Lawn SD, Butera ST, Shinnick TM. Tuberculosis unleashed: the impact of human immunodeficiency virus infection on the host granulomatous response to Mycobacterium tuberculosis. Microbes Infect (2002) 4:635-46. doi:10.1016/S1286-4579(02)01582-4.
133. WHO Publications, Guidelines, Reports on HIV/AIDS Available from: http://www.who.int/publications/en/.
134. Geldmacher C, Zumla A, Hoelscher M. Interaction between HIV and Mycobacterium tuberculosis: HIV-1-induced CD4 T-cell depletion and the development of active tuberculosis. Curr Opin HIV AIDS (2012) 7:268-75. doi:10.1097/COH.0b013e3283524e32.
135. Sonnenberg P, Glynn JR, Fielding K, Murray J, Godfrey-Faussett P, Shearer S. How soon after infection with HIV does the risk of tuberculosis start to increase? A retrospective cohort study in South African gold miners. J Infect Dis (2005) 191:150-8. doi:10.1086/426827.
136. Sonnenberg P, Murray J, Glynn JR, Shearer S, Kambashi B, Godfrey-Faussett P. HIV-1 and recurrence, relapse, and reinfection of tuberculosis after cure: a cohort study in South African mineworkers. Lancet (2001) 358:1687-93. doi:10.1016/S0140-6736(01)06712-5.
137. Lawn SD, Myer L, Edwards D, Bekker LG, Wood R. Short-term and long-term risk of tuberculosis associated with CD4 cell recovery during antiretroviral therapy in South Africa. AIDS (2009) 23:1717-25. doi:10.1097/QAD.0b013e32832d3b6d.
138. Kizza HM, Rodriguez B, Quinones-Mateu M, Mirza M, Aung H, Yen-Lieberman B, et al. Persistent replication of human immunodeficiency virus type 1 despite treatment of pulmonary tuberculosis in dually infected subjects. Clin Diagn Lab Immunol (2005) 12:1298-304.
139. Geldmacher C, Schuetz A, Ngwenyama N, Casazza JP, Sanga E, Saathoff E, et al. Early depletion of Mycobacterium tuberculosis specific T helper 1 cell responses after HIV-1 infection. J Infect Dis (2008) 198:1590-8. doi:10.1086/593017.
140. Kalsdorf B, Scriba TJ, Wood K, Day CL, Dheda K, Dawson R, et al. HIV-1 infection impairs the bronchoalveolar T-cell response to mycobacteria. Am J Respir Crit Care Med (2009) 180:1262-70. doi:10.1164/rccm.200907-1011OC.
141. Mansoor N, Scriba TJ, de Kock M, Tameris M, Abel B, Keyser A, et al. HIV-1 infection in infants severely impairs the immune response induced by Bacille Calmette-Guerin vaccine. J Infect Dis (2009) 199:982-90. doi:10.1086/597304.
142. Rangaka MX, Diwakar L, Seldon R, van Cutsem G, Meintjes GA, Morroni C, et al. Clinical, immunological, and epidemiological importance of antituberculosis T cell responses in HIV-infected Africans. Clin Infect Dis (2007) 44:1639-46. doi:10.1086/518234.
143. + memory T-cell phenotype at the site of disease in extrapulmonary tuberculosis. Eur J Immunol (2012) 42:147-57. doi:10.1002/eji.201141927.
144. Wilkinson KA, Seldon R, Meintjes G, Rangaka MX, Hanekom WA, Maartens G, et al. Dissection of regenerating T-cell responses against tuberculosis in HIV-infected adults sensitized by Mycobacterium tuberculosis. Am J Respir Crit Care Med (2009) 180:674-83. doi:10.1164/rccm.200904-0568OC.
145. Day CL, Mkhwanazi N, Reddy S, Mncube Z, van der Stok M, Klenerman P, et al. Detection of polyfunctional Mycobacterium tuberculosis-specific T cells and association with viral load in HIV-1-infected persons. J Infect Dis (2008) 197:990-9. doi:10.1086/529048.
146. Weiner J, Maertzdorf J, Kaufmann SH. The dual role of biomarkers for understanding basic principles and devising novel intervention strategies in tuberculosis. Ann N Y Acad Sci (2013) 1283:22-9. doi:10.1111/j.1749-6632.2012.06802.x.