Inflammation in tuberculosis: Interactions, imbalances and interventions

Current Opinion in Immunology

Volumn 25, Issue 4, 2013, Pages 441-449

  Kaufmann, Stefan H E ^a   Dorhoi, Anca ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CATHEPSIN; CYTOKINE; ICOSANOID; INTERFERON; INTERLEUKIN 1; MATRIX METALLOPROTEINASE; MICRORNA; MYCOBACTERIUM VACCINE; SERINE PROTEINASE INHIBITOR; TUMOR NECROSIS FACTOR;

ADAPTIVE IMMUNITY; BACTERIAL SURVIVAL; CELL DEATH; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG SAFETY; GRANULOMA; HOST PATHOGEN INTERACTION; HUMAN; INFLAMMATION; METABOLIC REGULATION; MOLECULAR INTERACTION; NONHUMAN; PATHOGENESIS; PERSONALIZED MEDICINE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); REVIEW; SIGNAL TRANSDUCTION; TISSUE REPAIR; TUBERCULOSIS; TUBERCULOSIS CONTROL;

ANIMALS; CELL DEATH; HUMANS; INFLAMMATION; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 84884169017     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.05.005     Document Type: Review

References (80)

1. Nathan C. Points of control in inflammation. Nature 2002, 420:846-852.
2. Medzhitov R. Origin and physiological roles of inflammation. Nature 2008, 454:428-435.
3. Lamkanfi M., Dixit V.M. Inflammasomes and their roles in health and disease. Annu Rev Cell Dev Biol 2012, 28:137-161.
4. Nathan C., Ding A. Nonresolving inflammation. Cell 2010, 140:871-882.
5. Kang D.D., Lin Y., Moreno J.R., Randall T.D., Khader S.A. Profiling early lung immune responses in the mouse model of tuberculosis. PLoS ONE 2011, 6:e16161.
6. O'Kane C.M., Boyle J.J., Horncastle D.E., Elkington P.T., Friedland J.S. Monocyte-dependent fibroblast CXCL8 secretion occurs in tuberculosis and limits survival of mycobacteria within macrophages. J Immunol 2007, 178:3767-3776.
7. Lin Y., Zhang M., Barnes P.F. Chemokine production by a human alveolar epithelial cell line in response to Mycobacterium tuberculosis. Infect Immun 1998, 66:1121-1126.
8. Slight S.R., Rangel-Moreno J., Gopal R., Lin Y., Fallert Junecko B.A., Mehra S., Selman M., Becerril-Villanueva E., Baquera-Heredia J., Pavon L., Kaushal D., Reinhart T.A., Randall T.D., Khader S.A. CXCR5(+) T helper cells mediate protective immunity against tuberculosis. J Clin Invest 2013, 123:712-726.
9. Dinarello C.A. IL-1: discoveries, controversies and future directions. Eur J Immunol 2010, 40:599-606.
10. Fremond C.M., Togbe D., Doz E., Rose S., Vasseur V., Maillet I., Jacobs M., Ryffel B., Quesniaux V.F. IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol 2007, 179:1178-1189.
11. Yamada H., Mizumo S., Horai R., Iwakura Y., Sugawara I. Protective role of interleukin-1 in mycobacterial infection in IL-1 alpha/beta double-knockout mice. Lab Invest 2000, 80:759-767.
12. Sugawara I., Yamada H., Hua S., Mizuno S. Role of interleukin (IL)-1 type 1 receptor in mycobacterial infection. Microbiol Immunol 2001, 45:743-750.
13. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002, 10:417-426.
14. Schroder K., Tschopp J. The inflammasomes. Cell 2010, 140:821-832.
15. Mishra B.B., Moura-Alves P., Sonawane A., Hacohen N., Griffiths G., Moita L.F., Anes E. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell Microbiol 2010, 12:1046-1063.
16. Koo I.C., Wang C., Raghavan S., Morisaki J.H., Cox J.S., Brown E.J. ESX-1-dependent cytolysis in lysosome secretion and inflammasome activation during mycobacterial infection. Cell Microbiol 2008, 10:1866-1878.
17. Saiga H., Kitada S., Shimada Y., Kamiyama N., Okuyama M., Makino M., Yamamoto M., Takeda K. Critical role of AIM2 in Mycobacterium tuberculosis infection. Int Immunol 2012, 24:637-644.
18. Walter K., Holscher C., Tschopp J., Ehlers S. NALP3 is not necessary for early protection against experimental tuberculosis. Immunobiology 2010, 215:804-811.
19. Dorhoi A., Nouailles G., Jorg S., Hagens K., Heinemann E., Pradl L., Oberbeck-Muller D., Duque-Correa M.A., Reece S.T., Ruland J., Brosch R., Tschopp J., Gross O., Kaufmann S.H. Activation of the NLRP3 inflammasome by Mycobacterium tuberculosis is uncoupled from susceptibility to active tuberculosis. Eur J Immunol 2012, 42:374-384.
20. McElvania T.E., Allen I.C., Hulseberg P.D., Sullivan J.T., McCann J.R., Sandor M., Braunstein M., Ting J.P. Granuloma formation and host defense in chronic Mycobacterium tuberculosis infection requires PYCARD/ASC but not NLRP3 or caspase-1. PLoS ONE 2010, 5:e12320.
21. Mayer-Barber K.D., Barber D.L., Shenderov K., White S.D., Wilson M.S., Cheever A., Kugler D., Hieny S., Caspar P., Nunez G., Schlueter D., Flavell R.A., Sutterwala F.S., Sher A. Caspase-1 independent IL-1beta production is critical for host resistance to Mycobacterium tuberculosis and does not require TLR signaling in vivo. J Immunol 2010, 184:3326-3330.
22. Mayer-Barber K.D., Andrade B.B., Barber D.L., Hieny S., Feng C.G., Caspar P., Oland S., Gordon S., Sher A. Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 2011, 35:1023-1034.
23. Abdalla H., Srinivasan L., Shah S., Mayer-Barber K.D., Sher A., Sutterwala F.S., Briken V. Mycobacterium tuberculosis infection of dendritic cells leads to partially caspase-1/11-independent IL-1beta and IL-18 secretion but not to pyroptosis. PLoS ONE 2012, 7:e40722.
24. Mishra B.B., Rathinam V.A., Martens G.W., Martinot A.J., Kornfeld H., Fitzgerald K.A., Sassetti C.M. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1beta. Nat Immunol 2013, 14:52-60.
25. Liu P.T., Modlin R.L. Human macrophage host defense against Mycobacterium tuberculosis. Curr Opin Immunol 2008, 20:371-376.
26. Shenoy A.R., Wellington D.A., Kumar P., Kassa H., Booth C.J., Cresswell P., MacMicking J.D. GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science 2012, 336:481-485.
27. Kim B.H., Shenoy A.R., Kumar P., Das R., Tiwari S., MacMicking J.D. A family of IFN-gamma-inducible 65-kD GTPases protects against bacterial infection. Science 2011, 332:717-721.
28. Maertzdorf J., Ota M.O., Repsilber D., Mollenkopf H.J., Weiner J., Hill P.C., Kaufmann S.H.E. Functional correlations of pathogenesis-driven gene expression signatures in tuberculosis. PLoS ONE 2011, 6:e26938.
29. Maertzdorf J., Repsilber D., Parida S.K., Stanley K., Roberts T., Black G., Walzl G., Kaufmann S.H. Human gene expression profiles of susceptibility and resistance in tuberculosis. Genes Immun 2011, 12:15-22.
30. Maertzdorf J., Weiner J., Kaufmann S.H. Enabling biomarkers for tuberculosis control. Int J Tuberc Lung Dis 2012, 16:1140-1148.
31. Fabri M., Stenger S., Shin D.M., Yuk J.M., Liu P.T., Realegeno S., Lee H.M., Krutzik S.R., Schenk M., Sieling P.A., Teles R., Montoya D., Iyer S.S., Bruns H., Lewinsohn D.M., Hollis B.W., Hewison M., Adams J.S., Steinmeyer A., Zugel U., Cheng G., Jo E.K., Bloom B.R., Modlin R.L. Vitamin D is required for IFN-gamma-mediated antimicrobial activity of human macrophages. Sci Transl Med 2011, 3:104ra102.
32. Shi C.S., Shenderov K., Huang N.N., Kabat J., Abu-Asab M., Fitzgerald K.A., Sher A., Kehrl J.H. Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 2012, 13:255-263.
33. Novikov A., Cardone M., Thompson R., Shenderov K., Kirschman K.D., Mayer-Barber K.D., Myers T.G., Rabin R.L., Trinchieri G., Sher A., Feng C.G. Mycobacterium tuberculosis triggers host type I IFN signaling to regulate IL-1beta production in human macrophages. J Immunol 2011, 187:2540-2547.
34. Teles R.M., Graeber T.G., Krutzik S.R., Montoya D., Schenk M., Lee D.J., Komisopoulou E., Kelly-Scumpia K., Chun R., Iyer S.S., Sarno E.N., Rea T.H., Hewison M., Adams J.S., Popper S.J., Relman D.A., Stenger S., Bloom B.R., Cheng G., Modlin R.L. Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science 2013, 339:1448-1453.
35. Arnoldi J., Gerdes J., Flad H.D. Immunohistologic assessment of cytokine production of infiltrating cells in various forms of leprosy. Am J Pathol 1990, 137:749-753.
36. Tobin D.M., Vary J.C., Ray J.P., Walsh G.S., Dunstan S.J., Bang N.D., Hagge D.A., Khadge S., King M.C., Hawn T.R., Moens C.B., Ramakrishnan L. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 2010, 140:717-730.
37. Tobin D.M., Roca F.J., Oh S.F., McFarland R., Vickery T.W., Ray J.P., Ko D.C., Zou Y., Bang N.D., Chau T.T., Vary J.C., Hawn T.R., Dunstan S.J., Farrar J.J., Thwaites G.E., King M.C., Serhan C.N., Ramakrishnan L. Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 2012, 148:434-446.
38. Divangahi M., Desjardins D., Nunes-Alves C., Remold H.G., Behar S.M. Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol 2010, 11:751-758.
39. Rajaram M.V., Ni B., Morris J.D., Brooks M.N., Carlson T.K., Bakthavachalu B., Schoenberg D.R., Torrelles J.B., Schlesinger L.S. Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc Natl Acad Sci U S A 2011, 108:17408-17413.
40. Jayaraman P., Sada-Ovalle I., Nishimura T., Anderson A.C., Kuchroo V.K., Remold H.G., Behar S.M. IL-1beta Promotes antimicrobial immunity in macrophages by regulating TNFR signaling and caspase-3 activation. J Immunol 2013, 190:4196-4204.
41. Ma F., Xu S., Liu X., Zhang Q., Xu X., Liu M., Hua M., Li N., Yao H., Cao X. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat Immunol 2011, 12:861-869.
42. Bogunovic D., Byun M., Durfee L.A., Abhyankar A., Sanal O., Mansouri D., Salem S., Radovanovic I., Grant A.V., Adimi P., Mansouri N., Okada S., Bryant V.L., Kong X.F., Kreins A., Velez M.M., Boisson B., Khalilzadeh S., Ozcelik U., Darazam I.A., Schoggins J.W., Rice C.M., Al-Muhsen S., Behr M., Vogt G., Puel A., Bustamante J., Gros P., Huibregtse J.M., Abel L., Boisson-Dupuis S., Casanova J.L. Mycobacterial disease and impaired IFN-gamma immunity in humans with inherited ISG15 deficiency. Science 2012, 337:1684-1688.
43. Divangahi M., Behar S.M., Remold H. Dying to live: how the death modality of the infected macrophage affects immunity to tuberculosis. Adv Exp Med Biol 2013, 783:103-120.
44. Chen M., Divangahi M., Gan H., Shin D.S., Hong S., Lee D.M., Serhan C.N., Behar S.M., Remold H.G. Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J Exp Med 2008, 205:2791-2801.
45. Divangahi M., Chen M., Gan H., Desjardins D., Hickman T.T., Lee D.M., Fortune S., Behar S.M., Remold H.G. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 2009, 10:899-906.
46. Davis J.M., Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009, 136:37-49.
47. Martin C.J., Booty M.G., Rosebrock T.R., Nunes-Alves C., Desjardins D.M., Keren I., Fortune S.M., Remold H.G., Behar S.M. Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe 2012, 12:289-300.
48. Torchinsky M.B., Garaude J., Martin A.P., Blander J.M. Innate immune recognition of infected apoptotic cells directs T(H)17 cell differentiation. Nature 2009, 458:78-82.
49. Danelishvili L., Everman J.L., McNamara M.J., Bermudez L.E. Inhibition of the plasma-membrane-associated serine protease cathepsin G by Mycobacterium tuberculosis Rv3364c suppresses caspase-1 and pyroptosis in macrophages. Front Microbiol 2011, 2:281.
50. Lee J., Repasy T., Papavinasasundaram K., Sassetti C., Kornfeld H. Mycobacterium tuberculosis induces an atypical cell death mode to escape from infected macrophages. PLoS ONE 2011, 6:e18367.
51. Welin A., Eklund D., Stendahl O., Lerm M. Human macrophages infected with a high burden of ESAT-6-expressing M. tuberculosis undergo caspase-1- and cathepsin B-independent necrosis. PLoS ONE 2011, 6:e20302.
52. Robinson N., McComb S., Mulligan R., Dudani R., Krishnan L., Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat Immunol 2012, 13:954-962.
53. Kaczmarek A., Vandenabeele P., Krysko D.V. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 2013, 38:209-223.
54. Roca F.J., Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013, 153:521-534.
55. Repasy T., Lee J., Marino S., Martinez N., Kirschner D.E., Hendricks G., Baker S., Wilson A.A., Kotton D.N., Kornfeld H. Intracellular bacillary burden reflects a burst size for Mycobacterium tuberculosis in vivo. PLoS Pathog 2013, 9:e1003190.
56. Yang C.T., Cambier C.J., Davis J.M., Hall C.J., Crosier P.S., Ramakrishnan L. Neutrophils exert protection in the early tuberculous granuloma by oxidative killing of mycobacteria phagocytosed from infected macrophages. Cell Host Microbe 2012, 12:301-312.
57. Egen J.G., Rothfuchs A.G., Feng C.G., Horwitz M.A., Sher A., Germain R.N. Intravital imaging reveals limited antigen presentation and T cell effector function in mycobacterial granulomas. Immunity 2011, 34:807-819.
58. Volkman H.E., Pozos T.C., Zheng J., Davis J.M., Rawls J.F., Ramakrishnan L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010, 327:466-469.
59. Elkington P., Shiomi T., Breen R., Nuttall R.K., Ugarte-Gil C.A., Walker N.F., Saraiva L., Pedersen B., Mauri F., Lipman M., Edwards D.R., Robertson B.D., D'Armiento J., Friedland J.S. MMP-1 drives immunopathology in human tuberculosis and transgenic mice. J Clin Invest 2011, 121:1827-1833.
60. Reece S.T., Loddenkemper C., Askew D.J., Zedler U., Schommer-Leitner S., Stein M., Mir F.A., Dorhoi A., Mollenkopf H.J., Silverman G.A., Kaufmann S.H. Serine protease activity contributes to control of Mycobacterium tuberculosis in hypoxic lung granulomas in mice. J Clin Invest 2010, 120:3365-3376.
61. Buckley C.D., Gilroy D.W., Serhan C.N., Stockinger B., Tak P.P. The resolution of inflammation. Nat Rev Immunol 2013, 13:59-66.
62. Chiang N., Fredman G., Backhed F., Oh S.F., Vickery T., Schmidt B.A., Serhan C.N. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 2012, 484:524-528.
63. Coussens A.K., Wilkinson R.J., Hanifa Y., Nikolayevskyy V., Elkington P.T., Islam K., Timms P.M., Venton T.R., Bothamley G.H., Packe G.E., Darmalingam M., Davidson R.N., Milburn H.J., Baker L.V., Barker R.D., Mein C.A., Bhaw-Rosun L., Nuamah R., Young D.B., Drobniewski F.A., Griffiths C.J., Martineau A.R. Vitamin D accelerates resolution of inflammatory responses during tuberculosis treatment. Proc Natl Acad Sci U S A 2012, 109:15449-15454.
64. Sereti I., Rodger A.J., French M.A. Biomarkers in immune reconstitution inflammatory syndrome: signals from pathogenesis. Curr Opin HIV AIDS 2010, 5:504-510.
65. Andries K., Verhasselt P., Guillemont J., Gohlmann H.W., Neefs J.M., Winkler H., Van G.J., Timmerman P., Zhu M., Lee E., Williams P., de C.D., Huitric E., Hoffner S., Cambau E., Truffot-Pernot C., Lounis N., Jarlier V. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 2005, 307:223-227.
66. Raviglione M., Marais B., Floyd K., Lonnroth K., Getahun H., Migliori G.B., Harries A.D., Nunn P., Lienhardt C., Graham S., Chakaya J., Weyer K., Cole S., Kaufmann S.H., Zumla A. Scaling up interventions to achieve global tuberculosis control: progress and new developments. Lancet 2012, 379:1902-1913.
67. Weyer K., Mirzayev F., Migliori G., Van G.W., D'Ambrosio L., Zignol M., Floyd K., Centis R., Cirillo D., Tortoli E., Gilpin C., Iragena J., Falzon D., Raviglione M Rapid molecular TB diagnosis: evidence, policy-making and global implementation of Xpert(R)MTB/RIF. Eur Respir J 2012, 10.1183/09031936.00157212.
68. Von Reyn C.F., Mtei L., Arbeit R., Waddell R., Cole B., Mackenzie T., Matee M., Bakari M., Tvaroha S., Adams L.V., Horsburgh C.R., Pallangyo K. Prevention of tuberculosis in Bacille Calmette-Guérin-primed. HIV-infected adults boosted with an inactivated whole-cell mycobacterial vaccine. AIDS 2010, 24:675-685. The DarDar Study Group.
69. Kaufmann S.H. Fact and fiction in tuberculosis vaccine research: 10 years later. Lancet Infect Dis 2011, 11:633-640.
70. Kaufmann S.H. Tuberculosis vaccine development: strength lies in tenacity. Trends Immunol 2012, 33:373-379.
71. Grode L., Ganoza C.A., Brohm C., Weiner J., Eisele B., Kaufmann S.H.E. Safety and immunogenicity of the recombinant BCG vaccine VPM1002 in a phase 1 open-label randomized clnical trial. Vaccine 2013, 31:1340-1348.
72. van Dissel J.T., Arend S.M., Prins C., Bang P., Tingskov P.N., Lingnau K., Nouta J., Klein M.R., Rosenkrands I., Ottenhoff T.H., Kromann I., Doherty T.M., Andersen P. Ag85B-ESAT-6 adjuvanted with IC31 promotes strong and long-lived Mycobacterium tuberculosis specific T cell responses in naive human volunteers. Vaccine 2010, 28:3571-3581.
73. Aagaard C., Hoang T., Dietrich J., Cardona P.J., Izzo A., Dolganov G., Schoolnik G.K., Cassidy J.P., Billeskov R., Andersen P. A multistage tuberculosis vaccine that confers efficient protection pre- and post-exposure. Nat Med 2011, 17:189-194.
74. Bertholet S., Ireton G.C., Ordway D.J., Windish H.P., Pine S.O., Kahn M., Phan T., Orme I.M., Vedvick T.S., Baldwin S.L., Coler R.N., Reed S.G. A defined tuberculosis vaccine candidate boosts BCG and protects against multidrug-resistant Mycobacterium tuberculosis. Sci Transl Med 2010, 2:53ra74.
75. Coler R.N., Bertholet S., Pine S.O., Orr M.T., Reese V., Windish H.P., Davis C., Kahn M., Baldwin S.L., Reed S.G. Therapeutic immunization against Mycobacterium tuberculosis is an effective adjunct to antibiotic treatment. J Infect Dis 2013, 207:1242-1252.
76. Tameris M.D., Hatherill M., Landry B.S., Scriba T.J., Snowden M.A., Lockhart S., Shea J.E., McClain J.B., Hussey G.D., Hanekom W.A., Mahomed H., McShane H. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 2013, 381:1021-1028.
77. Berry M.P., Graham C.M., McNab F.W., Xu Z., Bloch S.A., Oni T., Wilkinson K.A., Banchereau R., Skinner J., Wilkinson R.J., Quinn C., Blankenship D., Dhawan R., Cush J.J., Mejias A., Ramilo O., Kon O.M., Pascual V., Banchereau J., Chaussabel D., O'Garra A. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010, 466:973-977.
78. Maertzdorf J., Weiner J., Mollenkopf H.-J., TBornotTB Network, Bauer T., Prasse A., Mueller-Quernheim J., Kaufmann S.H.E. Common patterns and disease-related signatures in tuberculosis and sarcoidosis. Proc Natl Acad Sci U S A 2012, 109:7853-7858.
79. Jacobsen M., Repsilber D., Gutschmidt A., Neher A., Feldmann K., Mollenkopf H.J., Ziegler A., Kaufmann S.H. Candidate biomarkers for discrimination between infection and disease caused by Mycobacterium tuberculosis. J Mol Med 2007, 85:613-621.
80. Weiner J., Parida S.K., Maertzdorf J., Black G.F., Repsilber D., Telaar A., Mohney R.P., Arndt-Sullivan C., Ganoza C.A., Fae K.C., Walzl G., Kaufmann S.H.E. Biomarkers of inflammation, immunosuppression and stress with active disease are revealed by metabolomic profiling of tuberculosis patients. PLoS ONE 2012, 7:e40221.