Aberrant inflammasome activation characterizes tuberculosis-associated immune reconstitution inflammatory syndrome

Journal of Immunology

Volumn 196, Issue 10, 2016, Pages 4052-4063

  Tan, Hong Yien ^a   Yong, Yean Kong ^a   Shankar, Esaki M ^a   Paukovics, Geza ^b   Ellegard, Rada ^c   Larsson, Marie ^c   Kamarulzaman, Adeeba ^a,d   French, Martyn A ^e,f   Crowe, Suzanne M ^b,g,h  

^a UNIVERSITY OF MALAYA   (Malaysia)

^b MACFARLANE BURNET INSTITUTE FOR MEDICAL RESEARCH AND PUBLIC HEALTH   (Australia)

^c LINKÖPING UNIVERSITY   (Sweden)

^d UNIVERSITY MALAYA MEDICAL CENTRE   (Malaysia)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^f ROYAL PERTH HOSPITAL   (Australia)

^g ALFRED HOSPITAL   (Australia)

^h MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ABSENT IN MELANOMA 2 PROTEIN; ANTIRETROVIRUS AGENT; CD4 ANTIGEN; CRYOPYRIN; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 8; MEMBRANE COFACTOR PROTEIN; MESSENGER RNA; MITOCHONDRIAL DNA; NITRIC OXIDE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG; AIM2 PROTEIN, HUMAN; DNA BINDING PROTEIN;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CORRELATION ANALYSIS; DISEASE ASSOCIATION; DNA DETERMINATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; MACROPHAGE; MACROPHAGE ACTIVATION; MAJOR CLINICAL STUDY; MIXED INFECTION; MONOCYTE; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUBERCULOSIS; UPREGULATION; BLOOD; CELL CULTURE; CELL SELF-RENEWAL; COMPLICATION; GENETICS; HIV INFECTIONS; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHYSIOLOGY; SYNDROME;

ANTI-RETROVIRAL AGENTS; CASPASE 1; CELL DEATH; CELL SELF RENEWAL; CELLS, CULTURED; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; HIV INFECTIONS; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-18; INTERLEUKIN-1BETA; MACROPHAGES; NITRIC OXIDE; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; SYNDROME; TUBERCULOSIS;

EID: 84975031810     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502203     Document Type: Article

References (65)

1. Egger, M., M. May, G. Chêne, A. N. Phillips, B. Ledergerber, F. Dabis, D. Costagliola, A. D'Arminio Monforte, F. de Wolf, P. Reiss, et al; ART Cohort Collaboration. 2002. Prognosis of HIV-1-infected patients starting highly active antiretroviral therapy: a collaborative analysis of prospective studies. Lancet 360: 119-129.
2. When To Start Consortium. 2009. Timing of initiation of antiretroviral therapy in AIDS-free HIV-1-infected patients: a collaborative analysis of 18 HIV cohort studies. Lancet 373: 1352-1363.
3. Müller, M., S. Wandel, R. Colebunders, S. Attia, H. Furrer, and M. Egger, IeDEA Southern and Central Africa. 2010. Immune reconstitution inflammatory syndrome in patients starting antiretroviral therapy for HIV infection: a systematic review and meta-analysis. Lancet Infect. Dis. 10: 251-261.
4. Tan, H. Y., Y. K. Yong, S. H. Lim, S. Ponnampalavanar, S. F. Omar, Y. K. Pang, A. Kamarulzaman, P. Price, S. M. Crowe, and M. A. French. 2014. Tuberculosis (TB)-associated immune reconstitution inflammatory syndrome in TB-HIV coinfected patients in Malaysia: prevalence, risk factors, and treatment outcomes. Sex. Health 11: 532-539.
5. French, M. A. 2009. HIV/AIDS: immune reconstitution inflammatory syndrome: a reappraisal. Clin. Infect. Dis. 48: 101-107.
6. Tan, D. B., Y. K. Yong, H. Y. Tan, A. Kamarulzaman, L. H. Tan, A. Lim, I. James, M. French, and P. Price. 2008. Immunological profiles of immune restoration disease presenting as mycobacterial lymphadenitis and cryptococcal meningitis. HIV Med. 9: 307-316.
7. Manabe, Y. C., R. Breen, T. Perti, E. Girardi, and T. R. Sterling. 2009. Unmasked tuberculosis and tuberculosis immune reconstitution inflammatory disease: a disease spectrum after initiation of antiretroviral therapy. J. Infect. Dis. 199: 437-444.
8. Meintjes, G., H. Rabie, R. J. Wilkinson, and M. F. Cotton. 2009. Tuberculosisassociated immune reconstitution inflammatory syndrome and unmasking of tuberculosis by antiretroviral therapy. Clin. Chest Med. 30: 797-810.
9. Crothers, K., and L. Huang. 2009. Pulmonary complications of immune reconstitution inflammatory syndromes in HIV-infected patients. Respirology 14: 486-494.
10. Bourgarit, A., G. Carcelain, V. Martinez, C. Lascoux, V. Delcey, B. Gicquel, E. Vicaut, P. H. Lagrange, D. Sereni, and B. Autran. 2006. Explosion of tuberculin-specific Th1-responses induces immune restoration syndrome in tuberculosis and HIV co-infected patients. AIDS 20: F1-F7.
11. Antonelli, L. R., Y. Mahnke, J. N. Hodge, B. O. Porter, D. L. Barber, R. DerSimonian, J. H. Greenwald, G. Roby, J. Mican, A. Sher, et al. 2010. Elevated frequencies of highly activated CD4+ T cells in HIV+ patients developing immune reconstitution inflammatory syndrome. Blood 116: 3818-3827.
12. Mahnke, Y. D., J. H. Greenwald, R. DerSimonian, G. Roby, L. R. Antonelli, A. Sher, M. Roederer, and I. Sereti. 2012. Selective expansion of polyfunctional pathogen-specific CD4+ T cells in HIV-1-infected patients with immune reconstitution inflammatory syndrome. Blood 119: 3105-3112.
13. Tadokera, R., G. Meintjes, K. H. Skolimowska, K. A. Wilkinson, K. Matthews, R. Seldon, N. N. Chegou, G. Maartens, M. X. Rangaka, K. Rebe, et al. 2011. Hypercytokinaemia accompanies HIV-tuberculosis immune reconstitution inflammatory syndrome. Eur. Respir. J. 37: 1248-1259.
14. Meintjes, G., K. H. Skolimowska, K. A. Wilkinson, K. Matthews, R. Tadokera, A. Conesa-Botella, R. Seldon, M. X. Rangaka, K. Rebe, D. J. Pepper, et al. 2012. Corticosteroid-modulated immune activation in the tuberculosis immune reconstitution inflammatory syndrome. Am. J. Respir. Crit. Care Med. 186: 369-377.
15. Ravimohan, S., N. Tamuhla, A. P. Steenhoff, R. Letlhogile, K. Nfanyana, S. L. Bellamy, R. R. MacGregor, R. Gross, D. Weissman, and G. P. Bisson. 2015. Immunological profiling of tuberculosis-associated immune reconstitution inflammatory syndrome and non-immune reconstitution inflammatory syndrome death in HIV-infected adults with pulmonary tuberculosis starting antiretroviral therapy: a prospective observational cohort study. Lancet Infect. Dis. 15: 429-438.
16. Narendran, G., B. B. Andrade, B. O. Porter, C. Chandrasekhar, P. Venkatesan, P. A. Menon, S. Subramanian, S. Anbalagan, K. P. Bhavani, S. Sekar, et al. 2013. Paradoxical tuberculosis immune reconstitution inflammatory syndrome (TBIRIS) in HIV patients with culture confirmed pulmonary tuberculosis in India and the potential role of IL-6 in prediction. PLoS One 8: e63541.
17. Conradie, F., A. S. Foulkes, P. Ive, X. Yin, K. Roussos, D. K. Glencross, D. Lawrie, W. Stevens, L. J. Montaner, I. Sanne, and L. Azzoni. 2011. Natural killer cell activation distinguishes Mycobacterium tuberculosis-mediated immune reconstitution syndrome from chronic HIV and HIV/MTB coinfection. J. Acquir. Immune Defic. Syndr. 58: 309-318.
18. Pean, P., E. Nerrienet, Y. Madec, L. Borand, D. Laureillard, M. Fernandez, O. Marcy, C. Sarin, K. Phon, S. Taylor, et al; Cambodian Early versus Late Introduction of Antiretroviral Drugs (CAMELIA) study team. 2012. Natural killer cell degranulation capacity predicts early onset of the immune reconstitution inflammatory syndrome (IRIS) in HIV-infected patients with tuberculosis. Blood 119: 3315-3320.
19. Marais, S., G. Meintjes, D. J. Pepper, L. E. Dodd, C. Schutz, Z. Ismail, K. A. Wilkinson, and R. J. Wilkinson. 2013. Frequency, severity, and prediction of tuberculous meningitis immune reconstitution inflammatory syndrome. Clin. Infect. Dis. 56: 450-460.
20. Bourgarit, A., G. Carcelain, A. Samri, C. Parizot, M. Lafaurie, S. Abgrall, V. Delcey, E. Vicaut, D. Sereni, and B. Autran, PARADOX Study Group. 2009. Tuberculosis-associated immune restoration syndrome in HIV-1-infected patients involves tuberculin-specific CD4 Th1 cells and KIR-negative gammadelta T cells. J. Immunol. 183: 3915-3923.
21. Wilkinson, K. A., N. F. Walker, G. Meintjes, A. Deffur, M. P. Nicol, K. H. Skolimowska, K. Matthews, R. Tadokera, R. Seldon, G. Maartens, et al. 2015. Cytotoxic mediators in paradoxical HIV-tuberculosis immune reconstitution inflammatory syndrome. J. Immunol. 194: 1748-1754.
22. Andrade, B. B., A. Singh, G. Narendran, M. E. Schechter, K. Nayak, S. Subramanian, S. Anbalagan, S. M. Jensen, B. O. Porter, L. R. Antonelli, et al. 2014. Mycobacterial antigen driven activation of CD14++CD162 monocytes is a predictor of tuberculosis-associated immune reconstitution inflammatory syndrome. PLoS Pathog. 10: e1004433.
23. Tan, D. B., A. Lim, Y. K. Yong, S. Ponnampalavanar, S. Omar, A. Kamarulzaman, M. A. French, and P. Price. 2011. TLR2-induced cytokine responses may characterize HIV-infected patients experiencing mycobacterial immune restoration disease. AIDS 25: 1455-1460.
24. Tran, H. T., R. Van den Bergh, T. N. Vu, K. Laukens, W. Worodria, M. M. Loembé, R. Colebunders, L. Kestens, P. De Baetselier, and G. Raes, TBIRIS Study Group. 2014. The role of monocytes in the development of tuberculosis-associated immune reconstitution inflammatory syndrome. Immunobiology 219: 37-44.
25. Oliver, B. G., J. H. Elliott, P. Price, M. Phillips, V. Saphonn, M. C. Vun, J. M. Kaldor, D. A. Cooper, and M. A. French. 2010. Mediators of innate and adaptive immune responses differentially affect immune restoration disease associated with Mycobacterium tuberculosis in HIV patients beginning antiretroviral therapy. J. Infect. Dis. 202: 1728-1737.
26. Tan, H. Y., Y. K. Yong, B. B. Andrade, E. M. Shankar, S. Ponnampalavanar, S. F. Omar, G. Narendran, A. Kamarulzaman, S. Swaminathan, I. Sereti, et al. 2015. Plasma interleukin-18 levels are a biomarker of innate immune responses that predict and characterize tuberculosis-associated immune reconstitution inflammatory syndrome. AIDS 29: 421-431.
27. Gracie, J. A., S. E. Robertson, and I. B. McInnes. 2003. Interleukin-18. J. Leukoc. Biol. 73: 213-224.
28. Netea, M. G., A. Simon, F. van de Veerdonk, B. J. Kullberg, J. W. Van der Meer, and L. A. Joosten. 2010. IL-1β processing in host defense: beyond the inflammasomes. PLoS Pathog. 6: e1000661.
29. Dinarello, C. A., D. Novick, S. Kim, and G. Kaplanski. 2013. Interleukin-18 and IL-18 binding protein. Front. Immunol. 4: 289.
30. Novick, D., S. Kim, G. Kaplanski, and C. A. Dinarello. 2013. Interleukin-18, more than a Th1 cytokine. Semin. Immunol. 25: 439-448.
31. Schroder, K., and J. Tschopp. 2010. The inflammasomes. Cell 140: 821-832.
32. van de Veerdonk, F. L., M. G. Netea, C. A. Dinarello, and L. A. Joosten. 2011. Inflammasome activation and IL-1β and IL-18 processing during infection. Trends Immunol. 32: 110-116.
33. Lamkanfi, M., and V. M. Dixit. 2009. The inflammasomes. PLoS Pathog. 5: e1000510.
34. Mishra, B. B., V. A. Rathinam, G. W. Martens, A. J. Martinot, H. Kornfeld, K. A. Fitzgerald, and C. M. Sassetti. 2013. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1β. Nat. Immunol. 14: 52-60.
35. Denes, A., G. Lopez-Castejon, and D. Brough. 2012. Caspase-1: is IL-1 just the tip of the ICEberg? Cell Death Dis. 3: e338.
36. Bergsbaken, T., S. L. Fink, and B. T. Cookson. 2009. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7: 99-109.
37. Fink, S. L., and B. T. Cookson. 2005. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73: 1907-1916.
38. Broderick, L., and H. M. Hoffman. 2014. cASCading specks. Nat. Immunol. 15: 698-700.
39. LaRock, C. N., and B. T. Cookson. 2013. Burning down the house: cellular actions during pyroptosis. PLoS Pathog. 9: e1003793.
40. Doitsh, G., N. L. Galloway, X. Geng, Z. Yang, K. M. Monroe, O. Zepeda, P. W. Hunt, H. Hatano, S. Sowinski, I. Muñoz-Arias, and W. C. Greene. 2014. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505: 509-514.
41. Belibasakis, G. N., and A. Johansson. 2012. Aggregatibacter actinomycetemcomitans targets NLRP3 and NLRP6 inflammasome expression in human mononuclear leukocytes. Cytokine 59: 124-130.
42. Lauring, A. S., T. H. Lee, J. N. Martin, P. W. Hunt, S. G. Deeks, and M. Busch. 2012. Lack of evidence for mtDNA as a biomarker of innate immune activation in HIV infection. PLoS One 7: e50486.
43. Rayamajhi, M., and E. A. Miao. 2013. Just say NO to NLRP3. Nat. Immunol. 14: 12-14.
44. Mao, K., S. Chen, M. Chen, Y. Ma, Y. Wang, B. Huang, Z. He, Y. Zeng, Y. Hu, S. Sun, et al. 2013. Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Res. 23: 201-212.
45. Loza, M. J., and B. Perussia. 2004. The IL-12 signature: NK cell terminal CD56+high stage and effector functions. J. Immunol. 172: 88-96.
46. O'Garra, A., P. S. Redford, F. W. McNab, C. I. Bloom, R. J. Wilkinson, and M. P. Berry. 2013. The immune response in tuberculosis. Annu. Rev. Immunol. 31: 475-527.
47. Vergne, I., J. Chua, S. B. Singh, and V. Deretic. 2004. Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20: 367-394.
48. Meena, L. S., and Rajni. 2010. Survival mechanisms of pathogenic Mycobacterium tuberculosis H37Rv. FEBS J. 277: 2416-2427.
49. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15: 323-350.
50. Yang, C. S., J. M. Yuk, and E. K. Jo. 2009. The role of nitric oxide in mycobacterial infections. Immune Netw. 9: 46-52.
51. Gallegos, A. M., J. W. van Heijst, M. Samstein, X. Su, E. G. Pamer, and M. S. Glickman. 2011. A g interferon independent mechanism of CD4 T cell mediated control of M. tuberculosis infection in vivo. PLoS Pathog. 7: e1002052.
52. Diedrich, C. R., and J. L. Flynn. 2011. HIV-1/Mycobacterium tuberculosis coinfection immunology: how does HIV-1 exacerbate tuberculosis? Infect. Immun. 79: 1407-1417.
53. Tomlinson, G. S., L. C. Bell, N. F. Walker, J. Tsang, J. S. Brown, R. Breen, M. Lipman, D. R. Katz, R. F. Miller, B. M. Chain, et al. 2014. HIV-1 infection of macrophages dysregulates innate immune responses to Mycobacterium tuberculosis by inhibition of interleukin-10. J. Infect. Dis. 209: 1055-1065.
54. Dorhoi, A., G. Nouailles, S. Jörg, K. Hagens, E. Heinemann, L. Pradl, D. Oberbeck-Müller, M. A. Duque-Correa, S. T. Reece, J. Ruland, et al. 2012. Activation of the NLRP3 inflammasome by Mycobacterium tuberculosis is uncoupled from susceptibility to active tuberculosis. Eur. J. Immunol. 42: 374-384.
55. Lai, R. P., G. Meintjes, K. A. Wilkinson, C. M. Graham, S. Marais, H. Van der Plas, A. Deffur, C. Schutz, C. Bloom, I. Munagala, et al. 2015. HIV-tuberculosisassociated immune reconstitution inflammatory syndrome is characterized by Toll-like receptor and inflammasome signalling. Nat. Commun. 6: 8451.
56. Mishra, B. B., P. Moura-Alves, A. Sonawane, N. Hacohen, G. Griffiths, L. F. Moita, and E. Anes. 2010. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell. Microbiol. 12: 1046-1063.
57. Lee, H. M., J. Kang, S. J. Lee, and E. K. Jo. 2013. Microglial activation of the NLRP3 inflammasome by the priming signals derived from macrophages infected with mycobacteria. Glia 61: 441-452.
58. Nakahira, K., J. A. Haspel, V. A. Rathinam, S. J. Lee, T. Dolinay, H. C. Lam, J. A. Englert, M. Rabinovitch, M. Cernadas, H. P. Kim, et al. 2011. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12: 222-230.
59. Hirata, J., J. Kotani, M. Aoyama, S. Kashiwamura, H. Ueda, Y. Kuroda, M. Usami, H. Okamura, and S. Marukawa. 2008. A role for IL-18 in human neutrophil apoptosis. Shock 30: 628-633.
60. Eisenbarth, S. C., O. R. Colegio, W. O'Connor, F. S. Sutterwala, and R. A. Flavell. 2008. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453: 1122-1126.
61. Conforti-Andreoni, C., P. Ricciardi-Castagnoli, and A. Mortellaro. 2011. The inflammasomes in health and disease: from genetics to molecular mechanisms of autoinflammation and beyond. Cell. Mol. Immunol. 8: 135-145.
62. Cinel, I., and S. M. Opal. 2009. Molecular biology of inflammation and sepsis: a primer. Crit. Care Med. 37: 291-304.
63. Lamkanfi, M., and V. M. Dixit. 2012. Inflammasomes and their roles in health and disease. Annu. Rev. Cell Dev. Biol. 28: 137-161.
64. Masters, S. L., M. Gerlic, D. Metcalf, S. Preston, M. Pellegrini, J. A. O'Donnell, K. McArthur, T. M. Baldwin, S. Chevrier, C. J. Nowell, et al. 2012. NLRP1 inflammasome activation induces pyroptosis of hematopoietic progenitor cells. Immunity 37: 1009-1023.
65. Puren, A. J., G. Fantuzzi, and C. A. Dinarello. 1999. Gene expression, synthesis, and secretion of interleukin 18 and interleukin 1β are differentially regulated in human blood mononuclear cells and mouse spleen cells. Proc. Natl. Acad. Sci. USA 96: 2256-2261.