Mycobacterium tuberculosis infection of dendritic cells leads to partially caspase-1/11-independent IL-1β and IL-18 secretion but not to pyroptosis

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Abdalla, Hana ^a   Srinivasan, Lalitha ^a   Shah, Swati ^a   Mayer Barber, Katrin D ^b   Sher, Alan ^b   Sutterwala, Fayyaz S ^c,d   Briken, Volker ^a  

^a Bldg 142   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN ASC; CASPASE 11; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN NLRC 4; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CARRIER PROTEIN; CASP11 PROTEIN, MOUSE; CASPASE; CIAS1 PROTEIN, MOUSE; CYTOSKELETON PROTEIN; HOMEODOMAIN PROTEIN; PYCARD PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL GENE; BACTERIAL SECRETION SYSTEM; BONE MARROW DERIVED DENDRITIC CELL; CELL DEATH; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ESX 1 SECRETION SYSTEM; ESXA GENE; GENE DELETION; HOST CELL; INNATE IMMUNITY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PYRONECROSIS; PYROPTOSIS; TUBERCULOSIS; ANIMAL; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; NECROSIS; SECRETION (PROCESS);

MUS; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CARRIER PROTEINS; CASPASE 1; CASPASES; CYTOSKELETAL PROTEINS; DENDRITIC CELLS; HOMEODOMAIN PROTEINS; INFLAMMASOMES; INTERLEUKIN-18; INTERLEUKIN-1BETA; MICE; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; NECROSIS; TUBERCULOSIS;

EID: 84864258349     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040722     Document Type: Article

References (62)

1. Pedra JH, Cassel SL, Sutterwala FS, (2009) Sensing pathogens and danger signals by the inflammasome. Curr Opin Immunol 21: 10-16.
2. Schroder K, Tschopp J, (2010) The inflammasomes. Cell 140: 821-832.
3. Ting JP, Lovering RC, Alnemri ES, Bertin J, Boss JM, et al. (2008) The NLR gene family: a standard nomenclature. Immunity 28: 285-287.
4. Ting JP, Willingham SB, Bergstralh DT, (2008) NLRs at the intersection of cell death and immunity. Nat Rev Immunol 8: 372-379.
5. Bergsbaken T, Fink SL, Cookson BT, (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7: 99-109.
6. Fink SL, Cookson BT, (2006) Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8: 1812-1825.
7. Chen Y, Smith MR, Thirumalai K, Zychlinsky A, (1996) A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J 15: 3853-3860.
8. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, et al. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96: 2396-2401.
9. Fink SL, Bergsbaken T, Cookson BT, (2008) Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci U S A 105: 4312-4317.
10. Bergsbaken T, Cookson BT, (2007) Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog 3: e161.
11. Dye C, Williams BG, (2010) The population dynamics and control of tuberculosis. Science 328: 856-861.
12. Briken V, Miller JL, (2008) Living on the edge: inhibition of host cell apoptosis by Mycobacterium tuberculosis. Future Microbiol 3: 415-422.
13. Pieters J, (2008) Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3: 399-407.
14. Russell DG, (2007) Who puts the tubercle in tuberculosis? Nat Rev Microbiol 5: 39-47.
15. Behar SM, Divangahi M, Remold HG, (2010) Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol 8: 668-674.
16. Philips JA, Ernst JD, (2012) Tuberculosis pathogenesis and immunity. Annu Rev Pathol 7: 353-384.
17. Sugawara I, Yamada H, Kaneko H, Mizuno S, Takeda K, et al. (1999) Role of interleukin-18 (IL-18) in mycobacterial infection in IL-18-gene-disrupted mice. Infect Immun 67: 2585-2589.
18. Sugawara I, Yamada H, Hua S, Mizuno S, (2001) Role of interleukin (IL)-1 type 1 receptor in mycobacterial infection. Microbiol Immunol 45: 743-750.
19. Fremond CM, Togbe D, Doz E, Rose S, Vasseur V, et al. (2007) IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol 179: 1178-1189.
20. Mayer-Barber KD, Barber DL, Shenderov K, White SD, Wilson MS, et al. (2010) Caspase-1 independent IL-1beta production is critical for host resistance to mycobacterium tuberculosis and does not require TLR signaling in vivo. J Immunol 184: 3326-3330.
21. Schneider BE, Korbel D, Hagens K, Koch M, Raupach B, et al. (2010) A role for IL-18 in protective immunity against Mycobacterium tuberculosis. Eur J Immunol 40: 396-405.
22. Koo IC, Wang C, Raghavan S, Morisaki JH, Cox JS, et al. (2008) ESX-1-dependent cytolysis in lysosome secretion and inflammasome activation during mycobacterial infection. Cell Microbiol 10: 1866-1878.
23. McElvania Tekippe E, Allen IC, Hulseberg PD, Sullivan JT, McCann JR, et al. (2010) Granuloma formation and host defense in chronic Mycobacterium tuberculosis infection requires PYCARD/ASC but not NLRP3 or caspase-1. PLoS One 5: e12320.
24. Mishra BB, Moura-Alves P, Sonawane A, Hacohen N, Griffiths G, et al. (2010) Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell Microbiol 12: 1046-1063.
25. Dorhoi A, Nouailles G, Jorg S, Hagens K, Heinemann E, et al. (2011) Activation of the NLRP3 inflammasome by Mycobacterium tuberculosis is uncoupled from susceptibility to active tuberculosis. Eur J Immunol.
26. Netea MG, Nold-Petry CA, Nold MF, Joosten LA, Opitz B, et al. (2009) Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 113: 2324-2335.
27. Netea MG, Simon A, van de Veerdonk F, Kullberg BJ, Van der Meer JW, et al. (2010) IL-1beta processing in host defense: beyond the inflammasomes. PLoS Pathog 6: e1000661.
28. Jiao X, Lo-Man R, Guermonprez P, Fiette L, Deriaud E, et al. (2002) Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity. J Immunol 168: 1294-1301.
29. Wolf AJ, Linas B, Trevejo-Nunez GJ, Kincaid E, Tamura T, et al. (2007) Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol 179: 2509-2519.
30. Urdahl KB, Shafiani S, Ernst JD, (2011) Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol 4: 288-293.
31. Blomgran R, Desvignes L, Briken V, Ernst JD, (2012) Mycobacterium tuberculosis inhibits neutrophil apoptosis, leading to delayed activation of naive CD4 T cells. Cell Host Microbe 11: 81-90.
32. Walter K, Holscher C, Tschopp J, Ehlers S, (2010) NALP3 is not necessary for early protection against experimental tuberculosis. Immunobiology 215: 804-811.
33. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S, et al. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479: 117-121.
34. Master SS, Rampini SK, Davis AS, Keller C, Ehlers S, et al. (2008) Mycobacterium tuberculosis prevents inflammasome activation. Cell Host Microbe 3: 224-232.
35. Kurenuma T, Kawamura I, Hara H, Uchiyama R, Daim S, et al. (2009) The RD1 locus in the Mycobacterium tuberculosis genome contributes to activation of caspase-1 via induction of potassium ion efflux in infected macrophages. Infect Immun 77: 3992-4001.
36. Carlsson F, Kim J, Dumitru C, Barck KH, Carano RA, et al. (2010) Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection. PLoS Pathog 6: e1000895.
37. Stanley SA, Raghavan S, Hwang WW, Cox JS, (2003) Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci U S A 100: 13001-13006.
38. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ, et al. (2003) The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci U S A 100: 12420-12425.
39. Kleinnijenhuis J, Joosten LA, van de Veerdonk FL, Savage N, van Crevel R, et al. (2009) Transcriptional and inflammasome-mediated pathways for the induction of IL-1beta production by Mycobacterium tuberculosis. Eur J Immunol 39: 1914-1922.
40. Steinman RM, Idoyaga J, (2010) Features of the dendritic cell lineage. Immunol Rev 234: 5-17.
41. Tian T, Woodworth J, Skold M, Behar SM, (2005) In vivo depletion of CD11c+ cells delays the CD4+ T cell response to Mycobacterium tuberculosis and exacerbates the outcome of infection. J Immunol 175: 3268-3272.
42. Bodnar KA, Serbina NV, Flynn JL, (2001) Fate of Mycobacterium tuberculosis within murine dendritic cells. Infect Immun 69: 800-809.
43. Hickman SP, Chan J, Salgame P, (2002) Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J Immunol 168: 4636-4642.
44. Abdallah AM, Gey van Pittius NC, Champion PA, Cox J, Luirink J, et al. (2007) Type VII secretion - mycobacteria show the way. Nat Rev Microbiol 5: 883-891.
45. Simeone R, Bottai D, Brosch R, (2009) ESX/type VII secretion systems and their role in host-pathogen interaction. Curr Opin Microbiol 12: 4-10.
46. Majlessi L, Brodin P, Brosch R, Rojas MJ, Khun H, et al. (2005) Influence of ESAT-6 secretion system 1 (RD1) of Mycobacterium tuberculosis on the interaction between mycobacteria and the host immune system. J Immunol 174: 3570-3579.
47. Li P, Allen H, Banerjee S, Franklin S, Herzog L, et al. (1995) Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80: 401-411.
48. Miggin SM, Palsson-McDermott E, Dunne A, Jefferies C, Pinteaux E, et al. (2007) NF-kappaB activation by the Toll-IL-1 receptor domain protein MyD88 adapter-like is regulated by caspase-1. Proc Natl Acad Sci U S A 104: 3372-3377.
49. Mariathasan S, Monack DM, (2007) Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 7: 31-40.
50. Miller JL, Velmurugan K, Cowan MJ, Briken V, (2010) The Type I NADH Dehydrogenase of Mycobacterium tuberculosis Counters Phagosomal NOX2 Activity to Inhibit TNF-α-Mediated Host Cell Apoptosis. PLoS Pathog 6.
51. Pan H, Yan BS, Rojas M, Shebzukhov YV, Zhou H, et al. (2005) Ipr1 gene mediates innate immunity to tuberculosis. Nature 434: 767-772.
52. Mantegazza AR, Savina A, Vermeulen M, Pérez L, Geffner J, et al. (2008) NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells. Blood 112: 4712-4722.
53. Gandotra S, Jang S, Murray PJ, Salgame P, Ehrt S, (2007) Nucleotide-binding oligomerization domain protein 2-deficient mice control infection with Mycobacterium tuberculosis. Infect Immun 75: 5127-5134.
54. Divangahi M, Mostowy S, Coulombe F, Kozak R, Guillot L, et al. (2008) NOD2-deficient mice have impaired resistance to Mycobacterium tuberculosis infection through defective innate and adaptive immunity. J Immunol 181: 7157-7165.
55. Hsu LC, Ali SR, McGillivray S, Tseng PH, Mariathasan S, et al. (2008) A NOD2-NALP1 complex mediates caspase-1-dependent IL-1beta secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc Natl Acad Sci U S A 105: 7803-7808.
56. Pan Q, Mathison J, Fearns C, Kravchenko VV, Da Silva Correia J, et al. (2007) MDP-induced interleukin-1beta processing requires Nod2 and CIAS1/NALP3. J Leukoc Biol 82: 177-183.
57. Kuranaga E, (2012) Beyond apoptosis: caspase regulatory mechanisms and functions in vivo. Genes Cells.
58. Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, et al. (2011) Caspase signalling controls microglia activation and neurotoxicity. Nature 472: 319-324.
59. Beausejour A, Grenier D, Goulet JP, Deslauriers N, (1998) Proteolytic activation of the interleukin-1beta precursor by Candida albicans. Infect Immun 66: 676-681.
60. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
61. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, et al. (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213-218.
62. Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, et al. (2006) Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.