Caspase-1 but not caspase-11 is required for NLRC4-mediated pyroptosis and restriction of infection by flagellated Legionella species in mouse macrophages and in vivo

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 2303-2311

  Cerqueira, Daiane M ^a   Pereira, Marcelo S F ^a   Silva, Alexandre L N ^a   Cunha, Larissa D ^a   Zamboni, Dario S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 11; CRYOPYRIN; FLAGELLIN; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; NOD LIKE RECEPTOR C4 PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CASP11 PROTEIN, MOUSE; CASPASE; INTERLEUKIN 1BETA; IPAF PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; IN VIVO STUDY; INFECTION CONTROL; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYROPTOSIS; 129 MOUSE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL LINE; CLASSIFICATION; FLAGELLUM; FLUORESCENCE MICROSCOPY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; LEGIONELLA; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CASPASE 1; CASPASES; CELL LINE; CELLS, CULTURED; ENZYME ACTIVATION; FLAGELLA; HOST-PATHOGEN INTERACTIONS; INTERLEUKIN-1BETA; LEGIONELLA; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; PYROPTOSIS; SPECIES SPECIFICITY;

EID: 84940118670     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501223     Document Type: Article

References (47)

1. Newton, H. J., D. K. Ang, I. R. van Driel, and E. L. Hartland. 2010. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin. Microbiol. Rev. 23: 274-298.
2. Swanson, M. S., and B. K. Hammer. 2000. Legionella pneumophila pathogesesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54: 567-613.
3. Asrat, S., D. A. de Jesús, A. D. Hempstead, V. Ramabhadran, and R. R. Isberg. 2014. Bacterial pathogen manipulation of host membrane trafficking. Annu. Rev. Cell Dev. Biol. 30: 79-109.
4. Charpentier, X., J. E. Gabay, M. Reyes, J. W. Zhu, A. Weiss, and H. A. Shuman. 2009. Chemical genetics reveals bacterial and host cell functions critical for type IV effector translocation by Legionella pneumophila. PLoS Pathog. 5: e1000501.
5. Hubber, A., and C. R. Roy. 2010. Modulation of host cell function by Legionella pneumophila type IV effectors. Annu. Rev. Cell Dev. Biol. 26: 261-283.
6. Yamamoto, Y., T. W. Klein, C. A. Newton, R. Widen, and H. Friedman. 1988. Growth of Legionella pneumophila in thioglycolate-elicited peritoneal macrophages from A/J mice. Infect. Immun. 56: 370-375.
7. Diez, E., S. H. Lee, S. Gauthier, Z. Yaraghi, M. Tremblay, S. Vidal, and P. Gros. 2003. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 33: 55-60.
8. Wright, E. K., S. A. Goodart, J. D. Growney, V. Hadinoto, M. G. Endrizzi, E. M. Long, K. Sadigh, A. L. Abney, I. Bernstein-Hanley, and W. F. Dietrich. 2003. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13: 27-36.
9. Massis, L. M., and D. S. Zamboni. 2011. Innate immunity to Legionella pneumophila. Front. Microbiol. 2: 109.
10. Vance, R. E. 2010. Immunology taught by bacteria. J. Clin. Immunol. 30: 507-511.
11. Zamboni, D. S., K. S. Kobayashi, T. Kohlsdorf, Y. Ogura, E. M. Long, R. E. Vance, K. Kuida, S. Mariathasan, V. M. Dixit, R. A. Flavell, et al. 2006. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 7: 318-325.
12. Lightfield, K. L., J. Persson, S. W. Brubaker, C. E. Witte, J. von Moltke, E. A. Dunipace, T. Henry, Y. H. Sun, D. Cado, W. F. Dietrich, et al. 2008. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 9: 1171-1178.
13. Amer, A., L. Franchi, T. D. Kanneganti, M. Body-Malapel, N. Ozören, G. Brady, S. Meshinchi, R. Jagirdar, A. Gewirtz, S. Akira, and G. Núñez. 2006. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281: 35217-35223.
14. Franchi, L., A. Amer, M. Body-Malapel, T. D. Kanneganti, N. Ozören, R. Jagirdar, N. Inohara, P. Vandenabeele, J. Bertin, A. Coyle, et al. 2006. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1b in salmonella-infected macrophages. Nat. Immunol. 7: 576-582.
15. Miao, E. A., C. M. Alpuche-Aranda, M. Dors, A. E. Clark, M. W. Bader, S. I. Miller, and A. Aderem. 2006. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1b via Ipaf. Nat. Immunol. 7: 569-575.
16. Molofsky, A. B., B. G. Byrne, N. N. Whitfield, C. A. Madigan, E. T. Fuse, K. Tateda, and M. S. Swanson. 2006. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 203: 1093-1104.
17. Ren, T., D. S. Zamboni, C. R. Roy, W. F. Dietrich, and R. E. Vance. 2006. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2: e18.
18. Pereira, M. S., G. F. Morgantetti, L. M. Massis, C. V. Horta, J. I. Hori, and D. S. Zamboni. 2011. Activation of NLRC4 by flagellated bacteria triggers caspase-1-dependent and -independent responses to restrict Legionella pneumophila replication in macrophages and in vivo. J. Immunol. 187: 6447-6455.
19. Pereira, M. S., G. G. Marques, J. E. Dellama, and D. S. Zamboni. 2011. The Nlrc4 inflammasome contributes to restriction of pulmonary infection by flagellated Legionella spp. that trigger pyroptosis. Front. Microbiol. 2: 33.
20. Silveira, T. N., and D. S. Zamboni. 2010. Pore formation triggered by Legionella spp. is an Nlrc4 inflammasome-dependent host cell response that precedes pyroptosis. Infect. Immun. 78: 1403-1413.
21. Bergsbaken, T., S. L. Fink, and B. T. Cookson. 2009. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7: 99-109.
22. Miao, E. A., I. A. Leaf, P. M. Treuting, D. P. Mao, M. Dors, A. Sarkar, S. E. Warren, M. D. Wewers, and A. Aderem. 2010. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11: 1136-1142.
23. Kayagaki, N., S. Warming, M. Lamkanfi, L. Vande Walle, S. Louie, J. Dong, K. Newton, Y. Qu, J. Liu, S. Heldens, et al. 2011. Non-canonical inflammasome activation targets caspase-11. Nature 479: 117-121.
24. Rathinam, V. A., S. K. Vanaja, L. Waggoner, A. Sokolovska, C. Becker, L. M. Stuart, J. M. Leong, and K. A. Fitzgerald. 2012. TRIF licenses caspase-11- dependent NLRP3 inflammasome activation by Gram-negative bacteria. Cell 150: 606-619.
25. Case, C. L., L. J. Kohler, J. B. Lima, T. Strowig, M. R. de Zoete, R. A. Flavell, D. S. Zamboni, and C. R. Roy. 2013. Caspase-11 stimulates rapid flagellinindependent pyroptosis in response to Legionella pneumophila. Proc. Natl. Acad. Sci. USA 110: 1851-1856.
26. Akhter, A., K. Caution, A. Abu Khweek, M. Tazi, B. A. Abdulrahman, D. H. Abdelaziz, O. H. Voss, A. I. Doseff, H. Hassan, A. K. Azad, et al. 2012. Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity 37: 35-47.
27. Cunha, L. D., and D. S. Zamboni. 2013. Subversion of inflammasome activation and pyroptosis by pathogenic bacteria. Front. Cell. Infect. Microbiol. 3: 76.
28. Feeley, J. C., R. J. Gibson, G. W. Gorman, N. C. Langford, J. K. Rasheed, D. C. Mackel, and W. B. Baine. 1979. Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J. Clin. Microbiol. 10: 437-441.
29. Marim, F. M., T. N. Silveira, D. S. Lima, Jr., and D. S. Zamboni. 2010. A method for generation of bone marrow-derived macrophages from cryopreserved mouse bone marrow cells. PLoS One 5: e15263.
30. Zamboni, D. S., S. McGrath, M. Rabinovitch, and C. R. Roy. 2003. Coxiella burnetii express type IV secretion system proteins that function similarly to components of the Legionella pneumophila Dot/Icm system. Mol. Microbiol. 49: 965-976.
31. Kuida, K., J. A. Lippke, G. Ku, M. W. Harding, D. J. Livingston, M. S. Su, and R. A. Flavell. 1995. Altered cytokine export and apoptosis in mice deficient in interleukin-1b converting enzyme. Science 267: 2000-2003.
32. Lara-Tejero, M., F. S. Sutterwala, Y. Ogura, E. P. Grant, J. Bertin, A. J. Coyle, R. A. Flavell, and J. E. Galán. 2006. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203: 1407-1412.
33. Broz, P., K. Newton, M. Lamkanfi, S. Mariathasan, V. M. Dixit, and D. M. Monack. 2010. Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J. Exp. Med. 207: 1745-1755.
34. Miao, E. A., D. P. Mao, N. Yudkovsky, R. Bonneau, C. G. Lorang, S. E. Warren, I. A. Leaf, and A. Aderem. 2010. Innate immune detection of the type III se- cretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. USA 107: 3076-3080.
35. Case, C. L., S. Shin, and C. R. Roy. 2009. Asc and Ipaf inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect. Immun. 77: 1981-1991.
36. Fortier, A., K. Doiron, M. Saleh, S. Grinstein, and P. Gros. 2009. Restriction of Legionella pneumophila replication in macrophages requires concerted action of the transcriptional regulators Irf1 and Irf8 and nod-like receptors Naip5 and Nlrc4. Infect. Immun. 77: 4794-4805.
37. Storek, K. M., and D. M. Monack. 2015. Bacterial recognition pathways that lead to inflammasome activation. Immunol. Rev. 265: 112-129.
38. Wang, S., M. Miura, Y. K. Jung, H. Zhu, E. Li, and J. Yuan. 1998. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92: 501-509.
39. Aachoui, Y., I. A. Leaf, J. A. Hagar, M. F. Fontana, C. G. Campos, D. E. Zak, M. H. Tan, P. A. Cotter, R. E. Vance, A. Aderem, and E. A. Miao. 2013. Caspase- 11 protects against bacteria that escape the vacuole. Science 339: 975-978.
40. Casson, C. N., A. M. Copenhaver, E. E. Zwack, H. T. Nguyen, T. Strowig, B. Javdan, W. P. Bradley, T. C. Fung, R. A. Flavell, I. E. Brodsky, and S. Shin. 2013. Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog. 9: e1003400.
41. Pilla, D. M., J. A. Hagar, A. K. Haldar, A. K. Mason, D. Degrandi, K. Pfeffer, R. K. Ernst, M. Yamamoto, E. A. Miao, and J. Coers. 2014. Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc. Natl. Acad. Sci. USA 111: 6046-6051.
42. Hagar, J. A., D. A. Powell, Y. Aachoui, R. K. Ernst, and E. A. Miao. 2013. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341: 1250-1253.
43. Kayagaki, N., M. T. Wong, I. B. Stowe, S. R. Ramani, L. C. Gonzalez, S. Akashi-Takamura, K. Miyake, J. Zhang, W. P. Lee, A. Muszynski, et al. 2013. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341: 1246-1249.
44. Meunier, E., M. S. Dick, R. F. Dreier, N. Schürmann, D. Kenzelmann Broz, S. Warming, M. Roose-Girma, D. Bumann, N. Kayagaki, K. Takeda, et al. 2014. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFNinduced GTPases. Nature 509: 366-370.
45. Shi, J., Y. Zhao, Y. Wang, W. Gao, J. Ding, P. Li, L. Hu, and F. Shao. 2014. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514: 187-192.
46. Barry, K. C., M. F. Fontana, J. L. Portman, A. S. Dugan, and R. E. Vance. 2013. IL-1a signaling initiates the inflammatory response to virulent Legionella pneumophila in vivo. J. Immunol. 190: 6329-6339.
47. Broz, P., T. Ruby, K. Belhocine, D. M. Bouley, N. Kayagaki, V. M. Dixit, and D. M. Monack. 2012. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490: 288-291.