Differential roles of caspase-1 and caspase-11 in infection and inflammation

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Ming Man, Si ^a   Karki, Rajendra ^a   Briard, Benoit ^a   Burton, Amanda ^a   Gingras, Sebastien ^a   Pelletier, Stephane ^a   Kanneganti, Thirumala Devi ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CASP1 PROTEIN, MOUSE; CASP11 PROTEIN, MOUSE; CASPASE; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; IPAF PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; NLRC3 PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL; BACTERIAL INFECTION; C57BL MOUSE; CELL CULTURE; FEMALE; GENETICS; MALE; METABOLISM; MOUSE; MYCOSIS; PYROPTOSIS;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BACTERIAL INFECTIONS; CALCIUM-BINDING PROTEINS; CASPASE 1; CASPASES; CELLS, CULTURED; FEMALE; INFLAMMASOMES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-18; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MYCOSES; PYROPTOSIS;

EID: 85016159886     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep45126     Document Type: Article

References (106)

1. Martinon, F., Tschopp, J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117, 561-574 (2004).
2. Man, S. M., Kanneganti, T. D. Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nature reviews. Immunology 16, 7-21 (2016).
3. Kostura, M. J., et al. Identification of a monocyte specific pre-interleukin 1 beta convertase activity. Proceedings of the National Academy of Sciences of the United States of America 86, 5227-5231 (1989).
4. Black, R. A., Kronheim, S. R., Sleath, P. R. Activation of interleukin-1 beta by a co-induced protease. FEBS letters 247, 386-390 (1989).
5. Ghayur, T., et al. Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 386, 619-623 (1997).
6. Auron, P. E., et al. Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proceedings of the National Academy of Sciences of the United States of America 81, 7907-7911 (1984).
7. March, C. J., et al. Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature 315, 641-647 (1985).
8. Ushio, S., et al. Cloning of the cDNA for human IFN-gamma-inducing factor, expression in Escherichia coli, studies on the biologic activities of the protein. Journal of immunology 156, 4274-4279 (1996).
9. Okamura, H., et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 378, 88-91 (1995).
10. Gu, Y., et al. Activation of interferon-gamma inducing factor mediated by interleukin-1 beta converting enzyme. Science 275, 206-209 (1997).
11. Thornberry, N. A., et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356, 768-774 (1992).
12. Martinon, F., Burns, K., Tschopp, J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Molecular cell 10, 417-426 (2002).
13. Man, S. M., Kanneganti, T. D. Regulation of inflammasome activation. Immunological reviews 265, 6-21 (2015).
14. Kuida, K., et al. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267, 2000-2003 (1995).
15. Li, P., et al. 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 (1995).
16. Kayagaki, N., et al. Non-canonical inflammasome activation targets caspase-11. Nature 479, 117-121 (2011).
17. Broz, P., et al. Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. The Journal of experimental medicine 207, 1745-1755 (2010).
18. Man, S. M., et al. Inflammasome activation causes dual recruitment of NLRC4 and NLRP3 to the same macromolecular complex. Proceedings of the National Academy of Sciences of the United States of America 111, 7403-7408 (2014).
19. Miao, E. A., et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nature immunology 7, 569-575 (2006).
20. Franchi, L., et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nature immunology 7, 576-582 (2006).
21. Amer, A., et al. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. The Journal of biological chemistry 281, 35217-35223 (2006).
22. Mariathasan, S., et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430, 213-218 (2004).
23. Mariathasan, S., et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232 (2006).
24. Kanneganti, T. D., et al. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and doublestranded RNA. The Journal of biological chemistry 281, 36560-36568 (2006).
25. Kanneganti, T. D., et al. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440, 233-236 (2006).
26. Martinon, F., Petrilli, V., Mayor, A., Tardivel, A., Tschopp, J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241 (2006).
27. Man, S. M., Karki, R., Kanneganti, T. D. AIM2 inflammasome in infection, cancer, autoimmunity: Role in DNA sensing, inflammation, innate immunity. European journal of immunology 46, 269-280 (2016).
28. Man, S. M., Karki, R., Kanneganti, T. D. DNA-sensing inflammasomes: regulation of bacterial host defense and the gut microbiota. Pathogens and disease 74, ftw028 (2016).
29. Rathinam, V. A., et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nature immunology 11, 395-402 (2010).
30. Fernandes-Alnemri, T., Yu, J. W., Datta, P., Wu, J., Alnemri, E. S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458, 509-513 (2009).
31. Fernandes-Alnemri, T., et al. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nature immunology 11, 385-393 (2010).
32. Hornung, V., et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458, 514-518 (2009).
33. Roberts, T. L., et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057-1060 (2009).
34. Burckstummer, T., et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nature immunology 10, 266-272 (2009).
35. Wu, J., Fernandes-Alnemri, T., Alnemri, E. S. Involvement of the AIM2, NLRC4, NLRP3 inflammasomes in caspase-1 activation by Listeria monocytogenes. J Clin Immunol 30, 693-702 (2010).
36. Tsuchiya, K., et al. Involvement of absent in melanoma 2 in inflammasome activation in macrophages infected with Listeria monocytogenes. Journal of immunology 185, 1186-1195 (2010).
37. Sauer, J. D., et al. Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell host & microbe 7, 412-419 (2010).
38. Meixenberger, K., et al. Listeria monocytogenes-infected human peripheral blood mononuclear cells produce IL-1beta, depending on listeriolysin O and NLRP3. Journal of immunology 184, 922-930 (2010).
39. Kim, S., et al. Listeria monocytogenes is sensed by the NLRP3 and AIM2 inflammasome. European journal of immunology 40, 1545-1551 (2010).
40. Warren, S. E., et al. Cutting edge: Cytosolic bacterial DNA activates the inflammasome via Aim2. Journal of immunology 185, 818-821 (2010).
41. Mueller, N. J., Wilkinson, R. A., Fishman, J. A. Listeria monocytogenes infection in caspase-11-deficient mice. Infection and immunity 70, 2657-2664 (2002).
42. Kayagaki, N., et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341, 1246-1249 (2013).
43. Shi, J., et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514, 187-192 (2014).
44. Hagar, J. A., Powell, D. A., Aachoui, Y., Ernst, R. K., Miao, E. A. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341, 1250-1253 (2013).
45. Mariathasan, S., Weiss, D. S., Dixit, V. M., Monack, D. M. Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. The Journal of experimental medicine 202, 1043-1049 (2005).
46. Man, S. M., et al. The transcription factor IRF1 and guanylate-binding proteins target activation of the AIM2 inflammasome by Francisella infection. Nature immunology 16, 467-475 (2015).
47. Meunier, E., et al. Guanylate-binding proteins promote activation of the AIM2 inflammasome during infection with Francisella novicida. Nature immunology 16, 476-484 (2015).
48. Jones, J. W., et al. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proceedings of the National Academy of Sciences of the United States of America 107, 9771-9776 (2010).
49. Man, S. M., et al. IRGB10 Liberates Bacterial Ligands for Sensing by the AIM2 and Caspase-11-NLRP3 Inflammasomes. Cell 167(382-396), e317 (2016).
50. Ruhl, S., Broz, P. Caspase-11 activates a canonical NLRP3 inflammasome by promoting K(+ ) efflux. European journal of immunology 45, 2927-2936 (2015).
51. Lamkanfi, M., et al. Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. Journal of immunology 185, 4385-4392 (2010).
52. Wang, S., et al. Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92, 501-509 (1998).
53. Yang, D., He, Y., Munoz-Planillo, R., Liu, Q., Nunez, G. Caspase-11 Requires the Pannexin-1 Channel and the Purinergic P2X7 Pore to Mediate Pyroptosis and Endotoxic Shock. Immunity 43, 923-932 (2015).
54. van de Veerdonk, F. L., Joosten, L. A., Netea, M. G. The interplay between inflammasome activation and antifungal host defense. Immunological reviews 265, 172-180 (2015).
55. Karki, R., et al. Concerted Activation of the AIM2 and NLRP3 Inflammasomes Orchestrates Host Protection against Aspergillus Infection. Cell host & microbe 17, 357-368 (2015).
56. Segal, B. H. Aspergillosis. The New England journal of medicine 360, 1870-1884 (2009).
57. Vande Walle, L., Lamkanfi, M. Pyroptosis. Current Biology 26, R568-R572 (2016).
58. Akhter, A., et al. Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity 37, 35-47 (2012).
59. Caution, K., et al. Caspase-11 and caspase-1 differentially modulate actin polymerization via RhoA and Slingshot proteins to promote bacterial clearance. Sci Rep-Uk 5 (2015).
60. Aachoui, Y., et al. Canonical Inflammasomes Drive IFN-gamma to Prime Caspase-11 in Defense against a Cytosol-Invasive Bacterium. Cell host & microbe 18, 320-332 (2015).
61. Wang, S., et al. Identification and characterization of Ich-3, a member of the interleukin-1beta converting enzyme (ICE)/Ced-3 family and an upstream regulator of ICE. The Journal of biological chemistry 271, 20580-20587 (1996).
62. Fassy, F., et al. Enzymatic activity of two caspases related to interleukin-1beta-converting enzyme. European journal of biochemistry/FEBS 253, 76-83 (1998).
63. Knodler, L. A., et al. Noncanonical Inflammasome Activation of Caspase-4/Caspase-11 Mediates Epithelial Defenses against Enteric Bacterial Pathogens. Cell host & microbe 16, 249-256 (2014).
64. Gurung, P., et al. Toll or interleukin-1 receptor (TIR) domain-containing adaptor inducing interferon-beta (TRIF)-mediated caspase-11 protease production integrates Toll-like receptor 4 (TLR4) protein-and Nlrp3 inflammasome-mediated host defense against enteropathogens. The Journal of biological chemistry 287, 34474-34483 (2012).
65. Broz, P., et al. Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490, 288-291 (2012).
66. Rathinam, V. A., et al. TRIF Licenses Caspase-11-Dependent NLRP3 Inflammasome Activation by Gram-Negative Bacteria. Cell 150, 606-619 (2012).
67. Schauvliege, R., Vanrobaeys, J., Schotte, P., Beyaert, R. Caspase-11 gene expression in response to lipopolysaccharide and interferon-gamma requires nuclear factor-kappa B and signal transducer and activator of transcription (STAT) 1. The Journal of biological chemistry 277, 41624-41630 (2002).
68. Sander, L. E., et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474, 385-389 (2011).
69. Shi, J., et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526, 660-665. (2015).
70. Kayagaki, N., et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signaling. Nature 526, 666-671 (2015).
71. He, W. T., et al. Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion. Cell research 25, 1285-1298 (2015).
72. Ding, J., et al. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535, 111-116 (2016).
73. Aglietti, R. A., et al. GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proceedings of the National Academy of Sciences of the United States of America (2016).
74. Liu, X., et al. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535, 153-158 (2016).
75. Sborgi, L., et al. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. The EMBO journal (2016).
76. Chen, X., et al. Pyroptosis is driven by non-selective gasdermin-D pore and its morphology is different from MLKL channelmediated necroptosis. Cell research 26, 1007-1020 (2016).
77. Kang, S. J., et al. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. The Journal of cell biology 149, 613-622 (2000).
78. Zanoni, I., et al. An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells. Science 352, 1232-1236 (2016).
79. Pierini, R., et al. AIM2/ASC triggers caspase-8-dependent apoptosis in Francisella-infected caspase-1-deficient macrophages. Cell death and differentiation 19, 1709-1721 (2012).
80. Lai, X. H., Golovliov, I., Sjostedt, A. Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infection and immunity 69, 4691-4694 (2001).
81. Wickstrum, J. R., et al. Francisella tularensis induces extensive caspase-3 activation and apoptotic cell death in the tissues of infected mice. Infection and immunity 77, 4827-4836 (2009).
82. Pearson, J. S., et al. A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature 501, 247-251 (2013).
83. Li, S., et al. Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature 501, 242-246 (2013).
84. Hemrajani, C., et al. NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proceedings of the National Academy of Sciences of the United States of America 107, 3129-3134 (2010).
85. Lara-Tejero, M., et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. The Journal of experimental medicine 203, 1407-1412 (2006).
86. Raupach, B., Peuschel, S. K., Monack, D. M., Zychlinsky, A. Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection. Infection and immunity 74, 4922-4926 (2006).
87. Sellin, M. E., et al. Epithelium-Intrinsic NAIP/NLRC4 Inflammasome Drives Infected Enterocyte Expulsion to Restrict Salmonella Replication in the Intestinal Mucosa. Cell host & microbe 16, 237-248 (2014).
88. Man, S. M., et al. Actin polymerization as a key innate immune effector mechanism to control Salmonella infection. Proceedings of the National Academy of Sciences of the United States of America 111, 17588-17593 (2014).
89. Thurston, T. L., et al. Growth inhibition of cytosolic Salmonella by caspase-1 and caspase-11 precedes host cell death. Nature communications 7, 13292 (2016).
90. Sokolovska, A., et al. Activation of caspase-1 by the NLRP3 inflammasome regulates the NADPH oxidase NOX2 to control phagosome function. Nature immunology 14, 543-553 (2013).
91. Zaki, M. H., et al. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32, 379-391 (2010).
92. Allen, I. C., et al. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. The Journal of experimental medicine 207, 1045-1056 (2010).
93. Dupaul-Chicoine, J., et al. Control of intestinal homeostasis, colitis, colitis-associated colorectal cancer by the inflammatory caspases. Immunity 32, 367-378 (2010).
94. Demon, D., et al. Caspase-11 is expressed in the colonic mucosa and protects against dextran sodium sulfate-induced colitis. Mucosal immunology 7, 1480-1491 (2014).
95. Williams, T. M., et al. Caspase-11 Attenuates Gastrointestinal Inflammation and Experimental Colitis Pathogenesis. American journal of physiology. Gastrointestinal and liver physiology 308, G139-150 (2014).
96. Oficjalska, K., et al. Protective Role for Caspase-11 during Acute Experimental Murine Colitis. Journal of immunology 194, 1252-1260 (2014).
97. Baker, P. J., et al. NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. European journal of immunology 45, 2918-2926 (2015).
98. Schmid-Burgk, J. L., et al. Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells. European journal of immunology 45, 2911-2917 (2015).
99. Kajiwara, Y., et al. A critical role for human caspase-4 in endotoxin sensitivity. Journal of immunology 193, 335-343 (2014).
100. Vigano, E., et al. Human caspase-4 and caspase-5 regulate the one-step non-canonical inflammasome activation in monocytes. Nature communications 6, 8761 (2015).
101. Casson, C. N., et al. Human caspase-4 mediates noncanonical inflammasome activation against gram-negative bacterial pathogens. Proceedings of the National Academy of Sciences of the United States of America (2015).
102. Case, C. L., et al. Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila. Proceedings of the National Academy of Sciences of the United States of America 110, 1851-1856 (2013).
103. Hu, B., et al. The DNA-sensing AIM2 inflammasome controls radiation-induced cell death and tissue injury. Science 354, 765-768 (2016).
104. Pelletier, S., Gingras, S., Green, D. R. Mouse Genome Engineering via CRISPR-Cas9 for Study of Immune Function. Immunity 42, 18-27 (2015).
105. Bae, S., Park, J., Kim, J. S. Cas-OFFinder: a fast and versatile algorithm that searches for potential off-target sites of Cas9 RNAguided endonucleases. Bioinformatics 30, 1473-1475 (2014).
106. Girardin, H., Latge, J. P., Srikantha, T., Morrow, B., Soll, D. R. Development of DNA probes for fingerprinting Aspergillus fumigatus. J Clin Microbiol 31, 1547-1554 (1993).