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

Volumn 112, Issue 21, 2015, Pages 6688-6693

  Casson, Cierra N ^a   Yu, Janet ^a   Reyes, Valeria M ^a   Taschuk, Frances O ^a   Yadav, Anjana ^b   Copenhaver, Alan M ^a   Nguyen, Hieu T ^a   Collman, Ronald G ^b   Shin, Sunny ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Caspase 4; Gram negative bacteria; Inflammasome; Innate immunity; Primary macrophages

Indexed keywords

CASPASE 11; CASPASE 4; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; CASP4 PROTEIN, HUMAN; INITIATOR CASPASE; LIPOPOLYSACCHARIDE;

ARTICLE; BACTERIAL INFECTION; BACTERIUM MUTANT; CELL DEATH; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOSOL; EPITHELIUM CELL; GENETIC TRANSFECTION; GRAM NEGATIVE BACTERIUM; HOST CELL; HUMAN; HUMAN CELL; KERATINOCYTE; LEGIONELLA PNEUMOPHILA; MACROPHAGE; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN MODIFICATION; REGULATORY MECHANISM; SUPERNATANT; TRANSFORMED CELL LINE; TYPE III SECRETION SYSTEM; TYPE IV SECRETION SYSTEM; ANIMAL; CELL CULTURE; ENZYMOLOGY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIA (MICROORGANISMS); MURINAE; NEGIBACTERIA;

ANIMALS; CASPASE 1; CASPASES, INITIATOR; CELL DEATH; CELLS, CULTURED; GRAM-NEGATIVE BACTERIA; HUMANS; INFLAMMASOMES; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; LEGIONELLA PNEUMOPHILA; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; SALMONELLA TYPHIMURIUM; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84930225289     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421699112     Document Type: Article

References (48)

1. Janeway CA, Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197-216.
2. Harton JA, Linhoff MW, Zhang J, Ting JP-Y (2002) Cutting edge: CATERPILLER: A large family of mammalian genes containing CARD, pyrin, nucleotide-binding, and leucinerich repeat domains. J Immunol 169(8):4088-4093.
3. Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: Discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6(1):10-21.
4. Martinon F, Burns K, Tschopp J (2002) The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10(2):417-426.
5. Li P, 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(3):401-411.
6. Kuida K, et al. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267(5206):2000-2003.
7. Kayagaki N, et al. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479(7371):117-121.
8. Rathinam VAK, et al. (2012) TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150(3):606-619.
9. Gurung P, et al. (2012) Toll or interleukin-1 receptor (TIR) domain-containing adaptor inducing interferon-β (TRIF)-mediated caspase-11 protease production integrates Toll-like receptor 4 (TLR4) protein- and Nlrp3 inflammasome-mediated host defense against enteropathogens. J Biol Chem 287(41):34474-34483.
10. Broz P, et al. (2012) Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490(7419):288-291.
11. Aachoui Y, et al. (2013) Caspase-11 protects against bacteria that escape the vacuole. Science 339(6122):975-978.
12. Lamkanfi M, Dixit VM (2014) Mechanisms and functions of inflammasomes. Cell 157(5):1013-1022.
13. Case CL, et al. (2013) Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila. Proc Natl Acad Sci USA 110(5):1851-1856.
14. Casson CN, et al. (2013) Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog 9(6):e1003400.
15. Wang S, et al. (1998) Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92(4):501-509.
16. Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA (2013) Cytoplasmic LPS activates caspase-11: Implications in TLR4-independent endotoxic shock. Science 341(6151):1250-1253.
17. Kayagaki N, et al. (2013) Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341(6151):1246-1249.
18. Akhter A, et al. (2012) Caspase-11 promotes the fusion of phagosomes harboring pathogenic bacteria with lysosomes by modulating actin polymerization. Immunity 37(1):35-47.
19. Kamens J, et al. (1995) Identification and characterization of ICH-2, a novel member of the interleukin-1 beta-converting enzyme family of cysteine proteases. J Biol Chem 270(25):15250-15256.
20. Munday NA, et al. (1995) Molecular cloning and pro-apoptotic activity of ICErelII and ICErelIII, members of the ICE/CED-3 family of cysteine proteases. J Biol Chem 270(26): 15870-15876.
21. Kamada S, Funahashi Y, Tsujimoto Y (1997) Caspase-4 and caspase-5, members of the ICE/CED-3 family of cysteine proteases, are CrmA-inhibitable proteases. Cell Death Differ 4(6):473-478.
22. Shi J, et al. (2014) Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514(7521):187-192.
23. McDade JE, et al. (1977) Legionnaires' disease: Isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297(22):1197-1203.
24. Marra A, Blander SJ, Horwitz MA, Shuman HA (1992) Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci USA 89(20):9607-9611.
25. Berger KH, Isberg RR (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7(1):7-19.
26. Isberg RR, O'Connor TJ, Heidtman M (2009) The Legionella pneumophila replication vacuole: Making a cosy niche inside host cells. Nat Rev Microbiol 7(1):13-24.
27. Knodler LA, et al. (2014) Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 16(2):249-256.
28. Ossina NK, et al. (1997) Interferon-gamma modulates a p53-independent apoptotic pathway and apoptosis-related gene expression. J Biol Chem 272(26):16351-16357.
29. Lin XY, Choi MS, Porter AG (2000) Expression analysis of the human caspase-1 sub-family reveals specific regulation of the CASP5 gene by lipopolysaccharide and interferon-gamma. J Biol Chem 275(51):39920-39926.
30. Galán JE, Lara-Tejero M, Marlovits TC, Wagner S (2014) Bacterial type III secretion systems: Specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68:415-438.
31. Brodsky IE, et al. (2010) A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 7(5): 376-387.
32. LaRock CN, Cookson BT (2012) The Yersinia virulence effector YopM binds caspase-1 to arrest inflammasome assembly and processing. Cell Host Microbe 12(6):799-805.
33. Kobayashi T, et al. (2013) The Shigella OspC3 effector inhibits caspase-4, antagonizes inflammatory cell death, and promotes epithelial infection. Cell Host Microbe 13(5): 570-583.
34. Kajiwara Y, et al. (2014) A critical role for human caspase-4 in endotoxin sensitivity. J Immunol 193(1):335-343.
35. Meunier E, et al. (2014) Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 509(7500):366-370.
36. Pilla DM, et al. (2014) Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS. Proc Natl Acad Sci USA 111(16):6046-6051.
37. Man SM, et al. (2014) Inflammasome activation causes dual recruitment of NLRC4 and NLRP3 to the same macromolecular complex. Proc Natl Acad Sci USA 111(20):7403-7408.
38. Li H, Willingham SB, Ting JP-Y, Re F (2008) Cutting edge: Inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J Immunol 181(1):17-21.
39. Hitomi J, et al. (2004) Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J Cell Biol 165(3):347-356.
40. Sollberger G, Strittmatter GE, Kistowska M, French LE, Beer H-D (2012) Caspase-4 is required for activation of inflammasomes. J Immunol 188(4):1992-2000.
41. Feldmeyer L, et al. (2007) The inflammasome mediates UVB-induced activation and secretion of interleukin-1beta by keratinocytes. Curr Biol 17(13):1140-1145.
42. Sano R, Reed JC (2013) ER stress-induced cell death mechanisms. Biochim Biophys Acta 1833(12):3460-3470.
43. Murakami T, et al. (2012) Critical role for calcium mobilization in activation of the NLRP3 inflammasome. Proc Natl Acad Sci USA 109(28):11282-11287.
44. Horwitz MA, Silverstein SC (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest 66(3):441-450.
45. Swanson MS, Isberg RR (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63(9):3609-3620.
46. Berger KH, Merriam JJ, Isberg RR (1994) Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol Microbiol 14(4):809-822.
47. Lilo S, Zheng Y, Bliska JB (2008) Caspase-1 activation in macrophages infected with Yersinia pestis KIM requires the type III secretion system effector YopJ. Infect Immun 76(9):3911-3923.
48. Palmer LE, Hobbie S, Galán JE, Bliska JB (1998) YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-alpha production and downregulation of the MAP kinases p38 and JNK. Mol Microbiol 27(5):953-965.