Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages

PLoS Pathogens

Volumn 3, Issue 8, 2007, Pages 1082-1091

  Suzuki, Toshihiko ^a   Franchi, Luigi ^b   Toma, Claudia ^a   Ashida, Hiroshi ^c   Ogawa, Michinaga ^c   Yoshikawa, Yuko ^c   Mimuro, Hitomi ^c   Inohara, Naohiro ^b   Sasakawa, Chihiro ^c,d   Nuñez, Gabriel ^b  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CYTOSOL RECEPTOR; FLAGELLIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; IPAF RECEPTOR; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; UNCLASSIFIED DRUG; 3-METHYLADENINE; ADENINE; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CYTOSKELETON PROTEIN; DRUG DERIVATIVE; IPAF PROTEIN, MOUSE; PYCARD PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BACTERIAL INFECTION; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; LEGIONELLA; MACROPHAGE; MOUSE; NONHUMAN; PHAGOSOME; SALMONELLA; SHIGELLA; ANIMAL; APOPTOSIS; BIOSYNTHESIS; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; NECROSIS; PATHOLOGY; PHYSIOLOGY; SHIGELLA FLEXNERI;

BACTERIA (MICROORGANISMS); LEGIONELLA; SALMONELLA; SHIGELLA;

ADENINE; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BONE MARROW CELLS; CALCIUM-BINDING PROTEINS; CASPASE 1; CELLS, CULTURED; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE SILENCING; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NECROSIS; SHIGELLA FLEXNERI;

EID: 34548434775     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0030111     Document Type: Article

References (52)

1. Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216.
2. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
3. Inohara N, Chamaillard M, McDonald C, Nuñez G (2005) NOD-LRR proteins: Role in host-microbial interactions and inflammatory disease. Annu Rev Biochem 74: 355-383.
4. Ting JP, Davis BK (2005) CATERPILLER: A novel gene family important in immunity, cell death, and diseases. Annu Rev Immunol 23: 387-414.
5. Martinon F, Tschopp J (2004) Inflammatory caspases: Linking an intracellular innate immune system to autoinflammatory diseases. Cell 117: 561-574.
6. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
7. Kanneganti TD, Özören N, Body-Malapel M, Amer A, Park JH, et al. (2006) Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440: 233-236.
8. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
9. 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.
10. 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.
11. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Özören N, et al. (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7: 576-582.
12. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, et al. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575.
13. Zamboni DS, Kobayashi KS, Kohlsdorf T, Ogura Y, Long EM, et al. (2006) The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol 7: 318-325.
14. Amer A, Franchi L, Kanneganti TD, Body-Malapel M, Özören N, et al. (2006) Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J Biol Chem 281: 35217-35223.
15. Mariathasan S, Weiss DS, Dixit VM, Monack DM (2005) Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J Exp Med 202: 1043-1049.
16. Sansonetti PJ, Phalipon A, Arondel J, Thirumalai K, Banerjee S, et al. (2000) Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12: 581-590.
17. Maeda S, Hsu LC, Liu H, Bankston LA, Iimura M, et al. (2005) Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science 307: 734-738.
18. Nadiri A, Wolinski MK, Saleh M (2006) The inflammatory caspases: Key players in the host response to pathogenic invasion and sepsis. J Immunol 177: 4239-4245.
19. Suzuki T, Sasakawa C (2001) Molecular basis of the intracellular spreading of Shigella. Infect Immun 69: 5959-5966.
20. Carlsson F, Brown EJ (2006) Actin-based motility of intracellular bacteria, and polarized surface distribution of the bacterial effector molecules. J Cell Physiol 209: 288-296.
21. Fink SL, Cookson BT (2005) Apoptosis, pyroptosis, and necrosis: Mechanistic description of dead and dying eukaryotic cells. Infect Immun 73: 1907-1916.
22. Brennan MA, Cookson BT (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31-40.
23. Suzuki T, Nakanishi K, Tsutsui H, Iwai H, Akira S, et al. (2005) A novel caspase-1/toll-like receptor 4-independent pathway of cell death induced by cytosolic Shigella in infected macrophages. J Biol Chem 280: 14042-14050.
24. Hilbi H, Moss JE, Hersh D, Chen Y, Arondel J, et al. (1998) Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem 273: 32895-32900.
25. Molofsky AB, Byrne BG, Whitfield NN, Madigan CA, Fuse ET, et al. (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203: 1093-1104.
26. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18. doi:10.1371/journal. ppat.0020018
27. Wei J, Goldberg MB, Burland V, Venkatesan MM, Deng W, et al. (2003) Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect Immun 71: 2775-2786.
28. Jin Q, Yuan Z, Xu J, Wang Y, Shen Y, et al. (2002) Genome sequence of Shigella flexneri 2a: Insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res 30: 4432-4441.
29. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
30. Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57: 77-100.
31. Chilcott GS, Hughes KT (2000) Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol Mol Biol Rev 64: 694-708.
32. Baehrecke EH (2005) Autophagy: Dual roles in life and death? Nat Rev Mol Cell Biol 6: 505-510.
33. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, et al. (2004) Autophagy defends cells against invading group A Streptococcus. Science 306: 1037-1040.
34. Ogawa M, Sasakawa C (2006) Bacterial evasion of the autophagic defense system. Curr Opin Microbiol 9: 62-68.
35. Shintani T, Klionsky DJ (2004) Autophagy in health and disease: A double-edged sword. Science 306: 990-995.
36. Swanson MS, Molofsky AB (2005) Autophagy and inflammatory cell death, partners of innate immunity. Autophagy 1: 174-176.
37. Swanson MS (2006) Autophagy: Eating for good health. J Immunol 177: 4945-4951.
38. Noda T, Ohsumi Y (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273: 3963-3966.
39. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E (2005) Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1: 84-91.
40. Amer AO, Swanson MS (2005) Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol 7: 765-778.
41. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, et al. (2005) Escape of intracellular Shigella from autophagy. Science 307: 727-731.
42. Kirkegaard K, Taylor MP, Jackson WT (2004) Cellular autophagy: Surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2: 301-314.
43. 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.
44. Masumoto J, Dowds TA, Schaner P, Chen FF, Ogura Y, et al. (2003) ASC is an activating adaptor for NF-kappa B and caspase-8-dependent apoptosis. Biochem Biophys Res Commun 303: 69-73.
45. Lamkanfi M, Amer A, Kanneganti TD, Muñoz-Planillo R, Chen G, et al. (2007) The Nod-like receptor (NLR) family member Naip5/Birc1e restricts Legionella pneumophila growth independently of caspase-1 activation. J Immunol 178: 8022-8027.
46. Sasakawa C, Kamata K, Sakai T, Murayama Y, Makino S, et al. (1986) Molecular alteration of the 140-megadalton plasmid associated with loss of virulence and congo red binding activity in Shigella flexneri. Infect Immun 51: 470-475.
47. Watarai M, Tobe T, Yoshikawa M, Sasakawa C (1995) Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J 14: 2461-2470.
48. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
49. Uematsu S, Jang MH, Chevrier N, Guo Z, Kumagai Y, et al. (2006) Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 7: 868-874.
50. Tobe T, Nagai S, Okada N, Adler B, Yoshikawa M, et al. (1991) Temperature-regulated expression of invasion genes in Shigella flexneri is controlled through the transcriptional activation of the virB gene on the large plasmid. Mol Microbiol 5: 887-893.
51. Özören N, Masumoto J, Franchi L, Kanneganti TD, Body-Malapel M, et al. (2006) Distinct roles of TLR2 and the adaptor ASC in IL-1beta/IL-18 secretion in response to Listeria monocytogenes. J Immunol 176: 4337-4342.
52. Suzuki M, Mimuro H, Suzuki T, Park M, Yamamoto T, et al. (2005) Interaction of CagA with Crk plays an important role in Helicobacter pylori-induced loss of gastric epithelial cell adhesion. J Exp Med 202: 1235-1247.