Salmonella-induced SipB-independent cell death requires Toll-like receptor-4 signalling via the adapter proteins Tram and Trif

Immunology

Volumn 122, Issue 2, 2007, Pages 222-229

  Cook, Pamela ^a   Tötemeyer, Sabine ^a   Stevenson, Catherine ^a   Fitzgerald, Katherine A ^b   Yamamoto, Masahiro ^c   Akira, Shizuo ^c   Maskell, Duncan J ^a   Bryant, Clare E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Bacterial infection; Cell death; Monocyte macrophages; Toll like receptor

Indexed keywords

INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN TRAM; PROTEIN TRIF; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL MEMBRANE; CONTROLLED STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLOSIS; SEROTYPE; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BACTERIAL PROTEINS; CASPASE 1; CELL DEATH; CELLS, CULTURED; INTERLEUKIN-1BETA; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 34548597000     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2007.02631.x     Document Type: Article

References (50)

1. Chen LM, Kaniga K, Galan JE. Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 1996 21 : 1101 15.
2. Guilloteau LA, Wallis TS, Gautier AV, MacIntyre S, Platt DJ, Lax AJ. The Salmonella virulence plasmid enhances Salmonella-induced lysis of macrophages and influences inflammatory responses. Infect Immun 1996 64 : 3385 93.
3. Lindgren SW, Stojiljkovic I, Heffron F. Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc Natl Acad Sci USA 1996 93 : 4197 201.
4. Monack DM, Raupach B, Hromockyj AE, Falkow S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 1996 93 : 9833 8.
5. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 1999 96 : 2396 401.
6. Monack DM, Navarre WW, Falkow S. Salmonella-induced macrophage death. the role of caspase-1 in death and inflammation. Microbes Infect 2001 3 : 1201 12.
7. Baumler AJ, Tsolis RM, Valentine PJ, Ficht TA, Heffron F. Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid. Infect Immun 1997 65 : 2254 9.
8. Guiney DG. The role of host cell death in Salmonella infections. Curr Top Microbiol Immunol 2005 289 : 131 50.
9. Raupach B, Peuschel SK, Monack DM, 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. Infect Immun 2006 74 : 4922 6.
10. Lara-Tejero M, Sutterwala FS, Ogura Y, Grant EP, Bertin J, Coyle AJ, Flavell RA, Galan JE. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med 2006 203 : 1407 12.
11. Santos RL, Tsolis RM, Baumler AJ, Smith R. 3rd, Adams LG. Salmonella enterica serovar typhimurium induces cell death in bovine monocyte-derived macrophages by early sipB-dependent and delayed sipB-independent mechanisms. Infect Immun 2001 69 : 2293 301.
12. van der Velden AW, Lindgren SW, Worley MJ, Heffron F. Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype typhimurium. Infect Immun 2000 68 : 5702 9.
13. Browne SH, Lesnick ML, Guiney DG. Genetic requirements for salmonella-induced cytopathology in human monocyte-derived macrophages. Infect Immun 2002 70 : 7126 35.
14. Hsu LC, Park JM, Zhang K et al. The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 2004 428 : 341 5.
15. Libby SJ, Lesnick M, Hasegawa P, Weidenhammer E, Guiney DG. The Salmonella virulence plasmid spv genes are required for cytopathology in human monocyte-derived macrophages. Cell Microbiol 2000 2 : 49 58.
16. Uematsu S, Akira S. Toll-like receptors and innate immunity. J Mol Med 2006 84 : 712 25.
17. O'Neill LA. How Toll-like receptors signal: what we know and what we don't know. Curr Opin Immunol 2006 18 : 3 9.
18. Aliprantis AO, Yang RB, Mark MR et al. Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. Science 1999 285 : 736 9.
19. Aliprantis AO, Yang RB, Weiss DS, Godowski P, Zychlinsky A. The apoptotic signaling pathway activated by Toll-like receptor-2. EMBO J 2000 19 : 3325 36.
20. Barber GN. Host defense, viruses and apoptosis. Cell Death Differ 2001 8 : 113 26.
21. Ruckdeschel K, Mannel O, Richter K, Jacobi CA, Trulzsch K, Rouot B, Heesemann J. Yersinia outer protein P of Yersinia enterocolitica simultaneously blocks the nuclear factor-kappa B pathway and exploits lipopolysaccharide signaling to trigger apoptosis in macrophages. J Immunol 2001 166 : 1823 31.
22. Weiss DS, Raupach B, Takeda K, Akira S, Zychlinsky A. Toll-like receptors are temporally involved in host defense. J Immunol 2004 172 : 4463 9.
23. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999 162 : 3749 52.
24. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 1999 11 : 115 22.
25. Yamamoto M, Sato S, Hemmi H et al. Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 2002 420 : 324 9.
26. Yamamoto M, Sato S, Hemmi H et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003 301 : 640 3.
27. Yamamoto M, Sato S, Hemmi H et al. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 2003 4 : 1144 50.
28. Hormaeche CE. Natural resistance to Salmonella typhimurium in different inbred mouse strains. Immunology 1979 37 : 311 8.
29. Royle MC, Totemeyer S, Alldridge LC, Maskell DJ, Bryant CE. Stimulation of Toll-like receptor 4 by lipopolysaccharide during cellular invasion by live Salmonella typhimurium is a critical but not exclusive event leading to macrophage responses. J Immunol 2003 170 : 5445 54.
30. Totemeyer S, Kaiser P, Maskell DJ, Bryant CE. Sublethal infection of C57BL/6 mice with Salmonella enterica Serovar Typhimurium leads to an increase in levels of Toll-like receptor 1 (TLR1), TLR2, and TLR9 mRNA as well as a decrease in levels of TLR6 mRNA in infected organs. Infect Immun 2005 73 : 1873 8.
31. Yrlid U, Svensson M, Johansson C, Wick MJ. Salmonella infection of bone marrow-derived macrophages and dendritic cells. influence on antigen presentation and initiating an immune response. FEMS Immunol Med Microbiol 2000 27 : 313 20.
32. Totemeyer S, Foster N, Kaiser P, Maskell DJ, Bryant CE. Toll-like receptor expression in C3H/HeN and C3H/HeJ mice during Salmonella enterica serovar Typhimurium infection. Infect Immun 2003 71 : 6653 7.
33. Weinstein DL, Lissner CR, Swanson RN, O'Brien AD. Macrophage defect and inflammatory cell recruitment dysfunction in Salmonella susceptible C3H/HeJ mice. Cell Immunol 1986 102 : 68 77.
34. Hueffer K, Galan JE. Salmonella-induced macrophage death: multiple mechanisms, different outcomes. Cell Microbiol 2004 6 : 1019 25.
35. Chow EK, O'Connell RM, Schilling S, Wang XF, Fu XY, Cheng G. TLR agonists regulate PDGF-B production and cell proliferation through TGF-beta/type I IFN crosstalk. EMBO J 2005 24 : 4071 81.
36. Hasan UA, Trinchieri G, Vlach J. Toll-like receptor signaling stimulates cell cycle entry and progression in fibroblasts. J Biol Chem 2005 280 : 20620 7.
37. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004 118 : 229 41.
38. Boise LH, Collins CM. Salmonella-induced cell death: apoptosis, necrosis or programmed cell death? Trends Microbiol 2001 9 : 64 7.
39. Brennan MA, Cookson BT. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 2000 38 : 31 40.
40. Fantuzzi G, Dinarello CA. Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol 1999 19 : 1 11.
41. Martinon F, Tschopp J. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 2004 117 : 561 74.
42. Mariathasan S, Newton K, Monack DM et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 2004 430 : 213 8.
43. Hernandez LD, Pypaert M, Flavell RA, Galan JE. A Salmonella protein causes macrophage cell death by inducing autophagy. J Cell Biol 2003 163 : 1123 31.
44. Xu Y, Kim SO, Li Y, Han J. Autophagy contributes to caspase-independent macrophage cell death. J Biol Chem 2006 281 : 19179 87.
45. Cogswell JP, Godlevski MM, Wisely GB, Clay WC, Leesnitzer LM, Ways JP, Gray JG. NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J Immunol 1994 153 : 712 23.
46. Fenton MJ, Clark BD, Collins KL, Webb AC, Rich A, Auron PE. Transcriptional regulation of the human prointerleukin 1 beta gene. J Immunol 1987 138 : 3972 9.
47. Turner M, Chantry D, Buchan G, Barrett K, Feldmann M. Regulation of expression of human IL-1 alpha and IL-1 beta genes. J Immunol 1989 143 : 3556 61.
48. Yamamoto M, Yaginuma K, Tsutsui H et al. ASC is essential for LPS-induced activation of procaspase-1 independently of TLR-associated signal adaptor molecules. Genes Cells 2004 9 : 1055 67.
49. Seki E, Tsutsui H, Nakano H et al. Lipopolysaccharide-induced IL-18 secretion from murine Kupffer cells independently of myeloid differentiation factor 88 that is critically involved in induction of production of IL-12 and IL-1beta. J Immunol 2001 166 : 2651 7.
50. Hoebe KX, Georgel P, Janssen E et al. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003 424 : 743 8.