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The Detrimental Role of Type I Interferon Signaling During Infection with Salmonella typhimurium

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Bacterial Activation of Type I Interferons

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Summary

Pathogenic Salmonella species reside in the phagosomes of infected cells and inject various virulence factors into the phagosome and cytoplasm of the host cell to evade the defense mechanisms. During infection of mice with Salmonella enterica serovar Typhimurium (S. typhimurium), which mimics the typhoid disease in humans, type I IFN signaling leads to rapid host fatality, and abrogation of this signaling leads to prolonged host survival. The detrimental role of type I IFN during Salmonella infection appears to be related to the modulation of inflammatory response.

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References

  1. Broz P, Monack DM (2013) Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol 13:551–565

    Article  PubMed  CAS  Google Scholar 

  2. Iwasaki A, Medzhitov R (2010) Regulation of adaptive immunity by the innate immune system. Science 327:291–295

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  3. Huber M, Kalis C, Keck S, Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, Beutler B, Galanos C, Freudenberg MA (2006) R-form LPS, the master key to the activation of TLR4/MD-2-positive cells. Eur J Immunol 36:701–711

    Article  PubMed  CAS  Google Scholar 

  4. Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, Huber M, Kalis C, Keck S, Galanos C, Freudenberg M, Beutler B (2005) CD14 is required for MyD88-independent LPS signaling. Nat Immunol 6:565–570

    Article  PubMed  CAS  Google Scholar 

  5. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  6. Wilkinson SG (1996) Bacterial lipopolysaccharides–themes and variations. Prog Lipid Res 35:283–343

    Article  PubMed  CAS  Google Scholar 

  7. Bowen WS, Minns LA, Johnson DA, Mitchell TC, Hutton MM, Evans JT (2012) Selective TRIF-dependent signaling by a synthetic toll-like receptor 4 agonist. Sci Signal 5:ra13

    Google Scholar 

  8. Janusch H, Brecker L, Lindner B, Alexander C, Gronow S, Heine H, Ulmer AJ, Rietschel ET, Zahringer U (2002) Structural and biological characterization of highly purified hepta-acyl lipid A present in the lipopolysaccharide of the Salmonella enterica sv. Minnesota Re deep rough mutant strain R595. J Endotoxin Res 8:343–356

    Article  PubMed  CAS  Google Scholar 

  9. Lapaque N, Takeuchi O, Corrales F, Akira S, Moriyon I, Howard JC, Gorvel JP (2006) Differential inductions of TNF-alpha and IGTP, IIGP by structurally diverse classic and non-classic lipopolysaccharides. Cell Microbiol 8:401–413

    Article  PubMed  CAS  Google Scholar 

  10. Toshchakov V, Jones BW, Perera PY, Thomas K, Cody MJ, Zhang S, Williams BR, Major J, Hamilton TA, Fenton MJ, Vogel SN (2002) TLR4, but not TLR2, mediates IFN-beta-induced STAT1alpha/beta-dependent gene expression in macrophages. Nat Immunol 3:392–398

    Article  PubMed  CAS  Google Scholar 

  11. Arpaia N, Godec J, Lau L, Sivick KE, McLaughlin LM, Jones MB, Dracheva T, Peterson SN, Monack DM, Barton GM (2011) TLR signaling is required for Salmonella typhimurium virulence. Cell 144:675–688

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  12. Wong CE, Sad S, Coombes BK (2009) Salmonella enterica serovar typhimurium exploits Toll-like receptor signaling during the host-pathogen interaction. Infect Immun 77:4750–4760

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  13. Gonzalez-Navajas JM, Lee J, David M, Raz E (2012) Immunomodulatory functions of type I interferons. Nat Rev Immunol 12:125–135

    PubMed  CAS  PubMed Central  Google Scholar 

  14. Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4:811–825

    Article  PubMed  CAS  Google Scholar 

  15. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A 107:3076–3080

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Lage SL, Buzzo CL, Amaral EP, Matteucci KC, Massis LM, Icimoto MY, Carmona AK, D’Imperio Lima MR, Rodrigues MM, Ferreira LC, Amarante-Mendes GP, Bortoluci KR (2013) Cytosolic flagellin-induced lysosomal pathway regulates inflammasome-dependent and -independent macrophage responses. Proc Natl Acad Sci U S A 110:E3321–E3330

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  17. Karlinsey JE, Tanaka S, Bettenworth V, Yamaguchi S, Boos W, Aizawa SI, Hughes KT (2000) Completion of the hook-basal body complex of the Salmonella typhimurium flagellum is coupled to FlgM secretion and fliC transcription. Mol Microbiol 37:1220–1231

    Article  PubMed  CAS  Google Scholar 

  18. Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT (2008) Energy source of flagellar type III secretion. Nature 451:489–492

    Article  PubMed  CAS  Google Scholar 

  19. Tseng PH, Matsuzawa A, Zhang W, Mino T, Vignali DA, Karin M (2010) Different modes of ubiquitination of the adaptor TRAF3 selectively activate the expression of type I interferons and proinflammatory cytokines. Nat Immunol 11:70–75

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  20. Hacker H, Tseng PH, Karin M (2011) Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat Rev Immunol 11:457–468

    Article  PubMed  Google Scholar 

  21. Man SM, Tourlomousis P, Hopkins L, Monie TP, Fitzgerald KA, Bryant CE (2013) Salmonella infection induces recruitment of caspase-8 to the inflammasome to modulate IL-1beta production. J Immunol 191:5239–5246

    Article  PubMed  CAS  Google Scholar 

  22. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96:2396–2401

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  23. Fuchs SY (2013) Hope and fear for interferon: the receptor-centric outlook on the future of interferon therapy. J Interferon Cytokine Res 33:211–225

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  24. Rosenberger CM, Scott MG, Gold MR, Hancock RE, Finlay BB (2000) Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J Immunol 164:5894–5904

    Article  PubMed  CAS  Google Scholar 

  25. Bruno VM, Hannemann S, Lara-Tejero M, Flavell RA, Kleinstein SH, Galan JE (2009) Salmonella typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog 5:e1000538

    Article  PubMed  PubMed Central  Google Scholar 

  26. Saraiva M, O’Garra A (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10:170–181

    Article  PubMed  CAS  Google Scholar 

  27. Nguyen T, Robinson N, Allison SE, Coombes BK, Sad S, Krishnan L (2013) IL-10 produced by trophoblast cells inhibits phagosome maturation leading to profound intracellular proliferation of Salmonella enterica typhimurium. Placenta 34:765–774

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  28. Chessler AD, Caradonna KL, Da’dara A, Burleigh BA (2011) Type I interferons increase host susceptibility to Trypanosoma cruzi infection. Infect Immun 79:2112–2119

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Majer O, Bourgeois C, Zwolanek F, Lassnig C, Kerjaschki D, Mack M, Muller M, Kuchler K (2012) Type I interferons promote fatal immunopathology by regulating inflammatory monocytes and neutrophils during Candida infections. PLoS Pathog 8:e1002811

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. Manca C, Tsenova L, Freeman S, Barczak AK, Tovey M, Murray PJ, Barry C, Kaplan G (2005) Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J Interferon Cytokine Res 25:694–701

    Google Scholar 

  31. O’Connell RM, Saha SK, Vaidya SA, Bruhn KW, Miranda GA, Zarnegar B, Perry AK, Nguyen BO, Lane TF, Taniguchi T, Miller JF, Cheng G (2004) Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200:437–445

    Article  PubMed  PubMed Central  Google Scholar 

  32. Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S (2012) Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar typhimurium. Nat Immunol 13:954–962

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  33. Kim KI, Malakhova OA, Hoebe K, Yan M, Beutler B, Zhang DE (2005) Enhanced antibacterial potential in UBP43-deficient mice against Salmonella typhimurium infection by up-regulating type I IFN signaling. J Immunol 175:847–854

    Article  PubMed  CAS  Google Scholar 

  34. Richer E, Yuki KE, Dauphinee SM, Lariviere L, Paquet M, Malo D (2011) Impact of Usp18 and IFN signaling in Salmonella-induced typhlitis. Genes Immun 12:531–543

    Article  PubMed  CAS  Google Scholar 

  35. Sgorbissa A, Brancolini C (2012) IFNs, ISGylation and cancer: Cui prodest? Cytokine Growth Factor Rev 23:307–314

    Article  PubMed  CAS  Google Scholar 

  36. Malakhova OA, Yan M, Malakhov MP, Yuan Y, Ritchie KJ, Kim KI, Peterson LF, Shuai K, Zhang DE (2003) Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev 17:455–460

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  37. Bukholm G, Degre M (1983) Effect of human leukocyte interferon on invasiveness of Salmonella species in HEp-2 cell cultures. Infect Immun 42:1198–1202

    PubMed  CAS  PubMed Central  Google Scholar 

  38. Bukholm G, Berdal BP, Haug C, Degre M (1984) Mouse fibroblast interferon modifies Salmonella typhimurium infection in infant mice. Infect Immun 45:62–66

    PubMed  CAS  PubMed Central  Google Scholar 

  39. Lamkanfi M, Dixit VM (2012) Inflammasomes and their roles in health and disease. Annu Rev Cell Dev Biol 28:137–161

    Article  PubMed  CAS  Google Scholar 

  40. Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I, Farlik M, Decker T, Du Pasquier RA, Romero P, Tschopp J (2011) Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34:213–223

    Article  PubMed  CAS  Google Scholar 

  41. Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C, Stuart LM, Leong JM, Fitzgerald KA (2012) TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150:606–619

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  42. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G (2010) Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 11:700–714

    Article  PubMed  CAS  Google Scholar 

  43. Thapa RJ, Nogusa S, Chen P, Maki JL, Lerro A, Andrake M, Rall GF, Degterev A, Balachandran S (2013) Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc Natl Acad Sci U S A 110:E3109–E3118

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  44. Ramos-Morales F (2012) Impact of Salmonella enterica type III secretion system effectors on the eukaryotic host cell. ISRN Cell Biol 2012:32

    Article  Google Scholar 

  45. de Weerd NA, Vivian JP, Nguyen TK, Mangan NE, Gould JA, Braniff SJ, Zaker-Tabrizi L, Fung KY, Forster SC, Beddoe T, Reid HH, Rossjohn J, Hertzog PJ (2013) Structural basis of a unique interferon-beta signaling axis mediated via the receptor IFNAR. Nat Immunol 14:901–907

    Article  PubMed  Google Scholar 

  46. Mahieu T, Park JM, Revets H, Pasche B, Lengeling A, Staelens J, Wullaert A, Vanlaere I, Hochepied T, van Roy F, Karin M, Libert C (2006) The wild-derived inbred mouse strain SPRET/Ei is resistant to LPS and defective in IFN-beta production. Proc Natl Acad Sci U S A 103:2292–2297

    Google Scholar 

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Authors and Affiliations

  1. Faculty of Medicine, Department of Biochemistry, Microbiology and Immunology, University of Ottawa, 451 Smyth Road, Ottawa, ON, Canada, K1H 8M5

    Bojan Shutinoski & Subash Sad

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  1. Bojan Shutinoski
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  2. Subash Sad
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Correspondence to Subash Sad .

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Editors and Affiliations

  1. Columbia University, New York, New York, USA

    Dane Parker

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© 2014 Springer International Publishing Switzerland

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Shutinoski, B., Sad, S. (2014). The Detrimental Role of Type I Interferon Signaling During Infection with Salmonella typhimurium . In: Parker, D. (eds) Bacterial Activation of Type I Interferons. Springer, Cham. https://doi.org/10.1007/978-3-319-09498-4_7

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