Type III IFNS are commonly induced by bacteria-sensing TLRS and reinforce epithelial barriers during infection

Journal of Immunology

Volumn 199, Issue 9, 2017, Pages 3271-3279

  Odendall, Charlotte ^a,b,c   Voak, Andrew A ^c   Kagan, Jonathan C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c GUY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; LAMBDA INTERFERON; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL INFECTION; BONE MARROW DERIVED DENDRITIC CELL; CELL MEMBRANE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SHIGELLA FLEXNERI; SHIGELLA SONNEI; ANIMAL; BACTERIUM; EPITHELIUM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; CELL LINE, TUMOR; EPITHELIUM; GENE EXPRESSION REGULATION; HUMANS; INTERFERONS; MICE; MICE, KNOCKOUT; TOLL-LIKE RECEPTORS;

EID: 85032030627     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1700250     Document Type: Article

References (54)

1. Kotenko, S. V., G. Gallagher, V. V. Baurin, A. Lewis-Antes, M. Shen, N. K. Shah, J. A. Langer, F. Sheikh, H. Dickensheets, and R. P. Donnelly. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4: 69-77.
2. Sheppard, P.,W. Kindsvogel,W. Xu, K. Henderson, S. Schlutsmeyer, T. E.Whitmore, R. Kuestner, U. Garrigues, C. Birks, J. Roraback, et al. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4: 63-68.
3. Onoguchi, K., M. Yoneyama, A. Takemura, S. Akira, T. Taniguchi, H. Namiki, and T. Fujita. 2007. Viral infections activate types I and III interferon genes through a common mechanism. J. Biol. Chem. 282: 7576-7581.
4. Mäkelä, S. M., P. Osterlund, and I. Julkunen. 2011. TLR ligands induce synergistic interferon-b and interferon-l1 gene expression in human monocytederived dendritic cells. Mol. Immunol. 48: 505-515.
5. Odendall, C., E. Dixit, F. Stavru, H. Bierne, K. M. Franz, A. F. Durbin, S. Boulant, L. Gehrke, P. Cossart, and J. C. Kagan. 2014. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 15: 717-726.
6. Sommereyns, C., S. Paul, P. Staeheli, and T. Michiels. 2008. IFN-lambda (IFNlambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 4: e1000017.
7. Lazear, H. M., T. J. Nice, and M. S. Diamond. 2015. Interferon-l: immune functions at barrier surfaces and beyond. Immunity 43: 15-28.
8. Coccia, E. M., M. Severa, E. Giacomini, D. Monneron, M. E. Remoli, I. Julkunen, M. Cella, R. Lande, and G. Uzé. 2004. Viral infection and Toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and monocyte-derived dendritic cells. Eur. J. Immunol. 34: 796-805.
9. Thomson, S. J., F. G. Goh, H. Banks, T. Krausgruber, S. V. Kotenko, B. M. Foxwell, and I. A. Udalova. 2009. The role of transposable elements in the regulation of IFN-lambda1 gene expression. Proc. Natl. Acad. Sci. USA 106: 11564-11569.
10. Bierne, H., L. Travier, T. Mahlako iv, L. Tailleux, A. Subtil, A. Lebreton, A. Paliwal, B. Gicquel, P. Staeheli, M. Lecuit, and P. Cossart. 2012. Activation of type III interferon genes by pathogenic bacteria in infected epithelial cells and mouse placenta. PLoS One 7: e39080.
11. Lebreton, A., G. Lakisic, V. Job, L. Fritsch, T. N. Tham, A. Camejo, P. J. Matteï, B. Regnault, M. A. Nahori, D. Cabanes, et al. 2011. A bacterial protein targets the BAHD1 chromatin complex to stimulate type III interferon response. Science 331: 1319-1321.
12. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
13. Noppert, S. J., K. A. Fitzgerald, and P. J. Hertzog. 2007. The role of type I interferons in TLR responses. Immunol. Cell Biol. 85: 446-457.
14. Brubaker, S. W., K. S. Bonham, I. Zanoni, and J. C. Kagan. 2015. Innate immune pattern recognition: a cell biological perspective. Annu. Rev. Immunol. 33: 257-290.
15. Ank, N., M. B. Iversen, C. Bartholdy, P. Staeheli, R. Hartmann, U. B. Jensen, F. Dagnaes-Hansen, A. R. Thomsen, Z. Chen, H. Haugen, et al. 2008. An important role for type III interferon (IFN-l/IL-28) in TLR-induced antiviral activity. J. Immunol. 180: 2474-2485.
16. Barton, G. M., and J. C. Kagan. 2009. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9: 535-542.
17. Kawai, T., and S. Akira. 2007. TLR signaling. Semin. Immunol. 19: 24-32.
18. Kagan, J. C., V. G. Magupalli, and H. Wu. 2014. SMOCs: supramolecular organizing centres that control innate immunity. Nat. Rev. Immunol. 14: 821-826.
19. Motshwene, P. G., M. C. Moncrieffe, J. G. Grossmann, C. Kao, M. Ayaluru, A. M. Sandercock, C. V. Robinson, E. Latz, and N. J. Gay. 2009. An oligomeric signaling platform formed by the Toll-like receptor signal transducers MyD88 and IRAK-4. J. Biol. Chem. 284: 25404-25411.
20. Gay, N. J., M. F. Symmons, M. Gangloff, and C. E. Bryant. 2014. Assembly and localization of Toll-like receptor signalling complexes. Nat. Rev. Immunol. 14: 546-558.
21. Lin, S. C., Y. C. Lo, and H. Wu. 2010. Helical assembly in the MyD88-IRAK4-IRAK2 complex in TLR/IL-1R signalling. Nature 465: 885-890.
22. Bonham, K. S., M. H. Orzalli, K. Hayashi, A. I. Wolf, C. Glanemann, W. Weninger, A. Iwasaki, D. M. Knipe, and J. C. Kagan. 2014. A promiscuous lipid-binding protein diversifies the subcellular sites of toll-like receptor signal transduction. Cell 156: 705-716.
23. Gay, N. J., M. Gangloff, and L. A. O'Neill. 2011. What the Myddosome structure tells us about the initiation of innate immunity. Trends Immunol. 32: 104-109.
24. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301: 640-643.
25. Nilsen, N. J., G. I. Vladimer, J. Stenvik, M. P. A. Orning, M. V. Zeid-Kilani, M. Bugge, B. Bergstroem, J. Conlon, H. Husebye, A. G. Hise, et al. 2015. A role for the adaptor proteins TRAM and TRIF in toll-like receptor 2 signaling. J. Biol. Chem. 290: 3209-3222.
26. Lazear, H. M., B. P. Daniels, A. K. Pinto, A. C. Huang, S. C. Vick, S. E. Doyle, M. Gale, R. S. Klein, and M. S. Diamond. 2015. Interferon-l restricts West Nile virus neuroinvasion by tightening the blood-brain barrier. Sci. Transl. Med. 7: 284ra59.
27. Lencer, W. I., C. Delp, M. R. Neutra, and J. L. Madara. 1992. Mechanism of cholera toxin action on a polarized human intestinal epithelial cell line: role of vesicular traffic. J. Cell Biol. 117: 1197-1209.
28. Hisamatsu, T., M. Suzuki, H. C. Reinecker, W. J. Nadeau, B. A. McCormick, and D. K. Podolsky. 2003. CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology 124: 993-1000.
29. Köhler, H., T. Sakaguchi, B. P. Hurley, B. A. Kase, H. C. Reinecker, and B. A. McCormick. 2007. Salmonella enterica serovar Typhimurium regulates intercellular junction proteins and facilitates transepithelial neutrophil and bacterial passage. [Published erratum appears in 2007 Am. J. Physiol. Gastrointest. Liver Physiol. 293: G1099.] Am. J. Physiol. Gastrointest. Liver Physiol. 293: G178-G187.
30. Hallstrom, K., and B. A. McCormick. 2011. Salmonella interaction with and passage through the intestinal mucosa: through the lens of the organism. Front. Microbiol. 2: 88.
31. Betts, J., and B. B. Finlay. 1992. Identification of Salmonella typhimurium invasiveness loci. Can. J. Microbiol. 38: 852-857.
32. Mills, D. M., V. Bajaj, and C. A. Lee. 1995. A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol. Microbiol. 15: 749-759.
33. Galán, J. E., and R. Curtiss, III. 1989. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86: 6383-6387.
34. Gerlach, R. G., N. Cláudio, M. Rohde, D. Jäckel, C. Wagner, and M. Hensel. 2008. Cooperation of Salmonella pathogenicity islands 1 and 4 is required to breach epithelial barriers. Cell. Microbiol. 10: 2364-2376.
35. Sakaguchi, T., H. Köhler, X. Gu, B. A. McCormick, and H. C. Reinecker. 2002. Shigella flexneri regulates tight junction-associated proteins in human intestinal epithelial cells. Cell. Microbiol. 4: 367-381.
36. Kotenko, S. V. 2011. IFN-ls. Curr. Opin. Immunol. 23: 583-590.
37. Lasfar, A., A. Lewis-Antes, S. V. Smirnov, S. Anantha, W. Abushahba, B. Tian, K. Reuhl, H. Dickensheets, F. Sheikh, R. P. Donnelly, et al. 2006. Characterization of the mouse IFN-lambda ligand-receptor system: IFN-lambdas exhibit antitumor activity against B16 melanoma. Cancer Res. 66: 4468-4477.
38. Sun, J., N. Li, K. S. Oh, B. Dutta, S. J. Vayttaden, B. Lin, T. S. Ebert, D. De Nardo, J. Davis, R. Bagirzadeh, et al. 2016. Comprehensive RNAi-based screening of human and mouse TLR pathways identifies species-specific preferences in signaling protein use. Sci. Signal. 9: ra3.
39. Lee, S. J., W. J. Kim, and S. K. Moon. 2012. Role of the p38 MAPK signaling pathway in mediating interleukin-28A-induced migration of UMUC-3 cells. Int. J. Mol. Med. 30: 945-952.
40. Medzhitov, R., P. Preston-Hurlburt, E. Kopp, A. Stadlen, C. Chen, S. Ghosh, and C. A. Janeway, Jr. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2: 253-258.
41. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 169: 6668-6672.
42. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122.
43. Kagan, J. C., T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov. 2008. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferonbeta. Nat. Immunol. 9: 361-368.
44. Robertson, M. J., F. M. Deane, P. J. Robinson, and A. McCluskey. 2014. Synthesis of Dynole 34-2, Dynole 2-24 and Dyngo 4a for investigating dynamin GTPase. Nat. Protoc. 9: 851-870.
45. Zanoni, I., R. Ostuni, L. R. Marek, S. Barresi, R. Barbalat, G. M. Barton, F. Granucci, and J. C. Kagan. 2011. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147: 868-880.
46. Krupna-Gaylord, M. A., D. Liveris, A. C. Love, G. P. Wormser, I. Schwartz, and M. M. Petzke. 2014. Induction of type I and type III interferons by Borrelia burgdorferi correlates with pathogenesis and requires linear plasmid 36. PLoS One 9: e100174.
47. Kawai, T., and S. Akira. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
48. Tanimura, N., S. Saitoh, F. Matsumoto, S. Akashi-Takamura, and K. Miyake. 2008. Roles for LPS-dependent interaction and relocation of TLR4 and TRAM in TRIF-signaling. Biochem. Biophys. Res. Commun. 368: 94-99.
49. Stack, J., S. L. Doyle, D. J. Connolly, L. S. Reinert, K. M. O'Keeffe, R. M. McLoughlin, S. R. Paludan, and A. G. Bowie. 2014. TRAM is required for TLR2 endosomal signaling to type I IFN induction. J. Immunol. 193: 6090-6102.
50. Dietrich, N., S. Lienenklaus, S. Weiss, and N. O. Gekara. 2010. Murine toll-like receptor 2 activation induces type I interferon responses from endolysosomal compartments. PLoS One 5: e10250.
51. Barbalat, R., L. Lau, R. M. Locksley, and G. M. Barton. 2009. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. [Published erratum appears in 2010 Nat. Immunol. 11: 543.] Nat. Immunol. 10: 1200-1207.
52. Seth, R. B., L. Sun, C. K. Ea, and Z. J. Chen. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
53. Dixit, E., S. Boulant, Y. Zhang, A. S. Lee, C. Odendall, B. Shum, N. Hacohen, Z. J. Chen, S. P. Whelan, M. Fransen, et al. 2010. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141: 668-681.
54. Rauch, I., F. Rosebrock, E. Hainzl, S. Heider, A. Majoros, S. Wienerroither, B. Strobl, S. Stockinger, L. Kenner, M. Muller, and T. Decker. 2015. Noncanonical effects of IRF9 in intestinal inflammation: more than type I and type III interferons. Mol. Cell. Biol. 35: 2332-2343.