Listeria monocytogenes induces IFNβ expression through an IFI16-, cGAS- and STING-dependent pathway

EMBO Journal

Volumn 33, Issue 15, 2014, Pages 1654-1666

  Hansen, Kathrine ^a   Prabakaran, Thaneas ^a   Laustsen, Anders ^a   Jørgensen, Sofie E ^a   Rahbæk, Stine H ^a   Jensen, Søren B ^a   Nielsen, Rikke ^a   Leber, Jess H ^b   Decker, Thomas ^c   Horan, Kristy A ^a   Jakobsen, Martin R ^a   Paludan, Søren R ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

innate immunity; interferon beta; Listeria monocytogenes

Indexed keywords

AMPICILLIN; BETA INTERFERON; CYTOKINE; INTERFERON INDUCIBLE PROTEIN 16; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIOLYSIS; BONE MARROW CELL; CONTROLLED STUDY; DNA TRANSFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HEK293 CELL LINE; INNATE IMMUNITY; INTRACELLULAR BACTERIUM; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STIMULATOR OF INTERFERON GENE;

INNATE IMMUNITY; INTERFERON BETA; LISTERIA MONOCYTOGENES;

ANIMALS; CELLS, CULTURED; CYTOSOL; DNA, BACTERIAL; GENE KNOCKDOWN TECHNIQUES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-BETA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NUCLEAR PROTEINS; NUCLEOTIDYLTRANSFERASES; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84905375825     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488029     Document Type: Article

References (47)

1. Abdullah Z, Schlee M, Roth S, Mraheil MA, Barchet W, Bottcher J, Hain T, Geiger S, Hayakawa Y, Fritz JH, Civril F, Hopfner KP, Kurts C, Ruland J, Hartmann G, Chakraborty T, Knolle PA, (2012) RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J 31: 4153-4164
2. Ablasser A, Goldeck M, Cavlar T, Deimling T, Witte G, Rohl I, Hopfner KP, Ludwig J, Hornung V, (2013) cGAS produces a 2-5-linked cyclic dinucleotide second messenger that activates STING. Nature 498: 380-384
3. Auerbuch V, Brockstedt DG, Meyer-Morse N, O'Riordan M, Portnoy DA, (2004) Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J Exp Med 200: 527-533
4. Barbuddhe SB, Chakraborty T, (2009) Listeria as an enteroinvasive gastrointestinal pathogen. Curr Top Microbiol Immunol 337: 173-195
5. Burdette DL, Monroe KM, Sotelo-Troha K, Iwig JS, Eckert B, Hyodo M, Hayakawa Y, Vance RE, (2011) STING is a direct innate immune sensor of cyclic di-GMP. Nature 478: 515-518
6. Carrero JA, Calderon B, Unanue ER, (2004) Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med 200: 535-540
7. Cavlar T, Deimling T, Ablasser A, Hopfner KP, Hornung V, (2013) Species-specific detection of the antiviral small-molecule compound CMA by STING. EMBO J 32: 1440-1450
8. Chan CW, Crafton E, Fan HN, Flook J, Yoshimura K, Skarica M, Brockstedt D, Dubensky TW, Stins MF, Lanier LL, Pardoll DM, Housseau F, (2006) Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat Med 12: 207-213
9. Conlon J, Burdette DL, Sharma S, Bhat N, Thompson M, Jiang Z, Rathinam VA, Monks B, Jin T, Xiao TS, Vogel SN, Vance RE, Fitzgerald KA, (2013) Mouse, but not human STING, binds and signals in response to the vascular disrupting agent 5,6-dimethylxanthenone-4-acetic acid. J Immunol 190: 5216-5225
10. Cossart P, Vicente MF, Mengaud J, Baquero F, Perez-Diaz JC, Berche P, (1989) Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun 57: 3629-3636
11. Crimmins GT, Herskovits AA, Rehder K, Sivick KE, Lauer P, Dubensky TW Jr, Portnoy DA, (2008) Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity. Proc Natl Acad Sci U S A 105: 10191-10196
12. Diner EJ, Burdette DL, Wilson SC, Monroe KM, Kellenberger CA, Hyodo M, Hayakawa Y, Hammond MC, Vance RE, (2013) The innate immune DNA sensor cGAS produces a noncanonical cyclic dinucleotide that activates human STING. Cell Rep 3: 1355-1361
13. Gao P, Ascano M, Wu Y, Barchet W, Gaffney BL, Zillinger T, Serganov AA, Liu Y, Jones RA, Hartmann G, Tuschl T, Patel DJ, (2013) Cyclic [G(2,5)pA(3,5)p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell 153: 1094-1107
14. Hamon M, Bierne H, Cossart P, (2006) Listeria monocytogenes: a multifaceted model. Nat Rev Microbiol 4: 423-434
15. Holm CK, Jensen SB, Jakobsen MR, Cheshenko N, Horan KA, Moller HB, Gonzalez-Dosal R, Rasmussen SB, Christensen MH, Yarovinsky TO, Rixon FJ, Herold BC, Fitzgerald KA, Paludan SR, (2012) Virus-cell fusion as a trigger of innate immunity dependent on the adaptor STING. Nat Immunol 13: 737-743
16. Horan KA, Hansen K, Jakobsen MR, Holm CK, Waggoner L, West JA, Unterholzner L, Iversen MB, Soby S, Thomson M, Jensen SB, Rasmussen SB, Ellermann-Eriksen S, Kurt-Jones EA, Landolfo S, Melchjorsen J, Bowie AG, Damania B, Fitzgerald KA, Paludan SR, (2013) Proteasomal degradation of herpes simplex virus capsids in macrophage releases DNA to the cytosol for recognition by DNA sensors. J Immunol 190: 2311-2319
17. Jakobsen MR, Bak RO, Andersen A, Berg RK, Jensen SB, Jin T, Laustsen A, Hansen K, Ostergaard LJ, Fitzgerald KA, Xiao T, Mikkelsen JG, Mogensen TH, Paludan SR, (2013) IFI16 senses DNA forms of the retroviral replication cycle and controls HIV-1 replication. PNAS 110: E4571-E4580
18. Jin L, Hill KK, Filak H, Mogan J, Knowles H, Zhang B, Perraud AL, Cambier JC, Lenz LL, (2011) MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J Immunol 187: 2595-2601
19. Jin TC, Perry A, Jiang JS, Smith P, Curry JA, Unterholzner L, Jiang ZZ, Horvath G, Rathinam VA, Johnstone RW, Hornung V, Latz E, Bowie AG, Fitzgerald KA, Xiao TS, (2012) Structures of the HIN domain: DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36: 561-571
20. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, Otageri P, Chandran B, (2011) IFI16 Acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-Associated Herpesvirus Infection. Cell Host Microbe 9: 363-375
21. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, Cossart P, (1992) L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68: 521-531
22. Leber JH, Crimmins GT, Raghavan S, Meyer-Morse NP, Cox JS, Portnoy DA, (2008) Distinct TLR- and NLR-mediated transcriptional responses to an intracellular pathogen. PLoS Pathog 4: e6
23. Li T, Diner BA, Chen J, Cristea IM, (2012) Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. PNAS 109: 10558-10563
24. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS, (2012) Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11: 469-480
25. McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, Joncker NT, Ishii KJ, Akira S, Colonna M, Chen ZJ, Fitzgerald KA, Hayakawa Y, Vance RE, (2009) A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med 206: 1899-1911
26. 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
27. Paludan SR, Bowie AG, (2013) Immune sensing of DNA. Immunity 38: 870-880
28. Parvatiyar K, Zhang Z, Teles RM, Ouyang S, Jiang Y, Iyer SS, Zaver SA, Schenk M, Zeng S, Zhong W, Liu Z, Modlin RL, Liu YJ, Cheng G, (2012) The helicase DDX41 recognizes the bacterial secondary messenger cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat Immunol 13: 1155-1161
29. Rasmussen SB, Horan KA, Holm CK, Stranks AJ, Mettenleiter TC, Simon AK, Jensen SB, Rixon FJ, He B, Paludan SR, (2011) Activation of autophagy by alpha-herpesviruses in myeloid cells is mediated by cytoplasmic viral DNA through a mechanism dependent on stimulator of IFN genes. J Immunol 187: 5268-5276
30. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE, Waggoner L, Vanaja SK, Monks BG, Ganesan S, Latz E, Hornung V, Vogel SN, Szomolanyi-Tsuda E, Fitzgerald KA, (2010) The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol 11: 395-402
31. Rayamajhi M, Humann J, Penheiter K, Andreasen K, Lenz LL, (2010) Induction of IFN-alphabeta enables Listeria monocytogenes to suppress macrophage activation by IFN-gamma. J Exp Med 207: 327-337
32. Sauer JD, Witte CE, Zemansky J, Hanson B, Lauer P, Portnoy DA, (2010) Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7: 412-419
33. Sauer JD, Sotelo-Troha K, von Moltke J, Monroe KM, Rae CS, Brubaker SW, Hyodo M, Hayakawa Y, Woodward JJ, Portnoy DA, Vance RE, (2011) The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect Immun 79: 688-694
34. Schwartz KT, Carleton JD, Quillin SJ, Rollins SD, Portnoy DA, Leber JH, (2012) Hyperinduction of host beta interferon by a Listeria monocytogenes strain naturally overexpressing the multidrug efflux pump MdrT. Infect Immun 80: 1537-1545
35. Solodova E, Jablonska J, Weiss S, Lienenklaus S, (2011) Production of IFN-beta during Listeria monocytogenes infection is restricted to monocyte/macrophage lineage. PLoS ONE 6: e18543
36. Stetson DB, Medzhitov R, (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24: 93-103
37. Stockinger S, Materna T, Stoiber D, Bayr L, Steinborn R, Kolbe T, Unger H, Chakraborty T, Levy DE, Muller M, Decker T, (2002) Production of type I IFN sensitizes macrophages to cell death induced by Listeria monocytogenes. J Immunol 169: 6522-6529
38. Stockinger S, Kastner R, Kernbauer E, Pilz A, Westermayer S, Reutterer B, Soulat D, Stengl G, Vogl C, Frenz T, Waibler Z, Taniguchi T, Rulicke T, Kalinke U, Muller M, Decker T, (2009) Characterization of the interferon-producing cell in mice infected with Listeria monocytogenes. PLoS Pathog 5: e1000355
39. Sun L, Wu J, Du F, Chen X, Chen ZJ, (2013) Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339: 786-791
40. Tanaka Y, Chen ZJ, (2012) STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal, 5: ra20.
41. Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F, (2009) The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 10: 1215-1221
42. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois C, Jin T, Xiao T, Fitzgerald P, Paludan SR, Bowie AG, (2010) IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11: 997-1004
43. Woodward JJ, Iavarone AT, Portnoy DA, (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328: 1703-1705
44. Wu J, Sun L, Chen X, Du F, Shi H, Chen C, Chen ZJ, (2013) Cyclic GMP-AMP Is an Endogenous Second Messenger in Innate Immune Signaling by Cytosolic DNA. Science 339: 826-830
45. Yang P, An H, Liu X, Wen M, Zheng Y, Rui Y, Cao X, (2010) The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat Immunol 11: 487-494
46. Zhang ZQ, Yuan B, Bao MS, Lu N, Kim T, Liu YJ, (2011) The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12: 959-965
47. Zhang X, Shi H, Wu J, Zhang X, Sun L, Chen C, Chen ZJ, (2013) Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell 51: 226-235