Identification of host cytosolic sensors and bacterial factors regulating the type I interferon response to Legionella pneumophila

PLoS Pathogens

Volumn 5, Issue 11, 2009, Pages

  Monroe, Kathryn M ^a   McWhirter, Sarah M ^a   Vance, Russell E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIAL RNA; INTERFERON; MDA5 PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; SDHA PROTEIN; UNCLASSIFIED DRUG; DDX58 PROTEIN, MOUSE; DEAD BOX PROTEIN; IFIH1PROTEIN, MOUSE; IPS 1 PROTEIN, MOUSE; IPS-1 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIUM IDENTIFICATION; CELL ACTIVATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; EMBRYO; ENZYME REGULATION; ENZYME REPRESSION; GENE TARGETING; HOST CELL; HUMAN; HUMAN CELL; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; MOUSE; NONHUMAN; PROTEIN SECRETION; SENSOR; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; GENETICS; HOST PATHOGEN INTERACTION; LEGIONNAIRE DISEASE; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; NEGIBACTERIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELLS, CULTURED; CYTOSOL; DEAD-BOX RNA HELICASES; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INTERFERON TYPE I; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION;

EID: 73549090166     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000665     Document Type: Article

References (60)

1. Fields BS, Benson RF, Besser RE (2002) Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 15: 506-526.
2. Horwitz MA, Silverstein SC (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest 66: 441-450.
3. Isberg RR, O'Connor TJ, Heidtman M (2009) The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7: 13-24.
4. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR (2006) A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc Natl Acad Sci U S A 103: 18745-18750.
5. Archer KA, Roy CR (2006) MyD88-dependent responses involving toll-like receptor 2 are important for protection and clearance of Legionella pneumophila in a mouse model of Legionnaires' disease. Infect Immun 74: 3325-3333.
6. Hawn TR, Berrington WR, Smith IA, Uematsu S, Akira S, et al. (2007) Altered inflammatory responses in TLR5-deficient mice infected with Legionella pneumophila. J Immunol 179: 6981-6987.
7. Hawn TR, Smith KD, Aderem A, Skerrett SJ (2006) Myeloid differentiation primary response gene (88)- and toll-like receptor 2-deficient mice are susceptible to infection with aerosolized Legionella pneumophila. J Infect Dis 193: 1693-1702.
8. Shin S, Case CL, Archer KA, Nogueira CV, Kobayashi KS, et al. (2008) Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog 4: e1000220. doi:10.1371/journal.ppat.1000220.
9. Amer A, Franchi L, Kanneganti TD, Body-Malapel M, Ozoren N, et al. (2006) Regulation of Legionella phagosome maturation and infection through flagellin and host IPAF. J Biol Chem 281: 35217-35223.
10. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, et al. (2008) Critical function for Naip5 in inflammasome activation by a conserved carboxyterminal domain of flagellin. Nat Immunol 9: 1171-1178.
11. 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.
12. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE (2006) Flagellindeficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18. doi:10.1371/journal.ppat.0020018.
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. Opitz B, Vinzing M, van Laak V, Schmeck B, Heine G, et al. (2006) Legionella pneumophila induced IFNbeta in lung epithelial cells via IPS-1 and IRF3 which also control bacterial replication. J Biol Chem 281: 36173-36179.
15. Stetson DB, Medzhitov R (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24: 93-103.
16. Coers J, Vance RE, Fontana MF, Dietrich WF (2007) Restriction of Legionella pneumophila growth in macrophages requires the concerted action of cytokine and Naip5/Ipaf signalling pathways. Cell Microbiol 9: 2344-2357.
17. Schiavoni G, Mauri C, Carlei D, Belardelli F, Pastoris MC, et al. (2004) Type I IFN protects permissive macrophages from Legionella pneumophila infection through an IFN-gamma-independent pathway. J Immunol 173: 1266-1275.
18. Stetson DB, Medzhitov R (2006) Type I interferons in host defense. Immunity 25: 373-381.
19. Pichlmair A, Reis e Sousa C (2007) Innate recognition of viruses. Immunity 27: 370-383.
20. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.
21. Seth RB, Sun L, Ea CK, Chen ZJ (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
22. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988.
23. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, et al. (2005) VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727-740.
24. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172.
25. Sun Q, Sun L, Liu HH, Chen X, Seth RB, et al. (2006) The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24: 633-642.
26. Ishii KJ, Coban C, Kato H, Takahashi K, Torii Y, et al. (2006) A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol 7: 40-48.
27. Cheng G, Zhong J, Chung J, Chisari FV (2007) Double-stranded DNA and double-stranded RNA induce a common antiviral signaling pathway in human cells. Proc Natl Acad Sci U S A 104: 9035-9040.
28. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, et al. (2009) RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol.
29. Chiu YH, Macmillan JB, Chen ZJ (2009) RNA Polymerase III Detects Cytosolic DNA and Induces Type I Interferons through the RIG-I Pathway. Cell 138: 576-591.
30. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, et al. (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448: 501-505.
31. Wang Z, Choi MK, Ban T, Yanai H, Negishi H, et al. (2008) Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc Natl Acad Sci U S A 105: 5477-5482.
32. Ishii KJ, Kawagoe T, Koyama S, Matsui K, Kumar H, et al. (2008) TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 451: 725-729.
33. Karaolis DK, Means TK, Yang D, Takahashi M, Yoshimura T, et al. (2007) Bacterial c-di-GMP is an immunostimulatory molecule. J Immunol 178: 2171-2181.
34. McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, et al. (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.
35. Roberts ZJ, Goutagny N, Perera PY, Kato H, Kumar H, et al. (2007) The chemotherapeutic agent DMXAA potently and specifically activates the TBK1-IRF-3 signaling axis. J Exp Med 204: 1559-1569.
36. Mancuso G, Midiri A, Biondo C, Beninati C, Zummo S, et al. (2007) Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J Immunol 178: 3126-3133.
37. Leber JH, Crimmins GT, Raghavan S, Meyer-Morse N, Cox JS, et al. (2008) Distinct TLR- and NLR-mediated transcriptional responses to an intracellular pathogen. PLoS Pathog 4: e6. doi:10.1371/journal.ppat.0040006.
38. O'Riordan M, Yi CH, Gonzales R, Lee KD, Portnoy DA (2002) Innate recognition of bacteria by a macrophage cytosolic surveillance pathway. Proc Natl Acad Sci U S A 99: 13861-13866.
39. 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.
40. 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.
41. O'Connell RM, Saha SK, Vaidya SA, Bruhn KW, Miranda GA, et al. (2004) Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J Exp Med 200: 437-445.
42. Charrel-Dennis M, Latz E, Halmen KA, Trieu-Cuot P, Fitzgerald KA, et al. (2008) TLR-independent type I interferon induction in response to an extracellular bacterial pathogen via intracellular recognition of its DNA. Cell Host Microbe 4: 543-554.
43. Henry T, Brotcke A, Weiss DS, Thompson LJ, Monack DM (2007) Type I interferon signaling is required for activation of the inflammasome during Francisella infection. J Exp Med 204: 987-994.
44. Roux CM, Rolan HG, Santos RL, Beremand PD, Thomas TL, et al. (2007) Brucella requires a functional Type IV secretion system to elicit innate immune responses in mice. Cell Microbiol 9: 1851-1869.
45. Stanley SA, Johndrow JE, Manzanillo P, Cox JS (2007) The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 178: 3143-3152.
46. Vogel JP, Andrews HL, Wong SK, Isberg RR (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
47. Fredericksen BL, Keller BC, Fornek J, Katze MG, Gale M Jr (2008) Establishment and maintenance of the innate antiviral response to West Nile Virus involves both RIG-I and MDA5 signaling through IPS-1. J Virol 82: 609-616.
48. Jiang Z, Georgel P, Du X, Shamel L, Sovath S, et al. (2005) CD14 is required for MyD88-independent LPS signaling. Nat Immunol 6: 565-570.
49. Wu L, Pan J, Thoroddsen V, Wysong DR, Blackman RK, et al. (2003) Novel small-molecule inhibitors of RNA polymerase III. Eukaryot Cell 2: 256-264.
50. Mancuso G, Gambuzza M, Midiri A, Biondo C, Papasergi S, et al. (2009) Bacterial recognition by TLR7 in the lysosomes of conventional dendritic cells. Nat Immunol 10: 587-594.
51. Lippmann J, Rothenburg S, Deigendesch N, Eitel J, Meixenberger K, et al. (2008) IFNbeta responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1 (DLM-1/DAI). Cell Microbiol 10: 2579-2588.
52. Rad R, Ballhorn W, Voland P, Eisenacher K, Mages J, et al. (2009) Extracellular and intracellular pattern recognition receptors cooperate in the recognition of Helicobacter pylori. Gastroenterology 136: 2247-2257.
53. Ensminger AW, Isberg RR (2009) Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr Opin Microbiol 12: 67-73.
54. Malathi K, Dong B, Gale M Jr, Silverman RH (2007) Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 448: 816-819.
55. Crimmins GT, Herskovits AA, Rehder K, Sivick KE, Lauer P, et al. (2008) Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity. Proc Natl Acad Sci U S A 105: 10191-10196.
56. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, et al. (2006) Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci U S A 103: 8459-8464.
57. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, et al. (1994) Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
58. Li P, Allen H, Banerjee S, Franklin S, Herzog L, et al. (1995) Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80: 401-411.
59. Decker T, Lohmann-Matthes ML (1988) A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 115: 61-69.
60. Kwon YM, Ricke SC (2000) Efficient amplification of multiple transposon-flanking sequences. J Microbiol Methods 41: 195-199.