Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Fontana, Mary F ^a   Banga, Simran ^b   Barry, Kevin C ^a   Shen, Xihui ^b   Tan, Yunhao ^b   Luo, Zhao Qing ^b   Vance, Russell E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; COLONY STIMULATING FACTOR; COLONY STIMULATING FACTOR 2; DOT PROTEIN; I KAPPA B; ICM PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 23P19; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHAPERONE; DOTA PROTEIN, LEGIONELLA PNEUMOPHILA; ICMS PROTEIN, LEGIONELLA PNEUMOPHILA; MEMBRANE PROTEIN; TRANSCRIPTION FACTOR; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL IMMUNITY; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; ENZYME INACTIVATION; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS INHIBITION; RECEPTOR UPREGULATION; TYPE IV SECRETION SYSTEM; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SECRETION; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA;

ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; CELLS, CULTURED; HOST-PATHOGEN INTERACTIONS; I-KAPPA B PROTEINS; IMMUNITY, INNATE; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR CHAPERONES; MUTATION; NF-KAPPA B; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTORS; VIRULENCE FACTORS;

EID: 79952203418     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001289     Document Type: Article

References (39)

1. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
2. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R, (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
3. Vance RE, Isberg RR, Portnoy DA, (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6: 10-21.
4. Medzhitov R, (2010) Innate immunity: quo vadis? Nat Immunol 11: 551-553.
5. Chisholm ST, Coaker G, Day B, Staskawicz BJ, (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
6. Fields BS, Benson RF, Besser RE, (2002) Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 15: 506-526.
7. Horwitz MA, Silverstein SC, (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest 66: 441-450.
8. Archer KA, Ader F, Kobayashi KS, Flavell RA, Roy CR, (2010) Cooperation between multiple microbial pattern recognition systems is important for host protection against the intracellular pathogen Legionella pneumophila. Infect Immun 78: 2477-2487.
9. Vance RE, (2010) Immunology taught by bacteria. J Clin Immunol 30: 507-511.
10. 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.
11. 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.
12. 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.
13. Monroe KM, McWhirter SM, Vance RE, (2009) Identification of host cytosolic sensors and bacterial factors regulating the type I interferon response to Legionella pneumophila. PLoS Pathog 5: e1000665.
14. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE, (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18.
15. Stetson DB, Medzhitov R, (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24: 93-103.
16. 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.
17. 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.
18. Stetson DB, Medzhitov R, (2006) Type I interferons in host defense. Immunity 25: 373-381.
19. Kastelein RA, Hunter CA, Cua DJ, (2007) Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu Rev Immunol 25: 221-242.
20. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, et al. (2008) Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 9: 1171-1178.
21. 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.
22. Wong WL, Brostrom MA, Kuznetsov G, Gmitter-Yellen D, Brostrom CO, (1993) Inhibition of protein synthesis and early protein processing by thapsigargin in cultured cells. Biochem J 289: 71-79.
23. Belyi Y, Tabakova I, Stahl M, Aktories K, (2008) Lgt: a family of cytotoxic glucosyltransferases produced by Legionella pneumophila. J Bacteriol 190: 3026-3035.
24. Shen X, Banga S, Liu Y, Xu L, Gao P, et al. (2009) Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response. Cell Microbiol 11: 911-926.
25. Belyi Y, Niggeweg R, Opitz B, Vogelsgesang M, Hippenstiel S, et al. (2006) Legionella pneumophila glucosyltransferase inhibits host elongation factor 1A. Proc Natl Acad Sci U S A 103: 16953-16958.
26. McCusker KT, Braaten BA, Cho MW, Low DA, (1991) Legionella pneumophila inhibits protein synthesis in Chinese hamster ovary cells. Infect Immun 59: 240-246.
27. Youngner JS, Stinebring WR, Taube SE, (1965) Influence of inhibitors of protein synthesis on interferon formation in mice. Virology 27: 541-550.
28. Carmody RJ, Ruan Q, Liou HC, Chen YH, (2007) Essential roles of c-Rel in TLR-induced IL-23 p19 gene expression in dendritic cells. J Immunol 178: 186-191.
29. Coornaert B, Carpentier I, Beyaert R, (2009) A20: central gatekeeper in inflammation and immunity. J Biol Chem 284: 8217-8221.
30. Hershko DD, Robb BW, Wray CJ, Luo GJ, Hasselgren PO, (2004) Superinduction of IL-6 by cycloheximide is associated with mRNA stabilization and sustained activation of p38 map kinase and NF-kappaB in cultured caco-2 cells. J Cell Biochem 91: 951-961.
31. Thorpe CM, Smith WE, Hurley BP, Acheson DW, (2001) Shiga toxins induce, superinduce, and stabilize a variety of C-X-C chemokine mRNAs in intestinal epithelial cells, resulting in increased chemokine expression. Infect Immun 69: 6140-6147.
32. Ichinohe T, Pang IK, Iwasaki A, (2010) Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol 11: 404-410.
33. Bruno VM, Hannemann S, Lara-Tejero M, Flavell RA, Kleinstein SH, et al. (2009) Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog 5: e1000538.
34. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, et al. (2009) A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 138: 114-128.
35. Hargreaves DC, Horng T, Medzhitov R, (2009) Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138: 129-145.
36. Dubin PJ, Kolls JK, (2007) IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol 292: L519-528.
37. Langrish CL, McKenzie BS, Wilson NJ, de Waal Malefyt R, Kastelein RA, et al. (2004) IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev 202: 96-105.
38. 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.
39. Krantz BA, Melnyk RA, Zhang S, Juris SJ, Lacy DB, et al. (2005) A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309: 777-781.