Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity

PLoS Pathogens

Volumn 2, Issue 3, 2006, Pages 0175-0183

  Ren, Tao ^a   Zamboni, Dario S ^b   Roy, Craig R ^b   Dietrich, William F ^a   Vance, Russell E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; INTERLEUKIN 1BETA CONVERTING ENZYME; MYELOID DIFFERENTIATION FACTOR 88; NAIP 5 PROTEIN; PROTEIN; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG; BIRC1E PROTEIN, MOUSE; NEURONAL APOPTOSIS INHIBITORY PROTEIN;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL MOTILITY; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; ESCHERICHIA COLI; FLAGELLUM; INNATE IMMUNITY; LEGIONELLA; LEGIONELLA PNEUMOPHILA; MACROPHAGE; MOUSE; MOUSE STRAIN; NONHUMAN; PROTEIN EXPRESSION; SALMONELLA; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IMMUNITY; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; MUTATION; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LEGIONELLA; LEGIONELLA PNEUMOPHILA; SALMONELLA;

ANIMALS; CASPASE 1; CELL DEATH; CYTOTOXICITY, IMMUNOLOGIC; FLAGELLIN; GENOTYPE; IMMUNITY; LEGIONELLA; MACROPHAGES; MICE; MICE, KNOCKOUT; MUTATION; NEURONAL APOPTOSIS-INHIBITORY PROTEIN; SALMONELLA; TOLL-LIKE RECEPTOR 5;

EID: 33645791082     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0020018     Document Type: Article

References (51)

1. Fields BS, Benson RF, Besser RE (2002) Legionella and Legionnaires' disease: 25 Years of investigation. Clin Microbiol Rev 15: 506-526.
2. Segal G, Purcell M, Shuman HA (1998) Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci U S A 95: 1669-1674.
3. Vogel JP, Andrews HL, Wong SK, Isberg RR (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
4. Luo ZQ, Isberg RR (2004) Multiple substrates of the Legionella pneumophila dot/icm system identified by interbacterial protein transfer. Proc Natl Acad Sci U S A 101: 841-846.
5. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295: 679-682.
6. Horwitz MA (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
7. Marra A, Blander SJ, Horwitz MA, Shuman HA (1992) Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci U S A 89: 9607-9611.
8. Yamamoto Y, Klein TW, Newton CA, Widen R, Friedman H (1988) Growth of Legionella pneumophila in thioglycolate-elicited peritoneal macrophages from A/J mice. Infect Immun 56: 370-375.
9. Diez E, Lee SH, Gauthier S, Yaraghi Z, Tremblay M, et al. (2003) Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat Genet 33: 55-60.
10. Wright EK, Goodart SA, Growney JD, Hadinoto V, Endrizzi MG, et al. (2003) Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr Biol 13: 27-36.
11. Inohara N, Chamaillard M, McDonald C, Nunez G (2004) NOD-LRR proteins: Role in host-microbial interactions and inflammatory disease. Annu Rev Biochem. E-pub 19 November 2004.
12. Ting JP, Davis BK (2005) CATERPILLER: A novel gene family important in immunity, cell death, and diseases. Annu Rev Immunol 23: 387-414.
13. Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, et al. (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4: 702-707.
14. Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jehanno M, et al. (2003) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300: 1584-1587.
15. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, et al. (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869-8872.
16. Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, et al. (2003) Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J Biol Chem 278: 5509-5512.
17. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, et al. (2005) Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307: 731-734.
18. Martinon F, Agostini L, Meylan E, Tschopp J (2004) Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr Biol 14: 1929-1934.
19. Boyden E, Dietrich WF (2006) Nature Genetics. Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat Genet 38: 240-244.
20. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, et al. (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213-218.
21. Heuner K, Steinert M (2003) The flagellum of Legionella pneumophila and its link to the expression of the virulent phenotype. Int J Med Microbiol 293: 133-143.
22. Merriam JJ, Mathur R, Maxfield-Boumil R, Isberg RR (1997) Analysis of the Legionella pneumophila fliI gene: Intracellular growth of a defined mutant defective for flagellum biosynthesis. Infect Immun 65: 2497-2501.
23. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by toll-like receptor 5. Nature 410: 1099-1103.
24. Hawn TR, Verbon A, Lettinga KD, Zhao LP, Li SS, et al. (2003) A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease. J Exp Med 198: 1563-1572.
25. Means TK, Hayashi F, Smith KD, Aderem A, Luster AD (2003) The toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol 170: 5165-5175.
26. 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.
27. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, et al. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267: 2000-2003.
28. 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.
29. Brennan MA, Cookson BT (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31-40.
30. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, et al. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96: 2396-2401.
31. Chen Y, Smith MR, Thirumalai K, Zychlinsky A (1996) A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J 15: 3853-3860.
32. Cookson BT, Brennan MA (2001) Pro-inflammatory programmed cell death. Trends Microbiol 9: 113-114.
33. Molofsky AB, Shetron-Rama LM, Swanson MS (2005) Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect Immun 73: 5720-5734.
34. Eichelberg K, Galan JE (2000) The flagellar sigma factor FliA (sigma(28)) regulates the expression of Salmonella genes associated with the centisome 63 type III secretion system. Infect Immun 68: 2735-2743.
35. Kirby JE, Isberg RR (1998) Legionnaires' disease: The pore macrophage and the legion of terror within. Trends Microbiol 6: 256-258.
36. Kirby JE, Vogel JP, Andrews HL, Isberg RR (1998) Evidence for pore-forming ability by Legionella pneumophila. Mol Microbiol 27: 323-336.
37. Viala J, Chaput C, Boneca IG, Cardona A, Girardin SE, et al. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5: 1166-1174.
38. Wadsworth SJ, Goldfine H (1999) Listeria monocytogenes phospholipase C-dependent calcium signaling modulates bacterial entry into J774 macrophage-like cells. Infect Immun 67: 1770-1778.
39. Coers J, Monahan C, Roy CR (1999) Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nat Cell Biol 1: 451-453.
40. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, et al. (2005) A C-terminal translocation signal required for dot/icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci U S A 102: 826-831.
41. Higgins DE, Shastri N, Portnoy DA (1999) Delivery of protein to the cytosol of macrophages using Escherichia coli K-12. Mol Microbiol 31: 1631-1641.
42. Sansonetti PJ, Phalipon A, Arondel J, Thirumalai K, Banerjee S, et al. (2000) Caspase-1 activation of IL-1beta and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12: 581-590.
43. Monack DM, Hersh D, Ghori N, Bouley D, Zychlinsky A, et al. (2000) Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med 192: 249-258.
44. Swanson MS, Fernandez-Moreira E (2002) A microbial strategy to multiply in macrophages: The pregnant pause. Traffic 3: 170-177.
45. Molofsky AB, Swanson MS (2004) Differentiate to thrive: Lessons from the Legionella pneumophila life cycle. Mol Microbiol 53: 29-40.
46. Derre I, Isberg RR (2004) Macrophages from mice with the restrictive Lgn1 allele exhibit multifactorial resistance to Legionella pneumophila. Infect Immun 72: 6221-6229.
47. Martinon F, Burns K, Tschopp J (2002) The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417-426.
48. Hueffer K, Galan JE (2004) Salmonella-induced macrophage death: Multiple mechanisms, different outcomes. Cell Microbiol 6: 1019-1025.
49. Chien M, Morozova I, Shi S, Sheng H, Chen J, et al. (2004) The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305: 1966-1968.
50. Rankin S, Li Z, Isberg RR (2002) Macrophage-induced genes of Legionella pneumophila: Protection from reactive intermediates and solute imbalance during intracellular growth. Infect Immun 70: 3637-3648.
51. Bates D, Epstein J, Boye E, Fahrner K, Berg H, et al. (2005) The Escherichia coli baby cell column: A novel cell synchronization method provides new insight into the bacterial cell cycle. Mol Microbiol 57: 380-391.