Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection

Journal of Experimental Medicine

Volumn 203, Issue 4, 2006, Pages 1093-1104

  Molofsky, Ari B ^a   Byrne, Brenda G ^a   Whitfield, Natalie N ^a   Madigan, Cressida A ^a,c   Fuse, Etsu T ^b   Tateda, Kazuhiro ^b   Swanson, Michele S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LISTERIOLYSIN; MONOMER; PROTEIN; PROTEIN NAIP5; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOSOL; ENZYME ACTIVITY; FEMALE; GENOTYPE PHENOTYPE CORRELATION; IMMUNE RESPONSE; INFLAMMATION; INNATE IMMUNITY; LEGIONELLA PNEUMOPHILA; LISTERIA MONOCYTOGENES; LUNG INFECTION; MACROPHAGE; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL TISSUE; IMMUNITY; MEMBRANE PERMEABILITY; MOLECULAR RECOGNITION; OLIGOMERIZATION; VIRULENCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; CELLS, CULTURED; CYTOSOL; FEMALE; FLAGELLIN; IMMUNITY, NATURAL; LEGIONELLA PNEUMOPHILA; MACROPHAGES; MICE; MICE, INBRED A; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NEURONAL APOPTOSIS-INHIBITORY PROTEIN; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

ANIMALIA; BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA; LISTERIA MONOCYTOGENES;

EID: 33645843633     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20051659     Document Type: Article

References (68)

1. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5:987-995.
2. Inohara, N., M. Chamaillard, C. McDonald, and G. Nunez. 2004. NOD-LRR Proteins: role in host-microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74:355-383.
3. Fortier, A., E. Diez, and P. Gros. 2005. Naip5/Birc1e and susceptibility to Legionella pneumophila. Trends Microbiol. 13:328-335.
4. Diez, E., S.H. Lee, S. Gauthier, Z. Yaraghi, M. Tremblay, S. Vidal, and P. Gros. 2003. Birc1e is the gene within the Lgn1 locus associated with resistance to Legionella pneumophila. Nat. Genet. 33:55-60.
5. Wright, E.K., S.A. Goodart, J.D. Growney, V. Hadinoto, M.G. Endrizzi, E.M. Long, K. Sadigh, A.L. Abney, I. Bernstein-Hanley, and W.F. Dietrich. 2003. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13:27-36.
6. Davoodi, J., L. Lin, J. Kelly, P. Liston, and A.E. MacKenzie. 2004. Neuronal apoptosis-inhibitory protein does not interact with Smac and requires ATP to bind caspase- 9. J. Biol. Chem. 279:40622-40628.
7. Maier, J.K., Z. Lahoua, N.H. Gendron, R. Fetni, A. Johnston, J. Davoodi, D. Rasper, S. Roy, R.S. Slack, D.W. Nicholson, and A.E. MacKenzie. 2002. The neuronal apoptosis inhibitory protein is a direct inhibitor of caspases 3 and 7. J. Neurosci. 22:2035-2043.
8. Martinon, F., and J. Tschopp. 2004. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell. 117:561-574.
9. Fink, S.L., and B.T. Cookson. 2005. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73:1907-1916.
10. Mariathasan, S., K. Newton, D.M. Monack, D. Vucic, D.M. French, W.P. Lee, M. Roose-Girma, S. Erickson, and V.M. Dixit. 2004. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature. 430:213-218.
11. Chen, Y., M.R. Smith, K. Thirumalai, and A. Zychlinsky. 1996. A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J. 15:3853-3860.
12. Brennan, M.A., and B.T. Cookson. 2000. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol. Microbiol. 38:31-40.
13. Suzuki, T., K. Nakanishi, H. Tsutsui, H. Iwai, S. Akira, N. Inohara, M. Chamaillard, G. Nunez, and C. Sasakawa. 2005. A novel caspase-1/toll-like receptor 4-independent pathway of cell death induced by cytosolic Shigella in infected macrophages. J. Biol. Chem. 280:14042-14050.
14. Zamboni, D.S., K.S. Kobayashi, T. Kohlsdorf, Y. Ogura, E.M. Long, R.E. Vance, K. Kuida, S. Mariathasan, V.M. Dixit, R.A. Flavell, W.F. Dietrich, and C.R. Roy. 2006. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 7:318-325.
15. Alli, O.A., L.Y. Gao, L.L. Pedersen, S. Zink, M. Radulic, M. Doric, and Y. Abu Kwaik. 2000. Temporal pore formation-mediated egress from macrophages and alveolar epithelial cells by Legionella pneumophila. Infect. Immun. 68:6431-6440.
16. Blackmon, J.A., M.D. Hicklin, and F.W. Chandler. 1978. Legionnaires' disease. Pathological and historical aspects of a 'new' disease. Arch. Pathol. Lab. Med. 102:337-343.
17. Brieland, J., P. Freeman, R. Kunkel, C. Chrisp, M. Hurley, J. Fantone, and C. Engleberg. 1994. Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J mice. A murine model of human Legionnaires' disease. Am. J. Pathol. 145:1537-1546.
18. Vogel, J.P., H.L. Andrews, S.K. Wong, and R.R. Isberg. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science. 279:873-876.
19. Kirby, J.E., J.P. Vogel, H.L. Andrews, and R.R. Isberg. 1998. Evidence of pore-forming ability by Legionella pneumophila. Mol. Microbiol. 27:323-336.
20. Molofsky, A.B., L.M. Shetron-Rama, and M.S. Swanson. 2005. Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect. Immun. 73:5720-5734.
21. Heuner, K., C. Dietrich, C. Skriwan, M. Steinert, and J. Hacker. 2002. Influence of the alternative sigma(28) factor on virulence and flagellum expression of Legionella pneumophila. Infect. Immun. 70:1604-1608.
22. Hawn, T.R., A. Verbon, K.D. Lettinga, L.P. Zhao, S.S. Li, R.J. Laws, S.J. Skerrett, B. Beutler, L. Schroeder, A. Nachman, 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.
23. Ricci, M.L., A. Torosantucci, M. Scaturro, P. Chiani, L. Baldassarri, and M.C. Pastoris. 2005. Induction of protective immunity by Legionella pneumophila flagellum in an A/J mouse model. Vaccine. 23:4811-4820.
24. Ramos, H.C., M. Rumbo, and J.C. Sirard. 2004. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12:509-517.
25. Hayashi, F., K.D. Smith, A. Ozinsky, T.R. Hawn, E.C. Yi, D.R. Goodlett, J.K. Eng, S. Akira, D.M. Underhill, and A. Aderem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature. 410:1099-1103.
26. Means, T.K., F. Hayashi, K.D. Smith, A. Aderem, and A.D. Luster. 2003. The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J. Immunol. 170:5165-5175.
27. Smith, K.D., E. Andersen-Nissen, F. Hayashi, K. Strobe, M.A. Bergman, S.L. Barrett, B.T. Cookson, and A. Aderem. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4:1247-1253.
28. Garcia-Calvo, M., E.P. Peterson, B. Leiting, R. Ruel, D.W. Nicholson, and N.A. Thornberry. 1998. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J. Biol. Chem. 273:32608-32613.
29. Muller, A., J. Hacker, and B. Brand. 1996. Evidence for apoptosis of human macrophage-like HL60 cells by Legionella pneumophila infection. Infect. Immun. 64:4900-4906.
30. Hagele, S., J. Hacker, and B. Brand. 1998. Legionella pneumophila kills human phagocytes but not protozoan host cells by inducing apoptotic cell death. FEMS Microbiol. Lett. 169:51-58.
31. Gao, L.Y., and Y. Abu Kwaik. 1999. Activation of caspase 3 during Legionella pneumophila-induced apoptosis. Infect. Immun. 67:4886-4894.
32. Neumeister, B., M. Faigle, K. Lauber, H. Northoff, and S. Wesselborg. 2002. Legionella pneumophila induces apoptosis via the mitochondrial death pathway. Microbiology. 148:3639-3650.
33. Zink, S.D., L. Pedersen, N.P. Cianciotto, and Y. Abu-Kwaik. 2002. The Dot/Icm type IV secretion system of Legionella pneumophila is essential for the induction of apoptosis in human macrophages. Infect. Immun. 70:1657-1663.
34. Molmeret, M., S.D. Zink, L. Han, A. Abu-Zant, R. Asari, D.M. Bitar, and Y. Abu Kwaik. 2004. Activation of caspase-3 by the Dot/Icm virulence system is essential for arrested biogenesis of the Legionella-containing phagosome. Cell. Microbiol. 6:33-48.
35. Abu-Zant, A., M. Santic, M. Molmeret, S. Jones, J. Helbig, and Y. Abu Kwaik. 2005. Incomplete activation of macrophage apoptosis during intracellular replication of Legionella pneumophila. Infect. Immun. 73:5339-5349.
36. Derre, I., and R.R. Isberg. 2004. Macrophages from mice with the restrictive Lgn1 allele exhibit multifactorial resistance to Legionella pneumophila. Infect. Immun. 72:6221-6229.
37. Sturgill-Koszycki, S., and M.S. Swanson. 2000. Legionella pneumophila replication vacuoles mature into acidic, endocytic organelles. J. Exp. Med. 192:1261-1272.
38. Martinon, F., K. Burns, and J. Tschopp. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol. Cell. 10:417-426.
39. Sexton, J.A., and J.P. Vogel. 2002. Type IVB secretion by intracellular pathogens. Traffic. 3:178-185.
40. Damiano, J.S., V. Oliveira, K. Welsh, and J.C. Reed. 2004. Heterotypic interactions among NACHT domains: implications for regulation of innate immune responses. Biochem. J. 381:213-219.
41. Mariathasan, S., D.S. Weiss, V.M. Dixit, and D.M. Monack. 2005. Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202:1043-1049.
42. Mariathasan, S., D.S. Weiss, K. Newton, J. McBride, K. O'Rourke, M. Roose-Girma, W.P. Lee, Y. Weinrauch, D.M. Monack, and V.M. Dixit. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 440:228-232.
43. Martinon, F., L. Agostini, E. Meylan, and J. Tschopp. 2004. Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr. Biol. 14:1929-1934.
44. Kanneganti, T.D., N. Ozoren, M. Body-Malapel, A. Amer, J.H. Park, L. Franchi, J. Whitfield, W. Barchet, M. Colonna, P. Vandenabeele, J. Bertin, A. Coyle, et al. 2006. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp 3. Nature. 440:233-236.
45. Damiano, J.S., R.M. Newman, and J.C. Reed. 2004. Multiple roles of CLAN (caspase-associated recruitment domain, leucine-rich repeat, and NAIP CIIA HET-E, and TP1-containing protein) in the mammalian innate immune response. J. Immunol. 173:6338-6345.
46. Bardill, J.P., J.L. Miller, and J.P. Vogel. 2005. IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol. 56:90-103.
47. Nagai, H., E.D. Cambronne, J.C. Kagan, J.C. Amor, R.A. Kahn, and C.R. Roy. 2005. A C-terminal translocation signal required for Dot/ Icm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. USA. 102:826-831.
48. Viala, J., C. Chaput, I.G. Boneca, A. Cardona, S.E. Girardin, A.P. Moran, R. Athman, S. Memet, M.R. Huerre, A.J. Coyle, et al. 2004. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5:1166-1174.
49. Bergman, M.A., L.A. Cummings, S.L. Barrett, K.D. Smith, J.C. Lara, A. Aderem, and B.T. Cookson. 2005. CD4+ T cells and toll-like receptors recognize Salmonella antigens expressed in bacterial surface organelles. Infect. Immun. 73:1350-1356.
50. Grundling, A., L.S. Burrack, H.G. Bouwer, and D.E. Higgins. 2004. Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc. Natl. Acad. Sci. USA. 101:12318-12323.
51. Andersen-Nissen, E., K.D. Smith, K.L. Strobe, S.L. Barrett, B.T. Cookson, S.M. Logan, and A. Aderem. 2005. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. USA. 102:9247-9252.
52. Molofsky, A.B., and M.S. Swanson. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40.
53. Amer, A.O., and M.S. Swanson. 2005. Autophagy is an immediate macrophage response to Legionella pneumophila. Cell. Microbiol. 7:765-778.
54. Kirkegaard, K., M.P. Taylor, and W.T. Jackson. 2004. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat. Rev. Microbiol. 2:301-314.
55. Debnath, J., E. Baehrecke, and G. Kroemer. 2005. Does autophagy contribute to cell death? Autophagy. 1:66-74.
56. Swanson, M.S., and A.B. Molofsky. 2005. Autophagy and inflammatory cell death, partners of innate immunity. Autophagy. 1:174-176.
57. Molofsky, A.B., and M.S. Swanson. 2003. Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol. Microbiol. 50:445-461.
58. Byrne, B., and M.S. Swanson. 1998. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect. Immun. 66:3029-3034.
59. Mandal, M., and K.D. Lee. 2002. Listeriolysin O-liposome-mediated cytosolic delivery of macromolecule antigen in vivo: enhancement of antigen-specific cytotoxic T lymphocyte frequency, activity, and tumor protection. Biochim. Biophys. Acta. 1563:7-17.
60. Herzyk, D.J., A.E. Berger, J.N. Allen, and M.D. Wewers. 1992. Sandwich ELISA formats designed to detect 17 kDa IL-1 beta significantly underestimate 35 kDa IL-1 beta. J. Immunol. Methods. 148:243-254.
61. Dinarello, C.A. 1992. ELISA kits based on monoclonal antibodies do not measure total IL-1 beta synthesis. J. Immunol. Methods. 148:255-259.
62. Tateda, K., T.A. Moore, J.C. Deng, M.W. Newstead, X. Zeng, A. Matsukawa, M.S. Swanson, K. Yamaguchi, and T.J. Standiford. 2001. Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia. J. Immunol. 166:3355-3361.
63. Bishop, D.K., and D.J. Hinrichs. 1987. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J. Immunol. 139:2005-2009.
64. Jones, S., and D. Portnoy. 1994. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect. Immun. 62:5608-5613.
65. Hammer, B.K., E.S. Tateda, and M.S. Swanson. 2002. A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol. Microbiol. 44:107-118.
66. Hammer, B.K., and M.S. Swanson. 1999. Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 33:721-731.
67. Merriam, J.J., R. Mathur, R. Maxfield-Boumil, and R.R. Isberg. 1997. Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis. Infect. Immun. 65:2497-2501.
68. Berger, K.H., and R.R. Isberg. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7:7-19.