Restriction of Legionella pneumophila replication in macrophages requires concerted action of the transcriptional regulators Irf1 and Irf8 and Nod-like receptors Naip5 and Nlrc4

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 4794-4805

  Fortier, Anne ^a   Doiron, Karine ^a   Saleh, Maya ^a   Grinstein, Sergio ^b   Gros, Philippe ^a  

^a MCGILL UNIVERSITY   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; PROTEIN NAIP5; PROTEIN NLRC4; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; GENE INTERACTION; GENE REPRESSION; HETEROZYGOSITY; INFECTION SENSITIVITY; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; LOSS OF FUNCTION MUTATION; MACROPHAGE; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, NORTHERN; CALCIUM-BINDING PROTEINS; FLAGELLIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PARASITE INTERACTIONS; INTERFERON REGULATORY FACTOR-1; INTERFERON REGULATORY FACTORS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MICE; MICE, TRANSGENIC; NEURONAL APOPTOSIS-INHIBITORY PROTEIN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHAGOSOMES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 70350454786     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01546-08     Document Type: Article

References (57)

1. Amer, A., L. Franchi, T. D. Kanneganti, M. Body-Malapel, N. Ozoren, G. Brady, S. Meshinchi, R. Jagirdar, A. Gewirtz, S. Akira, and G. Nunez. 2006. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281:35217-35223.
2. Berger, K. H., J. J. Merriam, and R. R. Isberg. 1994. Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol. Microbiol. 14:809-822.
3. Case, C. L., S. Shin, and C. R. Roy. 2009. Asc and Ipaf inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect. Immun. 77:1981-1991.
4. Clemens, D. L., and M. A. Horwitz. 1995. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181:257-270.
5. Coers, J., R. E. Vance, M. F. Fontana, and W. F. Dietrich. 2007. Restriction of Legionella pneumophila growth in macrophages requires the concerted action of cytokine and Naip5/Ipaf signalling pathways. Cell. Microbiol. 9:2344-2357.
6. 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.
7. Diez, E., M. C. Beckers, E. Ernst, C. J. DiDonato, L. R. Simard, C. Morissette, F. Gervais, S. I. Yoshida, and P. Gros. 1997. Genetic and physical mapping of the mouse host resistance locus Lgn1. Mamm. Genome 8:682-685. (Pubitemid 28060619)
8. 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.
9. Fortier, A., C. de Chastellier, S. Balor, and P. Gros. 2007. Birc1e/Naip5 rapidly antagonizes modulation of phagosome maturation by Legionella pneumophila. Cell. Microbiol. 9:910-923.
10. Fortier, A., E. Diez, and P. Gros. 2005. Naip5/Birc1e and susceptibility to Legionella pneumophila. Trends Microbiol. 13:328-335.
11. Franchi, L., A. Amer, M. Body-Malapel, T. D. Kanneganti, N. Ozoren, R. Jagirdar, N. Inohara, P. Vandenabeele, J. Bertin, A. Coyle, E. P. Grant, and G. Nunez. 2006. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat. Immunol. 7:576-582.
12. Franchi, L., J. H. Park, M. H. Shaw, N. Marina-Garcia, G. Chen, Y. G. Kim, and G. Nunez. 2008. Intracellular NOD-like receptors in innate immunity, infection and disease. Cell. Microbiol. 10:1-8.
13. Franchi, L., J. Stoolman, T. D. Kanneganti, A. Verma, R. Ramphal, and G. Nunez. 2007. Critical role for Ipaf in Pseudomonas aeruginosa-induced caspase-1 activation. Eur. J. Immunol. 37:3030-3039.
14. Fraser, D. W., T. R. Tsai, W. Orenstein, W. E. Parkin, H. J. Beecham, R. G. Sharrar, J. Harris, G. F. Mallison, S. M. Martin, J. E. McDade, C. C. Shepard, and P. S. Brachman. 1977. Legionnaires' disease: description of an epidemic of pneumonia. N. Engl. J. Med. 297:1189-1197.
15. Geddes, B. J., L. Wang, W. J. Huang, M. Lavellee, G. A. Manji, M. Brown, M. Jurman, J. Cao, J. Morgenstern, S. Merriam, M. A. Glucksmann, P. S. DiStefano, and J. Bertin. 2001. Human CARD12 is a novel CED4/Apaf-1 family member that induces apoptosis. Biochem. Biophys. Res. Commun. 284:77-82.
16. Growney, J. D., and W. F. Dietrich. 2000. High-resolution genetic and physical map of the Lgn1 interval in C57BL/6J implicates Naip2 or Naip5 in Legionella pneumophila pathogenesis. Genome Res. 10:1158-1171.
17. Hackam, D. J., O. D. Rotstein, W. Zhang, S. Gruenheid, P. Gros, and S. Grinstein. 1998. Host resistance to intracellular infection: mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification. J. Exp. Med. 188:351-364.
18. Holtschke, T., J. Lohler, Y. Kanno, T. Fehr, N. Giese, F. Rosenbauer, J. Lou, K. P. Knobeloch, L. Gabriele, J. F. Waring, M. F. Bachmann, R. M. Zinkernagel, H. C. Morse III, K. Ozato, and I. Horak. 1996. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 87:307-317.
19. Horwitz, M. A. 1983. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158:2108-2126.
20. Kaufmann, A. F., J. E. McDade, C. M. Patton, J. V. Bennett, P. Skaliy, J. C. Feeley, D. C. Anderson, M. E. Potter, V. F. Newhouse, M. B. Gregg, and P. S. Brachman. 1981. Pontiac fever: isolation of the etiologic agent (Legionella pneumophilia) and demonstration of its mode of transmission. Am. J. Epidemiol. 114:337-347.
21. Lamkanfi, M., A. Amer, T. D. Kanneganti, R. Munoz-Planillo, G. Chen, P. Vandenabeele, A. Fortier, P. Gros, and G. Nunez. 2007. The Nod-like receptor family member Naip5/Birc1e restricts Legionella pneumophila growth independently of caspase-1 activation. J. Immunol. 178:8022-8027. (Pubitemid 46898073)
22. Lightfield, K. L., J. Persson, S. W. Brubaker, C. E. Witte, J. von Moltke, E. A. Dunipace, T. Henry, Y. H. Sun, D. Cado, W. F. Dietrich, D. M. Monack, R. M. Tsolis, and R. E. Vance. 2008. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 9:1171-1178.
23. MacMicking, J. D. 2005. Immune control of phagosomal bacteria by p47 GTPases. Curr. Opin. Microbiol. 8:74-82.
24. 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. (Pubitemid 38902430)
25. Marquis, J. F., A. Nantel, R. LaCourse, L. Ryan, R. J. North, and P. Gros. 2008. Fibrotic response as a distinguishing feature of resistance and susceptibility to pulmonary infection with Mycobacterium tuberculosis in mice. Infect. Immun. 76:78-88.
26. Martinon, F., and J. Tschopp. 2007. Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ. 14:10-22. (Pubitemid 44911890)
27. Martinon, F., and J. Tschopp. 2004. Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117: 561-574. (Pubitemid 38692523)
28. Masumi, A., S. Tamaoki, I. M. Wang, K. Ozato, and K. Komuro. 2002. IRF-8/ICSBP and IRF-1 cooperatively stimulate mouse IL-12 promoter activity in macrophages. FEBS Lett. 531:348-353. (Pubitemid 35341222)
29. McDade, J. E., C. C. Shepard, D. W. Fraser, T. R. Tsai, M. A. Redus, and W. R. Dowdle. 1977. Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N. Engl. J. Med. 297:1197-1203.
30. Miao, E. A., C. M. Alpuche-Aranda, M. Dors, A. E. Clark, M. W. Bader, S. I. Miller, and A. Aderem. 2006. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7:569-575.
31. Miao, E. A., R. K. Ernst, M. Dors, D. P. Mao, and A. Aderem. 2008. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. USA 105:2562-2567.
32. Molofsky, A. B., B. G. Byrne, N. N. Whitfield, C. A. Madigan, E. T. Fuse, K. Tateda, and M. S. Swanson. 2006. Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 203: 1093-1104.
33. Ninio, S., and C. R. Roy. 2007. Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol. 15:372-380. (Pubitemid 47126854)
34. Ogura, Y., D. K. Bonen, N. Inohara, D. L. Nicolae, F. F. Chen, R. Ramos, H. Britton, T. Moran, R. Karaliuskas, R. H. Duerr, J. P. Achkar, S. R. Brant, T. M. Bayless, B. S. Kirschner, S. B. Hanauer, G. Nunez, and J. H. Cho. 2001. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411:603-606.
35. Ogura, Y., F. S. Sutterwala, and R. A. Flavell. 2006. The inflammasome: first line of the immune response to cell stress. Cell 126:659-662. (Pubitemid 44233635)
36. Opitz, B., M. Vinzing, V. van Laak, B. Schmeck, G. Heine, S. Gunther, R. Preissner, H. Slevogt, P. D. N'Guessan, J. Eitel, T. Goldmann, A. Flieger, N. Suttorp, and S. Hippenstiel. 2006. Legionella pneumophila induces IFNbeta in lung epithelial cells via IPS-1 and IRF3, which also control bacterial replication. J. Biol. Chem. 281:36173-36179.
37. Ren, T., D. S. Zamboni, C. R. Roy, W. F. Dietrich, and R. E. Vance. 2006. Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2:e18.
38. Robinson, C. G., and C. R. Roy. 2006. Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila. Cell. Microbiol. 8:793-805.
39. Roy, C. R., K. H. Berger, and R. R. Isberg. 1998. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28:663-674.
40. Segal, G., and H. A. Shuman. 1998. How is the intracellular fate of the Legionella pneumophila phagosome determined? Trends Microbiol. 6:253-255.
41. Sirard, J. C., C. Vignal, R. Dessein, and M. Chamaillard. 2007. Nod-like receptors: cytosolic watchdogs for immunity against pathogens. PLoS Pathog. 3:e152.
42. Sturgill-Koszycki, S., and M. S. Swanson. 2000. Legionella pneumophila replication vacuoles mature into acidic, endocytic organelles. J. Exp. Med. 192:1261-1272.
43. Sutterwala, F. S., and R. A. Flavell. 2009. NLRC4/IPAF: a CARD carrying member of the NLR family. Clin. Immunol. 130:2-6.
44. Suzuki, T., L. Franchi, C. Toma, H. Ashida, M. Ogawa, Y. Yoshikawa, H. Mimuro, N. Inohara, C. Sasakawa, and G. Nunez. 2007. Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog. 3:e111.
45. Tamura, T., H. Yanai, D. Savitsky, and T. Taniguchi. 2008. The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 26:535-584.
46. Tilney, L. G., O. S. Harb, P. S. Connelly, C. G. Robinson, and C. R. Roy. 2001. How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J. Cell Sci. 114:4637-4650.
47. Ting, J. P., R. C. Lovering, E. S. Alnemri, J. Bertin, J. M. Boss, B. K. Davis, R. A. Flavell, S. E. Girardin, A. Godzik, J. A. Harton, H. M. Hoffman, J. P. Hugot, N. Inohara, A. Mackenzie, L. J. Maltais, G. Nunez, Y. Ogura, L. A. Otten, D. Philpott, J. C. Reed, W. Reith, S. Schreiber, V. Steimle, and P. A. Ward. 2008. The NLR gene family: a standard nomenclature. Immunity 28:285-287.
48. Tschopp, J., F. Martinon, and K. Burns. 2003. NALPs: a novel protein family involved in inflammation. Nat. Rev. Mol. Cell Biol. 4:95-104.
49. Turcotte, K., S. Gauthier, L. M. Mitsos, C. Shustik, N. G. Copeland, N. A. Jenkins, J. C. Fournet, P. Jolicoeur, and P. Gros. 2004. Genetic control of myeloproliferation in BXH-2 mice. Blood 103:2343-2350. (Pubitemid 38326256)
50. Turcotte, K., S. Gauthier, A. Tuite, A. Mullick, D. Malo, and P. Gros. 2005. A mutation in the Icsbp1 gene causes susceptibility to infection and a chronic myeloid leukemia-like syndrome in BXH-2 mice. J. Exp. Med. 201:881-890.
51. Vila-del Sol, V., C. Punzon, and M. Fresno. 2008. IFN-gamma-induced TNF-alpha expression is regulated by interferon regulatory factors 1 and 8 in mouse macrophages. J. Immunol. 181:4461-4470.
52. Vinzing, M., J. Eitel, J. Lippmann, A. C. Hocke, J. Zahlten, H. Slevogt, D. N'Guessan, P., S. Gunther, B. Schmeck, S. Hippenstiel, A. Flieger, N. Suttorp, and B. Opitz. 2008. NAIP and Ipaf control Legionella pneumophila replication in human cells. J. Immunol. 180:6808-6815.
53. 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. (Pubitemid 28106283)
54. 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.
55. Yamamoto, Y., T. W. Klein, C. A. Newton, R. Widen, and H. Friedman. 1988. Growth of Legionella pneumophila in thioglycolate-elicited peritoneal macrophages from A/J. mice. Infect. Immun. 56:370-375.
56. Yoshida, S., Y. Goto, Y. Mizuguchi, K. Nomoto, and E. Skamene. 1991. Genetic control of natural resistance in mouse macrophages regulating intracellular Legionella pneumophila multiplication in vitro. Infect. Immun. 59:428-432.
57. 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.