Dependency of caspase-1 activation induced in macrophages by listeria monocytogenes on cytolysin, listeriolysin o after evasion from phagosome into the cytoplasm

Journal of Immunology

Volumn 180, Issue 12, 2008, Pages 7859-7868

  Hara, Hideki ^a   Tsuchiya, Kohsuke ^a   Nomura, Takamasa ^a   Kawamura, Ikuo ^a   Shoma, Shereen ^a   Mitsuyama, Masao ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLYSIN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 1BETA CONVERTING ENZYME; IVANOLYSIN; LISTERIOLYSIN O; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; BACTERIAL TOXIN; HEAT SHOCK PROTEIN; HEMOLYSIN; HLYA PROTEIN, LISTERIA MONOCYTOGENES;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; HOST PATHOGEN INTERACTION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL DEATH; CYTOPLASM; ENZYMOLOGY; FEMALE; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOGENICITY; PERITONEUM MACROPHAGE; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; BACTERIAL TOXINS; CASPASE 1; CELL DEATH; CELLS, CULTURED; CYTOPLASM; ENZYME ACTIVATION; FEMALE; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; INTERFERON TYPE II; INTERLEUKIN-12; INTERLEUKIN-18; LISTERIA MONOCYTOGENES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHAGOSOMES; PROTEIN TRANSPORT;

EID: 50949083791     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.12.7859     Document Type: Article

References (50)

1. Schuchat, A., B. Swaminathan, and C. V. Broomc. 1991. Epidemiology of human Iisteriosis. Clin. Microbiol. Rev. 4: 169-183.
2. Mocci, S., S. A. Dalrymple, R. Nishinakamura, and R. Murray. 1997. The cy-tokine stew and innate resistance to L. monocytogenes. Immuno.l Rev. 158: 107-114.
3. Cousens, L. P., and E. J. Wing. 2000. Innate defenses in the liver during Listeria infection. Immunol. Rev. 174: 150-159.
4. Edelson, B. T., and E. R. Unanue. 2000. Immunity to Listeria infection. Curr. Opin. Immunol 12: 425-431.
5. Cossart, P., M. F. Vicente, J. Mengaud, F. Baquero, J. C. Perez-Diaz, and P. Berche. 1989. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect. Immun. 57: 3629-3636.
6. Marquis, H., H. G. Bouwer, D. J. Hinrichs, and D. A. Portnoy. 1993. Intracyto-plasmic growth and virulence of Listeria monocytogenes auxotrophic mutants. Infect. Immun. 61: 3756-3760.
7. Portnoy, D. A., P. S. Jacks, and D. J. Hinrichs. 1988. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J. Exp. Med. 167: 1459-1471.
8. Thale, C., and A. F. Kiderlen. 2005. Sources of interferon-γ (IFN-γ) in early immune response to Listeria monocytogenes. Immunobiology 210: 673-683.
9. Plitas, G., U. I. Chaudhry, T. P. Kingham, J. R. Raab, and R. P. DeMatteo. 2007. NK dendritic cells are innate immune responders to Listeria monocytogenes infection: J. Immunol. 178: 4411-4416.
10. Yang, J., I. Kawamura, and M. Mitsuyama. 1997. Requirement of the initial production of 7 interferon in the generation of protective immunity of mice against Listeria monocytogenes. Infect. Immun. 65: 72-77.
11. Hara, H., I. Kawamura, T. Nomura, T. Tominaga, K. Tsuchiya, and M. Mitsuyama. 2007. Cytolysin-dependent escape of the bacterium from the phagosome is required but not sufficient for induction of the Thl immune respons'e against Listeria monocytogenes infection: distinct role of listeriolysin O determined by cytolysin gene replacement. Infect. Immun. 75: 3791-3801.
12. Tanabe, Y., H. Xiong, T. Nomura, M. Arakawa, and M. Mitsuyama. 1999. Induction of protective T cells against Listeria monocytogenes in mice by immunization with a listeriolysin O-negative avirulcnt strain of bacteria and liposome-encapsulated listeriolysin O. Infect. Immun. 67: 568-575.
13. Xiong, H., Y. Tanabe, S. Ohya, and M. Mitsuyama. 1998. Administration of killed bacteria together with listeriolysin O induces protective immunity against Listeria monocytogenes in mice. Immunology 94: 14-21.
14. Kayal, S., and A. Charbit. 2006. Listeriolysin O: a key protein of Listeria mono-cytogenes with multiple functions. FEMS Micrȯbiol. Rev. 30: 514-529.
15. Hof, H., and P. Hefner. 1988. Pathogenicity of Listeria monocytogenes in comparison to other Listeria species. Infection 16 (SuppL 2): S141-S144.
16. Haas, A., M. Dumbsky, and J. Kreft. 1992. Listeriolysin genes: complete sequence of ilo from Listeria ivanovii and of lso from Listeria seeligeri. Biochim Biophys. Acta 1130: 81-84.
17. Kimoto, T., I. Kawamura, C. Kohda, T. Nomura, K. Tsuchiya, Y. Ito, I. Watanabe, T. Kaku, E. Setianingrum, and M. Mitsuyama. 2003. Differences in γ interferon production induced by listeriolysin O and ivanolysin O result in different levels of protective immunity in mice infected with Listeria monocytogenes and Listeria ivanovii. Infect. Immun. 71: 2447-2454.
18. Seki, E., H. Tsutsui, N. M. Tsuji, N. Hayashi, K. Adachi, H. Nakano, S. Futatsugi-Yumikura, O. Takeuchi, K. Hoshino, S. Akira, et al. 2002. Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. J. Immunol. 169: 3863-3868.
19. Gu, Y., K. Kuida, H. Tsutsui, G. Ku, K. Hsiao, M. A. Fleming, N. Hayashi, K. Higashino, H. Okamura, K. Nakanishi, et al. 1997. Activation of interferon-γ inducing factor mediated by interleukin-1β converting enzyme. Science 275: 206-209.
20. Ozoren, N., J. Masumoto, L. Franchi, T. D. Kanneganti, M. Body-Malapel, I. Erturk, R. Jagirdar, L. Zhu, N. Inohara, J. Benin, et al. 2006. Distinct roles of TLR2 and the adaptor ASC in IL-1β/IL-18 secretion in response to Listeria monocytogenes. J. Immunol. 176: 4337-4342.
21. Cervantes, J., T. Nagata, M. Uchijima, K. Shibata, and Y. Koide. 2007. Intracy-tosolic Lisleria monocytogenes induces cell death through caspase-1 activation in murine macrophages. Cell Microbiol. 10: 41-52.
22. + for caspase-1 activation induced by intracellular and extracellular bacteria. J. Biol. Chem. 282: 18810-18818.
23. Ito, Y., I. Kawamura, C. Kohda, H. Baba, T. Nomura, T. Kimoto, I. Watanabe, and M. Mitsuyama. 2003. Seeligeriolysin O, a cholesterol-dependent cytolysin of Lisleria seeligeri, induces y interferon from spleen cells of mice. Infect. Immun. 71: 234-241.
24. Nomura, T., I. Kawamura, K. Tsuchiya, C. Kohda, H. Baba, Y. Ito, T. Kimoto, I. Watanabe, and M. Mitsuyama. 2002. Essential role of interleukin-12 (IL-12) and IL-18 for γ interferon production induced by listeriolysin O in mouse spleen cells. Infect. Immun. 70: 1049-1055.
25. Fukasawa, Y., I. Kawamura, R. Uchiyama, K. Yamamoto, T. Kaku, T. Tominaga, T. Nomura, S. Ichiyama, T. Ezaki, and M. Mitsuyama. 2005. Strcptomycin-de-pendent exhibition of cytokine-inducing activity in streptomycin-dependent My-cobacterium tuberculosis strain 18b. Infect. Immun. 73: 7051-7055.
26. 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.
27. Kanneganti, T. D., M. Body-Malapel, A. Amer, J. H. Park, J. Whitfield, L. Franchi, Z. F. Taraporewala, D. Miller, J. T. Patton, N. Inohara, and G. Nunez. 2006. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. BioL Chem. 281: 36560-36568.
28. Tsuji, N. M., H. Tsutsui, E. Seki, K. Kuida, H. Okamura, K. Nakanishi, and R. A. Flavell. 2004. Roles of caspase-1 in Lisleria infection in mice. Int. Immunol. 16: 335-343.
29. Pan, Q., J. Mathison, C. Fearns, V. V. Kravchenko, J. Da Silva Correia, H. M. Hoffman, K. S. Kobayashi, J. Benin, E. P. Grant, A. J. Coyle, et al. 2007. MDP-induced interleukin-1β processing requires Nod2 and CIAS1/NALP3. J. Leukocyte Biol. 82: 177-183.
30. Qu, Y., L. Franchi, G. Nunez, and G. R. Dubyak. 2007. Nonclassical IL-I β secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 179: 1913-1925.
31. Fink, S. L., and B. T. Cookson. 2006. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8: 1812-1825.
32. 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.
33. 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.
34. Bergsbaken, T., and B. T. Cookson. 2007. Macrophage activation redirects Yer-sinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog. 3: el61.
35. Park, J. M., V. H. Ng, S. Maeda, R. F. Rest, and M. Karin. 2004. Anthrolysin O and other gram-positive cytolysins are Toll-like receptor 4 agonists. J. Exp. Med. 200: 1647-1655.
36. Michel, E., K. A. Reich, R. Favier, P. Berche, and P. Cossart. 1990. Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol. Microbiol. 4: 2167-2178.
37. Watanabe, I, T. Nomura, T. Tominaga, K. Yamamoto, C. Kohda, I. Kawamura, and M. Mitsuyama. 2006. Dependence of the lethal effect of pore-forming hae-molysins of Gram-positive bacteria on cytolytic activity. J. Med. Microbiol. 55: 505-510.
38. Kohda, C., I. Kawamura, H. Baba, T. Nomura, Y. Ito, T. Kimoto, I. Watanabe. and M. Mitsuyama. 2002. Dissociated linkage of cytokine-inducing activity and cytotoxicity to different domains of listeriolysin O from Listeria monocytogenes. Infect. Immun. 70: 1334-1341.
39. Seki, E., H. Tsutsui, H. Nakano, N. Tsuji, K. Hoshino, O. Adachi, K. Adachi, S. Futatsugi, K. Kuida, O. Takeuchi, et al. 2001. Lipopolysaccharide- induced IL-18 secretion from murine Kupffer cells independently of myeloid differentiation factor 88 that is critically involved in induction of production of IL-12 and IL-1β. J. Immunol. 166: 2651-2657.
40. Glomski, I. J., M. M. Gedde, A. W. Tsang, J. A. Swanson, and D. A. Portnoy. 2002. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J. Cell Biol. 156: 1029-1038.
41. Decatur, A. L., and D. A. Portnoy. 2000. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes palhogenicity. Science 290: 992-995.
42. Nomura, T., I. Kawamura, C. Kohda, H. Baba, Y. Ito, T. Kimoto, I. Watanabe, and M. Mitsuyama. 2007. Irreversible loss of membrane-binding activity of List-eria-derivcd cytolysins in nonacidic conditions: a distinct difference from allied cytolysins produced by other Gram-positive bacteria. Microbiology 153: 2250-2258.
43. Moors, M. A., B. Levitt, P. Youngman, and D. A. Portnoy. 1999. Expression of listeriolysin O and ActA by intracellular and extracellular Lisleria monocyto-genes. Infect. Immun. 67: 131-139.
44. 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. Adcrem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
45. 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.
46. Franchi, L., A. Amer, M. Body-Malapel, T. D. Kanneganti, N. Ozoren, R. Jagirdar, N. Inohara, P. Vandenabeele, J. Berlin, A. Coyle, et al. 2006. Cy-tosolic flagellin requires Ipaf for activation of caspase-1 and interleukin lβ in salmonella-infected macrophages. Nat. Immunol. 7: 576-582.
47. 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 1β via Ipaf. Nat. Immunol. 7: 569-575.
48. Hemmi, H., T. Kaisho, O. Takeuchi, S. Sato, II. Sanjo, K. Hoshino, T. Horiuchi, H. Tomizawa, K. Takeda, and S. Akira. 2002. Small anti-viral compounds activate immune cells via the TLR7 MyD88-depcndent signaling pathway. Nat. Immunol. 3: 196-200.
49. Kanneganti, T. D., N. Ozoren, M. Body-Malapel, A. Amer, J. H. Park, L. Franchi, J. Whitfield, W. Barchet, M. Colonna, P. Vandenabeele, et al. 2006. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/NaIp3. Nature 440: 233-236.
50. Boyden, E. D., and W. F. Dietrich. 2006. Nalplb controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38: 240-244.