Cholesterol-dependent cytolysins induce rapid release of mature IL-1β from murine macrophages in a NLRP3 inflammasome and cathepsin B-dependent manner

Journal of Leukocyte Biology

Volumn 86, Issue 5, 2009, Pages 1227-1238

  Chu, Jessica ^a   Thomas, L Michael ^a   Watkins, Simon C ^a   Franchi, Luigi ^b   Núñez, Gabriel ^b   Salter, Russell D ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Bacterial; Cytokines; Inflammation

Indexed keywords

CALCIUM; CATHEPSIN B; CHOLESTEROL; CRYOPYRIN; CYTOLYSIN; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; PHOSPHOLIPASE A2; POTASSIUM; TETANOLYSIN O; TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CALCIUM TRANSPORT; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; EXPOSURE; IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE;

ANIMALS; CARRIER PROTEINS; CATHEPSIN B; CHOLESTEROL; CYTOTOXINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXOTOXINS; FLOW CYTOMETRY; GRAM-POSITIVE BACTERIA; INFLAMMATION; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; PEPSTATINS;

BACTERIA (MICROORGANISMS); EUKARYOTA; MURINAE; POSIBACTERIA;

EID: 70350726375     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0309164     Document Type: Article

References (58)

1. Billington, S. J., Jost, B. H., Songer, J. G. (2000) Thiol-activated cytolysins: structure, function and role in pathogenesis. FEMS Microbiol. Lett. 182, 197-205. (Pubitemid 30006905)
2. Palmer, M. (2001) The family of thiol-activated, cholesterol-binding cytolysins. Toxicon 39, 1681-1689.
3. Bhakdi, S., Tranum-Jensen, J., Sziegoleit, A. (1985) Mechanism of membrane damage by streptolysin-O. Infect. Immun. 47, 52-60.
4. Morgan, P. J., Hyman, S. C., Rowe, A. J., Mitchell, T. J., Andrew, P. W., Saibil, H. R. (1995) Subunit organization and symmetry of pore-forming, oligomeric pneumolysin. FEBS Lett. 371, 77-80.
5. Olofsson, A., Hebert, H., Thelestam, M. (1993) The projection structure of perfringolysin O (Clostridium perfringens α-toxin). FEBS Lett. 319, 125-127. (Pubitemid 23074283)
6. Watanabe, I., Nomura, T., Tominaga, T., Yamamoto, K., Kohda, C., Kawamura, I., Mitsuyama, M. (2006) Dependence of the lethal effect of pore-forming haemolysins of Gram-positive bacteria on cytolytic activity. J. Med. Microbiol. 55, 505-510.
7. Benton, K. A., Everson, M. P., Briles, D. E. (1995) A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect. Immun. 63, 448-455.
8. Berry, A. M., Yother, J., Briles, D. E., Hansman, D., Paton, J. C. (1989) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect. Immun. 57, 2037-2042. (Pubitemid 19186880)
9. Cowan, G. J., Atkins, H. S., Johnson, L. K., Titball, R. W., Mitchell, T. J. (2007) Immunization with anthrolysin O or a genetic toxoid protects against challenge with the toxin but not against Bacillus anthracis. Vaccine 25, 7197-7205. (Pubitemid 47464670)
10. Beauregard, K. E., Lee, K. D., Collier, R. J., Swanson, J. A. (1997) pH-Dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J. Exp. Med. 186, 1159-1163.
11. Geoffroy, C., Gaillard, J. L., Alouf, J. E., Berche, P. (1987) Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes. Infect. Immun. 55, 1641-1646. (Pubitemid 17084156)
12. Wei, Z., Schnupf, P., Poussin, M. A., Zenewicz, L. A., Shen, H., Goldfine, H. (2005) Characterization of Listeria monocytogenes expressing anthrolysin O and phosphatidylinositol-specific phospholipase C from Bacillus anthracis. Infect. Immun. 73, 6639-6646.
13. Mosser, E. M., Rest, R. (2006) The Bacillus anthracis cholesterol-dependent cytolysin, anthrolysin O, kills human neutrophils, monocytes and macrophages. BMC Microbiol. 6, 56.
14. Husmann, M., Dersch, K., Bobkiewicz, W., Beckmann, E., Veerachato, G., Bhakdi, S. (2006) Differential role of p38 mitogen activated protein kinase for cellular recovery from attack by pore-forming S. aureus [α]-toxin or streptolysin O. Biochem. Biophys. Res. Commun. 344, 1128-1134.
15. Walev, I., Hombach, M., Bobkiewicz, W., Fenske, D., Bhakdi, S., Husmann, M. (2001) Resealing of large transmembrane pores produced by streptolysin O in nucleated cells is accompanied by NF-κB activation and downstream events. FASEB J. 16, 237-239.
16. Idone, V., Tam, C., Goss, J. W., Toomre, D., Pypaert, M., Andrews, N. W. (2008) Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. J. Cell Biol. 180, 905-914.
17. Henderson, B., Wilson, M., Wren, B. (1997) Are bacterial exotoxins cytokine network regulators? Trends Microbiol. 5, 454-458. (Pubitemid 27504951)
18. Nishibori, T., Xiong, H., Kawamura, I., Arakawa, M., Mitsuyama, M. (1996) Induction of cytokine gene expression by listeriolysin O and roles of macrophages and NK cells. Infect. Immun. 64, 3188-3195. (Pubitemid 26256164)
19. Hackett, S. P., Stevens, D. L. (1992) Streptococcal toxic shock syndrome: synthesis of tumor necrosis factor and interleukin-1 by monocytes stimulated with pyrogenic exotoxin A and streptolysin O. J. Infect. Dis. 165, 879-885.
20. Houldsworth, S., Andrew, P. W., Mitchell, T. J. (1994) Pneumolysin stimulates production of tumor necrosis factor α and interleukin-1 β by human mononuclear phagocytes. Infect. Immun. 62, 1501-1503. (Pubitemid 24110854)
21. Arend, W. P., Palmer, G., Gabay, C. (2008) IL-1, IL-18, and IL-33 families of cytokines. Immunol. Rev. 223, 20-38. (Pubitemid 351986169)
22. Franchi, L., Eigenbrod, T., Munoz-Planillo, R., Nunez, G. (2009) The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 10, 241-247.
23. Martinon, F., Mayor, A., Tschopp, J. (2009) The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27, 229-265.
24. Pedra, J. H., Cassel, S. L., Sutterwala, F. S. (2009) Sensing pathogens and danger signals by the inflammasome. Curr. Opin. Immunol. 21, 10-16.
25. Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R. M., Curti, A., Idzko, M., Panther, E., Di Virgilio, F. (2006) The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176, 3877-3883. (Pubitemid 44264361)
26. Brough, D., Le Feuvre, R. A., Wheeler, R. D., Solovyova, N., Hilfiker, S., Rothwell, N. J., Verkhratsky, A. (2003) Ca2+ stores and Ca2+ entry differentially contribute to the release of IL-1 β and IL-1 α from murine macrophages. J. Immunol. 170, 3029-3036.
27. Andrei, C., Margiocco, P., Poggi, A., Lotti, L. V., Torrisi, M. R., Rubartelli, A. (2004) Phospholipases C and A2 control lysosome-mediated IL-1 β secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. USA 101, 9745-9750.
28. Sutterwala, F. S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G. S., Grant, E. P., Bertin, J., Coyle, A. J., Galan, J. E., Askenase, P. W., Flavell, R. A. (2006) Critical role for NALP3/CIAS1/cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327.
29. Locovei, S., Scemes, E., Qiu, F., Spray, D. C., Dahl, G. (2007) Pannexin1 is part of the pore forming unit of the P2X7 receptor death complex. FEBS Lett. 581, 483-488. (Pubitemid 46149626)
30. Pelegrin, P., Surprenant, A. (2006) Pannexin-1 mediates large pore formation and interleukin-1β release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082. (Pubitemid 44658525)
31. Kanneganti, T-D., Lamkanfi, M., Kim, Y-G., Chen, G., Park, J-H., Franchi, L., Vandenabeele, P., Nunez, G. (2007) Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 26, 433-443.
32. Mariathasan, S., Weiss, D. S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., Lee, W. P., Weinrauch, Y., Monack, D. M., Dixit, V. M. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232. (Pubitemid 43372102)
33. Le Feuvre, R. A., Brough, D., Iwakura, Y., Takeda, K., Rothwell, N. J. (2002) Priming of macrophages with lipopolysaccharide potentiates P2X7-mediated cell death via a caspase-1-dependent mechanism, independently of cytokine production. J. Biol. Chem. 277, 3210-3218.
34. Martinon, F., Petrilli, V., Mayor, A., Tardivel, A., Tschopp, J. (2006) Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241. (Pubitemid 43372104)
35. Hornung, V., Bauernfeind, F., Halle, A., Samstad, E. O., Kono, H., Rock, K. L., Fitzgerald, K. A., Latz, E. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856.
36. Dostert, C., Petrilli, V., Van Bruggen, R., Steele, C., Mossman, B. T., Tschopp, J. (2008) Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674-677. (Pubitemid 351928351)
37. Halle, A., Hornung, V., Petzold, G. C., Stewart, C. R., Monks, B. G., Reinheckel, T., Fitzgerald, K. A., Latz, E., Moore, K. J., Golenbock, D. T. (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nat. Immunol. 9, 857-865.
38. Willingham, S. B., Ting, J. P. (2008) NLRs and the dangers of pollution and aging. Nat. Immunol. 9, 831-833.
39. Schotte, P., Van Criekinge, W., Van de Craen, M., Van Loo, G., Desmedt, M., Grooten, J., Cornelissen, M., De Ridder, L., Vandekerckhove, J., Fiers, W., Vandenabeele, P., Beyaert, R. (1998) Cathepsin B-mediated activation of the proinflammatory caspase-11. Biochem. Biophys. Res. Commun. 251, 379-387. (Pubitemid 28498120)
40. Wang, S., Miura, M., Jung, Y. K., Zhu, H., Li, E., Yuan, J. (1998) Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92, 501-509. (Pubitemid 28101113)
41. Davies, J. Q., Gordon, S. (2005) Isolation and culture of murine macrophages. Methods Mol. Biol. 290, 91-103.
42. Qu, Y., Franchi, L., Nunez, G., Dubyak, G. R. (2007) Nonclassical IL-1 β secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 179, 1913-1925.
43. Ito, Y., Kawamura, I., Kohda, C., Tsuchiya, K., Nomura, T., Mitsuyama, M. (2005) Seeligeriolysin O, a protein toxin of Listeria seeligeri, stimulates macrophage cytokine production via Toll-like receptors in a profile different from that induced by other bacterial ligands. Int. Immunol. 17, 1597-1606. (Pubitemid 41754682)
44. Malley, R., Henneke, P., Morse, S. C., Cieslewicz, M. J., Lipsitch, M., Thompson, C. M., Kurt-Jones, E., Paton, J. C., Wessels, M. R., Golenbock, D. T. (2003) Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc. Natl. Acad. Sci. USA 100, 1966-1971. (Pubitemid 36254557)
45. Park, J. M., Ng, V. H., Maeda, S., Rest, R. F., Karin, M. (2004) Anthrolysin O and other Gram-positive cytolysins are Toll-like receptor 4 agonists. J. Exp. Med. 200, 1647-1655. (Pubitemid 40094188)
46. Srivastava, A., Henneke, P., Visintin, A., Morse, S. C., Martin, V., Watkins, C., Paton, J. C., Wessels, M. R., Golenbock, D. T., Malley, R. (2005) The apoptotic response to pneumolysin is Toll-like receptor 4 dependent and protects against pneumococcal disease. Infect. Immun. 73, 6479-6487. (Pubitemid 41368810)
47. Shoma, S., Tsuchiya, K., Kawamura, I., Nomura, T., Hara, H., Uchiyama, R., Daim, S., Mitsuyama, M. (2008) Critical involvement of pneumolysin in production of interleukin-1α and caspase-1-dependent cytokines in infection with Streptococcus pneumoniae in vitro: a novel function of pneumolysin in caspase-1 activation. Infect. Immun. 76, 1547-1557. (Pubitemid 351561998)
48. Solini, A., Chiozzi, P., Morelli, A., Fellin, R., Di Virgilio, F. (1999) Human primary fibroblasts in vitro express a purinergic P2X7 receptor coupled to ion fluxes, microvesicle formation and IL-6 release. J. Cell Sci. 112, 297-305. (Pubitemid 29080652)
49. Mehta, V. B., Hart, J., Wewers, M. D. (2001) ATP-stimulated release of interleukin (IL)-1β and IL-18 requires priming by lipopolysaccharide and is independent of caspase-1 cleavage. J. Biol. Chem. 276, 3820-3826. (Pubitemid 37371459)
50. Kahlenberg, J. M., Lundberg, K. C., Kertesy, S. B., Qu, Y., Dubyak, G. R. (2005) Potentiation of caspase-1 activation by the P2X7 receptor is dependent on TLR signals and requires NF-κB-driven protein synthesis. J. Immunol. 175, 7611-7622. (Pubitemid 41713461)
51. Yoshikawa, H., Kawamura, I., Fujita, M., Tsukada, H., Arakawa, M., Mitsuyama, M. (1993) Membrane damage and interleukin-1 production in murine macrophages exposed to listeriolysin O. Infect. Immun. 61, 1334-1339. (Pubitemid 23099203)
52. Gonzalez, M. R., Bischofberger, M., Pernot, L., van der Goot, F. G., Freche, B. (2008) Bacterial pore-forming toxins: the (w)hole story? Cell. Mol. Life Sci. 65, 493-507.
53. Gurcel, L., Abrami, L., Girardin, S., Tschopp, J., van der Goot, F. G. (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126, 1135-1145. (Pubitemid 44380297)
54. Kloft, N., Busch, T., Neukirch, C., Weis, S., Boukhallouk, F., Bobkiewicz, W., Cibis, I., Bhakdi, S., Husmann, M. (2009) Pore-forming toxins activate MAPK p38 by causing loss of cellular potassium. Biochem. Biophys. Res. Commun. 385, 503-506.
55. Walev, I., Reske, K., Palmer, M., Valeva, A., Bhakdi, S. (1995) Potassium-inhibited processing of IL-1 β in human monocytes. EMBO J. 14, 1607-1614.
56. Bhakdi, S., Muhly, M., Korom, S., Hugo, F. (1989) Release of interleukin- 1 β associated with potent cytocidal action of staphylococcal α-toxin on human monocytes. Infect. Immun. 57, 3512-3519. (Pubitemid 19259885)
57. Bhakdi, S., Bayley, H., Valeva, A., Walev, I., Walker, B., Kehoe, M., Palmer, M. (1996) Staphylococcal α-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch. Microbiol. 165, 73-79.
58. Lich, J. D., Arthur, J. C., Ting, J. P. Y. (2006) Cryopyrin: in from the cold. Immunity 24, 241-243.