Maturation modulates caspase-1-independent responses of dendritic cells to anthrax lethal toxin

Cellular Microbiology

Volumn 10, Issue 5, 2008, Pages 1190-1207

  Reig, Núria ^a   Jiang, Aimin ^b,c   Couture, Rachael ^b,c   Sutterwala, Fayyaz S ^b   Ogura, Yasunori ^b   Flavell, Richard A ^b   Mellman, Ira ^b,c   Van Der Goot, F Gisou ^a  

^a EPFL   (Switzerland)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; INTERLEUKIN 1BETA CONVERTING ENZYME; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2;

ANIMAL CELL; ARTICLE; BACILLUS ANTHRACIS; CELL DAMAGE; CELL DEATH; CELL MATURATION; CELL PROTECTION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVATION; IMMUNOMODULATION; INNATE IMMUNITY; KNOCKOUT MOUSE; MACROPHAGE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CARRIER PROTEINS; CASPASE 1; DENDRITIC CELLS; MACROPHAGES; MALE; MAP KINASE KINASE 1; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; SPECIES SPECIFICITY;

BACILLUS ANTHRACIS; MURINAE; MUS;

EID: 42149116277     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01121.x     Document Type: Article

References (74)

1. Abrami, L., Liu, S., Cosson, P., Leppla, S.H., and van der Goot, F.G. (2003) Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J Cell Biol 160: 321-328.
2. Abrami, L., Lindsay, M., Parton, R.G., Leppla, S.H., and van der Goot, F.G. (2004) Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway. J Cell Biol 166: 645-651.
3. Abrami, L., Reig, N., and van der Goot, F.G. (2005) Anthrax toxin: The long and winding road that leads to the kill. Trends Microbiol 13: 72-78.
4. Abrami, L., Leppla, S.H., and van der Goot, F.G. (2006) Receptor palmitoylation and ubiquitination regulate anthrax toxin endocytosis. J Cell Biol 172: 309-320.
5. Agrawal, A., Lingappa, J., Leppla, S.H., Agrawal, S., Jabbar, A., Quinn, C., and Pulendran, B. (2003) Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 424: 329-334.
6. Alileche, A., Serfass, E.R., Muehlbauer, S.M., Porcelli, S.A., and Brojatsch, J. (2005) Anthrax lethal toxin-mediated killing of human and murine dendritic cells impairs the adaptive immune response. PLoS Pathog 1: E19.
7. Baetz, D., Regula, K.M., Ens, K., Shaw, J., Kothari, S., Yurkova, N., and Kirshenbaum, L.A. (2005) Nuclear factor-kappaB-mediated cell survival involves transcriptional silencing of the mitochondrial death gene BNIP3 in ventricular myocytes. Circulation 112: 3777-3785.
8. Baldari, C.T., Tonello, F., Paccani, S.R., and Montecucco, C. (2006) Anthrax toxins: A paradigm of bacterial immune suppression. Trends Immunol 27: 434-440.
9. Boyden, E.D., and Dietrich, W.F. (2006) Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. [see comment] Nat Genet 38: 240-244.
10. Bradley, K.A., Mogridge, J., Mourez, M., Collier, R.J., and Young, J.A. (2001) Identification of the cellular receptor for anthrax toxin. Nature 414: 225-229.
11. Brennan, M.A., and Cookson, B.T. (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31-40.
12. Brittingham, K.C., Ruthel, G., Panchal, R.G., Fuller, C.L., Ribot, W.J., Hoover, T.A., et al. (2005) Dendritic cells endocytose Bacillus anthracis spores: Implications for anthrax pathogenesis. J Immunol 174: 5545-5552.
13. Cleret, A., Quesnel-Hellmann, A., Mathieu, J., Vidal, D., and Tournier, J.N. (2006) Resident CD11c+ lung cells are impaired by anthrax toxins after spore infection. J Infect Dis 194: 86-94.
14. Comer, J.E., Chopra, A.K., Peterson, J.W., and Konig, R. (2005) Direct inhibition of T-lymphocyte activation by anthrax toxins in vivo. Infect Immun 73: 8275-8281.
15. Conway, K.E., McConnell, B.B., Bowring, C.E., Donald, C.D., Warren, S.T., and Vertino, P.M. (2000) TMS1, a novel proapoptotic caspase recruitment domain protein, is a target of methylation-induced gene silencing in human breast cancers. Cancer Res 60: 6236-6242.
16. Cory, S., and Adams, J.M. (2002) The Bcl2 family: Regulators of the cellular life-or-death switch. Nat Rev Cancer 2: 647-656.
17. Creagh, E.M., and O'Neill, L.A. (2006) TLRs, NLRs and RLRs: A trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol 27: 352-357.
18. Duesbery, N.S., Webb, C.P., Leppla, S.H., Gordon, V.M., Klimpel, K.R., Copeland, T.D., et al. (1998) Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280: 734-737.
19. During, R.L., Li, W., Hao, B., Koenig, J.M., Stephens, D.S., Quinn, C.P., and Southwick, F.S. (2005) Anthrax lethal toxin paralyzes neutrophil actin-based motility. J Infect Dis 192: 837-845.
20. Erwin, J.L., DaSilva, L.M., Bavari, S., Little, S.F., Friedlander, A.M., and Chanh, T.C. (2001) Macrophage-derived cell lines do not express proinflammatory cytokines after exposure to Bacillus anthracis lethal toxin. Infect Immun 69: 1175-1177.
21. Fang, H., Cordoba-Rodriguez, R., Lankford, C.S., and Frucht, D.M. (2005) Anthrax lethal toxin blocks MAPK kinase-dependent IL-2 production in CD4+ T cells. J Immunol 174: 4966-4971.
22. Fang, H., Xu, L., Chen, T.Y., Cyr, J.M., and Frucht, D.M. (2006) Anthrax lethal toxin has direct and potent inhibitory effects on B cell proliferation and immunoglobulin production. J Immunol 176: 6155-6161.
23. Faustin, B., Lartigue, L., Bruey, J.M., Luciano, F., Sergienko, E., Bailly-Maitre, B., et al. (2007) Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell 25: 713-724.
24. Fink, S.L., and Cookson, B.T. (2007) Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol 9: 2562-2570.
25. Friedlander, A.M. (1986) Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J Biol Chem 261: 7123-7126.
26. Friedlander, A.M., Bhatnagar, R., Leppla, S.H., Johnson, L., and Singh, Y. (1993) Characterization of macrophage sensitivity and resistance to anthrax lethal toxin. Infect Immun 61: 245-252.
27. Garrett, W.S., Chen, L.M., Kroschewski, R., Ebersold, M., Turley, S., Trombetta, S., et al. (2000) Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102: 325-334.
28. Gatti, E., and Pierre, P. (2003) Understanding the cell biology of antigen presentation: The dendritic cell contribution. Curr Opin Cell Biol 15: 468-473.
29. Gordon, V.M., Klimpel, K.R., Arora, N., Henderson, M.A., and Leppla, S.H. (1995) Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect Immun 63: 82-87.
30. Gurcel, L., Abrami, L., Girardin, S., Tschopp, J., and 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.
31. Hersh, D., Monack, D.M., Smith, M.R., Ghori, N., Falkow, S., and Zychlinsky, A. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96: 2396-2401.
32. Hilbi, H., Moss, J.E., Hersh, D., Chen, Y., Arondel, J., Banerjee, S., et al. (1998) Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem 273: 32895-32900.
33. Hon, H., Rucker, E.B., 3rd, Hennighausen, L., and Jacob, J. (2004) bcl-xL is critical for dendritic cell survival in vivo. J Immunol 173: 4425-4432.
34. Hou, W.S., and Van Parijs, L. (2004) A Bcl-2-dependent molecular timer regulates the lifespan and immunogenicity of dendritic cells. Nat Immunol 5: 583-589.
35. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., et al. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176: 1693-1702.
36. Jiang, A., Bloom, O., Ono, S., Cui, W., Unternaehrer, J., Jiang, S., et al. (2007) Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 27: 610-624.
37. Karin, M., and Lin, A. (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221-227.
38. Kassam, A., Der S.D., and Mogridge J. (2005) Differentiation of human monocytic cell lines confers susceptibility to Bacillus anthracis lethal toxin. Cell Microbiol 7: 281-292.
39. Klimpel, K.R., Arora, N., and Leppla, S.H. (1994) Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol Microbiol 13: 1093-1100.
40. Kuida, K., Lippke, J.A., Ku, G., Harding, M.W., Livingston, D.J., Su, M.S., and Flavell, R.A. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267: 2000-2003.
41. Lara-Tejero, M., Sutterwala, F.S., Ogura, Y., Grant, E.P., Bertin, J., Coyle, A.J., et al. (2006) Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med 203: 1407-1412.
42. Leppla, S.H. (1988) Production and purification of anthrax toxin. Methods Enzymol 165: 103-116.
43. Liu, S., and Leppla, S.H. (2003) Cell surface tumor endothelium marker 8 cytoplasmic tail-independent anthrax toxin binding, proteolytic processing, oligomer formation and internalization. J Biol Chem 278: 5227-5234.
44. Lundqvist, A., Nagata, T., Kiessling, R., and Pisa, P. (2002) Mature dendritic cells are protected from Fas/CD95-mediated apoptosis by upregulation of Bcl-X (L). Cancer Immunol Immunother 51: 139-144.
45. Mariathasan, S., and Monack, D.M. (2007) Inflammasome adaptors and sensors: Intracellular regulators of infection and inflammation. Nat Rev Immunol 7: 31-40.
46. Mariathasan, S., Weiss, D.S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
47. Martinon, F., and Tschopp, J. (2004) Inflammatory caspases: Linking an intracellular innate immune system to autoinflammatory diseases. Cell 117: 561-574.
48. Martinon, F., Burns, K., and Tschopp, J. (2002) The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417-426.
49. Masumoto, J., Taniguchi, S., Ayukawa, K., Sarvotham, H., Kishino, T., Niikawa, N., et al. (1999) ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells. J Biol Chem 274: 33835-33838.
50. Meylan, E., Tschopp, J., and Karin, M. (2006) Intracellular pattern recognition receptors in the host response. Nature 442: 39-44.
51. Milne, J.C., Furlong, D., Hanna, P.C., Wall, J.S., and Collier, R.J. (1994) Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J Biol Chem 269: 20607-20612.
52. Moayeri, M., and Leppla, S.H. (2004) The roles of anthrax toxin in pathogenesis. Curr Opin Microbiol 7: 19-24.
53. Muehlbauer, S.M., Evering, T.H., Bonuccelli, G., Squires, R.C., Ashton, A.W., Porcelli, S.A., et al. (2007) Anthrax lethal toxin kills macrophages in a strain-specific manner by apoptosis or caspase-1-mediated necrosis. Cell Cycle 6: 758-766.
54. Ouaaz, F., Arron, J., Zheng, Y., Choi, Y., and Beg, A.A. (2002) Dendritic cell development and survival require distinct NF-kappaB subunits. Immunity 16: 257-270.
55. Paccani, S.R., Tonello, F., Ghittoni, R., Natale, M., Muraro, L., D'Elios, M.M., et al. (2005) Anthrax toxins suppress T lymphocyte activation by disrupting antigen receptor signaling. J Exp Med 201: 325-331.
56. Park, J.M., Greten, F.R., Li, Z.W., and Karin, M. (2002) Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297: 2048-2051.
57. Pellizzari, R., Guidi-Rontani, C., Vitale, G., Mock, M., and Montecucco, C. (1999) Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/IFNgamma-induced release of NO and TNFalpha. FEBS Lett 462: 199-204.
58. Philpott, N.J., Turner, A.J., Scopes, J., Westby, M., Marsh, J.C., Gordon-Smith, E.C., et al. (1996) The use of 7-amino actinomycin D in identifying apoptosis: Simplicity of use and broad spectrum of application compared with other techniques. Blood 87: 2244-2251.
59. Pierre, P., Turley, S.J., Gatti, E., Hull, M., Meltzer, J., Mirza, A., et al. (1997) Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388: 787-792.
60. Racoosin, E.L., and Swanson, J.A. (1989) Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J Exp Med 170: 1635-1648.
61. Roux, P.P., and Blenis, J. (2004) ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344.
62. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T.K., et al. (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23: 479-490.
63. Scobie, H.M., Rainey, G.J., Bradley, K.A., and Young, J.A. (2003) Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc Natl Acad Sci USA 100: 5170-5174.
64. Squires, R.C., Muehlbauer, S.M., and Brojatsch, J. (2007) Proteasomes control caspase-1 activation in anthrax lethal toxin-mediated cell killing. J Biol Chem 282: 34260-34267.
65. Steinman, R.M., Hawiger, D., and Nussenzweig, M.C. (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21: 685-711.
66. Sutterwala, F.S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G.S., Grant, E.P., et al. (2006) Critical role for NALP3/ CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of Caspase-1. Immunity 24: 317-327.
67. Tournier, J.N., Quesnel-Hellmann, A., Mathieu, J., Montecucco, C., Tang, W.J., Mock, M., et al. (2005) Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells. J Immunol 174: 4934-4941.
68. Trombetta, E.S., and Mellman, I. (2005) Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 23: 975-1028.
69. Tureci, O., Bian, H., Nestle, F.O., Raddrizzani, L., Rosinski, J.A., Tassis, A., et al. (2003) Cascades of transcriptional induction during dendritic cell maturation revealed by genome-wide expression analysis. FASEB J 17: 836-847.
70. Vitale, G., Bernardi, L., Napolitani, G., Mock, M., and Montecucco, C. (2000) Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem J 352 Part 3: 739-745.
71. Vitale, G., Pellizzari, R., Recchi, C., Napolitani, G., Mock, M., and Montecucco, C. (1998) Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem Biophys Res Commun 248: 706-711.
72. West, M.A., Wallin, R.P., Matthews, S.P., Svensson, H.G., Zaru, R., Ljunggren, H.G., et al. (2004) Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305: 1153-1157.
73. Wickliffe, K.E., Leppla, S.H., and Moayeri, M. (2008) Anthrax lethal toxin-induced inflammasome formation and caspase-1 activation are late events dependent on ion fluxes and the proteasome. Cell Microbiol 10: 332-343.
74. Wong, B.R., Josien, R., Lee, S.Y., Sauter, B., Li, H.L., Steinman, R.M., and Choi, Y. (1997) TRANCE (tumor necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor. J Exp Med 186: 2075-2080.