Direct Proteolytic Cleavage of NLRP1B Is Necessary and Sufficient for Inflammasome Activation by Anthrax Lethal Factor

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Chavarría Smith, Joseph ^a   Vance, Russell E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CRYOPYRIN; FLAGELLIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PROTEIN P17;

ANIMAL CELL; ANTHRAX; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; DNA TRANSFECTION; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LETHAL GENE; MOUSE; MUTATION; NONHUMAN; PROTEIN DEGRADATION; RAT; WESTERN BLOTTING;

ANIMALS; ANTIGENS, BACTERIAL; APOPTOSIS REGULATORY PROTEINS; BACILLUS ANTHRACIS; BACTERIAL TOXINS; CELL LINE, TRANSFORMED; HUMANS; INFLAMMASOMES; MICE; PROTEOLYSIS; RATS; RATS, INBRED F344;

BACILLUS ANTHRACIS; MUS; RATTUS;

EID: 84879508269     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003452     Document Type: Article

References (56)

1. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
2. Janeway CA Jr, (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54 Pt 1: 1-13.
3. Vance RE, Isberg RR, Portnoy DA, (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6: 10-21.
4. Fontana MF, Banga S, Barry KC, Shen X, Tan Y, et al. (2011) Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. PLoS Pathog 7: e1001289.
5. Shin S, Case CL, Archer KA, Nogueira CV, Kobayashi KS, et al. (2008) Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog 4: e1000220.
6. Boyer L, Magoc L, Dejardin S, Cappillino M, Paquette N, et al. (2011) Pathogen-derived effectors trigger protective immunity via activation of the Rac2 enzyme and the IMD or Rip kinase signaling pathway. Immunity 35: 536-549.
7. Keestra AM, Winter MG, Auburger JJ, Frassle SP, Xavier MN, et al. (2013) Manipulation of small Rho GTPases is a pathogen-induced process detected by NOD1. Nature 496: 233-237.
8. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, et al. (1998) Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280: 734-737.
9. Vitale G, Pellizzari R, Recchi C, Napolitani G, Mock M, et al. (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.
10. Chopra AP, Boone SA, Liang X, Duesbery NS, (2003) Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J Biol Chem 278: 9402-9406.
11. Bardwell AJ, Abdollahi M, Bardwell L, (2004) Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. Biochem J 378: 569-577.
12. Bergsbaken T, Fink SL, Cookson BT, (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7: 99-109.
13. Boyden ED, Dietrich WF, (2006) Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat Genet 38: 240-244.
14. Friedlander AM, (1986) Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J Biol Chem 261: 7123-7126.
15. Friedlander AM, Bhatnagar R, Leppla SH, Johnson L, Singh Y, (1993) Characterization of macrophage sensitivity and resistance to anthrax lethal toxin. Infect Immun 61: 245-252.
16. Newman ZL, Printz MP, Liu S, Crown D, Breen L, et al. (2010) Susceptibility to anthrax lethal toxin-induced rat death is controlled by a single chromosome 10 locus that includes rNlrp1. PLoS Pathog 6: e1000906.
17. Terra JK, Cote CK, France B, Jenkins AL, Bozue JA, et al. (2010) Cutting edge: resistance to Bacillus anthracis infection mediated by a lethal toxin sensitive allele of Nalp1b/Nlrp1b. J Immunol 184: 17-20.
18. Moayeri M, Crown D, Newman ZL, Okugawa S, Eckhaus M, et al. (2010) Inflammasome sensor Nlrp1b-dependent resistance to anthrax is mediated by caspase-1, IL-1 signaling and neutrophil recruitment. PLoS Pathog 6: e1001222.
19. Tschopp J, Martinon F, Burns K, (2003) NALPs: a novel protein family involved in inflammation. Nat Rev Mol Cell Biol 4: 95-104.
20. Ting JP, Lovering RC, Alnemri ES, Bertin J, Boss JM, et al. (2008) The NLR gene family: a standard nomenclature. Immunity 28: 285-287.
21. von Moltke J, Ayres JS, Kofoed EM, Chavarria-Smith J, Vance RE, (2012) Recognition of Bacteria by Inflammasomes. Annu Rev Immunol 31: 73-106.
22. Martinon F, Burns K, Tschopp J, (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417-426.
23. D'Osualdo A, Weichenberger CX, Wagner RN, Godzik A, Wooley J, et al. (2011) CARD8 and NLRP1 undergo autoproteolytic processing through a ZU5-like domain. PLoS One 6: e27396.
24. Frew BC, Joag VR, Mogridge J, (2012) Proteolytic processing of Nlrp1b is required for inflammasome activity. PLoS Pathog 8: e1002659.
25. Finger JN, Lich JD, Dare LC, Cook MN, Brown KK, et al. (2012) Autolytic proteolysis within the function to find domain (FIIND) is required for NLRP1 inflammasome activity. J Biol Chem 287: 25030-25037.
26. Zhao Y, Yang J, Shi J, Gong YN, Lu Q, et al. (2011) The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477: 596-600.
27. Kofoed EM, Vance RE, (2011) Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477: 592-595.
28. Roberts TL, Idris A, Dunn JA, Kelly GM, Burnton CM, et al. (2009) HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323: 1057-1060.
29. Burckstummer T, Baumann C, Bluml S, Dixit E, Durnberger G, et al. (2009) An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10: 266-272.
30. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, et al. (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458: 514-518.
31. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES, (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458: 509-513.
32. Ichinohe T, Pang IK, Iwasaki A, (2010) Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol 11: 404-410.
33. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
34. Chisholm ST, Coaker G, Day B, Staskawicz BJ, (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
35. Axtell MJ, Staskawicz BJ, (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
36. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL, (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389.
37. Fink SL, Bergsbaken T, Cookson BT, (2008) Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci U S A 105: 4312-4317.
38. Klimpel KR, Arora N, Leppla SH, (1994) Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol Microbiol 13: 1093-1100.
39. Wickliffe KE, Leppla SH, 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.
40. Wickliffe KE, Leppla SH, Moayeri M, (2008) Killing of macrophages by anthrax lethal toxin: involvement of the N-end rule pathway. Cell Microbiol 10: 1352-1362.
41. Levinsohn JL, Newman ZL, Hellmich KA, Fattah R, Getz MA, et al. (2012) Anthrax lethal factor cleavage of Nlrp1 is required for activation of the inflammasome. PLoS Pathog 8: e1002638.
42. Hellmich KA, Levinsohn JL, Fattah R, Newman ZL, Maier N, et al. (2012) Anthrax lethal factor cleaves mouse nlrp1b in both toxin-sensitive and toxin-resistant macrophages. PLoS One 7: e49741.
43. Park JM, Greten FR, Li ZW, Karin M, (2002) Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297: 2048-2051.
44. Zakharova MY, Kuznetsov NA, Dubiley SA, Kozyr AV, Fedorova OS, et al. (2009) Substrate recognition of anthrax lethal factor examined by combinatorial and pre-steady-state kinetic approaches. J Biol Chem 284: 17902-17913.
45. Turk BE, Wong TY, Schwarzenbacher R, Jarrell ET, Leppla SH, et al. (2004) The structural basis for substrate and inhibitor selectivity of the anthrax lethal factor. Nat Struct Mol Biol 11: 60-66.
46. von Moltke J, Trinidad NJ, Moayeri M, Kintzer AF, Wang SB, et al. (2012) Rapid induction of inflammatory lipid mediators by the inflammasome in vivo. Nature 490: 107-111.
47. Liao KC, Mogridge J, (2009) Expression of Nlrp1b inflammasome components in human fibroblasts confers susceptibility to anthrax lethal toxin. Infect Immun 77: 4455-4462.
48. Ali SR, Timmer AM, Bilgrami S, Park EJ, Eckmann L, et al. (2011) Anthrax toxin induces macrophage death by p38 MAPK inhibition but leads to inflammasome activation via ATP leakage. Immunity 35: 34-44.
49. Turk BE, (2007) Manipulation of host signalling pathways by anthrax toxins. Biochem J 402: 405-417.
50. Potempa J, Pike RN, (2009) Corruption of innate immunity by bacterial proteases. J Innate Immun 1: 70-87.
51. Toh EC, Huq NL, Dashper SG, Reynolds EC, (2010) Cysteine protease inhibitors: from evolutionary relationships to modern chemotherapeutic design for the treatment of infectious diseases. Curr Protein Pept Sci 11: 725-743.
52. Anderson J, Schiffer C, Lee SK, Swanstrom R, (2009) Viral protease inhibitors. Handb Exp Pharmacol 2009: 85-110.
53. Li H, Child MA, Bogyo M, (2012) Proteases as regulators of pathogenesis: examples from the Apicomplexa. Biochim Biophys Acta 1824: 177-185.
54. van der Hoorn RA, Kamoun S, (2008) From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell 20: 2009-2017.
55. Liao KC, Mogridge J, (2012) Activation of the Nlrp1b Inflammasome by Reduction of Cytosolic ATP. Infect Immun 81: 570-9.
56. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, et al. (2008) Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 9: 1171-1178.