Caspase-1 activity affects AIM2 speck formation/stability through a negative feedback loop

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue APR, 2013, Pages

  Juruj, C ^a,b,c   Lelogeais, V ^a,b,c   Pierini, R ^a,b,c   Perret, M ^a,b,c   Py, B F ^a,b,c   Jamilloux, Y ^a,b,c   Broz, P ^d   Ader, F ^a,b,c   Faure, M ^a,b,c   Henry, T ^a,b,c  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE LYON   (France)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AIM2; Caspase 1; Francisella tularensis; Inflammasome; Regulation

Indexed keywords

AIM2 INFLAMMASOME; AMINO ACID TRANSPORTER; BETA INTERFERON; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; LACTATE DEHYDROGENASE; LUCIFERASE; NIGERICIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AIM2 PROTEIN, MOUSE; CYTOSKELETON PROTEIN; NUCLEAR PROTEIN; PYCARD PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BACTERIAL STRAIN; CELL DEATH; CELL DIVISION; CONTROLLED STUDY; DNA TRANSFECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; FRANCISELLA NOVICIDA; GENE MUTATION; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE MICROSCOPY; LEGIONNAIRE DISEASE; MACROPHAGE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; REGULATORY MECHANISM; WESTERN BLOTTING; AIM2; ANIMAL; C57BL MOUSE; CASPASE-1; CELL LINE; FEEDBACK SYSTEM; FRANCISELLA TULARENSIS; GENE DELETION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE MUTANT;

AIM2; CASPASE-1; FRANCISELLA TULARENSIS; INFLAMMASOME; REGULATION;

ANIMALS; CASPASE 1; CELL DEATH; CELL LINE; CYTOSKELETAL PROTEINS; FEEDBACK; FRANCISELLA TULARENSIS; GENE DELETION; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR PROTEINS;

EID: 84882944786     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00014     Document Type: Article

References (48)

1. Amer, A., Franchi, L., Kanneganti, T. D., Body-Malapel, M., Ozoren, N., Brady, G., et al. (2006). Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281, 35217-35223.
2. Bauernfeind, F. G., Horvath, G., Stutz, A., Alnemri, E. S., Macdonald, K., Speert, D., et al. (2009). Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 183, 787-791.
3. Brodsky, I. E., and Monack, D. (2009). NLR-mediated control of inflammasome assembly in the host response against bacterial pathogens. Semin. Immunol. 21, 199-207.
4. Broms, J. E., Meyer, L., Sun, K., Lavander, M., and Sjostedt, A. (2012). Unique substrates secreted by the type VI secretion system of Francisella tularensis during intramacrophage infection. PLoS ONE 7:e50473. doi: 10.1371/journal.pone.0050473
5. Broz, P., von Moltke, J., Jones, J. W., Vance, R. E., and Monack, D. M. (2010). Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 8, 471-483.
6. Brunette, R. L., Young, J. M., Whitley, D. G., Brodsky, I. E., Malik, H. S., and Stetson, D. B. (2012). Extensive evolutionary and functional diversity among mammalian AIM2-like receptors. J. Exp. Med. 209, 1969-1983.
7. Burckstummer, T., Baumann, C., Bluml, S., Dixit, E., Durnberger, G., Jahn, H., et al. (2009). An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10, 266-272.
8. Case, C. L., and Roy, C. R. (2011). Asc modulates the function of NLRC4 in response to infection of macrophages by Legionella pneumophila. MBio 2:e00117-11. doi: 10.1128/mBio.00117-11
9. Chong, A., Wehrly, T. D., Child, R., Hansen, B., Hwang, S., Virgin, H. W., et al. (2012). Cytosolic clearance of replication-deficient mutants reveals Francisella tularensis interactions with the autophagic pathway. Autophagy 8, 1342-1356.
10. Cole, L. E., Santiago, A., Barry, E., Kang, T. J., Shirey, K. A., Roberts, Z. J., et al. (2008). Macrophage proinflammatory response to Francisella tularensis live vaccine strain requires coordination of multiple signaling pathways. J. Immunol. 180, 6885-6891.
11. Coll, R. C., and O'Neill, L. A. (2010). New insights into the regulation of signalling by toll-like receptors and nod-like receptors. J. Innate Immun. 2, 406-421.
12. Dombrowski, Y., Peric, M., Koglin, S., Kammerbauer, C., Goss, C., Anz, D., et al. (2011). Cytosolic DNA triggers inflammasome activation in keratinocytes in psoriatic lesions. Sci. Transl. Med. 3:82ra38. doi: 10.1126/scitranslmed.3002001
13. Fernandes-Alnemri, T., and Alnemri, E. S. (2008). Assembly, purification, and assay of the activity of the ASC pyroptosome. Methods Enzymol. 442, 251-270.
14. Fernandes-Alnemri, T., Wu, J., Yu, J. W., Datta, P., Miller, B., Jankowski, W., et al. (2007). The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 14, 1590-1604.
15. Fernandes-Alnemri, T., Yu, J. W., Juliana, C., Solorzano, L., Kang, S., Wu, J., et al. (2010). The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 11, 385-393.
16. Fink, S. L., and Cookson, B. T. (2006). Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8, 1812-1825.
17. 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.
18. Hayakawa, S., Shiratori, S., Yamato, H., Kameyama, T., Kitatsuji, C., Kashigi, F., et al. (2011). ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses. Nat. Immunol. 12, 37-44.
19. Henry, T., Brotcke, A., Weiss, D. S., Thompson, L. J., and Monack, D. M. (2007). Type I interferon signaling is required for activation of the inflammasome during Francisella infection. J. Exp. Med. 204, 987-994.
20. Hornung, V., Ablasser, A., Charrel-Dennis, M., Bauernfeind, F., Horvath, G., Caffrey, D. R., et al. (2009). AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458, 514-518.
21. Jeru, I., Duquesnoy, P., Fernandes-Alnemri, T., Cochet, E., Yu, J. W., Lackmy-Port-Lis, M., et al. (2008). Mutations in NALP12 cause hereditary periodic fever syndromes. Proc. Natl. Acad. Sci. U.S.A. 105, 1614-1619.
22. Jin, T., Perry, A., Jiang, J., Smith, P., Curry, J. A., Unterholzner, L., et al. (2012). Structures of the HIN domain: DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36, 561-571.
23. Jones, C. L., and Weiss, D. S. (2011). TLR2 signaling contributes to rapid inflammasome activation during F. novicida infection. PLoS ONE 6:e20609. doi: 10.1371/journal.pone.0020609
24. Jones, J. W., Kayagaki, N., Broz, P., Henry, T., Newton, K., O'Rourke, K., et al. (2010). Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. U.S.A. 107, 9771-9776.
25. Kaiser, W. J., Upton, J. W., Long, A. B., Livingston-Rosanoff, D., Daley-Bauer, L. P., Hakem, R., et al. (2011). RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 471, 368-372.
26. Kayagaki, N., Warming, S., Lamkanfi, M., Vande Walle, L., Louie, S., Dong, J., et al. (2011). Non-canonical inflammasome activation targets caspase-11. Nature 479, 117-121.
27. Lamkanfi, M., Kalai, M., Saelens, X., Declercq, W., and Vandenabeele, P. (2004). Caspase-1 activates nuclear factor of the kappa-enhancer in B cells independently of its enzymatic activity. J. Biol. Chem. 279, 24785-24793.
28. Lightfield, K. L., Persson, J., Brubaker, S. W., Witte, C. E., Von Moltke, J., Dunipace, E. A., et al. (2008). Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 9, 1171-1178.
29. Lindgren, H., Golovliov, I., Baranov, V., Ernst, R. K., Telepnev, M., and Sjostedt, A. (2004). Factors affecting the escape of Francisella tularensis from the phagolysosome. J. Med. Microbiol. 53, 953-958.
30. Mariathasan, S., Newton, K., Monack, D. M., Vucic, D., French, D. M., Lee, W. P., et al. (2004). Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430, 213-218.
31. Mariathasan, S., Weiss, D. S., Dixit, V. M., and Monack, D. M. (2005). Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202, 1043-1049.
32. 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.
33. Martinet, W., Schrijvers, D. M., Herman, A. G., and De Meyer, G. R. (2006). z-VAD-fmk-induced non-apoptotic cell death of macrophages: possibilities and limitations for atherosclerotic plaque stabilization. Autophagy 2, 312-314.
34. 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.
35. Mason, D. R., Beck, P. L., and Muruve, D. A. (2012). Nucleotide-binding oligomerization domain-like receptors and inflammasomes in the pathogenesis of non-microbial inflammation and diseases. J. Innate Immun. 4, 16-30.
36. Nakahira, K., Haspel, J. A., Rathinam, V. A., Lee, S. J., Dolinay, T., Lam, H. C., et al. (2011). Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12, 222-230.
37. Nothelfer, K., Dias Rodrigues, C., Bobard, A., Phalipon, A., and Enninga, J. (2011). Monitoring Shigella flexneri vacuolar escape by flow cytometry. Virulence 2, 54-57.
38. Pierini, R., Juruj, C., Perret, M., Jones, C. L., Mangeot, P., Weiss, D. S., et al. (2012). AIM2/ASC triggers caspase-8-dependent apoptosis in Francisella-infected caspase-1-deficient macrophages. Cell Death Differ. 19, 1709-1721.
39. Puri, A. W., Broz, P., Shen, A., Monack, D. M., and Bogyo, M. (2012). Caspase-1 activity is required to bypass macrophage apoptosis upon Salmonella infection. Nat. Chem. Biol. 8, 745-747.
40. Rathinam, V. A., Jiang, Z., Waggoner, S. N., Sharma, S., Cole, L. E., Waggoner, L., et al. (2010). The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11, 395-402.
41. Rathinam, V. A., Vanaja, S. K., and Fitzgerald, K. A. (2012). Regulation of inflammasome signaling. Nat. Immunol. 13, 333-342.
42. Roberts, T. L., Idris, A., Dunn, J. A., Kelly, G. M., Burnton, C. M., Hodgson, S., et al. (2009). HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057-1060.
43. Saitoh, T., Fujita, N., Jang, M. H., Uematsu, S., Yang, B. G., Satoh, T., et al. (2008). Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456, 264-268.
44. Sauer, J. D., Witte, C. E., Zemansky, J., Hanson, B., Lauer, P., and Portnoy, D. A. (2010). Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7, 412-419.
45. Shi, C. S., Shenderov, K., Huang, N. N., Kabat, J., Abu-Asab, M., Fitzgerald, K. A., et al. (2012). Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 13, 255-263.
46. Torriglia, A., and Lepretre, C. (2009). LEI/L-DNase II: interplay between caspase-dependent and independent pathways. Front. Biosci. 14, 4836-4847.
47. Veeranki, S., Duan, X., Panchanathan, R., Liu, H., and Choubey, D. (2011). IFI16 Protein mediates the anti-inflammatory actions of the type-I interferons through suppression of activation of Caspase-1 by inflammasomes. PLoS ONE 6:e27040. doi: 10.1371/journal.pone.0027040
48. Walsh, J. G., Logue, S. E., Luthi, A. U., and Martin, S. J. (2011). Caspase-1 promiscuity is counterbalanced by rapid inactivation of processed enzyme. J. Biol. Chem. 286, 32513-32524.