The adaptor ASC has extracellular and 'prionoid' activities that propagate inflammation

Nature Immunology

Volumn 15, Issue 8, 2014, Pages 727-737

  Franklin, Bernardo S ^a   Bossaller, Lukas ^b,c   De Nardo, Dominic ^a   Ratter, Jacqueline M ^a   Stutz, Andrea ^a   Engels, Gudrun ^a   Brenker, Christoph ^d   Nordhoff, Mark ^d   Mirandola, Sandra R ^d   Al Amoudi, Ashraf ^d   Mangan, Matthew S ^a,d   Zimmer, Sebastian ^a   Monks, Brian G ^a,c   Fricke, Martin ^b   Schmidt, Reinhold E ^b   Espevik, Terje ^e   Jones, Bernadette ^f   Jarnicki, Andrew G ^f   Hansbro, Philip M ^f   Busto, Patricia ^c   Marshak Rothstein, Ann ^c   Hornemann, Simone ^g   Aguzzi, Adriano ^g   Kastenmüller, Wolfgang ^a   Latz, Eicke ^a,c,d,e   more..

^a UNIVERSITY OF BONN   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^f UNIVERSITY OF NEWCASTLE   (Australia)

^g UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR ASC PROTEIN; ADAPTOR PROTEIN; AUTOANTIBODY; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNE DISEASE; CELL COMMUNICATION; CELL DAMAGE; CELL DEATH; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; EXTRACELLULAR FLUID; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFLAMMATION; INFLAMMATORY DISEASE; LUNG LAVAGE; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PYROPTOSIS;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; ANTIBODIES; APOPTOSIS; AUTOANTIBODIES; AUTOIMMUNE DISEASES; CARRIER PROTEINS; CASPASE 1; CASPASE INHIBITORS; CELL COMMUNICATION; CYTOSKELETAL PROTEINS; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; LYSOSOMES; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; PHAGOCYTOSIS; PRIONS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SIGNAL TRANSDUCTION;

EID: 84904692363     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2913     Document Type: Article

References (48)

1. Takeda, K., Kaisho, T. & Akira, S. Toll-like receptors. Annu. Rev. Immunol. 21, 335-376 (2003).
2. Latz, E. et al. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13, 397-411 (2013).
3. Masumoto, J. et al. ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells. J. Biol. Chem. 274, 33835-33838 (1999).
4. Fernandes-Alnemri, T. et al. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 14, 1590-1604 (2007).
5. Lu, A. et al. Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell 156, 1193-1206 (2014).
6. Cai, X. et al. Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell 156, 1207-1222 (2014).
7. Matsushita, K. et al. A splice variant of ASC regulates IL-1 release and aggregates differently from intact ASC. Mediators Inflamm. 2009, 287387 (2009).
8. Wu, H. Higher-order assemblies in a new paradigm of signal transduction. Cell 153, 287-292 (2013).
9. Proell, M., Gerlic, M., Mace, P.D., Reed, J.C. & Riedl, S.J. The CARD plays a critical role in ASC foci formation and inflammasome signalling. Biochem. J. 449, 613-621 (2013).
10. Faustin, B. et al. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol. Cell 25, 713-724 (2007).
11. Bergsbaken, T. et al. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7, 99-109 (2009).
12. Keller, M., Ruegg, A., Werner, S. & Beer, H.-D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 132, 818-831 (2008).
13. Balci-Peynircioglu, B. et al. Expression of ASC in renal tissues of familial Mediterranean fever patients with amyloidosis: postulating a role for ASC in AA type amyloid deposition. Exp. Biol. Med. (Maywood ) 233, 1324-1333 (2008).
14. Stutz, A., Horvath, G.L., Monks, B.G. & Latz, E. ASC speck formation as a readout for inflammasome activation. Methods Mol. Biol. 1040, 91-101 (2013).
15. Jakobs, C., Bartok, E., Kubarenko, A., Bauernfeind, F. & Hornung, V. Immunoblotting for active caspase-1. Methods Mol. Biol. 1040, 103-115 (2012).
16. Lima-Junior, D.S. et al. Inflammasome-derived IL-1 production induces nitric oxide-mediated resistance to Leishmania. Nat. Med. 19, 909-915 (2013).
17. Halle, A. et al. The NALP3 inflammasome is involved in the innate immune response to amyloid. Nat. Immunol. 9, 857-865 (2008).
18. Sheedy, F.J. et al. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat. Immunol. 14, 812-820 (2013).
19. Westwell-Roper, C., Dunne, A., Kim, M.L., Verchere, C.B. & Masters, S.L. Activating the NLRP3 inflammasome using the amyloidogenic peptide IAPP. Methods Mol. Biol. 1040, 9-18 (2013).
20. Duewell, P. et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361 (2010).
21. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856 (2008).
22. Martinon, F. et al. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241 (2006).
23. Dostert, C. et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674-677 (2008).
24. Masters, S.L. et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1 in type 2 diabetes. Nat. Immunol. 11, 897-904 (2010).
25. Duewell, P., Duewell, P., Latz, E. & Latz, E. Assessment and quantification of crystal-induced lysosomal damage. Methods Mol. Biol. 1040, 19-27 (2013).
26. Aguzzi, A. Cell biology: Beyond the prion principle. Nature 459, 924-925 (2009).
27. Hofmann, J.P. et al. Cell-to-cell propagation of infectious cytosolic protein aggregates. Proc. Natl. Acad. Sci. USA 110, 5951-5956 (2013).
28. Aguzzi, A., Nuvolone, M. & Zhu, C. The immunobiology of prion diseases. Nat. Rev. Immunol. 13, 888-902 (2013).
29. Aguzzi, A. & Falsig, J. Prion propagation, toxicity and degradation. Nat. Neurosci. 15, 936-939 (2012).
30. Wang, X. et al. The molecular basis of functional bacterial amyloid polymerization and nucleation. J. Biol. Chem. 283, 21530-21539 (2008).
31. Holmes, B.B. & Diamond, M.I. Cellular mechanisms of protein aggregate propagation. Curr. Opin. Neurol. 25, 721-726 (2012).
32. Sutterwala, F.S. et al. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 204, 3235-3245 (2007).
33. De Nardo, D., De Nardo, C.M. & Latz, E. New insights into mechanisms controlling the NLRP3 inflammasome and its role in lung disease. Am. J. Pathol. 184, 42-54 (2013).
34. Botelho, F.M. et al. IL-1/IL-1R1 expression in chronic obstructive pulmonary disease and mechanistic relevance to smoke-induced neutrophilia in mice. PLoS ONE 6, e28457 (2011).
35. Sci, E. et al. A new short-term mouse model of chronic obstructive pulmonary disease identifies a role for mast cell tryptase in pathogenesis. J. Allergy Clin. Immunol. 131, 752-762 (2013).
36. Marshak-Rothstein, A. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6, 823-835 (2006).
37. Leiss, H. et al. Pristane-induced lupus as a model of human lupus arthritis: evolvement of autoantibodies, internal organ and joint inflammation. CORD Conf. Proc. 22, 778-792 (2012).
38. Hou, F. et al. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146, 448-461 (2011).
39. Li, J. et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 150, 339-350 (2012).
40. Wu, B. et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 152, 276-289 (2012).
41. Bakele, M. et al. Localization and functionality of the inflammasome in neutrophils. J. Biol. Chem. 289, 5320-5329 (2014).
42. Adamczak, S. et al. Inflammasome proteins in cerebrospinal fluid of brain-injured patients as biomarkers of functional outcome. J. Neurosurg. 117, 1119-1125 (2012).
43. Meissner, F., Molawi, K. & Zychlinsky, A. Superoxide dismutase 1 regulates caspase-1 and endotoxic shock. Nat. Immunol. 9, 866-872 (2008).
44. de Rivero Vaccari, J.P. et al. A molecular platform in neurons regulates inflammation after spinal cord injury. J. Neurosci. 28, 3404-3414 (2008).
45. de Rivero Vaccari, J.P. et al. Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J. Cereb. Blood Flow Metab. 29, 1251-1261 (2009).
46. Stewart, C.R. et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 11, 155-161 (2010).
47. Fernandes-Alnemri, T., Fernandes-Alnemri, T., Alnemri, E.S. & Alnemri, E.S. Assembly, purification, and assay of the activity of the ASC pyroptosome. Methods Enzymol. 442, 251-270 (2008).
48. Kastenmüller, W., Torabi-Parizi, P., Subramanian, N., Lämmermann, T. & Germain, R.N.A. Spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread. Cell 150, 1235-1248 (2012).