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Review article: Biomedical intelligence

Vol. 147 No. 1516 (2017)

Prions, prionoid complexes and amyloids: the bad, the good and something in between

DOI
https://doi.org/10.4414/smw.2017.14424
Cite this as:
Swiss Med Wkly. 2017;147:w14424
Published
18.04.2017

Summary

Prions are infectious agents causing transmissible spongiform encephalopathies in humans and animals. These protein-based particles template conformational changes in a host-encoded prion protein to an insoluble self-like conformation. Prions are also present in yeast, where they support protein-based epigenetic inheritance. There is emerging evidence that prion-like (prionoid) particles can support a variety of pathological and beneficial functions. The recent data on the prionoid spread of other pathological amyloids are discussed in light of differences between prions and prion-like aggregates. On the other hand, prion-like action has also been found to support important functions such as memory, and amyloids were shown to have a variety of physiological roles from storage to scaffolding in simple organisms and in humans. Higher-order protein complexes play important roles in signalling. Many death-fold domains can polymerise upon nucleation to enhance sensitivity and induce a robust response. Although these polymers are structurally different from amyloids, some of them are characterised by prionoid activities, such as intercellular spread. The initial activation of these complexes is vital for organismal health, whereas prolonged activation leading to unresolved inflammation underlies autoinflammatory and other diseases. Prionoid complexes play important roles far beyond prion diseases and neurodegeneration.

References

  1. Chiti F, Dobson CM. Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem. 2006;75(1):333–66. https://doi.org/10.1146/annurev.biochem.75.101304.123901
  2. Sipe JD, Benson MD, Buxbaum JN, Ikeda S, Merlini G, Saraiva MJ, et al.; Nomenclature Committee of the International Society of Amyloidosis. Amyloid fibril protein nomenclature: 2012 recommendations from the Nomenclature Committee of the International Society of Amyloidosis. Amyloid. 2012;19(4):167–70. https://doi.org/10.3109/13506129.2012.734345
  3. Eisenberg D, Jucker M. The amyloid state of proteins in human diseases. Cell. 2012;148(6):1188–203. https://doi.org/10.1016/j.cell.2012.02.022
  4. Chiti F, Webster P, Taddei N, Clark A, Stefani M, Ramponi G, et al. Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc Natl Acad Sci USA. 1999;96(7):3590–4. https://doi.org/10.1073/pnas.96.7.3590
  5. Xiao Y, Ma B, McElheny D, Parthasarathy S, Long F, Hoshi M, et al. Aβ(1-42) fibril structure illuminates self-recognition and replication of amyloid in Alzheimer’s disease. Nat Struct Mol Biol. 2015;22(6):499–505. https://doi.org/10.1038/nsmb.2991
  6. Van Melckebeke H, Wasmer C, Lange A, Ab E, Loquet A, Böckmann A, et al. Atomic-resolution three-dimensional structure of HET-s(218-289) amyloid fibrils by solid-state NMR spectroscopy. J Am Chem Soc. 2010;132(39):13765–75. https://doi.org/10.1021/ja104213j
  7. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004;25(13):1605–12. https://doi.org/10.1002/jcc.20084
  8. Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CC. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol. 1997;273(3):729–39. https://doi.org/10.1006/jmbi.1997.1348
  9. Benzinger TL, Gregory DM, Burkoth TS, Miller-Auer H, Lynn DG, Botto RE, et al. Propagating structure of Alzheimer’s beta-amyloid(10-35) is parallel beta-sheet with residues in exact register. Proc Natl Acad Sci USA. 1998;95(23):13407–12. https://doi.org/10.1073/pnas.95.23.13407
  10. Tycko R. Solid-state NMR studies of amyloid fibril structure. Annu Rev Phys Chem. 2011;62(1):279–99. https://doi.org/10.1146/annurev-physchem-032210-103539
  11. Makin OS, Atkins E, Sikorski P, Johansson J, Serpell LC. Molecular basis for amyloid fibril formation and stability. Proc Natl Acad Sci USA. 2005;102(2):315–20. https://doi.org/10.1073/pnas.0406847102
  12. Nelson R, Sawaya MR, Balbirnie M, Madsen AO, Riekel C, Grothe R, et al. Structure of the cross-beta spine of amyloid-like fibrils. Nature. 2005;435(7043):773–8. https://doi.org/10.1038/nature03680
  13. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, Apostol MI, et al. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature. 2007;447(7143):453–7. https://doi.org/10.1038/nature05695
  14. Wu H, Fuxreiter M. The Structure and Dynamics of Higher-Order Assemblies: Amyloids, Signalosomes, and Granules. Cell. 2016;165(5):1055–66. https://doi.org/10.1016/j.cell.2016.05.004
  15. Knowles TP, Waudby CA, Devlin GL, Cohen SI, Aguzzi A, Vendruscolo M, et al. An analytical solution to the kinetics of breakable filament assembly. Science. 2009;326(5959):1533–7. https://doi.org/10.1126/science.1178250
  16. Arosio P, Knowles TP, Linse S. On the lag phase in amyloid fibril formation. Phys Chem Chem Phys. 2015;17(12):7606–18. https://doi.org/10.1039/C4CP05563B
  17. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science. 1982;216(4542):136–44. https://doi.org/10.1126/science.6801762
  18. Wang F, Wang X, Yuan CG, Ma J. Generating a prion with bacterially expressed recombinant prion protein. Science. 2010;327(5969):1132–5. https://doi.org/10.1126/science.1183748
  19. Baker HF, Ridley RM, Duchen LW, Crow TJ, Bruton CJ. Experimental induction of beta-amyloid plaques and cerebral angiopathy in primates. Ann N Y Acad Sci. 1993;695(1):228–31. https://doi.org/10.1111/j.1749-6632.1993.tb23057.x
  20. Baker HF, Ridley RM, Duchen LW, Crow TJ, Bruton CJ. Induction of beta (A4)-amyloid in primates by injection of Alzheimer’s disease brain homogenate. Comparison with transmission of spongiform encephalopathy. Mol Neurobiol. 1994;8(1):25–39. https://doi.org/10.1007/BF02778005
  21. Baker HF, Ridley RM, Wells GA. Experimental transmission of BSE and scrapie to the common marmoset. Vet Rec. 1993;132(16):403–6. https://doi.org/10.1136/vr.132.16.403
  22. Eisele YS, Bolmont T, Heikenwalder M, Langer F, Jacobson LH, Yan ZX, et al. Induction of cerebral beta-amyloidosis: intracerebral versus systemic Abeta inoculation. Proc Natl Acad Sci USA. 2009;106(31):12926–31. https://doi.org/10.1073/pnas.0903200106
  23. Eisele YS, Obermüller U, Heilbronner G, Baumann F, Kaeser SA, Wolburg H, et al. Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science. 2010;330(6006):980–2. https://doi.org/10.1126/science.1194516
  24. Langer F, Eisele YS, Fritschi SK, Staufenbiel M, Walker LC, Jucker M. Soluble Aβ seeds are potent inducers of cerebral β-amyloid deposition. J Neurosci. 2011;31(41):14488–95. https://doi.org/10.1523/JNEUROSCI.3088-11.2011
  25. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E, et al. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science. 2006;313(5794):1781–4. https://doi.org/10.1126/science.1131864
  26. Watts JC, Condello C, Stöhr J, Oehler A, Lee J, DeArmond SJ, et al. Serial propagation of distinct strains of Aβ prions from Alzheimer’s disease patients. Proc Natl Acad Sci USA. 2014;111(28):10323–8. https://doi.org/10.1073/pnas.1408900111
  27. Stöhr J, Condello C, Watts JC, Bloch L, Oehler A, Nick M, et al. Distinct synthetic Aβ prion strains producing different amyloid deposits in bigenic mice. Proc Natl Acad Sci USA. 2014;111(28):10329–34. https://doi.org/10.1073/pnas.1408968111
  28. Iba M, Guo JL, McBride JD, Zhang B, Trojanowski JQ, Lee VM. Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer’s-like tauopathy. J Neurosci. 2013;33(3):1024–37. https://doi.org/10.1523/JNEUROSCI.2642-12.2013
  29. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol. 2009;11(7):909–13. https://doi.org/10.1038/ncb1901
  30. Peeraer E, Bottelbergs A, Van Kolen K, Stancu IC, Vasconcelos B, Mahieu M, et al. Intracerebral injection of preformed synthetic tau fibrils initiates widespread tauopathy and neuronal loss in the brains of tau transgenic mice. Neurobiol Dis. 2015;73:83–95. https://doi.org/10.1016/j.nbd.2014.08.032
  31. Sanders DW, Kaufman SK, DeVos SL, Sharma AM, Mirbaha H, Li A, et al. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron. 2014;82(6):1271–88. https://doi.org/10.1016/j.neuron.2014.04.047
  32. Luk KC, Kehm VM, Zhang B, O’Brien P, Trojanowski JQ, Lee VM. Intracerebral inoculation of pathological α-synuclein initiates a rapidly progressive neurodegenerative α-synucleinopathy in mice. J Exp Med. 2012;209(5):975–86. https://doi.org/10.1084/jem.20112457
  33. Masuda-Suzukake M, Nonaka T, Hosokawa M, Oikawa T, Arai T, Akiyama H, et al. Prion-like spreading of pathological α-synuclein in brain. Brain. 2013;136(Pt 4):1128–38. https://doi.org/10.1093/brain/awt037
  34. Sacino AN, Brooks M, McGarvey NH, McKinney AB, Thomas MA, Levites Y, et al. Induction of CNS α-synuclein pathology by fibrillar and non-amyloidogenic recombinant α-synuclein. Acta Neuropathol Commun. 2013;1(1):38. https://doi.org/10.1186/2051-5960-1-38
  35. Jones DR, Delenclos M, Baine AT, DeTure M, Murray ME, Dickson DW, et al. Transmission of Soluble and Insoluble α-Synuclein to Mice. J Neuropathol Exp Neurol. 2015;74(12):1158–69.
  36. Prusiner SB, Woerman AL, Mordes DA, Watts JC, Rampersaud R, Berry DB, et al. Evidence for α-synuclein prions causing multiple system atrophy in humans with parkinsonism. Proc Natl Acad Sci USA. 2015;112(38):E5308–17. https://doi.org/10.1073/pnas.1514475112
  37. Lundmark K, Westermark GT, Nyström S, Murphy CL, Solomon A, Westermark P. Transmissibility of systemic amyloidosis by a prion-like mechanism. Proc Natl Acad Sci USA. 2002;99(10):6979–84. Erratum in: Proc Natl Acad Sci U S A. 2003 Mar 18;100(6):3543.https://doi.org/10.1073/pnas.092205999
  38. Solomon A, Richey T, Murphy CL, Weiss DT, Wall JS, Westermark GT, et al. Amyloidogenic potential of foie gras. Proc Natl Acad Sci USA. 2007;104(26):10998–1001. https://doi.org/10.1073/pnas.0700848104
  39. Zhang B, Une Y, Fu X, Yan J, Ge F, Yao J, et al. Fecal transmission of AA amyloidosis in the cheetah contributes to high incidence of disease. Proc Natl Acad Sci USA. 2008;105(20):7263–8. https://doi.org/10.1073/pnas.0800367105
  40. Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM, Miniaci MC, et al. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell. 2003;115(7):893–904. https://doi.org/10.1016/S0092-8674(03)01021-3
  41. Si K, Lindquist S, Kandel ER. A neuronal isoform of the aplysia CPEB has prion-like properties. Cell. 2003;115(7):879–91. https://doi.org/10.1016/S0092-8674(03)01020-1
  42. Si K, Choi YB, White-Grindley E, Majumdar A, Kandel ER. Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell. 2010;140(3):421–35. https://doi.org/10.1016/j.cell.2010.01.008
  43. Keleman K, Krüttner S, Alenius M, Dickson BJ. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci. 2007;10(12):1587–93. https://doi.org/10.1038/nn1996
  44. Majumdar A, Cesario WC, White-Grindley E, Jiang H, Ren F, Khan MR, et al. Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell. 2012;148(3):515–29. https://doi.org/10.1016/j.cell.2012.01.004
  45. Fioriti L, Myers C, Huang YY, Li X, Stephan JS, Trifilieff P, et al. The Persistence of Hippocampal-Based Memory Requires Protein Synthesis Mediated by the Prion-like Protein CPEB3. Neuron. 2015;86(6):1433–48. https://doi.org/10.1016/j.neuron.2015.05.021
  46. Stephan JS, Fioriti L, Lamba N, Colnaghi L, Karl K, Derkatch IL, et al. The CPEB3 Protein Is a Functional Prion that Interacts with the Actin Cytoskeleton. Cell Reports. 2015;11(11):1772–85. https://doi.org/10.1016/j.celrep.2015.04.060
  47. Drisaldi B, Colnaghi L, Fioriti L, Rao N, Myers C, Snyder AM, et al. SUMOylation Is an Inhibitory Constraint that Regulates the Prion-like Aggregation and Activity of CPEB3. Cell Reports. 2015;11(11):1694–702. https://doi.org/10.1016/j.celrep.2015.04.061
  48. Chakrabortee S, Kayatekin C, Newby GA, Mendillo ML, Lancaster A, Lindquist S. Luminidependens (LD) is an Arabidopsis protein with prion behavior. Proc Natl Acad Sci USA. 2016;113(21):6065–70. https://doi.org/10.1073/pnas.1604478113
  49. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, et al. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science. 2002;295(5556):851–5. https://doi.org/10.1126/science.1067484
  50. Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Rev Microbiol. 2006;60(1):131–47. https://doi.org/10.1146/annurev.micro.60.080805.142106
  51. Hammer ND, Schmidt JC, Chapman MR. The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc Natl Acad Sci USA. 2007;104(30):12494–9. https://doi.org/10.1073/pnas.0703310104
  52. Robinson LS, Ashman EM, Hultgren SJ, Chapman MR. Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein. Mol Microbiol. 2006;59(3):870–81. https://doi.org/10.1111/j.1365-2958.2005.04997.x
  53. Nenninger AA, Robinson LS, Hultgren SJ. Localized and efficient curli nucleation requires the chaperone-like amyloid assembly protein CsgF. Proc Natl Acad Sci USA. 2009;106(3):900–5. https://doi.org/10.1073/pnas.0812143106
  54. Nenninger AA, Robinson LS, Hammer ND, Epstein EA, Badtke MP, Hultgren SJ, et al. CsgE is a curli secretion specificity factor that prevents amyloid fibre aggregation. Mol Microbiol. 2011;81(2):486–99. https://doi.org/10.1111/j.1365-2958.2011.07706.x
  55. Zhou Y, Smith D, Leong BJ, Brännström K, Almqvist F, Chapman MR. Promiscuous cross-seeding between bacterial amyloids promotes interspecies biofilms. J Biol Chem. 2012;287(42):35092–103. https://doi.org/10.1074/jbc.M112.383737
  56. Branda SS, Chu F, Kearns DB, Losick R, Kolter R. A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol. 2006;59(4):1229–38. https://doi.org/10.1111/j.1365-2958.2005.05020.x
  57. Romero D, Aguilar C, Losick R, Kolter R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA. 2010;107(5):2230–4. https://doi.org/10.1073/pnas.0910560107
  58. Romero D, Vlamakis H, Losick R, Kolter R. An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol. 2011;80(5):1155–68. https://doi.org/10.1111/j.1365-2958.2011.07653.x
  59. Stöver AG, Driks A. Secretion, localization, and antibacterial activity of TasA, a Bacillus subtilis spore-associated protein. J Bacteriol. 1999;181(5):1664–72.
  60. Kearns DB, Chu F, Branda SS, Kolter R, Losick R. A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol. 2005;55(3):739–49. https://doi.org/10.1111/j.1365-2958.2004.04440.x
  61. Iconomidou VA, Vriend G, Hamodrakas SJ. Amyloids protect the silkmoth oocyte and embryo. FEBS Lett. 2000;479(3):141–5. https://doi.org/10.1016/S0014-5793(00)01888-3
  62. Hamodrakas SJ, Hoenger A, Iconomidou VA. Amyloid fibrillogenesis of silkmoth chorion protein peptide-analogues via a liquid-crystalline intermediate phase. J Struct Biol. 2004;145(3):226–35. https://doi.org/10.1016/j.jsb.2003.10.004
  63. Kenney JM, Knight D, Wise MJ, Vollrath F. Amyloidogenic nature of spider silk. Eur J Biochem. 2002;269(16):4159–63. https://doi.org/10.1046/j.1432-1033.2002.03112.x
  64. Knight DP, Knight MM, Vollrath F. Beta transition and stress-induced phase separation in the spinning of spider dragline silk. Int J Biol Macromol. 2000;27(3):205–10. https://doi.org/10.1016/S0141-8130(00)00124-0
  65. Vollrath F, Knight DP. Liquid crystalline spinning of spider silk. Nature. 2001;410(6828):541–8. https://doi.org/10.1038/35069000
  66. Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K, Rissman RA, et al. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science. 2009;325(5938):328–32. https://doi.org/10.1126/science.1173155
  67. Boke E, Ruer M, Wühr M, Coughlin M, Lemaitre R, Gygi SP, et al. Amyloid-like Self-Assembly of a Cellular Compartment. Cell. 2016;166(3):637–50. https://doi.org/10.1016/j.cell.2016.06.051
  68. Giraldo R. Defined DNA sequences promote the assembly of a bacterial protein into distinct amyloid nanostructures. Proc Natl Acad Sci USA. 2007;104(44):17388–93. https://doi.org/10.1073/pnas.0702006104
  69. Fernández-Tresguerres ME, de la Espina SM, Gasset-Rosa F, Giraldo R. A DNA-promoted amyloid proteinopathy in Escherichia coli. Mol Microbiol. 2010;77(6):1456–69. https://doi.org/10.1111/j.1365-2958.2010.07299.x
  70. Gasset-Rosa F, Coquel AS, Moreno-Del Álamo M, Chen P, Song X, Serrano AM, et al. Direct assessment in bacteria of prionoid propagation and phenotype selection by Hsp70 chaperone. Mol Microbiol. 2014;91(6):1070–87. https://doi.org/10.1111/mmi.12518
  71. Molina-García L, Gasset-Rosa F, Moreno-Del Álamo M, Fernández-Tresguerres ME, Moreno-Díaz de la Espina S, Lurz R, et al. Functional amyloids as inhibitors of plasmid DNA replication. Sci Rep. 2016;6:25425. https://doi.org/10.1038/srep25425
  72. Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, Kelly JW. Functional amyloid formation within mammalian tissue. PLoS Biol. 2005;4(1):e6. https://doi.org/10.1371/journal.pbio.0040006
  73. Wickner RB. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science. 1994;264(5158):566–9. https://doi.org/10.1126/science.7909170
  74. Patino MM, Liu JJ, Glover JR, Lindquist S. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science. 1996;273(5275):622–6. https://doi.org/10.1126/science.273.5275.622
  75. Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. In vitro propagation of the prion-like state of yeast Sup35 protein. Science. 1997;277(5324):381–3. https://doi.org/10.1126/science.277.5324.381
  76. Sparrer HE, Santoso A, Szoka FC, Jr, Weissman JS. Evidence for the prion hypothesis: induction of the yeast [PSI+] factor by in vitro- converted Sup35 protein. Science. 2000;289(5479):595–9. https://doi.org/10.1126/science.289.5479.595
  77. Bradley ME, Edskes HK, Hong JY, Wickner RB, Liebman SW. Interactions among prions and prion “strains” in yeast. Proc Natl Acad Sci USA. 2002;99(Suppl 4):16392–9. https://doi.org/10.1073/pnas.152330699
  78. Tanaka M, Collins SR, Toyama BH, Weissman JS. The physical basis of how prion conformations determine strain phenotypes. Nature. 2006;442(7102):585–9. https://doi.org/10.1038/nature04922
  79. Cai X, Chen J, Xu H, Liu S, Jiang QX, Halfmann R, et al. Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell. 2014;156(6):1207–22. https://doi.org/10.1016/j.cell.2014.01.063
  80. Hou F, Sun L, Zheng H, Skaug B, Jiang QX, Chen ZJ. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell. 2011;146(3):448–61. https://doi.org/10.1016/j.cell.2011.06.041
  81. Seth RB, Sun L, Ea CK, Chen ZJ. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell. 2005;122(5):669–82. https://doi.org/10.1016/j.cell.2005.08.012
  82. Tang ED, Wang CY. MAVS self-association mediates antiviral innate immune signaling. J Virol. 2009;83(8):3420–8. https://doi.org/10.1128/JVI.02623-08
  83. Xu H, He X, Zheng H, Huang LJ, Hou F, Yu Z, et al. Structural basis for the prion-like MAVS filaments in antiviral innate immunity. eLife. 2014;3:e01489. https://doi.org/10.7554/eLife.01489
  84. Hu Z, Zhou Q, Zhang C, Fan S, Cheng W, Zhao Y, et al. Structural and biochemical basis for induced self-propagation of NLRC4. Science. 2015;350(6259):399–404. https://doi.org/10.1126/science.aac5489
  85. Zhang L, Chen S, Ruan J, Wu J, Tong AB, Yin Q, et al. Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization. Science. 2015;350(6259):404–9. https://doi.org/10.1126/science.aac5789
  86. Diebolder CA, Halff EF, Koster AJ, Huizinga EG, Koning RI. Cryoelectron Tomography of the NAIP5/NLRC4 Inflammasome: Implications for NLR Activation. Structure. 2015;23(12):2349–57. https://doi.org/10.1016/j.str.2015.10.001
  87. Lu A, Magupalli VG, Ruan J, Yin Q, Atianand MK, Vos MR, et al. Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell. 2014;156(6):1193–206. https://doi.org/10.1016/j.cell.2014.02.008
  88. Baroja-Mazo A, Martín-Sánchez F, Gomez AI, Martínez CM, Amores-Iniesta J, Compan V, et al. The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol. 2014;15(8):738–48. https://doi.org/10.1038/ni.2919
  89. Franklin BS, Bossaller L, De Nardo D, Ratter JM, Stutz A, Engels G, et al. The adaptor ASC has extracellular and ‘prionoid’ activities that propagate inflammation. Nat Immunol. 2014;15(8):727–37. https://doi.org/10.1038/ni.2913
  90. Li J, McQuade T, Siemer AB, Napetschnig J, Moriwaki K, Hsiao YS, et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell. 2012;150(2):339–50. https://doi.org/10.1016/j.cell.2012.06.019
  91. Aguzzi A, Polymenidou M. Mammalian prion biology: one century of evolving concepts. Cell. 2004;116(2):313–27. https://doi.org/10.1016/S0092-8674(03)01031-6
  92. Prusiner SB. Prions. Proc Natl Acad Sci USA. 1998;95(23):13363–83. https://doi.org/10.1073/pnas.95.23.13363
  93. Aguzzi A, Calella AM. Prions: protein aggregation and infectious diseases. Physiol Rev. 2009;89(4):1105–52. https://doi.org/10.1152/physrev.00006.2009
  94. Küffer A, Lakkaraju AK, Mogha A, Petersen SC, Airich K, Doucerain C, et al. The prion protein is an agonistic ligand of the G protein-coupled receptor Adgrg6. Nature. 2016;536(7617):464–8. https://doi.org/10.1038/nature19312
  95. Brown P, Brandel JP, Sato T, Nakamura Y, MacKenzie J, Will RG, et al. Iatrogenic Creutzfeldt-Jakob disease, final assessment. Emerg Infect Dis. 2012;18(6):901–7. https://doi.org/10.3201/eid1806.120116
  96. Gajdusek DC, Gibbs CJ, Alpers M. Experimental transmission of a Kuru-like syndrome to chimpanzees. Nature. 1966;209(5025):794–6. https://doi.org/10.1038/209794a0
  97. Griffith JS. Self-replication and scrapie. Nature. 1967;215(5105):1043–4. https://doi.org/10.1038/2151043a0
  98. Büeler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, et al. Mice devoid of PrP are resistant to scrapie. Cell. 1993;73(7):1339–47. https://doi.org/10.1016/0092-8674(93)90360-3
  99. Collinge J. Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci. 2001;24(1):519–50. https://doi.org/10.1146/annurev.neuro.24.1.519
  100. Eraña H, Castilla J. The architecture of prions: how understanding would provide new therapeutic insights. Swiss Med Wkly. 2016;146:w14354.
  101. Caughey B, Raymond GJ, Bessen RA. Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J Biol Chem. 1998;273(48):32230–5. https://doi.org/10.1074/jbc.273.48.32230
  102. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, DeArmond SJ, et al. Synthetic mammalian prions. Science. 2004;305(5684):673–6. https://doi.org/10.1126/science.1100195
  103. Colby DW, Giles K, Legname G, Wille H, Baskakov IV, DeArmond SJ, et al. Design and construction of diverse mammalian prion strains. Proc Natl Acad Sci USA. 2009;106(48):20417–22. https://doi.org/10.1073/pnas.0910350106
  104. Makarava N, Kovacs GG, Bocharova O, Savtchenko R, Alexeeva I, Budka H, et al. Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol. 2010;119(2):177–87. https://doi.org/10.1007/s00401-009-0633-x
  105. Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature. 2001;411(6839):810–3. https://doi.org/10.1038/35081095
  106. Castilla J, Saá P, Hetz C, Soto C. In vitro generation of infectious scrapie prions. Cell. 2005;121(2):195–206. https://doi.org/10.1016/j.cell.2005.02.011
  107. Atarashi R, Moore RA, Sim VL, Hughson AG, Dorward DW, Onwubiko HA, et al. Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat Methods. 2007;4(8):645–50. https://doi.org/10.1038/nmeth1066
  108. Zhang Z, Zhang Y, Wang F, Wang X, Xu Y, Yang H, et al. De novo generation of infectious prions with bacterially expressed recombinant prion protein. FASEB J. 2013;27(12):4768–75. https://doi.org/10.1096/fj.13-233965
  109. Guo JL, Lee VM. Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nat Med. 2014;20(2):130–8. https://doi.org/10.1038/nm.3457
  110. Eraña H, Venegas V, Moreno J, Castilla J. Prion-like disorders and Transmissible Spongiform Encephalopathies: An overview of the mechanistic features that are shared by the various disease-related misfolded proteins. Biochem Biophys Res Commun. 2016;S0006-291X(16)31430-9. 10.1016/j.bbrc.2016.08.166
  111. Ashe KH, Aguzzi A. Prions, prionoids and pathogenic proteins in Alzheimer disease. Prion. 2013;7(1):55–9. https://doi.org/10.4161/pri.23061
  112. Aguzzi A, Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron. 2009;64(6):783–90. https://doi.org/10.1016/j.neuron.2009.12.016
  113. Chia R, Tattum MH, Jones S, Collinge J, Fisher EM, Jackson GS. Superoxide dismutase 1 and tgSOD1 mouse spinal cord seed fibrils, suggesting a propagative cell death mechanism in amyotrophic lateral sclerosis. PLoS One. 2010;5(5):e10627. https://doi.org/10.1371/journal.pone.0010627
  114. Laferriere F, Polymenidou M. Advances and challenges in understanding the multifaceted pathogenesis of amyotrophic lateral sclerosis. Swiss Med Wkly. 2015;145:w14054.
  115. Nussbaum JM, Schilling S, Cynis H, Silva A, Swanson E, Wangsanut T, et al. Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-β. Nature. 2012;485(7400):651–5. https://doi.org/10.1038/nature11060
  116. Jaunmuktane Z, Mead S, Ellis M, Wadsworth JD, Nicoll AJ, Kenny J, et al. Evidence for human transmission of amyloid-β pathology and cerebral amyloid angiopathy. Nature. 2015;525(7568):247–50. https://doi.org/10.1038/nature15369
  117. Frontzek K, Lutz MI, Aguzzi A, Kovacs GG, Budka H. Amyloid-β pathology and cerebral amyloid angiopathy are frequent in iatrogenic Creutzfeldt-Jakob disease after dural grafting. Swiss Med Wkly. 2016;146:w14287.
  118. Liebman SW, Chernoff YO. Prions in yeast. Genetics. 2012;191(4):1041–72. https://doi.org/10.1534/genetics.111.137760
  119. Wickner RB. Yeast and Fungal Prions. Cold Spring Harb Perspect Biol. 2016;8(9):a023531. https://doi.org/10.1101/cshperspect.a023531
  120. Masison DC, Wickner RB. Prion-inducing domain of yeast Ure2p and protease resistance of Ure2p in prion-containing cells. Science. 1995;270(5233):93–5. https://doi.org/10.1126/science.270.5233.93
  121. Michelitsch MD, Weissman JS. A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions. Proc Natl Acad Sci USA. 2000;97(22):11910–5. https://doi.org/10.1073/pnas.97.22.11910
  122. Sondheimer N, Lindquist S. Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell. 2000;5(1):163–72. https://doi.org/10.1016/S1097-2765(00)80412-8
  123. Tuite MF. Yeast prions and their prion-forming domain. Cell. 2000;100(3):289–92. https://doi.org/10.1016/S0092-8674(00)80663-7
  124. Alberti S, Halfmann R, King O, Kapila A, Lindquist S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell. 2009;137(1):146–58. https://doi.org/10.1016/j.cell.2009.02.044
  125. Wickner RB, Kelly AC. Prions are affected by evolution at two levels. Cell Mol Life Sci. 2016;73(6):1131–44. https://doi.org/10.1007/s00018-015-2109-6
  126. Krammer C, Kryndushkin D, Suhre MH, Kremmer E, Hofmann A, Pfeifer A, et al. The yeast Sup35NM domain propagates as a prion in mammalian cells. Proc Natl Acad Sci USA. 2009;106(2):462–7. https://doi.org/10.1073/pnas.0811571106
  127. Hofmann JP, Denner P, Nussbaum-Krammer C, Kuhn PH, Suhre MH, Scheibel T, et al. Cell-to-cell propagation of infectious cytosolic protein aggregates. Proc Natl Acad Sci USA. 2013;110(15):5951–6. https://doi.org/10.1073/pnas.1217321110
  128. de Moor CH, Richter JD. Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J. 1999;18(8):2294–303. https://doi.org/10.1093/emboj/18.8.2294
  129. Miniaci MC, Kim JH, Puthanveettil SV, Si K, Zhu H, Kandel ER, et al. Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron. 2008;59(6):1024–36. https://doi.org/10.1016/j.neuron.2008.07.036
  130. Fiumara F, Rajasethupathy P, Antonov I, Kosmidis S, Sossin WS, Kandel ER. MicroRNA-22 Gates Long-Term Heterosynaptic Plasticity in Aplysia through Presynaptic Regulation of CPEB and Downstream Targets. Cell Reports. 2015;11(12):1866–75. https://doi.org/10.1016/j.celrep.2015.05.034
  131. White-Grindley E, Li L, Mohammad Khan R, Ren F, Saraf A, Florens L, et al. Contribution of Orb2A stability in regulated amyloid-like oligomerization of Drosophila Orb2. PLoS Biol. 2014;12(2):e1001786. https://doi.org/10.1371/journal.pbio.1001786
  132. Chao HW, Tsai LY, Lu YL, Lin PY, Huang WH, Chou HJ, et al. Deletion of CPEB3 enhances hippocampus-dependent memory via increasing expressions of PSD95 and NMDA receptors. J Neurosci. 2013;33(43):17008–22. https://doi.org/10.1523/JNEUROSCI.3043-13.2013
  133. Kinoshita T, Seki M. Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol. 2014;55(11):1859–63. https://doi.org/10.1093/pcp/pcu125
  134. Lancaster AK, Nutter-Upham A, Lindquist S, King OD. PLAAC: a web and command-line application to identify proteins with prion-like amino acid composition. Bioinformatics. 2014;30(17):2501–2. https://doi.org/10.1093/bioinformatics/btu310
  135. Blanco LP, Evans ML, Smith DR, Badtke MP, Chapman MR. Diversity, biogenesis and function of microbial amyloids. Trends Microbiol. 2012;20(2):66–73. https://doi.org/10.1016/j.tim.2011.11.005
  136. Romero D, Kolter R. Functional amyloids in bacteria. Int Microbiol. 2014;17(2):65–73.
  137. Carrió M, González-Montalbán N, Vera A, Villaverde A, Ventura S. Amyloid-like properties of bacterial inclusion bodies. J Mol Biol. 2005;347(5):1025–37. https://doi.org/10.1016/j.jmb.2005.02.030
  138. Villaverde A. Bacterial inclusion bodies: an emerging platform for drug delivery and cell therapy. Nanomedicine (Lond). 2012;7(9):1277–9. https://doi.org/10.2217/nnm.12.100
  139. Slotta U, Hess S, Spiess K, Stromer T, Serpell L, Scheibel T. Spider silk and amyloid fibrils: a structural comparison. Macromol Biosci. 2007;7(2):183–8. https://doi.org/10.1002/mabi.200600201
  140. Monks JN, Yan B, Hawkins N, Vollrath F, Wang Z. Spider Silk: Mother Nature’s Bio-Superlens. Nano Lett. 2016;16(9):5842–5. https://doi.org/10.1021/acs.nanolett.6b02641
  141. Rising A, Johansson J. Toward spinning artificial spider silk. Nat Chem Biol. 2015;11(5):309–15. https://doi.org/10.1038/nchembio.1789
  142. Tokareva O, Jacobsen M, Buehler M, Wong J, Kaplan DL. Structure-function-property-design interplay in biopolymers: spider silk. Acta Biomater. 2014;10(4):1612–26. https://doi.org/10.1016/j.actbio.2013.08.020
  143. Knowles TP, Mezzenga R. Amyloid Fibrils as Building Blocks for Natural and Artificial Functional Materials. Adv Mater. 2016;28(31):6546–61. https://doi.org/10.1002/adma.201505961
  144. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, et al. The most infectious prion protein particles. Nature. 2005;437(7056):257–61. https://doi.org/10.1038/nature03989
  145. Caughey B, Lansbury PT, Jr. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci. 2003;26(1):267–98. https://doi.org/10.1146/annurev.neuro.26.010302.081142
  146. Richardson BE, Lehmann R. Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol. 2010;11(1):37–49. https://doi.org/10.1038/nrm2815
  147. Dosch R, Wagner DS, Mintzer KA, Runke G, Wiemelt AP, Mullins MC. Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. Dev Cell. 2004;6(6):771–80. https://doi.org/10.1016/j.devcel.2004.05.002
  148. Marlow FL, Mullins MC. Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish. Dev Biol. 2008;321(1):40–50. https://doi.org/10.1016/j.ydbio.2008.05.557
  149. Wu H. Higher-order assemblies in a new paradigm of signal transduction. Cell. 2013;153(2):287–92. https://doi.org/10.1016/j.cell.2013.03.013
  150. Ferrao R, Wu H. Helical assembly in the death domain (DD) superfamily. Curr Opin Struct Biol. 2012;22(2):241–7. https://doi.org/10.1016/j.sbi.2012.02.006
  151. Zeng W, Sun L, Jiang X, Chen X, Hou F, Adhikari A, et al. Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity. Cell. 2010;141(2):315–30. https://doi.org/10.1016/j.cell.2010.03.029
  152. Shi Y, Yuan B, Qi N, Zhu W, Su J, Li X, et al. An autoinhibitory mechanism modulates MAVS activity in antiviral innate immune response. Nat Commun. 2015;6:7811. https://doi.org/10.1038/ncomms8811
  153. Peisley A, Wu B, Yao H, Walz T, Hur S. RIG-I forms signaling-competent filaments in an ATP-dependent, ubiquitin-independent manner. Mol Cell. 2013;51(5):573–83. https://doi.org/10.1016/j.molcel.2013.07.024
  154. Peisley A, Wu B, Xu H, Chen ZJ, Hur S. Structural basis for ubiquitin-mediated antiviral signal activation by RIG-I. Nature. 2014;509(7498):110–4. https://doi.org/10.1038/nature13140
  155. Wu B, Peisley A, Tetrault D, Li Z, Egelman EH, Magor KE, et al. Molecular imprinting as a signal-activation mechanism of the viral RNA sensor RIG-I. Mol Cell. 2014;55(4):511–23. https://doi.org/10.1016/j.molcel.2014.06.010
  156. Dick MS, Sborgi L, Rühl S, Hiller S, Broz P. ASC filament formation serves as a signal amplification mechanism for inflammasomes. Nat Commun. 2016;7:11929. https://doi.org/10.1038/ncomms11929
  157. Wu B, Peisley A, Richards C, Yao H, Zeng X, Lin C, et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell. 2013;152(1-2):276–89. https://doi.org/10.1016/j.cell.2012.11.048
  158. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature. 2007;446(7138):916–20. https://doi.org/10.1038/nature05732
  159. Wu B, Hur S. How RIG-I like receptors activate MAVS. Curr Opin Virol. 2015;12:91–8. https://doi.org/10.1016/j.coviro.2015.04.004
  160. Rutsch F, MacDougall M, Lu C, Buers I, Mamaeva O, Nitschke Y, et al. A specific IFIH1 gain-of-function mutation causes Singleton-Merten syndrome. Am J Hum Genet. 2015;96(2):275–82. https://doi.org/10.1016/j.ajhg.2014.12.014
  161. Rice GI, del Toro Duany Y, Jenkinson EM, Forte GM, Anderson BH, Ariaudo G, et al. Gain-of-function mutations in IFIH1 cause a spectrum of human disease phenotypes associated with upregulated type I interferon signaling. Nat Genet. 2014;46(5):503–9. https://doi.org/10.1038/ng.2933
  162. Yoo YS, Park YY, Kim JH, Cho H, Kim SH, Lee HS, et al. The mitochondrial ubiquitin ligase MARCH5 resolves MAVS aggregates during antiviral signalling. Nat Commun. 2015;6:7910. https://doi.org/10.1038/ncomms8910
  163. Kayagaki N, Stowe IB, Lee BL, O’Rourke K, Anderson K, Warming S, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature. 2015;526(7575):666–71. https://doi.org/10.1038/nature15541
  164. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature. 2015;526(7575):660–5. https://doi.org/10.1038/nature15514
  165. Ding J, Wang K, Liu W, She Y, Sun Q, Shi J, et al. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature. 2016;535(7610):111–6. https://doi.org/10.1038/nature18590
  166. Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H, et al. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature. 2016;535(7610):153–8. https://doi.org/10.1038/nature18629
  167. Sborgi L, Rühl S, Mulvihill E, Pipercevic J, Heilig R, Stahlberg H, et al. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 2016;35(16):1766–78. https://doi.org/10.15252/embj.201694696
  168. Aglietti RA, Estevez A, Gupta A, Ramirez MG, Liu PS, Kayagaki N, et al. GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc Natl Acad Sci USA. 2016;113(28):7858–63. https://doi.org/10.1073/pnas.1607769113
  169. Vance RE. The NAIP/NLRC4 inflammasomes. Curr Opin Immunol. 2015;32:84–9. https://doi.org/10.1016/j.coi.2015.01.010
  170. Zhao Y, Shao F. The NAIP-NLRC4 inflammasome in innate immune detection of bacterial flagellin and type III secretion apparatus. Immunol Rev. 2015;265(1):85–102. https://doi.org/10.1111/imr.12293
  171. Hu Z, Yan C, Liu P, Huang Z, Ma R, Zhang C, et al. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science. 2013;341(6142):172–5. https://doi.org/10.1126/science.1236381
  172. Tenthorey JL, Kofoed EM, Daugherty MD, Malik HS, Vance RE. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol Cell. 2014;54(1):17–29. https://doi.org/10.1016/j.molcel.2014.02.018
  173. Lu A, Li Y, Schmidt FI, Yin Q, Chen S, Fu TM, et al. Molecular basis of caspase-1 polymerization and its inhibition by a new capping mechanism. Nat Struct Mol Biol. 2016;23(5):416–25. https://doi.org/10.1038/nsmb.3199
  174. Schmidt FI, Lu A, Chen JW, Ruan J, Tang C, Wu H, et al. A single domain antibody fragment that recognizes the adaptor ASC defines the role of ASC domains in inflammasome assembly. J Exp Med. 2016;213(5):771–90. https://doi.org/10.1084/jem.20151790
  175. Canna SW, de Jesus AA, Gouni S, Brooks SR, Marrero B, Liu Y, et al. An activating NLRC4 inflammasome mutation causes autoinflammation with recurrent macrophage activation syndrome. Nat Genet. 2014;46(10):1140–6. https://doi.org/10.1038/ng.3089
  176. Romberg N, Al Moussawi K, Nelson-Williams C, Stiegler AL, Loring E, Choi M, et al. Mutation of NLRC4 causes a syndrome of enterocolitis and autoinflammation. Nat Genet. 2014;46(10):1135–9. https://doi.org/10.1038/ng.3066
  177. Mariathasan S, Weiss DS, Newton K, McBride J, O’Rourke K, Roose-Girma M, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440(7081):228–32. https://doi.org/10.1038/nature04515
  178. Martinon F, Pétrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006;440(7081):237–41. https://doi.org/10.1038/nature04516
  179. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol. 2008;9(8):857–65. https://doi.org/10.1038/ni.1636
  180. Hafner-Bratkovič I, Benčina M, Fitzgerald KA, Golenbock D, Jerala R. NLRP3 inflammasome activation in macrophage cell lines by prion protein fibrils as the source of IL-1β and neuronal toxicity. Cell Mol Life Sci. 2012;69(24):4215–28. https://doi.org/10.1007/s00018-012-1140-0
  181. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature. 2009;458(7237):514–8. https://doi.org/10.1038/nature07725
  182. Fernandes-Alnemri T, Wu J, Yu JW, Datta P, Miller B, Jankowski W, et al. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 2007;14(9):1590–604. https://doi.org/10.1038/sj.cdd.4402194
  183. Broz P, von Moltke J, Jones JW, Vance RE, Monack DM. Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe. 2010;8(6):471–83. https://doi.org/10.1016/j.chom.2010.11.007
  184. Case CL, Shin S, Roy CR. Asc and Ipaf Inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect Immun. 2009;77(5):1981–91. https://doi.org/10.1128/IAI.01382-08
  185. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, Lee WP, et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature. 2004;430(6996):213–8. https://doi.org/10.1038/nature02664
  186. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008;9(8):847–56. https://doi.org/10.1038/ni.1631
  187. Adamczak S, Dale G, de Rivero Vaccari JP, Bullock MR, Dietrich WD, Keane RW. Inflammasome proteins in cerebrospinal fluid of brain-injured patients as biomarkers of functional outcome. J Neurosurg. 2012;117(6):1119–25. https://doi.org/10.3171/2012.9.JNS12815
  188. de Rivero Vaccari JP, Lotocki G, Alonso OF, Bramlett HM, Dietrich WD, Keane RW. Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J Cereb Blood Flow Metab. 2009;29(7):1251–61. https://doi.org/10.1038/jcbfm.2009.46
  189. Kagan JC, Magupalli VG, Wu H. SMOCs: supramolecular organizing centres that control innate immunity. Nat Rev Immunol. 2014;14(12):821–6. https://doi.org/10.1038/nri3757
  190. Qiao Q, Yang C, Zheng C, Fontán L, David L, Yu X, et al. Structural architecture of the CARMA1/Bcl10/MALT1 signalosome: nucleation-induced filamentous assembly. Mol Cell. 2013;51(6):766–79. https://doi.org/10.1016/j.molcel.2013.08.032
  191. Yang J, Liu Z, Xiao TS. Post-translational regulation of inflammasomes. Cell Mol Immunol. 2017;14(1):65–79. [Epub ahead of print 2016 Jun 27] http://www.nature.com/cmi/journal/v14/n1/full/cmi201629a.html
  192. Agostini L, Martinon F, Burns K, McDermott MF, Hawkins PN, Tschopp J. NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity. 2004;20(3):319–25. https://doi.org/10.1016/S1074-7613(04)00046-9