Structure and assembly of the mouse ASC inflammasome by combined NMR spectroscopy and cryo-electron microscopy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 43, 2015, Pages 13237-13242

  Sborgi, Lorenzo ^a   Ravotti, Francesco ^b   Dandey, Venkata P ^a   Dick, Mathias S ^a   Mazur, Adam ^a   Reckel, Sina ^a,e   Chami, Mohamed ^a   Scherer, Sebastian ^a   Huber, Matthias ^b   Böckmann, Anja ^c   Egelman, Edward H ^d   Stahlberg, Henning ^a   Broz, Petr ^a   Meier, Beat H ^b   Hiller, Sebastian ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^d UNIVERSITY OF VIRGINIA   (United States)

^e EPFL   (Switzerland)

Author keywords

ASC speck; Inflammation; Innate immune response; Protein filament; Protein structure

Indexed keywords

ADAPTOR PROTEIN; AMINO ACID; APOPTOSIS ASSOCIATED SPECK LIKE PROTEIN; INFLAMMASOME; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; PYCARD PROTEIN, MOUSE;

AMINO ACID SEQUENCE; ARTICLE; CRYOELECTRON MICROSCOPY; HYDROGEN BOND; IN VITRO STUDY; MACROPHAGE; MOUSE; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN STRUCTURE; STATIC ELECTRICITY; ANIMAL; CHEMISTRY; CONFOCAL MICROSCOPY; GENETICS; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; MOLECULAR CLONING; MOLECULAR MODEL; PROTEIN CONFORMATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CLONING, MOLECULAR; CRYOELECTRON MICROSCOPY; INFLAMMASOMES; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 84945567425     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1507579112     Document Type: Article

References (45)

1. Franchi L, Muñoz-Planillo R, Núñez G (2012) Sensing and reacting to microbes through the inflammasomes. Nat Immunol 13(4):325-332.
2. Lamkanfi M, Dixit VM (2014) Mechanisms and functions of inflammasomes. Cell 157(5):1013-1022.
3. Vanaja SK, Rathinam VA, Fitzgerald KA (2015) Mechanisms of inflammasome activation: Recent advances and novel insights. Trends Cell Biol 25(5):308-315.
4. Schroder K, Tschopp J (2010) The inflammasomes. Cell 140(6):821-832.
5. Walsh JG, Muruve DA, Power C (2014) Inflammasomes in the CNS. Nat Rev Neurosci 15(2):84-97.
6. Strowig T, Henao-Mejia J, Elinav E, Flavell R (2012) Inflammasomes in health and disease. Nature 481(7381):278-286.
7. Lamkanfi M, Dixit VM (2012) Inflammasomes and their roles in health and disease. Annu Rev Cell Dev Biol 28:137-161.
8. Hu Z, et al. (2013) Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341(6142):172-175.
9. Lu A, Wu H (2015) Structural mechanisms of inflammasome assembly. FEBS J 282(3):435-444.
10. Masumoto J, et al. (1999) ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells. J Biol Chem 274(48):33835-33838.
11. Srimathi T, et al. (2008) Mapping of POP1-binding site on pyrin domain of ASC. J Biol Chem 283(22):15390-15398.
12. Hiller S, et al. (2003) NMR structure of the apoptosis-and inflammation-related NALP1 pyrin domain. Structure 11(10):1199-1205.
13. Vajjhala PR, et al. (2014) Identification ofmultifaceted bindingmodes for pyrin and ASC pyrin domains gives insights into pyrin inflammasome assembly. J Biol Chem289(34):23504-23519.
14. de Alba E (2009) Structure and interdomain dynamics of apoptosis-associated specklike protein containing a CARD (ASC). J Biol Chem 284(47):32932-32941.
15. Liepinsh E, et al. (2003) The death-domain fold of the ASC PYRIN domain, presenting a basis for PYRIN/PYRIN recognition. J Mol Biol 332(5):1155-1163.
16. Lu A, et al. (2014) Unified polymerization mechanism for the assembly of ASCdependent inflammasomes. Cell 156(6):1193-1206.
17. Qiao Q, et al. (2013) Structural architecture of the CARMA1/Bcl10/MALT1 signalosome: Nucleation-induced filamentous assembly. Mol Cell 51(6):766-779.
18. Park HH, et al. (2007) Death domain assembly mechanism revealed by crystal structure of the oligomeric PIDDosome core complex. Cell 128(3):533-546.
19. Wasmer C, et al. (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319(5869):1523-1526.
20. Loquet A, et al. (2012) Atomic model of the type III secretion system needle. Nature 486(7402):276-279.
21. Debelouchina GT, Platt GW, Bayro MJ, Radford SE, Griffin RG (2010) Intermolecular alignment in β2-microglobulin amyloid fibrils. J Am Chem Soc 132(48):17077-17079.
22. Petkova AT, et al. (2002) A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99(26):16742-16747.
23. Meier BH, Böckmann A (2015) The structure of fibrils from 'misfolded' proteins. Curr Opin Struct Biol 30:43-49.
24. Lu JX, et al. (2013) Molecular structure of β-amyloid fibrils in Alzheimer's disease brain tissue. Cell 154(6):1257-1268.
25. Scherer S, et al. (2014) 2dx-automator: Implementation of a semiautomatic high-throughput high-resolution cryo-electron crystallography pipeline. J Struct Biol 186(2):302-307.
26. Li X, et al. (2013) Electron counting and beam-induced motion correction enable nearatomic-resolution single-particle cryo-EM. Nat Methods 10(6):584-590.
27. Egelman EH (2000) A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85(4):225-234.
28. Schuetz A, et al. (2010) Protocols for the sequential solid-state NMR spectroscopic assignment of a uniformly labeled 25 kDa protein: HET-s(1-227). ChemBioChem 11(11):1543-1551.
29. Ravotti F, et al. (September 24, 2015) Sequence-specific solid-state NMR assignments of the mouse ASC PYRIN domain in its filament form. Biomol NMR Assign, 10.1007/s12104-015-9647-6.
30. Igumenova TI, et al. (2004) Assignments of carbon NMR resonances for microcrystalline ubiquitin. J Am Chem Soc 126(21):6720-6727.
31. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
32. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160(1):65-73.
33. Kneller DG, Kuntz ID (1993) UCSF Sparky-an NMR display, annotation and assignment tool. J Cell Biochem 53(S17C):254-254.
34. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319(1):209-227.
35. Habenstein B, et al. (2011) Extensive de novo solid-state NMR assignments of the 33 kDa C-terminal domain of the Ure2 prion. J Biomol NMR 51(3):235-243.
36. Shen Y, Delaglio F, Cornilescu G, Bax A (2009) TALOS+: A hybrid method for predicting protein backbone torsion angles fromNMR chemical shifts. J Biomol NMR 44(4):213-223.
37. Morris GA, Freeman R (1979) Enhancement of nuclear magnetic resonance signals by polarization transfer. J Am Chem Soc 101(3):760-762.
38. Moriya M, et al. (2005) Role of charged and hydrophobic residues in the oligomerization of the PYRIN domain of ASC. Biochemistry 44(2):575-583.
39. Mariathasan S, Monack DM (2007) Inflammasome adaptors and sensors: Intracellular regulators of infection and inflammation. Nat Rev Immunol 7(1):31-40.
40. Broz P, von Moltke J, Jones JW, Vance RE, Monack DM (2010) Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 8(6):471-483.
41. Van Opdenbosch N, et al. (2014) Activation of the NLRP1b inflammasome independently of ASC-mediated caspase-1 autoproteolysis and speck formation. Nat Commun 5:3209.
42. Demers JP, et al. (2014) High-resolution structure of the Shigella type-III secretion needle by solid-state NMR and cryo-electron microscopy. Nat Commun 5:4976.
43. Lin SC, Lo YC, Wu H (2010) Helical assembly in the MyD88-IRAK4-IRAK2 complex in TLR/IL-1R signalling. Nature 465(7300):885-890.
44. Chen YR, Clark AC (2004) Kinetic traps in the folding/unfolding of procaspase-1 CARD domain. Protein Sci 13(8):2196-2206.
45. Güntert P, Dötsch V, Wider G, Wüthrich K (1992) Processing of multi-dimensional NMR data with the new software PROSA. J Biomol NMR 2(6):619-629.