Assembly-driven activation of the AIM2 foreign-dsDNA sensor provides a polymerization template for downstream ASC

Nature Communications

Volumn 6, Issue , 2015, Pages

  Morrone, Seamus R ^a   Matyszewski, Mariusz ^a   Yu, Xiong ^b   Delannoy, Michael ^a   Egelman, Edward H ^b   Sohn, Jungsan ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSENT IN MELANOMA 2 PROTEIN; ADAPTOR PROTEIN; APOPTOSIS ASSOCIATED SPECK FORMING PROTEIN; DOUBLE STRANDED DNA; INFLAMMASOME; UNCLASSIFIED DRUG; AIM2 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; DNA; DNA BINDING PROTEIN; IFI202B PROTEIN, MOUSE; MALTOSE BINDING PROTEIN; PYCARD PROTEIN, HUMAN; SIGNAL PEPTIDE;

DNA; LIGAND; POLYMERIZATION; PROTEIN; SYMMETRY;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BIOSENSOR; COMPLEX FORMATION; LIGAND BINDING; MUTAGENESIS; NUCLEOTIDE BINDING SITE; OLIGOMERIZATION; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ELECTRON MICROSCOPY; ESCHERICHIA COLI; GENETICS; INNATE IMMUNITY; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; CYTOSKELETAL PROTEINS; DNA; DNA-BINDING PROTEINS; ESCHERICHIA COLI; IMMUNITY, INNATE; INFLAMMASOMES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALTOSE-BINDING PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTAGENESIS;

EID: 84937902109     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8827     Document Type: Article

References (45)

1. Yoneyama, M., Onomoto, K., Jogi, M., Akaboshi, T. & Fujita, T. Viral RNA detection by RIG-I-like receptors. Curr. Opin. Immunol. 32, 48-53 (2015).
2. Del Toro Duany, Y., Wu, B. & Hur, S. MDA5-filament, dynamics and disease. Curr. Opin. Virol. 12C, 20-25 (2015).
3. Lu, A. & Wu, H. Structural mechanisms of inflammasome assembly. FEBS J. 282, 435-444 (2015).
4. Knipe, D. M. Nuclear sensing of viral DNA, epigenetic regulation of herpes simplex virus infection, and innate immunity. Virology 479-480C, 153-159 (2015).
5. Wu, H. Higher-order assemblies in a new paradigm of signal transduction. Cell 153, 287-292 (2013).
6. Kagan, J. C., Magupalli, V. G. & Wu, H. SMOCs: supramolecular organizing centres that control innate immunity. Nat. Rev. Immunol. 14, 821-826 (2014).
7. Lu, A. et al. Unified polymerization mechanism for the assembly of ASCdependent inflammasomes. Cell 156, 1193-1206 (2014).
8. Cai, X. et al. Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell 156, 1207-1222 (2014).
9. Wu, B. et al. Molecular imprinting as a signal-activation mechanism of the viral RNA sensor RIG-I. Mol. Cell 55, 511-523 (2014).
10. Wu, B. et al. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 152, 276-289 (2013).
11. Fernandes-Alnemri, T. et al. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 11, 385-393 (2010).
12. Orzalli, M. H., Conwell, S. E., Berrios, C., DeCaprio, J. A. & Knipe, D. M. Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. Proc. Natl Acad. Sci. USA 110, E4492-E4501 (2013).
13. Feng, Q. et al. MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep. 2, 1187-1196 (2012).
14. Mondini, M. et al. Role of the interferon-inducible gene IFI16 in the etiopathogenesis of systemic autoimmune disorders. Ann. NY Acad. Sci. 1110, 47-56 (2007).
15. Zhang, W. et al. AIM2 facilitates the apoptotic DNA-induced systemic lupus erythematosus via arbitrating macrophage functional maturation. J. Clin. Immunol. 33, 925-937 (2013).
16. Smith, S. & Jefferies, C. Role of DNA/RNA sensors and contribution to autoimmunity. Cytokine Growth Factor Rev. 25, 745-757 (2014).
17. Unterholzner, L. et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11, 997-1004 (2010).
18. Roberts, T. L. et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057-1060 (2009).
19. Hornung, V. et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458, 514-518 (2009).
20. Fernandes-Alnemri, T., Yu, J. W., Datta, P., Wu, J. & Alnemri, E. S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458, 509-513 (2009).
21. Burckstummer, T. et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10, 266-272 (2009).
22. Li, T., Chen, J. & Cristea, I. M. Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14, 591-599 (2013).
23. Morrone, S. R. et al. Cooperative assembly of IFI16 filaments on dsDNA provides insights into host defense strategy. Proc. Natl Acad. Sci. USA 111, E62-E71 (2014).
24. Kerur, N. et al. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpes virus infection. Cell Host Microbe 9, 363-375 (2011).
25. Monroe, K. M. et al. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343, 428-432 (2014).
26. VanLoock, M. S. et al. ATP-mediated conformational changes in the RecA filament. Structure 11, 187-196 (2003).
27. Galkin, V. E. et al. The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity. Structure 14, 983-992 (2006).
28. Peisley, A. et al. Kinetic mechanism for viral dsRNA length discrimination by MDA5 filaments. Proc. Natl Acad. Sci. USA 109, E3340-E3349 (2012).
29. Peisley, A. et al. Cooperative assembly and dynamic disassembly of MDA5 filaments for viral dsRNA recognition. Proc. Natl Acad. Sci. USA 108, 21010-21015 (2011).
30. Peisley, A., Wu, B., Yao, H., Walz, T. & Hur, S. RIG-I forms signalingcompetent filaments in an ATP-dependent, ubiquitin-independent manner. Mol. Cell 51, 573-583 (2013).
31. Schattgen, S. A. & Fitzgerald, K. A. The PYHIN protein family as mediators of host defenses. Immunol. Rev. 243, 109-118 (2011).
32. Jin, T. et al. Structures of the HIN domain: DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36, 561-571 (2012).
33. Jin, T., Perry, A., Smith, P., Jiang, J. & Xiao, T. S. Structure of the absent in melanoma 2 (AIM2) pyrin domain provides insights into the mechanisms of AIM2 autoinhibition and inflammasome assembly. J. Biol. Chem. 288, 13225-13235 (2013).
34. Lu, A., Kabaleeswaran, V., Fu, T., Magupalli, V. G. & Wu, H. Crystal structure of the F27G AIM2 PYD mutant and similarities of its self-association to DED/DED interactions. J. Mol. Biol. 426, 1420-1427 (2014).
35. Vajjhala, P. R., Mirams, R. E. & Hill, J. M. Multiple binding sites on the pyrin domain of ASC protein allow self-association and interaction with NLRP3 protein. J. Biol. Chem. 287, 41732-41743 (2012).
36. Ratsimandresy, R. A., Dorfleutner, A. & Stehlik, C. An update on PYRIN domain-containing pattern recognition receptors: from immunity to pathology. Front. Immunol. 4, 440 (2013).
37. Latz, E., Xiao, T. S. & Stutz, A. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13, 397-411 (2013).
38. Yin, Q. et al. Molecular mechanism for p202-mediated specific inhibition of AIM2 inflammasome activation. Cell Rep. 4, 327-339 (2013).
39. Veeranki, S., Duan, X., Panchanathan, R., Liu, H. & Choubey, D. 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 (2011).
40. Orzalli, M. H. & Knipe, D. M. Cellular sensing of viral DNA and viral evasion mechanisms. Annu. Rev. Microbiol. 68, 477-492 (2014).
41. Orzalli, M. H., DeLuca, N. A. & Knipe, D. M. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl Acad. Sci. USA 109, E3008-E3017 (2012).
42. Park, H. H. et al. The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annu. Rev. Immunol. 25, 561-586 (2007).
43. Qiao, Q. et al. Structural architecture of the CARMA1/Bcl10/MALT1 signalosome: nucleation-induced filamentous assembly. Mol. Cell 51, 766-779 (2013).
44. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
45. Frank, J. et al. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (1996).