Structures of pattern recognition receptors reveal molecular mechanisms of autoinhibition, ligand recognition and oligomerization

Current Opinion in Immunology

Volumn 26, Issue 1, 2014, Pages 14-20

  Chuenchor, Watchalee ^a   Jin, Tengchuan ^a   Ravilious, Geoffrey ^a   Xiao, T Sam ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE RECEPTOR; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; RIG 1 LIKE RECEPTOR; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; INTRACELLULAR SPACE; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; OLIGOMERIZATION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY;

ANIMALS; AUTOIMMUNITY; DOWN-REGULATION; GENE TARGETING; HUMANS; IMMUNITY, INNATE; LIGANDS; MULTIGENE FAMILY; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PATTERN RECOGNITION;

EID: 84887557126     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.10.009     Document Type: Review

References (56)

1. Janeway C.A., Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002, 20:197-216.
2. Kang J.Y., Lee J.-O. Structural biology of the Toll-like receptor family. Annu Rev Biochem 2011, 80:917-941.
3. Yoon S.-I., Kurnasov O., Natarajan V., Hong M., Gudkov A.V., Osterman A.L., Wilson I.A. Structural basis of TLR5-flagellin recognition and signaling. Science 2012, 335:859-864.
4. Tanji H., Ohto U., Shibata T., Miyake K., Shimizu T. Structural reorganization of the Toll-like receptor 8 dimer induced by agonistic ligands. Science 2013, 339:1426-1429.
5. Ewald S.E., Lee B.L., Lau L., Wickliffe K.E., Shi G.-P., Chapman H.A., Barton G.M. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 2008, 456:658-662.
6. Park B., Brinkmann M.M., Spooner E., Lee C.C., Kim Y.-M., Ploegh H.L. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat Immunol 2008, 9:1407-1414.
7. Sepulveda F.E., Maschalidi S., Colisson R., Heslop L., Ghirelli C., Sakka E., Lennon-DumEnil A.-M., Amigorena S., Cabanie L., Manoury B. Critical role for asparagine endopeptidase in endocytic toll-like receptor signaling in dendritic cells. Immunity 2009, 31:737-748.
8. Jin M.S., Kim S.E., Heo J.Y., Lee M.E., Kim H.M., Paik S.-G., Lee H., Lee J.-O. Crystal structure of the TLR1-TLR2 Heterodimer induced by binding of a tri-acylated lipopeptide. Cell 2007, 130:1071-1082.
9. Kim H.M., Park B.S., Kim J.-I., Kim S.E., Lee J., Oh S.C., Enkhbayar P., Matsushima N., Lee H., Yoo O.J., et al. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist eritoran. Cell 2007, 130:906-917.
10. Kang J.Y., Nan X., Jin M.S., Youn S.-J., Ryu Y.H., Mah S., Han S.H., Lee H., Paik S.-G., Lee J.-O. Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 2009, 31:873-884.
11. Park B.S., Song D.H., Kim H.M., Choi B.-S., Lee H., Lee J.-O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 2009, 458:1191-1195.
12. Choe J., Kelker M.S., Wilson I.A. Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 2005, 309:581-585.
13. Bell J.K., Botos I., Hall P.R., Askins J., Shiloach J., Segal D.M., Davies D.R. The molecular structure of the Toll-like receptor 3 ligand-binding domain. Proc Natl Acad Sci USA 2005, 102:10976-10980.
14. Zhou K., Kanai R., Lee P., Wang H.-W., Modis Y. Toll-like receptor 5 forms asymmetric dimers in the absence of flagellin. J Struct Biol 2012, 177:402-409.
15. Latz E., Verma A., Visintin A., Gong M., Sirois C.M., Klein D.C.G., Monks B.G., McKnight C.J., Lamphier M.S., Duprex W.P., et al. Ligand-induced conformational changes allosterically activate Toll-like receptor 9. Nat Immunol 2007, 8:772-779.
16. Leonard J.N., Ghirlando R., Askins J., Bell J.K., Margulies D.H., Davies D.R., Segal D.M. The TLR3 signaling complex forms by cooperative receptor dimerization. Proc Natl Acad Sci 2008, 105:258-263.
17. Liu L., Botos I., Wang Y., Leonard J.N., Shiloach J., Segal D.M., Davies D.R. Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 2008, 320:379-381.
18. Martinon F., Burns K., Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002, 10:417-426.
19. Atianand M.K., Rathinam V.A., Fitzgerald K.A. SnapShot: inflammasomes. Cell 2013, 153. 272-272.e1.
20. Kofoed E.M., Vance R.E. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 2011, 477:592-595.
21. ••].
22. Miao E.A., Alpuche-Aranda C.M., Dors M., Clark A.E., Bader M.W., Miller S.I., Aderem A. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1β via Ipaf. Nat Immunol 2006, 7:569-575.
23. Franchi L., Amer A., Body-Malapel M., Kanneganti T.-D., Özören N., Jagirdar R., Inohara N., Vandenabeele P., Bertin J., Coyle A., et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infected macrophages. Nat Immunol 2006, 7:576-582.
24. Hu Z., Yan C., Liu P., Huang Z., RuiMa, Zhang C., Wang R., Zhang Y., FabioMartinon D.H.J.J., Chai J. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 2013, 341:172-175.
25. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004, 5:730-737.
26. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441:101-105.
27. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.-M., Gale M., Akira S., et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 2005, 175:2851-2858.
28. Seth R.B., Sun L., Ea C.-K., Chen Z.J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF3. Cell 2005, 122:669-682.
29. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 2005, 6:981-988.
30. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R., Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nat Cell Biol 2005, 437:1167-1172.
31. Xu L.-G., Wang Y.-Y., Han K.-J., Li L.-Y., Zhai Z., Shu H.-B. VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol Cell 2005, 19:727-740.
32. Rothenfusser S., Goutagny N., DiPerna G., Gong M., Monks B.G., Schoenemeyer A., Yamamoto M., Akira S., Fitzgerald K.A. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J Immunol 2005, 175:5260-5268.
33. Jiang F., Ramanathan A., Miller M.T., Tang G.-Q., Gale M., Patel S.S., Marcotrigiano J. Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 2011, 479:423-427.
34. Kowalinski E., Lunardi T., McCarthy A.A., Louber J., Brunel J., Grigorov B., Gerlier D., Cusack S. Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 2011, 147:423-435.
35. Luo D., Ding S.C., Vela A., Kohlway A., Lindenbach B.D., Pyle A.M. Structural insights into RNA recognition by RIG-I. Cell 2011, 147:409-422.
36. Jiang X., Kinch L.N., Brautigam C.A., Chen X., Du F., Grishin N.V., Chen Z.J. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 2012, 36:959-973.
37. Hou F., Sun L., Zheng H., Skaug B., Jiang Q.-X., Chen Z.J. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 2011, 10.1016/j.cell.2011.06.041.
38. Wu B., Peisley A., Richards C., Yao H., Zeng X., Lin C., Chu F., Walz T., Hur S. Structural basis for dsRNA recognition, filament formation, and antiviral signal activation by MDA5. Cell 2013, 152:276-289.
39. Peisley A., Bin Wu, Yao H., Walz T., Hur S. RIG-I forms signaling-competent filaments in an ATP-dependent. Ubiquitin-independent manner. Mol Cell 2013, 51:1-11.
40. Patel J.R., Jain A., Chou Y.-Y., Baum A., Ha T., García-Sastre A. ATPase-driven oligomerization of RIG-I on RNA allows optimal activation of type-I interferon. EMBO Rep 2013, 14:780-787.
41. Goubau D., Deddouche S., Reis e Sousa C. Cytosolic sensing of viruses. Immunity 2013, 38:855-869.
42. Nistal-Villan E., Gack M.U., Martinez-Delgado G., Maharaj N.P., Inn K.S., Yang H., Wang R., Aggarwal A.K., Jung J.U., Garcia-Sastre A. Negative role of RIG-I serine 8 phosphorylation in the regulation of interferon-β production. J Biol Chem 2010, 285:20252-20261.
43. Wies E., Wang M.K., Maharaj N.P., Chen K., Zhou S., Finberg R.W., Gack M.U. Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling. Immunity 2013, 38:437-449.
44. Kersse K., Verspurten J., Berghe T.V., Vandenabeele P. The death-fold superfamily of homotypic interaction motifs. Trends Biochem Sci 2011, 36:541-552.
45. Feng M., Ding Z., Xu L., Kong L., Wang W., Jiao S., Shi Z., Greene M.I., Cong Y., Zhou Z. Structural and biochemical studies of RIG-I antiviral signaling. Protein Cell 2013, 4:142-154.
46. Moore C.B., Bergstralh D.T., Duncan J.A., Lei Y., Morrison T.E., Zimmermann A.G., Accavitti-Loper M.A., Madden V.J., Sun L., Ye Z., et al. NLRX1 is a regulator of mitochondrial antiviral immunity. Nature 2008, 451:573-577.
47. Lei Y., Wen H., Ting J.P.Y. The NLR protein, NLRX1, and its partner, TUFM, reduce type I interferon, and enhance autophagy. Autophagy 2013, 9:432-433.
48. Hong M., Yoon S.-I., Wilson I.A. Structure and functional characterization of the RNA-binding element of the NLRX1 innate immune modulator. Immunity 2012, 36:337-347.
49. Jin T., Perry A., Jiang J., Smith P., Curry J.A., Unterholzner L., Jiang Z., Horvath G., Rathinam V.A., Johnstone R.W., et al. Structures of the HIN domain:DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 2012, 36:561-571.
50. Ru H., Ni X., Zhao L., Crowley C., Ding W., Hung L.-W., Shaw N., Cheng G., Liu Z.-J. Structural basis for termination of AIM2-mediated signaling by p202. Cell Res 2013, 10.1038/cr.2013.52.
51. Yin Q., Sester D.P., Tian Y., Hsiao Y.-S., Lu A., Cridland J.A., Sagulenko V., Thygesen S.J., Choubey D., Hornung V., et al. Molecular mechanism for p202-mediated specific inhibition of AIM2 inflammasome activation. Cell Rep 2013, 4:327-339.
52. 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 2013, 288:13225-13235.
53. Medvedev A.E., Piao W., Shoenfelt J., Rhee S.H., Chen H., Basu S., Wahl L.M., Fenton M.J., Vogel S.N. Role of TLR4 tyrosine phosphorylation in signal transduction and endotoxin tolerance. J Biol Chem 2007, 282:16042-16053.
54. Lee K.-G., Xu S., Kang Z.-H., Huo J., Huang M., Liu D., Takeuchi O., Akira S., Lam K.-P. Bruton's tyrosine kinase phosphorylates Toll-like receptor 3 to initiate antiviral response. Proc Natl Acad Sci 2012, 109:5791-5796.
55. Qu Y., Misaghi S., Izrael-Tomasevic A., Newton K., Gilmour L.L., Lamkanfi M., Louie S., Kayagaki N., Liu J., Kömüves L., et al. Phosphorylation of NLRC4 is critical for inflammasome activation. Nature 2012, 490:539-542.
56. Gack M.U., Shin Y.C., Joo C.-H., Urano T., Liang C., Sun L., Takeuchi O., Akira S., Chen Z., Inoue S., et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007, 446:916-920.