Crystal structure of NOD2 and its implications in human disease

Nature Communications

Volumn 7, Issue , 2016, Pages

  Maekawa, Sakiko ^a   Ohto, Umeharu ^a   Shibata, Takuma ^b   Miyake, Kensuke ^b   Shimizu, Toshiyuki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b THE UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; OLIGOMER; ADENOSINE DIPHOSPHATE; LIGAND; MUTANT PROTEIN;

DISEASE INCIDENCE; IMMUNE RESPONSE; LIGAND; MUTATION; PROTEIN;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; GAIN OF FUNCTION MUTATION; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR INTERACTION; NONHUMAN; PROTEIN CONFORMATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DISEASES; LEPORIDAE; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; X RAY CRYSTALLOGRAPHY;

ORYCTOLAGUS CUNICULUS;

ADENOSINE DIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DISEASE; HUMANS; LIGANDS; MODELS, MOLECULAR; MUTANT PROTEINS; NOD2 SIGNALING ADAPTOR PROTEIN; PROTEIN DOMAINS; RABBITS;

EID: 84974623115     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11813     Document Type: Article

References (53)

1. Lamkanfi, M., Dixit, V. M. Mechanisms and functions of inflammasomes. Cell 157, 1013-1022 (2014).
2. Schroder, K., Tschopp, J. The inflammasomes. Cell 140, 821-832 (2010).
3. Takeuchi, O., Akira, S. Pattern recognition receptors and inflammation. Cell 140, 805-820 (2010).
4. von Moltke, J., Ayres, J. S., Kofoed, E. M., Chavarria-Smith, J., Vance, R. E. Recognition of bacteria by inflammasomes. Annu. Rev. Immunol. 31, 73-106 (2013).
5. Danot, O., Marquenet, E., Vidal-Ingigliardi, D., Richet, E. Wheel of life, wheel of death: a mechanistic insight into signaling by STAND proteins. Structure 17, 172-182 (2009).
6. Lelpe, D. D., Koonin, E. V., Aravind, L. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J. Mol. Biol. 343, 1-28 (2004).
7. Proell, M., Riedl, S. J., Fritz, J. H., Rojas, A. M., Schwarzenbacher, R. The Nod-like receptor (NLR) family: a tale of similarities and differences. PloS ONE 3, e2119 (2008).
8. Ting, J. P. Y. et al. The NLR gene family: a standard nomenclature. Immunity 28, 285-287 (2008).
9. Girardin, S. E. et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278, 8869-8872 (2003).
10. Girardin, S. E. et al. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278, 41702-41708 (2003).
11. Inohara, N. et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2. J. Biol. Chem. 278, 5509-5512 (2003).
12. Nakamura, N. et al. Endosomes are specialized platforms for bacterial sensing and NOD2 signalling. Nature 509, 240-244 (2014).
13. Correa, R. G., Milutinovic, S., Reed, J. C. Roles of NOD1 (NLRC1) and NOD2 (NLRC2) in innate immunity and inflammatory diseases. Biosci. Rep. 32, 597-608 (2012).
14. Gutierrez, O. et al. Induction of Nod2 in myelomonocytic and intestinal epithelial cells via nuclear factor-kappa B activation. J. Biol. Chem. 277, 41701-41705 (2002).
15. Ogura, Y. et al. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-kappa B. J. Biol. Chem. 276, 4812-4818 (2001).
16. Travassos, L. H. et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 11, 55-62 (2010).
17. Borzutzky, A. et al. NOD2-associated diseases: bridging innate immunity and autoinflammation. Clin. Immunol. 134, 251-261 (2010).
18. Ogura, Y. et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411, 603-606 (2001).
19. Hugot, J. P. et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411, 599-603 (2001).
20. Miceli-Richard, C. et al. CARD15 mutations in Blau syndrome. Nat. Genet. 29, 19-20 (2001).
21. Kanazawa, N. et al. Early-onset sarcoidosis and CARD15 mutations with constitutive nuclear factor-kappa B activation: common genetic etiology with Blau syndrome. Blood 105, 1195-1197 (2005).
22. Chamaillard, M. et al. Gene-environment interaction modulated by allelic heterogeneity in inflammatory diseases. Proc. Natl Acad. Sci. USA 100, 3455-3460 (2003).
23. Inohara, N., Nunez, G. NODs: Intracellular proteins involved in inflammation and apoptosis. Nat. Rev. Immunol. 3, 371-382 (2003).
24. Hugot, J. P. CARD15/NOD2 mutations in Crohn's disease. Ann. N Y Acad. Sci. 1072, 9-18 (2006).
25. Li, J. et al. Regulation of IL-8 and IL-1 beta expression in Crohn's disease associated NOD2/CARD15 mutations. Hum. Mol. Genet. 13, 1715-1725 (2004).
26. Maeda, S. et al. Nod2 mutation in Crohn's disease potentiates NF-kappa B activity and IL-10 processing. Science 307, 734-738 (2005).
27. Tanabe, T. et al. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J 23, 1587-1597 (2004).
28. Riedl, S. J., Li, W. Y., Chao, Y., Schwarzenbacher, R., Shi, Y. G. Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 434, 926-933 (2005).
29. Reubold, T. F., Wohlgemuth, S., Eschenburg, S. Crystal structure of full-length Apaf-1: how the death signal is relayed in the mitochondrial pathway of apoptosis. Structure 19, 1074-1083 (2011).
30. Yuan, S. J., Topf, M., Reubold, T. F., Eschenburg, S., Akey, C. W. Changes in Apaf-1 conformation that drive apoptosome assembly. Biochemistry 52, 2319-2327 (2013).
31. Yan, N. et al. Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans. Nature 437, 831-837 (2005).
32. Qi, S. Q. et al. Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4. Cell 141, 446-457 (2010).
33. Hu, Z. H. et al. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341, 172-175 (2013).
34. Lechtenberg, B. C., Mace, P. D., Riedl, S. J. Structural mechanisms in NLR inflammasome signaling. Curr. Opin. Struct. Biol. 29C, 17-25 (2014).
35. Boyle, J. P., Mayle, S., Parkhouse, R., Monie, T. P. Comparative genomic and sequence analysis provides insight into the molecular functionality of NOD1 and NOD2. Front. Immunol. 4, 317 (2013).
36. Parkhouse, R., Boyle, J. P., Monie, T. P. Blau syndrome polymorphisms in NOD2 identify nucleotide hydrolysis and helical domain 1 as signalling regulators. FEBS Lett. 588, 3382-3389 (2014).
37. Legrand-Poels, S. et al. Modulation of Nod2-dependent NF-kappaB signaling by the actin cytoskeleton. J. Cell. Sci. 120, 1299-1310 (2007).
38. Hu, Z. et al. Structural and biochemical basis for induced self-propagation of NLRC4. Science 350, 399-404 (2015).
39. Zhang, L. et al. Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization. Science 350, 404-409 (2015).
40. Apweiler, R. et al. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 32, D115-D119 (2004).
41. Zurek, B., Proell, M., Wagner, R. N., Schwarzenbacher, R., Kufer, T. A. Mutational analysis of human NOD1 and NOD2 NACHT domains reveals different modes of activation. Innate Immun. 18, 100-111 (2012).
42. Erzberger, J. P., Berger, J. M. Evolutionary relationships and structural mechanisms of AAA plus proteins. Annu. Rev. Biophys. Biomol. Struct. 35, 93-114 (2006).
43. Barnich, N. et al. GRIM-19 interacts with nucleotide oligomerization domain 2 and serves as downstream effector of anti-bacterial function in intestinal epithelial cells. J. Biol. Chem. 280, 19021-19026 (2005).
44. Kufer, T. A., Kremmer, E., Banks, D. J., Philpott, D. J. Role for erbin in bacterial activation of Nod2. Infect. Immun. 74, 3115-3124 (2006).
45. Lipinski, S. et al. RNAi screening identifies mediators of NOD2 signaling: implications for spatial specificity of MDP recognition. Proc. Natl Acad. Sci. USA 109, 21426-21431 (2012).
46. Barbe, F., Douglas, T., Saleh, M. Advances in Nod-like receptors (NLR) biology. Cytokine. Growth. Factor. Rev. 25, 681-697 (2014).
47. Otwinowski, Z., Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol. 276, 307-326 (1997).
48. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta. Crystallogr. D Biol. Crystallogr. 58, 1948-1954 (2002).
49. Emsley, P., Cowtan, K. Coot: model-building tools for molecular graphics. Acta. Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
50. Murshudov, G. N., Vagin, A. A., Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D 53, 240-255 (1997).
51. Vagin, A., Teplyakov, A. Molecular replacement with MOLREP. Acta. Crystallogr. D 66, 22-25 (2010).
52. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta. Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
53. McNicholas, S., Potterton, E., Wilson, K. S., Noble, M. E. M. Presenting your structures: the CCP4mg molecular-graphics software. Acta. Crystallogr. D 67, 386-394 (2011).