Crystal structure of the leucine-rich repeat domain of the NOD-like receptor NLRP1: Implications for binding of muramyl dipeptide

FEBS Letters

Volumn 588, Issue 18, 2014, Pages 3327-3332

  Reubold, Thomas F ^a   Hahne, Gernot ^b   Wohlgemuth, Sabine ^b   Eschenburg, Susanne ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; MURAMYL DIPEPTIDE; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; NLRP1 PROTEIN, HUMAN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; NALP1; NLR FAMILY PYRIN DOMAIN CONTAINING 1; NOD-LIKE RECEPTOR; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; STRUCTURAL HOMOLOGY; X RAY CRYSTALLOGRAPHY;

MURAMYL DIPEPTIDE; NALP1; NLR FAMILY PYRIN DOMAIN CONTAINING 1; NOD-LIKE RECEPTOR; PATHOGEN ASSOCIATED MOLECULAR PATTERN;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; APOPTOSIS REGULATORY PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84908681881     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.07.017     Document Type: Article

References (50)

1. H. Kumar, T. Kawai, and S. Akira Pathogen recognition by the innate immune system Int. Rev. Immunol. 30 2011 16 34
2. J.A. Mitchell, M.J. Paul-Clark, G.W. Clarke, S.K. McMaster, and N. Cartwright Critical role of toll-like receptors and nucleotide oligomerisation domain in the regulation of health and disease J. Endocrinol. 193 2007 323 330
3. T.D. Kanneganti, M. Lamkanfi, and G. Nunez Intracellular NOD-like receptors in host defense and disease Immunity 27 2007 549 559
4. Inohara, Chamaillard, C. McDonald, and G. Nunez NOD-LRR proteins: role in host-microbial interactions and inflammatory disease Annu. Rev. Biochem. 74 2005 355 383
5. J. Tschopp, F. Martinon, and K. Burns NALPs: a novel protein family involved in inflammation Nat. Rev. Mol. Cell Biol. 4 2003 95 104
6. K. Schroder, and J. Tschopp The inflammasomes Cell 140 2010 821 832
7. H. Wen, E.A. Miao, and J.P. Ting Mechanisms of NOD-like receptor-associated inflammasome activation Immunity 39 2013 432 441
8. B. Faustin Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation Mol. Cell 25 2007 713 724
9. S.E. Girardin, I.G. Boneca, J. Viala, M. Chamaillard, A. Labigne, G. Thomas, D.J. Philpott, and P.J. Sansonetti Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection J. Biol. Chem. 278 2003 8869 8872
10. S.E. Girardin Nod1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan Science 300 2003 1584 1587
11. F. Martinon, V. Petrilli, A. Mayor, A. Tardivel, and J. Tschopp Gout-associated uric acid crystals activate the NALP3 inflammasome Nature 440 2006 237 241
12. S. Mariathasan Cryopyrin activates the inflammasome in response to toxins and ATP Nature 440 2006 228 232
13. C. Dostert, V. Petrilli, R. Van Bruggen, C. Steele, B.T. Mossman, and J. Tschopp Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica Science 320 2008 674 677
14. H. Laroui l-Ala-gamma-d-Glu-meso-diaminopimelic acid (DAP) interacts directly with leucine-rich region domain of nucleotide-binding oligomerization domain 1, increasing phosphorylation activity of receptor-interacting serine/threonine-protein kinase 2 and its interaction with nucleotide-binding oligomerization domain 1 J. Biol. Chem. 286 2011 31003 31013
15. J. Mo, J.P. Boyle, C.B. Howard, T.P. Monie, B.K. Davis, and J.A. Duncan Pathogen sensing by nucleotide-binding oligomerization domain-containing protein 2 (NOD2) is mediated by direct binding to muramyl dipeptide and ATP J. Biol. Chem. 287 2012 23057 23067
16. M. Hong, S.I. Yoon, and I.A. Wilson Structure and functional characterization of the RNA-binding element of the NLRX1 innate immune modulator Immunity 36 2012 337 347
17. C. Stehlik, and J.C. Reed The PYRIN connection: novel players in innate immunity and inflammation J. Exp. Med. 200 2004 551 558
18. S. Hiller, A. Kohl, F. Fiorito, T. Herrmann, G. Wider, J. Tschopp, M.G. Grutter, and K. Wuthrich NMR structure of the apoptosis- and inflammation-related NALP1 pyrin domain Structure 11 2003 1199 1205
19. A.S. Pinheiro, M. Proell, C. Eibl, R. Page, R. Schwarzenbacher, and W. Peti Three-dimensional structure of the NLRP7 pyrin domain: insight into pyrin-pyrin-mediated effector domain signaling in innate immunity J. Biol. Chem. 285 2010 27402 27410
20. J.Y. Bae, and H.H. Park Crystal structure of NALP3 protein pyrin domain (PYD) and its implications in inflammasome assembly J. Biol. Chem. 286 2011 39528 39536
21. A.S. Pinheiro, C. Eibl, Z. Ekman-Vural, R. Schwarzenbacher, and W. Peti The NLRP12 pyrin domain: structure, dynamics, and functional insights J. Mol. Biol. 413 2011 790 803
22. M.Y. Su, C.I. Kuo, C.F. Chang, and C.I. Chang Three-dimensional structure of human NLRP10/PYNOD pyrin domain reveals a homotypic interaction site distinct from its mouse homologue PLoS One 8 2013 e67843
23. C. Eibl Structural and functional analysis of the NLRP4 pyrin domain Biochemistry 51 2012 7330 7341
24. F. Manon, A. Favier, G. Nunez, J.P. Simorre, and S. Cusack Solution structure of NOD1 CARD and mutational analysis of its interaction with the CARD of downstream kinase RICK J. Mol. Biol. 365 2007 160 174
25. Z. Hu Crystal structure of NLRC4 reveals its autoinhibition mechanism Science 341 2013 172 175
26. D.R. Mason, P.L. Beck, and D.A. Muruve Nucleotide-binding oligomerization domain-like receptors and inflammasomes in the pathogenesis of non-microbial inflammation and diseases J. Innate Immun. 4 2012 16 30
27. D. Chen, C. Duggan, T.B. Reden, L.M. Kooragayala, D.E. Texada, and M.P. Langford Calreticulin is a binding protein for muramyl dipeptide and peptidoglycan in RK13 cells Biochemistry 43 2004 11796 11801
28. D. Chen, D.E. Texada, C. Duggan, C. Liang, T.B. Reden, L.M. Kooragayala, and M.P. Langford Surface calreticulin mediates muramyl dipeptide-induced apoptosis in RK13 cells J. Biol. Chem. 280 2005 22425 22436
29. W. Kabsch Integration, scaling, space-group assignment and post-refinement Acta Crystallogr. D 66 2010 133 144
30. N. Eswar, D. Eramian, B. Webb, M.Y. Shen, and A. Sali Protein structure modeling with MODELLER Methods Mol. Biol. 426 2008 145 159
31. R.J. Johnson, J.G. McCoy, C.A. Bingman, G.N. Phillips Jr., and R.T. Raines Inhibition of human pancreatic ribonuclease by the human ribonuclease inhibitor protein J. Mol. Biol. 368 2007 434 449
32. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
33. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D 66 2010 486 501
34. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D 53 1997 240 255
35. A.V. Kajava Structural diversity of leucine-rich repeat proteins J. Mol. Biol. 277 1998 519 527
36. J. Bella, K.L. Hindle, P.A. McEwan, and S.C. Lovell The leucine-rich repeat structure Cell. Mol. Life Sci. 65 2008 2307 2333
37. J. Hofsteenge, B. Kieffer, R. Matthies, B.A. Hemmings, and S.R. Stone Amino acid sequence of the ribonuclease inhibitor from porcine liver reveals the presence of leucine-rich repeats Biochemistry 27 1988 8537 8544
38. B. Kobe, and J. Deisenhofer Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats Nature 366 1993 751 756
39. L. Holm, and P. Rosenstrom Dali server: conservation mapping in 3D Nucleic Acids Res. 38 2010 W545 W549
40. A.Y. Istomin, and A. Godzik Understanding diversity of human innate immunity receptors: analysis of surface features of leucine-rich repeat domains in NLRs and TLRs BMC Immunol. 10 2009 48
41. M. Proell, S.J. Riedl, J.H. Fritz, A.M. Rojas, and R. Schwarzenbacher The Nod-like receptor (NLR) family: a tale of similarities and differences PLoS One 3 2008 e2119
42. T. Tanabe Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition EMBO J. 23 2004 1587 1597
43. N. Eswar, B. Webb, M.A. Marti-Renom, M.S. Madhusudhan, D. Eramian, M.Y. Shen, U. Pieper, and A. Sali Comparative protein structure modeling using Modeller Curr. Protoc. Bioinform. 2006 (Chapter 5, Unit 5)
44. R.C. Hillig, and L. Renault Detecting and overcoming hemihedral twinning during the MIR structure determination of Rna1p Acta Crystallogr. D 62 2006 750 765
45. J.L. Tenthorey, E.M. Kofoed, M.D. Daugherty, H.S. Malik, and R.E. Vance Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes Mol. Cell 54 2014 17 29
46. L.C. Hsu A NOD2-NALP1 complex mediates caspase-1-dependent IL-1beta secretion in response to Bacillus anthracis infection and muramyl dipeptide Proc. Natl. Acad. Sci. USA 105 2008 7803 7808
47. F. Martinon, L. Agostini, E. Meylan, and J. Tschopp Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome Curr. Biol. 14 2004 1929 1934
48. S.I. Yoon, O. Kurnasov, V. Natarajan, M. Hong, A.V. Gudkov, A.L. Osterman, and I.A. Wilson Structural basis of TLR5-flagellin recognition and signaling Science 335 2012 859 864
49. T.F. Reubold, S. Wohlgemuth, and S. Eschenburg Crystal structure of full-length Apaf-1: how the death signal is relayed in the mitochondrial pathway of apoptosis Structure 19 2011 1074 1083
50. S. Yuan, X. Yu, J.M. Asara, J.E. Heuser, S.J. Ludtke, and C.W. Akey The holo-apoptosome: activation of procaspase-9 and interactions with caspase-3 Structure 19 2011 1084 1096