Structural analysis of the catalytic domain of tetanus neurotoxin

Toxicon

Volumn 45, Issue 7, 2005, Pages 929-939

  Rao, Krishnamurthy N ^a   Kumaran, Desigan ^a   Binz, Thomas ^b   Swaminathan, Subramanyam ^a  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Botulinum neurotoxin; Clostridium neurotoxin; Dual wavelength anomalous diffraction (DAD); Metalloprotease; Tetanus neurotoxin; X ray structure; Zinc

Indexed keywords

BOTULINUM TOXIN B; MEMBRANE PROTEIN; NEUROTOXIN; TETANUS TOXIN; WATER; ZINC ION;

ARTICLE; BINDING AFFINITY; CATALYSIS; EXPERIMENT; MEMBRANE VESICLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; TOXIN ANALYSIS; TOXIN STRUCTURE;

AMINO ACID SEQUENCE; BOTULINUM TOXINS; CATALYTIC DOMAIN; CRYSTALLIZATION; METALLOENDOPEPTIDASES; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; TETANUS TOXIN;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM;

EID: 19344372277     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2005.02.032     Document Type: Article

References (47)

1. R. Agarwal, S. Eswaramoorthy, D. Kumaran, T. Binz, and S. Swaminathan Structural analysis of botulinum neurotoxin type E catalytic domain and its mutant Glu212→Gln reveals the pivotal role of the Glu212 carboxylate in the catalytic pathway Biochemistry 43 2004 6637 6644
2. R. Agarwal, S. Eswaramoorthy, D. Kumaran, J.J. Dunn, and S. Swaminathan Cloning, high level expression, purification and crystallization of the full length Clostridium botulinum neurotoxin type E light chain Protein Expr. Purif. 34 2004 95 102
3. T. Binz, J. Blasi, S. Yamasaki, A. Baumeister, E. Link, T.C. Sudhof, R. Jahn, and H. Niemann Proteolysis of SNAP-25 by Types E and A botulinum neurotoxins J. Biol. Chem. 269 1994 1617 1620
4. 365 of the botulinum neurotoxin type A light chain are involved in transition state stabilization Biochemistry 41 2002 1717 1723
5. M.A. Breidenbach, and A. Brunger Substrate recognition strategy for botulinum neurotoxin serotype A Nature 432 2004 925 929
6. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. Delano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszwewski, M. Nilges, N.S. Pannu, R.J. Read, L.M. Rice, T. Somonsom, and G.L. Warren Crystallography and NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D54 1998 905 921
7. S.K. Burley, and G.A. Petsko Amino-aromatic interactions in proteins FEBS Lett. 203 1986 139 143
8. F. Cornille, L. Martin, C. Lenoir, D. Cussac, B.P. Roques, and M. Fourine-Zaluski Cooperative exosite dependent cleavage of synapotbrevin by tetanus toxin light chain J. Biol. Chem. 272 1997 3459 3464
9. K. Cowtan Joint CCP4 ESF-EACBM Newslett. Protein Crystallogr. 31 1994 34 38
10. E. De La Fortelle, and G. Bricogne Maximum-likelihood heavy atom parameter refinement in the MIR and MAD methods Meth. Enzymol. 276 1997 472 493
11. P. Emsley, C. Fotinou, I. Black, N.F. Fairweather, I.G. Charles, C. Watts, E. Hewitt, and N.W. Isaacs The structures of the H(C) fragment of tetanus toxin with carbohydrate subunit complexes provide insight into ganglioside binding J. Biol. Chem. 275 2000 8889 8894
12. S. Eswaramoorthy, D. Kumaran, J. Keller, and S. Swaminathan Role of metals in the biological activity of Clostridium botulinum neurotoxins Biochemistry 43 2004 2209 2216
13. V.D. Fillippis, L. Vangelista, G. Schiavo, F. Tonello, and C. Montecucco Structural studies on the zinc-endopeptidase light chain of tetanus neurotoxin Eur. J. Biochem. 229 1995 61 69
14. P. Foran, C.C. Shone, and J.O. Dolly Differences in the protease activities of tetanus and botulinum B toxins revealed by the cleavage of vesicle-associated membrane protein and various sized fragments Biochemistry 33 1994 15365 15374
15. A. Galazka, and F. Gasse The present status of tetanus and tetanus vaccination Curr. Top. Microbiol. Immunol. 195 1995 31 53
16. M.A. Hanson, and R.C. Stevens Cocrystal structure of synaptobrevin-ll bound to botulinum neurotoxin type B at 2.0 A resolution Nat. Struct. Biol. 7 2000 687 692
17. J. Jankovic, and M. Hallett Therapy with Botulinum Toxin 1994 Marcel Dekker New York
18. T.A. Jones, J. Zou, S. Cowtan, and M. Kjeldgaard Improved methods in building protein models in electron density map and the location of errors in these models Acta Crystallogr. A47 1991 110 119
19. G.J. Kleywegt, and T.A. Jones Detecting folding motifs and similarities in protein structures Meth. Enzymol. 277 1997 525 545
20. H. Kurazono, S. Mochida, T. Binz, U. Eisel, M. Quanz, O. Grebenstein, K. Wernars, B. Poulain, L. Tauc, and H. Niemann Minimal essential domains specifying toxicity of the light chains of tetanus toxin and botulinum neurotoxin type A J. Biol. Chem. 267 1992 14721 14729
21. D.B. Lacy, and R.C. Stevens Unravelling the structures and modes of action of bacterial toxins Curr. Opin. Struct. Biol. 8 1998 778 784
22. D.B. Lacy, and R.C. Stevens Sequence homology and structural analysis of clostridial neurotoxins J. Mol. Biol. 291 1999 1091 1104
23. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality for assessing the accuracy of protein structures J. Appl. Crystallogr. 26 1993 283 291
24. Y. Li, P. Foran, N.F. Fairweather, A. de Paiva, U. Weller, G. Dougan, and J.O. Dolly A single mutation in the recombinant light chain of tetanus toxin abolishes its proteolytic activity and removes the toxicity seen after reconstitution with native heavy chain Biochemistry 33 1994 7014 7020
25. H.T. McMahon, Y.A. Ushkaryov, L. Edelmann, E. Link, T. Binz, H. Niemann, R. Jahn, and T.C. Sudhof Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein Nature 364 1993 346 349
26. C. Montecucco, and G. Schiavo Structure and function of tetanus and botulinum neurotoxins Q. Rev. Biophys. 28 1995 423 472
27. J. Navaza, and P. Saludjian AMoRe: an automated molecular replacement program package Meth. Enzymol. 276 1997 581 594
28. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Meth. Enzymol. 276 1997 307 326
29. R. Pellizzari, O. Rossetto, L. Lozzi, S. Giovedi', E. Johnson, C.C. Shone, and C. Montecucco Structural determinants of the specificity for synaptic vesicle-associated membrane protein/synaptobrevin of tetanus and botulinum type B and G neurotoxins J. Biol. Chem. 271 1996 20353 20358
30. R. Rappuoli, A. Podda, M. Pizza, A. Covacci, A. Bartoloni, M.T. de Magistris, and L. Nencioni Progress towards the development of new vaccines against whooping cough Vaccine 10 1992 1027 1032
31. N.D. Rawlings, and A.J. Barrett Evolutionaly families of metallopeptidases Meth. Enzymol. 248 1995 183 228
32. M. Rigoni, P. Caccin, E.A. Johnson, C. Montecucco, and O. Rossetto Site-directed mutagenesis identifies active-site residues of the light chain of botulinum neurotoxin type A Biochem. Biophys. Res. Commun. 288 2001 1231 1237
33. O. Rossetto, P. Caccin, M. Rigoni, F. Tonello, N. Bortoletto, R.C. Stevens, and C. Montecucco Active-site mutagenesis of tetanus neurotoxin implicates TYR-375 and GLU-271 in metalloproteolytic activity Toxicon 39 2001 1151 1159
34. G. Schiavo, A. Santucci, B.R. Dasgupta, P.P. Metha, J. Jontes, F. Benfenati, M.C. Wilson, and C. Montecucco Botulinum neurotoxins serotypes A and E cleave SNAP-25 at distinct COOH-terminal peptide bonds FEBS Lett. 335 1993 99 103
35. G. Schiavo, O. Rossetto, F. Benfenati, B. Poulain, and C. Montecucco Tetanus and botulinum neurotoxins are zinc proteases specific for components of the neuroexocytosis apparatus Ann. NY. Acad. Sci. 710 1994 65 75
36. G. Schiavo, M. Matteoli, and C. Montecucco Neurotoxins affecting neuroexocytosis Physiol. Rev. 80 2000 717 766
37. B. Segelke, M. Knapp, S. Kadkhodayan, R. Balhorn, and B. Rupp Crystal structure of Clostridium botulinum neurotoxin protease in a product-bound state: evidence for noncanonical zinc protease activity Proc. Natl Acad. Sci. USA 101 2004 6888 6893
38. L.L. Simpson Molecular pharmacology of botulinum toxin and tetanus toxin Annu. Rev. Pharmacol. Toxicol. 26 1986 427 453
39. L.L. Simpson, A.B. Maksymowych, and S. Hao The role of zinc binding in the biological activity of botulinum toxin J. Biol. Chem. 276 2001 27034 27041
40. S. Swaminathan, and S. Eswaramoorthy Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B Nat. Struct. Biol. 7 2000 693 699
41. S. Swaminathan, S. Eswaramoorthy, and D. Kumaran Structure and enzymatic activity of botulinum neurotoxins Mov. Disord. 19 Suppl. 8 2004 S17 S22
42. T.C. Terwilliger, and J. Berendzen Automated structure solution for MIR and MAD Acta Crystallogr. D55 1997 849 861
43. F. Tonello, R. Pellizzari, S. Pasqualato, G. Grandi, E. Peggion, and C. Montecucco Recombinant and truncated tetanus neurotoxin light chain: cloning, expression, purification, and proteolytic activity Protein Expr. Purif. 15 1994 221 227
44. c of tetanus neurotoxin Nat. Struct. Biol. 4 1997 788 792
45. V.V. Vaidyanathan, K. Yoshino, M. Jahnz, C. Dorries, S. Bade, S. Nauenburg, H. Niemann, and T. Binz Proteolysis of SNAP-25 isoforms by botulinum neurotoxin types A, C, and E: domains and amino acid residues controlling the formation of enzyme-substrate complexes and cleavage J. Neurochem. 72 1999 327 337
46. P. Washbourne, R. Pellizzari, G. Baldini, M.C. Wilson, and C. Montecucco Botulinum neurotoxin A and E require the SNARE motif in SNAP-25 for proteolysis FEBS Lett. 418 1997 1 5
47. S. Yamasaki, Y. Hu, T. Binz, A. Kalkuhl, H. Kurazono, T. Tamura, R. Jahn, E. Kandel, and H. Niemann Synaptobrevin/vesicle-associated membrane protein (VAMP) of Aplysia californica: structure and proteolysis by tetanus toxin and botulinal neurotoxins type D and F Proc. Natl Acad. Sci. USA 91 1994 4688 4692