High-resolution crystal structure of HA33 of botulinum neurotoxin type B progenitor toxin complex

Biochemical and Biophysical Research Communications

Volumn 446, Issue 2, 2014, Pages 568-573

  Lee, Kwangkook ^a   Lam, Kwok Ho ^a   Kruel, Anna Magdalena ^b   Perry, Kay ^c   Rummel, Andreas ^b   Jin, Rongsheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c Cornell University ^*  (United States)

Author keywords

Botulinum neurotoxins; Carbohydrate receptor; Hemagglutinin; Host pathogen interaction; Progenitor toxin complex

Indexed keywords

BOTULINUM TOXIN B; N ACETYLNEURAMINIC ACID;

ARTICLE; BINDING AFFINITY; CLOSTRIDIUM BOTULINUM; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLIZATION; HOST SUSCEPTIBILITY; HYDROGEN BOND; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PURIFICATION;

CLOSTRIDIUM BOTULINUM;

BOTULINUM NEUROTOXINS; CARBOHYDRATE RECEPTOR; HEMAGGLUTININ; HOST-PATHOGEN INTERACTION; PROGENITOR TOXIN COMPLEX;

BINDING SITES; BOTULINUM TOXINS; COMPUTER SIMULATION; LACTOSE; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PROTEIN BINDING; WATER;

EID: 84897988018     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2014.03.008     Document Type: Article

References (40)

1. K.K. Hill, and T.J. Smith Genetic diversity within Clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes Curr. Top. Microbiol. Immunol. 364 2013 1 20
2. N. Dover, J.R. Barash, K.K. Hill, G. Xie, and S.S. Arnon Molecular characterization of a novel botulinum neurotoxin type H gene J. Infect. Dis. 209 2014 192 202
3. G. Schiavo, F. Benfenati, B. Poulain, O. Rossetto, P. Polverino de Laureto, B.R. DasGupta, and C. Montecucco Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin Nature 359 1992 832 835
4. J. Blasi, E.R. Chapman, E. Link, T. Binz, S. Yamasaki, P. De Camilli, T.C. Sudhof, H. Niemann, and R. Jahn Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25 Nature 365 1993 160 163
5. G. Schiavo, M. Matteoli, and C. Montecucco Neurotoxins affecting neuroexocytosis Physiol. Rev. 80 2000 717 766
6. M.D. Collins, and A.K. East Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins J. Appl. Microbiol. 84 1998 5 17
7. I. Ohishi, S. Sugii, and G. Sakaguchi Oral toxicities of Clostridium botulinum toxins in response to molecular size Infect. Immun. 16 1977 107 109
8. L.W. Cheng, B. Onisko, E.A. Johnson, J.R. Reader, S.M. Griffey, A.E. Larson, W.H. Tepp, L.H. Stanker, D.L. Brandon, and J.M. Carter Effects of purification on the bioavailability of botulinum neurotoxin type A Toxicology 249 2008 123 129
9. I. Ohishi Oral toxicities of Clostridium botulinum type A and B toxins from different strains Infect. Immun. 43 1984 487 490
10. G. Sakaguchi Clostridium botulinum toxins Pharmacol. Ther. 19 1982 165 194
11. G. Lin, W.H. Tepp, C.L. Pier, M.J. Jacobson, and E.A. Johnson Expression of the Clostridium botulinum A2 neurotoxin gene cluster proteins and characterization of the A2 complex Appl. Environ. Microbiol. 76 2010 40 47
12. S. Gu, and R. Jin Assembly and function of the botulinum neurotoxin progenitor complex Curr. Top. Microbiol. Immunol. 364 2013 21 44
13. S. Gu, S. Rumpel, J. Zhou, J. Strotmeier, H. Bigalke, K. Perry, C.B. Shoemaker, A. Rummel, and R. Jin Botulinum neurotoxin is shielded by NTNHA in an interlocked complex Science 335 2012 977 981
14. K. Lee, S. Gu, L. Jin, T.T. Le, L.W. Cheng, J. Strotmeier, A.M. Kruel, G. Yao, K. Perry, A. Rummel, and R. Jin Structure of a bimodular botulinum neurotoxin complex provides insights into its oral toxicity PLoS Pathog. 9 2013 e1003690
15. S. Amatsu, Y. Sugawara, T. Matsumura, K. Kitadokoro, and Y. Fujinaga Crystal structure of Clostridium botulinum whole hemagglutinin reveals a huge triskelion-shaped molecular complex J. Biol. Chem. 288 2013 35617 35625
16. K. Inoue, Y. Fujinaga, T. Watanabe, T. Ohyama, K. Takeshi, K. Moriishi, H. Nakajima, K. Inoue, and K. Oguma Molecular composition of Clostridium botulinum type A progenitor toxins Infect. Immun. 64 1996 1589 1594
17. A. Couesnon, Y. Pereira, and M.R. Popoff Receptor-mediated transcytosis of botulinum neurotoxin A through intestinal cell monolayers Cell. Microbiol. 10 2008 375 387
18. A. Couesnon, T. Shimizu, and M.R. Popoff Differential entry of botulinum neurotoxin A into neuronal and intestinal cells Cell. Microbiol. 11 2009 289 308
19. A. Couesnon, J. Molgo, C. Connan, and M.R. Popoff Preferential entry of botulinum neurotoxin A Hc domain through intestinal crypt cells and targeting to cholinergic neurons of the mouse intestine PLoS Pathog. 8 2012 e1002583
20. T. Nakamura, T. Tonozuka, A. Ide, T. Yuzawa, K. Oguma, and A. Nishikawa Sugar-binding sites of the HA1 subcomponent of Clostridium botulinum type C progenitor toxin J. Mol. Biol. 376 2008 854 867
21. T. Nakamura, T. Tonozuka, S. Ito, Y. Takeda, R. Sato, I. Matsuo, Y. Ito, K. Oguma, and A. Nishikawa Molecular diversity of the two sugar-binding sites of the beta-trefoil lectin HA33/C (HA1) from Clostridium botulinum type C neurotoxin Arch. Biochem. Biophys. 512 2011 69 77
22. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
23. 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
24. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132
25. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 213 221
26. A.T. Brunger Free R value: a novel statistical quantity for assessing the accuracy of crystal structures Nature 355 1992 472 475
27. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 12 21
28. S. Hayward, and H.J. Berendsen Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme Proteins 30 1998 144 154
29. G. Yao, K. Lee, S. Gu, K.H. Lam, and R. Jin Botulinum neurotoxin A complex recognizes host carbohydrates through its hemagglutinin component Toxins (Basel) 6 2014 624 635
30. J. Michel, J. Tirado-Rives, and W.L. Jorgensen Energetics of displacing water molecules from protein binding sites: consequences for ligand optimization J. Am. Chem. Soc. 131 2009 15403 15411
31. J.E. Ladbury Just add water! The effect of water on the specificity of protein-ligand binding sites and its potential application to drug design Chem. Biol. 3 1996 973 980
32. a values Proteins 61 2005 704 721
33. A.N. Thompson, D.J. Posson, P.V. Parsa, and C.M. Nimigean Molecular mechanism of pH sensing in KcsA potassium channels Proc. Natl. Acad. Sci. USA 105 2008 6900 6905
34. D.L. Weeks, and G. Sachs Sites of pH regulation of the urea channel of Helicobacter pylori Mol. Microbiol. 40 2001 1249 1259
35. J.C. Perez, and E.A. Groisman Acid pH activation of the PmrA/PmrB two-component regulatory system of Salmonella enterica Mol. Microbiol. 63 2007 283 293
36. D.S. Mueller, T. Kampmann, R. Yennamalli, P.R. Young, B. Kobe, and A.E. Mark Histidine protonation and the activation of viral fusion proteins Biochem. Soc. Trans. 36 2008 43 45
37. L.W. Cheng, and T.D. Henderson 2nd Comparison of oral toxicological properties of botulinum neurotoxin serotypes A and B Toxicon 58 2011 62 67
38. K. Hasegawa, T. Watanabe, T. Suzuki, A. Yamano, T. Oikawa, Y. Sato, H. Kouguchi, T. Yoneyama, K. Niwa, T. Ikeda, and T. Ohyama A novel subunit structure of Clostridium botulinum serotype D toxin complex with three extended arms J. Biol. Chem. 282 2007 24777 24783
39. J. Pei, B.H. Kim, and N.V. Grishin PROMALS3D: a tool for multiple protein sequence and structure alignments Nucleic Acids Res. 36 2008 2295 2300
40. P. Gouet, E. Courcelle, D.I. Stuart, and F. Metoz ESPript: analysis of multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308