Structural basis of the pH-dependent assembly of a botulinum neurotoxin complex

Journal of Molecular Biology

Volumn 426, Issue 22, 2014, Pages 3773-3782

  Matsui, Tsutomu ^a   Gu, Shenyan ^b   Lam, Kwok Ho ^b   Carter, Lester G ^a   Rummel, Andreas ^c   Mathews, Irimpan I ^a   Jin, Rongsheng ^b  

^a SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

botulinum neurotoxin; neurotoxin associated proteins; non toxic non hemagglutinin; progenitor toxin complex; X ray scattering

Indexed keywords

BOTULINUM TOXIN A; NEUROTOXIN; BOTULINUM TOXIN; NTNH PROTEIN, CLOSTRIDIUM BOTULINUM;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CURVE FITTING; GASTROINTESTINAL TRACT; MECHANICAL TORSION; MOLECULAR WEIGHT; NONHUMAN; SIGNAL NOISE RATIO; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; PH; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SMALL ANGLE SCATTERING; X RAY DIFFRACTION;

BOTULINUM TOXINS; CRYSTALLOGRAPHY, X-RAY; HYDROGEN-ION CONCENTRATION; NEUROTOXINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SCATTERING, SMALL ANGLE; X-RAY DIFFRACTION;

EID: 84908072421     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.09.009     Document Type: Article

References (39)

1. Hill KK, Smith TJ. Genetic diversity within Clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes. Curr Top Microbiol Immunol 2013;364: 1-20.
2. Dover N, Barash JR, Hill KK, Xie G, Arnon SS. Molecular characterization of a novel botulinum neurotoxin type H gene. J Infect Dis 2014;209:192-202.
3. Montecucco C, Schiavo G. Structure and function of tetanus and botulinum neurotoxins. Q Rev Biophys 1995;28:423-72.
4. Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, et al. Botulinum toxin as a biological weapon: medical and public health management. JAMA 2001;285: 1059-70.
5. Sugiyama H. Clostridium botulinum neurotoxin. Microbiol Rev 1980;44:419-48.
6. Ohishi I, Sugii S, Sakaguchi G. Oral toxicities of Clostridium botulinum toxins in response to molecular size. Infect Immun 1977;16:107-9.
7. Gu S, Jin R. Assembly and function of the botulinum neurotoxin progenitor complex. Curr Top Microbiol Immunol 2013;364: 21-44.
8. Gu S, Rumpel S, Zhou J, Strotmeier J, Bigalke H, Perry K, et al. Botulinum neurotoxin is shielded by NTNHA in an interlocked complex. Science 2012;335:977-81.
9. Lee K, Gu S, Jin L, Le TT, Cheng LW, Strotmeier J, et al. Structure of a bimodular botulinumneurotoxin complex provides insights into its oral toxicity. PLoS Pathog 2013;9:e1003690.
10. Lee K, Lam KH, Kruel AM, Perry K, Rummel A, Jin R. Highresolution crystal structure of HA33 of botulinum neurotoxin type B progenitor toxin complex. Biochem Biophys Res Commun 2014;446:568-73.
11. Benefield DA, Dessain SK, Shine N, Ohi MD, Lacy DB. Molecular assembly of botulinum neurotoxin progenitor complexes. Proc Natl Acad Sci USA 2013;110:5630-5.
12. Amatsu S, Sugawara Y, Matsumura T, Kitadokoro K, Fujinaga Y. Crystal structure of Clostridium botulinum whole hemagglutinin reveals a huge triskelion-shaped molecular complex. J Biol Chem 2013;288:35617-25.
13. Yao G, Lee K, Gu S, Lam KH, Jin R. Botulinum neurotoxin A complex recognizes host carbohydrates through its hemagglutinin component. Toxins 2014;6:624-35.
14. Lee K, Zhong X, Gu S, Kruel AM, Dorner MB, Perry K, et al. Molecular basis for disruption of E-cadherin adhesion by botulinum neurotoxin A complex. Science 2014;344: 1405-10.
15. Sugii S, Sakaguchi G. Molecular construction of Clostridium botulinum type A toxins. Infect Immun 1975;12:1262-70.
16. Cheng LW, Onisko B, Johnson EA, Reader JR, Griffey SM, Larson AE, et al. Effects of purification on the bioavailability of botulinum neurotoxin type A. Toxicology 2008;249:123-9.
17. Montal M. Botulinum neurotoxin: a marvel of protein design. Annu Rev Biochem 2010;79:591-617.
18. Lacy DB, Tepp W, Cohen AC, DasGupta BR, Stevens RC. Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nat Struct Biol 1998;5:898-902.
19. Sagane Y, Miyashita S-I, Miyata K, Matsumoto T, Inui K, Hayashi S, et al. Small-angle X-ray scattering reveals structural dynamics of the botulinum neurotoxin associating protein, nontoxic nonhemagglutinin. Biochem Biophys Res Commun 2012;425:256-60.
20. Petoukhov MV, Svergun DI. Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys J 2005;89:1237-50.
21. Putnam CD, Hammel M, Hura GL, Tainer JA. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q Rev Biophys 2007; 40:191-285.
22. Svergun DI, Petoukhov MV, Koch MHJ. Determination of domain structure of proteins from X-ray solution scattering. Biophys J 2001;80:2946-53.
23. Rambo RP, Tainer JA. Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law. Biopolymers 2011;95:559-71.
24. Kumaran D, Eswaramoorthy S, Furey W, Navaza J, Sax M, Swaminathan S. Domain organization in Clostridium botulinum neurotoxin type E is unique: its implication in faster translocation. J Mol Biol 2009;386:233-45.
25. Wang JF, Meng JH, Lawrence GW, Zurawski TH, Sasse A, Bodeker MO, et al. Novel chimeras of botulinum neurotoxins A and E unveil contributions from the binding, translocation, and protease domains to their functional characteristics. J Biol Chem 2008;283:16993-7002.
26. Smolsky IL, Liu P, Niebuhr M, Ito K, Weiss TM, Tsuruta H. Biological small-angle X-ray scattering facility at the Stanford synchrotron radiation laboratory. J Appl Crystallogr 2007;40: s453-8.
27. Huang TC, Toraya H, Blanton TN, Wu Y. X-ray powder diffraction analysis of silver behenate, a possible low-angle diffraction standard. J Appl Crystallogr 1993;26:180-4.
28. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM, Ellis PJ, et al. Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 2002;9:401-6.
29. Martel A, Liu P, Weiss TM, Niebuhr M, Tsuruta H. An integrated high-throughput data acquisition system for biological solution X-ray scattering studies. J Synchrotron Radiat 2012;19:431-4.
30. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Crystallogr 2003;36: 1277-82.
31. Svergun DI. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Crystallogr 1992;25:495-503.
32. Orthaber D, Bergmann A, Glatter O. SAXS experiments on absolute scale with Kratky systems using water as a secondary standard. J Appl Crystallogr 2000;33:218-25.
33. Fischer H, de Oliveira Neto M, Napolitano HB, Polikarpov I, Craievich AF. Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale. J Appl Crystallogr 2010;43: 101-9.
34. Kleywegt GJ, Zou JY, Kjeldgaard M, Jones TA, Around O. International Tables for Crystallography, Volume F. Crystallography of Biological Macromolecules. In: Rossmann MG, Arnold E, editors. Dordrecht, The Netherlands: Kluwer Academic; 2001. p. 353-356-66-367.
35. West AL, Evans SE, Gonzalez JM, Carter LG, Tsuruta H, Pozharski E, et al. Ni(II) coordination to mixed sites modulates DNA binding of HpNikR via a long-range effect. Proc Natl Acad Sci USA 2012;109:5633-8.
36. Petoukhov MV, Konarev PV, Kikhney AG, Svergun DI. ATSAS 2.1-towards automated and web-supported smallangle scattering data analysis. J Appl Crystallogr 2007;40: s223-8.
37. Schneidman-Duhovny D, Hammel M, Sali A. FoXS: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res 2010;38:W540-4.
38. Volkov VV, Svergun DI. Uniqueness of ab initio shape determination in small-angle scattering. J Appl Crystallogr 2003;36:860-4.
39. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 2004;25: 1605-12.