{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T20:47:06Z","timestamp":1790714826670,"version":"4.1.0"},"reference-count":45,"publisher":"Springer Science and Business Media LLC","issue":"7481","license":[{"start":{"date-parts":[[2013,11,17]],"date-time":"2013-11-17T00:00:00Z","timestamp":1384646400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nature"],"published-print":{"date-parts":[[2014,1]]},"DOI":"10.1038\/nature12732","type":"journal-article","created":{"date-parts":[[2013,11,15]],"date-time":"2013-11-15T17:14:14Z","timestamp":1384535654000},"page":"108-111","source":"Crossref","is-referenced-by-count":127,"title":["Structural basis for recognition of synaptic vesicle protein 2C by botulinum neurotoxin A"],"prefix":"10.1038","volume":"505","author":[{"given":"Roger M.","family":"Benoit","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Frey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manuel","family":"Hilbert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josta T.","family":"Kevenaar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mara M.","family":"Wieser","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian U.","family":"Stirnimann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"McMillan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tom","family":"Ceska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florence","family":"Lebon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rolf","family":"Jaussi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michel O.","family":"Steinmetz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gebhard F. X.","family":"Schertler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Casper C.","family":"Hoogenraad","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guido","family":"Capitani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard A.","family":"Kammerer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2013,11,17]]},"reference":[{"key":"BFnature12732_CR1","doi-asserted-by":"publisher","first-page":"1059","DOI":"10.1001\/jama.285.8.1059","volume":"285","author":"SS Arnon","year":"2001","unstructured":"Arnon, S. S. et al. Botulinum toxin as a biological weapon: medical and public health management. J. Am. Med. Assoc. 285, 1059\u20131070 (2001)","journal-title":"J. Am. Med. Assoc."},{"key":"BFnature12732_CR2","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.clindermatol.2003.11.013","volume":"22","author":"J Carruthers","year":"2004","unstructured":"Carruthers, J. & Carruthers, A. Botox: beyond wrinkles. Clin. Dermatol. 22, 89\u201393 (2004)","journal-title":"Clin. Dermatol."},{"key":"BFnature12732_CR3","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1046\/j.1365-2230.2000.00606.x","volume":"25","author":"AC Markey","year":"2000","unstructured":"Markey, A. C. Botulinum A exotoxin in cosmetic dermatology. Clin. Exp. Dermatol. 25, 173\u2013175 (2000)","journal-title":"Clin. Exp. Dermatol."},{"key":"BFnature12732_CR4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/j.1365-2958.1994.tb00396.x","volume":"13","author":"C Montecucco","year":"1994","unstructured":"Montecucco, C. & Schiavo, G. Mechanism of action of tetanus and botulinum neurotoxins. Mol. Microbiol. 13, 1\u20138 (1994)","journal-title":"Mol. Microbiol."},{"key":"BFnature12732_CR5","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1146\/annurev.biochem.051908.125345","volume":"79","author":"M Montal","year":"2010","unstructured":"Montal, M. Botulinum neurotoxin: a marvel of protein design. Annu. Rev. Biochem. 79, 591\u2013617 (2010)","journal-title":"Annu. Rev. Biochem."},{"key":"BFnature12732_CR6","doi-asserted-by":"publisher","first-page":"e1003369","DOI":"10.1371\/journal.ppat.1003369","volume":"9","author":"BP Jacky","year":"2013","unstructured":"Jacky, B. P. et al. Identification of fibroblast growth factor receptor 3 (FGFR3) as a protein receptor for botulinum neurotoxin serotype A (BoNT\/A). PLoS Pathogens 9, e1003369 (2013)","journal-title":"PLoS Pathogens"},{"key":"BFnature12732_CR7","doi-asserted-by":"publisher","first-page":"592","DOI":"10.1126\/science.1123654","volume":"312","author":"M Dong","year":"2006","unstructured":"Dong, M. et al. SV2 is the protein receptor for botulinum neurotoxin A. Science 312, 592\u2013596 (2006)","journal-title":"Science"},{"key":"BFnature12732_CR8","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1021\/bi052130w","volume":"45","author":"MW Vetting","year":"2006","unstructured":"Vetting, M. W. et al. Pentapeptide repeat proteins. Biochemistry 45, 1\u201310 (2006)","journal-title":"Biochemistry"},{"key":"BFnature12732_CR9","doi-asserted-by":"publisher","first-page":"W545","DOI":"10.1093\/nar\/gkq366","volume":"38","author":"L Holm","year":"2010","unstructured":"Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545\u2013W549 (2010)","journal-title":"Nucleic Acids Res."},{"key":"BFnature12732_CR10","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1016\/S0022-2836(77)80200-3","volume":"112","author":"FC Bernstein","year":"1977","unstructured":"Bernstein, F. C. et al. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535\u2013542 (1977)","journal-title":"J. Mol. Biol."},{"key":"BFnature12732_CR11","doi-asserted-by":"publisher","first-page":"1480","DOI":"10.1126\/science.1110699","volume":"308","author":"SS Hegde","year":"2005","unstructured":"Hegde, S. S. et al. A fluoroquinolone resistance protein from Mycobacterium tuberculosis that mimics DNA. Science 308, 1480\u20131483 (2005)","journal-title":"Science"},{"key":"BFnature12732_CR12","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1107\/S1744309110053315","volume":"67","author":"MW Vetting","year":"2011","unstructured":"Vetting, M. W., Hegde, S. S., Zhang, Y. & Blanchard, J. S. Pentapeptide-repeat proteins that act as topoisomerase poison resistance factors have a common dimer interface. Acta Crystallogr. F 67, 296\u2013302 (2011)","journal-title":"Acta Crystallogr. F"},{"key":"BFnature12732_CR13","doi-asserted-by":"publisher","first-page":"765","DOI":"10.1038\/nature03679","volume":"435","author":"R Krishnan","year":"2005","unstructured":"Krishnan, R. & Lindquist, S. L. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435, 765\u2013772 (2005)","journal-title":"Nature"},{"key":"BFnature12732_CR14","doi-asserted-by":"publisher","first-page":"11099","DOI":"10.1073\/pnas.1017504108","volume":"108","author":"AW Bryan Jr","year":"2011","unstructured":"Bryan, A. W., Jr, Starner-Kreinbrink, J. L., Hosur, R., Clark, P. L. & Berger, B. Structure-based prediction reveals capping motifs that inhibit \u03b2-helix aggregation. Proc. Natl Acad. Sci. USA 108, 11099\u201311104 (2011)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature12732_CR15","doi-asserted-by":"publisher","first-page":"2754","DOI":"10.1073\/pnas.052706099","volume":"99","author":"JS Richardson","year":"2002","unstructured":"Richardson, J. S. & Richardson, D. C. Natural \u03b2-sheet proteins use negative design to avoid edge-to-edge aggregation. Proc. Natl Acad. Sci. USA 99, 2754\u20132759 (2002)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature12732_CR16","doi-asserted-by":"publisher","first-page":"844","DOI":"10.1038\/nature03793","volume":"435","author":"C Ritter","year":"2005","unstructured":"Ritter, C. et al. Correlation of structural elements and infectivity of the HET-s prion. Nature 435, 844\u2013848 (2005)","journal-title":"Nature"},{"key":"BFnature12732_CR17","doi-asserted-by":"publisher","first-page":"1523","DOI":"10.1126\/science.1151839","volume":"319","author":"C Wasmer","year":"2008","unstructured":"Wasmer, C. et al. Amyloid fibrils of the HET-s(218\u2013289) prion form a \u03b2 solenoid with a triangular hydrophobic core. Science 319, 1523\u20131526 (2008)","journal-title":"Science"},{"key":"BFnature12732_CR18","doi-asserted-by":"publisher","first-page":"e1000129","DOI":"10.1371\/journal.ppat.1000129","volume":"4","author":"P Stenmark","year":"2008","unstructured":"Stenmark, P., Dupuy, J., Imamura, A., Kiso, M. & Stevens, R. C. Crystal structure of botulinum neurotoxin type A in complex with the cell surface co-receptor GT1b\u2014insight into the toxin-neuron interaction. PLoS Pathogens 4, e1000129 (2008)","journal-title":"PLoS Pathogens"},{"key":"BFnature12732_CR19","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1038\/2338","volume":"5","author":"DB Lacy","year":"1998","unstructured":"Lacy, D. B., Tepp, W., Cohen, A. C., DasGupta, B. R. & Stevens, R. C. Crystal structure of botulinum neurotoxin type A and implications for toxicity. Nature Struct. Biol. 5, 898\u2013902 (1998)","journal-title":"Nature Struct. Biol."},{"key":"BFnature12732_CR20","doi-asserted-by":"publisher","first-page":"5655","DOI":"10.1021\/bi3004928","volume":"51","author":"S Sun","year":"2012","unstructured":"Sun, S., Tepp, W. H., Johnson, E. A. & Chapman, E. R. Botulinum neurotoxins B and E translocate at different rates and exhibit divergent responses to GT1b and low pH. Biochemistry 51, 5655\u20135662 (2012)","journal-title":"Biochemistry"},{"key":"BFnature12732_CR21","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1016\/j.chom.2011.06.012","volume":"10","author":"S Sun","year":"2011","unstructured":"Sun, S. et al. Receptor binding enables botulinum neurotoxin B to sense low pH for translocation channel assembly. Cell Host Microbe 10, 237\u2013247 (2011)","journal-title":"Cell Host Microbe"},{"key":"BFnature12732_CR22","doi-asserted-by":"publisher","first-page":"e1000245","DOI":"10.1371\/journal.ppat.1000245","volume":"4","author":"A Fischer","year":"2008","unstructured":"Fischer, A., Mushrush, D. J., Lacy, D. B. & Montal, M. Botulinum neurotoxin devoid of receptor binding domain translocates active protease. PLoS Pathogens 4, e1000245 (2008)","journal-title":"PLoS Pathogens"},{"key":"BFnature12732_CR23","doi-asserted-by":"publisher","first-page":"5631","DOI":"10.1021\/bi9002138","volume":"48","author":"Z Fu","year":"2009","unstructured":"Fu, Z., Chen, C., Barbieri, J. T., Kim, J. J. & Baldwin, M. R. Glycosylated SV2 and gangliosides as dual receptors for botulinum neurotoxin serotype F. Biochemistry 48, 5631\u20135641 (2009)","journal-title":"Biochemistry"},{"key":"BFnature12732_CR24","doi-asserted-by":"publisher","first-page":"47","DOI":"10.2174\/187152607780090667","volume":"7","author":"S Cai","year":"2007","unstructured":"Cai, S. & Singh, B. R. Strategies to design inhibitors of Clostridium botulinum neurotoxins. Infect. Disord. Drug Targets 7, 47\u201357 (2007)","journal-title":"Infect. Disord. Drug Targets"},{"key":"BFnature12732_CR25","doi-asserted-by":"publisher","first-page":"S24","DOI":"10.1093\/ajhp\/61.suppl_6.S24","volume":"61","author":"ER Anderson Jr","year":"2004","unstructured":"Anderson, E. R., Jr Proper dose, preparation, and storage of botulinum neurotoxin serotype A. Am. J. Health Syst. Pharm. 61, S24\u2013S29 (2004)","journal-title":"Am. J. Health Syst. Pharm."},{"key":"BFnature12732_CR26","doi-asserted-by":"publisher","first-page":"2406","DOI":"10.1038\/nprot.2006.356","volume":"1","author":"S Kaech","year":"2006","unstructured":"Kaech, S. & Banker, G. Culturing hippocampal neurons. Nature Protocols 1, 2406\u20132415 (2006)","journal-title":"Nature Protocols"},{"key":"BFnature12732_CR27","doi-asserted-by":"publisher","first-page":"915","DOI":"10.1083\/jcb.201301011","volume":"201","author":"SA Spangler","year":"2013","unstructured":"Spangler, S. A. et al. Liprin-\u03b12 promotes the presynaptic recruitment and turnover of RIM1\/CASK to facilitate synaptic transmission. J. Cell Biol. 201, 915\u2013928 (2013)","journal-title":"J. Cell Biol."},{"key":"BFnature12732_CR28","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1016\/j.pep.2005.09.022","volume":"45","author":"RM Benoit","year":"2006","unstructured":"Benoit, R. M., Wilhelm, R. N., Scherer-Becker, D. & Ostermeier, C. An improved method for fast, robust, and seamless integration of DNA fragments into multiple plasmids. Protein Expr. Purif. 45, 66\u201371 (2006)","journal-title":"Protein Expr. Purif."},{"key":"BFnature12732_CR29","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1186\/1472-6750-10-56","volume":"10","author":"N Olieric","year":"2010","unstructured":"Olieric, N. et al. Automated seamless DNA co-transformation cloning with direct expression vectors applying positive or negative insert selection. BMC Biotechnol. 10, 56 (2010)","journal-title":"BMC Biotechnol."},{"key":"BFnature12732_CR30","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/j.pep.2005.01.016","volume":"41","author":"FW Studier","year":"2005","unstructured":"Studier, F. W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207\u2013234 (2005)","journal-title":"Protein Expr. Purif."},{"key":"BFnature12732_CR31","doi-asserted-by":"publisher","first-page":"1030","DOI":"10.1126\/science.1218231","volume":"336","author":"PA Karplus","year":"2012","unstructured":"Karplus, P. A. & Diederichs, K. Linking crystallographic model and data quality. Science 336, 1030\u20131033 (2012)","journal-title":"Science"},{"key":"BFnature12732_CR32","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1107\/S0907444909047337","volume":"66","author":"W Kabsch","year":"2010","unstructured":"Kabsch, W. XDS. Acta Crystallogr. D 66, 125\u2013132 (2010)","journal-title":"Acta Crystallogr. D"},{"key":"BFnature12732_CR33","doi-asserted-by":"publisher","first-page":"658","DOI":"10.1107\/S0021889807021206","volume":"40","author":"AJ McCoy","year":"2007","unstructured":"McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658\u2013674 (2007)","journal-title":"J. Appl. Crystallogr."},{"key":"BFnature12732_CR34","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1107\/S0907444912001308","volume":"68","author":"PV Afonine","year":"2012","unstructured":"Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D 68, 352\u2013367 (2012)","journal-title":"Acta Crystallogr. D"},{"key":"BFnature12732_CR35","doi-asserted-by":"publisher","first-page":"486","DOI":"10.1107\/S0907444910007493","volume":"66","author":"P Emsley","year":"2010","unstructured":"Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486\u2013501 (2010)","journal-title":"Acta Crystallogr. D"},{"key":"BFnature12732_CR36","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1107\/S0907444909042073","volume":"66","author":"VB Chen","year":"2010","unstructured":"Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12\u201321 (2010)","journal-title":"Acta Crystallogr. D"},{"key":"BFnature12732_CR37","unstructured":"DeLano, W. L. The PyMOL Molecular Graphics System. (DeLano Scientific, 2012)"},{"key":"BFnature12732_CR38","doi-asserted-by":"publisher","first-page":"10037","DOI":"10.1073\/pnas.181342398","volume":"98","author":"NA Baker","year":"2001","unstructured":"Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10037\u201310041 (2001)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature12732_CR39","doi-asserted-by":"publisher","first-page":"2256","DOI":"10.1107\/S0907444904026460","volume":"60","author":"E Krissinel","year":"2004","unstructured":"Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D 60, 2256\u20132268 (2004)","journal-title":"Acta Crystallogr. D"},{"key":"BFnature12732_CR40","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1002\/pro.5560050204","volume":"5","author":"EG Hutchinson","year":"1996","unstructured":"Hutchinson, E. G. & Thornton, J. M. PROMOTIF\u2014a program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212\u2013220 (1996)","journal-title":"Protein Sci."},{"key":"BFnature12732_CR41","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1038\/nprot.2009.2","volume":"4","author":"LA Kelley","year":"2009","unstructured":"Kelley, L. A. & Sternberg, M. J. Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4, 363\u2013371 (2009)","journal-title":"Nature Protocols"},{"key":"BFnature12732_CR42","doi-asserted-by":"publisher","first-page":"8343","DOI":"10.1021\/j100133a034","volume":"97","author":"H Heller","year":"1993","unstructured":"Heller, H., Schaefer, M. & Schulten, K. Molecular dynamics simulation of a bilayer of 200 lipids in the gel and in the liquid crystal phase. J. Phys. Chem. 97, 8343\u20138360 (1993)","journal-title":"J. Phys. Chem."},{"key":"BFnature12732_CR43","doi-asserted-by":"publisher","first-page":"774","DOI":"10.1016\/j.jmb.2007.05.022","volume":"372","author":"E Krissinel","year":"2007","unstructured":"Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774\u2013797 (2007)","journal-title":"J. Mol. Biol."},{"key":"BFnature12732_CR44","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1006\/abio.1998.2738","volume":"261","author":"YL Zhang","year":"1998","unstructured":"Zhang, Y. L. & Zhang, Z. Y. Low-affinity binding determined by titration calorimetry using a high-affinity coupling ligand: a thermodynamic study of ligand binding to protein tyrosine phosphatase 1B. Anal. Biochem. 261, 139\u2013148 (1998)","journal-title":"Anal. Biochem."},{"key":"BFnature12732_CR45","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/S0091-679X(10)97007-6","volume":"97","author":"LC Kapitein","year":"2010","unstructured":"Kapitein, L. C., Yau, K. W. & Hoogenraad, C. C. Microtubule dynamics in dendritic spines. Methods Cell Biol. 97, 111\u2013132 (2010)","journal-title":"Methods Cell Biol."}],"container-title":["Nature"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/nature12732.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nature12732","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nature12732.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,18]],"date-time":"2023-05-18T18:16:53Z","timestamp":1684433813000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/nature12732"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,11,17]]},"references-count":45,"journal-issue":{"issue":"7481","published-print":{"date-parts":[[2014,1]]}},"alternative-id":["BFnature12732"],"URL":"https:\/\/doi.org\/10.1038\/nature12732","relation":{},"ISSN":["0028-0836","1476-4687"],"issn-type":[{"value":"0028-0836","type":"print"},{"value":"1476-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,11,17]]}}}