Gaining ground: assays for therapeutics against botulinum neurotoxin

Simpson, 2004, Identification of the major steps in botulinum toxin action, Annu. Rev. Pharmacol. Toxicol., 44, 167, 10.1146/annurev.pharmtox.44.101802.121554 Montecucco, 2005, Botulinal neurotoxins: revival of an old killer, Curr. Opin. Pharmacol., 5, 274, 10.1016/j.coph.2004.12.006 Schantz, 1992, Properties and use of botulinum toxin and other microbial neurotoxins in medicine, Microbiol. Rev., 56, 80, 10.1128/MMBR.56.1.80-99.1992 Breidenbach, 2005, New insights into clostridial neurotoxin-SNARE interactions, Trends Mol. Med., 11, 377, 10.1016/j.molmed.2005.06.012 Wein, 2005, Analyzing a bioterror attack on the food supply: the case of botulinum toxin in milk, Proc. Natl. Acad. Sci. U. S. A., 102, 9984, 10.1073/pnas.0408526102 Arnon, 2001, Botulinum toxin as a biological weapon: medical and public health management, JAMA, 285, 1059, 10.1001/jama.285.8.1059 Foster, 2006, Botulinum neurotoxin - from laboratory to bedside, Neurotox Res., 9, 133, 10.1007/BF03033931 Dolly, 2009, Neuro-exocytosis: botulinum toxins as inhibitory probes and versatile therapeutics, Curr. Opin. Pharmacol., 9, 326, 10.1016/j.coph.2009.03.004 Truong, 2006, Botulinum toxin: clinical use, Parkinsonism Relat Disord, 12, 331, 10.1016/j.parkreldis.2006.06.002 Chen, 2009, Engineering botulinum neurotoxin to extend therapeutic intervention, Proc. Natl. Acad. Sci. U. S. A., 106, 9180, 10.1073/pnas.0903111106 Smith, 2009, Botulism and vaccines for its prevention, Vaccine, 27, D33, 10.1016/j.vaccine.2009.08.059 Horowitz, 2005, Botulinum toxin, Crit. Care Clin., 21, 825, 10.1016/j.ccc.2005.06.008 Brunger, 2008, Highly specific interactions between botulinum neurotoxins and synaptic vesicle proteins, Cell Mol. Life Sci., 65, 2296, 10.1007/s00018-008-8088-0 Dong, 2003, Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells, J. Cell. Biol., 162, 1293, 10.1083/jcb.200305098 Dong, 2006, SV2 is the protein receptor for botulinum neurotoxin A, Science, 312, 592, 10.1126/science.1123654 Rummel, 2007, Identification of the protein receptor binding site of botulinum neurotoxins B and G proves the double-receptor concept, Proc. Natl. Acad. Sci. U. S. A., 104, 359, 10.1073/pnas.0609713104 Bakry, 1991, Lectins from Triticum vulgaris and Limax flavus are universal antagonists of botulinum neurotoxin and tetanus toxin, J. Pharmacol. Exp. Ther., 258, 830 Kale, 2007, Synthesis of soluble multivalent glycoconjugates that target the Hc region of botulinum neurotoxin A, Bioorg. Med. Chem. Lett., 17, 2459, 10.1016/j.bmcl.2007.02.028 Simpson, 1983, Ammonium chloride and methylamine hydrochloride antagonize clostridial neurotoxins, J. Pharmacol. Exp. Ther., 225, 546 Simpson, 1994, Inhibition of vacuolar adenosine triphosphatase antagonizes the effects of clostridial neurotoxins but not phospholipase A2 neurotoxins, J. Pharmacol. Exp. Ther., 269, 256 Keller, 2004, Uptake of botulinum neurotoxin into cultured neurons, Biochemistry, 43, 526, 10.1021/bi0356698 Sorensen, 2005, SNARE complexes prepare for membrane fusion, Trends Neurosci., 28, 453, 10.1016/j.tins.2005.06.007 Willis, 2008, The strange case of the botulinum neurotoxin: using chemistry and biology to modulate the most deadly poison, Angew. Chem. Int. Ed. Engl., 47, 8360, 10.1002/anie.200705531 Zuniga, 2008, A potent peptidomimetic inhibitor of botulinum neurotoxin serotype A has a very different conformation than SNAP-25 substrate, Structure, 16, 1588, 10.1016/j.str.2008.07.011 Schmidt, 2005, Botulinum neurotoxin serotype F: identification of substrate recognition requirements and development of inhibitors with low nanomolar affinity, Biochemistry, 44, 4067, 10.1021/bi0477642 Schmidt, 1998, Type A botulinum neurotoxin proteolytic activity: development of competitive inhibitors and implications for substrate specificity at the S1’ binding subsite, FEBS Lett., 435, 61, 10.1016/S0014-5793(98)01041-2 Sukonpan, 2004, Synthesis of substrates and inhibitors of botulinum neurotoxin type A metalloprotease, J. Pept. Res., 63, 181, 10.1111/j.1399-3011.2004.00124.x Shone, 2006, The 5th International Conference on Basic and Therapeutic Aspects of Botulinum and Tetanus Neurotoxins. Workshop review: assays and detection, Neurotox. Res., 9, 205, 10.1007/BF03033940 Schmidt, 2003, Fluorigenic substrates for the protease activities of botulinum neurotoxins, serotypes A, B, and F, Appl. Environ. Microbiol., 69, 297, 10.1128/AEM.69.1.297-303.2003 Gul, 2004, Inhibition of the protease activity of the light chain of type A botulinum neurotoxin by aqueous extract from stinging nettle (Urtica dioica) leaf, Basic Clin. Pharmacol. Toxicol., 95, 215, 10.1111/j.1742-7843.2004.pto950503.x Adler, 2003, A capillary electrophoresis technique for evaluating botulinum neurotoxin B light chain activity, J. Protein Chem., 22, 441, 10.1023/B:JOPC.0000005459.00492.60 Anne, 2005, Partial protection against Botulinum B neurotoxin-induced blocking of exocytosis by a potent inhibitor of its metallopeptidase activity, Chembiochem, 6, 1375, 10.1002/cbic.200400398 Burnett, 2003, Novel small molecule inhibitors of botulinum neurotoxin A metalloprotease activity, Biochem. Biophys. Res. Commun., 310, 84, 10.1016/j.bbrc.2003.08.112 Kalandakanond, 2001, Cleavage of intracellular substrates of botulinum toxins A, C and D in a mammalian target tissue, J. Pharmacol. Exp. Ther., 296, 749 Ferracci, 2005, Synaptic vesicle chips to assay botulinum neurotoxins, Biochem. J., 391, 659, 10.1042/BJ20050855 Marconi, 2008, A protein chip membrane-capture assay for botulinum neurotoxin activity, Toxicol. Appl. Pharmacol., 233, 439, 10.1016/j.taap.2008.09.005 Hines, 2008, Use of a recombinant fluorescent substrate with cleavage sites for all botulinum neurotoxins in high-throughput screening of natural product extracts for inhibitors of serotypes A, B and E, Appl. Environ. Microbiol., 74, 653, 10.1128/AEM.01690-07 Anne, 2001, High-throughput fluorogenic assay for determination of botulinum type B neurotoxin protease activity, Anal. Biochem., 291, 253, 10.1006/abio.2001.5028 Mangru, 2005, Integrated bioassays in microfluidic devices: botulinum toxin assays, J. Biomol. Screen., 10, 788, 10.1177/1087057105278927 Dong, 2004, Using fluorescent sensors to detect botulinum neurotoxin activity in vitro and in living cells, Proc. Natl. Acad. Sci. U. S. A., 101, 14701, 10.1073/pnas.0404107101 Pires-Alves, 2009, Tandem fluorescent proteins as enhanced FRET-based substrates for botulinum neurotoxin activity, Toxicon, 53, 392, 10.1016/j.toxicon.2008.12.016 Bagramyan, 2008, Attomolar detection of botulinum toxin type A in complex biological matrices, PLoS ONE, 3, e2041, 10.1371/journal.pone.0002041 Poras, 2009, Detection and quantification of botulinum neurotoxin type a by a novel rapid in vitro fluorimetric assay, Appl. Environ. Microbiol., 75, 4382, 10.1128/AEM.00091-09 Cheng, 2009, Antibody protection against botulinum neurotoxin intoxication in mice, Infect. Immun., 77, 4305, 10.1128/IAI.00405-09 Boyer, 2005, From the mouse to the mass spectrometer: detection and differentiation of the endoproteinase activities of botulinum neurotoxins A-G by mass spectrometry, Anal. Chem., 77, 3916, 10.1021/ac050485f Kalb, 2006, The use of Endopep-MS for the detection of botulinum toxins A, B, E and F in serum and stool samples, Anal. Biochem., 351, 84, 10.1016/j.ab.2006.01.027 Gonzalez, 1998, Intracellular detection assays for high-throughput screening, Curr. Opin. Biotechnol., 9, 624, 10.1016/S0958-1669(98)80141-9 Cai, 2007, Botulism diagnostics: from clinical symptoms to in vitro assays, Crit. Rev. Microbiol., 33, 109, 10.1080/10408410701364562 Eubanks, 2005, Vitamin B2-mediated cellular photoinhibition of botulinum neurotoxin A, FEBS Lett., 579, 5361, 10.1016/j.febslet.2005.08.072 Hall, 2004, Novel application of an in vitro technique to the detection and quantification of botulinum neurotoxin antibodies, J. Immunol. Methods, 288, 55, 10.1016/j.jim.2004.02.011 Pellett, 2007, A neuronal cell-based botulinum neurotoxin assay for highly sensitive and specific detection of neutralizing serum antibodies, FEBS Lett., 581, 4803, 10.1016/j.febslet.2007.08.078 Foran, 2003, Evaluation of the therapeutic usefulness of botulinum neurotoxin B, C1, E and F compared with the long lasting type A. Basis for distinct durations of inhibition of exocytosis in central neurons, J. Biol. Chem., 278, 1363, 10.1074/jbc.M209821200 Sheridan, 2005, Primary cell culture for evaluation of botulinum neurotoxin antagonists, Toxicon, 45, 377, 10.1016/j.toxicon.2004.11.009 Stahl, 2007, Primary cultures of embryonic chicken neurons for sensitive cell-based assay of botulinum neurotoxin: implications for therapeutic discovery, J. Biomol. Screen., 12, 370, 10.1177/1087057106299163 Nuss, 2010, Development of cell-based assays to measure botulinum neurotoxin serotype A activity using cleavage-sensitive antibodies, J. Biomol. Screen., 15, 42, 10.1177/1087057109354779 Fang, 2006, A yeast assay probes the interaction between botulinum neurotoxin serotype B and its SNARE substrate, Proc. Natl. Acad. Sci. U. S. A., 103, 6958, 10.1073/pnas.0510816103 Thyagarajan, 2009, Capsaicin protects mouse neuromuscular junctions from the neuroparalytic effects of botulinum neurotoxin A, J. Pharmacol. Exp. Ther., 331, 361, 10.1124/jpet.109.156901 Yoneda, 2005, Comparison of the therapeutic indexes of different molecular forms of botulinum toxin type A, Eur. J. Pharmacol., 508, 223, 10.1016/j.ejphar.2004.12.007 Roxas-Duncan, 2009, Identification and biochemical characterization of small-molecule inhibitors of Clostridium botulinum neurotoxin serotype A, Antimicrob Agents Chemother., 53, 3478, 10.1128/AAC.00141-09 Dodd, 2005, Botulinum neurotoxin type A causes shifts in myosin heavy chain composition in muscle, Toxicon, 46, 196, 10.1016/j.toxicon.2005.03.022 Keller, 2006, Recovery from botulinum neurotoxin poisoning in vivo, Neuroscience, 139, 629, 10.1016/j.neuroscience.2005.12.029 Straughan, 2006, Progress in applying the Three Rs to the potency testing of Botulinum toxin type A, Altern. Lab. Anim., 34, 305, 10.1177/026119290603400314 Pickett, 2008, The in vivo rat muscle force model is a reliable and clinically relevant test of consistency among botulinum toxin preparations, Toxicon, 52, 455, 10.1016/j.toxicon.2008.06.021 Hubbell, 2000, Identifying conformational changes with site-directed spin labeling, Nat. Struct. Biol., 7, 735, 10.1038/78956 Mollaaghababa, 2000, Time-resolved site-directed spin-labeling studies of bacteriorhodopsin: loop-specific conformational changes in M, Biochemistry, 39, 1120, 10.1021/bi991963h Steinhoff, 1994, Time-resolved detection of structural changes during the photocycle of spin-labeled bacteriorhodopsin, Science, 266, 105, 10.1126/science.7939627 Stoevesandt, 2009, Protein microarrays: high-throughput tools for proteomics, Expert Rev. Proteomics, 6, 145, 10.1586/epr.09.2