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Botulinum Neurotoxins: Biology, Pharmacology, and Toxicology 1521-0081/69/2/200–235$25.00 https://doi.org/10.1124/pr.116.012658 PHARMACOLOGICAL REVIEWS Pharmacol Rev 69:200–235, April 2017 Copyright © 2017 by The Author(s) This is an open access article distributed under the CC BY-NC Attribution 4.0 International license. ASSOCIATE EDITOR: JEFFREY M. WITKIN Botulinum Neurotoxins: Biology, Pharmacology, and Toxicology Marco Pirazzini, Ornella Rossetto, Roberto Eleopra, and Cesare Montecucco Department of Biomedical Sciences, University of Padova, Italy (M.P., O.R., C.M.); Neurologic Department, University-Hospital S. Maria della Misericordia, Udine, Italy (R.E.); and Consiglio Nazionale delle Ricerche, Institute of Neuroscience, University of Padova, Italy (C.M.) Abstract. ....................................................................................201 I. Introduction. ..............................................................................201 A. Genetics and Structure of Botulinum Neurotoxins and Their Progenitor Toxin Complexes. ..............................................................................202 B. Molecular Architecture of Botulinum Neurotoxins . .....................................203 C. Metalloproteolytic Activity . ............................................................204 II. Biology. ....................................................................................204 Downloaded from A. Molecular Mechanism of Nerve Terminal Paralysis . .....................................204 1. Binding and Specificity. ............................................................204 2. Internalization into Nerve Terminals.. ................................................211 a. Long distance effects of botulinum neurotoxins. ....................................211 3. Membrane Translocation.. ............................................................212 4. Interchain Disulfide Reduction. ......................................................213 by guest on September 25, 2021 5. SNARE Protein Cleavage. ............................................................214 B. Duration of the Neuroparalysis Induced by Botulinum Neurotoxins .......................215 1. Reversibility of the Neuroparalysis Induced by Botulinum Neurotoxins. .............215 2. Reversibility of Botulinum Neurotoxin Action in Vitro and in Vivo. ...................216 III. Pharmacology . ..............................................................................216 A. Introduction .............................................................................216 B. Present Botulinum Neurotoxin Formulations . ..........................................217 C. Immunogenicity of Botulinum Neurotoxin Formulations . ...............................219 D. Clinical Applications of Botulinum Neurotoxins ..........................................219 1. Dystonias.............................................................................220 2. Spasticity.............................................................................221 3. Autonomic Disorders..................................................................221 4. Urologic Pathologic Conditions. ......................................................222 5. Pain. ..............................................................................222 a. Neuropathic pain. .................................................................223 b. Primary headaches. ............................................................223 6. Other Applications.. ..................................................................224 a. Gastroenterology and proctologic disorders. .....................................224 b. Depression. .......................................................................224 7. Cosmetic Uses. .......................................................................225 E. Adverse Effects . ........................................................................225 F. Contraindications and Drug Interactions . ................................................225 G. Botulinum Neurotoxin in Pregnancy .....................................................225 IV. Toxicity of Botulinum Neurotoxins...........................................................226 The authors’ research was supported by Fondazione Cariparo, the Axonomics project of Provincia di Trento, the Ministery of Defence, the University of Padova and the University of Udine. Address correspondence to: Cesare Montecucco, Department of Biomedical Sciences, University of Padova, via Ugo Bassi 58/B, 35131 Padova, Italy. E-mail: [email protected] https://doi.org/10.1124/pr.116.012658. 200 Biological Actions of Botulinum Neurotoxins 201 V. Conclusions . ..............................................................................228 Acknowledgments . ........................................................................228 References ..................................................................................228 Abstract——The study of botulinum neurotoxins specific market has reached the size of the one dedicated (BoNT) is rapidly progressing in many aspects. Novel to the treatment of medical syndromes. The pharmaco- BoNTs are being discovered owing to next generation logical properties and mode of action of BoNTs have sequencing, but their biologic and pharmacological shed light on general principles of neuronal transport properties remain largely unknown. The molecular and protein-protein interactions and are stimulat- structure of the large protein complexes that the toxin ingbasicsciencestudies.Moreover,thewidearray forms with accessory proteins, which are included in of BoNTs discovered and to be discovered and some BoNT type A1 and B1 pharmacological prepara- the production of recombinant BoNTs endowed with tions, have been determined. By far the largest effort has specific properties suggest novel uses in therapeutics been dedicated to the testing and validation of BoNTs as with increasing disease/symptom specifity. These recent therapeutic agents in an ever increasing number of developments are reviewed here to provide an updated applications, including pain therapy. BoNT type A1 has picture of the biologic mechanism of action of BoNTs, of been also exploited in a variety of cosmetic treatments, their increasing use in pharmacology and in cosmetics, alone or in combination with other agents, and this and of their toxicology. I. Introduction and autonomic nervous systems. Such paralysis becomes evident first at the level of ocular muscles and then Botulinum neurotoxins (BoNTs) are protein neuro- toxins produced by neurotoxigenic strains of anaerobic extends to the facial ones to reach respiratory muscles, and spore forming bacteria of the genus Clostridium causing respiratory failure. However, if the patient is (Clostridium botulinum, Clostridium butyrricum, Clos- mechanically ventilated and appropriately supported in tridium barati, and Clostridium argentinensis) (Smith an emergency room, usually recovery is complete, et al., 2015). However, an open reading frame similar to although it may take several months (Cherington, the bont genes was identified within the genome of 1998; Johnson and Montecucco, 2008). Weissella oryzae, a bacterium that shares some biologic The BoNTs have been traditionally classified into niches with Clostridia (Mansfield et al., 2015). This seven serotypes distinguishable with animal antisera BoNT-like is indeed a metalloprotease that cleaves and designated with alphabetical letters from A to G vesicle-associated membrane protein (VAMP) like tetanus (Smith et al., 2015). However, more recent molecular neurotoxin (TeNT) and several BoNTs do, but is serolog- genetic analysis, including the use of next generation ically different (Zornetta et al., 2016). The BoNTs cause sequencing techniques, have led to the discovery of the flaccid paralysis of botulism by inhibiting neurotrans- genes encoding for many novel BoNTs. They can be mitter release mainly at peripheral cholinergic nerve grouped within an existing serotype but are character- terminals of the skeletal and autonomic nervous system ized by different amino acid sequences (Gene Bank and (Burgen et al., 1949; Van der Kloot and Molgo, 1994; Uniprot databases). Although most, but not all, the Poulain et al., 1995; Rossetto et al., 2014). Botulism is a known antigenic properties of these variants are con- disease of vertebrate animals, including humans, where served, they have been dubbed as subtypes and in- presently, it is relatively rare owing to the improved dicated with the letter of the serotype followed by a techniques of food preparation that prevent the growth of number (Rossetto et al., 2014; Montecucco and Rasotto, anaerobes (Peck, 2006; Peck et al., 2011). BoNTs bind with 2015; Smith et al., 2015). For example, for serotype A: high affinity to peripheral cholinergic nerve terminals and … enter into their cytosol where they cleave SNARE proteins BoNT/A1, BoNT/A2 BoNT/An; for serotype B: BoNT/B1, … thus blocking the release of neurotransmitters (Rossetto BoNT/B2 BoNT/Bn, etc. In addition, some chimeric BoNTs et al., 2014; Rummel, 2015). were identified and labeled accordingly: BoNT/DC, There are different forms of botulism related to the BoNT/CD, BoNT/FA. These chimeric neurotoxins are the route of entry of the toxin into the body (intestine, result of past recombination events within the bont genes. anaerobic wounds, respiratory tract, intramuscular in- The biologic significance of such a large and growing jection of excessive doses) but, in any case, the key number of
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