Emerging opportunities for serotypes of botulinum neurotoxins

Toxins

Volumn 4, Issue 11, 2012, Pages 1196-1222

  Chen, Zhongxing Peng ^a,b,c   Glenn Morris, J ^a   Rodriguez, Ramon L ^a   Shukla, Aparna Wagle ^a   Tapia Núñez, John ^b   Okun, Michael S ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b ATIX Foundation   (Chile)

^c University for Development   (Chile)

Author keywords

Botulinum toxin serotypes; Neuro pharmacology toxins; Neurotoxins subtypes

Indexed keywords

BOTULINUM ANTISERUM; BOTULINUM TOXIN; BOTULINUM TOXIN A; BOTULINUM TOXIN B; BOTULINUM TOXIN C; BOTULINUM TOXIN D; BOTULINUM TOXIN E; BOTULINUM TOXIN F; BOTULINUM TOXIN G; PLACEBO; SNARE PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; AUTONOMIC NEUROPATHY; BACTERIAL GENOME; BACTERIAL METABOLISM; BLEPHAROSPASM; BLURRED VISION; BOTULISM; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CERVICAL DYSTONIA; CLOSTRIDIUM BOTULINUM; DRUG APPROVAL; DRUG FORMULATION; DRUG INDICATION; DRUG SAFETY; DYSPHAGIA; FACIAL NERVE DISEASE; FOCAL HAND DYSTONIA; FOOD AND DRUG ADMINISTRATION; FOOD CONTAMINATION; GOLD STANDARD; HEAD TREMOR; HEMATOMA; HUMAN; HYPERHIDROSIS; HYPERKINESIA; IMMUNOGENICITY; INJECTION SITE HEMATOMA; INJECTION SITE INFECTION; INJECTION SITE PAIN; INJECTION SITE REACTION; INTERNALIZATION; INTRACELLULAR TRANSPORT; LETHAL DOSE; MIGRAINE; MUSCLE WEAKNESS; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; OVERACTIVE BLADDER; PARALYSIS; PATHOPHYSIOLOGY; PHYSICAL CHEMISTRY; PROTEIN DEGRADATION; PTOSIS; RESPIRATORY TRACT DISEASE; REVIEW; RISK BENEFIT ANALYSIS; SEROTYPE; SPASTICITY; STRABISMUS BLEPHAROSPASM; TENSION HEADACHE; TOXICOKINETICS; TOXIN ANALYSIS; TOXIN STRUCTURE; TREMOR; XEROSTOMIA;

EID: 84870570364     PISSN: 20726651     EISSN: None     Source Type: Journal    
DOI: 10.3390/toxins4111196     Document Type: Review

References (130)

1. Jankovic, J. Disease-oriented approach to botulinum toxin use. Toxicon 2009, 54, 614-623.
2. Olesen, J.; Tfelt-Hansen, P. Licence for Botox in so-called chronic migraine. Lancet 2010, 376, 1825-1826; discussion 1826.
3. FDA approves Botox to treat specific form of urinary incontinence. Available online: http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm269509.htm?utm_campai gn=Google2&utm_source=fdaSearch&utm_medium=website&utm_term=BOTOX&utm_conten t=10 (accessed on 24 October 2011).
4. Hasler, W.L. The expanding spectrum of clinical uses for botulinum toxin: Healing of chronic anal fissures. Gastroenterology 1999, 116, 221-223.
5. Dykstra, D.D.; Sidi, A.A. Treatment of detrusor-sphincter dyssynergia with botulinum A toxin: A double-blind study. Arch. Phys. Med. Rehabil. 1990, 71, 24-26.
6. Snow, B.J.; Tsui, J.K.; Bhatt, M.H.; Varelas, M.; Hashimoto, S.A.; Calne, D.B. Treatment of spasticity with botulinum toxin: a double-blind study. Ann. Neurol. 1990, 28, 512-515.
7. Das, T.K.; Park, D.M. Effect of treatment with botulinum toxin on spasticity. Postgrad. Med. J. 1989, 65, 208-210.
8. Rollnik, J.D.; Tanneberger, O.; Schubert, M.; Schneider, U.; Dengler, R. Treatment of tension-type headache with botulinum toxin type A: A double-blind, placebo-controlled study. Headache 2000, 40, 300-305.
9. Carruthers, A.; Carruthers, J. Botulinum toxin products overview. Skin Ther. Lett. 2008, 13, 1-4.
10. Erbguth, F.J. Historical notes on botulism, Clostridium botulinum, botulinum toxin, and the idea of the therapeutic use of the toxin. Mov. Disord. 2004, 19, S2-S6.
11. Horowitz, B.Z. Type E botulism. Clin. Toxicol. (Phila) 2010, 48, 880-895.
12. Shapiro, R.L.; Hatheway, C.; Swerdlow, D.L. Botulism in the United States: A clinical and epidemiologic review. Ann. Intern. Med. 1998, 129, 221-228.
13. Hambleton, P. Clostridium botulinum toxins: A general review of involvement in disease, structure, mode of action and preparation for clinical use. J. Neurol. 1992, 239, 16-20.
14. Morris, J.G., Jr.; Hatheway, C.L. Botulism. In Infectious Diseases, 3rd ed.; Hoeprich, P.D., Eds. Harper & Row: Philadelphia, PA, USA, 1983.
15. Botulism-Information from the World Health Organization. J. Environ. Health. 2003, 65, 51-52.
16. Dressler, D.; Adib Saberi, F. Botulinum toxin: Mechanisms of action. Eur. Neurol. 2005, 53, 3-9.
17. Schiavo, G.; Matteoli, M.; Montecucco, C. Neurotoxins affecting neuroexocytosis. Physiol. Rev. 2000, 80, 717-766.
18. Minton, N.P. Molecular genetics of clostridial neurotoxins. Curr. Top Microbiol. Immunol. 1995, 195, 161-194.
19. Swaminathan, S.; Eswaramoorthy, S. Structural analysis of the catalytic and binding sites of Clostridium botulinum neurotoxin B. Nat. Struct. Biol. 2000, 7, 693-699.
20. Eswaramoorthy, S.; Kumaran, D.; Keller, J.; Swaminathan, S. Role of metals in the biological activity of Clostridium botulinum neurotoxins. Biochemistry 2004, 43, 2209-2216.
21. Mushrush, D.J.; Koteiche, H.A.; Sammons, M.A.; Link, A.J.; McHaourab, H.S.; Lacy, D.B. Studies of the mechanistic details of the pH-dependent association of botulinum neurotoxin with membranes. J. Biol. Chem. 2011, 286, 27011-27018.
22. ®: Summary of product characteristics. Merz Pharmaceuticals 2010. Available online: http://www.medicines.org.uk/emc/document.aspx?documentId=20666 (accessed on 10 September 2011).
23. Marvaud, J.C.; Eisel, U.; Binz, T.; Niemann, H.; Popoff, M.R. TetR is a positive regulator of the tetanus toxin gene in Clostridium tetani and is homologous to botR. Infect. Immun. 1998, 66, 5698-5702.
24. Johnson, E.A.; Bradshaw, M. Clostridium botulinum and its neurotoxins: A metabolic and cellular perspective. Toxicon 2001, 39, 1703-1722.
25. Schantz, E.J.; Johnson, E.A. Properties and use of botulinum toxin and other microbial neurotoxins in medicine. Microbiol. Rev. 1992, 56, 80-99.
26. Sakaguchi, G. Clostridium botulinum toxins. Pharmacol. Ther. 1982, 19, 165-194.
27. Chen, F.; Kuziemko, G.M.; Stevens, R.C. Biophysical characterization of the stability of the 150-kilodalton botulinum toxin, the nontoxic component, and the 900-kilodalton botulinum toxin complex species. Infect. Immun. 1998, 66, 2420-2425.
28. Grein, S.; Mander, G.J.; Taylor, H.V. XEOMIN is stable without refrigeration: Complexing proteins are not required for stability of botulinum neurotoxin type A preparations. Toxicon 2008, 51, 13.
29. Hill, K.K.; Smith, T.J.; Helma, C.H.; Ticknor, L.O.; Foley, B.T.; Svensson, R.T.; Brown, J.L.; Johnson, E.A.; Smith, L.A.; Okinaka, R.T.; et al. Genetic diversity among Botulinum Neurotoxin-producing clostridial strains. J. Bacteriol. 2007, 189, 818-832.
30. Skarin, H.; Hafstrom, T.; Westerberg, J.; Segerman, B. Clostridium botulinum group III: A group with dual identity shaped by plasmids, phages and mobile elements. BMC Genomics 2011, 12, 185.
31. Collins, M.D.; East, A.K. Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins. J. Appl. Microbiol. 1998, 84, 5-17.
32. Shukla, H.D.; Sharma, S.K. Clostridium botulinum: A bug with beauty and weapon. Crit. Rev. Microbiol. 2005, 31, 11-18.
33. Lindstrom, M.; Keto, R.; Markkula, A.; Nevas, M.; Hielm, S.; Korkeala, H. Multiplex PCR assay for detection and identification of Clostridium botulinum types A, B, E, and F in food and fecal material. Appl. Environ. Microbiol. 2001, 67, 5694-5699.
34. Montecucco, C.; Schiavo, G.; Dasgupta, B.R. Effect of pH on the interaction of botulinum neurotoxins A, B and E with liposomes. Biochem. J. 1989, 259, 47-53.
35. Jacobson, M.J.; Lin, G.; Tepp, W.; Dupuy, J.; Stenmark, P.; Stevens, R.C.; Johnson, E.A. Purification, modeling, and analysis of botulinum neurotoxin subtype A5 (BoNT/A5) from Clostridium botulinum strain A661222. Appl. Environ. Microbiol. 2011, 77, 4217-4222.
36. Umeda, K.; Seto, Y.; Kohda, T.; Mukamoto, M.; Kozaki, S. Genetic characterization of Clostridium botulinum associated with type B infant botulism in Japan. J. Clin. Microbiol. 2009, 47, 2720-2728.
37. Henkel, J.S.; Jacobson, M.; Tepp, W.; Pier, C.; Johnson, E.A.; Barbieri, J.T. Catalytic properties of botulinum neurotoxin subtypes A3 and A4. Biochemistry 2009, 48, 2522-2528.
38. Pier, C.L.; Chen, C.; Tepp, W.H.; Lin, G.; Janda, K.D.; Barbieri, J.T.; Pellett, S.; Johnson, E.A. Botulinum neurotoxin subtype A2 enters neuronal cells faster than subtype A1. FEBS Lett. 2011, 585, 199-206.
39. Chen, Y.; Korkeala, H.; Aarnikunnas, J.; Lindstrom, M. Sequencing the botulinum neurotoxin gene and related genes in Clostridium botulinum type E strains reveals orfx3 and a novel type E neurotoxin subtype. J. Bacteriol. 2007, 189, 8643-8650.
40. Kubota, T.; Watanabe, T.; Yokosawa, N.; Tsuzuki, K.; Indoh, T.; Moriishi, K.; Sanda, K.; Maki, Y.; Inoue, K.; Fujii, N. Epitope regions in the heavy chain of Clostridium botulinum type E neurotoxin recognized by monoclonal antibodies. Appl. Environ. Microbiol. 1997, 63, 1214-1218.
41. Lacy, D.B.; Stevens, R.C. Sequence homology and structural analysis of the clostridial neurotoxins. J. Mol. Biol. 1999, 291, 1091-1104.
42. Smith, T.J.; Lou, J.; Geren, I.N.; Forsyth, C.M.; Tsai, R.; Laporte, S.L.; Tepp, W.H.; Bradshaw, M.; Johnson, E.A.; Smith, L.A.; et al. Sequence variation within botulinum neurotoxin serotypes impacts antibody binding and neutralization. Infect. Immun. 2005, 73, 5450-5457.
43. Sesardic, D.; Das, R.E.; Corbel, M.J. Botulinum toxin. J. R. Soc. Med. 1994, 87, 307.
44. McLellan, K.; Das, R.E.; Ekong, T.A.; Sesardic, D. Therapeutic botulinum type A toxin: Factors affecting potency. Toxicon 1996, 34, 975-985.
45. Sesardic, D.; Jones, R.G.; Leung, T.; Alsop, T.; Tierney, R. Detection of antibodies against botulinum toxins. Mov. Disord. 2004, 19, S85-S91.
46. Sesardic, D.; McLellan, K.; Ekong, T.A.; Das, R.G. Refinement and validation of an alternative bioassay for potency testing of therapeutic botulinum type A toxin. Pharmacol. Toxicol. 1996, 78, 283-288.
47. Golan, D.E. Principles of Autonomic and Pheripheral Nervous System Pharmacology. In Principles of Pharmacology; The Physiopathology of Drugs, 2nd ed.; Wilkins, L.W., Ed.; Lippincott Williams: Philadelphia, PA, USA, 2008; pp. 107-125.
48. Verderio, C.; Rossetto, O.; Grumelli, C.; Frassoni, C.; Montecucco, C.; Matteoli, M. Entering neurons: Botulinum toxins and synaptic vesicle recycling. EMBO Rep. 2006, 7, 995-999.
49. Dong, M.; Liu, H.; Tepp, W.H.; Johnson, E.A.; Janz, R.; Chapman, E.R. Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin E into neurons. Mol. Biol. Cell 2008, 19, 5226-5237.
50. Dolly, J.O.; Lawrence, G.W.; Meng, J.; Wang, J.; Ovsepian, S.V. Neuro-exocytosis: botulinum toxins as inhibitory probes and versatile therapeutics. Curr. Opin. Pharmacol. 2009, 9, 326-335.
51. Li, G.; Rungger-Brandle, E.; Just, I.; Jonas, J.C.; Aktories, K.; Wollheim, C.B. Effect of disruption of actin filaments by Clostridium botulinum C2 toxin on insulin secretion in HIT-T15 cells and pancreatic islets. Mol. Biol. Cell 1994, 5, 1199-1213.
52. Marqueze, B.; Boudier, J.A.; Mizuta, M.; Inagaki, N.; Seino, S.; Seagar, M. Cellular localization of synaptotagmin I, II, and III mRNAs in the central nervous system and pituitary and adrenal glands of the rat. J. Neurosci. 1995, 15, 4906-4917.
53. Geppert, M.; Archer, B.T., III; Sudhof, T.C. Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J. Biol. Chem. 1991, 266, 13548-13552.
54. Dong, M.; Yeh, F.; Tepp, W.H.; Dean, C.; Johnson, E.A.; Janz, R.; Chapman, E.R. SV2 is the protein receptor for botulinum neurotoxin A. Science 2006, 312, 592-596.
55. Mahrhold, S.; Rummel, A.; Bigalke, H.; Davletov, B.; Binz, T. The synaptic vesicle protein 2C mediates the uptake of botulinum neurotoxin A into phrenic nerves. FEBS Lett. 2006, 580, 2011-2014.
56. Dong, M.; Richards, D.A.; Goodnough, M.C.; Tepp, W.H.; Johnson, E.A.; Chapman, E.R. Synaptotagmins I and II mediate entry of botulinum neurotoxin B into cells. J. Cell Biol. 2003, 162, 1293-1303.
57. Nishiki, T.; Tokuyama, Y.; Kamata, Y.; Nemoto, Y.; Yoshida, A.; Sato, K.; Sekiguchi, M.; Takahashi, M.; Kozaki, S. The high-affinity binding of Clostridium botulinum type B neurotoxin to synaptotagmin II associated with gangliosides GT1b/GD1a. FEBS Lett. 1996, 378, 253-257.
58. Tsukamoto, K.; Kohda, T.; Mukamoto, M.; Takeuchi, K.; Ihara, H.; Saito, M.; Kozaki, S. Binding of Clostridium botulinum type C and D neurotoxins to ganglioside and phospholipid. Novel insights into the receptor for clostridial neurotoxins. J. Biol. Chem. 2005, 280, 35164-35171.
59. Peng, L.; Tepp, W.H.; Johnson, E.A.; Dong, M. Botulinum neurotoxin D uses synaptic vesicle protein SV2 and gangliosides as receptors. PLoS Pathog. 2011, 7, e1002008.
60. Rummel, A.; Hafner, K.; Mahrhold, S.; Darashchonak, N.; Holt, M.; Jahn, R.; Beermann, S.; Karnath, T.; Bigalke, H.; Binz, T. Botulinum neurotoxins C, E and F bind gangliosides via a conserved binding site prior to stimulation-dependent uptake with botulinum neurotoxin F utilising the three isoforms of SV2 as second receptor. J. Neurochem. 2009, 110, 1942-1954.
61. 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 2009, 48, 5631-5641.
62. Rummel, A.; Karnath, T.; Henke, T.; Bigalke, H.; Binz, T. Synaptotagmins I and II act as nerve cell receptors for botulinum neurotoxin G. J. Biol. Chem. 2004, 279, 30865-30870.
63. Schmitt, J.; Karalewitz, A.; Benefield, D.A.; Mushrush, D.J.; Pruitt, R.N.; Spiller, B.W.; Barbieri, J.T.; Lacy, D.B. Structural analysis of botulinum neurotoxin type G receptor binding. Biochemistry 2010, 49, 5200-5205.
64. Hansson, H.A.; Holmgren, J.; Svennerholm, L. Ultrastructural localization of cell membrane GM1 ganglioside by cholera toxin. Proc. Natl. Acad. Sci. USA 1977, 74, 3782-3786.
65. Bullens, R.W.; O'Hanlon, G.M.; Wagner, E.; Molenaar, P.C.; Furukawa, K.; Plomp, J.J.; Willison, H.J. Complex gangliosides at the neuromuscular junction are membrane receptors for autoantibodies and botulinum neurotoxin but redundant for normal synaptic function. J. Neurosci. 2002, 22, 6876-6884.
66. Kitamura, M. Identification of RNA species in the RNA-toxin complex and structure of the complex in Clostridium botulinum type E. Biochem. Biophys. Res. Commun. 2002, 291, 154-157.
67. Yowler, B.C.; Kensinger, R.D.; Schengrund, C.L. Botulinum neurotoxin A activity is dependent upon the presence of specific gangliosides in neuroblastoma cells expressing synaptotagmin I. J. Biol. Chem. 2002, 277, 32815-32819.
68. Keller, J.E.; Cai, F.; Neale, E.A. Uptake of botulinum neurotoxin into cultured neurons. Biochemistry 2004, 43, 526-532.
69. Montecucco, C.; Rossetto, O.; Schiavo, G. Presynaptic receptor arrays for clostridial neurotoxins. Trends Microbiol. 2004, 12, 442-446.
70. Nuemket, N.; Tanaka, Y.; Tsukamoto, K.; Tsuji, T.; Nakamura, K.; Kozaki, S.; Yao, M.; Tanaka, I. Structural and mutational analyses of the receptor binding domain of botulinum D/C mosaic neurotoxin: Insight into the ganglioside binding mechanism. Biochem. Biophys. Res. Commun. 2011, 411, 433-439.
71. Benson, M.A.; Fu, Z.; Kim, J.J.; Baldwin, M.R. Unique ganglioside recognition strategies for clostridial neurotoxins. J. Biol. Chem. 2011, 286, 34015-34022.
72. Chai, Q.; Arndt, J.W.; Dong, M.; Tepp, W.H.; Johnson, E.A.; Chapman, E.R.; Stevens, R.C. Structural basis of cell surface receptor recognition by botulinum neurotoxin B. Nature 2006, 444, 1096-1100.
73. Poea-Guyon, S.; Amar, M.; Fossier, P.; Morel, N. Alternative splicing controls neuronal expression of v-ATPase subunit a1 and sorting to nerve terminals. J. Biol. Chem. 2006, 281, 17164-17172.
74. 2+-dependent exocytosis in PC12 cells. J. Biol. Chem. 1999, 274, 18893-18901.
75. Lafourcade, C.; Sobo, K.; Kieffer-Jaquinod, S.; Garin, J.; van der Goot, F.G. Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS One 2008, 3, e2758.
76. Schiavo, G.; Boquet, P.; Dasgupta, B.R.; Montecucco, C. Membrane interactions of tetanus and botulinum neurotoxins: A photolabelling study with photoactivatable phospholipids. J. Physiol. (Paris) 1990, 84, 180-187.
77. Sun, S.; Suresh, S.; Liu, H.; Tepp, W.H.; Johnson, E.A.; Edwardson, J.M.; Chapman, E.R. Receptor binding enables botulinum neurotoxin B to sense low pH for translocation channel assembly. Cell Host Microbe 2011, 10, 237-247.
78. Montal, M. Botulinum neurotoxin: A marvel of protein design. Annu. Rev. Biochem. 2010, 79, 591-617.
79. Swaminathan, S.; Eswaramoorthy, S. Crystallization and preliminary X-ray analysis of Clostridium botulinum neurotoxin type B. Acta Crystallogr. D Biol. Crystallogr. 2000, 56, 1024-1026.
80. Chen, S.; Barbieri, J.T. Multiple pocket recognition of SNAP25 by botulinum neurotoxin serotype E. J. Biol. Chem. 2007, 282, 25540-25547.
81. Foran, P.G.; Mohammed, N.; Lisk, G.O.; Nagwaney, S.; Lawrence, G.W.; Johnson, E.; Smith, L.; Aoki, K.R.; Dolly, J.O. 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. 2003, 278, 1363-1371.
82. Fernandez-Salas, E.; Ho, H.; Garay, P.; Steward, L.E.; Aoki, K.R. Is the light chain subcellular localization an important factor in botulinum toxin duration of action? Mov. Disord. 2004, 19, S23-S34.
83. Fernandez-Salas, E.; Steward, L.E.; Ho, H.; Garay, P.E.; Sun, S.W.; Gilmore, M.A.; Ordas, J.V.; Wang, J.; Francis, J.; Aoki, K.R. Plasma membrane localization signals in the light chain of botulinum neurotoxin. Proc. Natl. Acad. Sci. USA 2004, 101, 3208-3213.
84. Sharma, S.K.; Whiting, R.C. Methods for detection of Clostridium botulinum toxin in foods. J. Food Protect. 2005, 68, 1256-1263.
85. Metabiologics, I. Mouse Bioassays for Botulinum Toxins and Antibodies. Available online: http://www.metabiologics.com/(accessed on 11 November 2011).
86. Chen, S.; Karalewitz, A.P.; Barbieri, J.T. Insights into the different catalytic activities of Clostridium neurotoxins. Biochemistry 2012, 51, 3941-3947.
87. 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, 233-245.
88. Janz, R.; Südhof, T.C. SV2C is a synaptic vesicle protein with an unusually restricted localization: Anatomy of a synaptic vesicle protein family. Neuroscience 1999, 94, 1279-1290.
89. Dressler, D.; Saberi, F.A.; Barbosa, E.R. Botulinum toxin: Mechanisms of action. Arq. Neuropsiquiatr. 2005, 63, 180-185.
90. Kuehn, B.M. FDA requires black box warnings on labeling for botulinum toxin products. J. Am. Med. Assoc. 2009, 301, 2316.
91. Brashear, A. Clinical comparisons of botulinum neurotoxin formulations. Neurologist 2008, 14, 289-298.
92. Freitag, F.G. Botulinum toxin type A in chronic migraine. Expert Rev. Neurother. 2007, 7, 463-470.
93. Lew, M.F. Botulinum toxin type B (Myobloc, NeuroBloc): A new choice in cervical dystonia. Expert Rev. Neurother. 2001, 1, 143-152.
94. Holzer, S.E.; Ludlow, C.L. The swallowing side effects of botulinum toxin type A injection in spasmodic dysphonia. Laryngoscope 1996, 106, 86-92.
95. Kalra, H.K.; Magoon, E.H. Side effects of the use of botulinum toxin for treatment of benign essential blepharospasm and hemifacial spasm. Ophthalmic. Surg. 1990, 21, 335-338.
96. Price, J.; O'Day, J. Efficacy and side effects of botulinum toxin treatment for blepharospasm and hemifacial spasm. Aust. New Zeal. J. Ophthalmol. 1994, 22, 255-260.
97. Greene, P.; Fahn, S.; Diamond, B. Development of resistance to botulinum toxin type A in patients with torticollis. Mov. Disord. 1994, 9, 213-217.
98. Dressler, D.; Benecke, R. Autonomic side effects of botulinum toxin type B treatment of cervical dystonia and hyperhidrosis. Eur. Neurol. 2003, 49, 34-38.
99. Likhachev, S.A.; Rushkevich Iu, N.; Chernukha, T.N.; Veevnik, E.V. Efficacy and side-effects of the botulinum toxin A treatment in patients with focal dystonia (in Russian). Zh Nevrol Psikhiatr Im S S Korsakova 2009, 109, 27-31.
100. Jankovic, J.; Schwartz, K.S. Clinical correlates of response to botulinum toxin injections. Arch. Neurol. 1991, 48, 1253-1256.
101. Dolimbek, B.Z.; Jankovic, J.; Atassi, M.Z. Cross reaction of tetanus and botulinum neurotoxins A and B and the boosting effect of botulinum neurotoxins A and B on a primary anti-tetanus antibody response. Immunol. Invest. 2002, 31, 247-262.
102. Teixeira-Clerc, F.; Menez, A.; Kessler, P. How do short neurotoxins bind to a muscular-type nicotinic acetylcholine receptor? J. Biol. Chem. 2002, 277, 25741-25747.
103. Truong, D.; Duane, D.D.; Jankovic, J.; Singer, C.; Seeberger, L.C.; Comella, C.L.; Lew, M.F.; Rodnitzky, R.L.; Danisi, F.O.; Sutton, J.P.; et al. Efficacy and safety of botulinum type A toxin (Dysport) in cervical dystonia: Results of the first US randomized, double-blind, placebo-controlled study. Mov. Disord. 2005, 20, 783-791.
104. Frevert, J.; Dressler, D. Complexing proteins in botulinum toxin type A drugs: A help or a hindrance? Biologics 2010, 4, 325-332.
105. Atassi, M.Z.; Jankovic, J.; Steward, L.E.; Aoki, K.R.; Dolimbek, B.Z. Molecular immune recognition of botulinum neurotoxin B. The light chain regions that bind human blocking antibodies from toxin-treated cervical dystonia patients. Antigenic structure of the entire BoNT/B molecule. Immunobiology 2012, 217, 17-27.
106. Critchfield, J. Considering the immune response to botulinum toxin. Clin. J. Pain. 2002, 18, S133-S141.
107. Garcia-Rodriguez, C.; Geren, I.N.; Lou, J.; Conrad, F.; Forsyth, C.; Wen, W.; Chakraborti, S.; Zao, H.; Manzanarez, G.; Smith, T.J.; et al. Neutralizing human monoclonal antibodies binding multiple serotypes of botulinum neurotoxin. Protein Eng. Des. Sel. 2011, 24, 321-331.
108. Sankhla, C.; Jankovic, J.; Duane, D. Variability of the immunologic and clinical response in dystonic patients immunoresistant to botulinum toxin injections. Mov. Disord. 1998, 13, 150-154.
109. Jankovic, J.; Vuong, K.D.; Ahsan, J. Comparison of efficacy and immunogenicity of original versus current botulinum toxin in cervical dystonia. Neurology 2003, 60, 1186-1188.
110. Dressler, D.; Hallett, M. Immunological aspects of Botox, Dysport and Myobloc/NeuroBloc. Eur. J. Neurol. 2006, 13, 11-15.
111. Blumel, J.; Frever, J.; Schwaier, A. Comparative antigenicity of three preparations of botulinum neurotoxin type A in the rabbit. Neurotox. Res. 2006, 9, 238.
112. Kanovsky, P.; Bares, M.; Severa, S.; Richardson, A. Long-term efficacy and tolerability of 4-monthly versus yearly botulinum toxin type A treatment for lower-limb spasticity in children with cerebral palsy. Dev. Med. Child Neurol. 2009, 51, 436-445.
113. Flynn, D.D.; Ferrari-DiLeo, G.; Mash, D.C.; Levey, A.I. Differential regulation of molecular subtypes of muscarinic receptors in Alzheimer's disease. J. Neurochem. 1995, 64, 1888-1891.
114. Mrzljak, L.; Levey, A.I.; Goldman-Rakic, P.S. Association of m1 and m2 muscarinic receptor proteins with asymmetric synapses in the primate cerebral cortex: Morphological evidence for cholinergic modulation of excitatory neurotransmission. Proc. Natl. Acad. Sci. USA 1993, 90, 5194-5198.
115. Weiner, D.M.; Levey, A.I.; Brann, M.R. Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc. Natl. Acad. Sci. USA 1990, 87, 7050-7054.
116. Vilaro, M.T.; Palacios, J.M.; Mengod, G. Localization of m5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry. Neurosci. Lett. 1990, 114, 154-159.
117. Scarr, E. Muscarinic Receptors: Their Roles in Disorders of the Central Nervous System and Potential as Therapeutic Targets. CNS Neurosci. Ther. 2011, 18, 369-379.
118. Nakamura, K.; Kohda, T.; Umeda, K.; Yamamoto, H.; Mukamoto, M.; Kozaki, S. Characterization of the D/C mosaic neurotoxin produced by Clostridium botulinum associated with bovine botulism in Japan. Vet. Microbiol. 2010, 140, 147-154.
119. Antonucci, F.; Bozzi, Y.; Caleo, M. Intrahippocampal infusion of botulinum neurotoxin E (BoNT/E) reduces spontaneous recurrent seizures in a mouse model of mesial temporal lobe epilepsy. Epilepsia 2009, 50, 963-966.
120. Costantin, L.; Bozzi, Y.; Richichi, C.; Viegi, A.; Antonucci, F.; Funicello, M.; Gobbi, M.; Mennini, T.; Rossetto, O.; Montecucco, C.; et al. Antiepileptic effects of botulinum neurotoxin E. J. Neurosci. 2005, 25, 1943-1951.
121. Manno, I.; Antonucci, F.; Caleo, M.; Bozzi, Y. BoNT/E prevents seizure-induced activation of caspase 3 in the rat hippocampus. Neuroreport 2007, 18, 373-376.
122. Antonucci, F.; di Garbo, A.; Novelli, E.; Manno, I.; Sartucci, F.; Bozzi, Y.; Caleo, M. Botulinum neurotoxin E (BoNT/E) reduces CA1 neuron loss and granule cell dispersion, with no effects on chronic seizures, in a mouse model of temporal lobe epilepsy. Exp. Neurol. 2008, 210, 388-401.
123. Hou, Y.P.; Zhang, Y.P.; Song, Y.F.; Zhu, C.M.; Wang, Y.C.; Xie, G.L. Botulinum toxin type A inhibits rat pyloric myoelectrical activity and substance P release in vivo. Can. J. Physiol. Pharmacol. 2007, 85, 209-214.
124. Meng, J.; Wang, J.; Lawrence, G.; Dolly, J.O. Synaptobrevin I mediates exocytosis of CGRP from sensory neurons and inhibition by botulinum toxins reflects their anti-nociceptive potential. J. Cell. Sci. 2007, 120, 2864-2874.
125. Holtje, M.; Hofmann, F.; Lux, R.; Veh, R.W.; Just, I.; Ahnert-Hilger, G. Glutamate uptake and release by astrocytes are enhanced by Clostridium botulinum C3 protein. J. Biol. Chem. 2008, 283, 9289-9299.
126. O'Sullivan, G.A.; Mohammed, N.; Foran, P.G.; Lawrence, G.W.; Oliver Dolly, J. Rescue of exocytosis in botulinum toxin A-poisoned chromaffin cells by expression of cleavage-resistant SNAP-25. Identification of the minimal essential C-terminal residues. J. Biol. Chem. 1999, 274, 36897-36904.
127. Gazerani, P.; Pedersen, N.S.; Staahl, C.; Drewes, A.M.; Arendt-Nielsen, L. Subcutaneous Botulinum toxin type A reduces capsaicin-induced trigeminal pain and vasomotor reactions in human skin. Pain 2009, 141, 60-69.
128. Zuniga, C.; Diaz, S.; Piedimonte, F.; Micheli, F. Beneficial effects of botulinum toxin type A in trigeminal neuralgia. Arq. Neuropsiquiatr. 2008, 66, 500-503.
129. Piovesan, E.J.; Leite Lda, S.; Teive, H.G.; Kowacs, P.A.; Mulinari, R.A.; Radunz, V.; Utiumi, M.; Campos, H.G.; Werneck, L.C. Botulinum toxin type-A effect as a preemptive treatment in a model of acute trigeminal pain: A pre-clinical double-blind and placebo-controlled study. Arq. Neuropsiquiatr. 2011, 69, 56-63.
130. 2+-triggered exocytosis in neurons and endocrine cells demonstrated with an engineered neurotoxin. Biochemistry 2011, 50, 2711-2713.