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Published in: Journal of Neural Transmission 12/2016

01-12-2016 | Neurology and Preclinical Neurological Studies - Review Article

Botulinum toxin type A in motor nervous system: unexplained observations and new challenges

Authors: I. Matak, Z. Lacković, M. Relja

Published in: Journal of Neural Transmission | Issue 12/2016

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Abstract

In the motor system, botulinum toxin type A (BoNT/A) actions were classically attributed to its well-known peripheral anticholinergic actions in neuromuscular junctions. However, the enzymatic activity of BoNT/A, assessed by the detection of cleaved synaptosomal-associated protein 25 (SNAP-25), was recently detected in motor and sensory regions of the brainstem and spinal cord after toxin peripheral injection in rodents. In sensory regions, the function of BoNT/A activity is associated with its antinociceptive effects, while in motor regions we only know that BoNT/A activity is present. Is it possible that BoNT/A presence in central motor nuclei is without any function? In this brief review, we analyze this question. Limited data available in the literature warrant further investigations of BoNT/A actions in motor nervous system.
Literature
go back to reference Aymard C, Mazzocchio R, Marchand-Pauvert V (2013) Central effects of botulinum toxin A: depression of spinal recurrent inhibition after injection of calf muscles in stroke patients. Ann Phys Rehab Med 56(S1):e396–e397. doi:10.1016/j.rehab.2013.07.1016 CrossRef Aymard C, Mazzocchio R, Marchand-Pauvert V (2013) Central effects of botulinum toxin A: depression of spinal recurrent inhibition after injection of calf muscles in stroke patients. Ann Phys Rehab Med 56(S1):e396–e397. doi:10.​1016/​j.​rehab.​2013.​07.​1016 CrossRef
go back to reference Black J, Dolly O (1986) Interaction of 125I-labeled botulinum neurotoxins with nerve terminals. I. Ultrastructural autoradiographic localization and quantitation of distinct membrane acceptors for types A and B on motor nerves. J Cell Biol 103:521–534CrossRefPubMed Black J, Dolly O (1986) Interaction of 125I-labeled botulinum neurotoxins with nerve terminals. I. Ultrastructural autoradiographic localization and quantitation of distinct membrane acceptors for types A and B on motor nerves. J Cell Biol 103:521–534CrossRefPubMed
go back to reference Blasi J, Chapman ER, Link E, Binz T, Yamasaki S, De Camilli P, Südhof TC, Niemann H, Jahn R (1993) Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 365:160–163CrossRefPubMed Blasi J, Chapman ER, Link E, Binz T, Yamasaki S, De Camilli P, Südhof TC, Niemann H, Jahn R (1993) Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 365:160–163CrossRefPubMed
go back to reference Caron G, Marqueste T, Decherchi P (2015) Long-term effects of botulinum toxin complex type A injection on mechano- and metabo-sensitive afferent fibers originating from gastrocnemius muscle. PLoS ONE 10:e0140439CrossRefPubMedPubMedCentral Caron G, Marqueste T, Decherchi P (2015) Long-term effects of botulinum toxin complex type A injection on mechano- and metabo-sensitive afferent fibers originating from gastrocnemius muscle. PLoS ONE 10:e0140439CrossRefPubMedPubMedCentral
go back to reference Cullheim S, Kellerth JO (1978) A morphological study of the axons and recurrent axon collaterals of cat alpha-motoneurones supplying different hind-limb muscles. J Physiol 281:285–299CrossRefPubMedPubMedCentral Cullheim S, Kellerth JO (1978) A morphological study of the axons and recurrent axon collaterals of cat alpha-motoneurones supplying different hind-limb muscles. J Physiol 281:285–299CrossRefPubMedPubMedCentral
go back to reference Currà A, Trompetto C, Abbruzzese G, Berardelli A (2004) Central effects of botulinum toxin type A: evidence and supposition. Mov Disord 19(Suppl 8):S60–S64CrossRefPubMed Currà A, Trompetto C, Abbruzzese G, Berardelli A (2004) Central effects of botulinum toxin type A: evidence and supposition. Mov Disord 19(Suppl 8):S60–S64CrossRefPubMed
go back to reference Drinovac Vlah V, Bach-Rojecky L, Lacković Z (2016) Antinociceptive action of botulinum toxin type A in carrageenan-induced mirror pain. J Neural Transm (Vienna). doi:10.1007/s00702-016-1605-7 Drinovac Vlah V, Bach-Rojecky L, Lacković Z (2016) Antinociceptive action of botulinum toxin type A in carrageenan-induced mirror pain. J Neural Transm (Vienna). doi:10.​1007/​s00702-016-1605-7
go back to reference Filippi GM, Errico P, Santarelli R, Bagolini B, Manni E (1993) Botulinum A toxin effects on rat jaw muscle spindles. Acta Otolaryngol 113:400–404CrossRefPubMed Filippi GM, Errico P, Santarelli R, Bagolini B, Manni E (1993) Botulinum A toxin effects on rat jaw muscle spindles. Acta Otolaryngol 113:400–404CrossRefPubMed
go back to reference Habermann E (1974) 125I-labeled neurotoxin from Clostridium botulinum A: preparation, binding to synaptosomes and ascent to the spinal cord. Naunyn Schmiedebergs Arch Pharmacol 281:47–56CrossRefPubMed Habermann E (1974) 125I-labeled neurotoxin from Clostridium botulinum A: preparation, binding to synaptosomes and ascent to the spinal cord. Naunyn Schmiedebergs Arch Pharmacol 281:47–56CrossRefPubMed
go back to reference Hubbard K, Beske P, Lyman M, McNutt P (2015) Functional evaluation of biological neurotoxins in networked cultures of stem cell-derived central nervous system neurons. J Vis Exp. doi:10.3791/52361 PubMedPubMedCentral Hubbard K, Beske P, Lyman M, McNutt P (2015) Functional evaluation of biological neurotoxins in networked cultures of stem cell-derived central nervous system neurons. J Vis Exp. doi:10.​3791/​52361 PubMedPubMedCentral
go back to reference Jung HH, Lauterburg T, Burgunder JM (1997) Expression of neurotransmitter genes in rat spinal motoneurons after chemodenervation with botulinum toxin. Neuroscience 78:469–479CrossRefPubMed Jung HH, Lauterburg T, Burgunder JM (1997) Expression of neurotransmitter genes in rat spinal motoneurons after chemodenervation with botulinum toxin. Neuroscience 78:469–479CrossRefPubMed
go back to reference Lacković Z, Filipović B, Matak I, Helyes Z (2016) Activity of botulinum toxin type A in cranial dura: implications for treatment of migraine and other headaches. Br J Pharmacol 173:279–291. doi:10.1111/bph.13366. CrossRefPubMed Lacković Z, Filipović B, Matak I, Helyes Z (2016) Activity of botulinum toxin type A in cranial dura: implications for treatment of migraine and other headaches. Br J Pharmacol 173:279–291. doi:10.​1111/​bph.​13366.​ CrossRefPubMed
go back to reference Luvisetto S, Gazerani P, Cianchetti C, Pavone F (2015) Botulinum toxin type A as a therapeutic agent against headache and related disorders. Toxins (Basel) 7:3818–3844. doi:10.3390/toxins7093818 CrossRef Luvisetto S, Gazerani P, Cianchetti C, Pavone F (2015) Botulinum toxin type A as a therapeutic agent against headache and related disorders. Toxins (Basel) 7:3818–3844. doi:10.​3390/​toxins7093818 CrossRef
go back to reference Mariotti R, Bentivoglio M (1996) Botulinum toxin induces nitric oxide synthase activity in motoneurons. Neurosci Lett 219:25–28CrossRefPubMed Mariotti R, Bentivoglio M (1996) Botulinum toxin induces nitric oxide synthase activity in motoneurons. Neurosci Lett 219:25–28CrossRefPubMed
go back to reference Mika J, Rojewska E, Makuch W, Korostynski M, Luvisetto S, Marinelli S, Pavone F, Przewlocka B (2011) The effect of botulinum neurotoxin A on sciatic nerve injury-induced neuroimmunological changes in rat dorsal root ganglia and spinal cord. Neuroscience 175:358–366. doi:10.1016/j.neuroscience.2010.11.040 CrossRefPubMed Mika J, Rojewska E, Makuch W, Korostynski M, Luvisetto S, Marinelli S, Pavone F, Przewlocka B (2011) The effect of botulinum neurotoxin A on sciatic nerve injury-induced neuroimmunological changes in rat dorsal root ganglia and spinal cord. Neuroscience 175:358–366. doi:10.​1016/​j.​neuroscience.​2010.​11.​040 CrossRefPubMed
go back to reference Moreno-López B, de la Cruz RR, Pastor AM, Delgado-García JM (1997) Effects of botulinum neurotoxin type A on abducens motoneurons in the cat: alterations of the discharge pattern. Neuroscience 81:437–455CrossRefPubMed Moreno-López B, de la Cruz RR, Pastor AM, Delgado-García JM (1997) Effects of botulinum neurotoxin type A on abducens motoneurons in the cat: alterations of the discharge pattern. Neuroscience 81:437–455CrossRefPubMed
go back to reference Pastor AM, Moreno-López B, De La Cruz RR, Delgado-García JM (1997) Effects of botulinum neurotoxin type A on abducens motoneurons in the cat: ultrastructural and synaptic alterations. Neuroscience 81:457–478CrossRefPubMed Pastor AM, Moreno-López B, De La Cruz RR, Delgado-García JM (1997) Effects of botulinum neurotoxin type A on abducens motoneurons in the cat: ultrastructural and synaptic alterations. Neuroscience 81:457–478CrossRefPubMed
go back to reference Rosales RL, Arimura K, Takenaga S, Osame M (1996) Extrafusal and intrafusal muscle effects in experimental botulinum toxin-A injection. Muscle Nerve 19:488–496CrossRefPubMed Rosales RL, Arimura K, Takenaga S, Osame M (1996) Extrafusal and intrafusal muscle effects in experimental botulinum toxin-A injection. Muscle Nerve 19:488–496CrossRefPubMed
go back to reference Tyler HR (1963) Botulinus toxin: effect on the central nervous system of man. Science 139:847–848CrossRefPubMed Tyler HR (1963) Botulinus toxin: effect on the central nervous system of man. Science 139:847–848CrossRefPubMed
go back to reference Wang T, Martin S, Papadopulos A, Harper CB, Mavlyutov TA, Niranjan D, Glass NR, Cooper-White JJ, Sibarita JB, Choquet D, Davletov B, Meunier FA (2015) Control of autophagosome axonal retrograde flux by presynaptic activity unveiled using botulinum neurotoxin type A. J Neurosci 35:6179–6194. doi:10.1523/JNEUROSCI.3757-14.2015 CrossRefPubMedPubMedCentral Wang T, Martin S, Papadopulos A, Harper CB, Mavlyutov TA, Niranjan D, Glass NR, Cooper-White JJ, Sibarita JB, Choquet D, Davletov B, Meunier FA (2015) Control of autophagosome axonal retrograde flux by presynaptic activity unveiled using botulinum neurotoxin type A. J Neurosci 35:6179–6194. doi:10.​1523/​JNEUROSCI.​3757-14.​2015 CrossRefPubMedPubMedCentral
go back to reference Wiegand H, Erdmann G, Wellhoner HH (1976) 125I-labelled botulinum A neurotoxin: pharmacokinetics in cats after intramuscular injection. Naunyn Schmiedebergs Arch Pharmacol 292:161–165CrossRefPubMed Wiegand H, Erdmann G, Wellhoner HH (1976) 125I-labelled botulinum A neurotoxin: pharmacokinetics in cats after intramuscular injection. Naunyn Schmiedebergs Arch Pharmacol 292:161–165CrossRefPubMed
go back to reference Wohlfarth K, Schubert M, Rothe B, Elek J, Dengler R (2001) Remote F-wave changes after local botulinum toxin application. Clin Neurophysiol 112:636–640CrossRefPubMed Wohlfarth K, Schubert M, Rothe B, Elek J, Dengler R (2001) Remote F-wave changes after local botulinum toxin application. Clin Neurophysiol 112:636–640CrossRefPubMed
go back to reference Zhang X, Verge VM, Wiesenfeld-Hallin Z, Piehl F, Hökfelt T (1993) Expression of neuropeptides and neuropeptide mRNAs in spinal cord after axotomy in the rat, with special reference to motoneurons and galanin. Exp Brain Res 93:450–461CrossRefPubMed Zhang X, Verge VM, Wiesenfeld-Hallin Z, Piehl F, Hökfelt T (1993) Expression of neuropeptides and neuropeptide mRNAs in spinal cord after axotomy in the rat, with special reference to motoneurons and galanin. Exp Brain Res 93:450–461CrossRefPubMed
Metadata
Title
Botulinum toxin type A in motor nervous system: unexplained observations and new challenges
Authors
I. Matak
Z. Lacković
M. Relja
Publication date
01-12-2016
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 12/2016
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-016-1611-9

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Antinociceptive action of botulinum toxin type A in carrageenan-induced mirror pain