Botulinum Neurotoxin Chimeras Suppress Stimulation by Capsaicin of Rat Trigeminal Sensory Neurons In Vivo and In Vitro
Abstract
:1. Introduction
2. Results
2.1. Injection of LC/E-BoNT/A into the Right Whisker Pad of Rats Does Not Alter Their Weight Gain, Grooming, Exploratory, or Locomotor Behavior
2.2. LC/E-BoNT/A Causes Long-Lasting Preventative Alleviation of Acute Nocifensive Behavior Induced by Capsaicin in Rats
2.3. LC/E-BoNT/A Equally Diminishes Nocifensive Behavior Evoked by Capsaicin in Both Male and Female Rats
2.4. LC/E-BoNT/A Precludes the Induction of c-Fos Expression in the Trigeminal Nucleus caudalis (TNC) after Capsaicin Injection into the Whisker Pad; a Biochemical Indication of Reduced Nociceptor Activation
2.5. CGRP Release from TGNs Evoked by Strong Stimulation Is Diminished by LC/E-BoNT/A or BoNT/EA, whereas BoNT/A Only Reduces the Response to Lower Capsaicin Concentrations
3. Discussion
4. Conclusions
5. Materials and Methods
5.1. Materials
5.2. Animals
5.3. Drugs and Treatments
5.4. Behavioral Assessments and Capsaicin-Induced Pain-Related Response (Acute Nociception)
5.5. Collection and Fixation of Tissue
5.6. Immuno-Histochemistry
5.7. Isolation and Culturing of Rat Neonate TGNs
5.8. Quantitation of CGRP
5.9. Western Blotting and Quantification of SNAP-25 Cleavage
5.10. Data Analysis and Statistics
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Dolly, J.O.; Meng, J.; Wang, J.; Lawrence, G.W.; Bodeker, M.; Zurawski, T.H.; Sasse, A. Multiple Steps in the Blockade of Exocytosis by Botulinum Neurotoxins. In Botulinum Toxin: Therapeutic Clinical Practice and Science, 1st ed.; Atassi, M.Z., Ed.; Saunders Elsevier: Philadelphia, PA, USA, 2009; pp. 1–14. [Google Scholar]
- Dolly, J.O.; Wang, J.; Zurawski, T.H.; Meng, J. Novel therapeutics based on recombinant botulinum neurotoxins to normalize the release of transmitters and pain mediators. FEBS J. 2011, 278, 4454–4466. [Google Scholar] [CrossRef] [PubMed]
- Sudhof, T.C. The molecular machinery of neurotransmitter release (Nobel lecture). Angew. Chem. Int. Ed. Engl. 2014, 53, 12696–12717. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Dolly, J.O.; Black, J.; Williams, R.S.; Melling, J. Acceptors for botulinum neurotoxin reside on motor nerve terminals and mediate its internalization. Nature 1984, 307, 457–460. [Google Scholar] [CrossRef]
- Black, J.D.; Dolly, J.O. 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. 1986, 103, 521–534. [Google Scholar] [CrossRef]
- Black, J.D.; Dolly, J.O. Interaction of 125I-labeled botulinum neurotoxins with nerve terminals. II. Autoradiographic evidence for its uptake into motor nerves by acceptor-mediated endocytosis. J. Cell Biol. 1986, 103, 535–544. [Google Scholar] [CrossRef] [Green Version]
- Rossetto, O.; Pirazzini, M.; Fabris, F.; Montecucco, C. Botulinum Neurotoxins: Mechanism of Action. Handb. Exp. Pharmacol. 2021, 263, 35–47. [Google Scholar] [CrossRef]
- Ashton, A.C.; Dolly, J.O. Characterization of the inhibitory action of botulinum neurotoxin type A on the release of several transmitters from rat cerebrocortical synaptosomes. J. Neurochem. 1988, 50, 1808–1816. [Google Scholar] [CrossRef]
- McMahon, H.T.; Foran, P.; Dolly, J.O.; Verhage, M.; Wiegant, V.M.; Nicholls, D.G. Tetanus toxin and botulinum toxins type A and B inhibit glutamate, gamma-aminobutyric acid, aspartate, and met-enkephalin release from synaptosomes. Clues to the locus of action. J. Biol. Chem. 1992, 267, 21338–21343. [Google Scholar] [CrossRef]
- Purkiss, J.; Welch, M.; Doward, S.; Foster, K. Capsaicin-stimulated release of substance P from cultured dorsal root ganglion neurons: Involvement of two distinct mechanisms. Biochem. Pharmacol. 2000, 59, 1403–1406. [Google Scholar] [CrossRef]
- Welch, M.J.; Purkiss, J.R.; Foster, K.A. Sensitivity of embryonic rat dorsal root ganglia neurons to Clostridium botulinum neurotoxins. Toxicon 2000, 38, 245–258. [Google Scholar] [CrossRef]
- Durham, P.L.; Cady, R.; Cady, R. Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type A: Implications for migraine therapy. Headache 2004, 44, 35–42, discussion 42–33. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Meng, J.; Ovsepian, S.V.; Wang, J.; Pickering, M.; Sasse, A.; Aoki, K.R.; Lawrence, G.W.; Dolly, J.O. Activation of TRPV1 mediates calcitonin gene-related peptide release, which excites trigeminal sensory neurons and is attenuated by a retargeted botulinum toxin with anti-nociceptive potential. J. Neurosci. 2009, 29, 4981–4992. [Google Scholar] [CrossRef]
- Avona, A.; Mason, B.N.; Lackovic, J.; Wajahat, N.; Motina, M.; Quigley, L.; Burgos-Vega, C.; Moldovan Loomis, C.; Garcia-Martinez, L.F.; Akopian, A.N.; et al. Repetitive stress in mice causes migraine-like behaviors and calcitonin gene-related peptide-dependent hyperalgesic priming to a migraine trigger. Pain 2020, 161, 2539–2550. [Google Scholar] [CrossRef]
- Cui, M.; Khanijou, S.; Rubino, J.; Aoki, K.R. Subcutaneous administration of botulinum toxin A reduces formalin-induced pain. Pain 2004, 107, 125–133. [Google Scholar] [CrossRef]
- Bach-Rojecky, L.; Relja, M.; Lackovic, Z. Botulinum toxin type A in experimental neuropathic pain. J. Neural Transm. (Vienna) 2005, 112, 215–219. [Google Scholar] [CrossRef]
- Park, H.J.; Lee, Y.; Lee, J.; Park, C.; Moon, D.E. The effects of botulinum toxin A on mechanical and cold allodynia in a rat model of neuropathic pain. Can. J. Anaesth. 2006, 53, 470–477. [Google Scholar] [CrossRef] [Green Version]
- Zychowska, M.; Rojewska, E.; Makuch, W.; Luvisetto, S.; Pavone, F.; Marinelli, S.; Przewlocka, B.; Mika, J. Participation of pro- and anti-nociceptive interleukins in botulinum toxin A-induced analgesia in a rat model of neuropathic pain. Eur. J. Pharmacol. 2016, 791, 377–388. [Google Scholar] [CrossRef] [PubMed]
- Xiao, L.; Cheng, J.; Zhuang, Y.; Qu, W.; Muir, J.; Liang, H.; Zhang, D. Botulinum toxin type A reduces hyperalgesia and TRPV1 expression in rats with neuropathic pain. Pain Med. 2013, 14, 276–286. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Filipovic, B.; Matak, I.; Bach-Rojecky, L.; Lackovic, Z. Central action of peripherally applied botulinum toxin type A on pain and dural protein extravasation in rat model of trigeminal neuropathy. PLoS ONE 2012, 7, e29803. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shimizu, T.; Shibata, M.; Toriumi, H.; Iwashita, T.; Funakubo, M.; Sato, H.; Kuroi, T.; Ebine, T.; Koizumi, K.; Suzuki, N. Reduction of TRPV1 expression in the trigeminal system by botulinum neurotoxin type-A. Neurobiol. Dis. 2012, 48, 367–378. [Google Scholar] [CrossRef]
- Caterina, M.J.; Schumacher, M.A.; Tominaga, M.; Rosen, T.A.; Levine, J.D.; Julius, D. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 1997, 389, 816–824. [Google Scholar] [CrossRef]
- Basith, S.; Cui, M.; Hong, S.; Choi, S. Harnessing the Therapeutic Potential of Capsaicin and Its Analogues in Pain and Other Diseases. Molecules 2016, 21, 966. [Google Scholar] [CrossRef] [Green Version]
- Burstein, R.; Blumenfeld, A.M.; Silberstein, S.D.; Manack Adams, A.; Brin, M.F. Mechanism of Action of OnabotulinumtoxinA in Chronic Migraine: A Narrative Review. Headache 2020, 60, 1259–1272. [Google Scholar] [CrossRef]
- Aurora, S.K.; Dodick, D.W.; Turkel, C.C.; DeGryse, R.E.; Silberstein, S.D.; Lipton, R.B.; Diener, H.C.; Brin, M.F.; Group, P.C.M.S. OnabotulinumtoxinA for treatment of chronic migraine: Results from the double-blind, randomized, placebo-controlled phase of the PREEMPT 1 trial. Cephalalgia 2010, 30, 793–803. [Google Scholar] [CrossRef]
- Diener, H.C.; Dodick, D.W.; Aurora, S.K.; Turkel, C.C.; DeGryse, R.E.; Lipton, R.B.; Silberstein, S.D.; Brin, M.F.; Group, P.C.M.S. OnabotulinumtoxinA for treatment of chronic migraine: Results from the double-blind, randomized, placebo-controlled phase of the PREEMPT 2 trial. Cephalalgia 2010, 30, 804–814. [Google Scholar] [CrossRef]
- Dodick, D.W.; Turkel, C.C.; DeGryse, R.E.; Aurora, S.K.; Silberstein, S.D.; Lipton, R.B.; Diener, H.C.; Brin, M.F.; Group, P.C.M.S. OnabotulinumtoxinA for treatment of chronic migraine: Pooled results from the double-blind, randomized, placebo-controlled phases of the PREEMPT clinical program. Headache 2010, 50, 921–936. [Google Scholar] [CrossRef]
- Khalil, M.; Zafar, H.W.; Quarshie, V.; Ahmed, F. Prospective analysis of the use of OnabotulinumtoxinA (BOTOX) in the treatment of chronic migraine; real-life data in 254 patients from Hull, U.K. J. Headache Pain 2014, 15, 54. [Google Scholar] [CrossRef] [PubMed]
- Dominguez, C.; Pozo-Rosich, P.; Torres-Ferrus, M.; Hernandez-Beltran, N.; Jurado-Cobo, C.; Gonzalez-Oria, C.; Santos, S.; Monzon, M.J.; Latorre, G.; Alvaro, L.C.; et al. OnabotulinumtoxinA in chronic migraine: Predictors of response. A prospective multicentre descriptive study. Eur. J. Neurol. 2018, 25, 411–416. [Google Scholar] [CrossRef] [PubMed]
- Cernuda-Morollon, E.; Ramon, C.; Martinez-Camblor, P.; Serrano-Pertierra, E.; Larrosa, D.; Pascual, J. OnabotulinumtoxinA decreases interictal CGRP plasma levels in patients with chronic migraine. Pain 2015, 156, 820–824. [Google Scholar] [CrossRef] [PubMed]
- Lassen, L.H.; Jacobsen, V.B.; Haderslev, P.A.; Sperling, B.; Iversen, H.K.; Olesen, J.; Tfelt-Hansen, P. Involvement of calcitonin gene-related peptide in migraine: Regional cerebral blood flow and blood flow velocity in migraine patients. J. Headache Pain 2008, 9, 151–157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hansen, J.M.; Hauge, A.W.; Olesen, J.; Ashina, M. Calcitonin gene-related peptide triggers migraine-like attacks in patients with migraine with aura. Cephalalgia 2010, 30, 1179–1186. [Google Scholar] [CrossRef] [PubMed]
- Benemei, S.; Dussor, G. TRP Channels and Migraine: Recent Developments and New Therapeutic Opportunities. Pharmaceuticals (Basel) 2019, 12, 54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maraia, Z.; Ricci, D.; Rocchi, M.B.L.; Moretti, A.; Bufarini, C.; Cavaliere, A.; Peverini, M. Real-Life Analysis with Erenumab: First Target Therapy in the Episodic and Chronic Migraine’s Prophylaxis. J. Clin. Med. 2021, 10, 4425. [Google Scholar] [CrossRef]
- Edvinsson, L.; Haanes, K.A.; Warfvinge, K.; Krause, D.N. CGRP as the target of new migraine therapies - successful translation from bench to clinic. Nat. Rev. Neurol. 2018, 14, 338–350. [Google Scholar] [CrossRef]
- Goadsby, P.J.; Holland, P.R.; Martins-Oliveira, M.; Hoffmann, J.; Schankin, C.; Akerman, S. Pathophysiology of Migraine: A Disorder of Sensory Processing. Physiol. Rev. 2017, 97, 553–622. [Google Scholar] [CrossRef]
- Wang, J.; Meng, J.; Lawrence, G.W.; Zurawski, T.H.; Sasse, A.; Bodeker, M.O.; Gilmore, M.A.; Fernandez-Salas, E.; Francis, J.; Steward, L.E.; et al. Novel chimeras of botulinum neurotoxins A and E unveil contributions from the binding, translocation, and protease domains to their functional characteristics. J. Biol. Chem. 2008, 283, 16993–17002. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Casals-Diaz, L.; Zurawski, T.; Meng, J.; Moriarty, O.; Nealon, J.; Edupuganti, O.P.; Dolly, O. A novel therapeutic with two SNAP-25 inactivating proteases shows long-lasting anti-hyperalgesic activity in a rat model of neuropathic pain. Neuropharmacology 2017, 118, 223–232. [Google Scholar] [CrossRef] [PubMed]
- Gambeta, E.; Chichorro, J.G.; Zamponi, G.W. Trigeminal neuralgia: An overview from pathophysiology to pharmacological treatments. Mol. Pain 2020, 16, 1744806920901890. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ossipov, M.H.; Dussor, G.O.; Porreca, F. Central modulation of pain. J. Clin. Investig. 2010, 120, 3779–3787. [Google Scholar] [CrossRef] [Green Version]
- Chichorro, J.G.; Porreca, F.; Sessle, B. Mechanisms of craniofacial pain. Cephalalgia 2017, 37, 613–626. [Google Scholar] [CrossRef] [PubMed]
- Deuis, J.R.; Dvorakova, L.S.; Vetter, I. Methods Used to Evaluate Pain Behaviors in Rodents. Front. Mol. Neurosci. 2017, 10, 284. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Munro, G.; Jansen-Olesen, I.; Olesen, J. Animal models of pain and migraine in drug discovery. Drug Discov. Today 2017, 22, 1103–1111. [Google Scholar] [CrossRef] [PubMed]
- Percie du Sert, N.; Rice, A.S. Improving the translation of analgesic drugs to the clinic: Animal models of neuropathic pain. Br. J. Pharmacol. 2014, 171, 2951–2963. [Google Scholar] [CrossRef] [Green Version]
- Heinz, D.E.; Schottle, V.A.; Nemcova, P.; Binder, F.P.; Ebert, T.; Domschke, K.; Wotjak, C.T. Exploratory drive, fear, and anxiety are dissociable and independent components in foraging mice. Transl. Psychiatry 2021, 11, 318. [Google Scholar] [CrossRef]
- Coe, M.A.; Lofwall, M.R.; Walsh, S.L. Buprenorphine Pharmacology Review: Update on Transmucosal and Long-acting Formulations. J. Addict. Med. 2019, 13, 93–103. [Google Scholar] [CrossRef]
- Vuralli, D.; Wattiez, A.S.; Russo, A.F.; Bolay, H. Behavioral and cognitive animal models in headache research. J. Headache Pain 2019, 20, 11. [Google Scholar] [CrossRef]
- Miyashita, S.I.; Zhang, J.; Zhang, S.; Shoemaker, C.B.; Dong, M. Delivery of single-domain antibodies into neurons using a chimeric toxin-based platform is therapeutic in mouse models of botulism. Sci. Transl. Med. 2021, 13, 13. [Google Scholar] [CrossRef]
- Bach-Rojecky, L.; Lackovic, Z. Antinociceptive effect of botulinum toxin type a in rat model of carrageenan and capsaicin induced pain. Croat. Med. J. 2005, 46, 201–208. [Google Scholar] [PubMed]
- Luvisetto, S.; Vacca, V.; Cianchetti, C. Analgesic effects of botulinum neurotoxin type A in a model of allyl isothiocyanate- and capsaicin-induced pain in mice. Toxicon 2015, 94, 23–28. [Google Scholar] [CrossRef] [PubMed]
- Mogil, J.S. Qualitative sex differences in pain processing: Emerging evidence of a biased literature. Nat. Rev. Neurosci. 2020, 21, 353–365. [Google Scholar] [CrossRef] [PubMed]
- Doyle, H.H.; Eidson, L.N.; Sinkiewicz, D.M.; Murphy, A.Z. Sex Differences in Microglia Activity within the Periaqueductal Gray of the Rat: A Potential Mechanism Driving the Dimorphic Effects of Morphine. J. Neurosci. 2017, 37, 3202–3214. [Google Scholar] [CrossRef] [PubMed]
- Inyang, K.E.; Szabo-Pardi, T.; Wentworth, E.; McDougal, T.A.; Dussor, G.; Burton, M.D.; Price, T.J. The antidiabetic drug metformin prevents and reverses neuropathic pain and spinal cord microglial activation in male but not female mice. Pharmacol. Res. 2019, 139, 1–16. [Google Scholar] [CrossRef]
- Hunt, S.P.; Pini, A.; Evan, G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 1987, 328, 632–634. [Google Scholar] [CrossRef]
- Harriott, A.M.; Strother, L.C.; Vila-Pueyo, M.; Holland, P.R. Animal models of migraine and experimental techniques used to examine trigeminal sensory processing. J. Headache Pain 2019, 20, 91. [Google Scholar] [CrossRef]
- Hegarty, D.M.; Hermes, S.M.; Largent-Milnes, T.M.; Aicher, S.A. Capsaicin-responsive corneal afferents do not contain TRPV1 at their central terminals in trigeminal nucleus caudalis in rats. J. Chem. Neuroanat. 2014, 61–62, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Mangione, A.S.; Obara, I.; Maiaru, M.; Geranton, S.M.; Tassorelli, C.; Ferrari, E.; Leese, C.; Davletov, B.; Hunt, S.P. Nonparalytic botulinum molecules for the control of pain. Pain 2016, 157, 1045–1055. [Google Scholar] [CrossRef] [Green Version]
- Matak, I.; Bach-Rojecky, L.; Filipovic, B.; Lackovic, Z. Behavioral and immunohistochemical evidence for central antinociceptive activity of botulinum toxin A. Neuroscience 2011, 186, 201–207. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matak, I.; Rossetto, O.; Lackovic, Z. Botulinum toxin type A selectivity for certain types of pain is associated with capsaicin-sensitive neurons. Pain 2014, 155, 1516–1526. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lovrencic, L.; Matak, I.; Lackovic, Z. Association of Intranasal and Neurogenic Dural Inflammation in Experimental Acute Rhinosinusitis. Front. Pharmacol. 2020, 11, 586037. [Google Scholar] [CrossRef] [PubMed]
- Cha, M.; Sallem, I.; Jang, H.W.; Jung, I.Y. Role of transient receptor potential vanilloid type 1 in the trigeminal ganglion and brain stem following dental pulp inflammation. Int. Endod. J. 2020, 53, 62–71. [Google Scholar] [CrossRef] [PubMed]
- Matak, I.; Bolcskei, K.; Bach-Rojecky, L.; Helyes, Z. Mechanisms of Botulinum Toxin Type A Action on Pain. Toxins (Basel) 2019, 11, 459. [Google Scholar] [CrossRef] [Green Version]
- Ramachandran, R.; Yaksh, T.L. Therapeutic use of botulinum toxin in migraine: Mechanisms of action. Br. J. Pharmacol. 2014, 171, 4177–4192. [Google Scholar] [CrossRef]
- Julius, D. TRP channels and pain. Annu. Rev. Cell Dev. Biol. 2013, 29, 355–384. [Google Scholar] [CrossRef] [Green Version]
- Cholewinski, A.; Burgess, G.M.; Bevan, S. The role of calcium in capsaicin-induced desensitization in rat cultured dorsal root ganglion neurons. Neuroscience 1993, 55, 1015–1023. [Google Scholar] [CrossRef]
- Kim, Y.S.; Chu, Y.; Han, L.; Li, M.; Li, Z.; LaVinka, P.C.; Sun, S.; Tang, Z.; Park, K.; Caterina, M.J.; et al. Central terminal sensitization of TRPV1 by descending serotonergic facilitation modulates chronic pain. Neuron 2014, 81, 873–887. [Google Scholar] [CrossRef] [Green Version]
- Lawrence, G.W.; Zurawski, T.H.; Dong, X.; Dolly, J.O. Population Coding of Capsaicin Concentration by Sensory Neurons Revealed Using Ca(2+) Imaging of Dorsal Root Ganglia Explants from Adult pirt-GCaMP3 Mouse. Cell. Physiol. Biochem. 2021, 55, 428–448. [Google Scholar] [CrossRef]
- Baker, P.F.; Knight, D.E. Calcium-dependent exocytosis in bovine adrenal medullary cells with leaky plasma membranes. Nature 1978, 276, 620–622. [Google Scholar] [CrossRef] [PubMed]
- Meng, J.; Dolly, J.O.; Wang, J. Selective cleavage of SNAREs in sensory neurons unveils protein complexes mediating peptide exocytosis triggered by different stimuli. Mol. Neurobiol. 2014, 50, 574–588. [Google Scholar] [CrossRef] [PubMed]
- Molgo, J.; Thesleff, S. Studies on the mode of action of botulinum toxin type A at the frog neuromuscular junction. Brain Res. 1984, 297, 309–316. [Google Scholar] [CrossRef]
- Hayashi, T.; McMahon, H.; Yamasaki, S.; Binz, T.; Hata, Y.; Sudhof, T.C.; Niemann, H. Synaptic vesicle membrane fusion complex: Action of clostridial neurotoxins on assembly. EMBO J. 1994, 13, 5051–5061. [Google Scholar] [CrossRef] [PubMed]
- Otto, H.; Hanson, P.I.; Chapman, E.R.; Blasi, J.; Jahn, R. Poisoning by botulinum neurotoxin A does not inhibit formation or disassembly of the synaptosomal fusion complex. Biochem. Biophys. Res. Commun. 1995, 212, 945–952. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Zurawski, T.H.; Meng, J.; Lawrence, G.; Olango, W.M.; Finn, D.P.; Wheeler, L.; Dolly, J.O. A dileucine in the protease of botulinum toxin A underlies its long-lived neuroparalysis: Transfer of longevity to a novel potential therapeutic. J. Biol. Chem. 2011, 286, 6375–6385. [Google Scholar] [CrossRef] [Green Version]
- Khounlo, R.; Kim, J.; Yin, L.; Shin, Y.K. Botulinum Toxins A and E Inflict Dynamic Destabilization on t-SNARE to Impair SNARE Assembly and Membrane Fusion. Structure 2017, 25, 1679–1686 e1675. [Google Scholar] [CrossRef]
- Sakaba, T.; Stein, A.; Jahn, R.; Neher, E. Distinct kinetic changes in neurotransmitter release after SNARE protein cleavage. Science 2005, 309, 491–494. [Google Scholar] [CrossRef] [Green Version]
- Percie du Sert, N.; Ahluwalia, A.; Alam, S.; Avey, M.T.; Baker, M.; Browne, W.J.; Clark, A.; Cuthill, I.C.; Dirnagl, U.; Emerson, M.; et al. Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 2020, 18, e3000411. [Google Scholar] [CrossRef]
- Wang, J.; Meng, J.; Nugent, M.; Tang, M.; Dolly, J.O. Neuronal entry and high neurotoxicity of botulinum neurotoxin A require its N-terminal binding sub-domain. Sci. Rep. 2017, 7, 44474. [Google Scholar] [CrossRef] [Green Version]
- Romero-Reyes, M.; Akerman, S.; Nguyen, E.; Vijjeswarapu, A.; Hom, B.; Dong, H.W.; Charles, A.C. Spontaneous behavioral responses in the orofacial region: A model of trigeminal pain in mouse. Headache 2013, 53, 137–151. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paxinos, G.; Watson, C. The Rat Brain in Stereotaxic Coordinates, 5th ed.; Elsevier Academic Press: Burlington, MA, USA, 2005. [Google Scholar]
- Eckert, S.P.; Taddese, A.; McCleskey, E.W. Isolation and culture of rat sensory neurons having distinct sensory modalities. J. Neurosci. Methods 1997, 77, 183–190. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Antoniazzi, C.; Belinskaia, M.; Zurawski, T.; Kaza, S.K.; Dolly, J.O.; Lawrence, G.W. Botulinum Neurotoxin Chimeras Suppress Stimulation by Capsaicin of Rat Trigeminal Sensory Neurons In Vivo and In Vitro. Toxins 2022, 14, 116. https://doi.org/10.3390/toxins14020116
Antoniazzi C, Belinskaia M, Zurawski T, Kaza SK, Dolly JO, Lawrence GW. Botulinum Neurotoxin Chimeras Suppress Stimulation by Capsaicin of Rat Trigeminal Sensory Neurons In Vivo and In Vitro. Toxins. 2022; 14(2):116. https://doi.org/10.3390/toxins14020116
Chicago/Turabian StyleAntoniazzi, Caren, Mariia Belinskaia, Tomas Zurawski, Seshu Kumar Kaza, J. Oliver Dolly, and Gary W. Lawrence. 2022. "Botulinum Neurotoxin Chimeras Suppress Stimulation by Capsaicin of Rat Trigeminal Sensory Neurons In Vivo and In Vitro" Toxins 14, no. 2: 116. https://doi.org/10.3390/toxins14020116
APA StyleAntoniazzi, C., Belinskaia, M., Zurawski, T., Kaza, S. K., Dolly, J. O., & Lawrence, G. W. (2022). Botulinum Neurotoxin Chimeras Suppress Stimulation by Capsaicin of Rat Trigeminal Sensory Neurons In Vivo and In Vitro. Toxins, 14(2), 116. https://doi.org/10.3390/toxins14020116