Nicotinic acetylcholine receptors containing the α7-like subunit mediate contractions of muscles responsible for space positioning of the snail, Helix pomatia L. tentacle
Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia. The muscles receive central and peripheral excitatory cholinergic innervation lacking inhibitory innervation. Here, we investigate the pharmacology of ace...
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Published in | PloS one Vol. 9; no. 10; p. e109538 |
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Abstract | Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia. The muscles receive central and peripheral excitatory cholinergic innervation lacking inhibitory innervation. Here, we investigate the pharmacology of acetylcholine (ACh) responses in muscles to determine the properties of the ACh receptor (AChR), the functional availability of which was assessed using isotonic contraction measurement. Using broad spectrum of nicotinic and muscarinic ligands, we provide the evidence that contractions in the muscles are attributable to the activation of nAChRs that contain the α7-like subunit. Contractions could be evoked by nicotine, carbachol, succinylchloride, TMA, the selective α7-nAChR agonist choline chloride, 3-Bromocytisine and PNU-282987, and blocked by nAChR selective antagonists such as mytolon, hexamethonium, succinylchloride, d-tubocurarine, hemicholinium, DMDA (decamethonium), methyllycaconitine, α-Bungarotoxin (αBgTx) and α-Conotoxin IMI. The specific muscarinic agonist oxotremorine and arecoline failed to elicit contractions. Based on these pharmacological properties we conclude that the Na+ and Ca2+ permeable AChRs of the flexor muscle are nicotinic receptors that contain the α7-like subunit. Immunodetection experiments confirmed the presence of α7- or α7-like AChRs in muscle cells, and α4-AChRs in nerves innervating the muscle. These results support the conclusion that the slowly desensitizing αBgTx-sensitive responses obtained from flexor muscles are produced by activation of α7- like AChRs. This is the first demonstration of postsynaptic expression and an obligatory role for a functional α7-like nAChR in the molluscan periphery. |
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AbstractList | Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia. The muscles receive central and peripheral excitatory cholinergic innervation lacking inhibitory innervation. Here, we investigate the pharmacology of acetylcholine (ACh) responses in muscles to determine the properties of the ACh receptor (AChR), the functional availability of which was assessed using isotonic contraction measurement. Using broad spectrum of nicotinic and muscarinic ligands, we provide the evidence that contractions in the muscles are attributable to the activation of nAChRs that contain the α7-like subunit. Contractions could be evoked by nicotine, carbachol, succinylchloride, TMA, the selective α7-nAChR agonist choline chloride, 3-Bromocytisine and PNU-282987, and blocked by nAChR selective antagonists such as mytolon, hexamethonium, succinylchloride, d-tubocurarine, hemicholinium, DMDA (decamethonium), methyllycaconitine, α-Bungarotoxin (αBgTx) and α-Conotoxin IMI. The specific muscarinic agonist oxotremorine and arecoline failed to elicit contractions. Based on these pharmacological properties we conclude that the Na+ and Ca2+ permeable AChRs of the flexor muscle are nicotinic receptors that contain the α7-like subunit. Immunodetection experiments confirmed the presence of α7- or α7-like AChRs in muscle cells, and α4-AChRs in nerves innervating the muscle. These results support the conclusion that the slowly desensitizing αBgTx-sensitive responses obtained from flexor muscles are produced by activation of α7- like AChRs. This is the first demonstration of postsynaptic expression and an obligatory role for a functional α7-like nAChR in the molluscan periphery. Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia . The muscles receive central and peripheral excitatory cholinergic innervation lacking inhibitory innervation. Here, we investigate the pharmacology of acetylcholine (ACh) responses in muscles to determine the properties of the ACh receptor (AChR), the functional availability of which was assessed using isotonic contraction measurement. Using broad spectrum of nicotinic and muscarinic ligands, we provide the evidence that contractions in the muscles are attributable to the activation of nAChRs that contain the α7-like subunit. Contractions could be evoked by nicotine, carbachol, succinylchloride, TMA, the selective α7-nAChR agonist choline chloride, 3-Bromocytisine and PNU-282987, and blocked by nAChR selective antagonists such as mytolon, hexamethonium, succinylchloride, d-tubocurarine, hemicholinium, DMDA (decamethonium), methyllycaconitine, α-Bungarotoxin (αBgTx) and α-Conotoxin IMI. The specific muscarinic agonist oxotremorine and arecoline failed to elicit contractions. Based on these pharmacological properties we conclude that the Na + and Ca 2+ permeable AChRs of the flexor muscle are nicotinic receptors that contain the α7-like subunit. Immunodetection experiments confirmed the presence of α7- or α7-like AChRs in muscle cells, and α4-AChRs in nerves innervating the muscle. These results support the conclusion that the slowly desensitizing αBgTx-sensitive responses obtained from flexor muscles are produced by activation of α7- like AChRs. This is the first demonstration of postsynaptic expression and an obligatory role for a functional α7-like nAChR in the molluscan periphery. Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia . The muscles receive central and peripheral excitatory cholinergic innervation lacking inhibitory innervation. Here, we investigate the pharmacology of acetylcholine (ACh) responses in muscles to determine the properties of the ACh receptor (AChR), the functional availability of which was assessed using isotonic contraction measurement. Using broad spectrum of nicotinic and muscarinic ligands, we provide the evidence that contractions in the muscles are attributable to the activation of nAChRs that contain the α7-like subunit. Contractions could be evoked by nicotine, carbachol, succinylchloride, TMA, the selective α7-nAChR agonist choline chloride, 3-Bromocytisine and PNU-282987, and blocked by nAChR selective antagonists such as mytolon, hexamethonium, succinylchloride, d-tubocurarine, hemicholinium, DMDA (decamethonium), methyllycaconitine, α-Bungarotoxin (αBgTx) and α-Conotoxin IMI. The specific muscarinic agonist oxotremorine and arecoline failed to elicit contractions. Based on these pharmacological properties we conclude that the Na + and Ca 2+ permeable AChRs of the flexor muscle are nicotinic receptors that contain the α7-like subunit. Immunodetection experiments confirmed the presence of α7- or α7-like AChRs in muscle cells, and α4-AChRs in nerves innervating the muscle. These results support the conclusion that the slowly desensitizing αBgTx-sensitive responses obtained from flexor muscles are produced by activation of α7- like AChRs. This is the first demonstration of postsynaptic expression and an obligatory role for a functional α7-like nAChR in the molluscan periphery. |
Author | Kiss, Tibor Krajcs, Nóra Pirger, Zsolt Hernádi, László |
AuthorAffiliation | 1 Chemical Ecology and Neurobiology Group, Department of Experimental Zoology, Balaton Limnological Institute, MTA Centre for Ecological Research, Tihany, Hungary Chiba University Center for Forensic Mental Health, Japan 2 Adaptive Neuroetology MTA-CER, National Brain Project Team, Tihany, Hungary |
AuthorAffiliation_xml | – name: 1 Chemical Ecology and Neurobiology Group, Department of Experimental Zoology, Balaton Limnological Institute, MTA Centre for Ecological Research, Tihany, Hungary – name: 2 Adaptive Neuroetology MTA-CER, National Brain Project Team, Tihany, Hungary – name: Chiba University Center for Forensic Mental Health, Japan |
Author_xml | – sequence: 1 givenname: Tibor surname: Kiss fullname: Kiss, Tibor organization: Chemical Ecology and Neurobiology Group, Department of Experimental Zoology, Balaton Limnological Institute, MTA Centre for Ecological Research, Tihany, Hungary – sequence: 2 givenname: Nóra surname: Krajcs fullname: Krajcs, Nóra organization: Chemical Ecology and Neurobiology Group, Department of Experimental Zoology, Balaton Limnological Institute, MTA Centre for Ecological Research, Tihany, Hungary – sequence: 3 givenname: Zsolt surname: Pirger fullname: Pirger, Zsolt organization: Adaptive Neuroetology MTA-CER, National Brain Project Team, Tihany, Hungary – sequence: 4 givenname: László surname: Hernádi fullname: Hernádi, László organization: Chemical Ecology and Neurobiology Group, Department of Experimental Zoology, Balaton Limnological Institute, MTA Centre for Ecological Research, Tihany, Hungary |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25303328$$D View this record in MEDLINE/PubMed |
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Copyright | 2014 Kiss et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2014 Kiss et al 2014 Kiss et al |
Copyright_xml | – notice: 2014 Kiss et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2014 Kiss et al 2014 Kiss et al |
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DocumentTitleAlternate | Alpha7-Like Nicotinic Acetylcholine Receptors in Gastropod Muscle |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: TK. Performed the experiments: NK ZP LH. Analyzed the data: TK ZP NK. Contributed reagents/materials/analysis tools: TK. Wrote the paper: TK LH. |
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Snippet | Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia. The muscles... Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia . The muscles... Three recently discovered tentacle muscles are crucial to perform patterned movements of upper tentacles of the terrestrial snail, Helix pomatia . The muscles... |
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SubjectTerms | Acetylcholine receptors (muscarinic) Acetylcholine receptors (nicotinic) Activation alpha7 Nicotinic Acetylcholine Receptor - agonists alpha7 Nicotinic Acetylcholine Receptor - metabolism Animals Antagonists Aplysia Biology and Life Sciences Brain research Bungarotoxin Calcium ions Calcium permeability Carbachol Choline Contraction Desensitization Enzymes Helix (Snails) - physiology Helix pomatia Hexamethonium Innervation Methyllycaconitine Mollusca Movement - drug effects Movement - physiology Muscarinic Agonists - pharmacology Muscle contraction Muscle Contraction - drug effects Muscle Contraction - physiology Muscles Muscles - drug effects Muscles - physiology Nerves Neurobiology Neurons - drug effects Neurons - metabolism Neurosciences Nicotine Nicotinic Agonists - pharmacology Oxotremorine Permeability Pharmacology Physiology Receptors Receptors, Nicotinic - metabolism Rodents Synapses - drug effects Synapses - metabolism Tentacles Terrestrial environments Tubocurarine Zoology |
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Title | Nicotinic acetylcholine receptors containing the α7-like subunit mediate contractions of muscles responsible for space positioning of the snail, Helix pomatia L. tentacle |
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