G alpha(q)-coupled muscarinic acetylcholine receptors enhance nicotinic acetylcholine receptor signaling in Caenorhabditis elegans mating behavior.
In this study, we address why metabotropic and ionotropic cholinergic signaling pathways are used to facilitate motor behaviors. We demonstrate that a G alpha(q)-coupled muscarinic acetylcholine receptor (mAChR) signaling pathway enhances nicotinic acetylcholine receptor (nAChR) signaling to facilitate the insertion of the Caenorhabditis elegans male copulatory spicules into the hermaphrodite during mating. Previous studies showed that ACh (acetylcholine) activates nAChRs on the spicule protractor muscles to induce the attached spicules to extend from the tail. Using the mAChR agonist Oxo M (oxotremorine M), we identified a GAR-3(mAChR)-G alpha(q) pathway that promotes protractor muscle contraction by upregulating nAChR signaling before mating. GAR-3(mAChR) is expressed in the protractor muscles and in the spicule-associated SPC and PCB cholinergic neurons. However, ablation of these neurons or impairing cholinergic transmission reduces drug-induced spicule protraction, suggesting that drug-stimulated neurons directly activate muscle contraction. Behavioral analysis of gar-3 mutants indicates that, in wild-type males, GAR-3(mAChR) expression in the SPC and PCB neurons is required for the male to sustain rhythmic spicule muscle contractions during attempts to breach the vulva. We propose that the GAR-3(mAChR)/G alpha(q) pathway sensitizes the spicule neurons and muscles before and during mating so that the male can respond to hermaphrodite vulva efficiently.
Liu
Yishi
Y
Department of Biology, Texas A&M University, College Station, Texas 77843-3258, USA.
LeBoeuf
Brigitte
B
Garcia
L René
LR
D000109:Acetylcholine / Q000502:physiology*; D000818:Animals; D030801:Animals, Genetically Modified; D017173:Caenorhabditis elegans / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D002352:Carrier Proteins / Q000235:genetics / Q000502:physiology; D012734:Disorders of Sex Development; D043802:GTP-Binding Protein alpha Subunits, Gq-G11 / Q000172:deficiency / Q000235:genetics / Q000502:physiology*; D005835:Genitalia / Q000294:innervation / Q000502:physiology; D007527:Isoenzymes / Q000172:deficiency / Q000235:genetics / Q000502:physiology; D007978:Levamisole / Q000494:pharmacology; D018721:Muscarinic Agonists / Q000494:pharmacology; D009119:Muscle Contraction / Q000502:physiology; D020125:Mutation, Missense; D009474:Neurons / Q000502:physiology; D010095:Oxotremorine / Q000494:pharmacology; D010507:Periodicity; D054799:Phospholipase C beta; D015221:Potassium Channels / Q000172:deficiency / Q000235:genetics / Q000502:physiology; D011976:Receptors, Muscarinic / Q000172:deficiency / Q000235:genetics / Q000502:physiology*; D011978:Receptors, Nicotinic / Q000502:physiology*; D011993:Recombinant Fusion Proteins / Q000502:physiology; D019837:Ryanodine Receptor Calcium Release Channel / Q000187:drug effects; D012726:Sexual Behavior, Animal / Q000502:physiology*; D015398:Signal Transduction / Q000502:physiology; D050827:Syntaxin 1 / Q000172:deficiency / Q000235:genetics / Q000502:physiology; D010738:Type C Phospholipases / Q000172:deficiency / Q000235:genetics / Q000502:physiology; D050494:Vesicular Acetylcholine Transport Proteins / Q000172:deficiency / Q000235:genetics / Q000502:physiology
D029742:Caenorhabditis elegans Proteins; D002352:Carrier Proteins; C479565:Egl-30 protein, C elegans; C477876:GAR-3 protein, C elegans; D007527:Isoenzymes; D018721:Muscarinic Agonists; D015221:Potassium Channels; D011976:Receptors, Muscarinic; D011978:Receptors, Nicotinic; D011993:Recombinant Fusion Proteins; D019837:Ryanodine Receptor Calcium Release Channel; D050827:Syntaxin 1; C474006:UNC-103 protein, C elegans; C082365:Unc-17 protein, C elegans; C517631:Unc-38 protein, C elegans; C438601:Unc-68 protein, C elegans; D050494:Vesicular Acetylcholine Transport Proteins; C494215:unc-64 protein, C elegans; D007978:Levamisole; D010095:Oxotremorine; D010738:Type C Phospholipases; C517632:Egl-8 protein, C elegans; D054799:Phospholipase C beta; D043802:GTP-Binding Protein alpha Subunits, Gq-G11; D000109:Acetylcholine