Home LiteratureArticle Details
PMID: 12954868 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Genetic and cellular basis for acetylcholine inhibition of Caenorhabditis elegans egg-laying behavior.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 23 ·No. 22 ·2003-09-03 ·Pages 8060-9

Bany IA, Dong MQ, Koelle MR

Abstract

Egg-laying behavior in Caenorhabditis elegans is activated by signaling through the G-protein G(rho)q and inhibited by signaling through a second G-protein, G(rho)o. Activation of egg laying depends on the serotonergic hermaphrodite-specific neurons (HSNs), but the neurotransmitter(s) and cell(s) that signal to inhibit egg laying are not known. Mutants for G-protein signaling genes have well characterized defects in egg laying. Here we present an analysis of mutants for other genes reported to lack inhibition of egg laying. Of the nine strongest, six have morphological defects in the ventral-type C (VC) neurons, which synapse onto both the HSNs and the egg-laying muscles and are thus the third cell type comprising the egg-laying system. Laser-ablating VC neurons could also disrupt the inhibition of egg laying. The remaining three mutants (unc-4, cha-1, and unc-17) are defective for synthesis or packaging of acetylcholine in the VCs. The egg-laying defects of unc-4, cha-1, and unc-17 were rescued by VC-specific expression of the corresponding cDNAs. In addition, increasing synaptic acetylcholine by reducing acetylcholinesterase activity, with either mutations or the inhibitor aldicarb, decreased egg laying. Finally, we found that a knock-out for the HSN-expressed receptor G-protein-coupled acetylcholine receptor 2 (GAR-2) shows a partial defect in the inhibition of egg laying and fails to respond to aldicarb. Our results show that acetylcholine released from the VC neurons inhibits egg-laying behavior. This inhibition may be caused, in part, by acetylcholine signaling onto the HSN presynaptic terminals, via GAR-2, to inhibit neurotransmitter release.

MeSH Terms
Acetylcholine/metabolism,pharmacology Acetylcholinesterase/drug effects,genetics Animals Animals, Genetically Modified Behavior, Animal/drug effects,physiology Caenorhabditis elegans/drug effects,genetics,physiology Caenorhabditis elegans Proteins/genetics Cholinesterase Inhibitors/pharmacology DNA, Complementary/pharmacology GTP-Binding Proteins/metabolism Homeodomain Proteins/genetics Inhibition, Psychological Mutation Neurons/drug effects,pathology,physiology Nuclear Proteins/genetics Oviposition/drug effects,genetics,physiology Phenotype Receptors, Cholinergic/deficiency,genetics Signal Transduction/physiology Synapses/drug effects,metabolism
Chemicals
Caenorhabditis elegans Proteins Cholinesterase Inhibitors DNA, Complementary G protein-linked acetylcholine receptor 2 Homeodomain Proteins Nuclear Proteins Receptors, Cholinergic unc-4 protein, C elegans Acetylcholinesterase GTP-Binding Proteins Acetylcholine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bany I Amy
Department of Cell Biology, Yale University School of Medicine, New Haven, Connecticut 06520-8024, USA.
Dong Meng-Qiu
Koelle Michael R
References (45)
45 references, click to expand
  1. The C. elegans homeodomain gene unc-42 regulates chemosensory and glutamate receptor expression.
    Development. 1999 May;126(10):2241-51 PMID: 10207148
  2. Antagonism between G(o)alpha and G(q)alpha in Caenorhabditis elegans: the RGS protein EAT-16 is necessary for G(o)alpha signaling and regulates G(q)alpha activity.
    Genes Dev. 1999 Jul 15;13(14):1780-93 PMID: 10421631
  3. UNC-4/UNC-37-dependent repression of motor neuron-specific genes controls synaptic choice in Caenorhabditis elegans.
    Genes Dev. 1999 Nov 1;13(21):2774-86 PMID: 10557206
  4. Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans.
    Neuron. 1999 Oct;24(2):323-33 PMID: 10571227
  5. Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release.
    Neuron. 1999 Oct;24(2):335-46 PMID: 10571228
  6. Cloning and functional characterization of a Caenorhabditis elegans muscarinic acetylcholine receptor.
    Receptors Channels. 1999;6(6):415-24 PMID: 10635059
  7. Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites.
    Neuron. 1999 Sep;24(1):231-42 PMID: 10677040
  8. Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egg-laying.
    Genetics. 2000 Mar;154(3):1181-92 PMID: 10757762
  9. Neuronal nicotinic receptors, important new players in brain function.
    Eur J Pharmacol. 2000 Mar 30;393(1-3):3-10 PMID: 10770992
  10. Regulation of transmitter release by Unc-13 and its homologues.
    Curr Opin Neurobiol. 2000 Jun;10(3):303-11 PMID: 10851170
  11. Four genes encode acetylcholinesterases in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. cDNA sequences, genomic structures, mutations and in vivo expression.
    J Mol Biol. 2000 Jul 21;300(4):727-42 PMID: 10891266
  12. Multiple RGS proteins alter neural G protein signaling to allow C. elegans to rapidly change behavior when fed.
    Genes Dev. 2000 Aug 15;14(16):2003-14 PMID: 10950865
  13. Characterization of GAR-2, a novel G protein-linked acetylcholine receptor from Caenorhabditis elegans.
    J Neurochem. 2000 Nov;75(5):1800-9 PMID: 11032868
  14. Long-term nicotine adaptation in Caenorhabditis elegans involves PKC-dependent changes in nicotinic receptor abundance.
    J Neurosci. 2000 Dec 1;20(23):8802-11 PMID: 11102488
  15. G-protein signaling: satisfying the basic necessities of life.
    Curr Biol. 2000 Nov 30;10(23):R853-6 PMID: 11114530
  16. Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and its transcriptional corepressor UNC-37/groucho in Caenorhabditis elegans cholinergic motor neurons.
    J Neurosci. 2001 Mar 15;21(6):2001-14 PMID: 11245684
  17. Genes affecting the activity of nicotinic receptors involved in Caenorhabditis elegans egg-laying behavior.
    Genetics. 2001 Apr;157(4):1599-610 PMID: 11290716
  18. Identified neurons in C. elegans coexpress vesicular transporters for acetylcholine and monoamines.
    Am J Physiol Cell Physiol. 2001 Jun;280(6):C1616-22 PMID: 11350757
  19. Egg-laying defective mutants of the nematode Caenorhabditis elegans.
    Genetics. 1983 Aug;104(4):619-47 PMID: 11813735
  20. Fine tuning of sympathetic transmitter release via ionotropic and metabotropic presynaptic receptors.
    Pharmacol Rev. 2002 Mar;54(1):43-99 PMID: 11870260
  21. PAG-3, a Zn-finger transcription factor, determines neuroblast fate in C. elegans.
    Development. 2002 Apr;129(7):1763-74 PMID: 11923211
  22. The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM.
    Neuron. 2003 Jan 9;37(1):53-65 PMID: 12526772
  23. The structure of the nervous system of the nematode Caenorhabditis elegans.
    Philos Trans R Soc Lond B Biol Sci. 1986 Nov 12;314(1165):1-340 PMID: 22462104
  24. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons.
    Nature. 1988 Dec 15;336(6200):638-46 PMID: 3200316
  25. The acetylcholinesterase genes of C. elegans: identification of a third gene (ace-3) and mosaic mapping of a synthetic lethal phenotype.
    Neuron. 1988 Apr;1(2):165-73 PMID: 3272166
  26. The genetics of Caenorhabditis elegans.
    Genetics. 1974 May;77(1):71-94 PMID: 4366476
  27. Choline acetyltransferase-deficient mutants of the nematode Caenorhabditis elegans.
    Genetics. 1984 Feb;106(2):227-48 PMID: 6698395
  28. Levamisole-resistant mutants of the nematode Caenorhabditis elegans appear to lack pharmacological acetylcholine receptors.
    Neuroscience. 1980;5(6):967-89 PMID: 7402460
  29. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans.
    J Neurosci. 1995 Oct;15(10):6975-85 PMID: 7472454
  30. Muscarinic acetylcholine receptors: signal transduction through multiple effectors.
    FASEB J. 1995 May;9(8):619-25 PMID: 7768353
  31. Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans.
    Science. 1995 Mar 17;267(5204):1648-51 PMID: 7886454
  32. Participation of the protein Go in multiple aspects of behavior in C. elegans.
    Science. 1995 Mar 17;267(5204):1652-5 PMID: 7886455
  33. Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans.
    J Neurosci. 1994 Apr;14(4):2290-300 PMID: 8158270
  34. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter.
    Science. 1993 Jul 30;261(5121):617-9 PMID: 8342028
  35. EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins.
    Cell. 1996 Jan 12;84(1):115-25 PMID: 8548815
  36. Mutations in a C. elegans Gqalpha gene disrupt movement, egg laying, and viability.
    Neuron. 1996 May;16(5):999-1009 PMID: 8630258
  37. A genetic selection for Caenorhabditis elegans synaptic transmission mutants.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12593-8 PMID: 8901627
  38. The Caenorhabditis elegans gene unc-76 and its human homologs define a new gene family involved in axonal outgrowth and fasciculation.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3414-9 PMID: 9096408
  39. Genes that guide growth cones along the C. elegans ventral nerve cord.
    Development. 1997 Jul;124(13):2571-80 PMID: 9216999
  40. Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans.
    Dev Biol. 1998 Feb 1;194(1):72-85 PMID: 9473333
  41. Presynaptic receptors.
    Annu Rev Pharmacol Toxicol. 1998;38:201-27 PMID: 9597154
  42. Control of alternative behavioral states by serotonin in Caenorhabditis elegans.
    Neuron. 1998 Jul;21(1):203-14 PMID: 9697864
  43. UNC-115, a conserved protein with predicted LIM and actin-binding domains, mediates axon guidance in C. elegans.
    Neuron. 1998 Aug;21(2):385-92 PMID: 9728919
  44. Cloning and expression of a G protein-linked acetylcholine receptor from Caenorhabditis elegans.
    J Neurochem. 1999 Jan;72(1):58-65 PMID: 9886054
  45. Mammalian homologue of the Caenorhabditis elegans UNC-76 protein involved in axonal outgrowth is a protein kinase C zeta-interacting protein.
    J Cell Biol. 1999 Feb 8;144(3):403-11 PMID: 9971736
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-09-03
Pages
8060-9
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6740490
Subset
IM
Grants
NINDS NIH HHS · R01 NS036918 · United States
NINDS NIH HHS · NS36918 · United States
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2