Home LiteratureArticle Details
PMID: 9870940 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors.

Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, Huddleston D, Eiden LE, Rand JB

Abstract

We have identified the Caenorhabditis elegans homolog of the mammalian vesicular monoamine transporters (VMATs); it is 47% identical to human VMAT1 and 49% identical to human VMAT2. C. elegans VMAT is associated with synaptic vesicles in approximately 25 neurons, including all of the cells reported to contain dopamine and serotonin, plus a few others. When C. elegans VMAT is expressed in mammalian cells, it has serotonin and dopamine transport activity; norepinephrine, tyramine, octopamine, and histamine also have high affinity for the transporter. The pharmacological profile of C. elegans VMAT is closer to mammalian VMAT2 than VMAT1. The C. elegans VMAT gene is cat-1; cat-1 knock-outs are totally deficient for VMAT immunostaining and for dopamine-mediated sensory behaviors, yet they are viable and grow relatively well. The cat-1 mutant phenotypes can be rescued by C. elegans VMAT constructs and also (at least partially) by human VMAT1 or VMAT2 transgenes. It therefore appears that the function of amine neurotransmitters can be completely dependent on their loading into synaptic vesicles.

MeSH Terms
Amino Acid Sequence Animals Animals, Genetically Modified Biogenic Monoamines/physiology Biological Transport/physiology Caenorhabditis elegans/genetics Dopamine/analysis Genes, Helminth Genetic Code Humans Membrane Glycoproteins/deficiency,genetics Membrane Transport Proteins Molecular Sequence Data Mutation Neurons/chemistry Neuropeptides Phenotype Sequence Homology, Amino Acid Synaptic Vesicles/metabolism Vesicular Biogenic Amine Transport Proteins Vesicular Monoamine Transport Proteins
Chemicals
Biogenic Monoamines Membrane Glycoproteins Membrane Transport Proteins Neuropeptides SLC18A1 protein, human SLC18A2 protein, human Vesicular Biogenic Amine Transport Proteins Vesicular Monoamine Transport Proteins Dopamine
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Duerr J S
Program in Molecular and Cell Biology, Oklahoma Medical Research Foundation, Oklahoma City, Oklahoma 73104, USA.
Frisby D L
Gaskin J
Duke A
Asermely K
Huddleston D
Eiden L E
Rand J B
References (64)
64 references, click to expand
  1. Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11.
    J Neurosci. 1998 Mar 15;18(6):2084-96 PMID: 9482795
  2. Control of larval development by chemosensory neurons in Caenorhabditis elegans.
    Science. 1991 Mar 8;251(4998):1243-6 PMID: 2006412
  3. Vesicular neurotransmitter transporters: from bacteria to humans.
    Physiol Rev. 1995 Apr;75(2):369-92 PMID: 7724667
  4. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase.
    Proc Natl Acad Sci U S A. 1986 Nov;83(21):8122-6 PMID: 3095828
  5. Presence of the Caenorhabditis elegans spliced leader on different mRNAs and in different genera of nematodes.
    Genes Dev. 1988 Oct;2(10):1277-83 PMID: 3203906
  6. Neuronal localization of serotonin in the nematode Ascaris suum.
    J Comp Neurol. 1996 Apr 08;367(3):352-60 PMID: 8698897
  7. Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development.
    Nature. 1995 Apr 13;374(6523):640-3 PMID: 7715703
  8. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans.
    Neuron. 1991 Nov;7(5):729-42 PMID: 1660283
  9. Structure and organization of the Drosophila cholinergic locus.
    J Biol Chem. 1998 Jan 30;273(5):2706-13 PMID: 9446576
  10. Caenorhabditis elegans mutants defective in the functioning of the motor neurons responsible for egg laying.
    Genetics. 1989 Apr;121(4):703-21 PMID: 2721931
  11. Distinct pharmacological properties and distribution in neurons and endocrine cells of two isoforms of the human vesicular monoamine transporter.
    Proc Natl Acad Sci U S A. 1996 May 14;93(10):5166-71 PMID: 8643547
  12. Vinculin is essential for muscle function in the nematode.
    J Cell Biol. 1991 Aug;114(4):715-24 PMID: 1907975
  13. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes.
    Dev Biol. 1985 Sep;111(1):158-70 PMID: 3928418
  14. A suppressor mutation in the nematode acting on specific alleles of many genes.
    Nature. 1978 Oct 26;275(5682):715-9 PMID: 703836
  15. The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein.
    Neuron. 1991 Jan;6(1):113-22 PMID: 1846075
  16. Reserpine- and tetrabenazine-sensitive transport of (3)H-histamine by the neuronal isoform of the vesicular monoamine transporter.
    J Mol Neurosci. 1995;6(4):277-87 PMID: 8860238
  17. Vesicular neurotransmitter transporters. Potential sites for the regulation of synaptic function.
    Mol Neurobiol. 1997 Oct;15(2):165-91 PMID: 9396009
  18. Formation of the first cleavage spindle in nematode embryos.
    Dev Biol. 1984 Jan;101(1):61-72 PMID: 6692980
  19. Genesis of an organ: molecular analysis of the pha-1 gene.
    Development. 1994 Oct;120(10):3005-17 PMID: 7607088
  20. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans.
    J Neurosci. 1993 Dec;13(12):5407-17 PMID: 8254383
  21. A trans-spliced leader sequence on actin mRNA in C. elegans.
    Cell. 1987 Jun 19;49(6):753-61 PMID: 3581169
  22. A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans.
    Nature. 1995 May 4;375(6526):73-8 PMID: 7723846
  23. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene.
    Neuron. 1997 Aug;19(2):345-57 PMID: 9292724
  24. Chimeric vesicular monoamine transporters identify structural domains that influence substrate affinity and sensitivity to tetrabenazine.
    J Biol Chem. 1996 Feb 9;271(6):2979-86 PMID: 8621690
  25. Functional identification of a vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus.
    J Biol Chem. 1994 Sep 2;269(35):21929-32 PMID: 8071310
  26. 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
  27. Noradrenaline is essential for mouse fetal development.
    Nature. 1995 Apr 13;374(6523):643-6 PMID: 7715704
  28. Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans.
    Science. 1995 Mar 17;267(5204):1648-51 PMID: 7886454
  29. Organogenesis in C. elegans: positioning of neurons and muscles in the egg-laying system.
    Neuron. 1990 May;4(5):681-95 PMID: 2344407
  30. A novel method for producing anti-peptide antibodies. Production of site-specific antibodies to the T cell antigen receptor beta-chain.
    J Biol Chem. 1988 Feb 5;263(4):1719-25 PMID: 3276675
  31. Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans.
    J Neurosci. 1995 Oct;15(10):6975-85 PMID: 7472454
  32. The vesicular monoamine transporter 2 is present in small synaptic vesicles and preferentially localizes to large dense core vesicles in rat solitary tract nuclei.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8773-7 PMID: 7568015
  33. Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans.
    J Exp Zool. 1990 Mar;253(3):263-70 PMID: 2181052
  34. An improved approach to histofluorescence using the SPG method for tissue monoamines.
    J Neurosci Methods. 1980 Oct;3(1):1-5 PMID: 6164878
  35. The unc-86 gene product couples cell lineage and cell identity in C. elegans.
    Cell. 1990 Nov 30;63(5):895-905 PMID: 2257628
  36. Cloning and functional expression of a tetrabenazine sensitive vesicular monoamine transporter from bovine chromaffin granules.
    FEBS Lett. 1994 Jan 24;338(1):16-22 PMID: 8307150
  37. Genes necessary for directed axonal elongation or fasciculation in C. elegans.
    Neuron. 1992 Feb;8(2):307-22 PMID: 1739461
  38. Functional identification and molecular cloning of a human brain vesicle monoamine transporter.
    J Neurochem. 1993 Dec;61(6):2314-7 PMID: 8245983
  39. Expression cloning of a reserpine-sensitive vesicular monoamine transporter.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10993-7 PMID: 1438304
  40. 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
  41. The genetics of Caenorhabditis elegans.
    Genetics. 1974 May;77(1):71-94 PMID: 4366476
  42. Sensory regulation of male mating behavior in Caenorhabditis elegans.
    Neuron. 1995 Jan;14(1):79-89 PMID: 7826644
  43. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.
    EMBO J. 1991 Dec;10(12):3959-70 PMID: 1935914
  44. Dopaminergic neurons in the nematode Caenorhabditis elegans.
    J Comp Neurol. 1975 Sep 15;163(2):215-26 PMID: 240872
  45. Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants.
    J Neurosci. 1998 Jan 1;18(1):70-80 PMID: 9412487
  46. Post-embryonic development in the ventral cord of Caenorhabditis elegans.
    Philos Trans R Soc Lond B Biol Sci. 1976 Aug 10;275(938):287-97 PMID: 8804
  47. Knockout of the vesicular monoamine transporter 2 gene results in neonatal death and supersensitivity to cocaine and amphetamine.
    Neuron. 1997 Dec;19(6):1285-96 PMID: 9427251
  48. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons.
    Nature. 1988 Dec 15;336(6200):638-46 PMID: 3200316
  49. Preferential localization of a vesicular monoamine transporter to dense core vesicles in PC12 cells.
    J Cell Biol. 1994 Dec;127(5):1419-33 PMID: 7962100
  50. The pharynx of Caenorhabditis elegans.
    Philos Trans R Soc Lond B Biol Sci. 1976 Aug 10;275(938):299-325 PMID: 8805
  51. Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat.
    J Mol Neurosci. 1994 Fall;5(3):149-64 PMID: 7654518
  52. Egg-laying defective mutants of the nematode Caenorhabditis elegans.
    Genetics. 1983 Aug;104(4):619-47 PMID: 11813735
  53. Serotonin and octopamine in the nematode Caenorhabditis elegans.
    Science. 1982 May 28;216(4549):1012-4 PMID: 6805073
  54. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter.
    Science. 1993 Jul 30;261(5121):617-9 PMID: 8342028
  55. Cloning and expression of the vesamicol binding protein from the marine ray Torpedo. Homology with the putative vesicular acetylcholine transporter UNC-17 from Caenorhabditis elegans.
    FEBS Lett. 1994 Mar 28;342(1):97-102 PMID: 8143858
  56. Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: application of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots.
    J Cell Biol. 1984 Jul;99(1 Pt 1):20-8 PMID: 6203917
  57. A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter.
    Cell. 1992 Aug 21;70(4):539-51 PMID: 1505023
  58. 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
  59. Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans.
    Genetics. 1977 Jun;86(2 Pt. 1):275-87 PMID: 560330
  60. Genetic control of programmed cell death in the nematode C. elegans.
    Cell. 1986 Mar 28;44(6):817-29 PMID: 3955651
  61. Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans.
    Cell. 1991 May 31;65(5):837-47 PMID: 1710172
  62. The structure of the ventral nerve cord of Caenorhabditis elegans.
    Philos Trans R Soc Lond B Biol Sci. 1976 Aug 10;275(938):327-48 PMID: 8806
  63. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin.
    Cell. 1993 Jul 2;73(7):1291-305 PMID: 8391930
  64. Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action.
    Neuron. 1997 Dec;19(6):1271-83 PMID: 9427250
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1999-01-01
Pages
72-84
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6782383
Subset
IM
Grants
NIGMS NIH HHS · R01 GM038679 · United States
NIGMS NIH HHS · GM38679 · United States
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: product@genelibs.com