A genetic screen in Caenorhabditis elegans for dopamine neuron insensitivity to 6-hydroxydopamine identifies dopamine transporter mutants impacting transporter biosynthesis and trafficking

J Neurochem. 2005 Aug;94(3):774-85. doi: 10.1111/j.1471-4159.2005.03205.x. Epub 2005 Jun 30.

Abstract

The presynaptic dopamine (DA) transporter (DAT) is a major determinant of synaptic DA inactivation, an important target for psychostimulants including cocaine and amphetamine, and a mediator of DA neuron vulnerability to the neurotoxins 6-hydroxydopamine (6-OHDA) and 1-methyl-4-phenylpyridinium ion. To exploit genetic approaches for the study of DATs and neural degeneration, we exploited the visibility of green fluorescent protein (GFP)-tagged DA neurons in transgenic nematodes to implement a forward genetic screen for suppressors of 6-OHDA sensitivity. In our initial effort, we identified three novel dat-1 alleles conferring 6-OHDA resistance. Two of the dat-1 alleles derive from point mutations in conserved glycine residues (G55, G90) in contiguous DAT-1 transmembrane domains (TM1 and TM2, respectively), whereas the third allele results in altered translation of the transporter's COOH terminus. Our studies reveal biosynthetic, trafficking and functional defects in the DAT-1 mutants, exhibited both in vitro and in vivo. These studies validate a forward genetic approach to the isolation of DA neuron-specific toxin suppressors and point to critical contributions of the mutated residues, as well as elements of the DAT-1 COOH terminus, to functional expression of catecholamine transporters in neurons.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adrenergic Agents / pharmacology
  • Animals
  • Animals, Genetically Modified
  • Blotting, Western / methods
  • Caenorhabditis elegans
  • Cells, Cultured
  • Dopamine / metabolism*
  • Dopamine Plasma Membrane Transport Proteins
  • Genetic Testing / methods
  • Genomics / methods
  • Green Fluorescent Proteins / biosynthesis
  • Membrane Glycoproteins / biosynthesis
  • Membrane Glycoproteins / genetics*
  • Membrane Transport Proteins / biosynthesis
  • Membrane Transport Proteins / genetics*
  • Models, Molecular
  • Mutagenesis / physiology
  • Mutation*
  • Nerve Tissue Proteins / biosynthesis
  • Nerve Tissue Proteins / genetics*
  • Neurons / classification
  • Neurons / drug effects
  • Neurons / metabolism*
  • Oxidopamine / pharmacology
  • Protein Transport / genetics
  • RNA, Messenger / biosynthesis
  • Reverse Transcriptase Polymerase Chain Reaction / methods
  • Transfection / methods
  • Tritium / metabolism

Substances

  • Adrenergic Agents
  • Dopamine Plasma Membrane Transport Proteins
  • Membrane Glycoproteins
  • Membrane Transport Proteins
  • Nerve Tissue Proteins
  • RNA, Messenger
  • Tritium
  • Green Fluorescent Proteins
  • Oxidopamine
  • Dopamine