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PMID:27035941

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Citation

Uchigashima, M, Ohtsuka, T, Kobayashi, K and Watanabe, M (2016) Dopamine synapse is a neuroligin-2-mediated contact between dopaminergic presynaptic and GABAergic postsynaptic structures. Proc. Natl. Acad. Sci. U.S.A. 113:4206-11

Abstract

Midbrain dopamine neurons project densely to the striatum and form so-called dopamine synapses on medium spiny neurons (MSNs), principal neurons in the striatum. Because dopamine receptors are widely expressed away from dopamine synapses, it remains unclear how dopamine synapses are involved in dopaminergic transmission. Here we demonstrate that dopamine synapses are contacts formed between dopaminergic presynaptic and GABAergic postsynaptic structures. The presynaptic structure expressed tyrosine hydroxylase, vesicular monoamine transporter-2, and plasmalemmal dopamine transporter, which are essential for dopamine synthesis, vesicular filling, and recycling, but was below the detection threshold for molecules involving GABA synthesis and vesicular filling or for GABA itself. In contrast, the postsynaptic structure of dopamine synapses expressed GABAergic molecules, including postsynaptic adhesion molecule neuroligin-2, postsynaptic scaffolding molecule gephyrin, and GABAA receptor α1, without any specific clustering of dopamine receptors. Of these, neuroligin-2 promoted presynaptic differentiation in axons of midbrain dopamine neurons and striatal GABAergic neurons in culture. After neuroligin-2 knockdown in the striatum, a significant decrease of dopamine synapses coupled with a reciprocal increase of GABAergic synapses was observed on MSN dendrites. This finding suggests that neuroligin-2 controls striatal synapse formation by giving competitive advantage to heterologous dopamine synapses over conventional GABAergic synapses. Considering that MSN dendrites are preferential targets of dopamine synapses and express high levels of dopamine receptors, dopamine synapse formation may serve to increase the specificity and potency of dopaminergic modulation of striatal outputs by anchoring dopamine release sites to dopamine-sensing targets.

Links

PubMed PMC4839454 Online version:10.1073/pnas.1514074113

Keywords

Animals; Cell Adhesion Molecules, Neuronal/metabolism; Dopamine/metabolism; Mice; Mice, Knockout; Nerve Tissue Proteins/metabolism; Synapses/metabolism; gamma-Aminobutyric Acid/metabolism

Significance

Annotations

Gene product Qualifier GO Term Evidence Code with/from Aspect Extension Notes Status

MOUSE:DRD2

part_of

GO:0098982: GABA-ergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD2

part_of

GO:0098978: glutamatergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD2

part_of

GO:0099055: integral component of postsynaptic membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:DRD2

part_of

GO:0099056: integral component of presynaptic membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:DRD1

part_of

GO:0098982: GABA-ergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD1

part_of

GO:0098978: glutamatergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD1

part_of

GO:0099055: integral component of postsynaptic membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:DRD1

part_of

GO:0099056: integral component of presynaptic membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NLGN2

part_of

GO:0099060: integral component of postsynaptic specialization membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

Seeded From UniProt

complete

MOUSE:NLGN2

part_of

GO:0098691: dopaminergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD2

part_of

GO:0098978: glutamatergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0000061)
  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD2

part_of

GO:0099055: integral component of postsynaptic membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(GO:0098978)
  • part_of:(UBERON:0000061)
  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD2

part_of

GO:0099056: integral component of presynaptic membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(GO:0098982)
  • part_of:(UBERON:0000061)
  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:DRD2

part_of

GO:0098982: GABA-ergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0000061)
  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:NLGN2

part_of

GO:0098691: dopaminergic synapse

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(UBERON:0000061)
  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

MOUSE:NLGN2

part_of

GO:0099060: integral component of postsynaptic specialization membrane

ECO:0006003: electron microscopy evidence used in manual assertion

C

  • part_of:(GO:0098691)
  • part_of:(UBERON:0000061)
  • part_of:(UBERON:0002435)

Seeded From UniProt

complete

Notes

See also

References

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