Teneurins instruct synaptic partner matching in an olfactory map

Nature. 2012 Mar 18;484(7393):201-7. doi: 10.1038/nature10926.

Abstract

Neurons are interconnected with extraordinary precision to assemble a functional nervous system. Compared to axon guidance, far less is understood about how individual pre- and postsynaptic partners are matched. To ensure the proper relay of olfactory information in the fruitfly Drosophila, axons of ∼50 classes of olfactory receptor neurons (ORNs) form one-to-one connections with dendrites of ∼50 classes of projection neurons (PNs). Here, using genetic screens, we identified two evolutionarily conserved, epidermal growth factor (EGF)-repeat containing transmembrane Teneurin proteins, Ten-m and Ten-a, as synaptic-partner-matching molecules between PN dendrites and ORN axons. Ten-m and Ten-a are highly expressed in select PN-ORN matching pairs. Teneurin loss- and gain-of-function cause specific mismatching of select ORNs and PNs. Finally, Teneurins promote homophilic interactions in vitro, and Ten-m co-expression in non-partner PNs and ORNs promotes their ectopic connections in vivo. We propose that Teneurins instruct matching specificity between synaptic partners through homophilic attraction.

Publication types

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

MeSH terms

  • Animals
  • Axons / metabolism
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / metabolism*
  • Olfactory Pathways / physiology*
  • Olfactory Receptor Neurons / metabolism
  • Protein Binding
  • RNA Interference
  • Receptors, Cell Surface / metabolism*
  • Smell / physiology
  • Synapses / metabolism*
  • Tenascin / metabolism*

Substances

  • Drosophila Proteins
  • Receptors, Cell Surface
  • Ten-a protein, Drosophila
  • Ten-m protein, Drosophila
  • Tenascin