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Teneurins instruct synaptic partner matching in an olfactory map.

Hong W, Mosca TJ, Luo L - Nature (2012)

Bottom Line: 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.We propose that Teneurins instruct matching specificity between synaptic partners through homophilic attraction.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, California 94305, USA.

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.

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Teneurins are differentially expressed in matching PN and ORN classesa, Developing antennal lobes at 48 hrs APF stained by antibodies against Ten-m, Ten-a, and a neuropil marker, N-cadherin. Solid lines encircle the DA1 glomerulus (Ten-m low, Ten-a high). Dashed lines encircle the VA1d/VA1lm glomeruli (Ten-m high, Ten-a low). b-c, Ten-m and Ten-a proteins are undetectable following pan-neuronal RNAi of ten-m (b) and ten-a (c), respectively. d, A ten-a homozygous mutant eliminated the Ten-a antibody staining. e, Summary of elevated Ten-m and Ten-a expression in five select glomeruli. f-g, Expression of the Flp-out GFP reporter UAS>stop>mCD8GFP at the intersection of ten-m-GAL4 with ORN-specific ey-Flp (f) or with PN-specific GH146-Flp (g) in adult. h-i, Antibody staining of Ten-a in central neuron-specific RNAi (h) or in ORN-specific RNAi (i) at 48 hrs APF. Individual cell type-specific Teneurin expression patterns are schematically summarized at right (f-i). j, Combined expression patterns of Teneurins in PNs (left) and ORNs (right). Blue: Ten-m high; orange: Ten-a high.
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Figure 2: Teneurins are differentially expressed in matching PN and ORN classesa, Developing antennal lobes at 48 hrs APF stained by antibodies against Ten-m, Ten-a, and a neuropil marker, N-cadherin. Solid lines encircle the DA1 glomerulus (Ten-m low, Ten-a high). Dashed lines encircle the VA1d/VA1lm glomeruli (Ten-m high, Ten-a low). b-c, Ten-m and Ten-a proteins are undetectable following pan-neuronal RNAi of ten-m (b) and ten-a (c), respectively. d, A ten-a homozygous mutant eliminated the Ten-a antibody staining. e, Summary of elevated Ten-m and Ten-a expression in five select glomeruli. f-g, Expression of the Flp-out GFP reporter UAS>stop>mCD8GFP at the intersection of ten-m-GAL4 with ORN-specific ey-Flp (f) or with PN-specific GH146-Flp (g) in adult. h-i, Antibody staining of Ten-a in central neuron-specific RNAi (h) or in ORN-specific RNAi (i) at 48 hrs APF. Individual cell type-specific Teneurin expression patterns are schematically summarized at right (f-i). j, Combined expression patterns of Teneurins in PNs (left) and ORNs (right). Blue: Ten-m high; orange: Ten-a high.

Mentions: Both Drosophila Teneurins were endogenously expressed in the developing antennal lobe (Fig. 2a, S3). At 48 hrs after puparium formation (APF), when individual glomeruli just become identifiable, elevated Teneurin expression was evident in select glomeruli. The subset of glomeruli expressing elevated Ten-m was distinct but partially overlapping with that expressing elevated Ten-a (Fig. 2a,e). Teneurins were also detected at a low level in all glomeruli. Both basal and elevated Teneurin expressions were eliminated by pan-neuronal RNAi targeting the corresponding gene (Fig. 2b,c), suggesting that Teneurins are produced predominantly by neurons. In a ten-a mutant we generated (Fig. S2a), all Ten-a expression was eliminated, confirming antibody specificity (Fig. 2d).


Teneurins instruct synaptic partner matching in an olfactory map.

Hong W, Mosca TJ, Luo L - Nature (2012)

Teneurins are differentially expressed in matching PN and ORN classesa, Developing antennal lobes at 48 hrs APF stained by antibodies against Ten-m, Ten-a, and a neuropil marker, N-cadherin. Solid lines encircle the DA1 glomerulus (Ten-m low, Ten-a high). Dashed lines encircle the VA1d/VA1lm glomeruli (Ten-m high, Ten-a low). b-c, Ten-m and Ten-a proteins are undetectable following pan-neuronal RNAi of ten-m (b) and ten-a (c), respectively. d, A ten-a homozygous mutant eliminated the Ten-a antibody staining. e, Summary of elevated Ten-m and Ten-a expression in five select glomeruli. f-g, Expression of the Flp-out GFP reporter UAS>stop>mCD8GFP at the intersection of ten-m-GAL4 with ORN-specific ey-Flp (f) or with PN-specific GH146-Flp (g) in adult. h-i, Antibody staining of Ten-a in central neuron-specific RNAi (h) or in ORN-specific RNAi (i) at 48 hrs APF. Individual cell type-specific Teneurin expression patterns are schematically summarized at right (f-i). j, Combined expression patterns of Teneurins in PNs (left) and ORNs (right). Blue: Ten-m high; orange: Ten-a high.
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Related In: Results  -  Collection

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Figure 2: Teneurins are differentially expressed in matching PN and ORN classesa, Developing antennal lobes at 48 hrs APF stained by antibodies against Ten-m, Ten-a, and a neuropil marker, N-cadherin. Solid lines encircle the DA1 glomerulus (Ten-m low, Ten-a high). Dashed lines encircle the VA1d/VA1lm glomeruli (Ten-m high, Ten-a low). b-c, Ten-m and Ten-a proteins are undetectable following pan-neuronal RNAi of ten-m (b) and ten-a (c), respectively. d, A ten-a homozygous mutant eliminated the Ten-a antibody staining. e, Summary of elevated Ten-m and Ten-a expression in five select glomeruli. f-g, Expression of the Flp-out GFP reporter UAS>stop>mCD8GFP at the intersection of ten-m-GAL4 with ORN-specific ey-Flp (f) or with PN-specific GH146-Flp (g) in adult. h-i, Antibody staining of Ten-a in central neuron-specific RNAi (h) or in ORN-specific RNAi (i) at 48 hrs APF. Individual cell type-specific Teneurin expression patterns are schematically summarized at right (f-i). j, Combined expression patterns of Teneurins in PNs (left) and ORNs (right). Blue: Ten-m high; orange: Ten-a high.
Mentions: Both Drosophila Teneurins were endogenously expressed in the developing antennal lobe (Fig. 2a, S3). At 48 hrs after puparium formation (APF), when individual glomeruli just become identifiable, elevated Teneurin expression was evident in select glomeruli. The subset of glomeruli expressing elevated Ten-m was distinct but partially overlapping with that expressing elevated Ten-a (Fig. 2a,e). Teneurins were also detected at a low level in all glomeruli. Both basal and elevated Teneurin expressions were eliminated by pan-neuronal RNAi targeting the corresponding gene (Fig. 2b,c), suggesting that Teneurins are produced predominantly by neurons. In a ten-a mutant we generated (Fig. S2a), all Ten-a expression was eliminated, confirming antibody specificity (Fig. 2d).

Bottom Line: 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.We propose that Teneurins instruct matching specificity between synaptic partners through homophilic attraction.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, California 94305, USA.

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.

Show MeSH
Related in: MedlinePlus