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Teneurin 2 is expressed by the neurons of the thalamofugal visual system in situ and promotes homophilic cell-cell adhesion in vitro

Beatrix P. Rubin1,*, Richard P. Tucker2,*, Marianne Brown-Luedi1, Doris Martin1 and Ruth Chiquet-Ehrismann1,{dagger}

1 Friedrich Miescher Institute, Novartis Research Foundation, PO Box 2543, CH-4002 Basel, Switzerland
2 Department of Cell Biology and Human Anatomy, University of California at Davis, Davis, CA 95616, USA
* These authors contributed equally to this work



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  		Fig. 1. Expression of teneurin 2 in the visual system. (A) Anti-teneurin 2 labels the inner plexiform layer (IPL) and optic fiber layer (OFL) of the E11 retina. (B) The staining in the OFL extends through the optic nerve head and into the optic nerve (ON). (C) At E12 anti-teneurin 2 labels the IPL and OFL, with distinctive laminae being labeled in the former. (D) An adjacent section subjected to in situ hybridization with a teneurin 2 cRNA probe reveals teneurin 2 transcripts concentrated in the retinal ganglion cell layer (GCL). Nearby sections treated with a sense control probe were unlabeled (not shown). (E) The stratum opticum (SO) of the optic tectum is stained with anti-teneurin 2 at E11. (F) The deepest layer of the optic tectum, the stratum griseum periventriculare (SGP), is also labeled with anti-teneurin 2 at E11.

 


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  		Fig. 2. Expression of teneurin 2 in the avian central nervous system. (A) Whole-mount in situ hybridization with a teneurin 2 probe at E10. The whole brain has been cut at the midline and the medial surface is being viewed. In the forebrain (left and center), the visual Wulst (W), hippocampus (Hp), lateral septal nucleus (SL) and nuclei in the dorsal thalamus (dT) are strongly labeled. In the midbrain (right), teneurin 2 transcripts are seen in the optic tectum (OT). (B) Sections through the developing Hp followed by in situ hybridization show teneurin 2 transcripts in large neurons. (C) Sections through a brain incubated with a control probe show the low level of background. (D,E) At E18, anti-teneurin 2 labels the anterior dorsolateral thalamic nucleus (DLA) and the primary target of its efferent projections, the visual Wulst (W). (F-H) The mesencephalic tract (TSM), which is formed largely from Wulst efferent fibers, and targets of the Wulst like the pretectal nucleus (PT) are also stained with anti-teneurin 2 at E18. The nucleus of Edinger-Westphal (EW), which receives input from the pretectal nucleus, expresses teneurin 2 as well. (I,J) In addition to the thalamofugal visual pathway, another non-tectal target of retinal projections [the mesencephalic lentiform nucleus (LM)] and a source of projections back to the retina [the isthmo-optic nucleus (IO)] are positive for teneurin 2 at E18. (K) The triangular nucleus (T), which rests like a cap on the rotund nucleus (ROT), expresses teneurin 2. The ROT, which is part of the tectofugal visual pathway, does not. (L-N) A major site of teneurin 2 expression at E18 is the Hp and one of the principal targets of its efferent projections, the SL. The nucleus taeniae (Tn), which projects to the teneurin 2-positive parahippocampus, is also a site of teneurin 2 expression. (O) Sections incubated with preimmune serum are unlabeled.

 


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  		Fig. 3. Expression of teneurin 2 constructs. (A) Models of the four teneurin 2 proteins encoded by the constructs used for transfection. (B) Immunoblots with anti-teneurin 2 of cell extracts of COS-7 cells transfected with constructs CTEY, TEY, CTE and TE as indicated. Lanes TEY1 and TE1 represent immunoblots with anti-teneurin 2 of cell extracts of stable cell clones of HT1080 cells selected after transfection with TEY or TE, respectively. (C) Immunostaining of COS-7 cells with anti-teneurin 2 after transfection with the constructs indicated reveals cell surface expression. Note the numerous filopodia of cells transfected with the constructs containing the cytoplasmic domains (CTEY and CTE).

 


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  		Fig. 4. The long form of the extracellular domain of teneurin 2 induces morphological changes and aggregation of transfected HT1080 cells. (A) Phase-contrast pictures of parental HT1080 cells and cell clones transfected with the membrane-anchored short extracellular domain (TE1) or cell clones expressing the long extracellular domain (TEY1, TEY2 and TEY3). Note that TEY-transfected cell clones show increased cell spreading and more cell-cell contacts. (B) Staining of the actin cytoskeleton by RITC-phalloidin of the cells shown in A reveals mostly cortical actin staining and no increased stress fiber formation even in the highly spread cells. (C) Phase-contrast pictures of cells dissociated by EDTA treatment and incubated in suspension on a rotary shaker for 1 hour. All clones expressing the long extracellular domain of teneurin 2 aggregated, whereas the parental cells and the cells expressing the short form of teneurin 2 remained as single cells.

 


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  		Fig. 5. Time course and quantitative measurement of aggregation. (A) All clones expressing the long extracellular domain of teneurin 2 aggregate rapidly reaching aggregation indices of over 40% within 30 minutes. HT1080 cells and cells expressing the short form of teneurin 2 do not aggregate over the 90-minute incubation period. This experiment was repeated five times with the same qualitative results. (B) Photographs of typical aggregates formed by Cos-7 cells after transfection of the full length teneurin 2 construct CTEY together with an EGFP construct. Green cells formed tight aggregates excluding non-transfected cells in their center (a,b), whereas the aggregates of non-transfected cells were looser and smaller and only contained occasional green cells (c,d).

 


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  		Fig. 6. Expression of teneurin 2 constructs in Nb2a neuroblastoma cells. The following constructs were transiently expressed in Nb2a cells. CTE (A,B), TE (C,D), CTEY (E,F) and TEY (G,H). In the left panel (A,C,E,G), the staining pattern of the transfected teneurin 2 as revealed by anti-teneurin 2 staining is shown and the right panel reveals the actin cytoskeleton of the same cells by phalloidin staining (B,D,F,H). In each pair of pictures, arrows or arrowheads indicate sites of teneurin 2 expression that do (A,B,E,F) or do not (C,D,G,H) overlap with the actin staining.

 


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  		Fig. 7. The primary visual pathways of the chick and patterns of teneurin expression. (A) There are two primary visual circuits in birds, the tectofugal pathway and the thalamofugal pathway. (B) Teneurin 1 is expressed by neurons in at least two of the three major parts of the tectofugal pathway (expression in the telencephalon has not been examined). Teneurin 2 is expressed by the neurons of the thalamofugal visual pathway. See text for details and abbreviations.

 

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