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Teneurin-1 is expressed in interconnected regions of the developing brain and is processed in vivo.

Kenzelmann D, Chiquet-Ehrismann R, Leachman NT, Tucker RP - BMC Dev. Biol. (2008)

Bottom Line: Moreover we found complementary patterns of teneurin-1 and-2 expression in many parts of the brain, including the retina, optic tectum, olfactory bulb, and cerebellum as well as in brain nuclei involved in processing of sensory information.Finally, the teneurin-1 intracellular domain was found to contain a nuclear localization signal, which is required for nuclear localization in transfected cells.Our data support the hypothesis that teneurins can be proteolytically processed leading to the release of the intracellular domain and its translocation to the nucleus.

View Article: PubMed Central - HTML - PubMed

Affiliation: Friedrich Miescher Institute, Novartis Research Foundation, Maulbeerstr. 66, 4057 Basel, Switzerland. daniela.kenzelmann@fmi.ch

ABSTRACT

Background: Teneurins are a unique family of transmembrane proteins conserved from C. elegans and D. melanogaster to mammals. In vertebrates there are four paralogs (teneurin-1 to -4), all of which are expressed prominently in the developing central nervous system.

Results: Analysis of teneurin-1 expression in the developing chick brain by in situ hybridization and immunohistochemistry defined a unique, distinct expression pattern in interconnected regions of the brain. Moreover we found complementary patterns of teneurin-1 and-2 expression in many parts of the brain, including the retina, optic tectum, olfactory bulb, and cerebellum as well as in brain nuclei involved in processing of sensory information. Based on these expression patterns, we suspect a role for teneurins in neuronal connectivity. In contrast to the cell-surface staining of the antibody against the extracellular domain, an antibody recognizing the intracellular domain revealed nuclear staining in subpopulations of neurons and in undifferentiated mesenchyme. Western blot analysis of brain lysates showed the presence of N-terminal fragments of teneurin-1 containing the intracellular domain indicating that proteolytic processing occurs. Finally, the teneurin-1 intracellular domain was found to contain a nuclear localization signal, which is required for nuclear localization in transfected cells.

Conclusion: Teneurin-1 and -2 are expressed by distinct interconnected populations of neurons in the developing central nervous system. Our data support the hypothesis that teneurins can be proteolytically processed leading to the release of the intracellular domain and its translocation to the nucleus.

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Nuclear teneurin-1 intracellular domain is observed in subsets of neurons and in specific tissues. Schematic diagram of teneurin domain architecture and antibodies used in this study (A). Comparison of immunostaining with antibodies to the extracellular and intracellular domains in sections and in vitro (B to I). Neurons of the piriform cortex at E17 (B, C) and neurons found in the retinal ganglion cell layer at E12 (D, E) stained with anti-ICD. The anti-ICD labels nuclei in the piriform cortex and labels a subset of retinal ganglion cells (arrow), but other TuJ1-positive neurons (label not shown) in the retinal ganglion cell layer are labeled with anti-ICD teneurin-1 but do not exhibit nuclear staining (arrowhead). There are also TuJ1-positive neurons in the retinal ganglion cell layer that are negative for teneurin-1 (asterisk). Head mesenchyme at E7 stained with anti-EGF (F, G) and anti-ICD (H, I). In the head mesenchyme, the anti-ICD labels the nucleus of most cells, whereas the anti-EGF exhibits cell-surface staining. Green, teneurin-1; blue (Hoechst), nuclei.
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Figure 3: Nuclear teneurin-1 intracellular domain is observed in subsets of neurons and in specific tissues. Schematic diagram of teneurin domain architecture and antibodies used in this study (A). Comparison of immunostaining with antibodies to the extracellular and intracellular domains in sections and in vitro (B to I). Neurons of the piriform cortex at E17 (B, C) and neurons found in the retinal ganglion cell layer at E12 (D, E) stained with anti-ICD. The anti-ICD labels nuclei in the piriform cortex and labels a subset of retinal ganglion cells (arrow), but other TuJ1-positive neurons (label not shown) in the retinal ganglion cell layer are labeled with anti-ICD teneurin-1 but do not exhibit nuclear staining (arrowhead). There are also TuJ1-positive neurons in the retinal ganglion cell layer that are negative for teneurin-1 (asterisk). Head mesenchyme at E7 stained with anti-EGF (F, G) and anti-ICD (H, I). In the head mesenchyme, the anti-ICD labels the nucleus of most cells, whereas the anti-EGF exhibits cell-surface staining. Green, teneurin-1; blue (Hoechst), nuclei.

Mentions: Antibodies detecting the ICD (anti-ICD) or the ECD (anti-EGF and anti-ECD, see Fig. 3A) of teneurin-1 were used to detect teneurin-1 expression in brain homogenates harvested from chicken embryos.


Teneurin-1 is expressed in interconnected regions of the developing brain and is processed in vivo.

Kenzelmann D, Chiquet-Ehrismann R, Leachman NT, Tucker RP - BMC Dev. Biol. (2008)

Nuclear teneurin-1 intracellular domain is observed in subsets of neurons and in specific tissues. Schematic diagram of teneurin domain architecture and antibodies used in this study (A). Comparison of immunostaining with antibodies to the extracellular and intracellular domains in sections and in vitro (B to I). Neurons of the piriform cortex at E17 (B, C) and neurons found in the retinal ganglion cell layer at E12 (D, E) stained with anti-ICD. The anti-ICD labels nuclei in the piriform cortex and labels a subset of retinal ganglion cells (arrow), but other TuJ1-positive neurons (label not shown) in the retinal ganglion cell layer are labeled with anti-ICD teneurin-1 but do not exhibit nuclear staining (arrowhead). There are also TuJ1-positive neurons in the retinal ganglion cell layer that are negative for teneurin-1 (asterisk). Head mesenchyme at E7 stained with anti-EGF (F, G) and anti-ICD (H, I). In the head mesenchyme, the anti-ICD labels the nucleus of most cells, whereas the anti-EGF exhibits cell-surface staining. Green, teneurin-1; blue (Hoechst), nuclei.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2289808&req=5

Figure 3: Nuclear teneurin-1 intracellular domain is observed in subsets of neurons and in specific tissues. Schematic diagram of teneurin domain architecture and antibodies used in this study (A). Comparison of immunostaining with antibodies to the extracellular and intracellular domains in sections and in vitro (B to I). Neurons of the piriform cortex at E17 (B, C) and neurons found in the retinal ganglion cell layer at E12 (D, E) stained with anti-ICD. The anti-ICD labels nuclei in the piriform cortex and labels a subset of retinal ganglion cells (arrow), but other TuJ1-positive neurons (label not shown) in the retinal ganglion cell layer are labeled with anti-ICD teneurin-1 but do not exhibit nuclear staining (arrowhead). There are also TuJ1-positive neurons in the retinal ganglion cell layer that are negative for teneurin-1 (asterisk). Head mesenchyme at E7 stained with anti-EGF (F, G) and anti-ICD (H, I). In the head mesenchyme, the anti-ICD labels the nucleus of most cells, whereas the anti-EGF exhibits cell-surface staining. Green, teneurin-1; blue (Hoechst), nuclei.
Mentions: Antibodies detecting the ICD (anti-ICD) or the ECD (anti-EGF and anti-ECD, see Fig. 3A) of teneurin-1 were used to detect teneurin-1 expression in brain homogenates harvested from chicken embryos.

Bottom Line: Moreover we found complementary patterns of teneurin-1 and-2 expression in many parts of the brain, including the retina, optic tectum, olfactory bulb, and cerebellum as well as in brain nuclei involved in processing of sensory information.Finally, the teneurin-1 intracellular domain was found to contain a nuclear localization signal, which is required for nuclear localization in transfected cells.Our data support the hypothesis that teneurins can be proteolytically processed leading to the release of the intracellular domain and its translocation to the nucleus.

View Article: PubMed Central - HTML - PubMed

Affiliation: Friedrich Miescher Institute, Novartis Research Foundation, Maulbeerstr. 66, 4057 Basel, Switzerland. daniela.kenzelmann@fmi.ch

ABSTRACT

Background: Teneurins are a unique family of transmembrane proteins conserved from C. elegans and D. melanogaster to mammals. In vertebrates there are four paralogs (teneurin-1 to -4), all of which are expressed prominently in the developing central nervous system.

Results: Analysis of teneurin-1 expression in the developing chick brain by in situ hybridization and immunohistochemistry defined a unique, distinct expression pattern in interconnected regions of the brain. Moreover we found complementary patterns of teneurin-1 and-2 expression in many parts of the brain, including the retina, optic tectum, olfactory bulb, and cerebellum as well as in brain nuclei involved in processing of sensory information. Based on these expression patterns, we suspect a role for teneurins in neuronal connectivity. In contrast to the cell-surface staining of the antibody against the extracellular domain, an antibody recognizing the intracellular domain revealed nuclear staining in subpopulations of neurons and in undifferentiated mesenchyme. Western blot analysis of brain lysates showed the presence of N-terminal fragments of teneurin-1 containing the intracellular domain indicating that proteolytic processing occurs. Finally, the teneurin-1 intracellular domain was found to contain a nuclear localization signal, which is required for nuclear localization in transfected cells.

Conclusion: Teneurin-1 and -2 are expressed by distinct interconnected populations of neurons in the developing central nervous system. Our data support the hypothesis that teneurins can be proteolytically processed leading to the release of the intracellular domain and its translocation to the nucleus.

Show MeSH
Related in: MedlinePlus