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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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Teneurin-1 is expressed in many parts of the developing CNS. In situ hybridization at E17 with a teneurin-1 antisense probe (sense controls were negative). In the olfactory bulb (A), there is a strong hybridization signal in the mitral cell layer (mcl). The ganglion cell layer (gcl) is also positive, but the external plexiform layer (epl) is not. In the retina (B), the ganglion cell layer (gcl) is labelled intensely, and there is a faint signal in neurons of the inner nuclear layer (inl) adjacent to the inner plexiform layer (ipl). The pigment retina (pr) has dark melanosomes. The nucleus rotundus (C) contains large, scattered neurons that are positive for teneurin-1 mRNA. In the optic tectum (D) teneurin-1 mRNA is widespread, but is seen most clearly in the large neurons of the stratum griseum centrale (sgc). In the hindbrain (E) the nucleus laminaris (La) and nucleus magnocellularis (MCC) are labelled, as are Purkinje cells (Pcl) and other neurons in the cerebellum (F).
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Figure 1: Teneurin-1 is expressed in many parts of the developing CNS. In situ hybridization at E17 with a teneurin-1 antisense probe (sense controls were negative). In the olfactory bulb (A), there is a strong hybridization signal in the mitral cell layer (mcl). The ganglion cell layer (gcl) is also positive, but the external plexiform layer (epl) is not. In the retina (B), the ganglion cell layer (gcl) is labelled intensely, and there is a faint signal in neurons of the inner nuclear layer (inl) adjacent to the inner plexiform layer (ipl). The pigment retina (pr) has dark melanosomes. The nucleus rotundus (C) contains large, scattered neurons that are positive for teneurin-1 mRNA. In the optic tectum (D) teneurin-1 mRNA is widespread, but is seen most clearly in the large neurons of the stratum griseum centrale (sgc). In the hindbrain (E) the nucleus laminaris (La) and nucleus magnocellularis (MCC) are labelled, as are Purkinje cells (Pcl) and other neurons in the cerebellum (F).

Mentions: Teneurin-1 was widely expressed in the chick nervous system at embryonic day (E) 17. The strongest hybridization signals seen with the teneurin-1 antisense probe were in the mitral cells of the olfactory bulb (Fig. 1A), subpopulations of neurons in the hippocampus and piriform cortex (not shown, but see immunohistochemistry), retinal ganglion cells and cells found in the inner nuclear layer adjacent to the inner plexiform layer (Fig. 1B), the large neurons found within the rotund nucleus (Fig. 1C), and the neurons of the stratum griseum centrale of the optic tectum (Fig. 1D). In the hindbrain teneurin-1 mRNAs were found in the nucleus laminaris and nucleus magnocellularis (Fig. 1E) and throughout the cerebellum (Fig. 1F). Adjacent sections processed with a sense probe were unlabelled. Thus, the expression of teneurin-1 in the chicken embryo is more widespread than suggested by our earlier studies using a less sensitive radiolabeled probe that only detected the most abundant sites of expression in the visual system. In addition to the strong expression in interconnected subset of neurons in the tectofugal portions of the visual system (e.g., retinal ganglion cells, the stratum griseum centrale of the optic tectum and the rotund nucleus), teneurin-1 transcripts were also present in diverse brain regions involved in general sensation, olfaction, the processing of auditory information, and the coordination of complex motor behavior.


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)

Teneurin-1 is expressed in many parts of the developing CNS. In situ hybridization at E17 with a teneurin-1 antisense probe (sense controls were negative). In the olfactory bulb (A), there is a strong hybridization signal in the mitral cell layer (mcl). The ganglion cell layer (gcl) is also positive, but the external plexiform layer (epl) is not. In the retina (B), the ganglion cell layer (gcl) is labelled intensely, and there is a faint signal in neurons of the inner nuclear layer (inl) adjacent to the inner plexiform layer (ipl). The pigment retina (pr) has dark melanosomes. The nucleus rotundus (C) contains large, scattered neurons that are positive for teneurin-1 mRNA. In the optic tectum (D) teneurin-1 mRNA is widespread, but is seen most clearly in the large neurons of the stratum griseum centrale (sgc). In the hindbrain (E) the nucleus laminaris (La) and nucleus magnocellularis (MCC) are labelled, as are Purkinje cells (Pcl) and other neurons in the cerebellum (F).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC2289808&req=5

Figure 1: Teneurin-1 is expressed in many parts of the developing CNS. In situ hybridization at E17 with a teneurin-1 antisense probe (sense controls were negative). In the olfactory bulb (A), there is a strong hybridization signal in the mitral cell layer (mcl). The ganglion cell layer (gcl) is also positive, but the external plexiform layer (epl) is not. In the retina (B), the ganglion cell layer (gcl) is labelled intensely, and there is a faint signal in neurons of the inner nuclear layer (inl) adjacent to the inner plexiform layer (ipl). The pigment retina (pr) has dark melanosomes. The nucleus rotundus (C) contains large, scattered neurons that are positive for teneurin-1 mRNA. In the optic tectum (D) teneurin-1 mRNA is widespread, but is seen most clearly in the large neurons of the stratum griseum centrale (sgc). In the hindbrain (E) the nucleus laminaris (La) and nucleus magnocellularis (MCC) are labelled, as are Purkinje cells (Pcl) and other neurons in the cerebellum (F).
Mentions: Teneurin-1 was widely expressed in the chick nervous system at embryonic day (E) 17. The strongest hybridization signals seen with the teneurin-1 antisense probe were in the mitral cells of the olfactory bulb (Fig. 1A), subpopulations of neurons in the hippocampus and piriform cortex (not shown, but see immunohistochemistry), retinal ganglion cells and cells found in the inner nuclear layer adjacent to the inner plexiform layer (Fig. 1B), the large neurons found within the rotund nucleus (Fig. 1C), and the neurons of the stratum griseum centrale of the optic tectum (Fig. 1D). In the hindbrain teneurin-1 mRNAs were found in the nucleus laminaris and nucleus magnocellularis (Fig. 1E) and throughout the cerebellum (Fig. 1F). Adjacent sections processed with a sense probe were unlabelled. Thus, the expression of teneurin-1 in the chicken embryo is more widespread than suggested by our earlier studies using a less sensitive radiolabeled probe that only detected the most abundant sites of expression in the visual system. In addition to the strong expression in interconnected subset of neurons in the tectofugal portions of the visual system (e.g., retinal ganglion cells, the stratum griseum centrale of the optic tectum and the rotund nucleus), teneurin-1 transcripts were also present in diverse brain regions involved in general sensation, olfaction, the processing of auditory information, and the coordination of complex motor behavior.

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