Characterization of neurite outgrowth and ectopic synaptogenesis in response to photoreceptor dysfunction View Full Text


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Article Info

DATE

2012-12-27

AUTHORS

Stylianos Michalakis, Karin Schäferhoff, Isabella Spiwoks-Becker, Nawal Zabouri, Susanne Koch, Fred Koch, Michael Bonin, Martin Biel, Silke Haverkamp

ABSTRACT

In the mammalian retina, light signals generated in photoreceptors are passed to bipolar and horizontal cells via synaptic contacts. In various pathological conditions, these second-order neurons extend neurites into the outer nuclear layer (ONL). However, the molecular events associated with this neurite outgrowth are not known. Here, we characterized the morphological synaptic changes in the CNGA3/CNGB1 double-knockout (A3B1) mouse, a model of retinitis pigmentosa. In these mice, horizontal cells looked normal until postnatal day (p) 11, but started growing neurites into the ONL 1 day later. At p28, the number of sprouting processes decreased, but the remaining sprouts developed synapse-like contacts at rod cell bodies, with an ultrastructural appearance reminiscent of ribbon synapses. Hence, neurite outgrowth and ectopic synaptogenesis in the A3B1 retina were precisely timed events starting at p12 and p28, respectively. We therefore performed microarray analysis of retinal gene expression in A3B1 and wild-type mice at those ages to evaluate the genomic response underlying these two events. This analysis identified 163 differentially regulated genes in the A3B1 retina related to neurite outgrowth or plasticity of synapses. The global changes in gene expression in the A3B1 retina were consistent with activation of signaling pathways related to Tp53, Smad, and Stat3. Moreover, key molecules of these signaling pathways could be localized at or in close proximity to outgrowing neurites. We therefore propose that Tp53, Smad, and Stat3 signaling pathways contribute to the synaptic plasticity in the A3B1 retina. More... »

PAGES

1831-1847

References to SciGraph publications

  • 2004-09-26. Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function in NATURE NEUROSCIENCE
  • 2008-11-23. Bidirectional modulation of synaptic functions by Eph/ephrin signaling in NATURE NEUROSCIENCE
  • 2004-10. Parallel processing in the mammalian retina in NATURE REVIEWS NEUROSCIENCE
  • 2011-08-25. Schizophrenia as a disorder of disconnectivity in EUROPEAN ARCHIVES OF PSYCHIATRY AND CLINICAL NEUROSCIENCE
  • 2012-01-22. p53-dependent pathways in neurite outgrowth and axonal regeneration in CELL AND TISSUE RESEARCH
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1007/s00018-012-1230-z

    DOI

    http://dx.doi.org/10.1007/s00018-012-1230-z

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1028413005

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/23269435


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    33 schema:description In the mammalian retina, light signals generated in photoreceptors are passed to bipolar and horizontal cells via synaptic contacts. In various pathological conditions, these second-order neurons extend neurites into the outer nuclear layer (ONL). However, the molecular events associated with this neurite outgrowth are not known. Here, we characterized the morphological synaptic changes in the CNGA3/CNGB1 double-knockout (A3B1) mouse, a model of retinitis pigmentosa. In these mice, horizontal cells looked normal until postnatal day (p) 11, but started growing neurites into the ONL 1 day later. At p28, the number of sprouting processes decreased, but the remaining sprouts developed synapse-like contacts at rod cell bodies, with an ultrastructural appearance reminiscent of ribbon synapses. Hence, neurite outgrowth and ectopic synaptogenesis in the A3B1 retina were precisely timed events starting at p12 and p28, respectively. We therefore performed microarray analysis of retinal gene expression in A3B1 and wild-type mice at those ages to evaluate the genomic response underlying these two events. This analysis identified 163 differentially regulated genes in the A3B1 retina related to neurite outgrowth or plasticity of synapses. The global changes in gene expression in the A3B1 retina were consistent with activation of signaling pathways related to Tp53, Smad, and Stat3. Moreover, key molecules of these signaling pathways could be localized at or in close proximity to outgrowing neurites. We therefore propose that Tp53, Smad, and Stat3 signaling pathways contribute to the synaptic plasticity in the A3B1 retina.
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