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Research Articles, Cellular/Molecular

Retinal Detachment-Induced Müller Glial Cell Swelling Activates TRPV4 Ion Channels and Triggers Photoreceptor Death at Body Temperature

Hidetaka Matsumoto, Shouta Sugio, François Seghers, David Krizaj, Hideo Akiyama, Yasuki Ishizaki, Philippe Gailly and Koji Shibasaki
Journal of Neuroscience 10 October 2018, 38 (41) 8745-8758; DOI: https://doi.org/10.1523/JNEUROSCI.0897-18.2018
Hidetaka Matsumoto
1Departments of Ophthalmology,
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Shouta Sugio
2Molecular and Cellular Neurobiology, Gunma University Graduate School of Medicine, Maebashi 371-8511, Japan,
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François Seghers
3Laboratory of Cell Physiology, Institute of Neuroscience, Université catholique de Louvain, B-1200 Brussels, Belgium, and
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David Krizaj
4Department of Ophthalmology and Visual Sciences, Moran Eye Institute, University of Utah School of Medicine, Salt Lake City, Utah 84132
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Hideo Akiyama
1Departments of Ophthalmology,
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Yasuki Ishizaki
2Molecular and Cellular Neurobiology, Gunma University Graduate School of Medicine, Maebashi 371-8511, Japan,
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Philippe Gailly
3Laboratory of Cell Physiology, Institute of Neuroscience, Université catholique de Louvain, B-1200 Brussels, Belgium, and
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Koji Shibasaki
2Molecular and Cellular Neurobiology, Gunma University Graduate School of Medicine, Maebashi 371-8511, Japan,
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Abstract

Using region-specific injection of hyaluronic acid, we developed a mouse model of acute retinal detachment (RD) to investigate molecular mechanisms of photoreceptor cell death triggered by RD. We focused on the transient receptor potential vanilloid 4 (TRPV4) ion channel, which functions as a thermosensor, osmosensor, and/or mechanosensor. After RD, the number of apoptotic photoreceptors was reduced by ∼50% in TRPV4KO mice relative to wild-type mice, indicating the possible involvement of TRPV4 activation in RD-induced photoreceptor cell death. Furthermore, TRPV4 expressed in Müller glial cells can be activated by mechanical stimuli caused by RD-induced swelling of these cells, resulting in release of the cytokine MCP-1, which is reported as a mediator of Müller glia-derived strong mediator for RD-induced photoreceptor death. We also found that the TRPV4 activation by the Müller glial swelling was potentiated by body temperature. Together, our results suggest that RD adversely impacts photoreceptor viability via TRPV4-dependent cytokine release from Müller glial cells and that TRPV4 is part of a novel molecular pathway that could exacerbate the effects of hypoxia on photoreceptor survival after RD.

SIGNIFICANCE STATEMENT Identification of the mechanisms of photoreceptor death in retinal detachment is required for establishment of therapeutic targets for preventing loss of visual acuity. In this study, we found that TRPV4 expressed in Müller glial cells can be activated by mechanical stimuli caused by RD-induced swelling of these cells, resulting in release of the cytokine MCP-1, which is reported as a mediator of Müller glia-derived strong mediator for RD-induced photoreceptor death. We also found that the TRPV4 activation by the Müller glial swelling was potentiated by body temperature. Hence, TRPV4 inhibition could suppress cell death in RD pathological conditions and suggests that TRPV4 in Müller glial cells might be a novel therapeutic target for preventing photoreceptor cell death after RD.

  • glia
  • mechanical stimulus
  • retina
  • swelling
  • temperature
  • TRPV4

This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The Journal of Neuroscience: 38 (41)
Journal of Neuroscience
Vol. 38, Issue 41
10 Oct 2018
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Retinal Detachment-Induced Müller Glial Cell Swelling Activates TRPV4 Ion Channels and Triggers Photoreceptor Death at Body Temperature
Hidetaka Matsumoto, Shouta Sugio, François Seghers, David Krizaj, Hideo Akiyama, Yasuki Ishizaki, Philippe Gailly, Koji Shibasaki
Journal of Neuroscience 10 October 2018, 38 (41) 8745-8758; DOI: 10.1523/JNEUROSCI.0897-18.2018

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Retinal Detachment-Induced Müller Glial Cell Swelling Activates TRPV4 Ion Channels and Triggers Photoreceptor Death at Body Temperature
Hidetaka Matsumoto, Shouta Sugio, François Seghers, David Krizaj, Hideo Akiyama, Yasuki Ishizaki, Philippe Gailly, Koji Shibasaki
Journal of Neuroscience 10 October 2018, 38 (41) 8745-8758; DOI: 10.1523/JNEUROSCI.0897-18.2018
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Keywords

  • glia
  • mechanical stimulus
  • retina
  • swelling
  • temperature
  • TRPV4

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