Red‐shifted channelrhodopsin stimulation restores light responses in blind mice, macaque retina, and human retina
Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin‐2 exceeds the safety thresho...
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| Published in | EMBO molecular medicine Vol. 8; no. 11; pp. 1248 - 1264 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.11.2016
EMBO Press Wiley Open Access John Wiley and Sons Inc Springer Nature |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin‐2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red‐shifted light is vastly lower than that of blue light. Here, we show that a red‐shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind
rd1
mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV‐ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV‐ and lentivirus‐mediated optogenetic spike responses in ganglion cells of the postmortem human retina.
Synopsis
A red‐shifted channelrhodopsin (ReaChR) was targeted to retinal ganglion cells using three models in parallel: mouse, macaque, and human. Safe orange illumination was able to trigger light responses in all three systems.
The red‐shifted channelrhodopsin ReaChR restored light responses at the retinal, cortical, and behavioral levels in blind
rd1
mice, using light intensities below the safety limit for the human retina.
Optogenetic light responses were demonstrated in explanted postmortem macaque and human retina, infected
ex vivo
with viral vectors encoding ReaChR.
The study presents the first electrophysiological recordings of optogenetic light responses in ganglion cells obtained directly from the human fovea as well as the far peripheral human retina.
Graphical Abstract
A red‐shifted channelrhodopsin (ReaChR) was targeted to retinal ganglion cells using three models in parallel: mouse, macaque, and human. Safe orange illumination was able to trigger light responses in all three systems. |
|---|---|
| AbstractList | Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin‐2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red‐shifted light is vastly lower than that of blue light. Here, we show that a red‐shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV‐ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV‐ and lentivirus‐mediated optogenetic spike responses in ganglion cells of the postmortem human retina.
Synopsis
A red‐shifted channelrhodopsin (ReaChR) was targeted to retinal ganglion cells using three models in parallel: mouse, macaque, and human. Safe orange illumination was able to trigger light responses in all three systems.
The red‐shifted channelrhodopsin ReaChR restored light responses at the retinal, cortical, and behavioral levels in blind rd1 mice, using light intensities below the safety limit for the human retina.
Optogenetic light responses were demonstrated in explanted postmortem macaque and human retina, infected ex vivo with viral vectors encoding ReaChR.
The study presents the first electrophysiological recordings of optogenetic light responses in ganglion cells obtained directly from the human fovea as well as the far peripheral human retina.
A red‐shifted channelrhodopsin (ReaChR) was targeted to retinal ganglion cells using three models in parallel: mouse, macaque, and human. Safe orange illumination was able to trigger light responses in all three systems. Targeting the photosensitive ion channel channelrhodopsin-2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin-2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red-shifted light is vastly lower than that of blue light. Here, we show that a red-shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV-ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV- and lentivirus-mediated optogenetic spike responses in ganglion cells of the postmortem human retina.Targeting the photosensitive ion channel channelrhodopsin-2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin-2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red-shifted light is vastly lower than that of blue light. Here, we show that a red-shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV-ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV- and lentivirus-mediated optogenetic spike responses in ganglion cells of the postmortem human retina. Targeting the photosensitive ion channel channelrhodopsin-2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin-2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red-shifted light is vastly lower than that of blue light. Here, we show that a red-shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV-ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV- and lentivirus-mediated optogenetic spike responses in ganglion cells of the postmortem human retina. Targeting the photosensitive ion channel channelrhodopsin-2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin-2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red-shifted light is vastly lower than that of blue light. Here, we show that a red-shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV-ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV-and lentivirus-mediated optogenetic spike responses in ganglion cells of the post-mortem human retina. Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin‐2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red‐shifted light is vastly lower than that of blue light. Here, we show that a red‐shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV‐ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV‐ and lentivirus‐mediated optogenetic spike responses in ganglion cells of the postmortem human retina. Synopsis A red‐shifted channelrhodopsin (ReaChR) was targeted to retinal ganglion cells using three models in parallel: mouse, macaque, and human. Safe orange illumination was able to trigger light responses in all three systems. The red‐shifted channelrhodopsin ReaChR restored light responses at the retinal, cortical, and behavioral levels in blind rd1 mice, using light intensities below the safety limit for the human retina. Optogenetic light responses were demonstrated in explanted postmortem macaque and human retina, infected ex vivo with viral vectors encoding ReaChR. The study presents the first electrophysiological recordings of optogenetic light responses in ganglion cells obtained directly from the human fovea as well as the far peripheral human retina. Graphical Abstract A red‐shifted channelrhodopsin (ReaChR) was targeted to retinal ganglion cells using three models in parallel: mouse, macaque, and human. Safe orange illumination was able to trigger light responses in all three systems. Abstract Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin‐2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red‐shifted light is vastly lower than that of blue light. Here, we show that a red‐shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV‐ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV‐ and lentivirus‐mediated optogenetic spike responses in ganglion cells of the postmortem human retina. Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss caused by retinal degeneration. However, the high intensity of blue light necessary to activate channelrhodopsin‐2 exceeds the safety threshold of retinal illumination because of its strong potential to induce photochemical damage. In contrast, the damage potential of red‐shifted light is vastly lower than that of blue light. Here, we show that a red‐shifted channelrhodopsin (ReaChR), delivered by AAV injections in blind rd1 mice, enables restoration of light responses at the retinal, cortical, and behavioral levels, using orange light at intensities below the safety threshold for the human retina. We further show that postmortem macaque retinae infected with AAV ‐ReaChR can respond with spike trains to orange light at safe intensities. Finally, to directly address the question of translatability to human subjects, we demonstrate for the first time, AAV ‐ and lentivirus‐mediated optogenetic spike responses in ganglion cells of the postmortem human retina. |
| Author | Marre, Olivier Chaffiol, Antoine Macé, Emilie Lampič, Maruša Dalkara, Deniz Sengupta, Abhishek Forster, Valérie Caplette, Romain Lin, John Y Desrosiers, Mélissa Sahel, José‐Alain Picaud, Serge Duebel, Jens |
| AuthorAffiliation | 4 School of Medicine University of Tasmania Hobart Tasmania Australia 2 Sorbonne Universités UPMC Univ Paris 06 UMR_S 968 Institut de la Vision Paris France 6 Present address: Unit on Retinal Neurophysiology National Eye Institute and Graduate Partnerships Program National Institutes of Health Bethesda MD USA 3 CNRS UMR_7210 Paris France 1 INSERM U968 Paris France 5 Hôpital des Quinze‐Vingts Paris France |
| AuthorAffiliation_xml | – name: 3 CNRS UMR_7210 Paris France – name: 1 INSERM U968 Paris France – name: 5 Hôpital des Quinze‐Vingts Paris France – name: 2 Sorbonne Universités UPMC Univ Paris 06 UMR_S 968 Institut de la Vision Paris France – name: 4 School of Medicine University of Tasmania Hobart Tasmania Australia – name: 6 Present address: Unit on Retinal Neurophysiology National Eye Institute and Graduate Partnerships Program National Institutes of Health Bethesda MD USA |
| Author_xml | – sequence: 1 givenname: Abhishek surname: Sengupta fullname: Sengupta, Abhishek organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210, Unit on Retinal Neurophysiology, National Eye Institute and Graduate Partnerships Program, National Institutes of Health – sequence: 2 givenname: Antoine surname: Chaffiol fullname: Chaffiol, Antoine organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 3 givenname: Emilie surname: Macé fullname: Macé, Emilie organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 4 givenname: Romain surname: Caplette fullname: Caplette, Romain organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 5 givenname: Mélissa surname: Desrosiers fullname: Desrosiers, Mélissa organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 6 givenname: Maruša surname: Lampič fullname: Lampič, Maruša organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 7 givenname: Valérie surname: Forster fullname: Forster, Valérie organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 8 givenname: Olivier surname: Marre fullname: Marre, Olivier organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 9 givenname: John Y surname: Lin fullname: Lin, John Y organization: School of Medicine, University of Tasmania – sequence: 10 givenname: José‐Alain surname: Sahel fullname: Sahel, José‐Alain organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210, Hôpital des Quinze‐Vingts – sequence: 11 givenname: Serge surname: Picaud fullname: Picaud, Serge organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 12 givenname: Deniz surname: Dalkara fullname: Dalkara, Deniz email: deniz.dalkara@gmail.com organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 – sequence: 13 givenname: Jens orcidid: 0000-0002-9906-5597 surname: Duebel fullname: Duebel, Jens email: jens.duebel@inserm.fr organization: INSERM, U968, Sorbonne Universités, UPMC Univ Paris 06, UMR_S 968, Institut de la Vision, CNRS, UMR_7210 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27679671$$D View this record in MEDLINE/PubMed https://hal.sorbonne-universite.fr/hal-01375637$$DView record in HAL |
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| DOI | 10.15252/emmm.201505699 |
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| Keywords | primate vision restoration channelrhodopsin retina optogenetics Gene Therapy & Genetic Disease |
| Language | English |
| License | Attribution http://creativecommons.org/licenses/by/4.0 2016 The Authors. Published under the terms of the CC BY 4.0 license. Attribution: http://creativecommons.org/licenses/by This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Snippet | Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss... Targeting the photosensitive ion channel channelrhodopsin-2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating vision loss... Abstract Targeting the photosensitive ion channel channelrhodopsin‐2 (ChR2) to the retinal circuitry downstream of photoreceptors holds promise in treating... |
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| SubjectTerms | Animals channelrhodopsin Cortex Dependovirus - genetics EMBO16 EMBO27 Experiments Genetic Therapy - methods Genetic Vectors Human health and pathology Humans Lentivirus - genetics Life Sciences Light Macaca Membranes Mice Microscopy optogenetics Photoreceptors Phototherapy - methods primate Research Article Retina Retina - physiology Retinal degeneration Retinal Degeneration - therapy Retinal ganglion cells Rhodopsin - genetics Rhodopsin - metabolism Sensory Organs Transduction, Genetic Treatment Outcome vision restoration |
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| Title | Red‐shifted channelrhodopsin stimulation restores light responses in blind mice, macaque retina, and human retina |
| URI | https://link.springer.com/article/10.15252/emmm.201505699 https://onlinelibrary.wiley.com/doi/abs/10.15252%2Femmm.201505699 https://www.ncbi.nlm.nih.gov/pubmed/27679671 https://www.proquest.com/docview/2289996746 https://www.proquest.com/docview/1836726446 https://hal.sorbonne-universite.fr/hal-01375637 https://pubmed.ncbi.nlm.nih.gov/PMC5090658 https://doaj.org/article/754898926dc74e3a8b3a6c9af06db69b |
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