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All-optical electrophysiology in hiPSC-derived neurons with synthetic voltage sensors

Francesca Puppo, Sanaz Sadegh, Cleber A. Trujillo, Martin Thunemann, Evan Campbell, Matthieu Vandenberghe, Xiwei Shan, Ibrahim A Akkouh, View ORCID ProfileEvan W. Miller, View ORCID ProfileBrenda L. Bloodgood, Gabriel A. Silva, Anders M. Dale, View ORCID ProfileGaute T. Einevoll, View ORCID ProfileSrdjan Djurovic, View ORCID ProfileOle A. Andreassen, Alysson R. Muotri, View ORCID ProfileAnna Devor
doi: https://doi.org/10.1101/2021.01.18.427081
Francesca Puppo
1Department of Pediatrics and Department of Cellular & Molecular Medicine, University of California San Diego, School of Medicine, Center for Academic Research and Training in Anthropogeny (CARTA), Kavli Institute for Brain and Mind, La Jolla, CA 92037, USA
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  • For correspondence: fpuppo@health.ucsd.edu adevor@bu.edu
Sanaz Sadegh
2Department of Neurosciences, University of California San Diego, La Jolla, CA 92093, USA
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Cleber A. Trujillo
1Department of Pediatrics and Department of Cellular & Molecular Medicine, University of California San Diego, School of Medicine, Center for Academic Research and Training in Anthropogeny (CARTA), Kavli Institute for Brain and Mind, La Jolla, CA 92037, USA
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Martin Thunemann
3Department of Biomedical Engineering, Boston University, Boston, MA 02215, USA
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Evan Campbell
4Department of Neurobiology, University of California San Diego, La Jolla, CA 92093, USA
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Matthieu Vandenberghe
5NORMENT, KG Jebsen Centre for Neurodevelopmental Disorders, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway
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Xiwei Shan
1Department of Pediatrics and Department of Cellular & Molecular Medicine, University of California San Diego, School of Medicine, Center for Academic Research and Training in Anthropogeny (CARTA), Kavli Institute for Brain and Mind, La Jolla, CA 92037, USA
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Ibrahim A Akkouh
5NORMENT, KG Jebsen Centre for Neurodevelopmental Disorders, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway
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Evan W. Miller
6Department of Chemistry and Molecular & Cell Biology, University of California, Berkeley, CA 94720, USA
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  • ORCID record for Evan W. Miller
Brenda L. Bloodgood
4Department of Neurobiology, University of California San Diego, La Jolla, CA 92093, USA
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Gabriel A. Silva
7Department of Bioengineering, University of California San Diego, La Jolla, CA 92093, USA
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Anders M. Dale
8Department of Radiology, University of California San Diego, La Jolla, CA 92093, USA
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Gaute T. Einevoll
9Department of Physics, Norwegian University of Life Sciences, Ås & Department of Physics, University of Oslo, Oslo, Norway
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  • ORCID record for Gaute T. Einevoll
Srdjan Djurovic
10Department of Medical Genetics, Oslo University Hospital, Oslo, Norway and NORMENT, Department of Clinical Science, University of Bergen, Bergen, Norway
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Ole A. Andreassen
5NORMENT, KG Jebsen Centre for Neurodevelopmental Disorders, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway
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Alysson R. Muotri
1Department of Pediatrics and Department of Cellular & Molecular Medicine, University of California San Diego, School of Medicine, Center for Academic Research and Training in Anthropogeny (CARTA), Kavli Institute for Brain and Mind, La Jolla, CA 92037, USA
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Anna Devor
3Department of Biomedical Engineering, Boston University, Boston, MA 02215, USA
11Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Charlestown, MA, 02129, USA
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  • ORCID record for Anna Devor
  • For correspondence: fpuppo@health.ucsd.edu adevor@bu.edu
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Abstract

Voltage imaging and “all-optical electrophysiology” in human induced pluripotent stem cell (hiPSC)-derived neurons have opened unprecedented opportunities for high-throughput phenotyping of activity in neurons possessing unique genetic backgrounds of individual patients. While prior all-optical electrophysiology studies relied on genetically encoded voltage indicators, viral transduction of human neurons with large or multiple expression vectors can impact cell function and often lead to massive cell death. Here, we demonstrate an alternative protocol using a synthetic voltage sensor and genetically encoded optogenetic actuator that generate robust and reproducible results. We demonstrate the functionality of this method by measuring spontaneous and evoked activity in three independent hiPSC-derived neuronal cell lines with distinct genetic backgrounds.

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Posted January 19, 2021.
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All-optical electrophysiology in hiPSC-derived neurons with synthetic voltage sensors
Francesca Puppo, Sanaz Sadegh, Cleber A. Trujillo, Martin Thunemann, Evan Campbell, Matthieu Vandenberghe, Xiwei Shan, Ibrahim A Akkouh, Evan W. Miller, Brenda L. Bloodgood, Gabriel A. Silva, Anders M. Dale, Gaute T. Einevoll, Srdjan Djurovic, Ole A. Andreassen, Alysson R. Muotri, Anna Devor
bioRxiv 2021.01.18.427081; doi: https://doi.org/10.1101/2021.01.18.427081
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All-optical electrophysiology in hiPSC-derived neurons with synthetic voltage sensors
Francesca Puppo, Sanaz Sadegh, Cleber A. Trujillo, Martin Thunemann, Evan Campbell, Matthieu Vandenberghe, Xiwei Shan, Ibrahim A Akkouh, Evan W. Miller, Brenda L. Bloodgood, Gabriel A. Silva, Anders M. Dale, Gaute T. Einevoll, Srdjan Djurovic, Ole A. Andreassen, Alysson R. Muotri, Anna Devor
bioRxiv 2021.01.18.427081; doi: https://doi.org/10.1101/2021.01.18.427081

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