Hijacking of internal calcium dynamics by intracellularly residing viral rhodopsins

Ana-Sofia Eria-Oliveira, Mathilde Folacci, Anne Amandine Chassot, Sandrine Fedou, Nadine Thézé, Dmitrii Zabelskii, Alexey Alekseev, Ernst Bamberg, Valentin Gordeliy, Guillaume Sandoz, Michel Vivaudou

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Rhodopsins are ubiquitous light-driven membrane proteins with diverse functions, including ion transport. Widely distributed, they are also coded in the genomes of giant viruses infecting phytoplankton where their function is not settled. Here, we examine the properties of OLPVR1 (Organic Lake Phycodnavirus Rhodopsin) and two other type 1 viral channelrhodopsins (VCR1s), and demonstrate that VCR1s accumulate exclusively intracellularly, and, upon illumination, induce calcium release from intracellular IP3-dependent stores. In vivo, this light-induced calcium release is sufficient to remote control muscle contraction in VCR1-expressing tadpoles. VCR1s natively confer light-induced Ca2+ release, suggesting a distinct mechanism for reshaping the response to light of virus-infected algae. The ability of VCR1s to photorelease calcium without altering plasma membrane electrical properties marks them as potential precursors for optogenetics tools, with potential applications in basic research and medicine.
Original languageEnglish
Article number65
JournalNature Communications
Volume15
Issue number1
DOIs
Publication statusPublished - 1 Dec 2024
Externally publishedYes

Funding

We thank Pierre Thiébaud (Univ. Bordeaux, France) for assistance with Xenopus tadpoles, Jean Revilloud (IBS, Grenoble, France) for technical assistance, Christophe Moreau and Justine Magnat (IBS) for Xenopus frogs maintenance and oocytes preparation, Bruno Allard and Vincent Jacquemond (Univ. Lyon, France) and Maximilien Fürthauer (iBV, Nice, France) for preliminary tests, Christoph Fahlke (Inst. of Biological Information Processing, Jülich, Germany) for ChR2. We thank François Rassendren (iGF, Montpellier, France) for suggesting the use of a tethered GCaMP Ca sensor. Microscopy was performed in the MICA facility of the iBV-CNRS UMR 7277-INSERM U1091-UNS and we acknowledge the help of PRISM engineers Sameh Ben-Aicha and Baptiste Monterosso. This project was funded by grants from the Agence Nationale de la Recherche (ANR-15-CE11–0029–01 to MV and VG; ANR-19-CE11-0026 to MV, VG, and GS). Work in the Vivaudou and Gordeliy laboratories were supported by CNRS (Centre National de la Recherche Scientifique), CEA (Commissariat à l’Energie Atomique et aux énergies alternatives), and Université Grenoble Alpes. The Gordeliy laboratory operates under a CEA(IBS) and Research Center Juelich FZJ-IBI7 specific agreement. The Sandoz laboratory is funded by the French government, through the UCAJEDI Investments in the Future project from ANR (ANR-15-IDEX-01). The Sandoz and Vivaudou laboratories are members of the French National Laboratories of Excellence “Ion Channel Science and Therapeutics” (LabEX ICST) funded by a network grant from ANR (ANR-11-LABX-0015-01). ASO and MF were supported by doctoral fellowships from ANR and CEA, respectively. 2+ We thank Pierre Thiébaud (Univ. Bordeaux, France) for assistance with Xenopus tadpoles, Jean Revilloud (IBS, Grenoble, France) for technical assistance, Christophe Moreau and Justine Magnat (IBS) for Xenopus frogs maintenance and oocytes preparation, Bruno Allard and Vincent Jacquemond (Univ. Lyon, France) and Maximilien Fürthauer (iBV, Nice, France) for preliminary tests, Christoph Fahlke (Inst. of Biological Information Processing, Jülich, Germany) for ChR2. We thank François Rassendren (iGF, Montpellier, France) for suggesting the use of a tethered GCaMP Ca2+sensor. Microscopy was performed in the MICA facility of the iBV-CNRS UMR 7277-INSERM U1091-UNS and we acknowledge the help of PRISM engineers Sameh Ben-Aicha and Baptiste Monterosso. This project was funded by grants from the Agence Nationale de la Recherche (ANR-15-CE11–0029–01 to MV and VG; ANR-19-CE11-0026 to MV, VG, and GS). Work in the Vivaudou and Gordeliy laboratories were supported by CNRS (Centre National de la Recherche Scientifique), CEA (Commissariat à l’Energie Atomique et aux énergies alternatives), and Université Grenoble Alpes. The Gordeliy laboratory operates under a CEA(IBS) and Research Center Juelich FZJ-IBI7 specific agreement. The Sandoz laboratory is funded by the French government, through the UCAJEDI Investments in the Future project from ANR (ANR-15-IDEX-01). The Sandoz and Vivaudou laboratories are members of the French National Laboratories of Excellence “Ion Channel Science and Therapeutics” (LabEX ICST) funded by a network grant from ANR (ANR-11-LABX-0015-01). ASO and MF were supported by doctoral fellowships from ANR and CEA, respectively.

FundersFunder number
French National Laboratories of Excellence “Ion Channel Science and Therapeutics
LabEX ICSTANR-11-LABX-0015-01
Maximilien Fürthauer
Sandoz and Vivaudou laboratories
Université Grenoble AlpesANR-15-IDEX-01
Agence Nationale de la RechercheANR-15-CE11–0029–01, ANR-19-CE11-0026
Centre National de la Recherche Scientifique
Commissariat à l'Énergie Atomique et aux Énergies Alternatives
iGFUMR 7277-INSERM U1091-UNS

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