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Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp

Author

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  • Shiqiang Gao

    (Institute for Molecular Plant Physiology and Biophysics, Biocenter, Julius-Maximilians-University of Würzburg)

  • Jatin Nagpal

    (Buchmann Institute for Molecular Life Sciences, Goethe University
    Chemistry and Pharmacy, Institute of Biochemistry, Goethe University)

  • Martin W. Schneider

    (Buchmann Institute for Molecular Life Sciences, Goethe University
    Chemistry and Pharmacy, Institute of Biochemistry, Goethe University)

  • Vera Kozjak-Pavlovic

    (Biocenter, Julius-Maximilians-University of Würzburg)

  • Georg Nagel

    (Institute for Molecular Plant Physiology and Biophysics, Biocenter, Julius-Maximilians-University of Würzburg)

  • Alexander Gottschalk

    (Buchmann Institute for Molecular Life Sciences, Goethe University
    Chemistry and Pharmacy, Institute of Biochemistry, Goethe University
    Cluster of Excellence Frankfurt—Macromolecular Complexes (CEF-MC), Goethe University)

Abstract

Cyclic GMP (cGMP) signalling regulates multiple biological functions through activation of protein kinase G and cyclic nucleotide-gated (CNG) channels. In sensory neurons, cGMP permits signal modulation, amplification and encoding, before depolarization. Here we implement a guanylyl cyclase rhodopsin from Blastocladiella emersonii as a new optogenetic tool (BeCyclOp), enabling rapid light-triggered cGMP increase in heterologous cells (Xenopus oocytes, HEK293T cells) and in Caenorhabditis elegans. Among five different fungal CyclOps, exhibiting unusual eight transmembrane topologies and cytosolic N-termini, BeCyclOp is the superior optogenetic tool (light/dark activity ratio: 5,000; no cAMP production; turnover (20 °C) ∼17 cGMP s−1). Via co-expressed CNG channels (OLF in oocytes, TAX-2/4 in C. elegans muscle), BeCyclOp photoactivation induces a rapid conductance increase and depolarization at very low light intensities. In O2/CO2 sensory neurons of C. elegans, BeCyclOp activation evokes behavioural responses consistent with their normal sensory function. BeCyclOp therefore enables precise and rapid optogenetic manipulation of cGMP levels in cells and animals.

Suggested Citation

  • Shiqiang Gao & Jatin Nagpal & Martin W. Schneider & Vera Kozjak-Pavlovic & Georg Nagel & Alexander Gottschalk, 2015. "Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms9046
    DOI: 10.1038/ncomms9046
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    1. Sarah Baudet & Yvrick Zagar & Fiona Roche & Claudia Gomez-Bravo & Sandrine Couvet & Johann Bécret & Morgane Belle & Juliette Vougny & Sinthuya Uthayasuthan & Oriol Ros & Xavier Nicol, 2023. "Subcellular second messenger networks drive distinct repellent-induced axon behaviors," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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