Directly light-regulated binding of RGS-LOV photoreceptors to anionic membrane phospholipids

We report natural light–oxygen–voltage (LOV) photoreceptors with a blue light-switched, high-affinity (K D ∼ 10−7 M), and direct electrostatic interaction with anionic phospholipids. Membrane localization of one such photoreceptor, BcLOV4 from Botrytis cinerea, is directly coupled to its flavin phot...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2018-08, Vol.115 (33), p.E7720-E7727
Main Authors: Glantz, Spencer T., Berlew, Erin E., Jaber, Zaynab, Schuster, Benjamin S., Gardner, Kevin H., Chow, Brian Y.
Format: Article
Language:English
Subjects:
Binding
Binding sites
Bioinformatics
Biological Sciences
Botrytis - chemistry
Botrytis - genetics
Botrytis - metabolism
Computer applications
Cytosol
Electrostatic properties
Flavin
Fungal Proteins - chemistry
Fungal Proteins - genetics
Fungal Proteins - metabolism
Genetics
Homology
Kinetics
Lipids
Localization
Membrane Proteins - chemistry
Membrane Proteins - genetics
Membrane Proteins - metabolism
Membranes
Phospholipids
Phospholipids - chemistry
Phospholipids - metabolism
Photoreception
Photoreceptors
PNAS Plus
Protein structure
Proteins
Signal transmission
Structure-function relationships
Yeast
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Summary:We report natural light–oxygen–voltage (LOV) photoreceptors with a blue light-switched, high-affinity (K D ∼ 10−7 M), and direct electrostatic interaction with anionic phospholipids. Membrane localization of one such photoreceptor, BcLOV4 from Botrytis cinerea, is directly coupled to its flavin photocycle, and is mediated by a polybasic amphipathic helix in the linker region between the LOV sensor and its C-terminal domain of unknown function (DUF), as revealed through a combination of bioinformatics, computational protein modeling, structure–function studies, and optogenetic assays in yeast and mammalian cell line expression systems. In model systems, BcLOV4 rapidly translocates from the cytosol to plasma membrane (∼1 second). The reversible electrostatic interaction is nonselective among anionic phospholipids, exhibiting binding strengths dependent on the total anionic content of the membrane without preference for a specific headgroup. The in vitro and cellular responses were also observed with a BcLOV4 homolog and thus are likely to be general across the dikarya LOV class, whose members are associated with regulator of G-protein signaling (RGS) domains. Natural photoreceptors are not previously known to directly associate with membrane phospholipids in a light-dependent manner, and thus this work establishes both a photosensory signal transmission mode and a single-component optogenetic tool with rapid membrane localization kinetics that approaches the diffusion limit.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1802832115