The biophysical, molecular, and anatomical landscape of pigeon CRY4: A candidate light-based quantal magnetosensor
Tobias Hochstoeger, Tarek Al Said, Dante Maestre, Florian Walter, Alexandra Vilceanu, Miriam Pedron, Thomas D. Cushion, William D. Snider, Simon Nimpf, Grégory C. Nordmann, Lukas Landler, Nathaniel B. Edelman, Lennard Kruppa, Gerhard Dürnberger, Karl Mechtler, Stefan Schuechner, Egon Ogris, E. Pascal Malkemper, Stefan Weber, Erik Schleicher, David A. Keays
Abstract
The biophysical and molecular mechanisms that enable animals to detect magnetic fields are unknown. It has been proposed that birds have a light-dependent magnetic compass that relies on the formation of radical pairs within cryptochrome molecules. Using spectroscopic methods, we show that pigeon cryptochrome clCRY4 is photoreduced efficiently and forms long-lived spin-correlated radical pairs via a tetrad of tryptophan residues. We report that clCRY4 is broadly and stably expressed within the retina but enriched at synapses in the outer plexiform layer in a repetitive manner. A proteomic survey for retinal-specific clCRY4 interactors identified molecules that are involved in receptor signaling, including glutamate receptor-interacting protein 2, which colocalizes with clCRY4. Our data support a model whereby clCRY4 acts as an ultraviolet-blue photoreceptor and/or a light-dependent magnetosensor by modulating glutamatergic synapses between horizontal cells and cones.