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Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye

¹ Departments of Ophthalmology, ² Pharmacology, and ³ Chemistry, University of Washington, Seattle, WA 98195
⁴ Department of Molecular Physiology and Biophysics, Vanderbilt University Medical Center, Nashville, TN 37232
⁵ Departments of Ophthalmology, Biology, and Neurobiology and Anatomy, University of Utah Health Science Center, Salt Lake City, UT 84112

Address correspondence to Krzysztof Palczewski, Dept. of Ophthalmology, University of Washington, 1959 NE Pacific St., Box 356485, Seattle, WA 98195-6485. Tel.: (206) 543-9074. Fax: (206) 221-6784. email: palczews{at}u.washington.edu

Visual sensation in vertebrates is triggered when light strikes retinal photoreceptor cells causing photoisomerization of the rhodopsin chromophore 11-cis-retinal to all-trans-retinal. The regeneration of preillumination conditions of the photoreceptor cells requires formation of 11-cis-retinal in the adjacent retinal pigment epithelium (RPE). Using the intrinsic fluorescence of all-trans-retinyl esters, noninvasive two-photon microscopy revealed previously uncharacterized structures (6.9 ± 1.1 µm in length and 0.8 ± 0.2 µm in diameter) distinct from other cellular organelles, termed the retinyl ester storage particles (RESTs), or retinosomes. These structures form autonomous all-trans-retinyl ester-rich intracellular compartments distinct from other organelles and colocalize with adipose differentiation-related protein. As demonstrated by in vivo experiments using wild-type mice, the RESTs participate in 11-cis-retinal formation. RESTs accumulate in Rpe65^-/- mice incapable of carrying out the enzymatic isomerization, and correspondingly, are absent in the eyes of Lrat^-/- mice deficient in retinyl ester synthesis. These results indicate that RESTs located close to the RPE plasma membrane are essential components in 11-cis-retinal production.

Key Words: retinoid cycle; photoreceptor cells; two-photon microscopy; retinal pigment epithelial cells; rhodopsin

Abbreviations used in this paper: 3-D, three-dimensional; ADRP, adipose differentiation-related protein; CRALBP, cellular retinaldehyde-binding protein; LRAT, lecithin:retinol acyltransferase; REST, retinyl ester storage particle; ROS, rod outer segment; RPE, retinal pigment epithelium; RPE65, an RPE-specific 65-kD protein.

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