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Intrinsic differences in rod and cone membrane composition: implications for cone degeneration

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Abstract

Purpose

In many retinal pathological conditions, rod and cone degeneration differs. For example, the early-onset maculopathy Stargardts disease type 1 (STGD1) is typified by loss of cones while rods are often less affected. We wanted to examine whether there exist intrinsic membrane differences between rods and cones that might explain such features.

Methods

Abca4 mRNA and protein levels were quantified in rod- and cone-enriched samples from wild-type and Nrl−/− mice retinas; rod- and cone-enriched outer segments (ROS and COS respectively) were prepared from pig retinas, and total lipids were analyzed by flame ionization, chromatography, and tandem mass spectrometry. Immunohistochemical staining of cone-rich rodent Arvicanthis ansorgei retinas was conducted, and ultra-high performance liquid chromatography of lipid species in porcine ROS and COS was performed.

Results

Abca4 mRNA and Abca4 protein content was significantly higher (50–300%) in cone compared to rod-enriched samples. ROS and COS displayed dramatic differences in several lipids, including very long chain poly-unsaturated fatty acids (VLC-PUFAs), especially docosahexaenoic acid (DHA, 22:6n-3): ROS 20.6% DHA, COS 3.3% (p < 0.001). VLC-PUFAs (> 50 total carbons) were virtually absent from COS. COS were impoverished (> 6× less) in phosphatidylethanolamine compared to ROS. ELOVL4 (“ELOngation of Very Long chain fatty acids 4”) antibody labelled Arvicanthis cones only very weakly compared to rods. Finally, there were large amounts (905 a.u.) of the bisretinoid A2PE in ROS, whereas it was much lower (121 a.u., ~ 7.5-fold less) in COS fractions. In contrast, COS contained fivefold higher amounts of all-trans-retinal dimer (115 a.u. compared to 22 a.u. in rods).

Conclusions

Compared to rods, cones expressed higher levels of Abca4 mRNA and Abca4 protein, were highly impoverished in PUFA (especially DHA) and phosphatidylethanolamine, and contained significant amounts of all-trans-retinal dimer. Based on these and other data, we propose that in contrast to rods, cones are preferentially vulnerable to stress and may die through direct cellular toxicity in pathologies such as STGD1.

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Acknowledgements

The authors would like to acknowledge the expert technical assistance of Ms. Cathy Royer, and the courteous assistance of Mr. Fabrice Poncin, Supervisor, Copvial SA.

Funding

This study was funded by the Fondation de la Recherche Médicale (FC) (grant no. DPR20121125278), UNADEV-ITMO (DH), the Fondation de France/Association Berthe Fouassier (DMV), the International Retinal Research Foundation (DMV), the Agence Nationale de Recherche (no. ANR-08-MNP-038) (DH, NA and LB), and NEI grant RO1 EY012951 (JRS).

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  1. Daniela M. Verra and Perrine Spinnhirny contributed equally to the work.

Authors and Affiliations

  1. Département de Neurobiologie des Rythmes, Institut des Neurosciences Cellulaires et Intégratives, CNRS UPR 3212, 8 Allée Général Rouvillois, 67000, Strasbourg Cedex, France

    Daniela M. Verra, Perrine Spinnhirny, Cristina Sandu & David Hicks

  2. UMR 1324 Centre des Sciences du Goût et de l’Alimentation, Eye and Nutrition Research Group, INRA, Dijon, France

    Stéphane Grégoire, Niyazi Acar, Olivier Berdeaux & Lionel Brétillon

  3. UMR 6265 Centre des Sciences du Goût et de l’Alimentation, CNRS, Dijon, France

    Stéphane Grégoire, Niyazi Acar, Olivier Berdeaux & Lionel Brétillon

  4. Centre des Sciences du Goût et de l’Alimentation, Université de Bourgogne, Dijon, France

    Stéphane Grégoire, Niyazi Acar, Olivier Berdeaux & Lionel Brétillon

  5. Departments of Ophthalmology, and Pathology and Cell Biology, Columbia University Medical Center, New York, NY, USA

    Janet R. Sparrow

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The experiments presented in this paper were authorized by the french Ministry of Research, APAFIS#8472-2016121318254073 v10.

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Verra, D.M., Spinnhirny, P., Sandu, C. et al. Intrinsic differences in rod and cone membrane composition: implications for cone degeneration. Graefes Arch Clin Exp Ophthalmol 260, 3131–3148 (2022). https://doi.org/10.1007/s00417-022-05684-9

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