Bisretinoids of the Retina: Photo-Oxidation, Iron-Catalyzed Oxidation, and Disease Consequences

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Lipofuscin: mechanisms of age-related accumulation and influence on cell function12 1Guest Editor: Rajindar S. Sohal 2This article is part of a series of reviews on “Oxidative Stress and Aging.” The full list of papers may be found on the homepage of the journal.

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The bisretinoids of retinal pigment epithelium

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Formation of a Nonaoxirane from A2E, a Lipofuscin Fluorophore related to Macular Degeneration, and Evidence of Singlet Oxygen Involvement This work was supported by NIH grant GM 34509 (K.N.), NSF grant NSF-CHE-98-12676 (N.J.T. and S.J.), and NIH grant EY-12951 (J.R.S.).

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Novel Lipofuscin Bisretinoids Prominent in Human Retina and in a Model of Recessive Stargardt Disease

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Anthocyanins Protect Against A2E Photooxidation and Membrane Permeabilization in Retinal Pigment Epithelial Cells¶

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Comparison of the Aerobic Photoreactivity of A2E with its Precursor Retinal¶

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Quercetin and cyanidin-3-glucoside protect against photooxidation and photodegradation of A2E in retinal pigment epithelial cells

Wang, Y., Kim, H. J., & Sparrow, J. R. (2017) · Experimental Eye Research · doi:10.1016/j.exer.2017.04.010 · Cited by 71 · see citing works

The autofluorescent products of lipid peroxidation may not be lipofuscin-like

Eldred, G. E., & Katz, M. (1989) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(89)90007-5 · Cited by 69 · see citing works

THE PHOTOCHEMISTRY OF HUMAN RETINAL LIPOFUSCIN AS STUDIED BY EPR

Reszka, K. J., Eldred, G. E., Wang, R., Chignell, C. F., & Dillon, J. P. (1995) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1995.tb02400.x · Cited by 68 · see citing works

Quantitative Fundus Autofluorescence and Optical Coherence Tomography in PRPH2/RDS - and ABCA4 -Associated Disease Exhibiting Phenotypic Overlap

Duncker, T., Tsang, S. H., Woods, R. L., Lee, W., Zernant, J., Allikmets, R. L., Delori, F. C., & Sparrow, J. R. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-16343 · Cited by 67 · see citing works

Inhibition of Fe2+- and Fe3+- induced hydroxyl radical production by the iron-chelating drug deferiprone

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Quantifying Fundus Autofluorescence in Patients With Retinitis Pigmentosa

Schuerch, K., Woods, R. L., Lee, W., Duncker, T., Delori, F. C., Allikmets, R. L., Tsang, S. H., & Sparrow, J. R. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-21302 · Cited by 65 · see citing works

Iron promotes oxidative cell death caused by bisretinoids of retina

Ueda, K., Kim, H. J., Zhao, J., Song, Y., Dunaief, J. L., & Sparrow, J. R. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1722601115 · Cited by 65 · see citing works

The Oral Iron Chelator Deferiprone Protects Against Systemic Iron Overload–Induced Retinal Degeneration in Hepcidin Knockout Mice

Song, D., Zhao, L., Li, Y., Hadziahmetovic, M., Song, Y., Connelly, J., Spino, M., & Dunaief, J. L. (2014) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-14568 · Cited by 58 · see citing works

Environmental Effects on the Photochemistry of A2-E, a Component of Human Retinal Lipofuscin¶

Ragauskaite, L., Heckathorn, R. C., & Gaillard, E. R. (2001) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2001)0740483eeotpo2.0.co2 · Cited by 58 · see citing works

A TEST OF THE SINGLET OXYGEN MECHANISM OF CATIONIC DYE PHOTOSENSITIZATION OF MITOCHONDRIAL DAMAGE

Bunting, J. R. (1992) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1992.tb04212.x · Cited by 58 · see citing works

Aging, proteotoxicity, mitochondria, glycation, NAD+ and carnosine: possible inter-relationships and resolution of the oxygen paradox

Hipkiss, A. R. (2010) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2010.00010 · Cited by 56 · see citing works

Singlet-oxygen Generation from A2E¶

Kanofsky, J. R., Sima, P. D., & Richter, C. (2003) · Photochemistry and Photobiology · doi:10.1562/0031-8655(2003)0770235sogfa2.0.co2 · Cited by 55 · see citing works

A Novel Bisretinoid of Retina Is an Adduct on Glycerophosphoethanolamine

Yamamoto, K., Yoon, K. D., Ueda, K., Hashimoto, M., & Sparrow, J. R. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.11-8632 · Cited by 53 · see citing works

Photophysical properties of 3,3′-dialkylthiacarbocyanine dyes in organized media: unilamellar liposomes and thin polymer films

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Mechanisms involved in A2E oxidation

Kim, S. R., Steffen Jockusch, B., Itagaki, Y., Turro, N. J., & Sparrow, J. R. (2008) · Experimental Eye Research · doi:10.1016/j.exer.2008.03.016 · Cited by 49 · see citing works

Anthocyanins Protect Against A2E Photooxidation and Membrane Permeabilization in Retinal Pigment Epithelial Cells¶

Jang, Y. P., Zhou, J., Nakanishi, K., & Sparrow, J. R. (2005) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2005.tb00221.x · Cited by 46 · see citing works

A mechanistic study of the photooxidation of A2E, a component of human retinal lipofuscin

Gaillard, E. R., Avalle, L. B., Keller, L. M. M., Wang, Z., Reszka, K., & Dillon, J. P. (2004) · Experimental Eye Research · doi:10.1016/j.exer.2004.05.005 · Cited by 45 · see citing works

Sunlight Exposure, Pigmentation, and Incident Age-Related Macular Degeneration

Klein, R., Howard, K. P., Iyengar, S. K., Sivakumaran, T. A., Meyers, K. J., Cruickshanks, K. J., & Klein, R. (2014) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-14602 · Cited by 43 · see citing works

Primary Photophysical Properties of A2E in Solution

Lamb, L. E., Ye, T., Haralampus-Grynaviski, N. M., Williams, T., Pawlak, A. M., Sarna, T., & Simon, J. D. (2001) · The Journal of Physical Chemistry B · doi:10.1021/jp0123177 · Cited by 41 · see citing works

Influence of dietary vitamin a on autofluorescence of leupeptin-induced inclusions in the retinal pigment epithelium

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Action spectra for the photoconsumption of oxygen by human ocular lipofuscin and lipofuscin extracts

Pawlak, A. M., Rôżanowska, M., Zaręba, M., Lamb, L. E., Simon, J. D., & Sarna, T. (2002) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(02)00260-6 · Cited by 41 · see citing works

Lipofuscin-mediated photodynamic stress induces adverse changes in nanomechanical properties of retinal pigment epithelium cells

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Photooxidation of RPE lipofuscin bisretinoids enhances fluorescence intensity

Kim, S. R., Jang, Y. P., & Sparrow, J. R. (2009) · Vision Research · doi:10.1016/j.visres.2009.09.015 · Cited by 37 · see citing works

Correlations between Photodegradation of Bisretinoid Constituents of Retina and Dicarbonyl Adduct Deposition

Zhou, J., Ueda, K., Zhao, J., & Sparrow, J. R. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.680363 · Cited by 34 · see citing works

Indirect Antioxidant Protection Against Photooxidative Processes Initiated in Retinal Pigment Epithelial Cells by a Lipofuscin Pigment

Zhou, J., Gao, X., Cai, B., & Sparrow, J. R. (2006) · Rejuvenation Research · doi:10.1089/rej.2006.9.256 · Cited by 33 · see citing works

Photochemical studies of A2-E

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Ferroxidase Hephaestin's Cell-Autonomous Role in the Retinal Pigment Epithelium

Wolkow, N., Song, D., Song, Y., Chu, S., Hadziahmetovic, M., Lee, J. C., Iacovelli, J., Grieco, S. F., & Dunaief, J. L. (2012) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.12.041 · Cited by 33 · see citing works

The lipid peroxidation theory of lipofuscinogenesis cannot yet be confirmed

Eldred, G. E., & Katz, M. L. (1991) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(91)90054-7 · Cited by 32 · see citing works

Novel bisretinoids of human retina are lyso alkyl ether glycerophosphoethanolamine-bearing A2PE species

Kim, H. J., & Sparrow, J. R. (2018) · Journal of Lipid Research · doi:10.1194/jlr.m084459 · Cited by 31 · see citing works

Liver-Specific, but Not Retina-Specific, Hepcidin Knockout Causes Retinal Iron Accumulation and Degeneration

Baumann, B. H., Shu, W., Song, Y., Sterling, J. K., Kozmík, Z., Lakhal‐Littleton, S., & Dunaief, J. L. (2019) · American Journal Of Pathology · doi:10.1016/j.ajpath.2019.05.022 · Cited by 31 · see citing works

Highly Differentiated Human Fetal RPE Cultures Are Resistant to the Accumulation and Toxicity of Lipofuscin-Like Material

Zhang, Q., Presswalla, F., Calton, M. A., Charniga, C. J., Stern, J. H., Temple, S., Vollrath, D., Zacks, D. N., Ali, R. R., Thompson, D. A., et al. (2019) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.19-26690 · Cited by 31 · see citing works

Quantitative Autofluorescence Intensities in Acute Zonal Occult Outer Retinopathy vs Healthy Eyes

Boudreault, K., Schuerch, K., Zhao, J., Lee, W., Cabral, T., Yannuzzi, L. A., Tsang, S. H., & Sparrow, J. R. (2017) · JAMA Ophthalmology · doi:10.1001/jamaophthalmol.2017.4499 · Cited by 29 · see citing works

Toward an Understanding of Bisretinoid Autofluorescence Bleaching and Recovery

Yamamoto, K., Zhou, J., Hunter, J. J., Williams, D. R., & Sparrow, J. R. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-9535 · Cited by 25 · see citing works

Bisretinoids mediate light sensitivity resulting in photoreceptor cell degeneration in mice lacking the receptor tyrosine kinase Mer

Zhao, J., Ueda, K., Riera, M., Kim, H. J., & Sparrow, J. R. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005949 · Cited by 25 · see citing works

A vicious cycle of bisretinoid formation and oxidation relevant to recessive Stargardt disease

Zhao, J., Kim, H. J., Ueda, K., Zhang, K., Montenegro, D., Dunaief, J. L., & Sparrow, J. R. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100259 · Cited by 25 · see citing works

Photo-products of retinal pigment epithelial bisretinoids react with cellular thiols.

Yoon, K. D., Yamamoto, K., Zhou, J., & Sparrow, J. R. (2011) · PubMed Central · Cited by 24 · see citing works

Photoreactivity of Bis-retinoid A2E Complexed with a Model Protein in Selected Model Systems

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Photobleaching and Fluorescence Recovery of RPE Bisretinoids

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Photo‐Fenton and Riboflavin‐photosensitized Processes of the Isoxaflutole Herbicide

Gatica, E. A., Possetto, D., Reynoso, A., Natera, J., Miskoski, S., Gerónimo, E. D., Bregliani, M. M., Pajares, A., & Massad, W. A. (2018) · Photochemistry and Photobiology · doi:10.1111/php.13047 · Cited by 10 · see citing works

A mathematical evaluation of dose-dependent PpIX fluorescence kinetics in vivo

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The Association of Cataract and Cataract Surgery With the Long-term Incidence of Age-Related Maculopathy

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The Antiapoptotic Effect of Low-dose UVB Irradiation in NIH3T3 Cells Involves Caspase Inhibition¶

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The Role of Vitamin A in Retinal Diseases

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Lipofuscin, Its Origin, Properties, and Contribution to Retinal Fluorescence as a Potential Biomarker of Oxidative Damage to the Retina

Rôżanowska, M. (2023) · Antioxidants · doi:10.3390/antiox12122111 · Cited by 59 · see citing works

Clearance phagocytosis by the retinal pigment epithelial during photoreceptor outer segment renewal: Molecular mechanisms and relation to retinal inflammation

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Histologic Cell Shape Descriptors for the Retinal Pigment Epithelium in Age-Related Macular Degeneration: A Comparison to Unaffected Eyes

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Recent advances in the analytical methods for quantitative determination of antioxidants in food matrices

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Cyanidin-3-glucoside improves the barrier function of retinal pigment epithelium cells by attenuating endoplasmic reticulum stress-induced apoptosis

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Retinal Pigment Epithelium Under Oxidative Stress: Chaperoning Autophagy and Beyond

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Photobiology of lipofuscin granules in the retinal pigment epithelium cells of the eye: norm, pathology, age

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Retinal Pigment Epithelium Pigment Granules: Norms, Age Relations and Pathology

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Antioxidants and Mechanistic Insights for Managing Dry Age-Related Macular Degeneration

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Autophagy in drusen biogenesis secondary to age‐related macular degeneration

Hyttinen, J. M. T., Koskela, A. K. J., Błasiak, J., & Kaarniranta, K. (2024) · Acta Ophthalmologica · doi:10.1111/aos.16744 · Cited by 20 · see citing works

Chemiexcitation and melanin in photoreceptor disc turnover and prevention of macular degeneration

Lyu, Y., Tschulakow, A., Wang, K., Brash, D. E., & Schraermeyer, U. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2216935120 · Cited by 14 · see citing works

Water-Soluble Products of Photooxidative Destruction of the Bisretinoid A2E Cause Proteins Modification in the Dark

Dontsov, A. E., Yakovleva, M. A., Трофимова, Н. Н., Sakina, N. L., Gulin, A. A., Aybush, A. V., Gostev, F. E., Vasin, A., Feldman, T. B., & Оstrovsky, М. А. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031534 · Cited by 15 · see citing works

Photodegradation of Lipofuscin in Suspension and in ARPE-19 Cells and the Similarity of Fluorescence of the Photodegradation Product with Oxidized Docosahexaenoate

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Cyanidin-3-glucoside protects the photooxidative damage of retinal pigment epithelium cells by regulating sphingolipid signaling and inhibiting MAPK pathway

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Plasma Metabolites Associated with OCT Features of Age-Related Macular Degeneration

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Understanding the Mechanism of Light-Induced Age-Related Decrease in Melanin Concentration in Retinal Pigment Epithelium Cells

Dontsov, A. E., Yakovleva, M. A., Vasin, A. A., Gulin, A. A., Aybush, A. V., Nadtochenko, V. A., & Оstrovsky, М. А. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713099 · Cited by 11 · see citing works

Macular Pigment Carotenoids and Bisretinoid A2E

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Integrative Landscape of Dry AMD Pathogenesis, Models, and Emerging Therapeutic Strategies

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Singlet Oxygen Quenching by Resveratrol Derivatives †

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Melanosomes degrade lipofuscin and precursors that are derived from photoreceptor membrane turnover in the retinal pigment epithelium—an explanation for the origin of the melanolipofuscin granulePreprint

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Retinoid Synthesis Regulation by Retinal Cells in Health and Disease

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Reactive Oxygen Species Regulation Across Retinitis Pigmentosa Animal Models: A 25-Year Systematized Review

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Oxidative Stress, Neuroinflammation and Neurodegeneration: The Chicken, the Egg and the Dinosaur

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Transcriptomic Changes Predict Metabolic Alterations in LC3 Associated Phagocytosis in Aged Mice

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Specialised features of melanosomes in health and disease in the retinal pigment epithelium

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Quantitative autofluorescence is increased in clinically unaffected fellow eyes from patients with posterior uveitis

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Photooxidation Dynamics of Lipofuscin in the Presence of Carotenoid-Binding Protein AstaP: Fluorescence Lifetime Imaging and Pigment Composition Analysis

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Aster-B Modulates Oxidative Stress Responses and Carotenoid Distribution in ARPE-19 Cells

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The roles of glycerophospholipids in the aging retina and age-related macular degeneration

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Inflammasomes in the pathobiology of degenerative retinopathies

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Impact of Oxidized Lipids in the pathogenic mechanism of Age-Related Macular Degeneration

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Disease mechanisms revealed in the P23H opsin knock-in mouse model of retinitis pigmentosa

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Kinsenoside alleviates retinal pigment epithelium cell injury in age-related macular degeneration-like retinal injury through exosome-associated modulation of JNK/MAPK signaling

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Age-Related Changes in bis-Retinoids of Lipofuscin Granules in Human Retinal Pigment Epithelium Cells

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The bisretinoids of retinal pigment epithelium

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Bisretinoid Lipofuscin in the Retinal Pigment Epithelium: Oxidative Processes and Disease Implications

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Cultured Müller cells from mammals can synthesize and accumulate retinyl esters

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Bisretinoid Photodegradation Is Likely Not a Good Thing

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Bisretinoid phospholipid and vitamin A aldehyde: shining a light

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