The bisretinoids of retinal pigment epithelium

Sparrow, Janet R.; Gregory-Roberts, Emily; Yamamoto, Kazunori; Blonska, Anna; Ghosh, Shanti Kaligotla; Ueda, Keiko; Zhou, Jilin

doi:10.1016/j.preteyeres.2011.12.001

Cited by 396Retinal Diseases and TreatmentsRetinal Development and DisordersRetinoids in leukemia and cellular processes

The bisretinoids of retinal pigment epithelium

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Sparrow, Janet R., Gregory-Roberts, Emily, Yamamoto, Kazunori, Blonska, Anna, Ghosh, Shanti Kaligotla, Ueda, Keiko, Zhou, Jilin·2012·Progress in Retinal and Eye Research

DOI 10.1016/j.preteyeres.2011.12.001PMC PMC3288746

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Abstract

The retina exhibits an inherent autofluorescence that is imaged ophthalmoscopically as fundus autofluorescence. In clinical settings, fundus autofluorescence examination aids in the diagnosis and follow-up of many retinal disorders. Fundus autofluorescence originates from the complex mixture of bisretinoid fluorophores that are amassed by retinal pigment epithelial (RPE) cells as lipofuscin. Unlike the lipofuscin found in other cell-types, this material does not form as a result of oxidative stress. Rather, the formation is attributable to non-enzymatic reactions of vitamin A aldehyde in photoreceptor cells; transfer to RPE occurs upon phagocytosis of photoreceptor outer segments. These fluorescent pigments accumulate even in healthy photoreceptor cells and are generated as a consequence of the light capturing function of the cells. Nevertheless, the formation of this material is accelerated in some retinal disorders including recessive Stargardt disease and ELOVL4-related retinal degeneration. As such, these bisretinoid side-products are implicated in the disease processes that threaten vision. In this article, we review our current understanding of the composition of RPE lipofuscin, the structural characteristics of the various bisretinoids, their related spectroscopic features and the biosynthetic pathways by which they form. We will revisit factors known to influence the extent of the accumulation and therapeutic strategies being used to limit bisretinoid formation. Given their origin from vitamin A aldehyde, an isomer of the visual pigment chromophore, it is not surprising that the bisretinoids of retina are light sensitive molecules. Accordingly, we will discuss recent findings that implicate the photodegradation of bisretinoid in the etiology of age-related macular degeneration.

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Dysfunction of phagocytosis, lysosomal degradation, and waste removal by the RPE can lead to severe retinopathies, including age-related macular degeneration.
“Dysfunction of such processes as phagocytosis, lysosomal degradation, and removal of waste products by the RPE can lead to severe retinopathies, including age-related macular degeneration (AMD).”
From Chemistry of the Retinoid (Visual) Cycle (2014) · cites this paper as [270]
Section 7.7 links RPE bisretinoid lipofuscin photooxidation to processes that may predispose the macula to AMD. But section 1 does not identify failed phagocytosis, lysosomal degradation, or waste removal as causes of retinopathy; it specifically argues against inhibited lysosomal enzymes as the explanation for lipofuscin accumulation. The claimed causal chain is therefore broader than the paper supports. (LLM, conf=0.82)
Experimental — accuracy not yet measured
A2E cannot be further metabolized and RPE cells are postmitotic, so A2E and related bisretinoids accumulate in the RPE in the form of lipofuscin deposits.
“As A2E can not be further metabolized and as RPE cells are postmitotic, A2E and related bisretinoids accumulate in the RPE in the form of lipofuscin deposits.”
From The Role of Vitamin A in Retinal Diseases (2022) · cites this paper as [74]
Section 1 (page unavailable) says RPE lipofuscin accumulates with age and suggests that lysosomal enzymes do not recognize bisretinoid structures; Section 2.1 identifies A2E as a lipofuscin constituent. The paper does not establish postmitotic RPE cells as the reason for accumulation, and its Section 5 account of A2E photodegradation does not support the absolute claim that A2E cannot be further metabolized. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Although abundant lipofuscin accumulation is involved in the aetiology of certain retinal diseases such as AMD, Best disease and ABCA4-retinopathy, it also accumulates at a lower level with age in the RPE of healthy eyes.
“Although abundant lipofuscin accumulation is involved in the aetiology of certain retinal diseases (e.g., AMD, Best disease and ABCA4-retinopathy), it accumulates at a lower level also with age in the RPE of healthy eyes [9,72,73,74,75].”
From The Role of Vitamin A in Retinal Diseases (2022) · cites this paper as [74]
Section 1 says RPE lipofuscin accumulates with age in healthy and diseased eyes, and section 7.1 identifies excessive accumulation in ABCA4-related disease. Section 7.7 proposes a possible contribution of lipofuscin products to AMD, but does not establish abundant accumulation as a cause of AMD; the retrieved passages do not address Best disease. Page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Lipofuscin compromises the function and viability of RPE cells and ultimately results in photoreceptor degeneration and a loss of vision.
“Lipofuscin is an autofluorescent cellular waste product that compromises the function and viability of RPE cells and ultimately results in photoreceptor degeneration and a loss of vision [54,69,73,74,75].”
From The Role of Vitamin A in Retinal Diseases (2022) · cites this paper as [74]
Section 5 (page unavailable in our copy) reports that light exposure of A2E-containing RPE cells can cause cell damage and death. Section 8 links lipofuscin accumulation to RPE atrophy and photoreceptor degeneration, but specifically as a generally accepted explanation in juvenile-onset recessive Stargardt disease. The citing sentence presents this as an inevitable effect of lipofuscin generally; the source does not establish that broader claim or the stated progression to vision loss. (LLM, conf=0.88)
Experimental — accuracy not yet measured
In the membranes of outer photoreceptor segments, nonenzymatically formed toxic bisretinoids are converted upon phagocytosis in the acidic environment of RPE phagolysosomes to bisretinoid pyridinium compound A2E and related bisretinoids.
“In the membranes of outer photoreceptor segments are nonenzymatically formed toxic bisretinoids. Upon phagocytosis, these bisretinoids are in the acidic environment of RPE phagolysosomes converted to bisretinoid pyridinium compound A2E and related bisretinoids [54,69,70,71,72,73,74].”
From The Role of Vitamin A in Retinal Diseases (2022) · cites this paper as [74]
Section 3.2 (page unavailable) reports nonenzymatic steps in bisretinoid formation and identifies A2PE in photoreceptor outer segments as the immediate precursor of A2E. It says A2PE is cleaved by phospholipase D, with that activity present in RPE lysosomal fractions; it does not establish that an acidic phagolysosomal environment converts bisretinoids generally into A2E and related compounds. (LLM, conf=0.86)
Experimental — accuracy not yet measured

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Influence of early photoreceptor degeneration on lipofuscin in the retinal pigment epithelium
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Rpe65 Leu450Met variant is associated with reduced levels of the retinal pigment epithelium lipofuscin fluorophores A2E and iso-A2E
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The all-trans -retinal dimer series of lipofuscin pigments in retinal pigment epithelial cells in a recessive Stargardt disease model
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Functional characteristics of patients with retinal dystrophy that manifest abnormal parafoveal annuli of high density fundus autofluorescence; a review and update
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Interpretations of Fundus Autofluorescence from Studies of the Bisretinoids of the Retina
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Positively charged retinoids are potent and selective inhibitors of the trans-cis isomerization in the retinoid (visual) cycle
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Characterization of Peroxy-A2E and Furan-A2E Photooxidation Products and Detection in Human and Mouse Retinal Pigment Epithelial Cell Lipofuscin
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Lipid to Protein Chromophore Transfer in the Photolysis of Visual Pigments
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Small Molecule RPE65 Antagonists Limit the Visual Cycle and Prevent Lipofuscin Formation
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Methylglyoxal Can Modify GAPDH Activity and Structure
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Novel Lipofuscin Bisretinoids Prominent in Human Retina and in a Model of Recessive Stargardt Disease
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Proteome analysis of lipofuscin in human retinal pigment epithelial cells
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Dominant Negative Mechanism Underlies Autosomal Dominant Stargardt-like Macular Dystrophy Linked to Mutations in ELOVL4
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The Role of A2E in Prevention or Enhancement of Light Damage in Human Retinal Pigment Epithelial Cells¶
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Functional correlates of fundus autofluorescence abnormalities in patients with RPGR or RIMS1 mutations causing cone or cone rod dystrophy
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Development of a polyclonal antibody with broad epitope specificity for advanced glycation endproducts and localization of these epitopes in Bruch's membrane of the aging eye.
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Photoreceptor Cell Degeneration in Abcr –/– Mice
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Comparison of the Aerobic Photoreactivity of A2E with its Precursor Retinal¶
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The autofluorescent products of lipid peroxidation may not be lipofuscin-like
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A2-Rhodopsin: a new fluorophore isolated from photoreceptor outer segments
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THE PHOTOCHEMISTRY OF HUMAN RETINAL LIPOFUSCIN AS STUDIED BY EPR
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Role of the C Terminus of the Photoreceptor ABCA4 Transporter in Protein Folding, Function, and Retinal Degenerative Diseases
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Loss of ER retention and sequestration of the wild-type ELOVL4 by Stargardt disease dominant negative mutants.
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Mechanistic Studies of ABCR, the ABC Transporter in Photoreceptor Outer Segments Responsible for Autosomal Recessive Stargardt Disease
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Mole Quantity of RPE65 and Its Productivity in the Generation of 11-cis-Retinal from Retinyl Esters in the Living Mouse Eye
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Stargardt-like macular dystrophy protein ELOVL4 exerts a dominant negative effect by recruiting wild-type protein into aggresomes.
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Examining the proteins of functional retinal lipofuscin using proteomic analysis as a guide for understanding its origin.
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Rdh12 activity and effects on retinoid processing in the murine retina
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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
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Subunit structure and activity of glyceraldehyde-3-phosphate dehydrogenase from spinach chloroplasts
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A Novel Bisretinoid of Retina Is an Adduct on Glycerophosphoethanolamine
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Spatial localization of A2E in the retinal pigment epithelium
Grey, A. C., Crouch, R. K., Koutalos, Y., Schey, K. L., & Ablonczy, Z. (2011) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.10-7020 · Cited by 52 · see citing works
A2E, A Pigment of RPE Lipofuscin, is Generated from the Precursor, A2PE by a Lysosomal Enzyme Activity
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Age-related retinal pigment epithelium and Bruch's membrane degeneration in senescence-accelerated mouse.
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Rapid, Noninvasive Detection of Diabetes-Induced Retinal Metabolic Stress
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Electroretinographic evidence for altered phototransduction gain and slowed recovery from photobleaches in albino mice with a MET450 variant in RPE65
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Elovl4 5-bp deletion knock-in mouse model for Stargardt-like macular degeneration demonstrates accumulation of ELOVL4 and lipofuscin
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Action spectra for the photoconsumption of oxygen by human ocular lipofuscin and lipofuscin extracts
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Primary Photophysical Properties of A2E in Solution
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Retinal Degenerations: Biology, Diagnostics and Therapeutics
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Fluorescence spectroscopic detection of mitochondrial flavoprotein redox oscillations and transient reduction of the NADPH oxidase-associated flavoprotein in leukocytes
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The lipid peroxidation theory of lipofuscinogenesis cannot yet be confirmed
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Characterization of Dihydro-A2PE: An Intermediate in the A2E Biosynthetic Pathway
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Generation of fluorescent adducts of malondialdehyde and amino acids: toward an understanding of lipofuscin.
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Fundus Autofluorescence
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Recovery of Rod Photoresponses in ABCR-Deficient Mice
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Lipofuscin of the Retinal Pigment Epithelium
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Fluorescent Lipid Oxidation Products and Heme Spectra Index Antioxidant Efficacy in Kidney Tissue of Hamsters
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Effects of UVR and UVR-induced Cytokines on Production of Extracellular Matrix Proteins and Proteases by Dermal Fibroblasts Cultured in Collagen Gels¶
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5 of the 140 references couldn’t be matched to a known paper.

Research works printed but not linked: 4

Delori FC Keilhauer C Sparrow JR Staurenghi G Holz FG Schmitz-Valckenberg S Spaide RF Bird AC Origin of fundus autofluorescence Atlas of Fundus Autofluorescence Imaging 2007 Berlin Heidelberg Springer-Verlag 17 29
Majji AB Cao J Chang KY Hayashi A Aggarwal S Grebe RR de Juan E Invest Ophthalmol Vis Sci 2000 52 3936 3942 11053297
Michaelides M Lois N Forrester JV Fundus autofluorescence in cone and cone-rod dystrophies Fundus Autofluorescence 2009 Philadelphia Lippincott Williams and Wilkins 153 166
Nomura Y Takeda T Okuma Y The Senescence-Accelerated Mouse (SAM): An Animal Model of Senescence 2004 Amsterdam, The Netherlands Elsevier B.V.

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Retinoprotective Effects of Bilberry Anthocyanins via Antioxidant, Anti-Inflammatory, and Anti-Apoptotic Mechanisms in a Visible Light-Induced Retinal Degeneration Model in Pigmented Rabbits
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Serous business: Delineating the broad spectrum of diseases with subretinal fluid in the macula
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RUBCN/rubicon and EGFR regulate lysosomal degradative processes in the retinal pigment epithelium (RPE) of the eye
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Quantitative Fundus Autofluorescence and Optical Coherence Tomography in PRPH2/RDS - and ABCA4 -Associated Disease Exhibiting Phenotypic Overlap
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Antioxidant Drug Therapy Approaches for Neuroprotection in Chronic Diseases of the Retina
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Quantifying Fundus Autofluorescence in Patients With Retinitis Pigmentosa
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New insights into the role of autophagy in retinal and eye diseases.
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Retinal Pigment Epithelium Cell Death Is Associated With NLRP3 Inflammasome Activation by All- trans Retinal
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Photoreceptor cells as a source of fundus autofluorescence in recessive Stargardt disease
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Bisretinoid phospholipid and vitamin A aldehyde: shining a light
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Characterization of Stargardt Disease Using Polarization-Sensitive Optical Coherence Tomography and Fundus Autofluorescence Imaging
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Aberrant Lipid Metabolism and Complement Activation in Age-Related Macular Degeneration
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Authors: Sparrow, J. R., Gregory-Roberts, E., Yamamoto, K., Blonska, A., Ghosh, S. K., Ueda, K., & Zhou, J.
Affiliations: Columbia University Irving Medical Center (US)
Columbia University (US)
Corresponding author: Sparrow, Janet R.
ORCID: Sparrow, Janet R.
Ueda, Keiko
Venue: Progress in Retinal and Eye Research
Publisher: Elsevier BV
Published: 2012-03
Volume: 31
Issue: 2
Pages: 121-135
ISSN: 1350-9462 (ISSN-L)
DOI: 10.1016/j.preteyeres.2011.12.001
PMC: PMC3288746
OpenAlex: W2019731198
Cited by: 392
References: 140
Citations by year: 2026: 19 · 2025: 26 · 2024: 26 · 2023: 24 · 2022: 23 · 2021: 34 · 2020: 35 · 2019: 33 · 2018: 29 · 2017: 28 · 2016: 25 · 2015: 31 · 2014: 30 · 2013: 21 · 2012: 8
FWCI: 3.23
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Progress in Retinal and Eye Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Eye Institute (R01EY012951, EY 12951, P30EY019007)
Topics: Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
Keywords: bisretinoids, retinal pigment epithelium, lipofuscin, fundus autofluorescence, vitamin A aldehyde, photoreceptor outer segment phagocytosis, Stargardt disease, age-related macular degeneration, photodegradation, retinal degeneration
MeSH terms: Animals, Cattle, Fluorescence, Humans, Lipofuscin, Macular Degeneration, Retinaldehyde, Retinoids, Spectrometry, Fluorescence, Molecular Structure, Mice, Rats, Retinal Pigment Epithelium

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