Phototoxic damage to cone photoreceptors can be independent of the visual pigment: the porphyrin hypothesis.
Animals
Cell Line
Humans
Light
/ adverse effects
Lipofuscin
/ toxicity
Macaca fascicularis
Macular Degeneration
/ pathology
Porphyrins
/ metabolism
Retina
/ metabolism
Retinal Cone Photoreceptor Cells
/ metabolism
Retinal Pigment Epithelium
/ metabolism
Retinal Pigments
/ metabolism
Retinoids
/ toxicity
Swine
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
29 08 2020
29 08 2020
Historique:
received:
12
03
2020
accepted:
03
08
2020
revised:
01
08
2020
entrez:
31
8
2020
pubmed:
31
8
2020
medline:
21
4
2021
Statut:
epublish
Résumé
Lighting is rapidly changing with the introduction of light-emitting diodes (LEDs) in our homes, workplaces, and cities. This evolution of our optical landscape raises major concerns regarding phototoxicity to the retina since light exposure is an identified risk factor for the development of age-related macular degeneration (AMD). In this disease, cone photoreceptors degenerate while the retinal pigment epithelium (RPE) is accumulating lipofuscin containing phototoxic compounds such as A2E. Therefore, it remains unclear if the light-elicited degenerative process is initiated in cones or in the RPE. Using purified cone photoreceptors from pig retina, we here investigated the effect of light on cone survival from 390 to 510 nm in 10 nm steps, plus the 630 nm band. If at a given intensity (0.2 mW/cm²), the most toxic wavelengths are comprised in the visible-to-near-UV range, they shift to blue-violet light (425-445 nm) when exposing cells to a solar source filtered by the eye optics. In contrast to previous rodent studies, this cone photoreceptor phototoxicity is not related to light absorption by the visual pigment. Despite bright flavin autofluorescence of cone inner segment, excitation-emission matrix of this inner segment suggested that cone phototoxicity was instead caused by porphyrin. Toxic light intensities were lower than those previously defined for A2E-loaded RPE cells indicating cones are the first cells at risk for a direct light insult. These results are essential to normative regulations of new lighting but also for the prevention of human retinal pathologies since toxic solar light intensities are encountered even at high latitudes.
Identifiants
pubmed: 32862199
doi: 10.1038/s41419-020-02918-8
pii: 10.1038/s41419-020-02918-8
pmc: PMC7456424
doi:
Substances chimiques
A2-E (N-retinylidene-N-retinylethanolamine)
0
Lipofuscin
0
Porphyrins
0
Retinal Pigments
0
Retinoids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
711Références
Behar-Cohen, F. et al. Light-emitting diodes (LED) for domestic lighting: any risks for the eye? Prog. Retin. Eye Res. 30, 239–257 (2011).
doi: 10.1016/j.preteyeres.2011.04.002
Scientific Committee on Health, E. a. E. R. S. Opinion on potential risks to human health of Light Emitting Diodes (LEDs). https://ec.europa.eu/health/sites/health/files/scientific_committees/scheer/docs/scheer_o_011.pdf (2018).
Rambhatla, P. V., Brescoll, J., Hwang, F., Juzych, M. & Lim, H. W. Photosensitive disorders of the skin with ocular involvement. Clin. Dermatol. 33, 238–246 (2015).
doi: 10.1016/j.clindermatol.2014.10.016
Sui, G. Y. et al. Is sunlight exposure a risk factor for age-related macular degeneration? A systematic review and meta-analysis. Br. J. Ophthalmol. 97, 389–394 (2013).
doi: 10.1136/bjophthalmol-2012-302281
Arnault, E. et al. Phototoxic action spectrum on a retinal pigment epithelium model of age-related macular degeneration exposed to sunlight normalized conditions. PLoS ONE 8, e71398 (2013).
doi: 10.1371/journal.pone.0071398
Sparrow, J. R., Nakanishi, K. & Parish, C. A. The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells. Investig. Ophthalmol. Vis. Sci. 41, 1981–1989 (2000).
Noell, W. K., Walker, V. S., Kang, B. S. & Berman, S. Retinal damage by light in rats. Investig. Ophthalmol. 5, 450–473 (1966).
Reme, C. E. The dark side of light: rhodopsin and the silent death of vision the proctor lecture. Investig. Ophthalmol. Vis. Sci. 46, 2671–2682 (2005).
doi: 10.1167/iovs.04-1094
Fain, G. L. & Lisman, J. E. Light, Ca
Organisciak, D. T. & Vaughan, D. K. Retinal light damage: mechanisms and protection. Prog. Retin Eye Res. 29, 113–134 (2010).
doi: 10.1016/j.preteyeres.2009.11.004
Grimm, C. et al. Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat. Genet. 25, 63–66 (2000).
doi: 10.1038/75614
Sperling, H. G., Wright, A. A. & Mills, S. L. Color vision following intense green light exposure: data and a model. Vis. Res. 31, 1797–1812 (1991).
doi: 10.1016/0042-6989(91)90027-3
Kanan, Y., Moiseyev, G., Agarwal, N., Ma, J. X. & Al-Ubaidi, M. R. Light induces programmed cell death by activating multiple independent proteases in a cone photoreceptor cell line. Investig. Ophthalmol. Vis. Sci. 48, 40–51 (2007).
doi: 10.1167/iovs.06-0592
Krishnamoorthy, R. R. et al. Photo-oxidative stress down-modulates the activity of nuclear factor-kappaB via involvement of caspase-1, leading to apoptosis of photoreceptor cells. J. Biol. Chem. 274, 3734–3743 (1999).
doi: 10.1074/jbc.274.6.3734
Natoli, R. et al. The role of pyruvate in protecting 661W photoreceptor-like cells against light-induced cell death. Curr. Eye Res. 41, 1473–1481 (2016).
doi: 10.3109/02713683.2016.1139725
Balse, E. et al. Purification of mammalian cone photoreceptors by lectin panning and the enhancement of their survival in glia-conditioned medium. Investig. Ophthalmol. Vis. Sci. 46, 367–374 (2005).
doi: 10.1167/iovs.04-0695
Sharma, R., Williams, D. R., Palczewska, G., Palczewski, K. & Hunter, J. J. Two-photon autofluorescence imaging reveals cellular structures throughout the retina of the living primate eye. Investig. Ophthalmol. Vis. Sci. 57, 632–646 (2016).
doi: 10.1167/iovs.15-17961
Boulton, M., Rozanowska, M. & Rozanowski, B. Retinal photodamage. J. Photochem. Photobiol. B 64, 144–161 (2001).
doi: 10.1016/S1011-1344(01)00227-5
Monici, M. Cell and tissue autofluorescence research and diagnostic applications. Biotechnol. Annu. Rev. 11, 227–256 (2005).
doi: 10.1016/S1387-2656(05)11007-2
Croce, A. C. & Bottiroli, G. Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis. Eur. J. Histochem. 58, 2461 (2014).
pubmed: 25578980
pmcid: 4289852
Kam, J. H. et al. Mitochondrial absorption of short wavelength light drives primate blue retinal cones into glycolysis which may increase their pace of aging. Vis. Neurosci. 36, E007 (2019).
doi: 10.1017/S0952523819000063
Papayan, G., Petrishchev, N. & Galagudza, M. Autofluorescence spectroscopy for NADH and flavoproteins redox state monitoring in the isolated rat heart subjected to ischemia-reperfusion. Photodiagnosis Photodyn. Ther. 11, 400–408 (2014).
doi: 10.1016/j.pdpdt.2014.05.003
Benson, R. C., Meyer, R. A., Zaruba, M. E. & McKhann, G. M. Cellular autofluorescenc—is it due to flavins? J. Histochem. Cytochem. 27, 44–48 (1979).
doi: 10.1177/27.1.438504
Narayan, D. S., Wood, J. P., Chidlow, G. & Casson, R. J. A review of the mechanisms of cone degeneration in retinitis pigmentosa. Acta Ophthalmol. 94, 748–754 (2016).
doi: 10.1111/aos.13141
dos Santos, A. F., de Almeida, D. R. Q., Terra, L. F., Baptista, M. S. & Labriola, L. Photodynamic therapy in cancer treatment—an update review. J. Cancer Metastasis Treat. 5, 25, https://doi.org/10.20517/2394-4722.2018.83 (2019).
Kou, J., Dou, D. & Yang, L. Porphyrin photosensitizers in photodynamic therapy and its applications. Oncotarget 8, 81591–81603 (2017).
doi: 10.18632/oncotarget.20189
Sternberg, E. D, D. & C, B. Porphyrin-based photosensitizers for use in photodynamic therapy. Tetrahedron 54, 4151–4202 (1998).
doi: 10.1016/S0040-4020(98)00015-5
Vandersee, S., Beyer, M., Lademann, J. & Darvin, M. E. Blue-violet light irradiation dose dependently decreases carotenoids in human skin, which indicates the generation of free radicals. Oxid. Med. Cell Longev. 2015, 579675 (2015).
doi: 10.1155/2015/579675
Lee, J. B. et al. Blue light-induced oxidative stress in human corneal epithelial cells: protective effects of ethanol extracts of various medicinal plant mixtures. Investig. Ophthalmol. Vis. Sci. 55, 4119–4127 (2014).
doi: 10.1167/iovs.13-13441
Kaido, M. et al. Reducing short-wavelength blue light in dry eye patients with unstable tear film improves performance on tests of visual acuity. PLoS ONE 11, e0152936 (2016).
doi: 10.1371/journal.pone.0152936
Chen, Y., Liu, Y. & Dorn, G. W. II Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ. Res. 109, 1327–1331 (2011).
doi: 10.1161/CIRCRESAHA.111.258723
Young, R. W. Solar radiation and age-related macular degeneration. Surv. Ophthalmol. 32, 252–269 (1988).
doi: 10.1016/0039-6257(88)90174-9
Sliney, D. H. Exposure geometry and spectral environment determine photobiological effects on the human eye. Photochem. Photobiol. 81, 483–489 (2005).
doi: 10.1562/2005-02-14-RA-439.1
Pastuszka, M. et al. Ocular findings in Polish Armed Forces in Iraq and Afghanistan, a review of medical examinations by The Military Medical Commission in Lodz. Klin. Ocz. 115, 296–299 (2013).
Marie, M. et al. Light action spectrum on oxidative stress and mitochondrial damage in A2E-loaded retinal pigment epithelium cells. Cell Death Dis. 9, 287 (2018).
doi: 10.1038/s41419-018-0331-5
Zhang, Y. et al. in Retinal Degeneration Diseases and Experimental Therapy (eds Hollyfield, J. G., Anderson, R. E., & LaVail, M. M.) 309–318 (Kluwer Academic: Plenum Publishers, 2001).
Craft, C. M., Huang, J., Possin, D. E. & Hendrickson, A. Primate short-wavelength cones share molecular markers with rods. Adv. Exp. Med. Biol. 801, 49–56 (2014).
doi: 10.1007/978-1-4614-3209-8_7