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BMC Complementary Medicine and Therapies

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Open Access 01-12-2024 | Research

Delphinidins from Maqui Berry (Aristotelia chilensis) ameliorate the subcellular organelle damage induced by blue light exposure in murine photoreceptor-derived cells

Authors: Kanta Yamazaki, Kodai Ishida, Wataru Otsu, Aomi Muramatsu, Shinsuke Nakamura, Wakana Yamada, Hideshi Tsusaki, Hiroshi Shimoda, Hideaki Hara, Masamitsu Shimazawa

Published in: BMC Complementary Medicine and Therapies | Issue 1/2024

Abstract

Background

Blue light exposure is known to induce reactive oxygen species (ROS) production and increased endoplasmic reticulum stress, leading to apoptosis of photoreceptors. Maqui berry (Aristotelia chilensis) is a fruit enriched in anthocyanins, known for beneficial biological activities such as antioxidation. In this study, we investigated the effects of Maqui berry extract (MBE) and its constituents on the subcellular damage induced by blue light irradiation in mouse retina-derived 661W cells.

Methods

We evaluated the effects of MBE and its main delphinidins, delphinidin 3-O-sambubioside-5-O-glucoside (D3S5G) and delphinidin 3,5-O-diglucoside (D3G5G), on blue light-induced damage on retinal cell line 661W cells. We investigated cell death, the production of ROS, and changes in organelle morphology using fluorescence microscopy. The signaling pathway linked to stress response was evaluated by immunoblotting in the whole cell lysates or nuclear fractions. We also examined the effects of MBE and delphinidins against rotenone-induced mitochondrial dysfunction.

Results

Blue light-induced cell death, increased intracellular ROS generation and mitochondrial fragmentation, decreased ATP-production coupled respiration, caused lysosomal membrane permeabilization, and increased ATF4 protein level. Treatment with MBE and its main constituents, delphinidin 3-O-sambubioside-5-O-glucoside and delphinidin 3,5-O-diglucoside, prevented these defects. Furthermore, MBE and delphinidins also protected 661W cells from rotenone-induced cell death.

Conclusions

Maqui berry may be a useful protective agent for photoreceptors against the oxidative damage induced by exposure to blue light.

Graphical abstract

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Cruickshanks KJ, Klein R, Klein BE, Nondahl DM. Sunlight and the 5-year incidence of early age-related maculopathy: the beaver dam eye study. Arch Ophthalmol. 2001;119(2):246–50.PubMed

Kuse Y, Ogawa K, Tsuruma K, Shimazawa M, Hara H. Damage of photoreceptor-derived cells in culture induced by light emitting diode-derived blue light. Sci Rep. 2014;4:5223.CrossRefPubMedPubMedCentral

Ooe E, Tsuruma K, Kuse Y, Kobayashi S, Shimazawa M, Hara H. The involvement of ATF4 and S-opsin in retinal photoreceptor cell damage induced by blue LED light. Mol Vis. 2017;23:52–9.PubMedPubMedCentral

Nolfi-Donegan D, Braganza A, Shiva S. Mitochondrial electron transport chain: oxidative phosphorylation, oxidant production, and methods of measurement. Redox Biol. 2020;37:101674.CrossRefPubMedPubMedCentral

Godley BF, Shamsi FA, Liang FQ, Jarrett SG, Davies S, Boulton M. Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J Biol Chem. 2005;280(22):21061–6.CrossRefPubMed

Bellezza I. Oxidative stress in Age-Related Macular Degeneration: Nrf2 as therapeutic target. Front Pharmacol. 2018;9:1280.CrossRefPubMedPubMedCentral

Tanaka J, Kadekaru T, Ogawa K, Hitoe S, Shimoda H, Hara H. Maqui Berry (Aristotelia chilensis) and the constituent delphinidin glycoside inhibit photoreceptor cell death induced by visible light. Food Chem. 2013;139(1–4):129–37.CrossRefPubMed

Husain A, Chanana H, Khan SA, Dhanalekshmi UM, Ali M, Alghamdi AA, Ahmad A. Chemistry and pharmacological actions of Delphinidin, a Dietary Purple Pigment in Anthocyanidin and Anthocyanin forms. Front Nutr. 2022;9:746881.CrossRefPubMedPubMedCentral

Ooe E, Kuse Y, Yako T, Sogon T, Nakamura S, Hara H, Shimazawa M. Bilberry extract and anthocyanins suppress unfolded protein response induced by exposure to blue LED light of cells in photoreceptor cell line. Mol Vis. 2018;24:621–32.PubMedPubMedCentral

10.

Tan E, Ding XQ, Saadi A, Agarwal N, Naash MI, Al-Ubaidi MR. Expression of cone-photoreceptor-specific antigens in a cell line derived from retinal tumors in transgenic mice. Invest Ophthalmol Vis Sci. 2004;45(3):764–8.CrossRefPubMed

11.

Ishida K, Yako T, Tanaka M, Otsu W, Nakamura S, Shimazawa M, Tsusaki H, Hara H. Free-radical scavenger NSP-116 protects the corneal epithelium against UV-A and blue LED light exposure. Biol Pharm Bull. 2021;44(7):937–46.CrossRefPubMed

12.

Otsu W, Ishida K, Nakamura S, Shimazawa M, Tsusaki H, Hara H. Blue light-emitting diode irradiation promotes transcription factor EB-mediated lysosome biogenesis and lysosomal cell death in murine photoreceptor-derived cells. Biochem Biophys Res Commun. 2020;526(2):479–84.CrossRefPubMed

13.

Yako T, Kuse Y, Nakamura S, Shimazawa M, Motomura T, Hara H. The Protective Effect of Blue Light cutting particles mixed optical material against blue LED Light-Induced photoreceptor and cornea cell death. J Sci Technol Lighting. 2019;42:29–32.CrossRef

14.

Otsu W, Ishida K, Chinen N, Nakamura S, Shimazawa M, Tsusaki H, Hara H. Cigarette smoke extract and heated Tobacco products promote ferritin cleavage and iron accumulation in human corneal epithelial cells. Sci Rep. 2021;11(1):18555.CrossRefPubMedPubMedCentral

15.

Otsu W, Yako T, Sugisawa E, Nakamura S, Tsusaki H, Umigai N, Shimazawa M, Hara H. Crocetin protects against mitochondrial damage induced by UV-A irradiation in corneal epithelial cell line HCE-T cells. J Pharmacol Sci. 2022;150(4):279–88.CrossRefPubMed

16.

Liu GY, Sabatini DM. mTOR at the nexus of nutrition, growth, ageing and Disease. Nat Rev Mol Cell Biol. 2020;21(4):183–203.CrossRefPubMedPubMedCentral

17.

Yapa NMB, Lisnyak V, Reljic B, Ryan MT. Mitochondrial dynamics in health and Disease. FEBS Lett. 2021;595(8):1184–204.CrossRefPubMed

18.

Greenamyre JT, Cannon JR, Drolet R, Mastroberardino PG. Lessons from the rotenone model of Parkinson’s Disease. Trends Pharmacol Sci. 2010;31(4):141–2. author reply 142–143.CrossRefPubMedPubMedCentral

19.

Heinonen M. Antioxidant activity and antimicrobial effect of berry phenolics–a Finnish perspective. Mol Nutr Food Res. 2007;51(6):684–91.CrossRefPubMed

20.

Ogawa K, Sakakibara H, Iwata R, Ishii T, Sato T, Goda T, Shimoi K, Kumazawa S. Anthocyanin composition and antioxidant activity of the Crowberry (Empetrum nigrum) and other berries. J Agric Food Chem. 2008;56(12):4457–62.CrossRefPubMed

21.

Milbury PE, Vita JA, Blumberg JB. Anthocyanins are bioavailable in humans following an acute dose of cranberry juice. J Nutr. 2010;140(6):1099–104.CrossRefPubMed

22.

Schon C, Wacker R, Micka A, Steudle J, Lang S, Bonnlander B. Bioavailability Study of Maqui Berry Extract in healthy subjects. Nutrients 2018, 10(11).

23.

Kalt W, Blumberg JB, McDonald JE, Vinqvist-Tymchuk MR, Fillmore SA, Graf BA, O’Leary JM, Milbury PE. Identification of anthocyanins in the liver, eye, and brain of blueberry-fed pigs. J Agric Food Chem. 2008;56(3):705–12.CrossRefPubMed

24.

Matsumoto H, Nakamura Y, Iida H, Ito K, Ohguro H. Comparative assessment of distribution of blackcurrant anthocyanins in rabbit and rat ocular tissues. Exp Eye Res. 2006;83(2):348–56.CrossRefPubMed

25.

Kasai S, Shimizu S, Tatara Y, Mimura J, Itoh K. Regulation of Nrf2 by mitochondrial reactive oxygen species in Physiology and Pathology. Biomolecules 2020, 10(2).

26.

Kam JH, Hogg C, Fosbury R, Shinhmar H, Jeffery G. Mitochondria are specifically vulnerable to 420nm light in drosophila which undermines their function and is associated with reduced fly mobility. PLoS ONE. 2021;16(9):e0257149.CrossRefPubMedPubMedCentral

27.

Li JY, Zhang K, Xu D, Zhou WT, Fang WQ, Wan YY, Yan DD, Guo MY, Tao JX, Zhou WC, et al. Mitochondrial fission is required for Blue Light-Induced apoptosis and Mitophagy in Retinal neuronal R28 cells. Front Mol Neurosci. 2018;11:432.CrossRefPubMedPubMedCentral

28.

Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science. 2011;334(6056):678–83.CrossRefPubMedPubMedCentral

29.

Kim SG, Hoffman GR, Poulogiannis G, Buel GR, Jang YJ, Lee KW, Kim BY, Erikson RL, Cantley LC, Choo AY, et al. Metabolic stress controls mTORC1 lysosomal localization and dimerization by regulating the TTT-RUVBL1/2 complex. Mol Cell. 2013;49(1):172–85.CrossRefPubMed

30.

Heid ME, Keyel PA, Kamga C, Shiva S, Watkins SC, Salter RD. Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J Immunol. 2013;191(10):5230–8.CrossRefPubMed

31.

Wang F, Gomez-Sintes R, Boya P. Lysosomal membrane permeabilization and cell death. Traffic. 2018;19(12):918–31.CrossRefPubMed

32.

Strathearn KE, Yousef GG, Grace MH, Roy SL, Tambe MA, Ferruzzi MG, Wu QL, Simon JE, Lila MA, Rochet JC. Neuroprotective effects of anthocyanin- and proanthocyanidin-rich extracts in cellular models of Parkinson׳s Disease. Brain Res. 2014;1555:60–77.CrossRefPubMedPubMedCentral

Title: Delphinidins from Maqui Berry (Aristotelia chilensis) ameliorate the subcellular organelle damage induced by blue light exposure in murine photoreceptor-derived cells
Authors: Kanta Yamazaki
Kodai Ishida
Wataru Otsu
Aomi Muramatsu
Shinsuke Nakamura
Wakana Yamada
Hideshi Tsusaki
Hiroshi Shimoda
Hideaki Hara
Masamitsu Shimazawa
Publication date: 01-12-2024
Publisher: BioMed Central
Published in: BMC Complementary Medicine and Therapies / Issue 1/2024
Electronic ISSN: 2662-7671
DOI: https://doi.org/10.1186/s12906-023-04322-z

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Delphinidins from Maqui Berry (Aristotelia chilensis) ameliorate the subcellular organelle damage induced by blue light exposure in murine photoreceptor-derived cells

Abstract

Background

Methods

Results

Conclusions

Graphical abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Graphical abstract

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