Oxidative and carbonyl stress induced AMD and Codonopsis lanceolata ameliorates AMD via controlling oxidative and carbonyl stress.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
15 Jul 2024
Historique:
received: 26 02 2024
accepted: 08 07 2024
medline: 16 7 2024
pubmed: 16 7 2024
entrez: 15 7 2024
Statut: epublish

Résumé

Age-related macular degeneration (AMD) is one of the leading causes of blindness. AMD is currently incurable; the best solution is to prevent its occurrence. To develop drugs for AMD, it is crucial to have a model system that mimics the symptoms and mechanisms in patients. It is most important to develop safer and more effective anti-AMD drug. In this study, the dose of A2E and the intensity of blue light were evaluated to establish an appropriate atrophic in vitro model of AMD and anti-AMD effect and therapeutic mechanism of Codonopsis lanceolata. The experimental groups included a control group an AMD group treated with A2E and blue light, a lutein group treated with 25 μM lutein after AMD induction, and three groups treated with different doses of C. lanceolata (10, 20, and 50 μg/mL) after AMD induction. Intrinsic apoptotic pathway (Bcl-2 family), anti-oxidative system (Keap1/Nrf2/HO-1 antioxidant response element), and anti-carbonyl effect (4-hydroxynonenal [4-HNE]) were evaluated using immunofluorescence, MTT, TUNEL, FACS, and western blotting analyses. A2E accumulation in the cytoplasm of ARPE-19 cells depending on the dose of A2E. Cell viability of ARPE-19 cells according to the dose of A2E and/or blue light intensity. The population of apoptotic or necrotic cells increased based on the A2E dose and blue light intensity. Codonopsis lanceolata dose-dependently prevented cell death which was induced by A2E and blue light. The antiapoptotic effect of that was caused by activating Keap1/Nrf2/HO-1 pathway, suppressing 4-HNE, and modulating Bcl-2 family proteins like increase of antiapoptotic proteins such as Bcl-2 and Bcl-XL and decrease of proapoptotic protein such as Bim. Based on these findings, 30 μM A2E and 20 mW/cm

Identifiants

pubmed: 39009704
doi: 10.1038/s41598-024-67044-3
pii: 10.1038/s41598-024-67044-3
doi:

Substances chimiques

NF-E2-Related Factor 2 0
Plant Extracts 0
NFE2L2 protein, human 0
Antioxidants 0
Kelch-Like ECH-Associated Protein 1 0
Aldehydes 0
4-hydroxy-2-nonenal K1CVM13F96
KEAP1 protein, human 0
Proto-Oncogene Proteins c-bcl-2 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

16322

Subventions

Organisme : the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT)
ID : 2022R1A5A8033794

Informations de copyright

© 2024. The Author(s).

Références

Jonas, J. B. et al. Updates on the epidemiology of age-related macular degeneration. Asia-Pac J. Ophthalmol. 6, 493–497 (2017).
Wang, Y. et al. Global incidence, progression, and risk factors of age-related macular degeneration and projection of disease statistics in 30 years: A modeling study. Gerontol. 68, 721–735 (2022).
doi: 10.1159/000518822
The Eye Diseases Prevalence Research Group. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 122, 564–572 (2004).
doi: 10.1001/archopht.122.4.564
World Health Organization, Ageing and health. https://www.who.int/news-room/fact-sheets/detail/ageing-and-health . Accessed 26th Jan 2023 (2023).
Crouch, R. K., Koutalos, Y., Kono, M., Schey, K. & Ablonczy, Z. A2E and lipofuscin. Prog. Mol. Biol. Transl. Sci. 134, 449–463 (2015).
pubmed: 26310170 doi: 10.1016/bs.pmbts.2015.06.005
Lamb, L. E. & Simon, J. D. A2E: A component of ocular lipofuscin. Photochem. Photobiol. 79(2), 127–136 (2004).
pubmed: 15068025 doi: 10.1111/j.1751-1097.2004.tb00002.x
Chakravarthy, U. et al. Clinical risk factors for age-related macular degeneration: A systematic review and meta-analysis. BMC Ophthalmol. 10, 31 (2010).
pubmed: 21144031 pmcid: 3009619 doi: 10.1186/1471-2415-10-31
Zhang, Q. Y. et al. Overweight, obesity and risk of age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 57, 1276–1283 (2016).
pubmed: 26990164 doi: 10.1167/iovs.15-18637
Bhutto, I. & Lutty, G. Understanding age-related macular degeneration (AMD): Relationships between the photoreceptor/retinal pigment epithelium/Bruch’s membrane/choriocapillaris complex. Mol. Aspects Med. 33, 295–317 (2012).
pubmed: 22542780 pmcid: 3392421 doi: 10.1016/j.mam.2012.04.005
Cho, Y. K., Park, D. H. & Jeon, I. C. Medication trends for age-related macular degeneration. Int. J. Mol. Sci. 22, 11837 (2021).
pubmed: 34769270 pmcid: 8584051 doi: 10.3390/ijms222111837
Mainster, M. A. & Reichal, E. Transpupillary thermotherapy for age-related macular degeneration: Long-pulse photocoagulation, apoptosis, and heat shock proteins. Ophthalmic Surg. Lasers 31, 359–373 (2000).
pubmed: 11011704 doi: 10.3928/1542-8877-20000901-03
Bresnick, G. H. Diabetic maculopathy. A critical review highlighting diffuse macular edema. Ophthalmology 90, 1301–1317 (1983).
pubmed: 6664669 doi: 10.1016/S0161-6420(83)34388-8
Kapugi, M. & Cunningham, K. Corticosteroids. Orthop. Nurs. 38, 336–339 (2019).
pubmed: 31568125 doi: 10.1097/NOR.0000000000000595
Falavarjani, K. G. & Nguyen, Q. D. Adverse events and complications associated with intravitreal injection of anti-VEGF agents: A review of literature. Eye 27, 787–794 (2013).
pubmed: 23722722 doi: 10.1038/eye.2013.107
Moon, J. et al. Blue light effect on retinal pigment epithelial cells by display devices. Integr. Biol. 9(5), 436–443 (2017).
doi: 10.1039/C7IB00032D
Alaimo, A. et al. Toxicity of blue led light and A2E is associated to mitochondrial dynamics impairment in ARPE-19 cells: Implications for age-related macular degeneration. Arch. Toxicol. 93, 1401–1415 (2019).
pubmed: 30778631 doi: 10.1007/s00204-019-02409-6
Sparrow, J. R. & Cai, B. Blue light-induced apoptosis of A2E-containing RPE: Involvement of caspase-3 and protection by Bcl-2. Invest. Ophthalmol. Vis. Sci. 42(6), 1356–1362 (2001).
pubmed: 11328751
Govindaraju, V. K., Bodas, M. & Vij, N. Cigarette smoke induced autophagy-impairment regulates AMD pathogenesis mechanisms in ARPE-19 cells. PLoS ONE 12(8), e0182420 (2017).
pubmed: 28767736 pmcid: 5540403 doi: 10.1371/journal.pone.0182420
Hanus, J. et al. Induction of necrotic cell death by oxidative stress in retinal pigment epithelial cells. Cell Death Dis. 4, e965 (2013).
pubmed: 24336085 pmcid: 3877549 doi: 10.1038/cddis.2013.478
Kuo, S. C. et al. Potassium bromate-induced cell model of age-related macular degeneration in vitro. Mol. Med. Rep. 23(3), 216 (2021).
pubmed: 33495823 doi: 10.3892/mmr.2021.11855
Aung, K. H., Liu, H., Ke, Z., Jiang, S. & Huang, J. Glabridin attenuates the retinal degeneration induced by sodium iodate in vitro and in vivo. Front. Pharmacol. 11, 566699 (2020).
pubmed: 33178017 pmcid: 7593553 doi: 10.3389/fphar.2020.566699
Wang, L., Xu, M. L., Hu, J. H., Rasmussen, S. K. & Wang, M. H. Codonopsis laceolata extract induces G1/G1 arrest and apoptosis in human colon tumor HT-29 cells—involvement of ROS generation and polyamine depletion. Food Chem. Toxicol. 49, 149–154 (2011).
pubmed: 20940027 doi: 10.1016/j.fct.2010.10.010
Lee, J. S. et al. Codonopsis laceolata extract prevents diet-induced obesity in C57BL/6 mice. Nutrients 6, 4663–4677 (2014).
pubmed: 25353662 pmcid: 4245555 doi: 10.3390/nu6114663
Cha, A. et al. Antilipogenic and anti-inflammatory activities of Codonopsis laceolata in mice hepatic tissues after chronic ethanol feeding. J. Biomed. Biotechnol. 2012, 141395 (2012).
pubmed: 22013387 doi: 10.1155/2012/141395
Lee, Y. G. et al. Regulatory effects of Codonopsis laceolata on macrophage-mediated immune responses. J. Ethnopharmacol. 112, 180–188 (2007).
pubmed: 17418512 doi: 10.1016/j.jep.2007.02.026
Bok, S. H., Han, K. M., Boo, H. O., Cho, S. S. & Park, D. H. Codonopsis laceolata water extract ameliorates asthma severity by inducing Th2 cells’ and pulmonary epithelial cells’ apoptosis via NF-κB/COX-2 pathway. Processes 10, 1249 (2022).
doi: 10.3390/pr10071249
Parish, C. A., Hashimoto, M., Nakanishi, K., Dillon, J. & Janet, S. Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc. Natl. Acad. Sci. USA 95(25), 14609–14613 (1998).
pubmed: 9843937 pmcid: 24497 doi: 10.1073/pnas.95.25.14609
Song, S. Y. et al. Standardization of diploid Codonopsis laceolata root extract as an anti-hyperuricemic source. Processes 9, 2065 (2021).
doi: 10.3390/pr9112065
Taylor, H. R. et al. Visible light and risk of age-related macular degeneration. Trans. Am. Ophthalmol. Soc. 88, 163–173 (1990).
pubmed: 2095019 pmcid: 1298584
Sparrow, J. R., Parish, C. A., Hashimoto, M. & Nakanishi, K. A2E, a lipofuscin fluorophore, in human retinal pigmented epithelial cells in culture. Invest. Ophthalmol. Vis. Sci. 40(12), 2988–2995 (1999).
pubmed: 10549662
Cho, Y. K. et al. The age-related macular degeneration (AMD)-preventing mechanism of natural products. Processes 10, 678 (2022).
doi: 10.3390/pr10040678
Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol. 35(4), 495–516 (2007).
pubmed: 17562483 pmcid: 2117903 doi: 10.1080/01926230701320337
Loboda, A., Damulewicz, M., Pyza, E., Jozkowicz, A. & Dulak, J. Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: An evolutionarily conserved mechanism. Cell Mol. Life Sci. 73, 3221–3247 (2016).
pubmed: 27100828 pmcid: 4967105 doi: 10.1007/s00018-016-2223-0
Biswas, S. K. Does the interdependence between oxidative stress and inflammation explain the antioxidant paradox?. Oxid. Med. Cell Longev. 2016, 5698931 (2016).
pubmed: 26881031 pmcid: 4736408 doi: 10.1155/2016/5698931
Imammura, T. et al. Hydroxyl radicals cause fluctuation in intracellular ferrous ion levels upon light exposure during photoreceptor cell death. Exp. Eye Res. 129, 24–30 (2014).
doi: 10.1016/j.exer.2014.10.019
Marie, M. et al. Light action spectrum on oxidative stress and mitochondrial damage in A2E-loaded retinal pigment epithelium cells. Cell Death. Dis. 9(3), 287 (2018).
pubmed: 29459695 pmcid: 5833722 doi: 10.1038/s41419-018-0331-5
Kaczara, P., Sarna, T. & Burke, J. M. Dynamics of H
pubmed: 20100568 pmcid: 2839027 doi: 10.1016/j.freeradbiomed.2010.01.022
Evereklioglu, C. et al. Nitric oxide and lipid peroxidation are increased and associated with decreased antioxidant enzyme activities in patients with age-related macular degeneration. Documenta. Ophthalmol. 106, 129–136 (2003).
doi: 10.1023/A:1022512402811
Totan, Y. et al. Plasma malondialdehyde and nitric oxide levels in age related macular degeneration. Br. J. Ophthalmol. 85, 1426–1428 (2001).
pubmed: 11734513 pmcid: 1723807 doi: 10.1136/bjo.85.12.1426
Collins, T. Acute and Chronic Inflammation. In Robbins Pathologic Basis of Disease (eds Cotran, R. S. et al.) 50–88 (W.B. Saunders, 1999).
Flohe, L., Brigelius-Flohe, R., Saliou, C., Traber, M. G. & Packer, L. Redox regulation of NF-κB activation. Free Radical Bio. Med. 22(6), 1115–1126 (1997).
doi: 10.1016/S0891-5849(96)00501-1
de Freitas, S. M. et al. The Keap1/Nrf2-ARE pathway as a pharmacological target for chalcones. Molecules 23, 1803 (2018).
doi: 10.3390/molecules23071803
Lu, M. C., Ji, J. A., Jiang, Z. Y. & You, Q. D. The Keap1-Nrf2-ARE pathway as a potential preventive and therapeutic target: An update. Med. Res. Rev. 36, 924–963 (2016).
pubmed: 27192495 doi: 10.1002/med.21396
Zoccali, C., Mallamaci, F. & Tripepi, G. AGEs and carbonyl stress: Potential pathogenetic factors of long-term uraemic complications. Nephrol. Dial. Transplant 15(Suppl 2), 7–11 (2000).
pubmed: 11051031 doi: 10.1093/ndt/15.suppl_1.7
Kauppinen, A. H. et al. Oxidative stress activates NLRP3 inflammasomes in ARPE-19 cells-Implications for age-related macular degeneration (AMD). Immunol. Lett. 147, 29–33 (2012).
pubmed: 22698681 doi: 10.1016/j.imlet.2012.05.005
Long, E. K. & Picklo, M. J. Sr. Trans-4-hydroxy-2-hexenal, a product of n-3 fatty acid peroxidation: Make some room HNE…. Free Radic. Biol. Med. 49(1), 1–8 (2010).
pubmed: 20353821 doi: 10.1016/j.freeradbiomed.2010.03.015
Pinna, A., Boscia, F., Paligiannis, P., Carru, C. & Zinellu, A. Malondialdehyde levels in patients with age-related macular degeneration: A systematic review and meta-analysis. Retina 40(2), 195–203 (2020).
pubmed: 31972788 doi: 10.1097/IAE.0000000000002574
Chicheportiche, Y. et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J. Biol. Chem. 272, 32401–32410 (1997).
pubmed: 9405449 doi: 10.1074/jbc.272.51.32401
Ashkenazi, A. & Dixit, V. M. Death receptors: Signaling and modulation. Science 281, 1305–1308 (1998).
pubmed: 9721089 doi: 10.1126/science.281.5381.1305
Suliman, A., Lam, A., Datta, R. & Srivastava, R. K. Intracellular mechanisms of TRAIL: Apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 20, 2122–2133 (2001).
pubmed: 11360196 doi: 10.1038/sj.onc.1204282
Cory, S. & Adams, J. M. The Bcl2 family: Regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647–656 (2002).
pubmed: 12209154 doi: 10.1038/nrc883

Auteurs

Soon-Young Lee (SY)

College of Korean Medicine, Dongshin University, Naju, 58245, Jeonnam, Korea.

Yeon-Kyoung Cho (YK)

College of Health and Welfare, Dongshin University, Naju, 58245, Jeonnam, Korea.

Chun-Sik Bae (CS)

College of Veterinary Medicine, Chonnam National University, Gwangju, 61186, Korea.

Gyeyeop Kim (G)

College of Health and Welfare, Dongshin University, Naju, 58245, Jeonnam, Korea.

Min-Jae Lee (MJ)

College of Veterinary Medicine, Kangwon National University, Chuncheon, 24341, Gangwon, Korea.

Seung-Sik Cho (SS)

Department of Biomedicine, Health & Life Convergence Sciences, BK21 Four, Biomedical and Healthcare Research Institute, Mokpo National University, Muan, 58554, Jeonnam, Korea. sscho@mokpo.ac.kr.
Department of Pharmacy, College of Pharmacy, Mokpo National University, Muan, 58579, Jeonnam, Korea. sscho@mokpo.ac.kr.

In-Chul Jeon (IC)

College of Health and Welfare, Dongshin University, Naju, 58245, Jeonnam, Korea. icjeon@dsu.ac.kr.

Dae-Hun Park (DH)

College of Korean Medicine, Dongshin University, Naju, 58245, Jeonnam, Korea. dhj1221@hanmail.net.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH