Indenopyrene and Blue-Light Co-Exposure Impairs the Tightly Controlled Activation of Xenobiotic Metabolism in Retinal Pigment Epithelial Cells: A Mechanism for Synergistic Toxicity
Abstract
:1. Introduction
2. Results
2.1. IcdP/HEV-Induced Oxidative Stress Is Not a Direct Consequence of Photosensitized Oxidation Reactions
2.2. ROS Generation Is Stimulated by IcdP/HEV for at Least 6 h after Co-Exposure
2.3. IcdP/HEV Co-Exposure Leads to the Accumulation of Bulky DNA Adducts
2.4. Increased AhR Activation and Decreased Nrf2 Levels after IcdP/HEV Co-Exposure
2.5. IcdP/HEV Co-Exposure Leads to Transcriptional Over-Activation of CYP1 Genes
2.6. IcdP/HEV Co-Exposure Is Associated with a Depletion of GST Enzymes
3. Discussion
3.1. Photo-Oxidative Stress Is Not the Driving Mechanism of IcdP/HEV Synergistic Toxicity
3.2. IcdP/HEV Co-Exposure Induces an Unbalanced Metabolic Response in RPE Cells
3.3. Unbalanced Activation of Phase I and II Metabolism after IcdP/HEV Co-Exposure
3.4. α-Tocopherol Prevents Phase I and II Uncoupling
4. Materials and Methods
4.1. Cell Culture
4.2. Light Source and Dosimetry
4.3. Indeno[1,2,3-cd]Pyrene Exposure and Light Irradiation Procedure
4.4. Antioxidant/Quencher Treatments
4.5. Cytotoxicity Assessment
4.6. ROS Content and Accumulation Kinetics
4.7. IcdP-Related Genotoxicity Assessment
4.8. Expression of Genes Involved in PAH Metabolism
4.9. Protein Isolation and Western Blot Assays
4.10. Statistical Analysis
5. Concluding Remarks
Supplementary Materials
Author Contributions
Funding
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Boettner, E.A.; Wolter, J.R. Transmission of the ocular media. Investig. Ophthalmol. Vis. Sci. 1962, 1, 776–783. [Google Scholar]
- Taylor, H.R.; West, S.; Munoz, B.; Rosenthal, F.S.; Bressler, S.B.; Bressler, N.M. The long-term effects of visible light on the eye. Arch. Ophthalmol. 1992, 110, 99–104. [Google Scholar] [CrossRef]
- Sui, G.Y.; Liu, G.C.; Liu, G.Y.; Gao, Y.Y.; Deng, Y.; Wang, W.Y.; Tong, S.H.; Wang, L. Is sunlight exposure a risk factor for age-related macular degeneration? A systematic review and meta-analysis. Br. J. Ophthalmol. 2013, 97, 389–394. [Google Scholar] [CrossRef]
- Schick, T.; Ersoy, L.; Lechanteur, Y.T.; Saksens, N.T.; Hoyng, C.B.; den Hollander, A.I.; Kirchhof, B.; Fauser, S. History of Sunlight Exposure Is a Risk Factor for Age-Related Macular Degeneration. Retina 2016, 36, 787–790. [Google Scholar] [CrossRef]
- Bourne, R.R.; Stevens, G.A.; White, R.A.; Smith, J.L.; Flaxman, S.R.; Price, H.; Jonas, J.B.; Keeffe, J.; Leasher, J.; Naidoo, K.; et al. Causes of vision loss worldwide, 1990–2010: A systematic analysis. Lancet Glob. Health 2013, 1, e339–e349. [Google Scholar] [CrossRef]
- Wong, W.L.; Su, X.; Li, X.; Cheung, C.M.; Klein, R.; Cheng, C.Y.; Wong, T.Y. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: A systematic review and meta-analysis. Lancet Glob. Health 2014, 2, e106–e116. [Google Scholar] [CrossRef]
- Young, R.W. Pathophysiology of age-related macular degeneration. Surv. Ophthalmol. 1987, 31, 291–306. [Google Scholar] [CrossRef]
- Ambati, J.; Fowler, B.J. Mechanisms of age-related macular degeneration. Neuron 2012, 75, 26–39. [Google Scholar] [CrossRef]
- Shichi, H.; Atlas, S.A.; Nebert, D.W. Genetically regulated aryl hydrocarbon hydroxylase induction in the eye: Possible significance of the drug-metabolizing enzyme system for the retinal pigmented epithelium-choroid. Exp. Eye Res. 1975, 21, 557–567. [Google Scholar] [CrossRef]
- Schwartzman, M.L.; Masferrer, J.; Dunn, M.W.; McGiff, J.C.; Abraham, N.G. Cytochrome P450, drug metabolizing enzymes and arachidonic acid metabolism in bovine ocular tissues. Curr. Eye Res. 1987, 6, 623–630. [Google Scholar] [CrossRef]
- Strauss, O. The retinal pigment epithelium in visual function. Physiol. Rev. 2005, 85, 845–881. [Google Scholar] [CrossRef]
- Wihlmark, U.; Wrigstad, A.; Roberg, K.; Nilsson, S.E.; Brunk, U.T. Lipofuscin accumulation in cultured retinal pigment epithelial cells causes enhanced sensitivity to blue light irradiation. Free Radic. Biol. Med. 1997, 22, 1229–1234. [Google Scholar] [CrossRef] [PubMed]
- Winkler, B.S.; Boulton, M.E.; Gottsch, J.D.; Sternberg, P. Oxidative damage and age-related macular degeneration. Mol. Vis. 1999, 5, 32. [Google Scholar] [PubMed]
- King, A.; Gottlieb, E.; Brooks, D.G.; Murphy, M.P.; Dunaief, J.L. Mitochondria-derived reactive oxygen species mediate blue light-induced death of retinal pigment epithelial cells. Photochem. Photobiol. 2004, 79, 470–475. [Google Scholar]
- Wielgus, A.R.; Collier, R.J.; Martin, E.; Lih, F.B.; Tomer, K.B.; Chignell, C.F.; Roberts, J.E. Blue light induced A2E oxidation in rat eyes—Experimental animal model of dry AMD. Photochem. Photobiol. Sci. 2010, 9, 1505–1512. [Google Scholar] [CrossRef]
- Rozanowska, M.; Jarvis-Evans, J.; Korytowski, W.; Boulton, M.E.; Burke, J.M.; Sarna, T. Blue light-induced reactivity of retinal age pigment. In vitro generation of oxygen-reactive species. J. Biol. Chem. 1995, 270, 18825–18830. [Google Scholar] [CrossRef] [PubMed]
- 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. 2000, 41, 1981–1989. [Google Scholar]
- Sparrow, J.R.; Zhou, J.; Cai, B. DNA is a target of the photodynamic effects elicited in A2E-laden RPE by blue-light illumination. Investig. Ophthalmol. Vis. Sci. 2003, 44, 2245–2251. [Google Scholar] [CrossRef]
- Kim, S.R.; Jang, Y.P.; Jockusch, S.; Fishkin, N.E.; Turro, N.J.; Sparrow, J.R. The all-trans-retinal dimer series of lipofuscin pigments in retinal pigment epithelial cells in a recessive Stargardt disease model. Proc. Natl. Acad. Sci. USA 2007, 104, 19273–19278. [Google Scholar] [CrossRef]
- Smick, K.; Villette, T.; Boulton, M.; Brainard, G.C.; Jones, W.; Karpecki, P.; Melton, R.; Thomas, R.; Sliney, D.H.; Shechtman, D.L. Blue Light Hazard: New Knowledge, New Approaches to Maintaining Ocular Health; Report of a Roundtable; Essilor of America: New York, NY, USA, 2013. [Google Scholar]
- Zinflou, C.; Rochette, P.J. Absorption of blue light by cigarette smoke components is highly toxic for retinal pigmented epithelial cells. Arch. Toxicol. 2019, 93, 453–465. [Google Scholar] [CrossRef]
- Roberto, A.; Larsson, B.S.; Tjalve, H. Uptake of 7,12-dimethylbenz(a)anthracene and benzo(a)pyrene in melanin-containing tissues. Pharmacol. Toxicol. 1996, 79, 92–99. [Google Scholar] [CrossRef]
- Briede, J.J.; Godschalk, R.W.; Emans, M.T.; De Kok, T.M.; Van Agen, E.; Van Maanen, J.; Van Schooten, F.J.; Kleinjans, J.C. In vitro and in vivo studies on oxygen free radical and DNA adduct formation in rat lung and liver during benzo[a]pyrene metabolism. Free Radic. Res. 2004, 38, 995–1002. [Google Scholar] [CrossRef]
- Zangar, R.C.; Davydov, D.R.; Verma, S. Mechanisms that regulate production of reactive oxygen species by cytochrome P450. Toxicol. Appl. Pharmacol. 2004, 199, 316–331. [Google Scholar] [CrossRef] [PubMed]
- Shimada, T. Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab. Pharmacokinet. 2006, 21, 257–276. [Google Scholar] [CrossRef] [PubMed]
- Moorthy, B.; Chu, C.; Carlin, D.J. Polycyclic aromatic hydrocarbons: From metabolism to lung cancer. Toxicol. Sci. 2015, 145, 5–15. [Google Scholar] [CrossRef] [PubMed]
- Sims, P.; Grover, P.L.; Swaisland, A.; Pal, K.; Hewer, A. Metabolic activation of benzo(a)pyrene proceeds by a diol-epoxide. Nature 1974, 252, 326–328. [Google Scholar] [CrossRef] [PubMed]
- Rice, J.E.; Coleman, D.T.; Hosted, T.J., Jr.; LaVoie, E.J.; McCaustland, D.J.; Wiley, J.C., Jr. Identification of mutagenic metabolites of indeno[1,2,3-cd]pyrene formed in vitro with rat liver enzymes. Cancer Res. 1985, 45, 5421–5425. [Google Scholar]
- Rice, J.E.; Hosted, T.J., Jr.; DeFloria, M.C.; LaVoie, E.J.; Fischer, D.L.; Wiley, J.C., Jr. Tumor-initiating activity of major in vivo metabolites of indeno[1,2,3-cd]pyrene on mouse skin. Carcinogenesis 1986, 7, 1761–1764. [Google Scholar] [CrossRef] [PubMed]
- Genies, C.; Maitre, A.; Lefebvre, E.; Jullien, A.; Chopard-Lallier, M.; Douki, T. The extreme variety of genotoxic response to benzo[a]pyrene in three different human cell lines from three different organs. PLoS One 2013, 8, e78356. [Google Scholar] [CrossRef]
- Nebert, D.W.; Dalton, T.P.; Okey, A.B.; Gonzalez, F.J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279, 23847–23850. [Google Scholar] [CrossRef]
- Kohle, C.; Bock, K.W. Coordinate regulation of Phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2. Biochem. Pharmacol. 2007, 73, 1853–1862. [Google Scholar] [CrossRef]
- Nguyen, T.; Sherratt, P.J.; Pickett, C.B. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 2003, 43, 233–260. [Google Scholar] [CrossRef]
- Hankinson, O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 1995, 35, 307–340. [Google Scholar] [CrossRef] [PubMed]
- Thornton, J.; Edwards, R.; Mitchell, P.; Harrison, R.A.; Buchan, I.; Kelly, S.P. Smoking and age-related macular degeneration: A review of association. Eye 2005, 19, 935–944. [Google Scholar] [CrossRef] [PubMed]
- Chakravarthy, U.; Augood, C.; Bentham, G.C.; de Jong, P.T.; Rahu, M.; Seland, J.; Soubrane, G.; Tomazzoli, L.; Topouzis, F.; Vingerling, J.R.; et al. Cigarette smoking and age-related macular degeneration in the EUREYE Study. Ophthalmology 2007, 114, 1157–1163. [Google Scholar] [CrossRef] [PubMed]
- Patton, W.P.; Routledge, M.N.; Jones, G.D.; Lewis, S.E.; Archer, D.B.; Davies, R.J.; Chakravarthy, U. Retinal pigment epithelial cell DNA is damaged by exposure to benzo[a]pyrene, a constituent of cigarette smoke. Exp. Eye Res. 2002, 74, 513–522. [Google Scholar] [CrossRef]
- Sharma, A.; Neekhra, A.; Gramajo, A.L.; Patil, J.; Chwa, M.; Kuppermann, B.D.; Kenney, M.C. Effects of Benzo(e)Pyrene, a toxic component of cigarette smoke, on human retinal pigment epithelial cells in vitro. Investig. Ophthalmol. Vis. Sci. 2008, 49, 5111–5117. [Google Scholar] [CrossRef]
- Wang, A.L.; Lukas, T.J.; Yuan, M.; Du, N.; Handa, J.T.; Neufeld, A.H. Changes in retinal pigment epithelium related to cigarette smoke: Possible relevance to smoking as a risk factor for age-related macular degeneration. PLoS ONE 2009, 4, e5304. [Google Scholar] [CrossRef]
- Mansoor, S.; Gupta, N.; Patil, A.J.; Estrago-Franco, M.F.; Ramirez, C.; Migon, R.; Sapkal, A.; Kuppermann, B.D.; Kenney, M.C. Inhibition of apoptosis in human retinal pigment epithelial cells treated with benzo(e)pyrene, a toxic component of cigarette smoke. Investig. Ophthalmol. Vis. Sci. 2010, 51, 2601–2607. [Google Scholar] [CrossRef]
- Estrago-Franco, M.F.; Moustafa, M.T.; Riazi-Esfahani, M.; Sapkal, A.U.; Piche-Lopez, R.; Patil, A.J.; Sharma, A.; Falatoonzadeh, P.; Chwa, M.; Luczy-Bachman, G.; et al. Effects of Benzo(e)pyrene on Reactive Oxygen/Nitrogen Species and Inflammatory Cytokines Induction in Human RPE Cells and Attenuation by Mitochondrial-involved Mechanism. J. Ophthalmic. Vis. Res. 2016, 11, 385–393. [Google Scholar]
- Hoffmann, D.; Hoffmann, I.; El-Bayoumy, K. The less harmful cigarette: A controversial Issue. A Tribute to Ernst L. Wynder. Chem. Res. Toxicol. 2001, 14, 767–790. [Google Scholar] [CrossRef] [PubMed]
- Lodovici, M.; Akpan, V.; Evangelisti, C.; Dolara, P. Sidestream tobacco smoke as the main predictor of exposure to polycyclic aromatic hydrocarbons. J. Appl. Toxicol. 2004, 24, 277–281. [Google Scholar] [CrossRef]
- Vu, A.T.; Taylor, K.M.; Holman, M.R.; Ding, Y.S.; Hearn, B.; Watson, C.H. Polycyclic Aromatic Hydrocarbons in the Mainstream Smoke of Popular U.S. Cigarettes. Chem. Res. Toxicol. 2015, 28, 1616–1626. [Google Scholar] [CrossRef] [PubMed]
- Neal, M.S.; Zhu, J.; Foster, W.G. Quantification of benzo[a]pyrene and other PAHs in the serum and follicular fluid of smokers versus non-smokers. Reprod. Toxicol. 2008, 25, 100–106. [Google Scholar] [CrossRef]
- Pleil, J.D.; Stiegel, M.A.; Sobus, J.R.; Tabucchi, S.; Ghio, A.J.; Madden, M.C. Cumulative exposure assessment for trace-level polycyclic aromatic hydrocarbons (PAHs) using human blood and plasma analysis. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2010, 878, 1753–1760. [Google Scholar] [CrossRef] [PubMed]
- Song, X.F.; Chen, Z.Y.; Zang, Z.J.; Zhang, Y.N.; Zeng, F.; Peng, Y.P.; Yang, C. Investigation of polycyclic aromatic hydrocarbon level in blood and semen quality for residents in Pearl River Delta Region in China. Environ. Int. 2013, 60, 97–105. [Google Scholar] [CrossRef]
- Soeur, J.; Belaidi, J.P.; Chollet, C.; Denat, L.; Dimitrov, A.; Jones, C.; Perez, P.; Zanini, M.; Zobiri, O.; Mezzache, S.; et al. Photo-pollution stress in skin: Traces of pollutants (PAH and particulate matter) impair redox homeostasis in keratinocytes exposed to UVA1. J. Dermatol. Sci. 2017, 86, 162–169. [Google Scholar] [CrossRef]
- Foote, C.S. Definition of type I and type II photosensitized oxidation. Photochem. Photobiol. 1991, 54, 659. [Google Scholar] [CrossRef]
- Baptista, M.S.; Cadet, J.; Di Mascio, P.; Ghogare, A.A.; Greer, A.; Hamblin, M.R.; Lorente, C.; Nunez, S.C.; Ribeiro, M.S.; Thomas, A.H.; et al. Type I and Type II Photosensitized Oxidation Reactions: Guidelines and Mechanistic Pathways. Photochem. Photobiol. 2017, 93, 912–919. [Google Scholar] [CrossRef]
- Gao, D.; Luo, Y.; Guevara, D.; Wang, Y.; Rui, M.; Goldwyn, B.; Lu, Y.; Smith, E.C.; Lebwohl, M.; Wei, H. Benzo[a]pyrene and its metabolites combined with ultraviolet A synergistically induce 8-hydroxy-2’-deoxyguanosine via reactive oxygen species. Free Radic. Biol. Med. 2005, 39, 1177–1183. [Google Scholar] [CrossRef]
- Toyooka, T.; Ibuki, Y.; Takabayashi, F.; Goto, R. Coexposure to benzo[a]pyrene and UVA induces DNA damage: First proof of double-strand breaks in a cell-free system. Environ. Mol. Mutagen. 2006, 47, 38–47. [Google Scholar] [CrossRef] [PubMed]
- Douki, T.; Ksoury, Z.; Marie, C.; Favier, A.; Ravanat, J.L.; Maitre, A. Genotoxicity of combined exposure to polycyclic aromatic hydrocarbons and UVA—A mechanistic study. Photochem. Photobiol. 2008, 84, 1133–1140. [Google Scholar] [CrossRef] [PubMed]
- Sidorova, Y.A.; Grishanova, A.Y.; Lyakhovich, V.V. Transcriptional activation of cytochrome P450 1A1 with alpha-tocopherol. Bull. Exp. Biol. Med. 2004, 138, 233–236. [Google Scholar] [CrossRef] [PubMed]
- Sidorova, Y.A.; Grishanova, A.Y. Inhibitory effect of alpha-tocopherol on benzo(a)pyrene-induced CYPA1 activity in rat liver. Bull. Exp. Biol. Med. 2005, 140, 517–520. [Google Scholar] [CrossRef]
- Brunmark, P.; Harriman, S.; Skipper, P.L.; Wishnok, J.S.; Amin, S.; Tannenbaum, S.R. Identification of subdomain IB in human serum albumin as a major binding site for polycyclic aromatic hydrocarbon epoxides. Chem. Res. Toxicol. 1997, 10, 880–886. [Google Scholar] [CrossRef]
- Kwack, S.J.; Lee, B.M. Correlation between DNA or protein adducts and benzo[a]pyrene diol epoxide I-triglyceride adduct detected in vitro and in vivo. Carcinogenesis 2000, 21, 629–632. [Google Scholar] [CrossRef]
- Pollenz, R.S. The aryl-hydrocarbon receptor, but not the aryl-hydrocarbon receptor nuclear translocator protein, is rapidly depleted in hepatic and nonhepatic culture cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol. Pharmacol. 1996, 49, 391–398. [Google Scholar]
- Pollenz, R.S. The mechanism of AH receptor protein down-regulation (degradation) and its impact on AH receptor-mediated gene regulation. Chem. Biol. Interact. 2002, 141, 41–61. [Google Scholar] [CrossRef]
- Pollenz, R.S. Specific blockage of ligand-induced degradation of the Ah receptor by proteasome but not calpain inhibitors in cell culture lines from different species. Biochem. Pharmacol. 2007, 74, 131–143. [Google Scholar] [CrossRef]
- Lekas, P.; Tin, K.L.; Lee, C.; Prokipcak, R.D. The human cytochrome P450 1A1 mRNA is rapidly degraded in HepG2 cells. Arch. Biochem. Biophys. 2000, 384, 311–318. [Google Scholar] [CrossRef]
- Spink, D.C.; Katz, B.H.; Hussain, M.M.; Spink, B.C.; Wu, S.J.; Liu, N.; Pause, R.; Kaminsky, L.S. Induction of CYP1A1 and CYP1B1 in T-47D human breast cancer cells by benzo[a]pyrene is diminished by arsenite. Drug Metab. Dispos. 2002, 30, 262–269. [Google Scholar] [CrossRef]
- Spink, D.C.; Wu, S.J.; Spink, B.C.; Hussain, M.M.; Vakharia, D.D.; Pentecost, B.T.; Kaminsky, L.S. Induction of CYP1A1 and CYP1B1 by benzo(k)fluoranthene and benzo(a)pyrene in T-47D human breast cancer cells: Roles of PAH interactions and PAH metabolites. Toxicol. Appl. Pharmacol. 2008, 226, 213–224. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Joseph, J.A. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 1999, 27, 612–616. [Google Scholar] [CrossRef] [PubMed]
- Hruszkewycz, A.M.; Canella, K.A.; Peltonen, K.; Kotrappa, L.; Dipple, A. DNA polymerase action on benzo[a]pyrene-DNA adducts. Carcinogenesis 1992, 13, 2347–2352. [Google Scholar] [CrossRef]
- Lipinski, L.J.; Ross, H.L.; Zajc, B.; Sayer, J.M.; Jerina, D.M.; Dipple, A. Effect of single benzo[a]pyrene diol epoxide-deoxyguanosine adducts on the action of DNA polymerases in vitro. Int. J. Oncol. 1998, 13, 269–273. [Google Scholar] [CrossRef] [PubMed]
- Hsu, G.W.; Huang, X.; Luneva, N.P.; Geacintov, N.E.; Beese, L.S. Structure of a high fidelity DNA polymerase bound to a benzo[a]pyrene adduct that blocks replication. J. Biol. Chem. 2005, 280, 3764–3770. [Google Scholar] [CrossRef] [PubMed]
- Ayala-Torres, S.; Chen, Y.; Svoboda, T.; Rosenblatt, J.; Van Houten, B. Analysis of gene-specific DNA damage and repair using quantitative polymerase chain reaction. Methods 2000, 22, 135–147. [Google Scholar] [CrossRef]
- Jung, D.; Cho, Y.; Meyer, J.N.; Di Giulio, R.T. The long amplicon quantitative PCR for DNA damage assay as a sensitive method of assessing DNA damage in the environmental model, Atlantic killifish (Fundulus heteroclitus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2009, 149, 182–186. [Google Scholar] [CrossRef] [PubMed]
- Ponti, M.; Forrow, S.M.; Souhami, R.L.; D’Incalci, M.; Hartley, J.A. Measurement of the sequence specificity of covalent DNA modification by antineoplastic agents using Taq DNA polymerase. Nucleic Acids Res. 1991, 19, 2929–2933. [Google Scholar] [CrossRef]
- Furda, A.; Santos, J.H.; Meyer, J.N.; Van Houten, B. Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. Methods Mol. Biol. 2014, 1105, 419–437. [Google Scholar]
- Ye, J.; Coulouris, G.; Zaretskaya, I.; Cutcutache, I.; Rozen, S.; Madden, T.L. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 2012, 13, 134. [Google Scholar] [CrossRef]
- Oz, O.; Aras Ates, N.; Tamer, L.; Yildirim, O.; Adiguzel, U. Glutathione S-transferase M1, T1, and P1 gene polymorphism in exudative age-related macular degeneration: A preliminary report. Eur. J. Ophthalmol. 2006, 16, 105–110. [Google Scholar] [CrossRef] [PubMed]
- Mallet, J.D.; Dorr, M.M.; Drigeard Desgarnier, M.C.; Bastien, N.; Gendron, S.P.; Rochette, P.J. Faster DNA Repair of Ultraviolet-Induced Cyclobutane Pyrimidine Dimers and Lower Sensitivity to Apoptosis in Human Corneal Epithelial Cells than in Epidermal Keratinocytes. PLoS ONE 2016, 11, e0162212. [Google Scholar] [CrossRef] [PubMed]
- Barouki, R.; Coumoul, X.; Fernandez-Salguero, P.M. The aryl hydrocarbon receptor, more than a xenobiotic-interacting protein. FEBS Lett. 2007, 581, 3608–3615. [Google Scholar] [CrossRef] [PubMed]
- Bortoli, S.; Boutet-Robinet, E.; Lagadic-Gossmann, D.; Huc, L. Nrf2 and AhR in metabolic reprogramming after contaminant exposure. Curr. Opin. Toxicol. 2018, 8, 34–41. [Google Scholar] [CrossRef]
- Hunter, A.; Spechler, P.A.; Cwanger, A.; Song, Y.; Zhang, Z.; Ying, G.S.; Hunter, A.K.; Dezoeten, E.; Dunaief, J.L. DNA methylation is associated with altered gene expression in AMD. Investig. Ophthalmol. Vis. Sci. 2012, 53, 2089–2105. [Google Scholar] [CrossRef]
- Lee, W.H.; Joshi, P.; Wen, R. Glutathione S-transferase pi isoform (GSTP1) expression in murine retina increases with developmental maturity. Adv. Exp. Med. Biol. 2014, 801, 23–30. [Google Scholar]
- Bhosale, P.; Larson, A.J.; Frederick, J.M.; Southwick, K.; Thulin, C.D.; Bernstein, P.S. Identification and characterization of a Pi isoform of glutathione S-transferase (GSTP1) as a zeaxanthin-binding protein in the macula of the human eye. J. Biol. Chem. 2004, 279, 49447–49454. [Google Scholar] [CrossRef]
- Arunkumar, R.; Calvo, C.M.; Conrady, C.D.; Bernstein, P.S. What do we know about the macular pigment in AMD: The past, the present, and the future. Eye 2018, 32, 992–1004. [Google Scholar] [CrossRef]
- Hammond, B.R., Jr.; Wooten, B.R.; Snodderly, D.M. Cigarette smoking and retinal carotenoids: Implications for age-related macular degeneration. Vision Res. 1996, 36, 3003–3009. [Google Scholar] [CrossRef]
- Nolan, J.M.; Stack, J.; OO, D.; Loane, E.; Beatty, S. Risk factors for age-related maculopathy are associated with a relative lack of macular pigment. Exp. Eye Res. 2007, 84, 61–74. [Google Scholar] [CrossRef] [PubMed]
- Kim, K.H.; Jahan, S.A.; Kabir, E.; Brown, R.J. A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environ. Int. 2013, 60, 71–80. [Google Scholar] [CrossRef] [PubMed]
- Chang, K.H.; Hsu, P.Y.; Lin, C.J.; Lin, C.L.; Juo, S.H.; Liang, C.L. Traffic-related air pollutants increase the risk for age-related macular degeneration. J. Investig. Med. 2019, 67, 1076–1081. [Google Scholar] [CrossRef] [PubMed]
- Chua, S.Y.L.; Warwick, A.; Peto, T.; Balaskas, K.; Moore, A.T.; Reisman, C.; Desai, P.; Lotery, A.J.; Dhillon, B.; Khaw, P.T.; et al. Association of ambient air pollution with age-related macular degeneration and retinal thickness in UK Biobank. Br. J. Ophthalmol. 2021, 106, 705–711. [Google Scholar] [CrossRef]
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Zinflou, C.; Rochette, P.J. Indenopyrene and Blue-Light Co-Exposure Impairs the Tightly Controlled Activation of Xenobiotic Metabolism in Retinal Pigment Epithelial Cells: A Mechanism for Synergistic Toxicity. Int. J. Mol. Sci. 2023, 24, 17385. https://doi.org/10.3390/ijms242417385
Zinflou C, Rochette PJ. Indenopyrene and Blue-Light Co-Exposure Impairs the Tightly Controlled Activation of Xenobiotic Metabolism in Retinal Pigment Epithelial Cells: A Mechanism for Synergistic Toxicity. International Journal of Molecular Sciences. 2023; 24(24):17385. https://doi.org/10.3390/ijms242417385
Chicago/Turabian StyleZinflou, Corinne, and Patrick J. Rochette. 2023. "Indenopyrene and Blue-Light Co-Exposure Impairs the Tightly Controlled Activation of Xenobiotic Metabolism in Retinal Pigment Epithelial Cells: A Mechanism for Synergistic Toxicity" International Journal of Molecular Sciences 24, no. 24: 17385. https://doi.org/10.3390/ijms242417385