Astaxanthin Inhibits Autophagic Cell Death Induced by Bisphenol A in Human Dermal Fibroblasts
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Cells
2.3. Inhibitor Treatment
2.4. Cell Viability Assay
2.5. Quantitative Real-Time Polymerase Chain Reaction (qRT-PCR)
2.6. Detection of Intracellular Reactive Oxygen Species (ROS)
2.7. Western Blot Analysis
2.8. Flow Cytometry
2.9. Statistical Analysis
3. Results
3.1. Inhibitory Effect of Astaxanthin on the Dermal Cell Death and Autophagy Induced by BPA
3.2. Antioxidative Effect of Astaxanthin on the Production of ROS in NHDF Treated with BPA
3.3. Astaxanthin Inhibits ERK Activation Triggered by BPA
3.4. Inhibitory Effects of Astaxanthin on the Phosphorylation of NF-κB Stimulated by BPA
3.5. Astaxanthin Regulates the Autophagic Cell Death Triggered by BPA
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
- Zulkifli, S.; Rahman, A.A.; Kadir, S.; Nor, N.S.M. Bisphenol A and its effects on the systemic organs of children. Eur. J. Pediatr. 2021, 1–17. [Google Scholar] [CrossRef] [PubMed]
- Bhandari, R.K.; Deem, S.L.; Holliday, D.K.; Jandegian, C.M.; Kassotis, C.D.; Nagel, S.C.; Tillitt, D.E.; Vom Saal, F.S.; Rosenfeld, C.S. Effects of the environmental estrogenic contaminants bisphenol A and 17α-ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species. Gen. Comp. Endocrinol. 2015, 214, 195–219. [Google Scholar] [CrossRef] [PubMed]
- Mahemuti, L.; Chen, Q.; Coughlan, M.C.; Qiao, C.; Chepelev, N.L.; Florian, M.; Dong, D.; Woodworth, R.G.; Yan, J.; Cao, X.L.; et al. Bisphenol A induces DSB-ATM-p53 signaling leading to cell cycle arrest, senescence, autophagy, stress response, and estrogen release in human fetal lung fibroblasts. Arch. Toxicol. 2018, 92, 1453–1469. [Google Scholar] [CrossRef] [PubMed]
- Dyring-Andersen, B.; Lovendorf, M.B.; Coscia, F.; Santos, A.; Moller, L.B.P.; Colaco, A.R.; Niu, L.; Bzorek, M.; Doll, S.; Andersen, J.L.; et al. Spatially and cell-type resolved quantitative proteomic atlas of healthy human skin. Nat. Commun. 2020, 11, 5587. [Google Scholar] [CrossRef]
- Sorrell, J.M.; Arnold, I.C. Fibroblast heterogeneity: More than skin deep. J. Cell Sci. 2004, 117, 667–675. [Google Scholar] [CrossRef] [Green Version]
- Bogaki, T.; Mitani, K.; Oura, Y.; Ozeki, K. Effects of ethyl-α-D-glucoside on human dermal fibroblasts. Biosci. Biotechnol. Biochem. 2017, 81, 1706–1711. [Google Scholar] [CrossRef] [Green Version]
- Aldag, C.; Nogueira Teixeira, D.; Leventhal, P.S. Skin rejuvenation using cosmetic products containing growth factors, cytokines, and matrikines: A review of the literature. Clin. Cosmet Investig. Dermatol. 2016, 9, 411–419. [Google Scholar] [CrossRef] [Green Version]
- Zalko, D.; Jacques, C.; Duplan, H.; Bruel, S.; Perdu, E. Viable skin efficiently absorbs and metabolizes bisphenol A. Chemosphere 2011, 82, 424–430. [Google Scholar] [CrossRef] [Green Version]
- Lv, Y.; Lu, S.; Dai, Y.; Rui, C.; Wang, Y.; Zhou, Y.; Li, Y.; Pang, Q.; Fan, R. Higher dermal exposure of cashiers to BPA and its association with DNA oxidative damage. Environ. Int. 2017, 98, 69–74. [Google Scholar] [CrossRef]
- Mizushima, N. Autophagy: Process and function. Genes Dev. 2007, 21, 2861–2873. [Google Scholar] [CrossRef] [Green Version]
- Gu, Y.; Han, J.; Jiang, C.; Zhang, Y. Biomarkers, oxidative stress and autophagy in skin aging. Ageing Res. Rev. 2020, 59, 101036. [Google Scholar] [CrossRef]
- Liu, Y.; Levine, B. Autosis and autophagic cell death: The dark side of autophagy. Cell Death Differ. 2015, 22, 367–376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kishimoto, Y.; Yoshida, H.; Kondo, K. Potential Anti-Atherosclerotic Properties of Astaxanthin. Mar. Drugs. 2016, 14, 35. [Google Scholar] [CrossRef] [PubMed]
- Sztretye, M.; Dienes, B.; Gonczi, M.; Czirjak, T.; Csernoch, L.; Dux, L.; Szentesi, P.; Keller-Pinter, A. Astaxanthin: A Potential Mitochondrial-Targeted Antioxidant Treatment in Diseases and with Aging. Oxid. Med. Cell. Longev. 2019, 2019, 3849692. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, X.; Wang, B.; Lin, S.; Jing, L.; Mao, C.; Xu, P.; Lv, C.; Liu, W.; Zuo, J. Astaxanthin inhibits apoptosis in alveolar epithelial cells type II in vivo and in vitro through the ROS-dependent mitochondrial signalling pathway. J. Cell. Mol. Med. 2014, 18, 2198–2212. [Google Scholar] [CrossRef]
- Zuluaga, M.; Gueguen, V.; Letourneur, D.; Pavon-Djavid, G. Astaxanthin-antioxidant impact on excessive Reactive Oxygen Species generation induced by ischemia and reperfusion injury. Chem. Biol. Interact. 2018, 279, 145–158. [Google Scholar] [CrossRef]
- Liu, X.; Shibata, T.; Hisaka, S.; Osawa, T. Astaxanthin inhibits reactive oxygen species-mediated cellular toxicity in dopaminergic SH-SY5Y cells via mitochondria-targeted protective mechanism. Brain Res. 2009, 1254, 18–27. [Google Scholar] [CrossRef]
- Kim, J.H.; Choi, W.; Lee, J.H.; Jeon, S.J.; Choi, Y.H.; Kim, B.W.; Chang, H.I.; Nam, S.W. Astaxanthin inhibits H2O2-mediated apoptotic cell death in mouse neural progenitor cells via modulation of p38 and MEK signaling pathways. J. Microbiol. Biotechnol. 2009, 19, 1355–1363. [Google Scholar] [CrossRef]
- Xue, X.L.; Han, X.D.; Li, Y.; Chu, X.F.; Miao, W.M.; Zhang, J.L.; Fan, S.J. Astaxanthin attenuates total body irradiation-induced hematopoietic system injury in mice via inhibition of oxidative stress and apoptosis. Stem Cell Res. Ther. 2017, 8, 7. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.; Yang, L.; Guo, Y.; Zhang, T.; Qiao, X.; Wang, J.; Xu, J.; Xue, C. Hydrophilic Astaxanthin: PEGylated Astaxanthin Fights Diabetes by Enhancing the Solubility and Oral Absorbability. J. Agric. Food Chem. 2020, 68, 3649–3655. [Google Scholar] [CrossRef]
- Davinelli, S.; Nielsen, M.E.; Scapagnini, G. Astaxanthin in Skin Health, Repair, and Disease: A Comprehensive Review. Nutrients 2018, 10, 522. [Google Scholar] [CrossRef] [Green Version]
- Fang, Q.; Guo, S.; Zhou, H.; Han, R.; Wu, P.; Han, C. Astaxanthin protects against early burn-wound progression in rats by attenuating oxidative stress-induced inflammation and mitochondria-related apoptosis. Sci. Rep. 2017, 7, 41440. [Google Scholar] [CrossRef]
- Kim, D.W.; Choi, C.H.; Park, J.P.; Lee, S.J. Nanospheres Loaded with Curcumin Improve the Bioactivity of Umbilical Cord Blood-Mesenchymal Stem Cells via c-Src Activation During the Skin Wound Healing Process. Cells 2020, 9, 1467. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.Y.; Lee, Y.M.; Kim, D.W.; Min, T.; Lee, S.J. Nanosphere Loaded with Curcumin Inhibits the Gastrointestinal Cell Death Signaling Pathway Induced by the Foodborne Pathogen Vibrio Vulnificus. Cells 2020, 9, 631. [Google Scholar] [CrossRef] [Green Version]
- Bryk, D.; Olejarz, W.; Zapolska-Downar, D. Mitogen-activated protein kinases in atherosclerosis. Postepy Hig. Med. Dosw. (Online) 2014, 68, 10–22. [Google Scholar] [CrossRef]
- Wu, D.; Luo, N.; Wang, L.; Zhao, Z.; Bu, H.; Xu, G.; Yan, Y.; Che, X.; Jiao, Z.; Zhao, T.; et al. Hydrogen sulfide ameliorates chronic renal failure in rats by inhibiting apoptosis and inflammation through ROS/MAPK and NF-kappaB signaling pathways. Sci. Rep. 2017, 7, 455. [Google Scholar] [CrossRef] [PubMed]
- Singh, K.N.; Patil, S.; Barkate, H. Protective effects of astaxanthin on skin: Recent scientific evidence, possible mechanisms, and potential indications. J. Cosmet Dermatol. 2020, 19, 22–27. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Li, Z.; Han, H.; Luo, G.; Zhou, B.; Wang, S.; Wang, J. Impairment of object recognition memory by maternal bisphenol A exposure is associated with inhibition of Akt and ERK/CREB/BDNF pathway in the male offspring hippocampus. Toxicology 2016, 341–343, 56–64. [Google Scholar] [CrossRef]
- Kumar, A.; Takada, Y.; Boriek, A.M.; Aggarwal, B.B. Nuclear factor-kappaB: Its role in health and disease. J. Mol. Med. 2004, 82, 434–448. [Google Scholar] [CrossRef]
- Luo, J.L.; Kamata, H.; Karin, M. IKK/NF-κB signaling: Balancing life and death-a new approach to cancer therapy. J. Clin. Investig. 2005, 115, 2625–2632. [Google Scholar] [CrossRef] [Green Version]
- Park, A.; Koh, H.C. NF-κB/mTOR-mediated autophagy can regulate diquat-induced apoptosis. Arch. Toxicol. 2019, 93, 1239–1253. [Google Scholar] [CrossRef]
- An, Y.; Zhang, H.; Wang, C.; Jiao, F.; Xu, H.; Wang, X.; Luan, W.; Ma, F.; Ni, L.; Tang, X.; et al. Activation of ROS/MAPKs/NF-κB/NLRP3 and inhibition of efferocytosis in osteoclast-mediated diabetic osteoporosis. FASEB J. 2019, 33, 12515–12527. [Google Scholar] [CrossRef] [Green Version]
- Tak, P.P.; Firestein, G.S. NF-κB: A key role in inflammatory diseases. J. Clin. Investig. 2001, 107, 7–11. [Google Scholar] [CrossRef]
- Lawrence, T.; Bebien, M.; Liu, G.Y.; Nizet, V.; Karin, M. IKKα limits macrophage NF-κB activation and contributes to the resolution of inflammation. Nature 2005, 434, 1138–1143. [Google Scholar] [CrossRef]
- Lidke, D.S.; Huang, F.; Post, J.N.; Rieger, B.; Wilsbacher, J.; Thomas, J.L.; Pouyssegur, J.; Jovin, T.M.; Lenormand, P. ERK nuclear translocation is dimerization-independent but controlled by the rate of phosphorylation. J. Biol. Chem. 2010, 285, 3092–3102. [Google Scholar] [CrossRef] [Green Version]
- Kang, R.; Zeh, H.J.; Lotze, M.T.; Tang, D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011, 18, 571–580. [Google Scholar] [CrossRef] [PubMed]
- Obara, K.; Ohsumi, Y. Atg14: A key player in orchestrating autophagy. Int. J. Cell Biol. 2011, 2011, 713435. [Google Scholar] [CrossRef] [Green Version]
- Kabeya, Y.; Mizushima, N.; Ueno, T.; Yamamoto, A.; Kirisako, T.; Noda, T.; Kominami, E.; Ohsumi, Y.; Yoshimori, T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19, 5720–5728. [Google Scholar] [CrossRef] [PubMed]
- Shpilka, T.; Weidberg, H.; Pietrokovski, S.; Elazar, Z. Atg8: An autophagy-related ubiquitin-like protein family. Genome Biol. 2011, 12, 226. [Google Scholar] [CrossRef] [PubMed]
- Lang, T.; Schaeffeler, E.; Bernreuther, D.; Bredschneider, M.; Wolf, D.H.; Thumm, M. Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J. 1998, 17, 3597–3607. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otomo, C.; Metlagel, Z.; Takaesu, G.; Otomo, T. Structure of the human ATG12~ATG5 conjugate required for LC3 lipidation in autophagy. Nat. Struct. Mol. Biol. 2013, 20, 59–66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Copetti, T.; Bertoli, C.; Dalla, E.; Demarchi, F.; Schneider, C. p65/RelA modulates BECN1 transcription and autophagy. Mol. Cell Biol. 2009, 29, 2594–2608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Djavaheri-Mergny, M.; Maiuri, M.C.; Kroemer, G. Cross talk between apoptosis and autophagy by caspase-mediated cleavage of Beclin 1. Oncogene 2010, 29, 1717–1719. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Lim, S.-R.; Kim, D.-W.; Sung, J.; Kim, T.H.; Choi, C.-H.; Lee, S.-J. Astaxanthin Inhibits Autophagic Cell Death Induced by Bisphenol A in Human Dermal Fibroblasts. Antioxidants 2021, 10, 1273. https://doi.org/10.3390/antiox10081273
Lim S-R, Kim D-W, Sung J, Kim TH, Choi C-H, Lee S-J. Astaxanthin Inhibits Autophagic Cell Death Induced by Bisphenol A in Human Dermal Fibroblasts. Antioxidants. 2021; 10(8):1273. https://doi.org/10.3390/antiox10081273
Chicago/Turabian StyleLim, Seong-Ryeong, Do-Wan Kim, Junghee Sung, Tae Hoon Kim, Chang-Hyung Choi, and Sei-Jung Lee. 2021. "Astaxanthin Inhibits Autophagic Cell Death Induced by Bisphenol A in Human Dermal Fibroblasts" Antioxidants 10, no. 8: 1273. https://doi.org/10.3390/antiox10081273