Chitooligosaccharides Derivatives Protect ARPE-19 Cells against Acrolein-Induced Oxidative Injury
Abstract
:1. Introduction
2. Results and Discussion
2.1. Characterization of Chitooligosaccharides and N-Acetylated Chitooligosaccharides
2.2. Protective Effect of COSs and NACOs against Acrolein-Induced Cell Death
2.3. Protective Effect of COS–5 and N–5 against Acrolein-Induced Oxidative Stress
2.4. COS–5 and N–5 Improved Mitochondrial Function in Acrolein-Treated ARPE-19 Cells
2.5. N–5 Promoted Nrf2 Nuclear Translocation and Increased Antioxidant Enzyme Expression
3. Materials and Methods
3.1. Materials
3.2. Chitosan Oligosaccharide (COSs) Preparation and Purification
3.3. N-Acetylated Chitooligosaccharide (NACOs) Preparation and Purification
3.4. MTT Assay for Cell Viability
3.5. Antioxidant Enzyme Activities, ROS Generation, and Intracellular GSH Levels Assay
3.6. Confocal Imaging
3.7. Mitochondrial Dysfunction Evaluation
3.8. Western Blot
3.9. Real-Time PCR
3.10. Statistical Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Wong, W.L.; Su, X.Y.; Li, X.; Cheung, C.M.G.; 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] [Green Version]
- Yan, Y.T.; Ren, Y.F.; Li, X.M.; Zhang, X.X.; Guo, H.Q.; Han, Y.T.; Hu, J.X. A polysaccharide from green tea (Camellia sinensis L.) protects human retinal endothelial cells against hydrogen peroxide-induced oxidative injury and apoptosis. Int. J. Biol. Macromol. 2018, 115, 600–607. [Google Scholar] [CrossRef]
- Zhang, X.H.; Bohner, A.; Bhuvanagiri, S.; Uehara, H.; Upadhyay, A.K.; Emerson, L.L.; Bondalapati, S.; Muddana, S.K.; Fang, D.; Li, M.L.; et al. Targeted Intraceptor Nanoparticle for Neovascular Macular Degeneration: Preclinical Dose Optimization and Toxicology Assessment. Mol. Ther. 2017, 25, 1606–1615. [Google Scholar] [CrossRef] [Green Version]
- Handa, J.T.; Rickman, C.B.; Dick, A.D.; Gorin, M.B.; Miller, J.W.; Toth, C.A.; Ueffing, M.; Zarbin, M.; Farrer, L.A. A systems biology approach towards understanding and treating non-neovascular age-related macular degeneration. Nat. Commun. 2019, 10, 3347. [Google Scholar] [CrossRef] [Green Version]
- Felszeghy, S.; Viiri, J.; Paterno, J.J.; Hyttinen, J.M.T.; Koskela, A.; Chen, M.; Leinonen, H.; Tanila, H.; Kivinen, N.; Koistinen, A.; et al. Loss of NRF-2 and PGC-1alpha genes leads to retinal pigment epithelium damage resembling dry age-related macular degeneration. Redox Biol. 2019, 20, 1–12. [Google Scholar] [CrossRef]
- Abd, A.J.; Kanwar, R.K.; Kanwar, J.R. Aged macular degeneration: Current therapeutics for management and promising new drug candidates. Drug Discov. Today 2017, 22, 1671–1679. [Google Scholar] [CrossRef]
- Koskela, A.; Manai, F.; Basagni, F.; Liukkonen, M.; Rosini, M.; Govoni, S.; Dal Monte, M.; Smedowski, A.; Kaarniranta, K.; Amadio, M. Nature-Inspired Hybrids (NIH) Improve Proteostasis by Activating Nrf2-Mediated Protective Pathways in Retinal Pigment Epithelial Cells. Antioxidants 2022, 11, 1385. [Google Scholar] [CrossRef]
- Chuang, C.J.; Wang, M.L.; Yeh, J.H.; Chen, T.C.; Tsou, S.C.; Lee, Y.J.; Chang, Y.Y.; Lin, H.W. The Protective Effects of alpha-Mangostin Attenuate Sodium Iodate-Induced Cytotoxicity and Oxidative Injury via Mediating SIRT-3 Inactivation via the PI3K/AKT/PGC-1 alpha Pathway. Antioxidants 2021, 10, 1870. [Google Scholar] [CrossRef]
- Wen, X.W.; Li, S.; Zhang, Y.F.; Zhu, L.; Xi, X.T.; Zhang, S.Y.; Li, Y. Recombinant human klotho protects against hydrogen peroxide-mediated injury in human retinal pigment epithelial cells via the PI3K/Akt-Nrf2/HO-1 signaling pathway. Bioengineered 2022, 13, 11767–11781. [Google Scholar] [CrossRef]
- Jeung, I.C.; Jee, D.; Rho, C.R.; Kang, S. Melissa officinalis L. Extracts Protect Human Retinal Pigment Epithelial Cells against Oxidative Stress-Induced Apoptosis. Int. J. Med. Sci. 2016, 13, 139–146. [Google Scholar] [CrossRef] [Green Version]
- Datta, S.; Cano, M.; Ebrahimi, K.; Wang, L.; Handa, J.T. The impact of oxidative stress and inflammation on RPE degeneration in non-neovascular AMD. Prog. Retin. Eye Res. 2017, 60, 201–218. [Google Scholar] [CrossRef] [PubMed]
- Yao, J.; Bi, H.E.; Sheng, Y.; Cheng, L.B.; Wendu, R.L.; Wang, C.H.; Cao, G.F.; Jiang, Q. Ultraviolet (UV) and Hydrogen Peroxide Activate Ceramide-ER Stress-AMPK Signaling Axis to Promote Retinal Pigment Epithelium (RPE) Cell Apoptosis. Int. J. Mol. Sci. 2013, 14, 10355–10368. [Google Scholar] [CrossRef] [Green Version]
- Nashine, S.; Nesburn, A.B.; Kuppermann, B.D.; Kenney, M.C. Role of Resveratrol in Transmitochondrial AMD RPE Cells. Nutrients 2020, 12, 159. [Google Scholar] [CrossRef] [Green Version]
- Cao, G.F.; Liu, Y.; Yang, W.; Wan, J.; Yao, J.; Wan, Y.S.; Jiang, Q. Rapamycin sensitive mTOR activation mediates nerve growth factor (NGF) induced cell migration and pro-survival effects against hydrogen peroxide in retinal pigment epithelial cells. Biochem. Biophys. Res. Commun. 2011, 414, 499–505. [Google Scholar] [CrossRef]
- Goncalves, I.R.; Brouillet, S.; Soulie, M.C.; Gribaldo, S.; Sirven, C.; Charron, N.; Boccara, M.; Choquer, M. Genome-wide analyses of chitin synthases identify horizontal gene transfers towards bacteria and allow a robust and unifying classification into fungi. BMC Evol. Biol. 2016, 16, 252. [Google Scholar] [CrossRef] [Green Version]
- Chua, E.T.; Shekh, A.Y.; Eltanahy, E.; Thomas-Hall, S.R.; Schenk, P.M. Effective Harvesting ofNannochloropsisMicroalgae Using Mushroom Chitosan: A Pilot-Scale Study. Front. Bioeng. Biotechnol. 2020, 8, 711. [Google Scholar] [CrossRef]
- Ahmad, S.I.; Ahmad, R.; Khan, M.S.; Kant, R.; Shahid, S.; Gautam, L.; Hasan, G.M.; Hassan, M.I. Chitin and its derivatives: Structural properties and biomedical applications. Int. J. Biol. Macromol. 2020, 164, 526–539. [Google Scholar] [CrossRef]
- Bonin, M.; Sreekumar, S.; Cord-Landwehr, S.; Moerschbacher, B.M. Preparation of Defined Chitosan Oligosaccharides Using Chitin Deacetylases. Int. J. Mol. Sci. 2020, 21, 7835. [Google Scholar] [CrossRef]
- Yuan, X.B.; Zheng, J.P.; Jiao, S.M.; Cheng, G.; Feng, C.; Du, Y.G.; Liu, H.T. A review on the preparation of chitosan oligosaccharides and application to human health, animal husbandry and agricultural production. Carbohydr. Polym. 2019, 220, 60–70. [Google Scholar] [CrossRef]
- Tao, W.J.; Sun, W.J.; Liu, L.J.; Wang, G.; Xiao, Z.P.; Pei, X.; Wang, M.Q. Chitosan Oligosaccharide Attenuates Nonalcoholic Fatty Liver Disease Induced by High Fat Diet through Reducing Lipid Accumulation, Inflammation and Oxidative Stress in C57BL/6 Mice. Mar. Drugs 2019, 17, 645. [Google Scholar] [CrossRef] [Green Version]
- Mattaveewong, T.; Wongkrasant, P.; Chanchai, S.; Pichyangkura, R.; Chatsudthipong, V.; Muanprasat, C. Chitosan oligosaccharide suppresses tumor progression in a mouse model of colitis-associated colorectal cancer through AMPK activation and suppression of NF-kappa B and mTOR signaling. Carbohydr. Polym. 2016, 145, 30–36. [Google Scholar] [CrossRef]
- Fang, I.M.; Yang, C.H.; Yang, C.M.; Chen, M.S. Chitosan Oligosaccharides Attenuates Oxidative-Stress Related Retinal Degeneration in Rats. PLoS ONE 2013, 8, e77323. [Google Scholar] [CrossRef]
- Xu, W.; Huang, H.C.; Lin, C.J.; Jiang, Z.F. Chitooligosaccharides protect rat cortical neurons against copper induced damage by attenuating intracellular level of reactive oxygen species. Bioorg. Med. Chem. Lett. 2010, 20, 3084–3088. [Google Scholar] [CrossRef]
- Hao, C.; Gao, L.X.; Zhang, Y.R.; Wang, W.; Yu, G.L.; Guan, H.S.; Zhang, L.J.; Li, C.X. Acetylated Chitosan Oligosaccharides Act as Antagonists against Glutamate-Induced PC12 Cell Death via Bcl-2/Bax Signal Pathway. Mar. Drugs 2015, 13, 1267–1289. [Google Scholar] [CrossRef] [Green Version]
- Chang, S.H.; Wu, C.H.; Tsai, G.J. Effects of chitosan molecular weight on its antioxidant and antimutagenic properties. Carbohydr. Polym. 2018, 181, 1026–1032. [Google Scholar] [CrossRef]
- Morando, M.; Yao, Y.; Martin-Santamaria, S.; Zhu, Z.; Xu, T.; Canada, F.J.; Zhang, Y.; Jimenez-Barbero, J. Mimicking chitin: Chemical synthesis, conformational analysis, and molecular recognition of the beta(1→3) N-acetylchitopentaose analogue. Chemistry 2010, 16, 4239–4249. [Google Scholar] [CrossRef]
- Li, K.C.; Liu, S.; Xing, R.G.; Qin, Y.K.; Li, P.C. Preparation, characterization and antioxidant activity of two partially N-acetylated chitotrioses. Carbohydr. Polym. 2013, 92, 1730–1736. [Google Scholar] [CrossRef]
- Xiong, C.N.; Wu, H.G.; Wei, P.; Pan, M.; Tuo, Y.Q.; Kusakabe, I.; Du, Y.G. Potent angiogenic inhibition effects of deacetylated chitohexaose separated from chitooligosaccharides and its mechanism of action in vitro. Carbohydr. Res. 2009, 344, 1975–1983. [Google Scholar] [CrossRef]
- Wei, X.L.; Wang, Y.F.; Xiao, J.B.; Xia, W.S. Separation of chitooligosaccharides and the potent effects on gene expression of cell surface receptor CR3. Int. J. Biol. Macromol. 2009, 45, 432–436. [Google Scholar] [CrossRef]
- Liang, C.Y.; Ling, Y.; Wei, F.; Huang, L.J.; Li, X.M. A novel antibacterial biomaterial mesh coated by chitosan and tigecycline for pelvic floor repair and its biological performance. Regen. Biomater. 2020, 7, 483–490. [Google Scholar] [CrossRef]
- Sun, L.J.; Luo, C.; Long, H.A.; Wei, D.Z.; Liu, H.K. Acrolein is a mitochondrial toxin: Effects on respiratory function and enzyme activities in isolated rat liver mitochondria. Mitochondrion 2006, 6, 136–142. [Google Scholar] [CrossRef]
- Feng, Z.H.; Liu, Z.B.; Li, X.S.; Jia, H.Q.; Sun, L.J.; Tian, C.A.; Jia, L.H.; Liu, J.K. alpha-Tocopherol is an effective Phase II enzyme inducer: Protective effects on acrolein-induced oxidative stress and mitochondrial dysfunction in human retinal pigment epithelial cells. J. Nutr. Biochem. 2010, 21, 1222–1231. [Google Scholar] [CrossRef]
- Li, Y.; Zou, X.; Cao, K.; Xu, J.; Yue, T.T.; Dai, F.; Zhou, B.; Lu, W.Y.; Feng, Z.H.; Liu, J.K. Curcumin analog 1, 5-bis (2-trifluoromethylphenyl)-1, 4-pentadieN–3-one exhibits enhanced ability on Nrf2 activation and protection against acrolein-induced ARPE-19 cell toxicity. Toxicol. Appl. Pharm. 2013, 272, 726–735. [Google Scholar] [CrossRef]
- Li, X.; Liu, Z.B.; Luo, C.; Jia, H.Q.; Sun, L.J.; Hou, B.; Shen, W.; Packer, L.; Cotman, C.W.; Liu, J.K. Lipoamide protects retinal pigment epithelial cells from oxidative stress and mitochondrial dysfunction. Free Radic. Biol. Med. 2008, 44, 1465–1474. [Google Scholar] [CrossRef] [Green Version]
- Jin, L.; Abrahams, J.P.; Skinner, R.; Petitou, M.; Pike, R.N.; Carrell, R.W. The anticoagulant activation of antithrombin by heparin. Proc. Natl. Acad. Sci. USA 1997, 94, 14683–14688. [Google Scholar] [CrossRef] [Green Version]
- Wang, K.; Zhu, X.; Zhang, K.; Yao, Y.; Zhuang, M.; Tan, C.Y.; Zhou, F.F.; Zhu, L. Puerarin inhibits amyloid beta-induced NLRP3 inflammasome activation in retinal pigment epithelial cells via suppressing ROS-dependent oxidative and endoplasmic reticulum stresses. Exp. Cell Res. 2017, 357, 335–340. [Google Scholar] [CrossRef]
- Zhu, C.; Dong, Y.C.; Liu, H.L.; Ren, H.; Cui, Z.H. Hesperetin protects against H2O2- triggered oxidative damage via upregulation of the Keap1-Nrf2/ HO-1 signal pathway in ARPE-19 cells. Biomed. Pharmacother. 2017, 88, 124–133. [Google Scholar] [CrossRef]
- Zalewska-Ziob, M.; Adamek, B.; Kasperczyk, J.; Romuk, E.; Hudziec, E.; Chwalinska, E.; Dobija-Kubica, K.; Rogozinski, P.; Brulinski, K. Activity of Antioxidant Enzymes in the Tumor and Adjacent Noncancerous Tissues of Non-Small-Cell Lung Cancer. Oxidative Med. Cell. Longev. 2019, 2019, 2901840. [Google Scholar] [CrossRef] [Green Version]
- Sena, L.A.; Li, S.; Jairaman, A.; Prakriya, M.; Ezponda, T.; Hildeman, D.A.; Wang, C.R.; Schumacker, P.T.; Licht, J.D.; Perlman, H.; et al. Mitochondria Are Required for Antigen-Specific T Cell Activation through Reactive Oxygen Species Signaling. Immunity 2013, 38, 225–236. [Google Scholar] [CrossRef] [Green Version]
- Li, X.; Zhou, C.R.; Chen, X.F.; Zhao, M.Y. Subcellular localization of chitosan oligosaccharides in living cells. Chin. Sci. Bull. 2014, 59, 2449–2454. [Google Scholar] [CrossRef]
- Chu, X.Y.; Liu, Y.M.; Zhang, H.Y. Activating or Inhibiting Nrf2? Trends Pharmacol. Sci. 2017, 38, 953–955. [Google Scholar] [CrossRef]
- Ma, Q. Role of Nrf2 in Oxidative Stress and Toxicity. Annu. Rev. Pharmacol. 2013, 53, 401–426. [Google Scholar] [CrossRef] [Green Version]
- Jia, L.H.; Liu, Z.B.; Sun, L.J.; Miller, S.S.; Ames, B.N.; Cotman, C.W.; Liu, J.K. Acrolein, a toxicant in cigarette smoke, causes oxidative damage and mitochondrial dysfunction in RPE cells: Protection by (R)-alpha-lipoic acid. Investig. Ophthalmol. Vis. Sci. 2007, 48, 339–348. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, D.; Wang, J.T.; Tan, L.J.; Sun, C.Y.; Dong, J.N. Synthesis of N-furoyl chitosan and chito-oligosaccharides and evaluation of their antioxidant activity in vitro. Int. J. Biol. Macromol. 2013, 59, 391–395. [Google Scholar] [CrossRef]
- Sun, T.; Zhou, D.X.; Mao, F.; Zhu, Y.N. Preparation of low-molecular-weight carboxymethyl chitosan and their superoxide anion scavenging activity. Eur. Polym. J. 2007, 43, 652–656. [Google Scholar] [CrossRef]
- Li, K.C.; Xing, R.G.; Liu, S.; Li, R.F.; Qin, Y.K.; Meng, X.T.; Li, P.C. Separation of chito-oligomers with several degrees of polymerization and study of their antioxidant activity. Carbohydr. Polym. 2012, 88, 896–903. [Google Scholar] [CrossRef]
- Qu, D.F.; Han, J.Z. Investigation of the antioxidant activity of chitooligosaccharides on mice with high-fat diet. Rev. Bras. Zootec. 2016, 45, 661–666. [Google Scholar] [CrossRef] [Green Version]
- Chen, L.; Zhu, Y.Q.; Zhou, J.; Wu, R.; Yang, N.; Bao, Q.B.; Xu, X.R. Luteolin Alleviates Epithelial-Mesenchymal Transformation Induced by Oxidative Injury in ARPE-19 Cell via Nrf2 and AKT/GSK-3 beta Pathway. Oxidative Med. Cell. Longev. 2022, 2022, 2265725. [Google Scholar]
- Chen, W.P.; Ye, Y.X.; Wu, Z.R.; Lin, J.L.; Wang, Y.T.; Ding, Q.; Yang, X.R.; Yang, W.; Lin, B.Q.; Lin, B.Q. Temporary Upregulation of Nrf2 by Naringenin Alleviates Oxidative Damage in the Retina and ARPE-19 Cells. Oxidative Med. Cell. Longev. 2021, 2021, 4053276. [Google Scholar] [CrossRef]
- Shivarudrappa, A.H.; Ponesakki, G. Lutein reverses hyperglycemia-mediated blockage of Nrf2 translocation by modulating the activation of intracellular protein kinases in retinal pigment epithelial (ARPE-19) cells. J. Cell Commun. Signal. 2020, 14, 207–221. [Google Scholar] [CrossRef]
- Li, Y.; Hu, Z.T.; Chen, B.; Bu, Q.; Lu, W.J.; Deng, Y.; Zhu, R.M.; Shao, X.; Hou, J.; Zhao, J.X.; et al. Taurine attenuates methamphetamine-induced autophagy and apoptosis in PC12 cells through mTOR signaling pathway. Toxicol. Lett. 2012, 215, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Xu, Q.L.; Liu, M.Z.; Chao, X.H.; Zhang, C.L.; Yang, H.; Chen, J.H.; Zhao, C.X.; Zhou, B. Acidifiers Attenuate Diquat-Induced Oxidative Stress and Inflammatory Responses by Regulating NF-kappa B/MAPK/COX-2 Pathways in IPEC-J2 Cells. Antioxidants 2022, 11, 2002. [Google Scholar] [CrossRef]
- Wang, X.L.; Jiang, H.; Zhang, N.; Cai, C.; Li, G.Y.; Hao, J.J.; Yu, G.L. Anti-diabetic activities of agaropectin-derived oligosaccharides from Gloiopeltis furcata via regulation of mitochondrial function. Carbohydr. Polym. 2020, 229, 115482. [Google Scholar] [CrossRef]
- Lin, C.W.; Huang, H.H.; Yang, C.M.; Yang, C.H. Protective effect of chitosan oligosaccharides on blue light light-emitting diode induced retinal pigment epithelial cell damage. J. Funct. Foods 2018, 49, 12–19. [Google Scholar] [CrossRef]
- Han, S.X.; Chen, J.J.; Hua, J.J.; Hu, X.J.; Jian, S.H.; Zheng, G.X.; Wang, J.; Li, H.R.; Yang, J.L.; Hejtmancik, J.F.; et al. MITF protects against oxidative damage-induced retinal degeneration by regulating the NRF2 pathway in the retinal pigment epithelium. Redox Biol. 2020, 34, 101537. [Google Scholar] [CrossRef]
- You, L.T.; Peng, H.L.Y.; Liu, J.; Cai, M.R.; Wu, H.M.; Zhang, Z.Q.; Bai, J.; Yao, Y.; Dong, X.X.; Yin, X.B.; et al. Catalpol Protects ARPE-19 Cells against Oxidative Stress via Activation of the Keap1/Nrf2/ARE Pathway. Cells 2021, 10, 2635. [Google Scholar] [CrossRef]
Molecular Formula | Mw | m/z | |
---|---|---|---|
COS–2 | C12H24N2O9 | 340.1 | [M + H]+ = 341.2 [M + Na]+ = 363.2 |
COS–3 | C18H35N3O13 | 501.2 | [M + H]+ = 502.3 [2M + H]+ = 1003.7 |
COS–4 | C24H46N4O17 | 662.3 | [M + H]+ = 663.4 |
COS–5 | C30H57N5O21 | 823.4 | [M + H]+ = 824.6 [M + 2H]+ = 412.8 |
COS–6 | C36H68N6O25 | 984.5 | [M + H]+ = 985.9 [M + 2H]+ = 493.5 |
N–2 | C16H28N2O11 | 424.4 | [M + H]+ = 425.2 |
[M + Na]+ = 447.2 | |||
N–3 | C24H41N3O16 | 627.6 | [M + H]+ = 628.3 |
[2M + H]+ = 1255.5 | |||
N–4 | C32H54N4O21 | 830.8 | [M + H]+ = 831.3 |
N–5 | C40H67N5O26 | 1033.9 | [M + H]+ = 1034.4 |
N–6 | C48H80N6O31 | 1237.1 | [M + H]+ = 1237.8 |
Sample | NMR Data (ppm) | ||||||||
---|---|---|---|---|---|---|---|---|---|
C=O | CH3 | C1 | C2 | C3 | C4 | C5 | C6 | ||
COS–3 | GlcN″ | 100.4 | 58.5 | 74.4 | 72.3 | 79.1 | 62.9 | ||
GlcN′ | 100.2 | 58.5 | 79.1 | 77.4 | 72.8 | 62.7 | |||
GlcNβ | 95.3 | 59.3 | 70.6 | 79.1 | 72.6 | 62.7 | |||
GlcNα | 91.6 | 56.9 | 70.6 | 79.1 | 72.6 | 62.7 | |||
N–3 | GlcNAc″ | 174.8 | 22.6 22.5 22.3 | 101.8 | 56.0 | 73.9 | 70.1 | 76.3 | 61.0 |
GlcNAc′ | 101.6 | 55.4 | 72.6 | 79.6 | 74.9 | 60.4 | |||
GlcNAcβ | 95.2 | 56.5 | 72.9 | 79.6 | 75.0 | 60.5 | |||
GlcNAcα | 90.8 | 54.1 | 69.6 | 80.1 | 70.4 | 60.4 |
Primers | Forward | Reverse |
---|---|---|
HO-1 | GGTCCTTACACTCAGCTTTCT | CATAGGCTCCTTCCTCCTTTC |
NQO1 | AAAGGACCCTTCCGGAGTAA | CCATCCTTCCAGGATTTGAA |
β-actin | ACCCTGAAGTACCCCATCGAG | GGATAGCACAGCCTGGATAGCA |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 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
Yang, C.; Yang, R.; Gu, M.; Hao, J.; Wang, S.; Li, C. Chitooligosaccharides Derivatives Protect ARPE-19 Cells against Acrolein-Induced Oxidative Injury. Mar. Drugs 2023, 21, 137. https://doi.org/10.3390/md21030137
Yang C, Yang R, Gu M, Hao J, Wang S, Li C. Chitooligosaccharides Derivatives Protect ARPE-19 Cells against Acrolein-Induced Oxidative Injury. Marine Drugs. 2023; 21(3):137. https://doi.org/10.3390/md21030137
Chicago/Turabian StyleYang, Cheng, Rongrong Yang, Ming Gu, Jiejie Hao, Shixin Wang, and Chunxia Li. 2023. "Chitooligosaccharides Derivatives Protect ARPE-19 Cells against Acrolein-Induced Oxidative Injury" Marine Drugs 21, no. 3: 137. https://doi.org/10.3390/md21030137