Fucoidan protects ARPE-19 cells from oxidative stress via normalization of reactive oxygen species generation through the Ca2+-dependent ERK signaling pathway

Li,Xiaoxia; Zhao,Haiyan; Wang,Qingfa; Liang,Hongyan; Jiang,Xiaofeng

doi:10.3892/mmr.2015.3224

Fucoidan protects ARPE-19 cells from oxidative stress via normalization of reactive oxygen species generation through the Ca2+-dependent ERK signaling pathway

Authors:
- Xiaoxia Li
- Haiyan Zhao
- Qingfa Wang
- Hongyan Liang
- Xiaofeng Jiang
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Affiliations: Department of Clinical Biochemistry Laboratory, The Fourth Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150001, P.R. China, Department of Ophthalmology, Central Hospital of Liaoyang City, Liaoyang, Liaoning 111000, P.R. China, Department of Emergency, The First Affiliated Hospital of Jiamusi University, Jiamusi, Heilongjiang 154002, P.R. China
Published online on: January 19, 2015 https://doi.org/10.3892/mmr.2015.3224
Pages: 3746-3752

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Abstract

Diabetic retinopathy (DR) is a common complication of diabetes mellitus (DM) and it is the main cause of loss of vision. In previous years, interest in the biological activities of marine organisms has intensified. The effect of fucoidan from the seaweed Fucus vesiculosus on the molecular mechanisms of numerous diseases has been studied, while to date, its effect on DR was yet to be investigated. Therefore, the aim of the present study was to evaluate the role of fucoidan in DR. The human retinal pigment epithelial cell line ARPE‑19 was exposed to high D‑glucose in the presence or absence of fucoidan. Cell viability was monitored using MTT and lactate dehydrogenase assays. The intracellular reactive oxygen species (ROS) generation was measured using fluorescence spectrophotometry. Cell apoptosis was measured by flow cytometry using Annexin V‑fluorescein isothiocyanate staining. Ca2+ influx was measured with a calcium imaging system and the activation of the extracellular signal‑regulated kinase (ERK) protein was evaluated using western blot analysis. The non‑toxic fucoidan protected ARPE‑19 cells from high glucose‑induced cell death and normalized high glucose‑induced generation of ROS. Fucoidan also inhibited high glucose‑induced cell apoptosis, as well as the Ca2+ influx and ERK1/2 phosphorylation in ARPE‑19 cells. Taken together, these findings indicated that fucoidan protects ARPE‑19 cells against high glucose‑induced oxidative damage via normalization of ROS generation through the Ca2+‑dependent ERK signaling pathway.

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1	Wang J, Yang MM, Rong SS, Ng TK, Li YB and Liu XM: Association of paraoxonase gene polymorphisms with diabetic nephropathy and retinopathy. Mol Med Rep. 8:1845–1851. 2013.PubMed/NCBI
2	Lorenzi M and Gerhardinger C: Early cellular and molecular changes induced by diabetes in the retina. Diabetologia. 44:791–804. 2001. View Article : Google Scholar : PubMed/NCBI
3	Yuan Z, Feng W, Hong J, Zheng Q, Shuai J and Ge Y: p38MAPK and ERK promote nitric oxide production in cultured human retinal pigmented epithelial cells induced by high concentration glucose. Nitric Oxide. 20:9–15. 2009. View Article : Google Scholar
4	Yu T, Robotham JL and Yoon Y: Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci USA. 103:2653–2658. 2006. View Article : Google Scholar : PubMed/NCBI
5	Yu T, Sheu SS, Robotham JL and Yoon Y: Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc Res. 79:341–351. 2008. View Article : Google Scholar : PubMed/NCBI
6	Winkler BS, Boulton ME, Gottsch JD and Sternberg P: Oxidative damage and age-related macular degeneration. Mol Vis. 5:321999.PubMed/NCBI
7	Cai J, Nelson KC, Wu M, Sternberg P Jr, Jones DP, et al: Oxidative stress and protection of the RPE. Prog Retin Eye Res. 19:205–221. 2000. View Article : Google Scholar : PubMed/NCBI
8	Myers SP, O’Connor J, Fitton JH, Brooks L, Rolfe M, Connellan P, Wohlmuth H, Cheras PA and Morris C: A combined Phase I and II open-label study on the immunomodulatory effects of seaweed extract nutrient complex. Biologics. 5:45–60. 2011.PubMed/NCBI
9	Li C, Gao Y, Xing Y, Zhu H, Shen J and Tian J: Fucoidan, a sulfated polysaccharide from brown algae, against myocardial ischemia-reperfusion injury in rats via regulating the inflammation response. Food Chem Toxicol. 49:2090–2095. 2011. View Article : Google Scholar : PubMed/NCBI
10	Nishiura H, Tokita K, Li Y, Harada K, Woodruff TM, Taylor SM, Nsiama TK, Nishino N and Yamamoto T: The role of the ribosomal protein S19 C-terminus in Gi protein-dependent alternative activation of p38 MAP kinase via the C5a receptor in HMC-1 cells. Apoptosis. 15:966–981. 2010. View Article : Google Scholar : PubMed/NCBI
11	Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680–685. 1970. View Article : Google Scholar : PubMed/NCBI
12	Kyhse-Andersen J: Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods. 10:203–209. 1984. View Article : Google Scholar : PubMed/NCBI
13	Rastogi RP, Singh SP, Häder DP and Sinha RP: Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2′,7′-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 793. Biochem Biophys Res Commun. 397:603–607. 2010. View Article : Google Scholar : PubMed/NCBI
14	Jackson GR, Owsley C and Curcio CA: Photoreceptor degeneration and dysfunction in aging and age-related maculopathy. Ageing Res Rev. 1:381–396. 2002. View Article : Google Scholar : PubMed/NCBI
15	Zarbin MA: Age-related macular degeneration: review of pathogenesis. Eur J Ophthalmol. 8:199–206. 1998.
16	Allen DA, Yaqoob MM and Harwood SM: Mechanisms of high glucose-induced apoptosis and its relationship to diabetic complications. J Nutr Biochem. 16:705–713. 2005. View Article : Google Scholar : PubMed/NCBI
17	Brownlee M: Biochemistry and molecular cell biology of diabetic complications. Nature. 414:813–820. 2001. View Article : Google Scholar : PubMed/NCBI
18	Giddabasappa A, Bauler M, Yepuru M, Chaum E, Dalton JT and Eswaraka J: 17-β estradiol protects ARPE-19 cells from oxidative stress through estrogen receptor-β, Invest. Ophthalmol Vis Sci. 51:5278–5287. 2010. View Article : Google Scholar
19	Lee JE, Lee RA, Kim KH and Lee JH: Induction of apoptosis with diallyl disulfide in AGS gastric cancer cell line. J Korean Surg Soc. 81:85–95. 2011. View Article : Google Scholar : PubMed/NCBI
20	Dong X, Li Z, Wang W, Zhang W, Liu S and Zhang X: Protective effect of canolol from oxidative stress-induced cell damage in ARPE-19 cells via an ERK mediated antioxidative pathway. Mol Vis. 17:2040–2048. 2011.PubMed/NCBI
21	Castro R, Sun XH, Liu XB, Martinez JR and Zhang GH: Inhibition of Ca²⁺ influx by surfactant in NR8383 alveolar macrophages. Inflamm Res. 57:489–496. 2008. View Article : Google Scholar : PubMed/NCBI
22	Glotin AL, Calipel A, Brossas JY, Faussat AM, Tréton J and Mascarelli F: Sustained versus transient ERK1/2 signaling underlies the antiand proapoptotic effects of oxidative stress in human RPE cells, Invest. Ophthalmol Vis Sci. 47:4614–4623. 2006. View Article : Google Scholar
23	Guillonneau X, Régnier-Ricard F, Dupuis C, Courtois Y and Mascarelli F: Paracrine effects of phosphorylated and excreted FGF1 by retinal pigmented epithelial cells. Growth Factors. 15:95–112. 1998. View Article : Google Scholar : PubMed/NCBI
24	Cai L: Suppression of nitrative damage by metallothionein in diabetic heart contributes to the prevention of cardiomyopathy. Free Radic Biol Med. 41:851–861. 2006. View Article : Google Scholar : PubMed/NCBI
25	Qin S, McLaughlin AP and De Vries GW: Protection of RPE cells from oxidative injury by 15-deoxy-delta12,14-prostaglandin J2 by augmenting GSH and activating MAPK. Invest Ophthalmol Vis Sci. 47:5098–5105. 2006. View Article : Google Scholar : PubMed/NCBI