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Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 1862462, 10 pages
https://doi.org/10.1155/2018/1862462
Research Article

Antioxidant and Anti-Inflammatory Effects of Blueberry Anthocyanins on High Glucose-Induced Human Retinal Capillary Endothelial Cells

1Institute of Farm Product Processing, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
2Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
3Department of Food Science and Engineering, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China

Correspondence should be addressed to Jianzhong Zhou; moc.621@kculzjz and Zhongquan Sui; moc.liamg@iusgnirps

Received 1 September 2017; Revised 16 November 2017; Accepted 25 December 2017; Published 22 February 2018

Academic Editor: Ilaria Peluso

Copyright © 2018 Wuyang Huang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. Fan, Y. Qiao, J. Huang, and M. Tang, “Protective effects of Panax notoginseng Saponins against high glucose-induced oxidative injury in rat retinal capillary endothelial cells,” Evidence-Based Complementary and Alternative Medicine, vol. 2016, Article ID 5326382, 9 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. C.-f. Wang, J.-r. Yuan, D. Qin et al., “Protection of tauroursodeoxycholic acid on high glucose-induced human retinal microvascular endothelial cells dysfunction and streptozotocin-induced diabetic retinopathy rats,” Journal of Ethnopharmacology, vol. 185, pp. 162–170, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Lorenzi and C. Gerhardinger, “Early cellular and molecular changes induced by diabetes in the retina,” Diabetologia, vol. 44, no. 7, pp. 791–804, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Zhang, Z. Zhang, and P. F. Kador, “Polyol effects on growth factors and MAPK signaling in rat retinal capillary cells,” Journal of Ocular Pharmacology and Therapeutics, vol. 30, no. 1, pp. 4–11, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. D. S. London and B. Beezhold, “A phytochemical-rich diet may explain the absence of age-related decline in visual acuity of Amazonian hunter-gatherers in Ecuador,” Nutrition Research, vol. 35, no. 2, pp. 107–117, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Ghosh and T. Konishi, “Anthocyanins and anthocyanin-rich extracts: role in diabetes and eye function,” Asia Pacific Journal of Clinical Nutrition, vol. 16, no. 2, pp. 200–208, 2007. View at Google Scholar
  7. S. S. Paik, E. Jeong, S. W. Jung et al., “Anthocyanins from the seed coat of black soybean reduce retinal degeneration induced by N-methyl-N-nitrosourea,” Experimental Eye Research, vol. 97, no. 1, pp. 55–62, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. S. H. Shim, J. M. Kim, C. Y. Choi, C. Y. Kim, and K. H. Park, “Ginkgo biloba extract and bilberry anthocyanins improve visual function in patients with normal tension glaucoma,” Journal of Medicinal Food, vol. 15, no. 9, pp. 818–823, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. S. H. Lee, E. Jeong, S.-S. Paik et al., “Cyanidin-3-glucoside extracted from mulberry fruit can reduce N-methyl-N-nitrosourea-induced retinal degeneration in rats,” Current Eye Research, vol. 39, no. 1, pp. 79–87, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Nakamura, J. Tanaka, T. Imada, H. Shimoda, and K. Tsubota, “Delphinidin 3,5-O-diglucoside, a constituent of the maqui berry (Aristotelia chilensis) anthocyanin, restores tear secretion in a rat dry eye model,” Journal of Functional Foods, vol. 10, pp. 346–354, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Kalt, A. Hanneken, P. Milbury, and F. Tremblay, “Recent research on polyphenolics in vision and eye health,” Journal of Agricultural and Food Chemistry, vol. 58, no. 7, pp. 4001–4007, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Wang, L. Zhao, F. Lu et al., “Retinoprotective effects of bilberry anthocyanins via antioxidant, anti-inflammatory, and anti-apoptotic mechanisms in a visible light-induced retinal degeneration model in pigmented rabbits,” Molecules, vol. 20, no. 12, pp. 22395–22410, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Wang, D. Zhang, Y. X. Liu, D. Wang, J. Liu, and B. P. Ji, “The protective effects of berry-derived anthocyanins against visible light-induced damage in human retinal pigment epithelial cells,” Journal of the Science of Food and Agriculture, vol. 95, no. 5, pp. 936–944, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Bell, D. J. Lamport, L. T. Butler, and C. M. Williams, “A study of glycaemic effects following acute anthocyanin-rich blueberry supplementation in healthy young adults,” Food & Function, vol. 8, no. 9, pp. 3104–3110, 2017. View at Publisher · View at Google Scholar · View at Scopus
  15. S. A. Johnson, A. Figueroa, N. Navaei et al., “Daily blueberry consumption improves blood pressure and arterial stiffness in postmenopausal women with pre- and stage 1-hypertension: a randomized, double-blind, placebo-controlled clinical trial,” Journal of the Academy of Nutrition and Dietetics, vol. 115, no. 3, pp. 369–377, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Liu, D. Zhang, J. Hu et al., “Visible light-induced lipid peroxidation of unsaturated fatty acids in the retina and the inhibitory effects of blueberry polyphenols,” Journal of Agricultural and Food Chemistry, vol. 63, no. 42, pp. 9295–9305, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Li, R. Deng, X. Hua et al., “Blueberry component pterostilbene protects corneal epithelial cells from inflammation via anti-oxidative pathway,” Scientific Reports, vol. 6, no. 1, article 19408, 2016. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Liu, X. Song, Y. Han et al., “Identification of anthocyanin components of wild Chinese blueberries and amelioration of light-induced retinal damage in pigmented rabbit using whole berries,” Journal of Agricultural and Food Chemistry, vol. 59, no. 1, pp. 356–363, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Li, J. Feng, W.-Y. Huang, and X.-T. An, “Composition of polyphenols and antioxidant activity of rabbiteye blueberry (Vaccinium ashei) in Nanjing,” Journal of Agricultural and Food Chemistry, vol. 61, no. 3, pp. 523–531, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. E. C. Leal, C. A. Aveleira, Á. F. Castilho et al., “High glucose and oxidative/nitrosative stress conditions induce apoptosis in retinal endothelial cells by a caspase-independent pathway,” Experimental Eye Research, vol. 88, no. 5, pp. 983–991, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. X. Zhu, K. Wang, K. Zhang et al., “Tetramethylpyrazine protects retinal capillary endothelial cells (TR-iBRB2) against IL-1β-induced nitrative/oxidative stress,” International Journal of Molecular Sciences, vol. 16, no. 9, pp. 21775–21790, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Ago, T. Kitazono, H. Ooboshi et al., “Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase,” Circulation, vol. 109, no. 2, pp. 227–233, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Schroder, M. Zhang, S. Benkhoff et al., “Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase,” Circulation Research, vol. 110, no. 9, pp. 1217–1225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. F.-Y. Tang, F.-Y. Liu, and X.-W. Xie, “Association of angiotensin-converting enzyme and endothelial nitric oxide synthase gene polymorphisms with vascular disease in ESRD patients in a Chinese population,” Molecular and Cellular Biochemistry, vol. 319, no. 1-2, pp. 33–39, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Dursun, H. G. Durakbasi-Dursun, R. Dursun, S. Baris, and L. Akduman, “Angiotensin-converting enzyme gene and endothelial nitric oxide synthase gene polymorphisms in Behçet’s disease with or without ocular involvement,” Inflammation Research, vol. 58, no. 7, pp. 401–405, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Barton, F. Cosentino, R. P. Brandes, P. Moreau, S. Shaw, and T. F. Luscher, “Anatomic heterogeneity of vascular aging: role of nitric oxide and endothelin,” Hypertension, vol. 30, no. 4, pp. 817–824, 1997. View at Publisher · View at Google Scholar · View at Scopus
  27. D. F. Fitzpatrick, S. L. Hirschfield, T. Ricci, P. Jantzen, and R. G. Coffey, “Endothelium-dependent vasorelaxation caused by various plant extracts,” Journal of Cardiovascular Pharmacology, vol. 26, no. 1, pp. 90–95, 1995. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Nakamura, H. Matsumoto, and K. Todoki, “Endothelium-dependent vasorelaxation induced by black currant concentrate in rat thoracic aorta,” The Japanese Journal of Pharmacology, vol. 89, no. 1, pp. 29–35, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. P. J. Andrew and B. Mayer, “Enzymatic function of nitric oxide synthases,” Cardiovascular Research, vol. 43, no. 3, pp. 521–531, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. W. Y. Huang, X. N. Wang, C. Y. Li, Z. Yan, and W. M. Zhang, “Angiotensin I-converting enzyme inhibitory effects of malvidin and its glycosides from blueberry in endothelial cells,” Basic & Clinical Pharmacology & Toxicology, vol. 119, p. 21, 2016. View at Google Scholar
  31. M. Clozel, G. A. Gray, V. Breu, B. M. Löffler, and R. Osterwalder, “The endothelin ETB receptor mediates both vasodilation and vasoconstriction in vivo,” Biochemical and Biophysical Research Communications, vol. 186, no. 2, pp. 867–873, 1992. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Gardlik and I. Fusekova, “Pharmacologic therapy for diabetic retinopathy,” Seminars in Ophthalmology, vol. 30, no. 4, pp. 252–263, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. M. E. Cooper, D. Vranes, S. Youssef et al., “Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes,” Diabetes, vol. 48, no. 11, pp. 2229–2239, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. B. D. Manning and L. C. Cantley, “AKT/PKB signaling: navigating downstream,” Cell, vol. 129, no. 7, pp. 1261–1274, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. K. Olsson, A. Dimberg, J. Kreuger, and L. Claesson-Welsh, “VEGF receptor signalling? in control of vascular function,” Nature Reviews Molecular Cell Biology, vol. 7, no. 5, pp. 359–371, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Morbidelli, S. Donnini, and M. Ziche, “Role of nitric oxide in the modulation of angiogenesis,” Current Pharmaceutical Design, vol. 9, no. 7, pp. 521–530, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. N. Jiang, X. L. Chen, H. W. Yang, and Y. R. Ma, “Effects of nuclear factor κB expression on retinal neovascularization and apoptosis in a diabetic retinopathy rat model,” International Journal of Ophthalmology, vol. 8, no. 3, pp. 448–452, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Tornatore, A. K. Thotakura, J. Bennett, M. Moretti, and G. Franzoso, “The nuclear factor kappa B signaling pathway: integrating metabolism with inflammation,” Trends in Cell Biology, vol. 22, no. 11, pp. 557–566, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Khalfaoui, G. Lizard, and A. Ouertani-Meddeb, “Adhesion molecules (ICAM-1 and VCAM-1) and diabetic retinopathy in type 2 diabetes,” Journal of Molecular Histology, vol. 39, no. 2, pp. 243–249, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Paixão, T. C. P. Dinis, and L. M. Almeida, “Malvidin-3-glucoside protects endothelial cells up-regulating endothelial NO synthase and inhibiting peroxynitrite-induced NF-kB activation,” Chemico-Biological Interactions, vol. 199, no. 3, pp. 192–200, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Wang, Y. Huo, L. Zhao et al., “Cyanidin-3-glucoside and its phenolic acid metabolites attenuate visible light-induced retinal degeneration in vivo via activation of Nrf2/HO-1 pathway and NF-κB suppression,” Molecular Nutrition & Food Research, vol. 60, no. 7, pp. 1564–1577, 2016. View at Publisher · View at Google Scholar · View at Scopus