Sodium Tanshinone IIA Silate Alleviates High Glucose Induced Barrier Impairment of Human Retinal Pigment Epithelium through the Reduction of NF-κB Activation via the AMPK/p300 Pathway

References

• Xu YX, Jiang ZX, Huang JH, Meng QL, Coh P, Tao LM. The association between toll-like receptor 4 polymorphisms and diabetic retinopathy in Chinese patients with type 2 diabetes. Brit J Ophthalmol. 2015;99:1301–05. doi:10.1136/bjophthalmol-2015-306677.
   PubMed Web of Science ®Google Scholar
• Pavan B, Dalpiaz A. Retinal pigment epithelial cells as a therapeutic tool and target against retinopathies. Drug Discov Today. 2018;23:1672–79. doi:10.1016/j.drudis.2018.06.009.
   PubMed Web of Science ®Google Scholar
• You ZP, Chen SS, Yang ZY, Li SR, Xiong F, Liu T, SH F. GEP100/ARF6 regulates VEGFR2 signaling to facilitate high glucose induced epithelial-mesenchymal transition and cell permeability in RPE cells. Am J Physiol Cell Physiol. 2019;316:C782–C791. doi:10.1152/ajpcell.00312.2018.
   Web of Science ®Google Scholar
• Xia T, Rizzolo LJ. Effects of diabetic retinopathy on the barrier functions of the retinal pigment epithelium. Vision Res. 2017;139:72–81. doi:10.1016/j.visres.2017.02.006.
   PubMed Web of Science ®Google Scholar
• Misra P. AMP activated protein kinase: a next generation target for total metabolic control. Expert Opin Ther Targets. 2008;12:91–100. doi:10.1517/14728222.12.1.91.
   PubMed Web of Science ®Google Scholar
• Kim YS, Kim M, Choi MY, Lee DH, Roh GS, Kim HJ, Kang SS, Cho GJ, Hong EK, Choi WS. Alpha-lipoic acid reduces retinal cell death in diabetic mice. Biochem Biophys Res Commun. 2018;503:1307–14. doi:10.1016/j.bbrc.2018.07.041.
   PubMed Web of Science ®Google Scholar
• Xu L, Kong L, Wang J, Ash JD. Stimulation of AMPK prevents degeneration of photoreceptors and the retinal pigment epithelium. Proc Natl Acad Sci U S A. 2018;115:10475–80. doi:10.1073/pnas.1802724115.
   PubMed Web of Science ®Google Scholar
• Navarro JF, Mora C. Role of inflammation in diabetic complications. Nephrol Dial Transplant. 2005;20:2601–04. doi:10.1093/ndt/gfi155.
   PubMed Web of Science ®Google Scholar
• Salminen A, Hyttinen JM, Kaarniranta K. AMP-activated protein kinase inhibits NF-kappaB signaling and inflammation: impact on healthspan and lifespan. J Mol Med (Berl). 2011;89:667–76. doi:10.1007/s00109-011-0748-0.
   PubMed Web of Science ®Google Scholar
• Kauppinen A, Suuronen T, Ojala J, Kaarniranta K, Salminen A. Antagonistic crosstalk between NF-kappaB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal. 2013;25:1939–48. doi:10.1016/j.cellsig.2013.06.007.
   PubMed Web of Science ®Google Scholar
• Ciccarelli M, Vastolo V, Albano L, Lecce M, Cabaro S, Liotti A, Longo M, Oriente F, Russo GL, Macchia PE, et al. Glucose-induced expression of the homeotic transcription factor Prep1 is associated with histone post-translational modifications in skeletal muscle. Diabetologia. 2016;59:176–86. doi:10.1007/s00125-015-3774-6.
   PubMed Web of Science ®Google Scholar
• Zhou L, Zuo Z, Chow MS. Danshen: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J Clin Pharmacol. 2005;45:1345–59. doi:10.1177/0091270005282630.
   PubMed Web of Science ®Google Scholar
• Jiang B, Zhang L, Wang Y, Li M, Wu W, Guan S, Liu X, Yang M, Wang J, Guo DA. Tanshinone IIA sodium sulfonate protects against cardiotoxicity induced by doxorubicin in vitro and in vivo. Food Chem Toxicol. 2009;47:1538–44. doi:10.1016/j.fct.2009.03.038.
   PubMed Web of Science ®Google Scholar
• Yuan FY, Zhang M, Xu P, Xu D, Chen P, Ren M, Sun Q, Chen JY, Du J, Tang XL. Tanshinone IIA improves diabetes mellitus via the NF-kappaB-induced AMPK signal pathway. Exp Ther Med. 2018;16:4225–31. doi:10.3892/etm.2018.6674.
   PubMed Web of Science ®Google Scholar
• Wu WY, Yan H, Wang XB, Gui YZ, Gao F, Tang XL, Qin YL, Su M, Chen T, Wang YP. Sodium tanshinone IIA silate inhibits high glucose-induced vascular smooth muscle cell proliferation and migration through activation of AMP-activated protein kinase. PLoS One. 2014;9:e94957. doi:10.1371/journal.pone.0094957.
   PubMed Web of Science ®Google Scholar
• Pavan B, Capuzzo A, Forlani G. High glucose-induced barrier impairment of human retinal pigment epithelium is ameliorated by treatment with Goji berry extracts through modulation of cAMP levels. Exp Eye Res. 2014;120:50–54. doi:10.1016/j.exer.2013.12.006.
   PubMed Web of Science ®Google Scholar
• Garcia-Ramirez M, Hernandez C, Palomer X, Vazquez-Carrera M, Simo R. Fenofibrate prevents the disruption of the outer blood retinal barrier through downregulation of NF-kappaB activity. Acta Diabetol. 2016;53:109–18. doi:10.1007/s00592-015-0759-3.
   PubMed Web of Science ®Google Scholar
• Zou XL, Wang GF, Li DD, Chen JX, Zhang CL, Yu YZ, Zhou WJ, Zou YP, Rao BQ. Protection of tight junction between RPE cells with tissue factor targeting peptide. Int J Ophthalmol. 2018;11:1594–99. doi:10.18240/ijo.2018.10.04.
   PubMed Web of Science ®Google Scholar
• Juuti-Uusitalo K, Nieminen M, Treumer F, Ampuja M, Kallioniemi A, Klettner A, Skottman H. Effects of cytokine activation and oxidative stress on the function of the human embryonic stem cell-derived retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 2015;56:6265–74. doi:10.1167/iovs.15-17333.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Qiu J, Wang X, Zhang Y, Xia M. AMP-activated protein kinase suppresses endothelial cell inflammation through phosphorylation of transcriptional coactivator p300. Arterioscler Thromb Vasc Biol. 2011;31:2897–908. doi:10.1161/ATVBAHA.111.237453.
   PubMed Web of Science ®Google Scholar
• Zhang J, Zhang Y, Xiao F, Liu Y, Wang J, Gao H, Rong S, Yao Y, Li J, Xu G. The peroxisome proliferator-activated receptor gamma agonist pioglitazone prevents NF-kappaB activation in cisplatin nephrotoxicity through the reduction of p65 acetylation via the AMPK-SIRT1/p300 pathway. Biochem Pharmacol. 2016;101:100–11. doi:10.1016/j.bcp.2015.11.027.
   PubMed Web of Science ®Google Scholar
• Simo R, Villarroel M, Corraliza L, Hernandez C, Garcia-Ramirez M. The retinal pigment epithelium: something more than a constituent of the blood-retinal barrier–implications for the pathogenesis of diabetic retinopathy. J Biomed Biotechnol. 2010;2010:190724. doi:10.1155/2010/190724.
   PubMedGoogle Scholar
• Chen Q, Tang L, Xin G, Li S, Ma L, Xu Y, Zhuang M, Xiong Q, Wei Z, Xing Z, et al. Oxidative stress mediated by lipid metabolism contributes to high glucose-induced senescence in retinal pigment epithelium. Free Radic Biol Med. 2019;130:48–58. doi:10.1016/j.freeradbiomed.2018.10.419.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Xi X, Mei Y, Zhao X, Zhou L, Ma M, Liu S, Zha X, Yang Y. High-glucose induces retinal pigment epithelium mitochondrial pathways of apoptosis and inhibits mitophagy by regulating ROS/PINK1/Parkin signal pathway. Biomed Pharmacother. 2019;111:1315–25. doi:10.1016/j.biopha.2019.01.034.
   PubMed Web of Science ®Google Scholar
• Harhaj NS, Antonetti DA. Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol. 2004;36:1206–37. doi:10.1016/j.biocel.2003.08.007.
   PubMed Web of Science ®Google Scholar
• Leal EC, Manivannan A, Hosoya K, Terasaki T, Cunha-Vaz J, Ambrosio AF, Forrester JV. Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2007;48:5257–65. doi:10.1167/iovs.07-0112.
   PubMed Web of Science ®Google Scholar
• Aveleira CA, Lin CM, Abcouwer SF, Ambrosio AF, Antonetti DA. TNF-alpha signals through PKCzeta/NF-kappaB to alter the tight junction complex and increase retinal endothelial cell permeability. Diabetes. 2010;59:2872–82. doi:10.2337/db09-1606.
   PubMed Web of Science ®Google Scholar
• DH J, Yun JH, Cho CS, Kim JH, Kim JH, Cho CH. Interaction between microglia and retinal pigment epithelial cells determines the integrity of outer blood-retinal barrier in diabetic retinopathy. Glia. 2019;67:321–31. doi:10.1002/glia.23542.
   PubMed Web of Science ®Google Scholar
• WY W, Wang WY, Ma YL, Yan H, Wang XB, Qin YL, Su M, Chen T, Wang YP. Sodium tanshinone IIA silate inhibits oxygen-glucose deprivation/recovery-induced cardiomyocyte apoptosis via suppression of the NF-kappaB/TNF-alpha pathway. Br J Pharmacol. 2013;169:1058–71. doi:10.1111/bph.12185.
   PubMed Web of Science ®Google Scholar
• Quivy V, Van Lint C. Regulation at multiple levels of NF-kappaB-mediated transactivation by protein acetylation. Biochem Pharmacol. 2004;68:1221–29. doi:10.1016/j.bcp.2004.05.039.
   PubMed Web of Science ®Google Scholar
• Kim YS, Kim M, Choi MY, Lee DH, Roh GS, Kim HJ, Kang SS, Cho GJ, Kim SJ, Yoo JM, et al. Metformin protects against retinal cell death in diabetic mice. Biochem Biophys Res Commun. 2017;492:397–403. doi:10.1016/j.bbrc.2017.08.087.
   PubMed Web of Science ®Google Scholar
• Vancura A, Nagar S, Kaur P, Bu P, Bhagwat M, Vancurova I. Reciprocal regulation of AMPK/SNF1 and protein acetylation. Int J Mol Sci. 2018;19:3314. doi: 10.3390/ijms19113314.
   Web of Science ®Google Scholar
• Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science. 2001;293:1653–57. doi:10.1126/science.1062374.
   PubMed Web of Science ®Google Scholar
• Hwang SL, Yang JH, Jeong YT, Kim YD, Li X, Lu Y, Chang YC, Son KH, Chang HW. Tanshinone IIA improves endoplasmic reticulum stress-induced insulin resistance through AMP-activated protein kinase. Biochem Biophys Res Commun. 2013;430:1246–52. doi:10.1016/j.bbrc.2012.12.066.
   PubMed Web of Science ®Google Scholar
• Li X, Park SJ, Jin F, Deng Y, Yang JH, Chang JH, Kim DY, Kim JA, Lee YJ, Murakami M, et al. Tanshinone IIA suppresses FcepsilonRI-mediated mast cell signaling and anaphylaxis by activation of the Sirt1/LKB1/AMPK pathway. Biochem Pharmacol. 2018;152:362–72. doi:10.1016/j.bcp.2018.04.015.
   PubMed Web of Science ®Google Scholar