Shengmai injection attenuates the cerebral ischemia/reperfusion induced autophagy via modulation of the AMPK, mTOR and JNK pathways

References

• Ayuso MI, Hernández-Jiménez M, Martín ME, Salinas M, AlcÃzar A. 2010. New hierarchical phosphorylation pathway of the translational repressor eIF4E-binding protein 1 (4E-BP1) in ischemia-reperfusion stress. J Biol Chem. 285:34355–34363.
   PubMed Web of Science ®Google Scholar
• Bansal S, Sangha KS, Khatri P. 2013. Drug treatment of acute ischemic stroke. Am J Cardiovasc Drugs. 13:57–69.
   PubMed Web of Science ®Google Scholar
• Chen J, Yao Y, Chen H, Kwong JS, Chen J. 2012. Shengmai (a traditional Chinese herbal medicine) for heart failure. Cochrane Database Syst Rev. 11:CD005052
   Google Scholar
• Chen Z, Lu T, Yue X, Wei N, Jiang Y, Chen M, Ni G, Liu X, Xu G. 2010. Neuroprotective effect of ginsenoside Rb1 on glutamate-induced neurotoxicity: with emphasis on autophagy. Neurosci Lett. 482:264–268.
   PubMed Web of Science ®Google Scholar
• Cheng HY, Hsieh MT, Wu CR, Tsai FH, Lu TC, Hsieh CC, Li WC, Lin YT, Peng WH. 2008. Schizandrin protects primary cultures of rat cortical cells from glutamate-induced excitotoxicity. J Pharmacol Sci. 107:21–31.
   PubMed Web of Science ®Google Scholar
• Chu CT, Plowey ED, Dagda RK, Hickey RW, Cherra SJ 3rd, Clark RS. 2009. Autophagy in neurite injury and neurodegeneration: in vitro and in vivo models. Meth Enzymol. 453:217–249.
   PubMed Web of Science ®Google Scholar
• Cui D, Wang L, Qi A, Zhou Q, Zhang X, Jiang W. 2012. Propofol prevents autophagic cell death following oxygen and glucose deprivation in PC12 cells and cerebral ischemia-reperfusion injury in rats. PLoS One. 7:e35324.
   PubMed Web of Science ®Google Scholar
• De Meyer GR, Martinet W. 2009. Autophagy in the cardiovascular system. Biochim Biophys Acta. 1793:1485–1495.
   PubMed Web of Science ®Google Scholar
• Fu P, Peng C, Ding JY, Asmaro K, Sullivan JM, Guthikonda M, Ding Y. 2013. Acute administration of ethanol reduces apoptosis following ischemic stroke in rats. Neurosci Res. 76:93–97.
   PubMed Web of Science ®Google Scholar
• Gao L, Jiang T, Guo J, Liu Y, Cui G, Gu L, Su L, Zhang Y. 2012. Inhibition of autophagy contributes to ischemic postconditioning-induced neuroprotection against focal cerebral ischemia in rats. PLoS One. 7:e46092.
   PubMed Web of Science ®Google Scholar
• Garcia JH, Wagner S, Liu KF, Hu XJ. 1995. Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats Statistical validation. Stroke. 26:627–634.
   PubMed Web of Science ®Google Scholar
• Gu JH, Ge JB, Li M, Wu F, Zhang W, Qin ZH. 2012. Inhibition of NF-κB activation is associated with anti-inflammatory and anti-apoptotic effects of Ginkgolide B in a mouse model of cerebral ischemia/reperfusion injury. Eur J Pharm Sci. 47:652–660.
   PubMed Web of Science ®Google Scholar
• Guo C, Tong L, Xi M, Yang H, Dong H, Wen A. 2012. Neuroprotective effect of calycosin on cerebral ischemia and reperfusion injury in rats. J Ethnopharmacol. 144:768–774.
   PubMed Web of Science ®Google Scholar
• Guo Z, Cao G, Yang H, Zhou H, Li L, Cao Z, Yu B, Kou J. 2014. A combination of four active compounds alleviates cerebral ischemia reperfusion injury in correlation with inhibition of autophagy and modulation of AMPK/mTOR and jnk pathways. J Neurosci Res. 92:1295–1306.
   PubMed Web of Science ®Google Scholar
• Hashimoto R, Yu J, Koizumi H, Ouchi Y, Okabe T. 2012. Ginsenoside Rb1 prevents MPP(+)-induced apoptosis in PC12 cells by stimulating estrogen receptors with consequent activation of ERK1/2, Akt and inhibition of SAPK/JNK, p38 MAPK. Evid Based Complement Alternat Med. 2012:693717.
   PubMed Web of Science ®Google Scholar
• Hill MD, Martin RH, Mikulis D, Wong JH, Silver FL, Terbrugge KG, Milot G, Clark WM, Macdonald RL, Kelly ME, et al. 2012. Safety and efficacy of NA-1 in patients with iatrogenic stroke after endovascular aneurysm repair (ENACT): a phase 2, randomised, double-blind, placebo-controlled trial. Lancet Neurol. 11:942–950.
   PubMed Web of Science ®Google Scholar
• Huang J, Li Y, Tang Y, Tang G, Yang GY, Wang Y. 2013. CXCR4 antagonist AMD3100 protects blood-brain barrier integrity and reduces inflammatory response after focal ischemia in mice. Stroke. 44:190–197.
   PubMed Web of Science ®Google Scholar
• Huang P, Zhou CM. Qin-Hu, Liu YY, Hu BH, Chang X, Zhao XR, Xu XS, Li Q, Wei XH. 2012. Cerebralcare Granule(R) attenuates blood-brain barrier disruption after middle cerebral artery occlusion in rats. Exp Neurol. 237:453–463.
   PubMed Web of Science ®Google Scholar
• Jiang M, Li J, Peng Q, Liu Y, Liu W, Luo C, Peng J, Li J, Yung KK, Mo Z. 2014. Neuroprotective effects of bilobalide on cerebral ischemia and reperfusion injury are associated with inhibition of pro-inflammatory mediator production and down-regulation of JNK1/2 and p38 MAPK activation. J Neuroinflammation. 11:167
   PubMed Web of Science ®Google Scholar
• Khayyam N, Thavendiranathan P, Carmichael FJ, Kus B, Jay V, Burnham WM. 1999. Neuroprotective effects of acetylsalicylic acid in an animal model of focal brain ischemia. Neuroreport. 10:371–374.
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, Guan KL. 2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 13:132–141.
   PubMed Web of Science ®Google Scholar
• Kiyono K, Suzuki HI, Matsuyama H, Morishita Y, Komuro A, Kano MR, Sugimoto K, Miyazono K. 2009. Autophagy is activated by TGF-beta and potentiates TGF-beta-mediated growth inhibition in human hepatocellular carcinoma cells. Cancer Res. 69:8844–8852.
   PubMed Web of Science ®Google Scholar
• Koh PO. 2008. Melatonin prevents ischemic brain injury through activation of the mTOR/p70S6 kinase signaling pathway. Neurosci Lett. 444:74–78.
   PubMed Web of Science ®Google Scholar
• Koh PO, Cho JH, Won CK, Lee HJ, Sung JH, Kim MO. 2008. Estradiol attenuates the focal cerebral ischemic injury through mTOR/p70S6 kinase signaling pathway. Neurosci Lett. 436:62–66.
   PubMed Web of Science ®Google Scholar
• Kost A, Kasprowska D, Labuzek K, Wiaderkiewicz R, Gabryel B. (2011). Autophagy in brain ischemia. Postȩpy Hig Med Dośw [Online].Avaliable at:http://www.researchgate.net/publication/51630233.Accessed on 13 August 2015.
   Google Scholar
• Kroemer G, Mariño G, Levine B. 2010. Autophagy and the integrated stress response. Mol Cell. 40:280–293.
   PubMed Web of Science ®Google Scholar
• Lee IY, Lee CC, Chang CK, Chien CH, Lin MT. 2005. Sheng mai san, a Chinese herbal medicine, protects against renal ischaemic injury during heat stroke in the rat. Clin Exp Pharmacol Physiol. 32:742–748.
   PubMed Web of Science ®Google Scholar
• Lee KW, Jung SY, Choi SM, Yang EJ. 2012. Effects of ginsenoside Re on LPS-induced inflammatory mediators in BV2 microglial cells. BMC Complement Altern Med. 12:196.
   PubMed Web of Science ®Google Scholar
• Levine B, Kroemer G. 2008. Autophagy in the pathogenesis of disease. Cell. 132:27–42.
   PubMed Web of Science ®Google Scholar
• Li J, McCullough LD. 2010. Effects of AMP-activated protein kinase in cerebral ischemia. J Cereb Blood Flow Metab. 30:480–492.
   PubMed Web of Science ®Google Scholar
• Liu L, Fang YQ, Xue ZF, He YP, Fang RM, Li L. 2012. β-Asarone attenuates ischemia-reperfusion-induced autophagy in rat brains via modulating JNK, p-JNK, Bcl-2 and Beclin 1. Eur J Pharmacol. 680:34–40.
   PubMed Web of Science ®Google Scholar
• Liu Q, Kou JP, Yu BY. 2011. Ginsenoside Rg1 protects against hydrogen peroxide-induced cell death in PC12 cells via inhibiting NF-κB activation. - activation. Neurochem Int. 58:119–125.
   PubMed Web of Science ®Google Scholar
• Lu T, Jiang Y, Zhou Z, Yue X, Wei N, Chen Z, Ma M, Xu G, Liu X. 2011. Intranasal ginsenoside Rb1 targets the brain and ameliorates cerebral ischemia/reperfusion injury in rats. Biol Pharm Bull. 34:1319–1324.
   PubMed Web of Science ®Google Scholar
• Macrez R, Ali C, Toutirais O, Le Mauff B, Defer G, Dirnagl U, Vivien D. 2011. Stroke and the immune system: from pathophysiology to new therapeutic strategies. Lancet Neurol. 10:471–480.
   PubMed Web of Science ®Google Scholar
• Matsui Y, Kyoi S, Takagi H, Hsu CP, Hariharan N, Ago T, Vatner SF, Sadoshima J. 2008. Molecular mechanisms and physiological significance of autophagy during myocardial ischemia and reperfusion. Autophagy. 4:409–415.
   PubMed Web of Science ®Google Scholar
• McCullough LD, Zeng Z, Li H, Landree LE, McFadden J, Ronnett GV. 2005. Pharmacological inhibition of AMP-activated protein kinase provides neuroprotection in stroke. J Biol Chem. 280:20493–20502.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yoshimori T, Levine B. 2010. Methods in mammalian autophagy research. Cell. 140:313–326.
   PubMed Web of Science ®Google Scholar
• Nam HG, Kim W, Yoo DY, Choi JH, Won MH, Hwang IK, Jeong JH, Hwang HS, Moon SM. 2013. Chronological changes and effects of AMP-activated kinase in the hippocampal CA1 region after transient forebrain ischemia in gerbils. Neurol Res. 35:395–405.
   PubMed Web of Science ®Google Scholar
• Ozbal S, Erbil G, Kocdor H, Tuğyan K, Pekçetin C, Ozoğul C. 2008. The effects of selenium against cerebral ischemia-reperfusion injury in rats. Neurosci Lett. 438:265–269.
   PubMed Web of Science ®Google Scholar
• Powers WJ, Derdeyn CP, Biller J, Coffey CS, Hoh BL, Jauch EC, Johnston KC, Johnston SC, Khalessi AA, Kidwell CS, et al. 2015. 2015 American Heart Association/American Stroke Association focused update of the 2013 guidelines for the early management of patients with acute ischemic stroke regarding endovascular treatment: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 46:3020–3035.
   PubMed Web of Science ®Google Scholar
• Pamenter ME, Perkins GA, McGinness AK, Gu XQ, Ellisman MH, Haddad GG. 2012. Autophagy and apoptosis are differentially induced in neurons and astrocytes treated with an in vitro mimic of the ischemic penumbra. PLoS One. 7:e51469.
   PubMed Web of Science ®Google Scholar
• Park JS, Manzanero S, Chang JW, Choi Y, Baik SH, Cheng YL, Li YI, Gwon AR, Woo HN, Jang J. 2012. Calsenilin contributes to neuronal cell death in ischemic stroke. Brain Pathol. 23:402–412.
   PubMed Web of Science ®Google Scholar
• Puyal J, Clarke PG. 2009. Targeting autophagy to prevent neonatal stroke damage. Autophagy. 5:1060–1061.
   PubMed Web of Science ®Google Scholar
• Rami A, Langhagen A, Steiger S. 2008. Focal cerebral ischemia induces upregulation of Beclin 1 and autophagy-like cell death. Neurobiol Dis. 29:132–141.
   PubMed Web of Science ®Google Scholar
• Reggiori F, Klionsky DJ. 2002. Autophagy in the eukaryotic cell. Eukaryotic Cell. 1:11–21.
   PubMed Web of Science ®Google Scholar
• Sheng R, Zhang LS, Han R, Liu XQ, Gao B, Qin ZH. 2010. Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy. 6:482–494.
   PubMed Web of Science ®Google Scholar
• Szydlowska K, Tymianski M. 2010. Calcium, ischemia and excitotoxicity. Cell Calcium. 47:122–129.
   PubMed Web of Science ®Google Scholar
• Shen K, Wang Y, Zhang Y, Zhou H, Song Y, Cao Z, Kou J, Yu B. 2015. Cocktail of four active components derived from Sheng Mai San inhibits hydrogen peroxide-induced PC12 cell apoptosis linked with the caspase-3/ROCK1/MLC pathway. Rejuvenation Res. 18:517–527.
   PubMed Web of Science ®Google Scholar
• Tian F, Deguchi K, Yamashita T, Ohta Y, Morimoto N, Shang J, Zhang X, Liu N, Ikeda Y, Matsuura T, et al. 2010. In vivo imaging of autophagy in a mouse stroke model. Autophagy. 6:1107–1114.
   PubMed Web of Science ®Google Scholar
• Wang XM, Zhao C, Wang SX, Lin XY, Liu XL. 2015. Research on Xueshuantong injection through blood brain barrier. Drug Eval Res. 38:384–389.
   Google Scholar
• Wang N, Minatoguchi S, Arai M, Uno Y, Nishida Y, Hashimoto K, Xue-Hai C, Fukuda K, Akao S, Takemura G, et al. 2002. Sheng-Mai-San is protective against post-ischemic myocardial dysfunction in rats through its opening of the mitochondrial KATP channels. Circ J. 66:763–768.
   PubMed Web of Science ®Google Scholar
• Wei X, Ye X, Xie Y, Zou Y, Zhao X, Han J, Wang X, Ma Y, Bi Q, Xie Q, et al. 2011. Post-marketed re-evaluation of fleabane injection and Dengzhan Shengmai capsule study on treatment in patients with ischemic stroke. Zhongguo Zhong Yao Za Zhi. 36:2789–2792.
   PubMedGoogle Scholar
• Wei Y, Pattingre S, Sinha S, Bsaaik M, Levine B. 2008. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell. 30:678–688.
   PubMed Web of Science ®Google Scholar
• Winters L, Winters T, Gorup D, Mitrečić D, Curlin M, Križ J, Gajovic S. 2013. Expression analysis of genes involved in TLR2-related signaling pathway: Inflammation and apoptosis after ischemic brain injury. Neuroscience. 238:87–96.
   PubMed Web of Science ®Google Scholar
• Wirawan E, Lippens S, Vanden Berghe T, Romagnoli A, Fimia GM, Piacentini M, Vandenabeele P. 2012. Beclin1: a role in membrane dynamics and beyond. Autophagy. 8:6–17.
   PubMed Web of Science ®Google Scholar
• Wong CH, Crack PJ. 2008. Modulation of neuro-inflammation and vascular response by oxidative stress following cerebral ischemia-reperfusion injury. Curr Med Chem. 15:1–14.
   PubMed Web of Science ®Google Scholar
• Xie R, Wang P, Ji X, Zhao H. 2013. Ischemic post-conditioning facilitates brain recovery after stroke by promoting Akt/mTOR activity in nude rats. J Neurochem. 127:723–732.
   PubMed Web of Science ®Google Scholar
• Xu M, Zhang HL. 2011. Death and survival of neuronal and astrocytic cells in ischemic brain injury: a role of autophagy. Acta Pharmacol Sin. 32:1089–1099.
   PubMed Web of Science ®Google Scholar
• Xu BB, Liu CQ, Gao X, Zhang WQ, Wang SW, Cao YL. 2005. Possible mechanisms of the protection of ginsenoside Re against MPTP-induced apoptosis in substantia nigra neurons of Parkinson's disease mouse model. J Asian Nat Prod Res. 7:215–224.
   PubMed Web of Science ®Google Scholar
• Yan W, Zhang H, Bai X, Liu Y, Dong H, Xiong L. 2011. Autophagy activation is involved in neuroprotection induced by hyperbaric oxygen preconditioning against focal cerebral ischemia in rats. Brain Res. 1402:109–121.
   PubMed Web of Science ®Google Scholar
• Yang HP, Li L, Chai CZ, Kou JP, Yu BY, Yan YQ. 2013. Neuroprotective effect of Shengmai Injection on expression of tissue factor and related signal pathways in mice with cerebral ischemia- reperfusion injury. Chin J Exp Trad Med Formulae. 19:191–196.
   Google Scholar
• Yang Z, Klionsky DJ. 2010. Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol. 22:124–131.
   PubMed Web of Science ®Google Scholar
• Yuan QL, Yang CX, Xu P, Gao XQ, Deng L, Chen P, Sun ZL, Chen QY. 2007. Neuroprotective effects of ginsenoside Rb1 on transient cerebral ischemia in rats. Brain Res. 1167:1–12.
   PubMed Web of Science ®Google Scholar
• Yousuf S, Atif F, Ahmad M, Hoda N, Ishrat T, Khan B, Islam F, et al. 2009. Resveratrol exerts its neuroprotective effect by modulating mitochondrial dysfunctions and associated cell death during cerebral ischemia. Brain Res. 1250:242–253.
   PubMed Web of Science ®Google Scholar
• Zhang F, Yin W, Chen J. 2004. Apoptosis in cerebral ischemia: executional and regulatory signaling mechanisms. Neurol Res. 26:835–845.
   PubMed Web of Science ®Google Scholar
• Zheng C, Han J, Xia W, Shi S, Liu J, Ying W. 2012. NAD(+) administration decreases ischemic brain damage partially by blocking autophagy in a mouse model of brain ischemia. Neurosci Lett. 512:67–71.
   PubMed Web of Science ®Google Scholar