Salvianolic acid A alleviates ischemic brain injury through the inhibition of inflammation and apoptosis and the promotion of neurogenesis in mice

Free Radical Biology and Medicine

Volumn 99, Issue , 2016, Pages 508-519

  Chien, Mei Yin ^b,k   Chuang, Cheng Hung ^c   Chern, Chang Ming ^e,f   Liou, Kou Tong ^l   Liu, Der Zen ^b,g   Hou, Yu Chang ^d,h   Shen, Yuh Chiang ^a,i,j  

^a NATIONAL RESEARCH INSTITUTE OF CHINESE MEDICINE   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c HUNGKUANG UNIVERSITY   (Taiwan)

^d TAO YUAN GENERAL HOSPITAL   (Taiwan)

^e TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^f NATIONAL YANG MING UNIVERSITY   (Taiwan)

^g HSUAN CHUANG UNIVERSITY   (Taiwan)

^h CHUNG YUAN CHRISTIAN UNIVERSITY   (Taiwan)

ⁱ NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^j NATIONAL TAIPEI UNIVERSITY OF NURSING AND HEALTH SCIENCES   (Taiwan)

^k KO DA PHARMACEUTICAL CO LTD   (Taiwan)

^l CHINESE CULTURE UNIVERSITY   (Taiwan)

more..

Author keywords

Cdk5, doublecortin; Glycogen synthase kinase 3 (GSK3); Ischemic stroke; Salvianolic acid A (SalA); catenin

Indexed keywords

3 NITROTYROSINE; ALTEPLASE; ANTIINFLAMMATORY AGENT; BETA CATENIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CAFFEIC ACID DERIVATIVE; CASPASE 3; CYCLIN DEPENDENT KINASE 5; DOUBLECORTIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; MICROTUBULE ASSOCIATED PROTEIN 1; NEUROPROTECTIVE AGENT; OCCLUDIN; PROTEIN BCL 2; PROTEIN P25; SALVIANOLIC ACID A; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; ANTIOXIDANT; BCL2 PROTEIN, MOUSE; CDK5 PROTEIN, MOUSE; CTNNB1 PROTEIN, MOUSE; DOUBLECORTIN PROTEIN; GSK3B PROTEIN, MOUSE; LACTIC ACID DERIVATIVE; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE; NONSTEROID ANTIINFLAMMATORY AGENT; RELA PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; BRAIN INFARCTION; BRAIN ISCHEMIA; CONTROLLED STUDY; DENTATE GYRUS; DENTATE GYRUS GRANULAR LAYER; DISEASE SEVERITY; ENZYME ACTIVATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MORTALITY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SURVIVAL RATE; UPREGULATION; ANIMAL; CEREBROVASCULAR ACCIDENT; DISEASE MODEL; DRUG ADMINISTRATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; SURVIVAL ANALYSIS;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; APOPTOSIS; BETA CATENIN; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; BRAIN-DERIVED NEUROTROPHIC FACTOR; CAFFEIC ACIDS; CYCLIN-DEPENDENT KINASE 5; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3 BETA; INJECTIONS, INTRAVENOUS; LACTATES; MALE; MICE; MICE, INBRED ICR; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEUROPEPTIDES; PROTO-ONCOGENE PROTEINS C-BCL-2; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STROKE; SURVIVAL ANALYSIS; TRANSCRIPTION FACTOR RELA;

EID: 84987944990     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.09.006     Document Type: Article

References (35)

1. [1] Cardiovascular diseases (CVDs), Enferemedades cerebrovasculares Nota informativa. Available online at: 〈http://www.who.int/mediacentre/factsheets/fs317/en/〉, 2015.
2. [2] Lapchak, P.A., Neuroprotective and neurotrophic curcuminoids to treat stroke: a translational perspective. Expert Opin. Investig. Drug 20 (2011), 13–22.
3. [3] Ridder, D.A., Schwaninger, M., NF-kappaB signaling in cerebral ischemia. Neuroscience 158 (2009), 995–1006.
4. [4] Fernandez-Lopez, D., Faustino, J., Daneman, R., Zhou, L., Lee, S.Y., Derugin, N., Wendland, M.F., Vexler, Z.S., Blood-brain barrier permeability is increased after acute adult stroke but not neonatal stroke in the rat. J. Neurosci. 32 (2012), 9588–9600.
5. [5] Harari, O.A., Liao, J.K., NF-κB and innate immunity in ischemic stroke. Ann. NY Acad. Sci. 1207 (2010), 32–40.
6. [6] Chuang, D.M., Wang, Z., Chiu, C.T., GSK-3 as a target for lithium-induced neuroprotection against excitotoxicity in neuronal cultures and animal models of ischemic stroke. Front. Mol. Neurosci. 4 (2011), 15–27.
7. [7] Slevin, M., Krupinski, J., Cyclin-dependent kinase-5 targeting for ischaemic stroke. Curr. Opin. Pharmacol. 9 (2009), 119–124.
8. [8] Kawauchi, T., Cdk5 regulates multiple cellular events in neural development, function and disease. Dev. Growth Differ. 56 (2014), 335–348.
9. [9] Chern, C.M., Liao, J.F., Wang, Y.H., Shen, Y.C., Melatonin ameliorates neural function by promoting endogenous neurogenesis through the MT2 melatonin receptor in ischemic-stroke mice. Free Radic. Biol. Med. 52 (2012), 1634–1647.
10. [10] Chern, C.M., Wang, Y.H., Liou, K.T., Hou, Y.C., Chen, C.C., Shen, Y.C., 2-Methoxystypandrone ameliorates brain function through preserving BBB integrity and promoting neurogenesis in mice with acute ischemic stroke. Biochem. Pharmacol. 87 (2014), 502–514.
11. [11] Pan, H., Li, D., Fang, F., Chen, D., Qi, L., Zhang, R., Xu, T., Sun, H., Salvianolic acid A demonstrates cardioprotective effects in rat hearts and cardiomyocytes after ischemia/reperfusion injury. J. Cardiovasc. Pharmacol. 58 (2011), 535–542.
12. [12] Fan, H., Yang, L., Fu, F., Xu, H., Meng, Q., Zhu, H., Teng, L., Yang, M., Zhang, L., Zhang, Z., Liu, K., Cardioprotective effects of salvianolic acid a on myocardial ischemia-reperfusion injury in vivo and in vitro. Evid. Based Complement. Altern. Med., 508938, 2012.
13. [13] Wang, S.B., Pang, X.B., Zhao, Y., Wang, Y.H., Zhang, L., Yang, X.Y., Fang, L.H., Du, G.H., Protection of salvianolic acid A on rat brain from ischemic damage via soluble epoxide hydrolase inhibition. J. Asian Nat. Prod. Res. 14 (2012), 1084–1092.
14. [14] Oh, K.S., Oh, B.K., Mun, J., Seo, H.W., Lee, B.H., Salvianolic acid A suppress lipopolysaccharide-induced NF-κB signaling pathway by targeting IKKβ. Int. Immunopharmacol. 11 (2011), 1901–1906.
15. [15] Huang, J., Qin, Y., Liu, B., Li, G.Y., Ouyang, L., Wang, J.H., In silico analysis and experimental validation of molecular mechanisms of salvianolic acid A-inhibited LPS-stimulated inflammation, in RAW264.7 macrophages. Cell Prolif. 46 (2013), 595–605.
16. [16] Li, L., Xu, T., Du, Y., Pan, D., Wu, W., Zhu, H., Zhang, Y., Li, D., Salvianolic acid A attenuates cell apoptosis, oxidative stress, Akt and NF-κB activation in angiotensin-II induced murine peritoneal macrophages. Curr. Pharm. Biotechnol. 17 (2016), 283–290.
17. [17] Kim, H.H., Sawada, N., Soydan, G., Lee, H.S., Zhou, Z., Hwang, S.K., Waeber, C., Moskowitz, M.A., Liao, J.K., Additive effects of statin and dipyridamole on cerebral blood flow and stroke protection. J. Cereb. Blood Flow Metab. 28 (2008), 1285–1293.
18. [18] Wang, H.W., Liou, K.T., Wang, Y.H., Lu, C.K., Lin, Y.L., Lee, I.J., Huang, S.T., Tsai, Y.H., Cheng, Y.C., Lin, H.J., Shen, Y.C., Deciphering the neuroprotective mechanisms of Bu-yang Huan-wu decoction by an integrative neurofunctional and genomic approach in ischemic stroke mice. J. Ethnopharmacol. 138 (2011), 22–33.
19. [19] Lucas, J.J., Hernandez, F., Gomez-Ramos, P., Moran, M.A., Hen, R., Avila, J., Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 20 (2001), 27–39.
20. [20] Sirerol-Piquer, M., Gomez-Ramos, P., Hernandez, F., Perez, M., Moran, M.A., Fuster-Matanzo, A., Lucas, J.J., Avila, J., García-Verdugo, J.M., GSK3beta overexpression induces neuronal death and a depletion of the neurogenic niches in the dentate gyrus. Hippocampus 21 (2011), 910–922.
21. [21] McEntee, M.F., Chiu, C.H., Whelan, J., Relationship of beta-catenin and Bcl-2 expression to sulindac-induced regression of intestinal tumors in Min mice. Carcinogenesis 20 (1999), 635–640.
22. [22] Tanaka, T., Serneo, F.F., Tseng, H.C., Kulkarni, A.B., Tsai, L.H., Gleeson, J.G., Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41 (2004), 215–227.
23. [23] Tanaka, T., Serneo, F.F., Higgins, C., Gambello, M.J., Wynshaw-Boris, A., Gleeson, J.G., Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165 (2004), 709–721.
24. [24] Tan, X., Chen, Y., Li, J., Li, X., Miao, Z., Xin, N., Zhu, J., Ge, W., Feng, Y., Xu, X., The inhibition of Cdk5 activity after hypoxia/ischemia injury reduces infarct size and promotes functional recovery in neonatal rats. Neuroscience 290 (2015), 552–560.
25. [25] Zheng, Y.L., Amin, N.D., Hu, Y.F., Rudrabhatla, P., Shukla, V., Kanungo, J., Kesavapany, S., Grant, P., Albers, W., Pant, H.C., A 24-residue peptide (p5), derived from p35, the Cdk5 neuronal activator, specifically inhibits Cdk5-p25 hyperactivity and tau hyperphosphorylation. J. Biol. Chem. 285 (2010), 34202–34212.
26. [26] Kawauchi, T., Chihama, K., Nishimura, Y.V., Nabeshima, Y., Hoshino, M., MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/p25, and JNK. Biochem. Biophys. Res. Commun. 331 (2005), 50–55.
27. [27] Barros-Miñones, L., Martín-de-Saavedra, D., Perez-Alvarez, S., Orejana, L., Suquía, V., Goñi-Allo, B., Hervias, I., López, M.G., Jordan, J., Aguirre, N., Puerta, E., Inhibition of calpain-regulated p35/cdk5 plays a central role in sildenafil-induced protection against chemical hypoxia produced by malonate. Biochim. Biophys. Acta, 705–717, 1832, 2013.
28. [28] Lee, J.H., Kim, K.T., Induction of cyclin-dependent kinase 5 and its activator p35 through the extracellular-signal-regulated kinase and protein kinase A pathways during retinoic-acid mediated neuronal differentiation in human neuroblastoma SK-N-BE(2)C cells. J. Neurochem. 91 (2004), 634–647.
29. [29] Shah, K., Lahiri, D.K., Cdk5 activity in the brain – multiple paths of regulation. J. Cell Sci. 127 (2014), 2391–2400.
30. [30] Wen, Y., Planel, E., Herman, M., Figueroa, H.Y., Wang, L., Liu, L., Lau, L.F., Yu, W.H., Duff, K.E., Interplay between cyclin-dependent kinase 5 and glycogen synthase kinase 3 beta mediated by neuregulin signaling leads to differential effects on tau phosphorylation and amyloid precursor protein processing. J. Neurosci. 28 (2008), 2624–2632.
31. [31] Yu, X., Zhang, L., Yang, X., Li, X., Du, G., Salvianolic acid a improves the intestinal motility in diabetic rats through antioxidant capacity and up-regulation of nNOS. J. Dig. Dis., 2016 (Epub ahead of print).
32. [32] Wu, P., Yan, Y., Ma, L.L., Hou, B.Y., He, Y.Y., Zhang, L., Niu, Z.R., Song, J.K., Pang, X.C., Yang, X.Y., Du, G.H., Effects of the Nrf2 modulator salvianolic acid a alone or combined with metformin on diabetes-associated macrovascular and renal injury. J. Biol. Chem., 2016 (Epub ahead of print).
33. [33] Xu, H., Li, Y., Che, X., Tian, H., Fan, H., Liu, K., Metabolism of salvianolic acid A and antioxidant activities of its methylated metabolites. Drug Metab. Dispos. 42 (2014), 274–281.
34. [34] Hou, Y.C., Liou, K.T., Chern, C.M., Wang, Y.H., Liao, J.F., Chang, S., Chou, Y.H., Shen, Y.C., Preventive effect of silymarin in cerebral ischemia-reperfusion-induced brain injury in rats possibly through impairing NF-κB and STAT-1 activation. Phytomedicine 17 (2010), 963–973.
35. [35] Bathina, S., Das, U.N., Brain-derived neurotrophic factor and its clinical implications. Arch. Med. Sci. 11 (2015), 1164–1178.