Tanshinones and mental diseases: from chemistry to medicine
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Sana Javed
, Barbara Budzyńska
Abstract
The prevalence of mental diseases, especially neurodegenerative disorders, is ever-increasing, while treatment options for such disorders are limited and insufficient. In this scarcity of available medication, it is a feasible strategy to search for potential drugs among natural compounds, such as those found in plants. One such plant source is the root of Chinese sage, Salvia miltiorrhiza Bunge (Labiatae), which contains several compounds reported to possess neuroprotective activities. The most important of these compounds are tanshinones, which have been reported to possess ameliorative activity against a myriad of mental diseases such as Alzheimer’s disease, cerebral ischemia/reperfusion injury, and glioma, along with promoting neuronal differentiation and manifesting antinociceptive and anticonvulsant outcomes. This review offers a critical evaluation of the utility of tanshinones to treat mental illnesses, and sheds light on the underlying mechanisms through which these naturally occurring compounds confer neuroprotection.
Conflict of interest statement: The authors declare that they have no conflict of interest.
References
Adams, Jr, J.D. (2013). Treatment of stroke with danshen, Salvia miltiorrhiza. Traditional Chinese Medicine: Scientific Basis for its Use. James D. Adams, Eric J. Lien, eds. (Cambridge, UK: RSC) 31, p. 186.10.1039/9781849737852-00186Search in Google Scholar
Ahmed, T., Abdollahi, M., Daglia, M., Nabavi, S.F., and Nabavi, S.M. (2015). Berberine and neurodegeneration: a review of literature. Pharmacol. Rep. 67, 970–979.10.1016/j.pharep.2015.03.002Search in Google Scholar PubMed
Alinezhad, H., Azimi, R., Zare, M., Ebrahimzadeh, M.A., Eslami, S., Nabavi, S.F., and Nabavi, S.M. (2013). Antioxidant and antihemolytic activities of ethanolic extract of flowers, leaves, and stems of Hyssopus officinalis L. Var. angustifolius. Int. J. Food Prop. 16, 1169–1178.10.1080/10942912.2011.578319Search in Google Scholar
Bi, H.C., Law, F.C., Zhong, G.P., Xu, C.S., Pan, Y., Ding, L., Chen, X., Zhao, L.Z., Xu, Q., and Huang, M. (2007). Study of tanshinone IIA tissue distribution in rat by liquid chromatography-tandem mass spectrometry method. Biomed. Chromatogr. 21, 473–479.10.1002/bmc.778Search in Google Scholar PubMed
Bi, H.C., Zuo, Z., Chen, X., Xu, C.S., Wen, Y.Y., Sun, H.Y., Zhao, L.Z., Pan, Y., Deng, Y., and Liu, P.Q. (2008). Preclinical factors affecting the pharmacokinetic behaviour of tanshinone IIA, an investigational new drug isolated from Salvia miltiorrhiza for the treatment of ischaemic heart diseases. Xenobiotica 38, 185–222.10.1080/00498250701767675Search in Google Scholar PubMed
Brattlie, J., Xiec, J., and Belding, E. (2013). Modern drug discovery from Chinese materia medica used in traditional Chinese medicine. Traditional Chinese Medicine: Scientific Basis for Its Use. James D. Adams, Eric J. Lien, eds. (Cambridge, UK: RSC) 31, p. 81.10.1039/9781849737852-00081Search in Google Scholar
Buenafe, O.E., Orellana-Paucar, A., Maes, J., Huang, H., Ying, X., De Borggraeve, W., Crawford, A.D., Luyten, W., Esguerra, C.V., and de Witte, P. (2013). Tanshinone IIA exhibits anticonvulsant activity in zebrafish and mouse seizure models. ACS Chem. Neurosci. 4, 1479–1487.10.1021/cn400140eSearch in Google Scholar PubMed PubMed Central
Cai, H., Wen, X., Wen, L., Tirelli, N., Zhang, X., Zhang, Y., Su, H., Yang, F., and Chen, G. (2014). Enhanced local bioavailability of single or compound drugs delivery to the inner ear through application of PLGA nanoparticles via round window administration. Int. J. Nanomed. 9, 5591–5601.10.2147/IJN.S72555Search in Google Scholar PubMed PubMed Central
Cao, F.L., Su, X.J., Wang, Y., Xu, M., and Shan, L. (2014). Antinociceptive effects of systemic tanshinone IIA on visceral and somatic persistent nociception and pain hypersensitivity in rats. Pharmacol. Biochem. Behav. 124, 74–80.10.1016/j.pbb.2014.05.005Search in Google Scholar PubMed
Cao, F.L., Xu, M., Wang, Y., Gong, K.R., and Zhang, J.T. (2015). Tanshinone IIA attenuates neuropathic pain via inhibiting glial activation and immune response. Pharmacol. Biochem. Behav. 128, 1–7.10.1016/j.pbb.2014.11.004Search in Google Scholar PubMed
Chen, X., Zhou, Z.W., Xue, C., Li, X.X., and Zhou, S.F. (2007). Role of P-glycoprotein in restricting the brain penetration of tanshinone IIA, a major active constituent from the root of Salvia miltiorrhiza Bunge, across the blood-brain barrier. Xenobiotica 37, 635–678.10.1080/00498250701411258Search in Google Scholar PubMed
Chen, W., Sun, C., Wang, H., Huang, M., Zhu, G., Zhu, B., and Liu, F. (2010). Effect of tanshinone IIA pretreatment on IL-1β and RelA mRNA expression in rats with focal cerebral ischemia. J. South. Med. University 30, 2115–2118.Search in Google Scholar
Chen, L., Bi, X., Zhu, L., Qiu, Y., Ding, S., and Deng, B. (2011). Flavonoids of puerarin versus tanshinone II A for ischemic stroke: a randomized controlled trial. J. Chinese Integr. Med. 9, 1215–1220.10.3736/jcim20111109Search in Google Scholar PubMed
Chen, Y., Wu, X., Yu, S., Fauzee, N.J.S., Wu, J., Li, L., Zhao, J., and Zhao, Y. (2012a). Neuroprotective capabilities of tanshinone IIA against cerebral ischemia/reperfusion injury via anti-apoptotic pathway in rats. Biol. Pharm. Bull. 35, 164–170.10.1248/bpb.35.164Search in Google Scholar PubMed
Chen, Y., Wu, X., Yu, S., Lin, X., Wu, J., Li, L., Zhao, J., and Zhao, Y. (2012b). Neuroprotection of tanshinone IIA against cerebral ischemia/reperfusion injury through inhibition of macrophage migration inhibitory factor in rats. PLoS One 7, e40165.10.1371/journal.pone.0040165Search in Google Scholar PubMed PubMed Central
Chen, F., Zhang, J., He, Y., Fang, X., Wang, Y., and Chen, M. (2016). Glycyrrhetinic acid-decorated and reduction-sensitive micelles to enhance the bioavailability and anti-hepatocellular carcinoma efficacy of tanshinone IIA. Biomater. Sci. 4, 167–182.10.1039/C5BM00224ASearch in Google Scholar
Cheng, T.O. (2006). Danshen: a versatile Chinese herbal drug for the treatment of coronary heart disease. Int. J. Cardiol. 113, 437–438.10.1016/j.ijcard.2005.10.026Search in Google Scholar PubMed
Cheng, T.O. (2007). Cardiovascular effects of Danshen. Int. J. Cardiol. 121, 9–22.10.1016/j.ijcard.2007.01.004Search in Google Scholar PubMed
Curti, V., Capelli, E., Boschi, F., Nabavi, S.F., Bongiorno, A.I., Habtemariam, S., Nabavi, S.M., and Daglia, M. (2014). Modulation of human miR-17–3p expression by methyl 3-O-methyl gallate as explanation of its in vivo protective activities. Mol. Nutr. Food Res. 58, 1776–1784.10.1002/mnfr.201400007Search in Google Scholar PubMed
Dai, H., Li, X., Li, X., Bai, L., Li, Y., and Xue, M. (2012). Coexisted components of Salvia miltiorrhiza enhance intestinal absorption of cryptotanshinone via inhibition of the intestinal P-gp. Phytomedicine 19, 1256–1262.10.1016/j.phymed.2012.08.007Search in Google Scholar PubMed
Devi, K.P., Rajavel, T., Nabavi, S.F., Setzer, W.N., Ahmadi, A., Mansouri, K., and Nabavi, S.M. (2015). Hesperidin: a promising anticancer agent from nature. Ind. Crops Prod. 76, 582–589.10.1016/j.indcrop.2015.07.051Search in Google Scholar
Di Lorenzo, A., Nabavi, S.F., Sureda, A., Moghaddam, A.H., Khanjani, S., Arcidiaco, P., Nabavi, S.M., and Daglia, M. (2015). Antidepressive-like effects and antioxidant activity of green tea and GABA green tea in a mouse model of post-stroke depression. Mol. Nutr. food Res. 60, 566–579.10.1002/mnfr.201500567Search in Google Scholar PubMed
Doige, C.A. and Luzzi Ames, G. (1993). ATP-dependent transport systems in bacteria and humans: relevance to cystic fibrosis and multidrug resistance. Ann. Rev. Microbiol. 47, 291–319.10.1146/annurev.mi.47.100193.001451Search in Google Scholar PubMed
Dong, K., Xu, W., Yang, J., Qiao, H., and Wu, L. (2009). Neuroprotective effects of tanshinone IIA on permanent focal cerebral ischemia in mice. Phytother. Res. 23, 608–613.10.1002/ptr.2615Search in Google Scholar PubMed
Dong, Y., Morris-Natschke, S.L., and Lee, K.H. (2011). Biosynthesis, total syntheses, and antitumor activity of tanshinones and their analogs as potential therapeutic agents. Nat. Prod. Rep. 28, 529–542.10.1039/c0np00035cSearch in Google Scholar PubMed
Ghosh, N., Ghosh, R., Bhat, Z.A., Mandal, V., Bachar, S.C., Nima, N.D., Sunday, O.O., and Mandal, S.C. (2014). Advances in herbal medicine for treatment of ischemic brain injury. Nat. Prod. Commun. 9, 1045–1055.10.1177/1934578X1400900739Search in Google Scholar
González, M.A. (2014). Synthetic derivatives of aromatic abietane diterpenoids and their biological activities. Eur. J. Med. Chem. 87, 834–842.10.1016/j.ejmech.2014.10.023Search in Google Scholar PubMed
Han, J.Y., Fan, J.Y., Horie, Y., Miura, S., Cui, D.H., Ishii, H., Hibi, T., Tsuneki, H., and Kimura, I. (2008). Ameliorating effects of compounds derived from Salvia miltiorrhiza root extract on microcirculatory disturbance and target organ injury by ischemia and reperfusion. Pharmacol. Ther. 117, 280–295.10.1016/j.pharmthera.2007.09.008Search in Google Scholar PubMed
Hao, H., Wang, G., Cui, N., Li, J., Xie, L., and Ding, Z. (2006). Pharmacokinetics, absorption and tissue distribution of tanshinone IIA solid dispersion. Planta Med. 72, 1311–1317.10.1055/s-2006-951698Search in Google Scholar PubMed
Hao, X., Shi, M., Cui, L., Xu, C., Zhang, Y., and Kai, G. (2015). Effects of methyl jasmonate and salicylic acid on tanshinone production and biosynthetic gene expression in transgenic Salvia miltiorrhiza hairy roots. Biotechnol. Appl. Biochem. 62, 24–31.10.1002/bab.1236Search in Google Scholar PubMed
He, T., Zou, Q., Feng, Z., and Zhang, Z. (2009). Study of sodium tanshinone II A sulfonate tissue distribution in rat by liquid chromatography/tandem mass spectrometry. Arzneimittel-Forschung 60, 660–666.10.1055/s-0031-1296344Search in Google Scholar PubMed
He, C.E., Wei, J., Jin, Y., and Chen, S. (2010a). Bioactive components of the roots of Salvia miltiorrhizae: changes related to harvest time and germplasm line. Ind. Crops Prod. 32, 313–317.10.1016/j.indcrop.2010.05.009Search in Google Scholar
He, Z., Pan, Z., and Lu, W. (2010b). Neuroprotective effects of tanshinone II A on vascular dementia in rats. China J. Chinese Mater. Med. 35, 1883–1886.10.4268/cjcmm20101426Search in Google Scholar PubMed
Hei, M., Liu, F., and Luo, Y. (2010). Effect of tanshinone IIA on phosphorylated NMDA receptor 1 expression and intracellular free calcium concentration in neonatal SD rats with hypoxic ischemic brain damage. J. Cent. South Univ. Med. Sci. 35, 940–946.Search in Google Scholar
Hei, M., Luo, Y., Zhang, X., and Liu, F. (2011). Tanshinone IIa alleviates the biochemical changes associated with hypoxic ischemic brain damage in a rat model. Phytother. Res. 25, 1865–1869.10.1002/ptr.3500Search in Google Scholar PubMed
Hou, J.J., Wu, W.Y., Da, J., Yao, S., Long, H.L., Yang, Z., Cai, L.Y., Yang, M., Liu, X., Jiang, B.H., et al. (2011). Ruggedness and robustness of conversion factors in method of simultaneous determination of multi-components with single reference standard. J. Chromatogr. A. 1218, 5618–5627.10.1016/j.chroma.2011.06.058Search in Google Scholar PubMed
Hu, T., Wang, L., Zhang, L., Lu, L., Shen, J., Chan, R.L., Li, M., Wu, W.K., To, K.K., and Cho, C.H. (2015). Sensitivity of apoptosis-resistant colon cancer cells to tanshinones is mediated by autophagic cell death and p53-independent cytotoxicity. Phytomedicine 22, 536–544.10.1016/j.phymed.2015.03.010Search in Google Scholar PubMed
Huang, X., Li, Y., Li, J., Feng, Y., and Xu, X. (2014). Tanshinone IIA dampens the cell proliferation induced by ischemic insult in rat astrocytes via blocking the activation of HIF-1α/SDF-1 signaling. Life Sci. 112, 59–67.10.1016/j.lfs.2014.07.020Search in Google Scholar PubMed
Jiang, P., Li, C., Xiang, Z., and Jiao, B. (2014). Tanshinone IIA reduces the risk of Alzheimer’s disease by inhibiting iNOS, MMP-2 and NF-κBp65 transcription and translation in the temporal lobes of rat models of Alzheimer’s disease. Mol. Med. Rep. 10, 689–894.10.3892/mmr.2014.2254Search in Google Scholar PubMed
Jin, U.H., Suh, S.J., Chang, H.W., Son, J.K., Lee, S.H., Son, K.H., Chang, Y.C., and Kim, C.H. (2008). Tanshinone IIA from Salvia miltiorrhiza BUNGE inhibits human aortic smooth muscle cell migration and MMP-9 activity through AKT signaling pathway. J. Cell. Biochem. 104, 15–26.10.1002/jcb.21599Search in Google Scholar PubMed
Jing, X., Wei, X., Ren, M., Wang, L., Zhang, X., and Lou, H. (2016). Neuroprotective effects of tanshinone I against 6-OHDA-induced oxidative stress in cellular and mouse model of Parkinson’s disease through upregulating Nrf2. Neurochem. Res. 41, 779–786.10.1007/s11064-015-1751-6Search in Google Scholar PubMed
Kai, G., Xu, H., Zhou, C., Liao, P., Xiao, J., Luo, X., You, L., and Zhang, L. (2011). Metabolic engineering tanshinone biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. Metab. Eng. 13, 319–327.10.1016/j.ymben.2011.02.003Search in Google Scholar PubMed
Lam, B., Lo, A., Sun, X., Luo, H., Chung, S., and Sucher, N. (2003). Neuroprotective effects of tanshinones in transient focal cerebral ischemia in mice. Phytomedicine 10, 286–291.10.1078/094471103322004776Search in Google Scholar PubMed
Laule, O., Fürholz, A., Chang, H.S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., and Lange, M. (2003). Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 100, 6866–6871.10.1073/pnas.1031755100Search in Google Scholar PubMed PubMed Central
Lee, J.C., Park, J.H., Park, O.K., Kim, I.H., Yan, B.C., Ahn, J.H., Kwon, S.H., Choi, J.H., Kim, J.D., and Won, M.H. (2013). Neuroprotective effects of tanshinone I from Danshen extract in a mouse model of hypoxia-ischemia. Anat. Cell Biol. 46, 183–190.10.5115/acb.2013.46.3.183Search in Google Scholar PubMed PubMed Central
Li, L.X., Dai, J.P., Ru, L.Q., Yin, G.F., and Zhao, B. (2004). Effects of tanshinone on neuropathological changes induced by amyloid b-peptide injection in rat hippocampus. Acta Pharmacol Sin. 25, 861–868.Search in Google Scholar
Li, H., Zhang, Z., Ma, L., and Chen, X. (2007). Preparation of tanshinone microemulsion and its absorption in rat intestine in situ. China J. Chinese Mater. Med. 32, 1024–1027.Search in Google Scholar
Li, M.H., Chen, J.M., Peng, Y., Wu, Q., and Xiao, P.G. (2008) Investigation of Danshen and related medicinal plants in China. J. Ethnopharmacol. 120, 419–426.10.1016/j.jep.2008.09.013Search in Google Scholar PubMed
Li, M.H., Peng, Y, and Xiao P.G. (2010). Distribution of tanshinones in the genus Salvia (family Lamiaceae) from China and its systematic significance. J. Systematics Evol. 48, 118–122.10.1111/j.1759-6831.2010.00070.xSearch in Google Scholar
Li, J., Wen, P.Y., Li, W.W., and Zhou, J. (2015a). Upregulation effects of tanshinone IIA on the expressions of NeuN, Nissl body, and IκB and downregulation effects on the expressions of GFAP and NF-κB in the brain tissues of rat models of Alzheimer’s disease. NeuroReport 26, 758–766.10.1097/WNR.0000000000000419Search in Google Scholar PubMed
Li, Y.H., Wang, F.Y., Feng, C.Q., and Yang, X.F. (2015b). Studies on the active constituents in radix Salviae miltiorrhizae and their protective effects on cerebral ischemia reperfusion injury and its mechanism. Pharmacogn. Mag. 11, 69.10.4103/0973-1296.149706Search in Google Scholar PubMed PubMed Central
Lin, W., Deng, J., Lu, M., Ou, X., Lin, N., Yang, G., and Liang, H. (2008). The research in production of Danshen in three main cultivations in China. J Chin Med Mater. 31, 338–340.Search in Google Scholar
Lin, T.Y., Lu, C.W., Huang, S.K., and Wang, S.J. (2013). Tanshinone IIA, a constituent of Danshen, inhibits the release of glutamate in rat cerebrocortical nerve terminals. J. Ethnopharmacol. 147, 488–496.10.1016/j.jep.2013.03.045Search in Google Scholar PubMed
Liu, J., Zhu, J., Du, Z., and Qin, B. (2005). Preparation and pharmacokinetic evaluation of tashinone IIA solid lipid nanoparticles. Drug Dev. Ind. Pharm. 31, 551–556.10.1080/03639040500214761Search in Google Scholar PubMed
Liu, T., Jin, H., Sun, Q.R., Xu, J.H., and Hu, H.T. (2010). The neuroprotective effects of tanshinone IIA on β-amyloid-induced toxicity in rat cortical neurons. Neuropharmacology 59, 595–604.10.1016/j.neuropharm.2010.08.013Search in Google Scholar PubMed
Liu, P., Li J, Liu J, Yang, J, and Fan, Y. (2012). Release behavior of tanshinone IIA sustained-release pellets based on crack formation theory. J. Pharm. Sci. 101, 2811–2820.10.1002/jps.23199Search in Google Scholar PubMed
Liu, X., An, C., Jin, P., Liu, X., and Wang, L. (2013). Protective effects of cationic bovine serum albumin-conjugated PEGylated tanshinone IIA nanoparticles on cerebral ischemia. Biomaterials 34, 817–830.10.1016/j.biomaterials.2012.10.017Search in Google Scholar PubMed
Liu, S., Yang, Z., and Sun X. (2014). Simultaneous determination of six Salvia miltiorrhiza gradients in rat plasma and brain by LC-MS/MS. China J. Chinese Mater. Med. 39, 1704–1708.Search in Google Scholar
Lu, D.Y., Leung, Y.M., Huang, S.M., and Wong, K.L. (2010). Bradykinin-induced cell migration and COX-2 production mediated by the bradykinin B1 receptor in glioma cells. J. Cell. Biochem. 110, 141–150.10.1002/jcb.22520Search in Google Scholar PubMed
Ming, Q., Han, T., Li, W., Zhang, Q., Zhang, H., Zheng, C., Huang, F., Rahman, K., and Qin, L. (2012). Tanshinone IIA and tanshinone I production by Trichoderma atroviride D16, an endophytic fungus in Salvia miltiorrhiza. Phytomedicine 19, 330–333.10.1016/j.phymed.2011.09.076Search in Google Scholar PubMed
Nabavi, S.F., Nabavi, S.M., Mirzaei, M., and Moghaddam, A.H. (2012a). Protective effect of quercetin against sodium fluoride induced oxidative stress in rat’s heart. Food Funct. 3, 437–441.10.1039/c2fo10264aSearch in Google Scholar PubMed
Nabavi, S.F., Nabavi, S.M., Moghaddam, A.H., Naqinezhad, A., Bigdellou, R., and Mohammadzadeh, S. (2012b). Protective effects of Allium paradoxum against gentamicin-induced nephrotoxicity in mice. Food Funct. 3, 28–29.10.1039/C1FO10173KSearch in Google Scholar
Nabavi, S.M., Nabavi, S.F., Eslami, S., and Moghaddam, A.H. (2012c). In vivo protective effects of quercetin against sodium fluoride-induced oxidative stress in the hepatic tissue. Food Chem. 132, 931–935.10.1016/j.foodchem.2011.11.070Search in Google Scholar
Nabavi, S.F., Nabavi, S.M., Ebrahimzadeh, M.A., Eslami, B., and Jafari, N. (2013a). In vitro antioxidant and antihemolytic activities of hydroalcoholic extracts of Allium scabriscapum Boiss. & Ky. aerial parts and bulbs. Int. J. Food Prop. 16, 713–722.10.1080/10942912.2011.565902Search in Google Scholar
Nabavi, S.F., Nabavi, S.M., Ebrahimzadeh, M.A., Jafari, N., and Yazdanpanah, S. (2013b). Biological activities of freshwater algae, Spirogyra singularis Nordstedt. J. Aquat. Food Prod. Technol. 22, 58–65.10.1080/10498850.2011.624292Search in Google Scholar
Nabavi, S.F., Nabavi, S.M., Setzer, W.N., Nabavi, S.A., Nabavi, S.A., and Ebrahimzadeh, M.A. (2013c). Antioxidant and antihemolytic activity of lipid-soluble bioactive substances in avocado fruits. Fruits 68, 185–193.10.1051/fruits/2013066Search in Google Scholar
Nabavi, S.F., Daglia, M., Moghaddam, A.H., Habtemariam, S., and Nabavi, S.M. (2014). Curcumin and liver disease: from chemistry to medicine. Compr. Rev. Food Sci. Food Safe. 13, 62–77.10.1111/1541-4337.12047Search in Google Scholar
Nabavi, S.F., Russo, G.L., Daglia, M., and Nabavi, S.M. (2015a). Role of quercetin as an alternative for obesity treatment: you are what you eat! Food Chem. 179, 305–310.10.1016/j.foodchem.2015.02.006Search in Google Scholar
Nabavi, S.M., Marchese, A., Izadi, M., Curti, V., Daglia, M., and Nabavi, S.F. (2015b) Plants belonging to the genus Thymus as antibacterial agents: from farm to pharmacy. Food Chem. 173, 339–347.10.1016/j.foodchem.2014.10.042Search in Google Scholar
Nakao, M. and Fukushima, T. (1934). On the chemical composition of Salvia miltiorrhiza (Chinese drug Tan-shen). J. Pharmac. Soc. Japan 54, 154–162.10.1248/yakushi1881.54.9_844Search in Google Scholar
Ng, T., Liu, F., and Wang, Z. (2000). Antioxidative activity of natural products from plants. Life Sci. 66, 709–723.10.1016/S0024-3205(99)00642-6Search in Google Scholar
Orhan, I., Daglia, M., Nabavi, S.F., Loizzo, M., Sobarzo-Sanchez, E., and Nabavi, S.M. (2015). Flavonoids and dementia: an update. Curr. Med. Chem. 22, 1004–1015.10.2174/0929867322666141212122352Search in Google Scholar
Pan, X., Niu, G., and Liu, H. (2001). Microwave-assisted extraction of tanshinones from Salvia miltiorrhiza bunge with analysis by high-performance liquid chromatography. J. Chromatogr. A 922, 371–375.10.1016/S0021-9673(01)00949-9Search in Google Scholar
Park, O.K., Choi, J.H., Park, J.H., Kim, I.H., Yan, B.C., Ahn, J.H., Kwon, S.H., Lee, J.C., Kim, Y.S., Kim, M., et al. (2012). Comparison of neuroprotective effects of five major lipophilic diterpenoids from Danshen extract against experimentally induced transient cerebral ischemic damage. Fitoterapia 83, 1666–1674.10.1016/j.fitote.2012.09.020Search in Google Scholar PubMed
Park, J.H., Park, O.K., Cho, J.H., Chen, B.H., Kim, I.H., Ahn, J.H., Lee, J.C., Yan, B.C., Yoo, K.Y., Lee, C.H., et al. (2014a). Anti-inflammatory effect of tanshinone I in neuroprotection against cerebral ischemia-reperfusion injury in the gerbil hippocampus. Neurochem. Res. 39, 1300–1312.10.1007/s11064-014-1312-4Search in Google Scholar PubMed
Park, J.H., Park, O.K., Yan, B., Ahn, J.H., Kim, I.H., Lee, J.C., Kwon, S.H., Yoo, K.Y., Lee, C.H., Hwang, I.K., et al. (2014b). Neuroprotection via maintenance or increase of antioxidants and neurotrophic factors in ischemic gerbil hippocampus treated with tanshinone I. Chinese Med. J. 127, 3396–3405.Search in Google Scholar
Prince, M., Bryce, R., Albanese, E., Wimo, A., Ribeiro, W., and Ferri, C.P. (2013). The global prevalence of dementia: a systematic review and metaanalysis. Alzheimer’s Dement. 9, 63–75.e62.10.1016/j.jalz.2012.11.007Search in Google Scholar PubMed
Qian, Y.H., Xiao, Q., and Xu, J. (2012). The protective effects of tanshinone IIA on β-amyloid protein (1–42)-induced cytotoxicity via activation of the Bcl-xL pathway in neuron. Brain Res. Bull. 88, 354–358.10.1016/j.brainresbull.2012.03.007Search in Google Scholar PubMed
Ren, Y., Houghton, P.J., Hider, R.C., and Howes, M. (2004). Novel diterpenoid acetylcholinesterase inhibitors from Salvia miltiorrhiza. Planta Med. 70, 201–204.10.1055/s-2004-815535Search in Google Scholar PubMed
Ren, B., Zhang, Y.X., Zhou, H.X., Sun, F.W., Zhang, Z.F., Wei, Z.F., Zhang, C.Y., and Si, D.W. (2015). Tanshinone IIA prevents the loss of nigrostriatal dopaminergic neurons by inhibiting NADPH oxidase and iNOS in the MPTP model of Parkinson’s disease. J. Neurol. Sci. 348, 142–152.10.1016/j.jns.2014.11.026Search in Google Scholar PubMed
Rhiu, S., Chae, M.K., Lee, E.J., Lee, J.B., and Yoon, J.S. (2014). Effect of tanshinone IIA in an in vitro model of Graves’ orbitopathy. Invest. Ophthalmol. Vis. Sci. 55, 5900–5910.10.1167/iovs.14-14008Search in Google Scholar PubMed
Russo, M., Russo, G.L., Daglia, M., Kasi, P.D., Ravi, S., Nabavi, S.F., and Nabavi, S.M. (2016). Understanding genistein in cancer: the ‘good’ and the ‘bad’ effects: a review. Food Chem. 196, 589–600.10.1016/j.foodchem.2015.09.085Search in Google Scholar PubMed
Shang, Y.H., Jin-Feng, T., Min, H., and Xiao-Yu, X. (2013). Progress on the protective effect of compounds from natural medicines on cerebral ischemia. Chinese J. Nat. Med. 11, 588–595.10.3724/SP.J.1009.2013.00588Search in Google Scholar
Shi, L.L., Yang, W.N., Chen, X.L., Zhang, J.S., Yang, P.B., Hu, X.D., Han, H., Qian, Y.H., and Liu, Y. (2012). The protective effects of tanshinone IIA on neurotoxicity induced by β-amyloid protein through calpain and the p35/Cdk5 pathway in primary cortical neurons. Neurochem. Int. 61, 227–235.10.1016/j.neuint.2012.04.019Search in Google Scholar PubMed
Slusarczyk, S., Topolski, J., Domaradzki, K., Adams, M., Hamburger, M., and Matkowski, A. (2015). Isolation and fast selective determination of nor-abietanoid diterpenoids from Perovskia atriplicifolia roots using LC-ESI-MS/MS with multiple reaction monitoring. Nat. Prod. Commun. 10, 1149–1152.10.1177/1934578X1501000703Search in Google Scholar
Song, J., Qi, J., Ren, C., Fu, J., and Zhang, Y. (2000). Dynamics of growth and total tanshinones accumulation in crown gall cultures of Salvia miltiorrhiza. Acta Pharm. Sin. 35, 929–931.Search in Google Scholar
Sun, S., Yin, Y., Yin, X., Cao, F., Luo, D., Zhang, T., Li, Y., and Ni, L. (2012). Anti-nociceptive effects of tanshinone IIA (TIIA) in a rat model of complete Freund’s adjuvant (CFA)-induced inflammatory pain. Brain Res. Bull. 88, 581–588.10.1016/j.brainresbull.2012.06.002Search in Google Scholar PubMed
Tan, X., Li, J., Wang, X., Chen, N., Cai, B., Wang, G., Shan, H., Dong, D., Liu, Y., Li, X., et al. (2011). Tanshinone IIA protects against cardiac hypertrophy via inhibiting calcineurin/NFATc3 pathway. Int. J. Biol. Sci. 7, 383–389.10.7150/ijbs.7.383Search in Google Scholar PubMed PubMed Central
Tang, C., Xue, H.L., Huang, H.B., and Wang, X.G. (2010a). Tanshinone IIA inhibits constitutive STAT3 activation, suppresses proliferation, and induces apoptosis in rat C6 glioma cells. Neurosci. Lett. 470, 126–129.10.1016/j.neulet.2009.12.069Search in Google Scholar PubMed
Tang, C., Xue, H., Bai, C., Fu, R., and Wu, A. (2010b). The effects of tanshinone IIA on blood-brain barrier and brain edema after transient middle cerebral artery occlusion in rats. Phytomedicine 17, 1145–1149.10.1016/j.phymed.2010.03.017Search in Google Scholar PubMed
Tang, C., Xue, H.L., Bai, C.L., and Fu, R. (2011). Regulation of adhesion molecules expression in TNF-α-stimulated brain microvascular endothelial cells by tanshinone IIA: involvement of NF-κB and ROS generation. Phytother. Res 25, 376–380.10.1002/ptr.3278Search in Google Scholar PubMed
Tang, Q., Han, R., Xiao, H., Shen, J., Luo, Q., and Li, J. (2012). Neuroprotective effects of tanshinone IIA and/or tetramethylpyrazine in cerebral ischemic injury in vivo and in vitro. Brain Res. 1488, 81–91.10.1016/j.brainres.2012.09.034Search in Google Scholar PubMed
Tang, J., Zhu, C., Li, Z.H., Liu, X.Y., Sun, S.K., Zhang, T., Luo, Z.J., Zhang, H., and Li, W.Y. (2015). Inhibition of the spinal astrocytic JNK/MCP-1 pathway activation correlates with the analgesic effects of tanshinone IIA sulfonate in neuropathic pain. J. Neuroinflamm. 12, 57.10.1186/s12974-015-0279-7Search in Google Scholar PubMed PubMed Central
Tian, X.H. and Wu, J.H. (2013). Tanshinone derivatives: a patent review (January 2006-September 2012). Exp. Opin. Ther. Patents 23, 19–29.10.1517/13543776.2013.736494Search in Google Scholar PubMed
Wang, J.W. and Wu, J.Y. (2010). Tanshinone biosynthesis in Salvia miltiorrhiza and production in plant tissue cultures. Appl. Microbiol. Biotechnol. 88, 437–449.10.1007/s00253-010-2797-7Search in Google Scholar PubMed
Wang, Y.C. and Wang, Y.R. (2011). Levels of phenolic acids and tanshinones in Salvia miltiorrhiza Bge. cv. sativa and Salvia bowleyanae Dunn roots during growth. J. Biol. Active Prod. Nat. 1, 7–18.10.1080/22311866.2011.10719068Search in Google Scholar
Wang, A.M., Sha, S.H., Lesniak, W., and Schacht, J. (2003). Tanshinone (Salviae miltiorrhizae extract) preparations attenuate aminoglycoside-induced free radical formation in vitro and ototoxicity in vivo. Antimicrob. Agents Chemother. 47, 1836–1841.10.1128/AAC.47.6.1836-1841.2003Search in Google Scholar PubMed PubMed Central
Wang, J., Wang, X., Jiang, S., Yuan, S., Lin, P., Zhang, J., Lu, Y., Wang, Q., Xiong, Z., Wu, Y., et al. (2007a). Growth inhibition and induction of apoptosis and differentiation of tanshinone IIA in human glioma cells. J. Neuro-oncol. 82, 11–21.10.1007/s11060-006-9242-xSearch in Google Scholar PubMed
Wang, L., Jiang, X., Xu, W., and Li, C. (2007b). Complexation of tanshinone IIA with 2-hydroxypropyl-β-cyclodextrin: effect on aqueous solubility, dissolution rate, and intestinal absorption behavior in rats. Int. J. Pharm. 341, 58–67.10.1016/j.ijpharm.2007.03.046Search in Google Scholar PubMed
Wang, X., Morris-Natschke, S.L., and Lee, K.H. (2007c). New developments in the chemistry and biology of the bioactive constituents of tanshen. Med. Res. Rev. 27, 133–148.10.1002/med.20077Search in Google Scholar PubMed
Wang, L., Zhang, X., Liu, L., Cui, L., Yang, R., Li, M., and Du, W. (2010). Tanshinone II A down-regulates HMGB1, RAGE, TLR4, NF-κB expression, ameliorates BBB permeability and endothelial cell function, and protects rat brains against focal ischemia. Brain Res. 1321, 143–151.10.1016/j.brainres.2009.12.046Search in Google Scholar PubMed
Wang, W., Zheng, L.L., Wang, F., Hu, Z.L., Wu, W.N., Gu, J., and Chen, J.G. (2011). Tanshinone IIA attenuates neuronal damage and the impairment of long-term potentiation induced by hydrogen peroxide. J. Ethnopharmacol. 134, 147–155.10.1016/j.jep.2010.11.069Search in Google Scholar PubMed
Wang, J.G., Bondy, S.C., Zhou, L., Yang, F.Z., Ding, Z.G., Hu, Y., Tian, Y., Wen, P.Y., Luo, H., Wang, F., et al. (2014). Protective effect of tanshinone IIA against infarct size and increased HMGB1, NF-κB, GFAP and apoptosis consequent to transient middle cerebral artery occlusion. Neurochem. Res. 39, 295–304.10.1007/s11064-013-1221-ySearch in Google Scholar PubMed
Wang, D., Zhang, W., Wang, T., Li, N., Mu, H., Zhang, J., and Duan, J. (2015a). Unveiling the mode of action of two antibacterial tanshinone derivatives. Int. J. Mol. Sci. 16, 17668–17681.10.3390/ijms160817668Search in Google Scholar PubMed PubMed Central
Wang, S., Jing, H., Yang, H., Liu, Z., Guo, H., Chai, L., and Hu, L. (2015b). Tanshinone I selectively suppresses pro-inflammatory genes expression in activated microglia and prevents nigrostriatal dopaminergic neurodegeneration in a mouse model of Parkinson’s disease. J. Ethnopharmacol. 164, 247–255.10.1016/j.jep.2015.01.042Search in Google Scholar PubMed
Wen, P., Yang, F., Wang, F., Li, W., Zhou, L., Huang, L., and Zhou, J. (2012). Study on regulation of tanshinone II (A) on GFAP and ATPase and PDI of cerebral ischemia reperfusion injury in rats. J. Chinese Med. Mater. 35, 1628–1632.Search in Google Scholar
Wen, P., Luo, H., Zhou, L., Song, Z., Li, W., and Zhou, J. (2014). Effects of tanshinone IIA on the expressions of caspase-3, Akt and NF-κB in the brains of rat models of Alzheimer’s disease. Chinese J. Cell. Mol. Immunol. 30, 155–159.Search in Google Scholar
Wen, P.Y., Li, J., Lu, B.L., Liu, J., Yang, F.Z., Zhou, L., Luo, H., Li, W.W., and Zhou, J. (2016). Tanshinone IIA increases levels of NeuN, protein disulfide isomerase, and Na+/K+-ATPase and decreases evidence of microglial activation after cerebral ischemic injury. NeuroReport 27, 435–444.10.1097/WNR.0000000000000559Search in Google Scholar PubMed
Wu, C.T., Mulabagal, V., Nalawade, S.M., Chen, C.L., Yang, T.F., and Tsay, H.S. (2003). Isolation and quantitative analysis of cryptotanshinone, an active quinoid diterpene formed in callus of Salvia miltiorrhiza BUNGE. Biol. Pharm. Bull. 26, 845–848.10.1248/bpb.26.845Search in Google Scholar PubMed
Xia, W.J., Yang, M., Fok, T.F., Li, K., Chan, W.Y., Ng, P.C., Ng, H.K., Chik, K.W., Wang, C.C., Gu, G.J., et al. (2005). Partial neuroprotective effect of pretreatment with tanshinone IIA on neonatal hypoxia-ischemia brain damage. Pediatr. Res. 58, 784–790.10.1203/01.PDR.0000180550.99162.BCSearch in Google Scholar PubMed
Xiaoa, Y., Qing, W.X., Lan, M.S., and Ying, C.B. (2006). Sodium tanshinone IIA sulfonate derived from Slavia miltiorrhiza Bunge up-regulate the expression of prolactin releasing peptide (PrRP) in the medulla oblongata in ovariectomized rats. Biochem. Pharmacol. 72, 582–587.10.1016/j.bcp.2006.05.014Search in Google Scholar PubMed
Yan, H.X., Li, J., Li, Z.H., Zhang, W.L., and Liu, J.P. (2015a). Tanshinone IIA-loaded pellets developed for angina chronotherapy: deconvolution-based formulation design and optimization, pharmacokinetic and pharmacodynamic evaluation. Eur. J. Pharm. Sci. 76, 156–164.10.1016/j.ejps.2015.05.012Search in Google Scholar PubMed
Yan, H.M., Sun, E., Cui, L., Jia, X.B., and Jin, X. (2015b). Improvement in oral bioavailability and dissolution of tanshinone IIA by preparation of solid dispersions with porous silica. J. Pharm. Pharmacol. 67, 1207–1214.10.1111/jphp.12423Search in Google Scholar PubMed
Yang, L., Zhang, B., Yin, L., Cai, B., Shan, H., Zhang, L., Lu, Y., and Bi, Z. (2011). Tanshinone IIA prevented brain iron dyshomeostasis in cerebral ischemic rats. Cell. Physiol. Biochem. 27, 23–30.10.1159/000325202Search in Google Scholar PubMed
Yang, L., Guo, H., Dong, L., Wang, L., Liu, C., and Wang, X. (2014). Tanshinone IIA inhibits the growth, attenuates the stemness and induces the apoptosis of human glioma stem cells. Oncol. Rep. 32, 1303–1311.10.3892/or.2014.3293Search in Google Scholar PubMed
Yang, X., Yan, J., and Feng, J. (2016). Treatment with tanshinone IIA suppresses disruption of the blood-brain barrier and reduces expression of adhesion molecules and chemokines in experimental autoimmune encephalomyelitis. Eur. J. Pharmacol. 771, 18–28.10.1016/j.ejphar.2015.12.014Search in Google Scholar PubMed
Yin, Y., Huang, L., Liu, Y., Huang, S., Zhuang, J., Zhuang, X., Chen, X., Zhang, L., Wu, H., Shao, F., et al. (2008). Effect of tanshinone on the levels of nitric oxide synthase and acetylcholinesterase in the brain of Alzheimer’s disease rat model. Clin. Invest. Med. 31, 248–257.10.25011/cim.v31i5.4871Search in Google Scholar PubMed
Yu, X.Y., Lin, S.G., Zhou, Z.W., Chen, X., Liang, J., Duan, W., Yu, X.Q., Wen, J.Y., Chowbay, B., Li, C.G., et al. (2007). Role of P-glycoprotein in the intestinal absorption of tanshinone IIA, a major active ingredient in the root of Salvia miltiorrhiza Bunge. Curr. Drug Metab. 8, 325–340.10.2174/138920007780655450Search in Google Scholar PubMed
Yuan, J., Tao, L., and Xu, J. (1989). Immobilization of callus tissue cells of Salvia miltiorrhiza and the characteristics of their products. Chinese J. Biotechnol. 6, 199–205.Search in Google Scholar
Zhang, J., Huang, M., Guan, S., Bi, H.C., Pan, Y., Duan, W., Chan, S.Y., Chen, X., Hong, Y.H., Bian, J.S., et al. (2006). A mechanistic study of the intestinal absorption of cryptotanshinone, the major active constituent of Salvia miltiorrhiza. J. Pharmacol. Exp. Ther. 317, 1285–1294.10.1124/jpet.105.100701Search in Google Scholar PubMed
Zhang, F., Zheng, W., Pi, R., Mei, Z., Bao, Y., Gao, J., Tang, W., Chen, S., and Liu, P. (2009). Cryptotanshinone protects primary rat cortical neurons from glutamate-induced neurotoxicity via the activation of the phosphatidylinositol 3-kinase/Akt signaling pathway. Exp. Brain Res. 193, 109–118.10.1007/s00221-008-1600-9Search in Google Scholar PubMed
Zhang, W.J., Feng, J., Zhou, R., Ye, L.Y., Liu, H.L., Peng, L., Lou, J.N., and Li, C.H. (2010). Tanshinone IIA protects the human blood-brain barrier model from leukocyte-associated hypoxia-reoxygenation injury. Eur. J. Pharmacol. 648, 146–152.10.1016/j.ejphar.2010.08.040Search in Google Scholar PubMed
Zhang, L., Gan, W., and An, G. (2012). Influence of tanshinone IIa on heat shock protein 70, Bcl-2 and Bax expression in rats with spinal ischemia/reperfusion injury. Neural Regen. Res. 7, 2882.Search in Google Scholar
Zhang, X., Chen, G., Wen, L., Yang, F., Shao, A.L., Li, X., Long, W., and Mu, L. (2013). Novel multiple agents loaded PLGA nanoparticles for brain delivery via inner ear administration: in vitro and in vivo evaluation. Eur. J. Pharm. Sci. 48, 595–603.10.1016/j.ejps.2013.01.007Search in Google Scholar PubMed
Zhang, J., Li, Y., Fang, X., Zhou, D., Wang, Y., and Chen, M. (2014). TPGS-g-PLGA/Pluronic F68 mixed micelles for tanshinone IIA delivery in cancer therapy. Int. J. Pharm. 476, 185–198.10.1016/j.ijpharm.2014.09.017Search in Google Scholar PubMed
Zhao, J.L., Zhou, L.G., and Wu, J.Y. (2010). Effects of biotic and abiotic elicitors on cell growth and tanshinone accumulation in Salvia miltiorrhiza cell cultures. Appl. Microbiol. Biotechnol. 87, 137–144.10.1007/s00253-010-2443-4Search in Google Scholar PubMed
Zhao, Y., Xu, P., Hu, S., Du, L., Xu, Z., Zhang, H., Cui, W., Mak, S., Xu, D., Shen, J., et al. (2015). Tanshinone II A, a multiple target neuroprotectant, promotes caveolae-dependent neuronal differentiation. Eur J Pharmacol. 765, 437–446.10.1016/j.ejphar.2015.09.006Search in Google Scholar PubMed
ZhenQiao, S., JianHua, W., HongGang, W., FuJuan, Z., and LiWu, H. (2009). Studies of the floral biology, breeding characters of Salvia miltiorrhiza. Acta Hort. Sin. 36, 905–910.Search in Google Scholar
Zhou, W. and Ruigrok, T. (1990). Protective effect of danshen during myocardial ischemia and reperfusion: an isolated rat heart study. Am. J. Chinese Med. 18, 19–24.10.1142/S0192415X90000046Search in Google Scholar PubMed
Zhou, L., Zuo, Z., and Chow, M.S.S. (2005). Danshen: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J. Clin. Pharmacol. 45, 1345–1359.10.1177/0091270005282630Search in Google Scholar PubMed
Zhou, Z.W., Chen, X., Liang, J., Yu, X.Y., Wen, J.Y., and Zhou, S.F. (2007). Involvement of P-glycoprotein and multidrug resistance associated protein 1 in the transport of tanshinone IIB, a primary active diterpenoid quinone from the roots of Salvia miltiorrhiza, across the blood-brain barrier. Drug Metab. Lett. 1, 205–217.10.2174/187231207781369807Search in Google Scholar PubMed
Zhou, L., Zhou, J., and Liu, Y. (2013). Effect of tanshinone II A on the expressions of NeuN, GFAP and CD11b in Aβ1-42; induced newborn rat hippocampal slices in vitro. Chinese J. Cell. Mol. Immunol. 29, 1150–1154.Search in Google Scholar
Zhou, L., Bondy, S., Jian, L., Wen, P., Yang, F., Luo, H., Li, W., and Zhou, J. (2015a). Tanshinone IIA attenuates the cerebral ischemic injury-induced increase in levels of GFAP and of caspases-3 and-8. Neuroscience 288, 105–111.10.1016/j.neuroscience.2014.12.028Search in Google Scholar PubMed
Zhou, W.J., Gui, Q.F., Wu, Y., and Yang, Y.M. (2015b). Tanshinone IIA protects against methylglyoxal-induced injury in human brain microvascular endothelial cells. Int. J. Clin. Exp. Med. 8, 1985–1992.Search in Google Scholar
Zhu, S., Qian, Y., Shi, L., Yang, W., Feng, X., Li, C., and Liu, Y. (2010). Effect of tanshinone IIA on the change of calcium current induced by β-amyloid protein 25-35 in neurons of nucleus basalis of Meynert. J. Central South Univ. Med. Sci. 35, 840–846.Search in Google Scholar
©2016 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- The cholinergic system in the cerebellum: from structure to function
- Tanshinones and mental diseases: from chemistry to medicine
- Brain-derived neurotrophic factor: a mediator of inflammation-associated neurogenesis in Alzheimer’s disease
- SIRT1 as a therapeutic target for Alzheimer’s disease
- A systematic review of the neurobiological underpinnings of borderline personality disorder (BPD) in childhood and adolescence
- Neuroprotective properties of mitochondria-targeted antioxidants of the SkQ-type
- Imaging and machine learning techniques for diagnosis of Alzheimer’s disease
- Resting state functional magnetic resonance imaging processing techniques in stroke studies
Articles in the same Issue
- Frontmatter
- The cholinergic system in the cerebellum: from structure to function
- Tanshinones and mental diseases: from chemistry to medicine
- Brain-derived neurotrophic factor: a mediator of inflammation-associated neurogenesis in Alzheimer’s disease
- SIRT1 as a therapeutic target for Alzheimer’s disease
- A systematic review of the neurobiological underpinnings of borderline personality disorder (BPD) in childhood and adolescence
- Neuroprotective properties of mitochondria-targeted antioxidants of the SkQ-type
- Imaging and machine learning techniques for diagnosis of Alzheimer’s disease
- Resting state functional magnetic resonance imaging processing techniques in stroke studies