Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 4517486, 13 pages
https://doi.org/10.1155/2017/4517486
Research Article

Tanshinone IIA Inhibits Glutamate-Induced Oxidative Toxicity through Prevention of Mitochondrial Dysfunction and Suppression of MAPK Activation in SH-SY5Y Human Neuroblastoma Cells

1Center for Bioresources & Drug Discovery and School of Biosciences & Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou 510006, China
2School of Pharmaceutical Sciences, Wuhan University, Wuhan 430071, China
3Hunan Auragene Biotech Co., Ltd., Changsha 410013, China
4Guangdong Province Key Laboratory for Biotechnology Drug Candidates, Guangdong Pharmaceutical University, Guangzhou 510006, China

Correspondence should be addressed to Zebo Huang

Received 28 January 2017; Revised 17 April 2017; Accepted 2 May 2017; Published 11 June 2017

Academic Editor: Giuseppe Filomeni

Copyright © 2017 Haifeng Li 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. K. Gammon, “Neurodegenerative disease: brain windfall,” Nature, vol. 515, no. 7526, pp. 299-300, 2014. View at Publisher · View at Google Scholar
  2. R. L. Chen, J. S. Balami, M. M. Esiri, L. K. Chen, and A. M. Buchan, “Ischemic stroke in the elderly: an overview of evidence,” Nature Reviews Neurology, vol. 6, no. 5, pp. 256–265, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. A. J. Shah, F. Crespi, and C. Heidbreder, “Amino acid neurotransmitters: separation approaches and diagnostic value,” Journal of Chromatography B, vol. 781, no. 1-2, pp. 151–163, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Advokat and A. I. Pellegrin, “Excitatory amino acids and memory: evidence from research on Alzheimer’s disease and behavioral pharmacology,” Neuroscience & Biobehavioral Reviews, vol. 16, no. 1, pp. 13–24, 1992. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Mehta, M. Prabhakar, P. Kumar, R. Deshmukh, and P. L. Sharma, “Excitotoxicity: bridge to various triggers in neurodegenerative disorders,” European Journal of Pharmacology, vol. 698, no. 1–3, pp. 6–18, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. H. A. S. Ezza and Y. A. Khadrawyb, “Glutamate excitotoxicity and neurodegeneration,” Journal of Molecular and Genetic Medicine, vol. 8, no. 141, p. 1747-0862, 2014. View at Publisher · View at Google Scholar
  7. R. S. Sundaram, L. Gowtham, and B. S. Nayak, “The role of excitatory neurotransmitter glutamate in brain physiology and pathology,” Asian Journal of Pharmaceutical and Clinical Research, vol. 5, no. 2, pp. 1–7, 2012. View at Google Scholar
  8. X. X. Dong, Y. Wang, and Z. H. Qin, “Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases,” Acta Pharmacologica Sinica, vol. 30, no. 4, pp. 379–387, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. A. F. Schinder, E. C. Olson, N. C. Spitzer, and M. Montal, “Mitochondrial dysfunction is a primary event in glutamate neurotoxicity,” Journal of Neuroscience, vol. 16, no. 19, pp. 6125–6133, 1996. View at Google Scholar
  10. J. Li, W. Li, Z. G. Jiang, and H. A. Ghanbari, “Oxidative stress and neurodegenerative disorders,” International Journal of Molecular Sciences, vol. 14, no. 12, pp. 24438–24475, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature, vol. 443, no. 7113, pp. 787–795, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. S. S. Willard and S. Koochekpour, “Glutamate, glutamate receptors, and downstream signaling pathways,” International Journal of Biological Sciences, vol. 9, no. 9, pp. 948–959, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Izumi, N. Yamamoto, T. Matsuo et al., “Vulnerability to glutamate toxicity of dopaminergic neurons is dependent on endogenous dopamine and MAPK activation,” Journal of Neurochemistry, vol. 110, no. 2, pp. 745–755, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. C. Rivera-Cervantes, R. Castañeda-Arellano, R. D. Castro-Torres, G. Gudiño-Cabrera, A. Camins, and C. Beas-Zárate, “P38 MAPK inhibition protects against glutamate neurotoxicity and modifies NMDA and AMPA receptor subunit expression,” Journal of Molecular Neuroscience, vol. 55, no. 3, pp. 596–608, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Y. Su, Q. L. Ming, K. Rahman, T. Han, and L. P. Qin, “Salvia miltiorrhiza: traditional medicinal uses, chemistry, and pharmacology,” Chinese Journal of Natural Medicines, vol. 13, no. 3, pp. 163–182, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Gao, Z. Liu, H. Li, P. J. Little, P. Liu, and S. Xu, “Cardiovascular actions and therapeutic potential of tanshinone IIA,” Atherosclerosis, vol. 220, no. 1, pp. 3–10, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. B. Ren, Y. X. Zhang, H. X. Zhou et al., “Tanshinone IIA prevents the loss of nigrostriatal dopaminergic neurons by inhibiting NADPH oxidase and iNOS in the MPTP model of Parkinson’s disease,” Journal of the Neurological Sciences, vol. 348, no. 1-2, pp. 142–152, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Li, G. Han, and K. Wu, “Tanshinone IIA alleviates the AD phenotypes in APP and PS1 transgenic mice,” BioMed Research International, vol. 2016, Article ID 7631801, 8 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Y. Lin, C. W. Lu, S. K. Huang, and S. J. Wang, “Tanshinone IIA, a constituent of Danshen, inhibits the release of glutamate in rat cerebrocortical nerve terminals,” Journal of Ethnopharmacology, vol. 147, no. 2, pp. 488–496, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Lei, H. Li, Z. Fang et al., “Polysaccharides from Angelica sinensis alleviate neuronal cell injury caused by oxidative stress,” Neural Regeneration Research, vol. 9, no. 3, pp. 260–267, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Kim, S. C. Yoon, T. Y. Lee, and D. Jeong, “Discriminative cytotoxicity assessment based on various cellular damages,” Toxicology Letters, vol. 184, no. 1, pp. 13–17, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Guan, J. Xu, Y. Guo et al., “Pyrroloquinoline quinone against glutamate-induced neurotoxicity in cultured neural stem and progenitor cells,” International Journal of Developmental Neuroscience, vol. 42, pp. 37–45, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Ai, T. Jia, W. Ai et al., “Targeted delivery of doxorubicin through conjugation with EGF receptor-binding peptide overcomes drug resistance in human colon cancer cells,” British Journal of Pharmacology, vol. 168, no. 7, pp. 1719–1735, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. L. Xiao, H. Li, J. Zhang et al., “Salidroside protects Caenorhabditis elegans neurons from polyglutamine-mediated toxicity by reducing oxidative stress,” Molecules, vol. 19, no. 6, pp. 7757–7769, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. Q. Wang, Y. Huang, C. Qin et al., “Bioactive peptides from Angelica sinensis protein hydrolyzate delay senescence in Caenorhabditis elegans through antioxidant activities,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 8956981, 10 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Li, Y. Zhang, Y. Yuan et al., “Protective effects of selenium, vitamin E, and purple carrot anthocyanins on D-galactose-induced oxidative damage in blood, liver, heart and kidney rats,” Biological Trace Element Research, vol. 173, no. 2, pp. 433–442, 2016. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Li, B. Wang, F. Sun et al., “Mitochondrial respiratory dysfunctions of blood mononuclear cells link with cardiac disturbance in patients with early-stage heart failure,” Scientific Reports, vol. 5, p. 10229, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. M. K. Arjmandi, D. Moslemi, A. S. Zarrini et al., “Pre and post radiotherapy serum oxidant/antioxidant status in breast cancer patients: impact of age, BMI and clinical stage of the disease,” Reports of Practical Oncology and Radiotherapy, vol. 21, no. 3, pp. 141–148, 2016. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Tian, J. Cheng, J. Zhang et al., “Protection of pyruvate against glutamate excitotoxicity is mediated by regulating DAPK1 protein complex,” PloS One, vol. 9, no. 4, article e95777, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Zhang, R. Shi, H. Li et al., “Antioxidant and neuroprotective effects of Dictyophora indusiata polysaccharide in Caenorhabditis elegans,” Journal of Ethnopharmacology, vol. 192, pp. 413–422, 2016. View at Publisher · View at Google Scholar · View at Scopus
  31. Z. Huang, M. C. Banton, and A. Tunnacliffe, “Modeling anhydrobiosis: activation of the mitogen-activated protein kinase ERK by dehydration in both human cells and nematodes,” Journal of Experimental Zoology Part A Ecological Genetics and Physiology, vol. 313, no. 10, pp. 660–670, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. C. K. Vorwerk, J. Bonheur, M. R. Kreutz, E. B. Dreyer, and H. Laev, “GM1 ganglioside administration protects spinal neurons after glutamate excitotoxicity,” Restorative Neurology and Neuroscience, vol. 14, no. 1, pp. 47–51, 1999. View at Google Scholar
  33. X. G. Lei, J. H. Zhu, W. H. Cheng et al., “Paradoxical roles of antioxidant enzymes: basic mechanisms and health implications,” Physiological Reviews, vol. 96, no. 1, pp. 307–364, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. Z. Bezvenyuk, R. Miettinen, and V. Solovyan, “Chromatin condensation during glutamate-induced excitotoxicity of celebellar granule neurons precedes disintegration of nuclear DNA into high molecular weight DNA fragments,” Molecular Brain Research, vol. 110, no. 1, pp. 140–146, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Kroemer, L. Galluzzi, and C. Brenner, “Mitochondrial membrane permeabilization in cell death,” Physiological Reviews, vol. 87, no. 1, pp. 99–163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Karch and J. D. Molkentin, “Regulated necrotic cell death: the passive aggressive side of Bax and Bak,” Circulation Research, vol. 116, no. 11, pp. 1800–1809, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Singh, K. A. Mann, H. K. Mangat, and G. Kaur, “Prolonged glutamate excitotoxicity: effects on mitochondrial antioxidants and antioxidant enzymes,” Molecular and Cellular Biochemistry, vol. 243, no. 1-2, pp. 139–145, 2003. View at Google Scholar
  38. B. D. Shivasharan, P. Nagakannan, B. S. Thippeswamy, and V. P. Veerapur, “Protective effect of Calendula officinalis L. flowers against monosodium glutamate induced oxidative stress and excitotoxic brain damage in rats,” Indian Journal of Clinical Biochemistry, vol. 28, no. 3, pp. 292–298, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Regner, D. P. Schunemann, I. Grivicich et al., “Effects of toxic doses of glutamate on Cu-Zn and Mn/superoxide dismutases activities in human glioma cell lines,” Journal of Neuro-Oncology, vol. 71, no. 1, pp. 9–17, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Peluffo, L. Acarin, M. Faiz, B. Castellano, and B. Gonzalez, “Cu/Zn superoxide dismutase expression in the postnatal rat brain following an excitotoxic injury,” Journal of Neuroinflammation, vol. 2, no. 1, p. 12, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Li, J. C. Copin, L. F. Reola et al., “Reduced mitochondrial manganese-superoxide dismutase activity exacerbates glutamate toxicity in cultured mouse cortical neurons,” Brain Research, vol. 814, no. 1-2, pp. 164–170, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. P. J. Schwartz, A. Reaume, R. Scott, and J. T. Coyle, “Effects of over- and under-expression of Cu,Zn-superoxide dismutase on the toxicity of glutamate analogs in transgenic mouse striatum,” Brain Research, vol. 789, no. 1, pp. 32–39, 1998. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Jia, L. Zhang, X. Shi et al., “SOD2 mediates amifostine-induced protection against glutamate in PC12 cells,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 4202437, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Tang, X. Wu, T. Wang et al., “Tanshinone IIA attenuates atherosclerotic calcification in rat model by inhibition of oxidative stress,” Vascular Pharmacology, vol. 46, no. 6, pp. 427–438, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. A. C. Rego and C. R. Oliveira, “Mitochondrial dysfunction and reactive oxygen species in excitotoxicity and apoptosis: implications for the pathogenesis of neurodegenerative diseases,” Neurochemical Research, vol. 28, no. 10, pp. 1563–1574, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. B. I. Frohnert and D. A. Bernlohr, “Protein carbonylation, mitochondrial dysfunction, and insulin resistance,” Advances in Nutrition, vol. 4, no. 2, pp. 157–163, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. H. J. Jin, X. L. Xie, J. M. Ye, and C. G. Li, “Tanshinone IIA and cryptotanshinone protect against hypoxia-induced mitochondrial apoptosis in H9c2 cells,” PloS One, vol. 8, no. 1, article e51720, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. W. Boston-Howes, S. L. Gibb, E. O. Williams, P. Pasinelli, R. H. Brown Jr, and D. Trotti, “Caspase-3 cleaves and inactivates the glutamate transporter EAAT2,” Journal of Biological Chemistry, vol. 281, no. 20, pp. 14076–14084, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Sahin, A. Saxena, P. Joost, J. Lewerenz, and A. Methner, “Induction of Bcl-2 by functional regulation of G-protein coupled receptors protects from oxidative glutamate toxicity by increasing glutathione,” Free Radical Research, vol. 40, no. 11, pp. 1113–1123, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Gavaldà, E. Pérez-Navarro, J. M. García-Martínez, S. Marco, A. Benito, and J. Alberch, “Bax deficiency promotes an up-regulation of BimEL and Bak during striatal and cortical postnatal development, and after excitotoxic injury,” Molecular and Cellular Neuroscience, vol. 37, no. 4, pp. 663–672, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Howard, C. Bottino, S. Brooke, E. Cheng, R. G. Giffard, and R. Sapolsky, “Neuroprotective effects of bcl-2 overexpression in hippocampal cultures: interactions with pathways of oxidative damage,” Journal of Neurochemistry, vol. 83, no. 4, pp. 914–923, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Iriyama, Y. Kamei, S. Kozuma, and Y. Taketani, “Bax-inhibiting peptide protects glutamate-induced cerebellar granule cell death by blocking Bax translocation,” Neuroscience Letters, vol. 451, no. 1, pp. 11–15, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. T. A. Chen, F. Yang, G. M. Cole, and S. O. Chan, “Inhibition of caspase-3-like activity reduces glutamate induced cell death in adult rat retina,” Brain Research, vol. 904, no. 1, pp. 177–188, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. X. S. Zhang, S. Ha, X. L. Wang, Y. L. Shi, S. S. Duan, and Z. A. Li, “Tanshinone IIA protects dopaminergic neurons against 6-hydroxydopamine-induced neurotoxicity through miR-153/NF-E2-related factor 2/antioxidant response element signaling pathway,” Neuroscience, vol. 303, pp. 489–502, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Ma, Q. Fan, J. Yu, J. Xin, and C. Zhang, “Novel microemulsion of tanshinone IIA, isolated from Salvia miltiorrhiza Bunge, exerts anticancer activity through inducing apoptosis in hepatoma cells,” American Journal of Chinese Medicine, vol. 41, no. 1, pp. 197–210, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. P. Canoll and J. E. Goldman, “The interface between glial progenitors and gliomas,” Acta Neuropathologica, vol. 116, no. 5, pp. 465–477, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Dajas, “Life or death: neuroprotective and anticancer effects of quercetin,” Journal of Ethnopharmacology, vol. 143, no. 2, pp. 383–396, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. V. Chaparro-Huerta, M. E. Flores-Soto, G. Gudiño-Cabrera, M. C. Rivera-Cervantes, O. K. Bitzer-Quintero, and C. Beas-Zárate, “Role of p38 MAPK and pro-inflammatory cytokines expression in glutamate-induced neuronal death of neonatal rats,” International Journal of Developmental Neuroscience, vol. 26, no. 5, pp. 487–495, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Wada and J. M. Penninger, “Mitogen-activated protein kinases in apoptosis regulation,” Oncogene, vol. 23, no. 16, pp. 2838–2849, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Nistico, F. Florenzano, D. Mango et al., “Presynaptic c-Jun N-terminal kinase 2 regulates NMDA receptor-dependent glutamate release,” Scientific Reports, vol. 5, p. 9035, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Dong, S. Mao, J. Wei et al., “Tanshinone IIA protects PC12 cells from β-amyloid25-35-induced apoptosis via PI3K/Akt signaling pathway,” Molecular Biology Reports, vol. 39, no. 6, pp. 6495–6503, 2012. View at Publisher · View at Google Scholar · View at Scopus