Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 1832093, 17 pages
https://doi.org/10.1155/2017/1832093
Research Article

YiQiFuMai Powder Injection Protects against Ischemic Stroke via Inhibiting Neuronal Apoptosis and PKCδ/Drp1-Mediated Excessive Mitochondrial Fission

Department of Complex Prescription of TCM, State Key Laboratory of Natural Products, Jiangsu Key Laboratory of TCM Evaluation and Translational Research, China Pharmaceutical University, Nanjing, China

Correspondence should be addressed to Boyang Yu; moc.361@95uygnayob and Junping Kou; nc.ude.upc@uokgnipnuj

Received 3 June 2017; Revised 21 August 2017; Accepted 30 October 2017; Published 24 December 2017

Academic Editor: M. Dolores Martín-de-Saavedra

Copyright © 2017 Yingqiong Xu 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. M. Fisher and J. L. Saver, “Future directions of acute ischaemic stroke therapy,” The Lancet Neurology, vol. 14, no. 7, pp. 758–767, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. K. M. Barrett, B. K. Lal, and J. F. Meschia, “Stroke: advances in medical therapy and acute stroke intervention,” Current Cardiology Reports, vol. 17, no. 10, p. 79, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Manzanero, T. Santro, and T. V. Arumugam, “Neuronal oxidative stress in acute ischemic stroke: sources and contribution to cell injury,” Neurochemistry International, vol. 62, no. 5, pp. 712–718, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Baxter, Y. Chen, Y. Xu, and R. A. Swanson, “Mitochondrial dysfunction induced by nuclear poly(ADP-ribose) polymerase-1: a treatable cause of cell death in stroke,” Translational Stroke Research, vol. 5, no. 1, pp. 136–144, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Maheshwari, M. M. Misro, A. Aggarwal, R. K. Sharma, and D. Nandan, “Pathways involved in testicular germ cell apoptosis induced by H2O2 in vitro,” The FEBS Journal, vol. 276, no. 3, pp. 870–881, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Roshanzamir and R. Yazdanparast, “Quercetin attenuates cell apoptosis of oxidant-stressed SK-N-MC cells while suppressing up-regulation of the defensive element, HIF-1α,” Neuroscience, vol. 277, pp. 780–793, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. Z. T. Rong, X. J. Gong, H. B. Sun, Y. M. Li, and H. Ji, “Protective effects of oleanolic acid on cerebral ischemic damage in vivo and H2O2-induced injury in vitro,” Pharmaceutical Biology, vol. 49, no. 1, pp. 78–85, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. S. K. Rajput, A. K. Sharma, C. L. Meena, A. B. Pant, R. Jain, and S. S. Sharma, “Effect of L-pGlu-(1-benzyl)-l-His-l-Pro-NH2 against in-vitro and in-vivo models of cerebral ischemia and associated neurological disorders,” Biomedicine & Pharmacotherapy, vol. 84, pp. 1256–1265, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. M. J. Goldenthal and J. Marín-García, “Mitochondrial signaling pathways: a receiver/integrator organelle,” Molecular and Cellular Biochemistry, vol. 262, no. 1-2, pp. 1–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. O. S. Kornfeld, S. Hwang, M. Disatnik, C. H. Chen, N. Qvit, and D. Mochlyrosen, “Mitochondrial reactive oxygen species at the heart of the matter: new therapeutic approaches for cardiovascular diseases,” Circulation Research, vol. 116, no. 11, pp. 1783–1799, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. D. H. Cho, T. Nakamura, and S. A. Lipton, “Mitochondrial dynamics in cell death and neurodegeneration,” Cellular and Molecular Life Sciences, vol. 67, no. 20, pp. 3435–3447, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. V. J. Davies, A. J. Hollins, M. J. Piechota et al., “Opa1 deficiency in a mouse model of autosomal dominant optic atrophy impairs mitochondrial morphology, optic nerve structure and visual function,” Human Molecular Genetics, vol. 16, no. 11, pp. 1307–1318, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Grohm, S. W. Kim, U. Mamrak et al., “Inhibition of Drp1 provides neuroprotection in vitro and in vivo,” Cell Death & Differentiation, vol. 19, no. 9, pp. 1446–1458, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. X. M. Zhang, L. Zhang, G. Wang et al., “Suppression of mitochondrial fission in experimental cerebral ischemia: the potential neuroprotective target of p38 MAPK inhibition,” Neurochemistry International, vol. 90, pp. 1–8, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. A. R. Jang and P. O. Koh, “Ischemic brain injury decreases dynamin-like protein 1 expression in a middle cerebral artery occlusion animal model and glutamate-exposed HT22 cells,” Laboratory Animal Research, vol. 32, no. 4, pp. 194–199, 2016. View at Publisher · View at Google Scholar
  16. B. Cho, S. Y. Choi, H. M. Cho, H. J. Kim, and W. Sun, “Physiological and pathological significance of dynamin-related protein 1 (drp1)-dependent mitochondrial fission in the nervous system,” Experimental Neurobiology, vol. 22, no. 3, pp. 149–157, 2013. View at Publisher · View at Google Scholar
  17. R. J. Youle and M. Karbowski, “Mitochondrial fission in apoptosis,” Nature Reviews Molecular Cell Biology, vol. 6, no. 8, pp. 657–663, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Bossy-Wetzel, M. J. Barsoum, A. Godzik, R. Schwarzenbacher, and S. A. Lipton, “Mitochondrial fission in apoptosis, neurodegeneration and aging,” Current Opinion in Cell Biology, vol. 15, no. 6, pp. 706–716, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Balog, S. L. Mehta, and R. Vemuganti, “Mitochondrial fission and fusion in secondary brain damage after CNS insults,” Journal of Cerebral Blood Flow & Metabolism, vol. 36, no. 12, pp. 2022–2033, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Shimohata, H. Zhao, J. H. Sung, G. Sun, D. Mochlyrosen, and G. K. Steinberg, “Suppression of δPKC activation after focal cerebral ischemia contributes to the protective effect of hypothermia,” Journal of Cerebral Blood Flow & Metabolism, vol. 27, no. 8, pp. 1463–1475, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. X. Qi, M. H. Disatnik, N. Shen, R. A. Sobel, and D. Mochly-Rosen, “Aberrant mitochondrial fission in neurons induced by protein kinase C delta under oxidative stress conditions in vivo,” Molecular Biology of the Cell, vol. 22, no. 2, pp. 256–265, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. Q. Zhang, B. Wang, W. Liu, and Y. Deng, “Regulative effects of Yiqifumai injection on the activity of matrix metalloproteinase in rats with chronic heart failure,” Chinese Journal of Integrative Medicine on Cardio/Cerebrovascular Disease, vol. 14, no. 8, pp. 825–829, 2016. View at Google Scholar
  23. L. Xing, M. Jiang, L. Dong et al., “Cardioprotective effects of the YiQiFuMai injection and isolated compounds on attenuating chronic heart failure via NF-κB inactivation and cytokine suppression,” Journal of Ethnopharmacology, vol. 148, no. 1, pp. 239–245, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. F. Li, Y. S. Tan, H. L. Chen et al., “Identification of schisandrin as a vascular endothelium protective component in YiQiFuMai powder injection using HUVECs binding and HPLC-DAD-Q-TOF-MS/MS analysis,” Journal of Pharmacological Sciences, vol. 129, no. 1, pp. 1–8, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. Q. Yuan, J. Wang, Q.-H. Fang et al., “Attenuating effect of pretreatment with Yiqifumai on lipopolysaccharide-induced intestine injury and survival rate in rat,” Journal of Inflammation, vol. 8, no. 1, p. 10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Zhou, Y. Cao, and D. Q. Dou, “Protective effect of ginsenoside-Re against cerebral ischemia/reperfusion damage in rats,” Biological & Pharmaceutical Bulletin, vol. 29, no. 12, pp. 2502–2505, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. S. F. Nabavi, A. Sureda, S. Habtemariam, and S. M. Nabavi, “Ginsenoside Rd and ischemic stroke; a short review of literatures,” Journal of Ginseng Research, vol. 39, no. 4, pp. 299–303, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Ye, X. Zhang, X. Kong et al., “Ginsenoside Rd attenuates mitochondrial dysfunction and sequential apoptosis after transient focal ischemia,” Neuroscience, vol. 178, no. 3, pp. 169–180, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. M. S. Lee, J. Chao, J. C. Yen et al., “Schizandrin protects primary rat cortical cell cultures from glutamate-induced apoptosis by inhibiting activation of the MAPK family and the mitochondria dependent pathway,” Molecules, vol. 18, no. 1, pp. 354–372, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. C. P. Wang, G. C. Li, Y. W. Shi et al., “Neuroprotective effect of schizandrin A on oxygen and glucose deprivation/reperfusion-induced cell injury in primary culture of rat cortical neurons,” Journal of Physiology and Biochemistry, vol. 70, no. 3, pp. 735–747, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Yang, L. Xin, L. Zhang, L. Lin, G. Jing, and C. Hui, “Ginsenoside Rg1 suppressed inflammation and neuron apoptosis by activating PPARγ/HO-1 in hippocampus in rat model of cerebral ischemia-reperfusion injury,” International Journal of Clinical & Experimental Pathology, vol. 8, no. 3, pp. 2484–2494, 2015. View at Google Scholar
  32. Y. Nam, M. B. Wie, E. J. Shin et al., “Ginsenoside Re protects methamphetamine-induced mitochondrial burdens and proapoptosis via genetic inhibition of protein kinase C δ in human neuroblastoma dopaminergic SH-SY5Y cell lines,” Journal of Applied Toxicology, vol. 35, no. 8, pp. 927–944, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. E. J. Shin, S. W. Shin, T. T. L. Nguyen et al., “Ginsenoside re rescues methamphetamine-induced oxidative damage, mitochondrial dysfunction, microglial activation, and dopaminergic degeneration by inhibiting the protein kinase Cδ gene,” Molecular Neurobiology, vol. 49, no. 3, pp. 1400–1421, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. L. Yang, L. Jia, L. Kang et al., “Ginsenoside Rg5 increases cardiomyocyte resistance to ischemic injury through regulation of mitochondrial hexokinase-II and dynamin-related protein 1,” Cell Death & Disease, vol. 8, no. 2, article e2625, 2017. View at Publisher · View at Google Scholar
  35. G. Dong, T. Chen, X. Ren et al., “Rg1 prevents myocardial hypoxia/reoxygenation injury by regulating mitochondrial dynamics imbalance via modulation of glutamate dehydrogenase and mitofusin 2,” Mitochondrion, vol. 26, pp. 7–18, 2016. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Cao, H. Zhou, N. Jiang et al., “YiQiFuMai powder injection ameliorates cerebral ischemia by inhibiting endoplasmic reticulum stress-mediated neuronal apoptosis,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 5493279, 14 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  37. G. S. Cao, H. L. Chen, Y. Y. Zhang et al., “YiQiFuMai powder injection ameliorates the oxygen-glucose deprivation-induced brain microvascular endothelial barrier dysfunction associated with the NF-ĸB and ROCK1/MLC signaling pathways,” Journal of Ethnopharmacology, vol. 183, pp. 18–28, 2016. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Cao, X. Ye, Y. Xu et al., “YiQiFuMai powder injection ameliorates blood–brain barrier dysfunction and brain edema after focal cerebral ischemia–reperfusion injury in mice,” Drug Design Development & Therapy, vol. 10, no. 1, pp. 315–325, 2016. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Li, X. Fan, Y. Zhang et al., “Cardioprotection by combination of three compounds from ShengMai preparations in mice with myocardial ischemia/reperfusion injury through AMPK activation-mediated mitochondrial fission,” Scientific Reports, vol. 6, no. 1, article 37114, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Z. Longa, P. R. Weinstein, S. Carlson, and R. Cummins, “Reversible middle cerebral artery occlusion without craniectomy in rats,” Stroke, vol. 20, no. 1, pp. 84–91, 1989. View at Publisher · View at Google Scholar
  41. V. Zinchuk and O. Grossenbacher-Zinchuk, “Recent advances in quantitative colocalization analysis: focus on neuroscience,” Progress in Histochemistry and Cytochemistry, vol. 44, no. 3, pp. 125–172, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Wang, Q. Liu, Y. Xu et al., “Ginsenoside Rg1 protects against oxidative stress-induced neuronal apoptosis through myosin IIA-actin related cytoskeletal reorganization,” International Journal of Biological Sciences, vol. 12, no. 11, pp. 1341–1356, 2016. View at Publisher · View at Google Scholar · View at Scopus
  43. A. M. V. D. Bliek, Q. Shen, and S. Kawajiri, “Mechanisms of mitochondrial fission and fusion,” Cold Spring Harbor Perspectives in Biology, vol. 5, no. 6, article a011072, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Kim and Y. S. Song, “Mitochondrial dynamics altered by oxidative stress in cancer,” Free Radical Research, vol. 50, no. 10, pp. 1–16, 2016. View at Publisher · View at Google Scholar · View at Scopus
  45. I. Zaja, X. Bai, Y. Liu et al., “Cdk1, PKCδ and calcineurin-mediated Drp1 pathway contributes to mitochondrial fission-induced cardiomyocyte death,” Biochemical and Biophysical Research Communications, vol. 453, no. 4, pp. 710–721, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Lim, S. Y. Lee, H. H. Seo et al., “Regulation of mitochondrial morphology by positive feedback interaction between PKCδ and Drp1 in vascular smooth muscle cell,” Journal of Cellular Biochemistry, vol. 116, no. 4, pp. 648–660, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. M. C. White, R. Gao, W. Xu et al., “Inactivation of hnRNP K by expanded intronic AUUCU repeat induces apoptosis via translocation of PKCδ to mitochondria in spinocerebellar ataxia 10,” PLoS Genetics, vol. 6, no. 6, article e1000984, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. P. K. Majumder, P. Pandey, X. Sun et al., “Mitochondrial translocation of protein kinase C δ in phorbol ester-induced cytochrome c release and apoptosis,” The Journal of Biological Chemistry, vol. 275, no. 29, pp. 21793–21796, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. P. H. Reddy, T. P. Reddy, M. Manczak, M. J. Calkins, U. Shirendeb, and P. Mao, “Dynamin-related protein 1 and mitochondrial fragmentation in neurodegenerative diseases,” Brain Research Reviews, vol. 67, no. 1-2, pp. 103–118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Taguchi, N. Ishihara, A. Jofuku, T. Oka, and K. Mihara, “Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission,” Journal of Biological Chemistry, vol. 282, no. 15, pp. 11521–11529, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. N. Zhang, S. Wang, Y. Li, L. Che, and Q. Zhao, “A selective inhibitor of Drp1, mdivi-1, acts against cerebral ischemia/reperfusion injury via an anti-apoptotic pathway in rats,” Neuroscience Letters, vol. 535, no. 1, pp. 104–109, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Prasath and P. Bhavana, “Functional and morphological impact of ER stress on mitochondria,” Journal of Cellular Physiology, vol. 228, no. 9, pp. 1802–1818, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Li, Y. Wang, Y. Wang et al., “Pharmacological activation of AMPK prevents Drp1-mediated mitochondrial fission and alleviates endoplasmic reticulum stress-associated endothelial dysfunction,” Journal of Molecular and Cellular Cardiology, vol. 86, pp. 62–74, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. C. L. Murriel, E. Churchill, K. Inagaki, L. I. Szweda, and D. Mochlyrosen, “Protein kinase Cδ activation induces apoptosis in response to cardiac ischemia and reperfusion damage: a mechanism involving BAD and the mitochondria,” The Journal of Biological Chemistry, vol. 279, no. 46, pp. 47985–47991, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Nam, M. B. Wie, E. Shin et al., “Ginsenoside Re protects methamphetamine-induced mitochondrial burdens and proapoptosis via genetic inhibition of protein kinase C δ in human neuroblastoma dopaminergic SH-SY5Y cell lines,” Journal of Applied Toxicology, vol. 35, no. 8, pp. 927–944, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Yu, S. S. Sheu, J. L. Robotham, and Y. Yoon, “Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species,” Cardiovascular Research, vol. 79, no. 2, pp. 341–351, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. B. Kim, J. Park, K. T. Chang, and D. S. Lee, “Peroxiredoxin 5 prevents amyloid-beta oligomer-induced neuronal cell death by inhibiting ERK–Drp1-mediated mitochondrial fragmentation,” Free Radical Biology & Medicine, vol. 90, pp. 184–194, 2016. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. Wang, Y. Xu, Q. Liu et al., “Myosin IIA-related actomyosin contractility mediates oxidative stress-induced neuronal apoptosis,” Frontiers in Molecular Neuroscience, vol. 10, p. 75, 2017. View at Publisher · View at Google Scholar
  59. X. Li, H. Tao, K. Xie et al., “cAMP signaling prevents podocyte apoptosis via activation of protein kinase a and mitochondrial fusion,” PLoS One, vol. 9, no. 3, article e92003, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Karbowski, “Mitochondria on guard: role of mitochondrial fusion and fission in the regulation of apoptosis,” Advances in Experimental Medicine and Biology, vol. 687, pp. 131–142, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. M. E. Reyland and D. N. M. Jones, “Multifunctional roles of PKCδ: opportunities for targeted therapy in human disease,” Pharmacology & Therapeutics, vol. 165, pp. 1–13, 2016. View at Publisher · View at Google Scholar · View at Scopus