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Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 1401790, 9 pages
https://doi.org/10.1155/2017/1401790
Research Article

Baicalin Attenuates Subarachnoid Hemorrhagic Brain Injury by Modulating Blood-Brain Barrier Disruption, Inflammation, and Oxidative Damage in Mice

Intensive Care Unit, Guizhou Province People’s Hospital, Guiyang, Guizhou Province 550002, China

Correspondence should be addressed to Xianqing Shi; moc.621@gniqnaixihs

Received 31 May 2017; Revised 23 June 2017; Accepted 3 July 2017; Published 24 August 2017

Academic Editor: Aditya Sen

Copyright © 2017 Xianqing Shi 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. H. Lantigua, S. Ortega-Gutierrez, J. M. Schmidt et al., “Subarachnoid hemorrhage: who dies, and why?” Critical Care, vol. 19, p. 309, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. E. C. Haley Jr., N. F. Kassell, and J. C. Torner, “The International Cooperative Study on the timing of aneurysm surgery. The North American experience,” Stroke, vol. 23, pp. 205–214, 1992. View at Google Scholar
  3. C. P. Nolan and R. L. Macdonald, “Can angiographic vasospasm be used as a surrogate marker in evaluating therapeutic interventions for cerebral vasospasm?” Neurosurgical Focus, vol. 21, article E1, 2006. View at Publisher · View at Google Scholar
  4. S. Chen, H. Feng, P. Sherchan et al., “Controversies and evolving new mechanisms in subarachnoid hemorrhage,” Progress in Neurobiology, vol. 115, pp. 64–91, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Jeon, J. Ai, M. Sabri et al., “Neurological and neurobehavioral assessment of experimental subarachnoid hemorrhage,” BMC Neuroscience, vol. 10, p. 103, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. X. Lan, X. Han, Q. Li et al., “Pinocembrin protects hemorrhagic brain primarily by inhibiting toll-like receptor 4 and reducing M1 phenotype microglia,” Brain, Behavior, and Immunity, vol. 61, pp. 326–339, 2017. View at Publisher · View at Google Scholar
  7. X. Lan, W. Wang, Q. Li, and J. Wang, “The natural flavonoid pinocembrin: molecular targets and potential therapeutic applications,” Molecular Neurobiology, vol. 53, pp. 1794–1801, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Yuan, W. Liu, H. Zhu et al., “Curcumin attenuates blood-brain barrier disruption after subarachnoid hemorrhage in mice,” The Journal of Surgical Research, vol. 207, pp. 85–91, 2017. View at Publisher · View at Google Scholar
  9. C. P. Chang, W. T. Huang, B. C. Cheng, C. C. Hsu, and M. T. Lin, “The flavonoid baicalin protects against cerebrovascular dysfunction and brain inflammation in experimental heatstroke,” Neuropharmacology, vol. 52, pp. 1024–1033, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. K. L. Huang, C. S. Chen, C. W. Hsu et al., “Therapeutic effects of baicalin on lipopolysaccharide-induced acute lung injury in rats,” The American Journal of Chinese Medicine, vol. 36, pp. 301–311, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Y. Wan, X. Gong, L. Zhang, H. Z. Li, Y. F. Zhou, and Q. X. Zhou, “Protective effect of baicalin against lipopolysaccharide/D-galactosamine-induced liver injury in mice by up-regulation of heme oxygenase-1,” European Journal of Pharmacology, vol. 587, pp. 302–308, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. M. F. Zeng, L. M. Pan, H. X. Zhu, Q. C. Zhang, and L. W. Guo, “Comparative pharmacokinetics of baicalin in plasma after oral administration of Huang-Lian-Jie-Du-Tang or pure baicalin in MCAO and sham-operated rats,” Fitoterapia, vol. 81, pp. 490–496, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. P. L. Tsai and T. H. Tsai, “Pharmacokinetics of baicalin in rats and its interactions with cyclosporin A, quinidine and SKF-525A: a microdialysis study,” Planta Medica, vol. 70, pp. 1069–1074, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. N. R. Srinivas, “Baicalin, an emerging multi-therapeutic agent: pharmacodynamics, pharmacokinetics, and considerations from drug development perspectives,” Xenobiotica, vol. 40, pp. 357–367, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Schuller, D. Buhler, and N. Plesnila, “A murine model of subarachnoid hemorrhage,” Journal of Visualized Experiments, vol. 21, no. 81, article e50845, 2013. View at Publisher · View at Google Scholar
  16. T. Sugawara, R. Ayer, V. Jadhav, and J. H. Zhang, “A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model,” Journal of Neuroscience Methods, vol. 167, pp. 327–334, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Kraft, T. Schwarz, E. Gob et al., “The phosphodiesterase-4 inhibitor rolipram protects from ischemic stroke in mice by reducing blood-brain-barrier damage, inflammation and thrombosis,” Experimental Neurology, vol. 247, pp. 80–90, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Xi, Y. Hua, R. R. Bhasin, S. R. Ennis, R. F. Keep, and J. T. Hoff, “Mechanisms of edema formation after intracerebral hemorrhage: effects of extravasated red blood cells on blood flow and blood-brain barrier integrity,” Stroke, vol. 32, pp. 2932–2938, 2001. View at Google Scholar
  19. J. K. Lee and M. G. Tansey, “Microglia isolation from adult mouse brain,” Methods in Molecular Biology, vol. 1041, pp. 17–23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Sozen, R. Tsuchiyama, Y. Hasegawa et al., “Role of interleukin-1beta in early brain injury after subarachnoid hemorrhage in mice,” Stroke, vol. 40, pp. 2519–2525, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. B. V. Zlokovic, “The blood-brain barrier in health and chronic neurodegenerative disorders,” Neuron, vol. 57, pp. 178–201, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. J. S. Won, Y. B. Im, L. Key, I. Singh, and A. K. Singh, “The involvement of glucose metabolism in the regulation of inducible nitric oxide synthase gene expression in glial cells: possible role of glucose-6-phosphate dehydrogenase and CCAAT/enhancing binding protein,” The Journal of Neuroscience, vol. 23, pp. 7470–7478, 2003. View at Google Scholar
  23. Y. Kifle, J. Monnier, S. E. Chesrown, M. K. Raizada, and H. S. Nick, “Regulation of the manganese superoxide dismutase and inducible nitric oxide synthase gene in rat neuronal and glial cells,” Journal of Neurochemistry, vol. 66, pp. 2128–2135, 1996. View at Google Scholar
  24. K. Dohi, H. Ohtaki, T. Nakamachi et al., “Gp91phox (NOX2) in classically activated microglia exacerbates traumatic brain injury,” Journal of Neuroinflammation, vol. 7, p. 41, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. O. M. Ogundele, A. O. Omoaghe, D. C. Ajonijebu et al., “Glia activation and its role in oxidative stress,” Metabolic Brain Disease, vol. 29, pp. 483–493, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. J. van Gijn, R. S. Kerr, and G. J. Rinkel, “Subarachnoid haemorrhage,” Lancet, vol. 369, pp. 306–318, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. Q. Liu, J. Liu, P. Wang et al., “Poly-dimensional network comparative analysis reveals the pure pharmacological mechanism of baicalin in the targeted network of mouse cerebral ischemia,” Brain Research, vol. 1666, pp. 70–79, 2017. View at Publisher · View at Google Scholar
  28. A. Germano, D. d'Avella, C. Imperatore, G. Caruso, and F. Tomasello, “Time-course of blood-brain barrier permeability changes after experimental subarachnoid haemorrhage,” Acta Neurochirurgica, vol. 142, pp. 575–580, 2000, discussion 580-571. View at Google Scholar
  29. H. Johshita, N. F. Kassell, and T. Sasaki, “Blood-brain barrier disturbance following subarachnoid hemorrhage in rabbits,” Stroke, vol. 21, pp. 1051–1058, 1990. View at Google Scholar
  30. V. Z. Zheng and G. K. Wong, “Neuroinflammation responses after subarachnoid hemorrhage: a review,” Journal of Clinical Neuroscience, vol. 42, 2017. View at Publisher · View at Google Scholar
  31. N. Schallner, R. Pandit, R. LeBlanc 3rd et al., “Microglia regulate blood clearance in subarachnoid hemorrhage by heme oxygenase-1,” The Journal of Clinical Investigation, vol. 125, pp. 2609–2625, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. B. J. van Dijk, M. D. Vergouwen, M. M. Kelfkens, G. J. Rinkel, and E. M. Hol, “Glial cell response after aneurysmal subarachnoid hemorrhage - functional consequences and clinical implications,” Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, vol. 2016, pp. 492–505, 1862. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Kettenmann, U. K. Hanisch, M. Noda, and A. Verkhratsky, “Physiology of microglia,” Physiological Reviews, vol. 91, pp. 461–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Dinda, S. Dinda, S. DasSharma, R. Banik, A. Chakraborty, and M. Dinda, “Therapeutic potentials of baicalin and its aglycone, baicalein against inflammatory disorders,” European Journal of Medicinal Chemistry, vol. 131, pp. 68–80, 2017. View at Publisher · View at Google Scholar
  35. A. Bitto, F. Squadrito, N. Irrera et al., “Flavocoxid, a nutraceutical approach to blunt inflammatory conditions,” Mediators of Inflammation, vol. 2014, Article ID 790851, 8 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Li, G. Lin, and Z. Zuo, “Pharmacological effects and pharmacokinetics properties of Radix Scutellariae and its bioactive flavones,” Biopharmaceutics & Drug Disposition, vol. 32, pp. 427–445, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. L. A. O'Neill and C. Kaltschmidt, “NF-kappa B: a crucial transcription factor for glial and neuronal cell function,” Trends in Neurosciences, vol. 20, pp. 252–258, 1997. View at Google Scholar
  38. R. P. Ostrowski, A. R. Colohan, and J. H. Zhang, “Molecular mechanisms of early brain injury after subarachnoid hemorrhage,” Neurological Research, vol. 28, pp. 399–414, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Cahill, J. W. Calvert, and J. H. Zhang, “Mechanisms of early brain injury after subarachnoid hemorrhage,” Journal of Cerebral Blood Flow and Metabolism, vol. 26, pp. 1341–1353, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Zhang, J. Wu, X. Duan et al., “NADPH oxidase: a potential target for treatment of stroke,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 5026984, 9 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Hanggi and H. J. Steiger, “Nitric oxide in subarachnoid haemorrhage and its therapeutics implications,” Acta Neurochirurgica, vol. 148, pp. 605–613, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Ding, R. M. Starke, A. S. Dumont et al., “Therapeutic implications of estrogen for cerebral vasospasm and delayed cerebral ischemia induced by aneurysmal subarachnoid hemorrhage,” BioMed Research International, vol. 2014, Article ID 727428, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Iqbal, E. G. Hayman, C. Hong et al., “Inducible nitric oxide synthase (NOS-2) in subarachnoid hemorrhage: regulatory mechanisms and therapeutic implications,” Brain Circulation, vol. 2, pp. 8–19, 2016. View at Google Scholar
  44. T. Sayama, S. Suzuki, and M. Fukui, “Role of inducible nitric oxide synthase in the cerebral vasospasm after subarachnoid hemorrhage in rats,” Neurological Research, vol. 21, pp. 293–298, 1999. View at Google Scholar
  45. L. Zhang, Z. Li, D. Feng et al., “Involvement of Nox2 and Nox4 NADPH oxidases in early brain injury after subarachnoid hemorrhage,” Free Radical Research, vol. 51, pp. 316–328, 2017. View at Publisher · View at Google Scholar
  46. L. Gao, J. Hao, Y. Y. Niu et al., “Network pharmacology dissection of multiscale mechanisms of herbal medicines in stage IV gastric adenocarcinoma treatment,” Medicine (Baltimore), vol. 95, article e4389, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Xiang, Q. Zhang, B. Qi et al., “Chinese herbal medicines attenuate acute pancreatitis: pharmacological activities and mechanisms,” Frontiers in Pharmacology, vol. 8, p. 216, 2017. View at Publisher · View at Google Scholar