Procyanidin B2 attenuates neurological deficits and blood-brain barrier disruption in a rat model of cerebral ischemia

Molecular Nutrition and Food Research

Volumn 59, Issue 10, 2015, Pages 1930-1941

  Wu, Shuangchan ^a   Yue, Yuan ^a   Li, Jian ^a   Li, Zhike ^a   Li, Xiaofei ^a   Niu, Yunhui ^a   Xiang, Jin ^a   Ding, Hong ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Blood brain barrier; Ischemic stroke; Neurological deficits; Nrf2; Procyanidin B2

Indexed keywords

BIFLAVONOID; CATECHIN; GLUTATHIONE S-TRANSFERASE ALPHA; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; ISOENZYME; NEUROPROTECTIVE AGENT; NQO1 PROTEIN, RAT; PROANTHOCYANIDIN; PROCYANIDIN B2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE);

ANIMAL; BLOOD BRAIN BARRIER; BRAIN EDEMA; BRAIN ISCHEMIA; CEREBRAL ARTERY DISEASE; DISEASE MODEL; DRUG EFFECTS; DRUG INACTIVATION; MALE; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PATHOPHYSIOLOGY; PERMEABILITY; SPRAGUE DAWLEY RAT; TIGHT JUNCTION;

ANIMALS; BIFLAVONOIDS; BLOOD-BRAIN BARRIER; BRAIN EDEMA; BRAIN ISCHEMIA; CATECHIN; DISEASE MODELS, ANIMAL; GLUTATHIONE TRANSFERASE; HEME OXYGENASE-1; INACTIVATION, METABOLIC; INFARCTION, MIDDLE CEREBRAL ARTERY; ISOENZYMES; MALE; NAD(P)H DEHYDROGENASE (QUINONE); NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PERMEABILITY; PROANTHOCYANIDINS; RATS, SPRAGUE-DAWLEY; TIGHT JUNCTIONS;

EID: 84942818259     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500181     Document Type: Article

References (55)

1. Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J. et al., Executive summary: heart disease and stroke statistics-2014 update: a report from the American Heart Association. Circulation 2014, 129, 399-410.
2. Xiao, L., Xu, H., Zhang, Y., Wei, Z. et al., Quetiapine facilitates oligodendrocyte development and prevents mice from myelin breakdown and behavioral changes. Mol. Psychiatry 2008, 13, 697-708.
3. Tezuka, T., Tamura, M., Kondo, M. A., Sakaue, M. et al., Cuprizone short-term exposure: astrocytic IL-6 activation and behavioral changes relevant to psychosis. Neurobiol. Dis. 2013, 59, 63-68.
4. Jiang, M. J., Li, J., Peng, Q. X., Liu, Y. et al., Neuroprotective effects of bilobalide on cerebral ischemia and reperfusion injury are associated with inhibition of pro-inflammatory mediator production and down-regulation of JNK1/2 and p38 MAPK activation. J. Neuroinflammation 2014, 11, 1-17.
5. Eltzschig, H. K., Eckle, T., Ischemia and reperfusion-from mechanism to translation. Nat. Med. 2011, 17, 1391-1401.
6. Peng, Z., Wang, S., Chen, G., Cai, M. et al., Gastrodin alleviates cerebral ischemic damage in mice by improving anti-oxidant and anti-inflammation activities and inhibiting apoptosis pathway. Neurochem. Res. 2015, 40, 661-673.
7. Fang, W., Sha, L., Kodithuwakku, N. D., Wei, J. et al., Attenuated blood-brain barrier dysfunction by XQ-1H following ischemic stroke in hyperlipidemic rats. Mol. Neurobiol. 2014, 52, 162-175.
8. Alfieri, A., Srivastava, S., Siow, R. C., Cash, D. et al., Sulforaphane preconditioning of the Nrf2/HO-1 defense pathway protects the cerebral vasculature against blood-brain barrier disruption and neurological deficits in stroke. Free Radic. Biol. Med. 2013, 65, 1012-1022.
9. Yu, Y., Qin, J., Liu, M. Z., Ruan, Q. Y. et al., Role of Rho kinase in lysophosphatidic acid-induced altering of blood-brain barrier permeability. Int. J. Mol. Med. 2014, 33, 661-669.
10. Choi, J. S., Park, J., Suk, K., Moon, C. et al., Mild hypothermia attenuates intercellular adhesion molecule-1 induction via activation of extracellular signal-regulated kinase-1/2 in a focal cerebral ischemia model. Stroke Res. Treat. 2011, 2011, 1-9.
11. Huang, J., Li, Y. N., Tang, Y. H., Tang, G. H. et al., CXCR4 antagonist AMD3100 protects blood-brain barrier integrity and reduces inflammatory response after focal ischemia in mice. Stroke 2013, 44, 190-197.
12. Yue, Y., Wu, S., Zhang, H., Zhang, X. et al., Characterization and hepatoprotective effect of polysaccharides from Ziziphus jujuba Mill. var. spinosa (Bunge) Hu ex H. F. Chou sarcocarp. Food Chem. Toxicol. 2014, 74, 76-84.
13. Zhao, Y., Fu, B., Zhang, X., Zhao, T. et al., Paeonol pretreatment attenuates cerebral ischemic injury via upregulating expression of pAkt, Nrf2, HO-1 and ameliorating BBB permeability in mice. Brain Res. Bull. 2014, 109, 61-67.
14. Kobayashi, M., Yamamoto, M., Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 2005, 7, 385-394.
15. Yang, H., Xiao, L., Yuan, Y., Luo, X. et al., Procyanidin B2 inhibits NLRP3 inflammasome activation in human vascular endothelial cells. Biochem. Pharmacol. 2014, 92, 599-606.
16. Serra, A., Macia, A., Rubio, L., Angles, N. et al., Distribution of procyanidins and their metabolites in rat plasma and tissues in relation to ingestion of procyanidin-enriched or procyanidin-rich cocoa creams. Eur. J. Nutr. 2013, 52, 1029-1038.
17. Martinez-Micaelo, N., Gonzalez-Abuin, N., Pinent, M., Ardevol, A. et al., Procyanidin B inhibits inflammasome-mediated IL-1beta production in lipopolysaccharide-stimulated macrophages. Mol. Nutr. Food Res. 2015, 59, 262-269.
18. Duan, Y., Wang, Z., Zhang, H., He, Y. et al., Extremely low frequency electromagnetic field exposure causes cognitive impairment associated with alteration of the glutamate level, MAPK pathway activation and decreased CREB phosphorylation in mice hippocampus: reversal by procyanidins extracted from the lotus seedpod. Food Funct. 2014, 5, 2289-2297.
19. Chang, W. T., Shao, Z. H., Yin, J. J., Mehendale, S. et al., Comparative effects of flavonoids on oxidant scavenging and ischemia-reperfusion injury in cardiomyocytes. Eur. J. Pharmacol. 2007, 566, 58-66.
20. Arola-Arnal, A., Oms-Oliu, G., Crescenti, A., del Bas, J. M. et al., Distribution of grape seed flavanols and their metabolites in pregnant rats and their fetuses. Mol. Nutr. Food Res. 2013, 57, 1741-1752.
21. Sun, M., Zhao, Y., Gu, Y., Xu, C., Anti-inflammatory mechanism of taurine against ischemic stroke is related to down-regulation of PARP and NF-kappaB. Amino Acids 2012, 42, 1735-1747.
22. Liu, Y., Tang, G., Li, Y., Wang, Y. et al., Metformin attenuates blood-brain barrier disruption in mice following middle cerebral artery occlusion. J. Neuroinflammation 2014, 11, 1-12.
23. Mdzinarishvili, A., Kiewert, C., Kumar, V., Hillert, M. et al., Bilobalide prevents ischemia-induced edema formation in vitro and in vivo. Neuroscience 2007, 144, 217-222.
24. Chen, J., Li, Y., Wang, L., Zhang, Z. et al., Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001, 32, 1005-1011.
25. Elstner, E. F., Heupel, A., Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal. Biochem. 1976, 70, 616-620.
26. Sumner, J. B., Dounce, A. L., Crystalline catalase. Science 1937, 85, 366-367.
27. Ohkawa, H., Ohishi, N., Yagi, K., Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95, 351-358.
28. Lu, J., Shen, Y., Qian, H. Y., Liu, L. J. et al., Effects of mild hypothermia on the ROS and expression of caspase-3 mRNA and LC3 of hippocampus nerve cells in rats after cardiopulmonary resuscitation. World J. Emerg. Med. 2014, 5, 298-305.
29. Matsumoto, S., Friberg, H., Ferrand-Drake, M., Wieloch, T., Blockade of the mitochondrial permeability transition pore diminishes infarct size in the rat after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 1999, 19, 736-741.
30. Das, J., Ghosh, J., Roy, A., Sil, P. C., Mangiferin exerts hepatoprotective activity against D-galactosamine induced acute toxicity and oxidative/nitrosative stress via Nrf2-NFkappaB pathways. Toxicol. Appl. Pharmacol. 2012, 260, 35-47.
31. Jain, A. K., Jaiswal, A. K., Phosphorylation of tyrosine 568 controls nuclear export of Nrf2. J. Biol. Chem. 2006, 281, 12132-12142.
32. Nunez-Figueredo, Y., Pardo-Andreu, G. L., Ramirez-Sanchez, J., Delgado-Hernandez, R. et al., Antioxidant effects of JM-20 on rat brain mitochondria and synaptosomes: mitoprotection against Ca(2)(+)-induced mitochondrial impairment. Brain Res. Bull. 2014, 109, 68-76.
33. Choi, I. Y., Ju, C., Jalin, A. M. A. A., Lee, D. I. et al., Activation of cannabinoid CB2 receptor-mediated AMPK/CREB pathway reduces cerebral ischemic injury. Am. J. Pathol. 2013, 182, 928-939.
34. Bao, L., Cai, X., Zhang, Z., Li, Y., Grape seed procyanidin B2 ameliorates mitochondrial dysfunction and inhibits apoptosis via the AMP-activated protein kinase-silent mating type information regulation 2 homologue 1-PPARgamma co-activator-1alpha axis in rat mesangial cells under high-dose glucosamine. Br. J. Nutr. 2015, 113, 35-44.
35. Zhang, Z., Li, B. Y., Li, X. L., Cheng, M. et al., Proteomic analysis of kidney and protective effects of grape seed procyanidin B2 in db/db mice indicate MFG-E8 as a key molecule in the development of diabetic nephropathy. Biochim. Biophys. Acta 2013, 1832, 805-816.
36. Houde, V., Grenier, D., Chandad, F., Protective effects of grape seed proanthocyanidins against oxidative stress induced by lipopolysaccharides of periodontopathogens. J. Periodontol. 2006, 77, 1371-1379.
37. Alfieri, A., Srivastava, S., Siow, R. C., Modo, M. et al., Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke. J. Physiol. 2011, 589, 4125-4136.
38. Robert, A. M., Tixier, J. M., Robert, L., Legeais, J. M. et al., Effect of procyanidolic oligomers on the permeability of the blood-brain barrier. Pathol. Biol. 2001, 49, 298-304.
39. Zhang, L., Schallert, T., Zhang, Z. G., Jiang, Q. et al., A test for detecting long-term sensorimotor dysfunction in the mouse after focal cerebral ischemia. J. Neurosci. Methods 2002, 117, 207-214.
40. Cuello, A. C., Experimental neurotrophic factor therapy leads to cortical synaptic remodeling and compensates for behavioral deficits. J. Psychiatry Neurosci. 1997, 22, 46-55.
41. Schallert, T., Fleming, S. M., Leasure, J. L., Tillerson, J. L., Bland, S. T., CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39, 777-787.
42. Wu, S., Yue, Y., Tian, H., Tao, L. et al., Tramiprosate protects neurons against ischemic stroke by disrupting the interaction between PSD95 and nNOS. Neuropharmacology 2014, 83, 107-117.
43. Liu, T., Zhang, T., Yu, H., Shen, H., Xia, W., Adjudin protects against cerebral ischemia reperfusion injury by inhibition of neuroinflammation and blood-brain barrier disruption. J. Neuroinflammation 2014, 11, 1-10.
44. Brown, R. C., Davis, T. P., Calcium modulation of adherens and tight junction function: a potential mechanism for blood-brain barrier disruption after stroke. Stroke 2002, 33, 1706-1711.
45. Ohtsuki, S., Terasaki, T., Contribution of carrier-mediated transport systems to the blood-brain barrier as a supporting and protecting interface for the brain; importance for CNS drug discovery and development. Pharm. Res. 2007, 24, 1745-1758.
46. Bauer, H. C., Krizbai, I. A., Bauer, H., Traweger, A., "You Shall Not Pass"-tight junctions of the blood brain barrier. Front. Neurosci. 2014, 8, 1-21.
47. McCaffrey, G., Seelbach, M. J., Staatz, W. D., Nametz, N. et al., Occludin oligomeric assembly at tight junctions of the blood-brain barrier is disrupted by peripheral inflammatory hyperalgesia. J. Neurochem. 2008, 106, 2395-2409.
48. Bazzoni, G., Dejana, E., Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 2004, 84, 869-901.
49. Schreibelt, G., Kooij, G., Reijerkerk, A., van Doorn, R. et al., Reactive oxygen species alter brain endothelial tight junction dynamics via RhoA, PI3 kinase, and PKB signaling. FASEB J. 2007, 21, 3666-3676.
50. Alluri, H., Clayton, R. P., Sawant, D., Stagg, H. W. et al., Mitochondrial mechanisms that regulate blood-brain barrier endothelial cell hyperpermeability following oxygen-glucose deprivation and reoxygenation. FASEB J. 2013, 27, 725.
51. Musch, M. W., Walsh-Reitz, M. M., Chang, E. B., Roles of ZO-1, occludin, and actin in oxidant-induced barrier disruption. Am. J. Physiol.-Gastr. L. 2006, 290, G222-G231.
52. Calabrese, V., Cornelius, C., Dinkova-Kostova, A. T., Iavicoli, I. et al., Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity. Biochim. Biophys. Acta 2012, 1822, 753-783.
53. Yang, C. H., Zhang, X. J., Fan, H. G., Liu, Y., Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res. 2009, 1282, 133-141.
54. Rodriguez-Ramiro, I., Ramos, S., Bravo, L., Goya, L. et al., Procyanidin B2 induces Nrf2 translocation and glutathione S-transferase P1 expression via ERKs and p38-MAPK pathways and protect human colonic cells against oxidative stress. Eur. J. Nutr. 2012, 51, 881-892.
55. Yang, C., Zhang, X., Fan, H., Liu, Y., Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res. 2009, 1282, 133-141.