Therapeutic angiogenesis after ischemic stroke: Chinese medicines, bone marrow stromal cells (bmscs) and their combinational treatment

American Journal of Chinese Medicine

Volumn 42, Issue 1, 2014, Pages 61-77

  Zhang, Qian ^a   Zhao, Yong Hua ^a  

^a MACAU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Macao)

Author keywords

Angiogenesis; Bone Marrow Stromal Cells; Chinese Medicines; Combination Treatment; Ischemic Stroke; Review

Indexed keywords

8 O ACETYL SHANZHISIDE METHYL ESTER; ASTRAGALOSIDE IV; BUYANGHUANWU DECOCTION; CATALPOL; CHEMOKINE RECEPTOR CXCR4; CORNEL IRIDOID GLYCOSIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FERULIC ACID; FIBROBLAST GROWTH FACTOR 2; GINSENOSIDE RG 1; HYPOXIA INDUCIBLE FACTOR 1; IRIDOID; MATRIX METALLOPROTEINASE; NAOMAITONG; PLANT MEDICINAL PRODUCT; PLATELET DERIVED GROWTH FACTOR; PUERARIN; RESVERATROL; SHANZHISIDE METHYL ESTER; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BONE MARROW; BONE MARROW STROMAL CELL; BRAIN ISCHEMIA; CELL MIGRATION; CELL SURVIVAL; CHINESE MEDICINE; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; MORPHOGENESIS; NERVOUS SYSTEM DEVELOPMENT; PROTEIN EXPRESSION; STEM CELL TRANSPLANTATION; STROMA CELL; SYNAPTOGENESIS; UPREGULATION;

ALLOGRAFTS; ANIMALS; BONE MARROW TRANSPLANTATION; BRAIN; COMBINED MODALITY THERAPY; COUMARIC ACIDS; DRUGS, CHINESE HERBAL; GINSENOSIDES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; IRIDOID GLUCOSIDES; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE REGENERATION; NEUROGENESIS; NITRIC OXIDE SYNTHASE TYPE III; PHYTOTHERAPY; STROKE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84893518341     PISSN: 0192415X     EISSN: None     Source Type: Journal    
DOI: 10.1142/S0192415X14500049     Document Type: Article

References (100)

1. Adams, H.P., T.G. Brott, A.J. Furlan, C.R. Gomez, J. Grotta, C.M. Helgason, T. Kwiatkowski, P.D. Lyden, J.R. Marler, J. Torner, W. Feinberg, M. Mayberg and W. Thies. Guidelines for thrombolytic therapy for acute stroke: a supplement to the guidelines for the management of patients with acute ischemic stroke: a statement for healthcare professionals from a Special Writing Group of the Stroke. Circulation 94: 1167-1174, 1996.
2. Adams, H.P., R.J. Adams, T. Brott, G.J. del Zoppo, A. Furlan, L.B. Goldstein, R.L. Grubb, R. Higashida, C. Kidwell, T.G. Kwiatkowski, J.R. Marler and G.J. Hademenos. Guidelines for the early management of patients with ischemic stroke: ascientificstatement from the Stroke Council of the American Stroke Association. Stroke 34: 1056-1083, 2003.
3. Arai, K., G. Jin, D. Navaratna and E.H. Lo. Brain angiogenesis in developmental and pathological processes: neurovascular injury and angiogenic recovery after stroke. FEBS J. 276: 4644-4652, 2009.
4. Babaei, S., K. Teichert-Kuliszewska, Q. Zhang, N. Jones, D.J. Dument and D.J. Stewart. Angiogenic actions of angiopoietin-1 require endothelium-derived nitric oxide. Am. J. Pathol. 162: 1927-1936, 2003.
5. Bacigaluppi, M., S. Pluchino, L. Peruzzotti-Jametti, E. Kilic, U. Kilic, G. Salani, E. Brambilla, M.J. West, G. Comi, G. Martino and D.M. Hermann. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132: 2239-2251, 2009.
6. Bang, O.Y., J.S. Lee, P.H. Lee and G. Lee. Autologous mesenchymal stem cell transplantation in stroke patients. Ann. Neurol. 57: 874-882, 2005.
7. Barone, E., V. Calabrese and C. Mancuso. Ferulic acid and its therapeutic potential as a hormetin for age-related diseases. Biogerontology 10: 97-108, 2009.
8. Beck, H. and K.H. Plate. Angiogenesis after cerebral ischemia. Acta Neuropathol. 117: 481-496, 2009.
9. Bergers, G. and L.E. Benjamin. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 3: 401-410, 2003.
10. Cai, G.X. and B.Y. Liu. Effect of ultra-micronized Buyang Huanwu Decoction on neurological function, quality of life, and serum vascular endothelial growth factor in patients convalescent from cerebral infarction. Zhongguo Wei Zhong Bing Jijiu Yi Xue 22: 591-594, 2010.
11. Cai, G.X., B.Y. Liu, W. Liu, X.H. Tan, J.H. Rong, X.M. Chen, L. Tong and J.G. Shen. Buyang Huanwu Decoction can improve recovery of neurological function, reduce infarction volume, stimulate neural proliferation and modulate VEGF and Flk1 expressions in transient focal cerebral ischaemic rat brains. J. Ethnopharmacol. 113: 292-299, 2007.
12. Cao, J.Z., G.T. Yang and S.S. Liu. Effect of puerarin on apoptosis and the expression of c-fos protein in the hippocampus CA1 area during cerebral ischemia-reperfusion. Chin. J. Integr. Tradit. West. Med. Intens. Crit. Care 9: 238-240, 2002.
13. Chan, L.S., P.Y. Yue, N.K. Mak and R.N. Wong. Role of microRNA-214 in ginsenoside-Rg1-induced angiogenesis. Eur. J. Pharm. Sci. 38: 370-377, 2009.
14. Chang, L.P., Q.Y. Zhang, J.K. Han, C. Wei and Z.H. Jia. Experimental study on the interventional effects of Tongxinluo supermicropowder on angiogenesis of ischemic stroke rat. Chin. Pharm. Bull. 28: 1015-1018, 2012.
15. Chen, Y.J. Effect of Buyang Huanwu Decoction on serum vascular endothelial growthfactor level of the patients with acute cerebral infarction. J. Liaoning Univ. Tradit. Chin. Med. 11: 113-115, 2009.
16. Chen, J., Y. Li, M. Katakowski, X. Chen, L. Wang, D. Lu, M. Lu, S.C. Gautam and M. Chopp. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J. Neurosci. Res. 73: 778-786, 2003a.
17. Chen, J., Z.G. Zhang, Y. Li, L. Wang, Y.X. Xu, S.C. Gautam, M. Lu, Z. Zhu and M. Chopp. Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats. Circ. Res. 92: 692-699, 2003b.
18. Chen, J., Y. Li, R. Zhang, M. Katakowski, S.C. Gautam, Y. Xu, M. Lu, Z. Zhang and M. Chopp. Combination therapy of stroke in rats with a nitric oxide donor and human bone marrow stromal cells enhances angiogenesis and neurogenesis. Brain Res. 1005: 21-28, 2004.
19. Deng, Y.B., W.B. Ye, Z.Z. Hu, Y. Yan, Y. Wang, B.F. Takon, G.Q. Zhou and Y.F. Zhou. Intravenously administered BMSCs reduce neuronal apoptosis and promote neuronal proliferation through the release of VEGF after stroke in rats. Neurol. Res. 32: 148-156, 2010.
20. Dong, W.P., N.L. Li, D.K. Gao, H.N. Zhen, X. Zhang and F.F. Li. Resveratrol attenuates ischemic brain damage in the delayed phase after stroke and induces messenger RNA and protein express for angiogenic factors. J. Vasc. Surg. 48: 709-714, 2008.
21. Ferrara, N., K. Houck, L. Jakeman and D.W. Leung. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr. Rev. 13: 18-32, 1992.
22. Folkman, J. Tumour angiogenesis: therapeutic implications. N. Engl. J. Med. 285: 1182-1186, 1971.
23. Fukuda, S., S. Kaga, L. Zhan, D. Bagchi, D.K. Das, A. Bertelli and N. Maulik. Resveratrol ameliorates myocardial damage by inducing vascular endothelial growth factor-angiogenesis and tyrosine kinase receptor Flk-1. Cell Biochem. Biophys. 44: 43-49, 2006.
24. Gao, J.F., J.S. Li, Y.L. Zhou and K. Liu. Effects of Naomaitong Recipe on expressions of nuclear factor-kappaB and nitric-oxide synthases in brain tissue after focal cerebral ischemia reperfusion in aged rats. Zhong Xi Yi Jie He Xuebao 4: 530-534, 2006.
25. Gu, J., C.Q. Wang, H.H. Fan, H.Y. Ding, X.L. Xie, Y.M. Xu, B.Y. Wang and D.J. Huang. Effects of resveratrol on endothelial progenitor cells and their contributions to reendothelialization in intima-injured rats. J. Cardiovasc. Pharmacol. 47: 711-721, 2006.
26. Guo, J.W., J.Y. Li and Y. Huang. Effects of Chinese medicine for regulating sea of blood in brain combined with bone marrow stromal stem cell transplantation on angiogenesis in ischemic brain tissue of rats. J. Chin. Integr. Med. 7: 763-768, 2009.
27. Guo, J.W., C. Chen, Y. Huang and B. Li. Combinatorial effects of Naomai Yihao capsules and vascular endothelial growth factor gene-transfected bone marrow mesenchymal stem cells on angiogenesis in cerebral ischemic tissues in rats. J. Tradit. Chin. Med. 32: 87-92, 2012.
28. Guo, Y., Y.M. Wei and S.X. Liu. Research progress on application of astragalus in cerebrovascular diseases. Shanxi J. Tradit. Chin. Med. 23: 72-74, 2007.
29. Hashiguchi, A., S. Yano, M. Morioka, J. Hamada, Y. Ushio, Y. Takeuchi and K. Fukunaga. Up-regulation of endothelial nitric oxide synthase via phosphatidylinositol 3-kinase pathway contributes to ischemic tolerance in the CA1 subfield of gerbil hippocampus. J. Cereb. Blood Flow Metab. 24: 271-279, 2004.
30. Hayashi, T., K. Deguchi, S. Nagotani, H. Zhang, Y. Sehara, A. Tsuchiya and K. Abe. Cerebral ischemia and angiogenesis. Curr. Neurovasc. Res. 3: 119-129, 2006.
31. He, Z.G., G. Chen, H.F. Zhu, L. Ye and X.Y. Xu. Protective effects of puerarin on focal cerebral ischemia-reperfusion injury inrats. Chin. Pharm. Bull. 27: 1181-1182, 2011.
32. Hu, X.M., C.K. Yan and X.M. Hu. Effects of ginsenoside Rg1 on apoptosis induced by transient focal cerebral ischemia in rats. Chin. J. Clin. Pharmacol. Ther. 11: 192-196, 2006.
33. Hu, X.Y., W.X. Wang, M.J. Yu, X.B. Liu, R.R. Wu, F. Gao, X. Huang, J. Cao, X.J. Xie and J.A. Wang. Tongxinluo promotes mesenchymal stem cell tube formation in vitro. J. Zhejiang Univ. Sci. B 12: 644-651, 2011.
34. Jaquet, K., K. Krause, M. Tawakol-Khodai, S. Geidel and K.H. Kuck. Erythropoietin and VEGF exhibit equal angiogenic potential. Microvasc. Res. 64: 326-333, 2002.
35. Jiang, X., S. Namura and I. Nagala. Matrix metalloproteinase inhibitor KB-R7795 attenuates brain damage resulting from permanent focal cerebral ischemia in mice. Neuroscience 305: 41-44, 2001.
36. Jiang, W.L., S.P. Zhang, H.B. Zhu and J. Hou. Effect of 8-O-acetyl shanzhisidemethylester increases angiogenesis and improves functional recovery after stroke. Basic Clin. Pharm. Toxicol. 108: 21-27, 2010.
37. Jin, X.P., D.P. Hu, S.Z. Chen, Y.G. Du and J.M. Yu. Research on effect of puerarin on serum nitric oxide, malondialdehyde, superoxide dismutase in acute cerebral infarction. Chin. J. Integr. Tradit. West. Med. Intens. Crit. Care 8: 309-310, 2001.
38. Kaga, S., L. Zhan, M. Matsumoto and N. Maulik. Resveratrol enhances neovascularization in the infarcted rat myocardium through the induction of thioredoxin-1, heme oxygenase-1 and vascular endothelial growth factor. J. Mol. Cell. Cardiol. 39: 813-822, 2005.
39. Kelly, S., T.M. Bliss, A.K. Shah, G.H. Sun, M. Ma, W.C. Foo, J. Masel, M.A. Yenari, I.L. Weissman, N. Uchida, T. Palmer and G.K. Steinberg. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc. Natl. Acad. Sci. USA 101: 11839-11844, 2004.
40. Krupinski, J., J. Kaluza, P. Kumar, S. Kumar and J.M. Wang. Role of angiogenesis in patients with cerebral ischemic stroke. Stroke 25: 1794-1798, 1994.
41. Leung, K.W., H.M. Ng, M.K. Tang, C.C. Wong, R.N. Wong and A.S. Wong. Ginsenoside-Rg1 mediates a hypoxia-independent upregulation of hypoxia-inducible factor-1 to promote angiogenesis. Angiogenesis 14: 515-522, 2011.
42. Leung, K.W., Y.L. Pon, R.N. Wong and A.S. Wong. Ginsenoside-Rg1 induces vascular endothelial growth factor expression through the glucocorticoid receptor-related phosphatidylinositol 3-kinase/Akt and beta-catenin/T-cell factor-dependent pathway in human endothelial cells. J. Biol. Chem. 281: 36280-36288, 2006.
43. Li, C.Y., L. Li, Y.H. Li, H.X. Ai and L. Zhang. Effects of extract from Cornusofficinalis on nitric oxide and NF-B in cortex of cerebral infarction rat model. Chin. J. Chin. Mat. Med. 30: 1667-1670, 2005.
44. Li, J.S., K. Liu, M.H. Wang, J.X. Liu, Y.W. Zhao and Z.G. Liu. Modulation effect of Naomaitong on gelatinase system after cerebral ischemia/reperfusion in rats. Zhongguo Zhong Xi Yi Jie He Zazhi 26: 14-17, 2006.
45. Li, J.S., J.X. Liu, Y.S. Tian, W.H. Ren, X.F. Zhang and D.C. Wang. Effects of Naomaitong combined with mobilization of bone marrow mesenchymal stem cells on neuron apoptosis and expressions of Fas, FasL and caspase-3 proteins in rats with cerebral ischemia. J. Chin. Integr. Med. 7: 860-867, 2009.
46. Li, W.Y., Y. Wang, M.Q. Li and X.J. Tong. The effect of Astragaloside IV on angiogenesis in hippocampal region after cerebral ischemia-reperfusion in rats. Med. Recap. 17: 1727-1729, 2011.
47. Liang, Q.B., Y.A. Zou, X.L. Zhang, Q. Xue, H.J. Shi and R.Y. Li. Effects of Kangnao Liquid II on VEGF, Ang-1 and MVD of rats with focal cerebral ischemia-reperfusion injury. Chin. Pharm. 22: 1740-1743, 2011a.
48. Liang, S.L., B. Xu and Y.Y. Zhang. The effect of Astragalus injection on the expression of HIF-1 and VEGF in the cerebral tissue after focal cerebral ischemia. Prev. Treat. Cardiol. Cereb. Vasc. Dis. 11: 21-23, 2011b.
49. Lin, C.M., J.H. Chiu, I.H. Wu, B.W. Wang, C.M. Pan and Y.H. Chen. Ferulic acid augments angiogenesis via VEGF, PDGF and HIF-1. J. Nutr. Biochem. 21: 627-633, 2010.
50. Liu, K., J.S. Li, X.K. Yang, J.F. Gao, Y.L. Zhou, Y.W. Zhao, Z.G. Liu and J.X. Liu. Influences of Naomaitong on angiogenesis and Flk-1 expression in agedrats after cerebral ischemiareperfusion. J. Beijing Univ. Tradit. Chin. Med. 34: 42-47, 2011.
51. Manoonkitiwongsa, P.S., C. Jackson-Friedman, P.J. McMillan, R.L. Schultz and P.D. Lyden. Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J. Cereb. Blood Flow Metab. 21: 1223-1231, 2001.
52. Mei, A.N., J. Wang, Y.Q. Zhan, S.M. Zhang and Y.P. Jiang. Effect of Tongxinluo capsules on cortex angiogenesis and neuron apoptosis in rats with focal cerebral ischemia. J. Pract. Med. 22: 267-270, 2006.
53. Mora-Lee, S., M.S. Sirerol-Piquer, M. Gutiérrez-Pérez, U. Gomez-Pinedo, V.D. Roobrouck, T. López, M. Casado-Nieto, G. Abizanda, M.T. Rabena, C. Verfaille, F. Prósper and J.M. García-Verdugo. Therapeutic effects of hMAPC and hMSC transplantation after stroke in mice. PLoS One 7: e43683, 2012.
54. Nakashima, M.N., K. Ajiki, K. Nakashima and M. Takahashi. Possible role of nitric oxide in anxiety following transient cerebral ischemia in mice. J. Pharmacol. Sci. 91: 47-52, 2003.
55. Onteniente, B. and J. Polentes. Regenerative medicine for stroke-are we there yet? Cerebrovasc. Dis. 31: 544-551, 2011.
56. Pavlichenko, N., I. Sokolova, S. Vijde, E. Shvedova, G. Alexandrov, P. Krouglyakov, O. Fedotova, E.G. Gilerovich, D.G. Polyntsev and V.A. Otellin. Mesenchymal stem cells transplantation could be beneficial for treatment of experimental ischemic stroke in rats. Brain Res. 1233: 203-213, 2008.
57. Perou, C.M., T. Sørlie, M.B. Eisen, M. van de Rijn, S.S. Jeffrey, C.A. Rees, J.R. Pollack, D.T. Ross, H. Johnsen, L.A. Akslen, O. Fluge, A. Pergamenschikov, C. Williams, S.X. Zhu, P.E. Lønning, A.L. Børresen-Dale, P.O. Brown and D. Botstein. Molecular portraits of human breast tumours. Nature 406: 747-752, 2000.
58. Ramar, M., B. Manikandan, T. Raman, A. Priyadarsini, S. Palanisamy, M. Velayudam, A. Munusamy, N. Marimuthu Prabhu and B. Vaseeharan. Protective effect of ferulic acid and resveratrol against alloxan-induced diabetes in mice. Eur. J. Pharmacol. 690: 226-235, 2012.
59. Ren, X.Q., J.S. Li, Y.M. Feng and Y.Q. Lu. Neuro-protective effect of naomaitong to brain damage after focal cerebral ischemia reperfusion (I/R) in the aged rats. Zhongguo Zhong Yao Za Zhi 29: 66-70, 2004.
60. Romanic, A.M. and J.A. Madri. Extracellular matrix degrading proteinases in the nervous system. Brain Pathol. 14: 1455-1561, 1994.
61. Romanic, A.M., R.F. White, A.J. Arleth E.H. Ohlstein and F.C. Barone. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats. Inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29: 1020-1030, 1998.
62. Salvucci, O., L. Yao, S. Villalba, A. Sajewicz, S. Pittaluga and G. Tosato. Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1. Blood 99: 2703-2711, 2002.
63. Savitz, S.I., M. Chopp, R. Deans, S.T. Carmichael, D. Phinney and L. Wechsler. Stem cell therapy as an emerging paradigm for stroke (STEPS) II. Stroke 42: 825-829, 2011.
64. Seevinck, P.R., L.H. Deddens and R.M. Dijkhuizen. Magnetic resonance imaging of brain angiogenesis after stroke. Angiogenesis 13: 101-111, 2010.
65. Sengupta, S., S.A. Toh, L.A. Sellers, J.N. Skepper, P. Koolwijk, H.W. Leung, H.W. Yeung, R.N. Wong, R. Sasisekharan and T.P. Fan. Modulating angiogenesis: the yin and the yang in ginseng. Circulation 110: 1219-1225, 2004.
66. Shi, A.W., N. Gu, X.M. Liu, X. Wang and Y.Z. Peng. Ginsenoside Rg1 enhances endothelial progenitor cell angiogenic potency and prevents senescence in vitro. J. Int. Med. Res. 39: 1306-1318, 2011.
67. Simão, F., A.S. Pagnussat, J.H. Seo, D. Navaratna, W. Leung, J. Lok, S. Guo, C. Waeber, C.G. Salbego and E.H. Lo. Pro-angiogenic effects of resveratrol in brain endothelial cells: nitric oxide-mediated regulation of vascular endothelial growth factor and metalloproteinases. J. Cereb. Blood Flow Metab. 32: 884-895, 2012.
68. Slevin, M., P. Kumar, J. Gaffney, S. Kumar and J. Krupinski. Can angiogenesis be exploited to improve stroke outcome? Mechanisms and therapeutic potential. Clin. Sci. (Lond.) 111: 171-183, 2006.
69. Suárez-Monteagudo, C., P. Hernández-Ramírez, L. Alvarez-González, I. García-Maeso, K. de la Cuétara-Bernal, L. Castillo-Díaz, M.L. Bringas-Vega, G. Martínez-Aching, L.M. Morales-Chacón, M.M. Báez-Martín, C. Sánchez- Catasús, M. Carballo-Barreda, R. Rodríguez-Rojas, L. Gómez-Fernández, E. Alberti-Amador, C. Macías-Abraham, E.D. Balea, L.C. Rosales, L. Del Valle Pérez, B.B. Ferrer, R.M. González and J.A. Bergado. Autologous bone marrow stem cell neurotransplantation in stroke patients. An open study. Restor. Neurol. Neurosci. 27: 151-161, 2009.
70. Suhantja, A. and H. Hofman. Role of growth factors and their receptors in proliferation of mierovaseular endothelial cell. Mierosc. Res. Tech. 60: 70-77, 2003.
71. Sultana, R. Ferulic acid ethyl ester as a potential therapy in neurodegenerative disorders. Biochim. Biophys. Acta 1822: 748-752, 2012.
72. Tang, B., Y. Qu, D. Wang and D. Mu. Targeting hypoxia inducible factor-1: a novel mechanism of ginsenoside Rg1 for brain repair after hypoxia/ischemia brain damage. CNS Neurol. Disord. Drug Targets 10: 235-238, 2011.
73. Wang, B.H. and J.P. Ou-Yang. Pharmacological actions of sodium ferulate in cardiovascular system. Cardiovasc. Dmg Rev. 23: 161-172, 2005.
74. Wang, D.J., Q.Y. Li, S.J. Xu and N. Zeng. Effect of ginsenoside Rg1 on angiogenesis after neonatal hypoxia ischemia brain damage in rats. Sichuan Da Xue Xue Bao Yi Xue Ban 42: 503-507, 2011a.
75. Wang, Y., W.Y. Li, M.Q. Li, Y.Q. Guan, X.B. Zhang and W.Z. Lv. Effects of astragaloside IV combined with bone mesenchymal stem cell transplantation on angiogenesis after cerebral ischemia-reperfusion in rats. Anat. Res. 33: 323-326, 2011b.
76. Wang, X.D., T.X. Gu, E.Y. Shi, C.M. Lu and C. Wang. Effect and mechanism of panaxoside Rg1 on neovascularization in myocardial infarction rats. Chin. J. Integr. Med. 16: 162-166, 2010.
77. Wang, Y., Y. Deng and G.Q. Zhou. SDF-1alpha/CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res. 1195: 104-112, 2008.
78. World Health Organization. World Health Statistics 2008.
79. WHO Library Cataloguing-in-Publication Data. 40-51, 2008.
80. Xu, X.L. and S.L. Wang. Advances in clinical application of Astragalus preparation. J. Modern Clin. Med. 2: 138-140, 2006.
81. Yang, Y.X., L.Z. Ye, G. He, X.Y. Liang and Y.W. Mei. Effects of Tongxinluo on VEGF expression and angiogenesis of rats with cerebral infarction. Her. Med. 28: 182-184, 2009.
82. Yang, N., P. Chen, Z. Tao, N. Zhou, X. Gong, Z. Xu, M. Zhang, D. Zhang, B. Chen, Z. Tao and Z. Yang. Beneficial effects of ginsenoside-Rg1 on ischemia-induced angiogenesis in diabetic mice. Acta Biochim. Biophys. Sin. 44: 999-1005, 2012.
83. Yao, R.Q., L. Zhang, W. Wang and L. Li. Cornel iridoid glycoside promotes neurogenesis and angiogenesis and improves neurological function after focal cerebral ischemia in rats. Brain Res. Bull. 79: 69-76, 2009.
84. Yi, J.H., X.P. Huang, Y. Chen, Z.Y. Luo and C.C. Zhong. Studies on the iridoidglucosides of the root of Lamiophlomisrotata (Benth) Kudo, a medicinal plant in Tibet. Acta. Pharm. Sin. 32: 360-362, 1997.
85. Yin, Y.H. and X.G. Wu. Study on effect of Buyang Huanwu Decoction on expression of VEGF and Ang-1 in gerbils with cerebral ischemia-reperfusion. J. Clin. Exp. Med. 11: 487-491, 2012.
86. Yin, H., Z. Liu, F. Li, M. Ni, B. Wang, Y. Qiao, X. Xu, M. Zhang, J. Zhang, H. Lu and Y. Zhang. Ginsenoside-Rg1 enhances angiogenesis and ameliorates ventricular remodeling in a rat model of myocardial infarction. J. Mol. Med. (Berl.) 89: 363-375, 2011.
87. Yu, X.P., C.Q. Zhang, R.A. Qin, D.S. Zhou, H. Hu and X.F. Gao. Research on effect of endothelial growth factor of compound Salvia tablet on rats with cerebral ischemia. Chin. Arch. Tradit. Chin. Med. 28: 1145-1148, 2011.
88. Yuan, G.Q., Y.L. Wu and Z.H. Jia. Experimental study on effect of Tongxinluo on nerve cell apoptosis after cerebral ischemia in middle cerebral arterial obstructive model rats. Chin. J. Integr. Tradit. West. Med. 27: 720-723, 2007.
89. Zacharek, A., J. Chen, X. Cui, A. Li, Y. Li, C. Roberts, Y. Feng, Q. Gao and M. Chopp. Angiopoietin1= Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J. Cereb. Blood Flow Metab. 27: 1684-1691, 2007.
90. Zhang, C., Y. Li, J. Chen, Q. Gao, A. Zacharek, A. Kapke and M. Chopp. Bone marrow stromal cells upregulate expression of bone morphogenetic proteins 2 and 4, gap junction protein connexin-43 and synaptophysin after stroke in rats. Neuroscience 141: 687-695, 2006.
91. Zhang, K., L. Zhu and M. Fan. Oxygen, a key factor regulating cell behavior during neurogenesis and cerebral diseases. Front. Mol. Neurosci. 4: 5, 2011a.
92. Zhang, L., Q. Liu, L. Lu, X.P. Zhao, X.M. Gao and Y. Wang. Astragaloside IV stimulates angiogenesis and increases hypoxia-inducible factor-1 accumulation via phosphatidylinositol 3-kinase/Akt pathway. J. Pharmacol. Exp. Ther. 338: 485-491, 2011b.
93. Zhang, Y.K., X.Y. Han and Z.Y. Che. Effects of buyanghuanwu tang combined with bone marrow mesenchymal stem cell transplantation on the expression of VEGF and Ki-67 in the brain tissue of the cerebral ischemia-reperfusion model rat. J. Tradit. Chin. Med. 30: 278-282, 2010.
94. Zhang, Z and M. Chopp. Vascular endothelial growth factor and angiopoietins in focal cerebral ischemia. Trends Cardiovasc. Med. 12: 62-66, 2002.
95. Zhang, L., C.Y. Li, L. Zhao, W. Wang, L. Zhang and L. Li. Effects of cornel iridoid glycoside on nervous function and neuron damage in focal cerebral ischemic rats. Chin. J. Rehabil. Theory Pract. 13: 201-202, 2007.
96. Zhou, Q., W.J. Liao, W.T. Yang, X.Q. Hu, M.G. Cheng, L.F. Ren and B. Bi. Effects of sodium ferulate on neurological function and angiogenesis after reperfusion of focal cerebral ischemia in rats. Chin. J. Rehabil. Med. 21: 200-203, 2006.
97. Zhou, T.Z. and J.D. Liu. Effect of Puerarin injection on neurologic impairment and hemorrheology in patients with cerebral infarction. Chin. J. Pract. Nerv. Dis. 14: 45-46, 2011.
98. Zhou, X., L.H. Sun, Q. Fang and W.H. Shen. Effects of sodium ferulate on the function of platelet and endothelial cell in patients with acute cerebral infarction. Suzhou Univ. J. Med. Sci. 31: 304-306, 2011.
99. Zhu, Y.L. and W.Q. Yang. Effects of compound tablet of Red Sage root on the expression of VEGF in brain of rat during chronic cerebral ischemia. Chin. J. Pract. Nerv. Dis. 10: 26-27, 2007.
100. Zhu, H.F., D. Wan, Y. Luo, J.L. Zhou, L. Chen and X.Y. Xu. Catalpol increases brain angiogenesis and up-regulates VEGF and EPO in the rat after permanent middle cerebral artery occlusion. Int. J. Biol. Sci. 6: 443-453, 2010.