Transplantation of Flk-1+ human bone marrow-derived mesenchymal stem cells promotes angiogenesis and neurogenesis after cerebral ischemia in rats

European Journal of Neuroscience

Volumn 34, Issue 1, 2011, Pages 87-98

  Bao, Xinjie ^a   Feng, Ming ^a   Wei, Junji ^a   Han, Qin ^b   Zhao, Hao ^a   Li, Guilin ^a   Zhu, Zhaohui ^a   Xing, Haiqun ^a   An, Yihua ^c   Qin, Chuan ^d   Zhao, Robert Chunhua ^b   Wang, Renzhi ^a  

^a PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^b INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^c Beijing Institute of Neurological Surgery   (China)

^d INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

Author keywords

Apoptosis; Brain ischemia; Regeneration; Stem cell

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL TRANSPLANTATION; BRAIN BLOOD FLOW; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN METABOLISM; BRAIN PERFUSION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GLIA CELL; GLUCOSE METABOLISM; HIPPOCAMPUS; HUMAN; HUMAN CELL; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SUBVENTRICULAR ZONE;

ANIMALS; BEHAVIOR, ANIMAL; BONE MARROW CELLS; BRAIN ISCHEMIA; FEMALE; GLUCOSE; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROGENESIS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79960003566     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07733.x     Document Type: Article

References (39)

1. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z. & Lindvall, O. (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med., 8, 963-970.
2. Bang, O.Y., Lee, J.S., Lee, P.H. & Lee, G. (2005) Autologous mesenchymal stem cell transplantation in stroke patients. Ann. Neurol., 57, 874-882.
3. Beck, H. & Plate, K.H. (2009) Angiogenesis after cerebral ischemia. Acta Neuropathol., 117, 481-496.
4. Chen, X., Li, Y., Wang, L., Katakowski, M., Zhang, L., Chen, J., Xu, Y., Gautam, S.C. & Chopp, M. (2002) Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology, 22, 275-279.
5. Chen, J., Zhang, Z.G., Li, Y., Wang, L., Xu, Y.X., Gautam, S.C., Lu, M., Zhu, Z. & Chopp, M. (2003) Intravenous administration of human bone marrow stromal cells induces angiogenesis in the ischemic boundary zone after stroke in rats. Circ. Res., 92, 692-699.
6. Constantinescu, C.C. & Mukherjee, J. (2009) Performance evaluation of an Inveon PET preclinical scanner. Phys. Med. Biol., 54, 2885-2899.
7. Deng, W., Han, Q., Liao, L., Li, C., Ge, W., Zhao, Z., You, S., Deng, H. & Zhao, R.C. (2004) Allogeneic bone marrow-derived flk-1+Sca-1- mesenchymal stem cells leads to stable mixed chimerism and donor-specific tolerance. Exp. Hematol., 32, 861-867.
8. Fang, B., Shi, M., Liao, L., Yang, S., Liu, Y. & Zhao, R.C. (2003) Multiorgan engraftment and multilineage differentiation by human fetal bone marrow Flk1+/CD31-/CD34- progenitors. J. Hematother. Stem Cell Res., 12, 603-613.
9. Fang, B., Liao, L., Shi, M., Yang, S. & Zhao, R.C. (2004) Multipotency of Flk1+CD34- progenitors derived from human fetal bone marrow. J. Lab. Clin. Med., 143, 230-240.
10. Hacke, W., Kaste, M., Bluhmki, E., Brozman, M., Davalos, A., Guidetti, D., Larrue, V., Lees, K.R., Medeghri, Z., Machnig, T., Schneiger, D., Kummer, R., Wahlgren, N., Toni, D. & the ECASS Investigators. (2008) Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N. Engl. J. Med., 359, 1317-1329.
11. Hou, S., Wang, Y., Xu, M., Shen, D., Wang, J., Huang, F., Yu, Z. & Sun, F. (2008) Functional integration of newly generated neurons into striatum after cerebral ischemia in the adult rat brain. Stroke, 39, 2837-2844.
12. Irons, H., Lind, J.G., Wakade, C.G., Yu, G., Hadman, M., Carroll, J., Hess, D.C. & Borlongan, C.V. (2004) Intracerebral xenotransplantation of GFP mouse bone marrow stromal cells in intact and stroke rat brain: graft survival and immunologic response. Cell Transplant., 13, 283-294.
13. Kermani, P. & Hempstead, B. (2007) Brain-derived neurotrophic factor: a newly described mediator of angiogenesis. Trends Cardiovasc. Med., 17, 140-143.
14. Kim, S.S., Yoo, S.W., Park, T.S., Ahn, S.C., Jeong, H.S., Kim, J.W., Chang, D.Y., Cho, K.G., Kim, S.U., Huh, Y.B., Lee, J.E., Lee, S.Y., Lee, Y.D. & Suh-Kim, H.Y. (2008) Neural induction with neurogenin1 increases the therapeutic effects of mesenchymal stem cells in the ischemic brain. Stem Cells, 26, 2217-2228.
15. Krupinski, J., Kaluza, J., Kumar, P., Kumar, S. & Wang, J.M. (1994) Role of angiogenesis in patients with cerebral ischemic stroke. Stroke, 25, 1794-1798.
16. Lee, J.S., Hong, J.M., Moon, G.J., Lee, P.H., Ahn, Y.h., Bang, O.Y. & the STARTING Collaborators. (2010) A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells, 28, 1099-1106.
17. Leker, R.R., Toth, Z.E., Shahar, T., Cassiani-Ingoni, R., Szalayova, I., Key, S., Bratincsak, A. & Mezey, E. (2009) Transforming growth factor α induces angiogenesis and neurogenesis following stroke. Neuroscience, 163, 233-243.
18. Li, J., Zhu, H., Lu, S., Liu, Y., Li, Q., Ravenscroft, P., Xu, Y., Huang, L., Ma, C., Bezard, E., Zhao, R.C., Wang, R. & Qin, C. (2011) Migration and differentiation of human mesenchymal stem cells in the normal rat brain. Neurol. Res., 33, 84-92.
19. Liu, X., Zheng, S.X., Zhou, L.J. & Zhu, X.Z. (2000) Basic fibroblast growth factor up-regulates the expression of vascular endothelial growth factor in primary cultured rat astrocytes. Acta Pharmacol. Sin., 21, 19-22.
20. Liu, L., Sun, Z., Chen, B., Han, Q., Liao, L., Jia, M., Cao, Y., Ma, J., Sun, Q., Guo, M., Liu, Z., Ai, H. & Zhao, R.C. (2006) Ex vivo expansion and in vivo infusion of bone marrow-derived Flk-1+CD31-CD34- mesenchymal stem cells: feasibility and safety from monkey to human. Stem Cells Dev., 15, 349-357.
21. Liu, Y.P., Lang, B.T., Baskaya, M.K., Dempsey, R.J. & Vemuganti, R. (2009) The potential of neural stem cells to repair stroke-induced brain damage. Acta Neuropathol., 117, 469-480.
22. Nakano-Doi, A., Nakagomi, T., Fujikawa, M., Nakagomi, N., Kubo, S., Lu, S., Yoshikawa, H., Soma, T., Taguchi, A. & Matsuyama, T. (2010) Bone marrow mononuclear cells promote proliferation of endogenous neural stem cells through vascular niches after cerebral infarction. Stem Cells, 28, 1292-1302.
23. Nauta, A.J., Westerhuis, G., Kruisselbrink, A.B., Lurvink, E.G.A., Willemze, R. & Fibbe, W.E. (2006) Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood, 108, 2114-2120.
24. Schabitz, W.R., Steigleder, T., Cooper-Kuhn, C.M., Schwab, S., Sommer, C., Schneider, A. & Kuhn, H.G. (2007) Intravenous brain-derived neurotrophic factor enhances poststroke sensorimotor recovery and stimulates neurogenesis. Stroke, 38, 2165-2172.
25. Schott, R.J. & Morrow, L.A. (1993) Growth factors and angiogenesis. Cardiovasc. Res., 27, 1155-1161.
26. Shen, L.H., Li, Y., Chen, J., Cui, Y., Zhang, C., Kapke, A., Lu, M., Savant-Bhonsale, S. & Chopp, M. (2007a) One-year follow-up after bone marrow stromal cell treatment in middle-aged female rats with stroke. Stroke, 38, 2150-2156.
27. Shen, L.H., Li, Y., Chen, J., Zacharek, A., Gao, Q., Kapke, A., Lu, M., Raginski, K., Vanguri, P., Smith, A. & Chopp, M. (2007b) Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J. Cereb. Blood Flow Metab., 27, 6-13.
28. Shen, Q., Wang, Y., Kokovay, E., Lin, G., Chuang, S., Goderie, S.K., Roysam, B. & Temple, S. (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell, 3, 289-300.
29. Swanson, R.A., Morton, M.T., Tsao-Wu, G., Savalos, R.A., Davidson, C. & Sharp, F.R. (1990) A semiautomated method for measuring brain infarct volume. J. Cereb. Blood Flow Metab., 10, 290-293.
30. Taguchi, A., Soma, T., Tanaka, H., Kanda, T., Nishimura, H., Yoshikawa, H., Tsukamoto, Y., Iso, H., Fujimori, Y., Stern, D.M., Naritomi, H. & Matsuyama, T. (2004) Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest., 114, 330-338.
31. The STEPS Participants. (2009) Stem cell therapies as an emerging paradigm in stroke (STEPS): bridging basic and clinical science for cellular and neurogenic factor therapy in treating stroke. Stroke, 40, 510-515.
32. Visnyei, K., Tatsukawa, K.J., Erickson, R.I., Simonian, S., Oknaian, N., Carmichael, S.T. & Kornblum, H.I. (2006) Neural progenitor implantation restores metabolic deficits in the brain following striatal quinolinic acid lesion. Exp. Neurol., 197, 465-474.
33. Walczak, P., Zhang, J., Gilad, A.A., Kedziorek, D.A., Ruiz-Cabello, J., Young, R.G., Pittenger, M.F., Zijl, P.C.M., Huang, J. & Bulte, J.W.M. (2008) Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke, 39, 1569-1574.
34. Xu, G., Zhang, L., Ren, G., Yuan, Z., Zhang, Y., Zhao, R.C. & Shi, Y. (2007) Immunosuppressive properties of cloned bone marrow mesenchymal stem cells. Cell Res., 17, 240-248.
35. Zacharek, A., Chen, J., Cui, X., Li, A., Li, Y., Roberts, C., Feng, Y., Gao, Q. & Chopp, M. (2007) Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J. Cereb. Blood Flow Metab., 27, 1684-1691.
36. Zacharek, A., Shehadah, A., Chen, J., Cui, X., Roberts, C., Lu, M. & Chopp, M. (2010) Comparison of bone marrow stromal cells derived from stroke and normal rats for stroke treatment. Stroke, 41, 524-530.
37. Zhang, Z., Wang, R., Wang, R., Li, G., Wei, J., Li, Z., Feng, M., Kang, J., Du, W., Ma, W., Li, Y., Yang, Y. & Kong, Y. (2008) Transplantation of neural stem cells modified by human neurotrophin-3 promotes functional recovery after transient focal cerebral ischemia in rats. Neurosci. Lett., 444, 227-230.
38. Zhang, B., Liu, R., Shi, D., Liu, X., Chen, Y., Dou, X., Zhu, X., Lu, C., Liang, W., Liao, L., Zenke, M. & Zhao, R.C. (2009) Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2-dependent regulatory dendritic cell population. Blood, 113, 46-57.
39. Zhu, W., Fan, Y., Hao, Q., Shen, F., Hashimoto, T., Yang, G.Y., Gasmi, M., Bartus, R.T., Young, W.L. & Chen, Y. (2009) Postischemic IGF-1 gene transfer promotes neurovascular regeneration after experimental stroke. J. Cereb. Blood Flow Metab., 29, 1528-1537.