Endothelial progenitor cell transplantation improves long-term stroke outcome in mice

Annals of Neurology

Volumn 67, Issue 4, 2010, Pages 488-497

  Fan, Yongfeng ^a   Shen, Fanxia ^a,b   Frenzel, Tim ^a,c   Zhu, Wei ^a   Ye, Jianqin ^d   Liu, Jianrong ^a,b   Chen, Yongmei ^a   Su, Hua ^a   Young, William L ^a   Yang, Guo Yuan ^a,b,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; FLOW CYTOMETRY; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MIDDLE CEREBRAL ARTERY OCCLUSION; MONONUCLEAR CELL; MOUSE; NEUROPROTECTION; NONHUMAN; NUDE MOUSE; OUTCOMES RESEARCH; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; STROKE; TISSUE REGENERATION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD34; BEHAVIOR, ANIMAL; CADHERINS; CAPILLARIES; CEREBRAL INFARCTION; CHEMOKINE CXCL12; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTHELIUM; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HETEROCYCLIC COMPOUNDS; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; INJECTIONS, INTRAVENOUS; MAGNETIC RESONANCE IMAGING; MICE; MICE, NUDE; MOTOR ACTIVITY; NEOVASCULARIZATION, PHYSIOLOGIC; PSYCHOMOTOR PERFORMANCE; RECEPTORS, CXCR4; STEM CELL TRANSPLANTATION; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VON WILLEBRAND FACTOR;

EID: 77951758771     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.21919     Document Type: Article

References (43)

1. Miraglia S, Godfrey W, Yin AH, et al. A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 1997;90:5013-5021. (Pubitemid 28007218)
2. Quirici N, Soligo D, Caneva L, et al. Differentiation and expansion of endothelial cells from human bone marrow CD133(+) cells. Br J Haematol 2001;115:186-194. (Pubitemid 32995115)
3. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275: 964-967. (Pubitemid 27087709)
4. Werner N, Kosiol S, Schiegl T, et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005; 353:999-1007. (Pubitemid 41262334)
5. Shintani S, Murohara T, Ikeda H, et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001;103:2776-2779. (Pubitemid 32550062)
6. Ii M, Nishimura H, Iwakura A, et al. Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via "imported" nitric oxide synthase activity. Circulation 2005;111:1114-1120.
7. Kalka C, Masuda H, Takahashi T, et al. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 2000;97:3422-3427. (Pubitemid 30183318)
8. Kawamoto A, Tkebuchava T, Yamaguchi J, et al. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 2003;107:461-468. (Pubitemid 36158050)
9. Szmitko PE, Fedak PW, Weisel RD, et al. Endothelial progenitor cells: new hope for a broken heart. Circulation 2003;107: 3093-3100.
10. Faden A. Neuroprotection. NeuroRX 2004;1:3-4.
11. del Zoppo GJ. Lessons from stroke trials using anti-inflammatory approaches that have failed. Ernst Schering Res Found Workshop 2004;(47):155-184.
12. Sobrino T, Hurtado O, Moro MA, et al. The increase of circulating endothelial progenitor cells after acute ischemic stroke is associated with good outcome. Stroke 2007;38:2759-2764. (Pubitemid 47494015)
13. Chu K, Jung KH, Lee ST, et al. Circulating endothelial progenitor cells as a new marker of endothelial dysfunction or repair in acute stroke. Stroke 2008;39:1441-1447.
14. Rouhl RP, van Oostenbrugge RJ, Damoiseaux J, et al. Endothelial progenitor cell research in stroke: a potential shift in pathophysiological and therapeutical concepts. Stroke 2008;39: 2158-2165.
15. Zhang ZG, Zhang L, Jiang Q, Chopp M. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res 2002;90:284-288. (Pubitemid 34633929)
16. Ohta T, Kikuta K, Imamura H, et al. Administration of ex vivo-expanded bone marrow-derived endothelial progenitor cells attenuates focal cerebral ischemia-reperfusion injury in rats. Neurosurgery 2006;59:679-686.
17. Fan Y, Ye J, Shen F, et al. Interleukin-6 stimulates circulating blood-derived endothelial progenitor cell angiogenesis in vitro. J Cereb Blood Flow Metab 2008;28:90-98.
18. Fan Y, Shen F, Chen Y, et al. Overexpression of Netrin-1 induces neovascularization in the adult mouse brain. J Cereb Blood Flow Metab 2008;28:1543-1551.
19. Ward NL, Moore E, Noon K, et al. Cerebral angiogenic factors, angiogenesis, and physiological response to chronic hypoxia differ among four commonly used mouse strains. J Appl Physiol 2007;102:1927-1935. (Pubitemid 46701964)
20. Krenning G, van der Strate B, Schipper M, et al. CD34(+) cells augment endothelial cell differentiation of CD14(+) endothelial progenitor cells in vitro. J Cell Mol Med 2009;13:2521-2533.
21. Rookmaaker MB, Verhaar MC, Loomans CJ, et al. CD34+ cells home, proliferate, and participate in capillary formation, and in combination with CD34- cells enhance tube formation in a 3-dimensional matrix. Arterioscler Thromb Vasc Biol 2005;25:1843-1850.
22. Yodoi Y, Sasahara M, Kameda T, et al. Circulating hematopoietic stem cells in patients with neovascular age-related macular degeneration. Invest Ophthalmol Vis Sci 2007;48:5464-5472. (Pubitemid 351260846)
23. Yamaguchi J, Kusano KF, Masuo O, et al. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 2003;107: 1322-1328. (Pubitemid 36314418)
24. Taguchi A, Soma T, Tanaka H, et al. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 2004;114:330-338. (Pubitemid 39071605)
25. Shyu WC, Lin SZ, Chiang MF, et al. Intracerebral peripheral blood stem cell (CD34+) implantation induces neuroplasticity by enhancing beta1 integrin-mediated angiogenesis in chronic stroke rats. J Neurosci 2006;26:3444-3453.
26. Nonaka Y, Koumura A, Hyakkoku K, et al. Combination treatment with normobaric hyperoxia and cilostazol protects mice against focal cerebral ischemia-induced neuronal damage better than each treatment alone. J Pharmacol Exp Ther 2009;330:13-22.
27. Zhu W, Fan Y, Frenzel T, et al. Insulin growth factor-1 gene transfer enhances neurovascular remodeling and improves long-term stroke outcome in mice. Stroke 2008;39:1254-1261. (Pubitemid 351440699)
28. Storkebaum E, Lambrechts D, Carmeliet P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays 2004;26:943-954. (Pubitemid 39273068)
29. Sun Y, Jin K, Clark KR, et al. Adeno-associated virus-mediated delivery of BCL-w gene improves outcome after transient focal cerebral ischemia. Gene Ther 2003;10:115-122. (Pubitemid 36582583)
30. Balabanian K, Lagane B, Infantino S, et al. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 2005;280:35760-35766. (Pubitemid 41532769)
31. Petit I, Jin D, Rafii S. The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol 2007;28:299-307. (Pubitemid 46963141)
32. Hill WD, Hess DC, Martin-Studdard A, et al. SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 2004;63:84-96. (Pubitemid 38030236)
33. Bonig H, Priestley GV, Papayannopoulou T. Hierarchy of molecular-pathway usage in bone marrow homing and its shift by cytokines. Blood 2006;107:79-86. (Pubitemid 43053527)
34. Abbott JD, Huang Y, Liu D, et al. Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 2004;110:3300-3305. (Pubitemid 39557491)
35. Ceradini DJ, Kulkarni AR, Callaghan MJ, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004;10:858-864.
36. Walter DH, Haendeler J, Reinhold J, et al. Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endothelial progenitor cells from patients with coronary artery disease. Circ Res 2005;97:1142-1151. (Pubitemid 43755207)
37. Levoye A, Balabanian K, Baleux F, et al. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009;113:6085-6093.
38. Kalatskaya I, Berchiche YA, Gravel S, et al. AMD3100 is a CXCR7 ligand with allosteric agonist properties. Mol Pharmacol 2009;75: 1240-1247.
39. Hartmann TN, Grabovsky V, Pasvolsky R, et al. A crosstalk between intracellular CXCR7 and CXCR4 involved in rapid CXCL12-triggered integrin activation but not in chemokine-triggered motility of human T lymphocytes and CD34+ cells. J Leukoc Biol 2008;84:1130-1140.
40. Tabatabai G, Frank B, Mohle R, et al. Irradiation and hypoxia promote homing of haematopoietic progenitor cells towards gliomas by TGF-beta-dependent HIF-1alpha-mediated induction of CXCL12. Brain 2006;129:2426-2435. (Pubitemid 44522127)
41. Yoon CH, Hur J, Park KW, et al. Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation 2005;112:1618-1627. (Pubitemid 41324524)
42. Zemani F, Silvestre JS, Fauvel-Lafeve F, et al. Ex vivo priming of endothelial progenitor cells with SDF-1 before transplantation could increase their proangiogenic potential. Arterioscler Thromb Vasc Biol 2008;28:644-650. (Pubitemid 351651342)
43. Foubert P, Silvestre JS, Souttou B, et al. PSGL-1-mediated activation of EphB4 increases the proangiogenic potential of endothelial progenitor cells. J Clin Invest 2007;117:1527-1537. (Pubitemid 46871337)