Endothelial cells support survival, proliferation, and neuronal differentiation of transplanted adult ischemia-induced neural stem/progenitor cells after cerebral infarction

Stem Cells

Volumn 27, Issue 9, 2009, Pages 2185-2195

  Nakagomi, Nami ^a   Nakagomi, Takayuki ^b   Kubo, Shuji ^b   Nakano Doi, Akiko ^b   Saino, Orie ^b   Takata, Masashi ^b   Yoshikawa, Hiroo ^b   Stern, David M ^c   Matsuyama, Tomohiro ^b   Taguchi, Akihiko ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b HYOGO COLLEGE OF MEDICINE   (Japan)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Endothelial cells; Ischemia; Neural stem cell; Transplantation; Vascular niche

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; STROKE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL INFARCTION; ENDOTHELIAL CELLS; IMMUNOHISTOCHEMISTRY; MALE; MICE; NEURONS; STEM CELL TRANSPLANTATION; STEM CELLS;

MUS;

EID: 70349847390     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.161     Document Type: Article

References (52)

1. Erdo F, Trapp T, Buhrle C et al. [Embryonic stem cell therapy in experimental stroke: host-dependent malignant transformation]. Orv Hetil 2004;145:1307-1313.
2. Buhnemann C, Scholz A, Bernreuther C et al. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain 2006;129:3238-3248. (Pubitemid 44871439)
3. Hayashi J, Takagi Y, Fukuda H et al. Primate embryonic stem cell-derived neuronal progenitors transplanted into ischemic brain. J Cereb Blood Flow Metab 2006;26:906-914. (Pubitemid 43980407)
4. Okada S, Ishii K, Yamane J et al. In vivo imaging of engrafted NSCs: Its application in evaluating the optimal timing of transplantation for spinal cord injury. FASEB J 2005;19:1839-1841.
5. Ogawa Y, Sawamoto K, Miyata T et al. Transplantation of in vitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. J Neurosci Res 2002;69:925-933. (Pubitemid 34984709)
6. Darsalia V, Kallur T, Kokaia Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical NSCs grafted in stroke-damaged rat striatum. Eur J Neurosci 2007;26:605-614. (Pubitemid 47206801)
7. Doetsch F, Caille I, Lim DA et al. Subventricular zone astrocytes are NSCs in the adult mammalian brain. Cell 1999;97:703-716. (Pubitemid 29278045)
8. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996;16:2027-2033. (Pubitemid 26144015)
9. Takahashi K, Yasuhara T, Shingo T et al. Embryonic NSCs transplanted in middle cerebral artery occlusion model of rats demonstrated potent therapeutic effects, compared to adult NSCs. Brain Res 2008;1234:172-182.
10. Kameda M, Shingo T, Takahashi K et al. Adult neural stem and progenitor cells modified to secrete GDNF can protect, migrate and integrate after intracerebral transplantation in rats with transient forebrain ischemia. Eur J Neurosci 2007;26:1462-1478. (Pubitemid 47416525)
11. Hicks AU, Hewlett K, Windle V et al. Enriched environment enhances transplanted subventricular zone stem cell migration and functional recovery after stroke. Neuroscience 2007;146:31-40. (Pubitemid 46654609)
12. Toda H, Takahashi J, Iwakami N et al. Grafting NSCs improved the impaired spatial recognition in ischemic rats. Neurosci Lett 2001;316:9-12. (Pubitemid 33092021)
13. Shen Q, Wang Y, Kokovay E et al. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008;3:289-300.
14. Capela A, Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002;35:865-875.
15. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000;425:479-494.
16. Tavazoie M, Van der Veken L, Silva-Vargas V et al. A specialized vascular niche for adult NSCs. Cell Stem Cell 2008;3:279-288.
17. Louissaint A, Jr., Rao S, Leventhal C et al. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 2002;34:945-960. (Pubitemid 34722284)
18. Shen Q, Goderie SK, Jin L et al. Endothelial cells stimulate self-renewal and expand neurogenesis of NSCs. Science 2004;304:1338-1340. (Pubitemid 38697433)
19. Teng H, Zhang ZG, Wang L et al. Coupling of angiogenesis and neurogenesis in cultured endothelial cells and neural progenitor cells after stroke. J Cereb Blood Flow Metab 2008;28:764-771.
20. Jiao J, Chen DF. Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells 2008;26:1221-1230.
21. Arsenijevic Y, Villemure JG, Brunet JF et al. Isolation of multipotent neural precursors residing in the cortex of the adult human brain. Exp Neurol 2001;170:48-62. (Pubitemid 32641773)
22. Nakagomi T, Taguchi A, Fujimori Y et al. Isolation and characterization of neural stem/progenitor cells from post-stroke cerebral cortex in mice. Eur J Neurosci 2009;29:1842-1852.
23. Nunes MC, Roy NS, Keyoung HM et al. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 2003;9:439-447.
24. Weiss S, Dunne C, Hewson J et al. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 1996;16:7599-7609. (Pubitemid 26389699)
25. Parr AM, Kulbatski I, Zahir T et al. Transplanted adult spinal cordderived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 2008;155:760-770.
26. 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)
27. Taguchi A, Wen Z, Myojin K et al. Granulocyte colony-stimulating factor has a negative effect on stroke outcome in a murine model. Eur J Neurosci 2007;26:126-133. (Pubitemid 47035445)
28. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.
29. Kubo S, Seleme MC, Soifer HS et al. L1 retrotransposition in nondividing and primary human somatic cells. Proc Natl Acad Sci U S A 2006;103:8036-8041. (Pubitemid 43801048)
30. Campbell RE, Tour O, Palmer AE et al. A monomeric red fluorescent protein. Proc Natl Acad Sci U S A 2002;99:7877-7882.
31. Kimble DP. Hippocampus and internal inhibition. Psychol Bull 1968;70:285-295.
32. Song H, Stevens CF, Gage FH. Astroglia induce neurogenesis from adult NSCs. Nature 2002;417:39-44.
33. Stubbs D, Deproto J, Nie K et al. Neurovascular congruence during cerebral cortical development. Cereb Cortex 2009;19:i32-i41.
34. Javaherian A, Kriegstein A. A stem cell niche for intermediate progenitor cells of the embryonic cortex. Cereb Cortex 2009;19:i70-i77.
35. Lai B, Mao XO, Greenberg DA et al. Endothelium-induced proliferation and electrophysiological differentiation of human embryonic stem cell-derived neuronal precursors. Stem Cells Dev 2008;17:565-572. (Pubitemid 351948191)
36. Seghezzi G, Patel S, Ren CJ et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: An autocrine mechanism contributing to angiogenesis. J Cell Biol 1998;141:1659-1673. (Pubitemid 28309179)
37. Biro S, Yu ZX, Fu YM et al. Expression and subcellular distribution of basic fibroblast growth factor are regulated during migration of endothelial cells. Circ Res 1994;74:485-494. (Pubitemid 24064199)
38. Collins T, Ginsburg D, Boss JM et al. Cultured human endothelial cells express platelet-derived growth factor B chain: cDNA cloning and structural analysis. Nature 1985;316:748-750. (Pubitemid 16239356)
39. Leventhal C, Rafii S, Rafii D et al. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 1999;13:450-464. (Pubitemid 29337211)
40. Le Bras B, Barallobre MJ, Homman-Ludiye J et al. VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nat Neurosci 2006;9:340-348. (Pubitemid 43290963)
41. Reimers D, Lopez-Toledano MA, Mason I et al. Developmental expression of fibroblast growth factor (FGF) receptors in NSC progeny. Modulation of neuronal and glial lineages by basic Fgf treatment. Neurol Res 2001;23:612-621.
42. Yan YP, Sailor KA, Vemuganti R et al. Insulin-like growth factor-1 is an endogenous mediator of focal ischemia-induced neural progenitor proliferation. Eur J Neurosci 2006;24:45-54. (Pubitemid 44050665)
43. Erlandsson A, Enarsson M, Forsberg-Nilsson K. Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. J Neurosci 2001;21:3483-3491. (Pubitemid 32422812)
44. Li Q, Ford MC, Lavik EB et al. Modeling the neurovascular niche: VEGF- and BDNF-mediated cross-talk between NSCs and endothelial cells: an in vitro study. J Neurosci Res 2006;84:1656-1668. (Pubitemid 44892600)
45. Li Z, Wu JC, Sheikh AY et al. Differentiation, survival, and function of embryonic stem cell derived endothelial cells for ischemic heart disease. Circulation 2007;116:I46-54. (Pubitemid 47480769)
46. Walczak P, Chen N, Eve D et al. Long-term cultured human umbilical cord neural-like cells transplanted into the striatum of NOD SCID mice. Brain Res Bull 2007;74:155-163. (Pubitemid 47187924)
47. Roitbak T, Li L, Cunningham LA. Neural stem/progenitor cells promote endothelial cell morphogenesis and protect endothelial cells against ischemia via HIF-1alpha-regulated VEGF signaling. J Cereb Blood Flow Metab 2008;28:1530-1542.
48. Jin K, Wang X, Xie L et al. Evidence for stroke-induced neurogenesis in the human brain. Proc Natl Acad Sci U S A 2006;103:13198-13202. (Pubitemid 44338939)
49. Okada S, Nakamura M, Mikami Y et al. Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. J Neurosci Res 2004;76:265-276. (Pubitemid 38451214)
50. Nakashima K, Yanagisawa M, Arakawa H et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 1999;284:479-482. (Pubitemid 29289619)
51. Shihabuddin LS, Horner PJ, Ray J et al. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 2000;20:8727-8735.
52. Jiao JW, Feldheim DA, Chen DF. Ephrins as negative regulators of adult neurogenesis in diverse regions of the central nervous system. Proc Natl Acad Sci U S A 2008;105:8778-8783.