Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model

PLoS ONE

Volumn 2, Issue 1, 2007, Pages

  Lee, Hong J ^a,b,c   Kim, Kwang S ^a,c   Park, In H ^a   Kim, Seung U ^a,c  

^a Ajou University School of Medicine   (South Korea)

^b Korea University   (South Korea)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIOPEPTIDASE A; RETROVIRUS VECTOR; VASCULOTROPIN; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HEMORRHAGE; BRAIN TRANSPLANTATION; CELL BASED GENE THERAPY; CELL DIFFERENTIATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DNA MODIFICATION; FUNCTIONAL STATUS; GENE OVEREXPRESSION; GRAFT SURVIVAL; HUMAN; HUMAN CELL; MOUSE; NEURAL STEM CELL TRANSPLANTATION; NEUROPROTECTION; NONHUMAN; TREATMENT RESPONSE; TREND STUDY; ANIMAL; ANIMAL BEHAVIOR; CELL LINE; CELL SURVIVAL; CONVALESCENCE; CYTOLOGY; DISEASE MODEL; GENETICS; METABOLISM; METHODOLOGY; NERVE CELL; NICK END LABELING; PHYSIOLOGY; RAT; STEM CELL; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS; RATTUS;

ANIMALS; BEHAVIOR, ANIMAL; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; HUMANS; IN SITU NICK-END LABELING; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; NEURONS; RATS; RECOVERY OF FUNCTION; STEM CELL TRANSPLANTATION; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 34447274187     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000156     Document Type: Article

References (50)

1. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, et al. (2001) Spontaneous intracerebral hemorrhage. N Engl J Med 344: 1450-1460.
2. Inagawa T (2002) What are the actual incidence and mortality rates of intracerebral hemorrhage? Neurosurg Rev 25: 237-246.
3. Gebel JM, Broderick JP (2000) Intracerebral hemorrhage. Neurol Clin 18: 419-438.
4. NINDS ICH Workshop Participants (2005) Priorities for clinical research in intracerebral hemorrhage: report from a National Institute of Neurological Disorders and Stroke workshop. Stroke 36: 23-41.
5. McKay R (1997) Stem cells in the central nervous system. Science 276: 66-71.
6. Gage FH (2000) Mammalian neural stem cells. Science 287: 1433-1438.
7. Lindvall O, Kokaia Z, Martinez-Serano A (2004) Stem cell therapy for human neurodegenerative disorders. Nature Med 10 suppl: S42-S50.
8. Ishibashi S, Sakaguchi M, Kuroiwa T, Yamasaki M, Kanemura Y, et al. (2004) Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J Neurosci Res 78: 215-223.
9. Chu K, Kim M, Jeong SW, Kim SU, Yoon BW (2003) Human neural stem cells can migrate, differentiate, and integrate after intravenous transplantation in adult rats with transient forebrain ischemia. Neurosci Lett 343: 129-133.
10. Chu K, Kim M, Park KI, Jeong SW, Park HK, et al. (2004) Human neural stem cells improve sensorimotor deficits in the rat brain with experimental focal ischemia. Brain Res 1016: 145-153.
11. Chu K, Kim M, Chae SH, Jeong SW, Kang KS, et al. (2004) Distribution and in situ proliferation patterns of intravenously injected immortalized human neural stem cells in rats with focal cerebral ischemia. Neurosci Res 50: 459-465.
12. Jeong SW, Chu K, Jung KH, Kim SU, Kim M, et al. (2003) Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 34: 2258-2263.
13. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, et al. (2004) Transplanted human fetal neural stem cells survive, migrate and differentiate in ischemic rat cerebral cortex. Proc Nat Acad Sci USA 101: 11839-11844.
14. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, et al. (1998) Engraftable human neural stem cells respond to developmental cues, replace neurons, and express foreign genes. Nature Biotech 16: 1033-1039.
15. Kim SU (2004) Human neural stem cells genetically modified for brain repair in neurological disorders. Neuropathology 24: 159-171.
16. Cho T, Bae JH, Choi HB, Kim SS, McLarnon JG, et al. (2002) Human neural stem cells: Electrophysiological properties of voltage gated ion channels. Neuroreport 13: 1447-1452.
17. Ryu JK, Choi HB, Hatori K, Pelech S, McLarnon JM, et al. (2003) Adenosine triphosphate induces proliferation of human neural stem cells: Role of calcium and p70 ribosomal protein S6 kinase. J Neurosci Res 72: 352-362.
18. Kim SU, Park IH, Kim TH, Kim KS, Choi HB, et al. (2006) Brain transplantation of human neural stem cells transduced with tyrosine hydroxylase and GTP cyclohydrolase 1 provides functional improvement in animal models of Parkinson disease. Neuropathology 26: 129-140.
19. Ryu JK, Kim J, Hong SH, Choi HB, Lee MC, et al. (2004) Proactive transplantation of human neural stem cells blocks neuronal cell death in rat model of Huntington disease. Neurobiol Disease 16: 68-77.
20. Lee ST, Chu K, Park JE, Lee K, Kang L, et al. (2005) Intravenous administration of human neural stem cells induces functional recovery in Huntington's disease rat model. Neurosci Res 52: 243-249.
21. Meng XL, Shen JS, Ohashi T, Maeda H, Kim SU, et al. (2003) Brain transplantation of genetically engineered human neural stem cells globally corrects brain lesions in mucopolysacchridosis VII mouse. J Neurosci Res 74: 266-277.
22. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N (1989) Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309.
23. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, et al. (1998) Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343.
24. Hayashi T, Abe K, Suzuki H, Itoyama Y (1998) Reduction of ischemic damage by application of vascular endothelial factor in rat brain after transient ischemia. J Cereb Blood Flow Metab 18: 887-895.
25. Zhang ZG, Zhang L, Jiang Q, Zhang R, Davies K, et al. (2000) VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106: 829-838.
26. Harrigan MR, Ennis SR, Sullivan SE, Keep RF (2003) Effects of intraventricular infusion of vascular endothelial growth factor on cerebral flow, edema and infarct volume. Acta Neurochir 145: 49-53.
27. Sun Y, Jin K, Xie L, Childs J, Mao XO, et al. (2003) VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111: 1843-1851.
28. Kaya D, Ozdemir Y, Yemisci M, Tuncer N, Aktan S, et al. (2005) VEGF protects brain against focal ischemia without increasing blood-brain permeability when administered intracerebroventricularly. J Cereb Blood Flow Metab 25: 1111-1118.
29. Kim SU, Stern J, Kim MW, Pleasure DE (1983) Culture of purified rat astrocytes in serum-free medium supplemented with mitogen. Brain Res 274: 79-86.
30. Kim SU, Moretto G, Lee V, Yu RK (1986) Neuroimmunology of gangliosides in human neurons and glial cells in culture. J Neurosci Res 15: 303-321.
31. Del Bigio MR, Yan HJ, Buist R, Peeling J (1996) Experimental intracerebral hemorrhage in rats. Magnetic resonance imaging and histopathological correlates. Stroke 27: 2312-2320.
32. Puurunen K, Jolkkonen J, Sirvio J, Haapalinna A, Sivenius J (2001) An alpha(2)-adrenergic antagonist, atipamezole, facilitates behavioral recovery after focal cerebral ischemia in rats. Neuropharmacology 40: 597-606.
33. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482.497.
34. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
35. Paxinos G, Franklin K (2003) The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.
36. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4: 299-309.
37. Fagan SC, Hess DC, Hohnadel EJ, Pollock DM, Ergul A (2004) Targets for vascular protection after acute ischemic stroke. Stroke 35: 2220-2225.
38. Sharp FR, Ran R, Lu A, Tang Y, Strauss KI, et al. (2004) Hypoxic preconditioning protects against Ischemic brain injury. NeuroRx 1: 26-35.
39. Jin KL, Mao XO, Greenberg DA (2000) Vascular endothelial growth factor: direct neuroprotective effect in vitro ischemia. Proc Natl Acad Sci USA 97: 10242-10247.
40. Matsuzaki H, Tamatani M, Yamaguchi A, Namikawa K, Kiyama H, et al. (2001) Vascular endothelial growth factor rescues hippocampal neurons from glutamate-induced toxicity: signal transduction cascades. FASEB J 15: 1218-1220.
41. Svensson B, Peters M, Konig HG, Poppe M, Levkau B, et al. (2002) Vascular endothelial growth factor protects cultured rat hippocampal neurons against hypoxic injury via an antiexcitotoxic, caspase-independent mechanism. J. Cereb. Blood Flow Metab 22: 1170-1175.
42. Plate KH, Beck H, Danner S, Allegrini PR, Wiessner C (1999) Cell type specific upregulation of vascular endothelial growth factor in an MCA-occlusion model of cerebral infarct. J Neuropathol Exp Neurol 58: 654-666.
43. Wang Y, Kilic E, Kilic U, Weber B, Bassetti CL, et al. (2005) VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena. Brain 128: 52-63.
44. Proescholdt MA, Heiss JD, Walbridge S, Muhlhauser J, Capogrossi MC, et al. (1999) Vascular endothelial growth factor (VEGF) modulates vascular permeability and inflammation in rat brain. J Neuropathol Exp Neurol 58: 613-627.
45. Zhang Z, Chopp M (2002) Vascular endothelial growth factor and angiopoietins in focal cerebral ischemia. Trends Cardiovasc Med 12: 62-66.
46. Marti HH (2002) Vascular endothelial growth factor. Adv Exp Med Biol. 513: 375-394.
47. Friguls B, Justicia C, Pallas M, Planas AM (2001) Focal cerebral ischemia causes two emporal waves of Akt activation. Neuroreport 12: 3381-3384.
48. Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C (2003) PI3K/AKT and apoptosis: Size matters. Oncogene 22: 8983-8998.
49. Engleman JA, Luo J, Cantley LC (2006) The evolution of PI3-kinases as regulators of growth and metabolism. Nat Rev Genet 7: 606-619.
50. Rosenstein JM, Krum JM (2004) New roles for VEGF in nervous tissue-beyond blood vessels. Exp Neurol 187: 246-253.