Transplanted human embryonic neural stem cells survive, migrate, differentiate and increase endogenous nestin expression in adult rat cortical peri-infarction zone: Original Article

Neuropathology

Volumn 29, Issue 4, 2009, Pages 410-421

  Zhang, Pengbo ^a   Li, Jie ^a   Liu, Yong ^a   Chen, Xinlin ^a   Kang, Qianyan ^a  

^a MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Focal cerebral ischemia; Nestin; Neural stem cells; Peri infarction zone; Transplantation

Indexed keywords

1,1' DIOCTADECYL 6,6' DI(4 SULFOPHENYL) 3,3,3',3' TETRAMETHYLINDOCARBOCYANIN; FLUORESCENT DYE; GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; NEURON SPECIFIC NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION; CELL MIGRATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MALE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TEMPORAL LOBE; TREATMENT OUTCOME;

AGE FACTORS; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CEREBRAL INFARCTION; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MALE; NERVE TISSUE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; STEM CELL TRANSPLANTATION; TIME FACTORS;

EID: 67651243680     PISSN: 09196544     EISSN: 14401789     Source Type: Journal    
DOI: 10.1111/j.1440-1789.2008.00993.x     Document Type: Article

References (55)

1. Gage FH. Mammalian neural stem cells. Science 2000 287 : 1433 1438.
2. Ma W, Fitzgerald W, Liu QY et al. CNS stem and progenitor cell differentiation into functional neuronal circuits in three-dimensional collagen gels. Exp Neurol 2004 190 : 276 288.
3. Tamaki S, Eckert K, He D et al. Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J Neurosci Res 2002 69 : 976 986.
4. Emsley JG, Mitchell BD, Kempermann G, Macklis JD. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 2005 75 : 321 341.
5. Minger SL, Ekonomou A, Carta EM, Chinoy A, Perry RH, Ballard CG. Endogenous neurogenesis in the human brain following cerebral infarction. Regen Med 2007 2 : 69 74.
6. Zhang PB, Liu Y, Li J et al. Ependymal/subventricular zone cells migrate to the peri-infarct region and differentiate into neurons and astrocytes after focal cerebral ischemia in adult rats. Di Yi Jun Yi Da Xue Xue Bao 2005 25 : 1201 1206.
7. Zhang P, Liu Y, Li J et al. Decreased neuronal nitric oxide synthase expression and cell migration in the peri-infarction after focal cerebral ischemia in rats. Neuropathology 2007 27 : 347 354.
8. Wiltrout C, Lang B, Yan Y, Dempsey RJ, Vemuganti R. Repairing brain after stroke: a review on post-ischemic neurogenesis. Neurochem Int 2007 50 : 1028 1041.
9. Roitberg B. Transplantation for stroke. Neurol Res 2004 26 : 256 264.
10. Savitz SI, Rosenbaum DM, Dinsmore JH, Wechsler LR, Caplan LR. Cell transplantation for stroke. Ann Neurol 2002 52 : 266 275.
11. Kaufmann AM, Firlik AD, Fukui MB, Wechsler LR, Jungries CA, Yonas H. Ischemic core and penumbra in human stroke. Stroke 1999 30 : 93 99.
12. Memezawa H, Minamisawa H, Smith M-L, Siesjo BK. Ischemic penumbra in a model of reversible middle cerebral artery occlusion in the rat. Exp Brain Res 1992 89 : 67 78.
13. Ishibashi S, Sakaguchi M, Kuroiwa T et al. Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J Neurosci Res 2004 78 : 215 223.
14. 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 rats. J Neurosci Res 2002 69 : 925 933.
15. Touzani O, Roussel S, MacKenzie ET. The ischaemic penumbra. Curr Opin Neurol 2001 14 : 83 88.
16. Chu K, Kim M, Jeong SW, Kim SU, Yoon BW. Human neural stem cells can migrate, differentiate, and integrate after intravenous transplantation in adult rats with transient forebrain ischemia. Neurosci Lett 2003 343 : 129 133.
17. 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 : 906 149.
18. Park KI, Hack MA, Ourednik J et al. Acute injury directs the migration, proliferation, and differentiation of solid organ stem cells: evidence from the effect of hypoxia-ischemia in the CNS on clonal "reporter" neural stem cells. Exp Neurol 2006 199 : 156 178.
19. Shingo T, Sorokan ST, Shimazaki T, Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 2001 21 : 9733 9743.
20. Zhang P, Liu Y, Li J et al. Cell proliferation in ependymal/ subventricular zone and nNOS expression following focal cerebral ischemia in adult rats. Neurol Res 2006 28 : 91 96. (Pubitemid 43201835)
21. Gill R, Sibson NR, Hatfield RH et al. A comparison of the early development of ischaemic damage following permanent middle cerebral artery occlusion in rats as assessed using magnetic resonance imaging and histology. J Cereb Blood Flow Metab 1995 15 : 1 11.
22. Ooboshi H, Ibayashi S, Takada J, Yao H, Kitazono T, Fujishima M. Adenovirus-mediated gene transfer to ischemic brain: ischemic flow threshold for transgene expression. Stroke 2001 32 : 1043 1047.
23. Kelly S, Bliss TM, Shah AK et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. PNAS 2004 101 : 11839 11844.
24. Olstorn H, Moe MC, Roste GK, Bueters T, Langmoen IA. Transplantation of stem cells from the adult human brain to the adult rat brain. Neurosurgery 2007 60 : 1089 1099.
25. Jeong SW, Chu K, Jung KH, Kim SU, Kim M, Roh JK. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 2003 34 : 2258 2263.
26. Barone FC, Feuerstein GZ. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 1999 19 : 819 8349.
27. McDonald JW, Behrens MI, Chung C, Bhattacharyya T, Choi DW Susceptibility to apoptosis is enhanced in immature cortical neurons. Brain Res 1997 759 : 228 232.
28. Bacigaluppi M, Pluchino S, Martino G, Kilic E, Hermann DM. Neural stem/precursor cells for the treatment of ischemic stroke. J Neurol Sci 2008 265 : 73 77.
29. Hadani M, Freeman T, Munsiff A, Young W, Flamm E. Fetal cortical cells survive in focal cerebral infarct after permanent occlusion of the middle cerebral artery in adult rats. J Neurotrauma 1992 9 : 107 112.
30. Li P, Tessler A, Han SS, Fischer I, Rao MS, Selzer ME. Fate of immortalized human neuronal progenitor cells transplanted in rat spinal cord. Arch Neurol 2005 62 : 223 229.
31. Molcanyi M, Riess P, Bentz K et al. Trauma-associated inflammatory response impairs embryonic stem cell survival and integration after implantation into injured rat brain. J Neurotroma 2007 24 : 625 637.
32. Aleksandrova MA, Saburina IN, Poltavtseva RA, Revishchin AV, Korochkin LI, Sukhikh GT. Behavior of human neural progenitor cells transplanted to rat brain. Brain Res Dev Brain Res 2002 134 : 143 148.
33. Toda H, Takahashi J, Iwakami N et al. Grafting neural stem cells improved the impaired spatial recognition in ischemic rats. Neurosci Lett 2001 316 : 9 12.
34. Jin K, Sun Y, Xie L et al. Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat. Neurobiol Dis 2005 18 : 366 374.
35. Aarum J, Sandberg K, Haeberlein SL, Persson MA. Migration and differentiation of neural precursor cells can be directed by microglia. PNAS 2003 100 : 15983 15988.
36. Svendsen CN, Caldwell MA, Shen J et al. Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease. Exp Neurol 1997 148 : 135 146.
37. Chu K, Kim M, Park KI et al. Human neural stem cells improve sensorimotor deficits in the adult rat brain with experimental focal ischemia. Brain Res 2004 1016 : 145 153.
38. Modo M, Stroemer RP, Tang E, Patel S, Hodges H. Effects of implantation site of stem cell grafts on behavioral recovery from stroke damage. Stroke 2002 33 : 2270 2278.
39. Song H, Stevens CF, Gage FH. Astroglia induce neurogenesis from adult neural stem cells. Nature 2002 417 : 39 44.
40. Sanai N, Tramontin AD, Quiñones-Hinojosa A et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004 427 : 740 744.
41. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA. Control of synapse number by glia. Science 2001 291 : 657 661.
42. Darsalia V, Kallur T, Kokaia Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur J Neurosci 2007 26 : 605 614.
43. Wu P, Tarasenko YI, Gu Y, Huang LY, Coggeshall RE, Yu Y. Region-specific generation of cholinergic neurons from fetal human neural stem cells grafted in adult rat. Nat Neurosci 2002 5 : 1271 1278.
44. Duggal N, Schmidt-Kastner R, Hakim AM. Nestin expression in reactive astrocytes following focal cerebral ischemia in rats. Brain Res 1997 768 : 1 9.
45. Itoh T, Satou T, Nishida S, Hashimoto S, Ito H. Cultured rat astrocytes give rise to neural stem cells. Neurochem Res 2006 31 : 1381 1387.
46. Lin RC, Matesic DF, Marvin M, McKay RD, Brüstle O. Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 1995 2 : 79 85.
47. Shi M, Wei LC, Cao R, Chen LW. Enhancement of nestin protein- immunoreactivity induced by ionizing radiation in the forebrain ependymal regions of rats. Neurosci Res 2002 44 : 475 481.
48. Iwai M, Ikeda T, Hayashi T et al. Temporal profile of neural stem cell proliferation in the subventricular zone after ischemia/hypoxia in the neonatal rat brain. Neurol Res 2006 28 : 461 468.
49. Krum JM, Rosenstein JM. Transient coexpression of nestin, GFAP, and vascular endothelial growth factor in mature reactive astroglia following neural grafting or brain wounds. Exp Neurol 1999 160 : 348 360.
50. Maurer MH, Tripps WK, Feldmann RE Jr., Kuschinsky W. Expression of vascular endothelial growth factor and its receptors in rat neural stem cells. Neurosci Lett 2003 344 : 165 168.
51. Kalyani AJ, Mujtaba T, Rao MS. Expression of EGF and FGF receptor isoforms during neuroepithelial stem cell differentiation. J Neurobiol 1999 38 : 207 224.
52. Jin K, Mao XO, Sun Y, Xie L, Greenberg DA. Stem cell factor stimulates neurogenesis in vitro and in vivo. J Clin Invest 2002 110 : 311 319.
53. Lee HJ, Kim KS, Park IH, Kim SU. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS ONE 2007 2 : e156.
54. Sun Y, Jin K, Xie L et al. F-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 2003 111 : 1843 1851.
55. Matsuoka N, Nozaki K, Takagi Y et al. Adenovirus-mediated gene transfer of fibroblast growth factor-2 increases BrdU-positive cells after forebrain ischemia in gerbils. Stroke 2003 34 : 1519 1525.