Human nerual stem cells for brain repair

International Journal of Stem Cells

Volumn 1, Issue 1, 2008, Pages 27-35

  Kim, Seung U ^a,b   Lee, Hong J ^a   Park, In H ^a   Chu, Kon ^c   Lee, Soon T ^c   Kim, Manho ^c   Roh, Jae K ^c   Kim, Seung K ^c   Wang, Kyu C ^c  

^a Gachon University Gil Hospital   (South Korea)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c Seoul National University Hospital   (South Korea)

Author keywords

Amyotrophic lateral sclerosis; Brain cancer; Cell therapy; Gene transfer; Human neural stem cell; Huntington disease; Neurodegenrative diseases; Parkinson disease; Stem cell; Stroke; Transplantation

Indexed keywords

EID: 78349255864     PISSN: 20053606     EISSN: 20055447     Source Type: Journal    
DOI: 10.15283/ijsc.2008.1.1.27     Document Type: Review

References (80)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell line derived from human blastocysts. Science 1998;282: 1145-1147.
2. Shamblott MJ, Axelman J, Wang S, Bugg EM, Littlefield JW, Donovan PJ, Blumenthal PD, Huggins GR, Gearhart JD. Derivation of pluripotent stem cells from cultured juman primordial germ cells. Proc Natl Acad Sci USA 1998; 95:13726-13731.
3. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318: 1917-1920.
4. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-872.
5. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008;415:141-146.
6. Flax JD, Aurora S, Yang C, Simonin C, Wills AM, Billinghurst LL, Jendoubi M, Sidman RL, Wolfe JH, Kim SU, Snyder EY. Engraftable human neural stem cells re spond to developmental cues, replace neurons and express foreign genes. Nat Biotechnol 1998;16:1033-1039.
7. Kim SU. Human neural stem cells genetically modified for brain repair in neurological disorders. Neuropathology 2004;24:159-174.
8. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Medicine 2004;10 suppl:S42-S50.
9. Goldman S. Stem and progenitor cell-based therapy of the human central nervous system. Nat Biotech 2005;7:862-871.
10. Cho TS, Bae JH, Choi HB, Kim SS, Suh-Kim H, McLarnon J, Min CK, Kim SU. Human neural stem cells: Electrophysiological properties of voltage gated ion channels. Neuroreport 2002;13:1447-1452.
11. Ryu JK, Choi HB, Hatori K, Heisel R, Pelech S, McLarnon JG, Kim SU. Adenosine triphosphate induces proliferation of human neural stem cells: Role of calcium and p70 ribosomal protein S6 kinase. J Neurosci Res 2003;72:352-362.
12. Kim SU, Nagai A, Nakagawa E, Choi HB, Ban JH, Lee HJ, Lee MA, Lee YB, Park IH. Production and characterization of immortal human neural stem cell line with multipotent differentiation property. Methods Mol Biol 2008;438:103-121.
13. Chu K, Kim M, Jung KH, Jeon D, Lee ST, Kim J, Jeong SW, Kim SU, Lee SK, Shin HS, Roh JK. Human neural stem cell transplantation reduces spontaneous recurrent seizures following pilocarpine-induced status epilepticus in adult rats. Brain Res 2004;1023:213-221.
14. Meng X, Shen J, Ohashi T, Sly WS, Kim SU, Eto Y. Brain transplantation of genetically engineered human neural stem cells globally corrects brain lesions in mucopolysaccharidosis VII mouse. J Neurosci Res 2003;74:266-277.
15. Kish SJ, Shannak K, Hornykiewitcz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med 1988;318:876-880.
16. Agid Y. Parkinson's disease: Pathophysiology. Lancet 1991; 337:1321-1324.
17. Lang AE, Lozano AM. Parkinson's disease. First of two parts. N Engl J Med 1998;339:1044-1053.
18. Lang AE, Lozano AM. Parkinson's disease. Second of two parts. N Engl J Med 1998;339:1130-1143.
19. Lindvall O, Brundin P, Widner H, Rehncrona S, Gustavii B, Frackowiak R, Leenders KL, Sawle G, Rothwell JC, Marsden CD. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science 1990;247:574-577.
20. Olanow CW, Kordower J, Freeman T. Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci 1996;19:102-109.
21. Kordower JH, Goetz CG, Freeman TB, Olanow CW. Doparminergic transplants in patients with Parkinson's disease: Neuroanatomical correlates of clinical recovery. Exp Neurol 1997;144:41-46.
22. Hagell P, Brundin P. Cell survival and clinical outcome following intrastriatal transplantation in Parkinson disease. J Neuropath Exp Neurol 2002;60:741-752.
23. Yasuhara T, Matsukawa N, Hara K, Yu G, Xu L, Maki M, Date I, Yoon YI, Kim SU, Borlongan CV. Transplantation of neural stem cells exerts neuroprotection in a rat model of Parkinson disease. J Neurosci 2006;26:124497-12511.
24. Wolff JA, Fisher LJ, Xu L, Jinnah HA, Langlais PJ, Iuvone PM, O'Malley KL, Rosenberg MB, Shimohama S, Friedmann T. Grafting fibroblasts genetically modified to produce L-dopa in a rat model of Parkinson disease. Proc Natl Acad Sci USA 1989;86:9011-9014.
25. Fisher LJ, Jinnah HA, Kale LC, Higgins GA, Gage FH. Survival and function of intrastriatally grafted primary fibroblasts genetically modified to produce L-DOPA. Neuron 1991;6:371-380.
26. Kang UJ, Fisher LJ, Joh TH, O'Malley KL, Gage FH. Regulation of dopamine production by genetically modified primary fibroblasts. J Neurosci 1993;13:5203-5211.
27. Bencsics C, Wachtel SR, Milstien S, Hatakeyama K, Becker JB, Kang UJ. Double transduction with GTP cyclohydrolase1 and tyrosine hydroxylase is necessary for spontaneous synthesis of L-DOPA by primary fibroblasts. J Neurosci 1996;16:4449-4456.
28. Kim SU, Park IH, Kim TH, Kim KS, Choi HB, Hong SH, Bang JH, Lee MA, Joo IS, Lee CS, Kim YS. 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 2006;26:129-140.
29. Greenamyre JT, Shoulson I. Huntington disease. In: Calne D, editor. Neurodegenrative Disease. Philadelphia: WB Saunders; 1994. 65-704.
30. Harper PS. Huntington's disease. Philadelphia: W.B. Saunders; 1996.
31. Bachoud-Lévi AC, Rémy P, Nuyen JP, Brugières P, Lefaucheur JP, Bourdet C, Baudic S, Gaura V, Maison P, Haddad B, Boissé MF, Grandmougin T, Jény R, Bartolomeo P, Barba GD, Degos JD, Lisovoski F, Ergis AM, Pailhous E, Cesaro P, Hantraye P, Peschanski D. Motor and cognitive improvements in patients with Huntington's disease after neural transplnatation. Lancet 2000;356:1975-1979.
32. DiFiglia M. Excitotoxic injury of the neostriatum: A model for Huntington's disease. Trends Neurosci 1990;13:286-289.
33. Lee ST, Chu K, Park JE, Lee K, Kang L, Kim SW, Kim M. Intravenous administration of human neural stem cells induces functional recovery in Huntington's disease rat model. Neurosci Res 2005;52:243-249.
34. Lee ST, Park JE, Lee K, Kang L, Chu K, Kim SU, Kim M, Roh JK. Noninvasive method of immortalized neural stem-like cell transplantation in an experimental model of Huntington's disease. J Neurosci Meth 2006;52:250-254.
35. Beal MF, Brouillet E, Jenkins BG, Ferrante RJ, Kowall NW, Miller JM, Storey E, Srivastava R, Rosen BR, Hyman BT. Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J Neurosci 1993;13:4181-4192.
36. Ryu JK, Kim J, Cho SJ, Hatori K, Nagai A, Choi HB, Lee MC, McLarnon JG, Kim SU. Proactive transplantation of human neural stem cells blocks neuronal cell death in rat model of Huntington disease. Neurobiol Disease 2004;16: 68-77.
37. Kim M, Lee ST, Chu K, Kim SU. Stem cell-based cell therapy for Huntington disease: A review. Neuropathology 2008;28:1-9.
38. Hudson AJ. Amyotrophic Lateral Sclerosis: Concepts in Pathogenesis and Etiology. Toronto: University of Toronto Press; 1990.
39. Rowland LP, Shneider NA. Amyotrophic lateral sclerosis. New Engl J Med 2001;344:1688-1700.
40. Klein SM, Behrstock S, McHugh J, Hoffmann K, Wallace K, Suzuki M, Aebischer P, Svendsen CN. GDNF delivery using human neural progenitor cells in a rat model of ALS. Human Gene Ther 2005;16:509-521.
41. Azzouz M, Ralph GS, Storkebaum E, Walmsley LE, Mitrophanous KA, Kingsman SM, Carmeliet P, Mazarakis ND. VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 2004;429:413-417.
42. Gurney ME, Pu H, Chiu AY, et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994;264:1772-1775.
43. Kim SU, Hwang DH, Kim BG, Park IH, Joo IS. Human neural stem cells over-expressing VEGF provide behavioral improvement, disease onset delay and survival extension in transgenic ALS mice. Mol Ther 2008;16 Suppl 1:S32.
44. Marshall J, Thomas DJ. Cerebrovascular disease. In: Asbury A, McKhann G, McDonald W, editors. Diseases of the Nervous System. Philadelphia: WB Saunders; 1988. 1101-1135.
45. Savitz SI, Rosenbaum DM, Dinsmore JH, Wechsler LR, Caplan LR. Cell transplantation for stroke. Ann Neurol 2002;52:266-275.
46. 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 forbrain ischemia. Neuroci Lett 2003;343:637-643.
47. Sinn DI, Lee ST, Chu K, Jung KH, Kim EH, Kim JM, Park DK, Song EC, Kim BS, Yoon SS, Kim M, Roh JK. Combined treatment of vascular endothelial growth factor and human neural stem cells in experimental focal cerebral ischemia. Neurosci Res 2005;53:384-390.
48. Jeong SW, Chu K, Kim MH, Kim SU, Roh JK. Human neural stem cell transplantation in experimental intracerebral hemorrhage. Stroke 2003;34:2258-2263.
49. Lee HJ, Kim KS, Kim EJ, Choi HB, Lee KH, Park IH, Ko Y, Jeong SW, Kim SU. Brain transplantation of human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 2007;25:211-224.
50. Lee HJ, Kim KS, Kim EJ, Park IH, Kim SU. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS One 2007;1/e156:1-14.
51. Chu K, Jung K, Kim SJ, Lee ST, Kim J, Park HK, Song E, Kim SU, Kim M, Lee SK, Roh JK. Transplantation of human neural stem cells protect against ischemia in a preventive mode via hypoxia-inducible factor-1α stabilization in the host brain. Brain Res 2008;1207:182-192.
52. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, Sharp FR. Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol 2000;48:285-296.
53. Lee ST, Chu K, Jung KH, Kim SJ, Kim DH, Kang KM, Hong NH, Kim JH, Ban JJ, Park HK, Kim SU, Park CG, Lee SK, Kim M, Roh JK. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in hemorrhagic stroke. Brain 2008;26:1-14.
54. Black PM, Loeffler J. Cancer of the Nervous System. Blackwell: Oxford; 2005.
55. Packer RJ, Cogen P, Vezina G, Rorke LB. Medulloblastoma: clinical and biologic aspects. Neuro-oncol 1999;1:232-250.
56. Surawicz TS, McCarthy BJ, Kupelian V, Jukich P, Bruner JM, Davis FG. Descriptive epidemiology of primary brain and CNS tumors: results from the central brain tumor registry of the United States, 1990-1994. Neuro-Oncology 1999;1: 14-25.
57. Edelstein ML, Abedi MR, Wixon J. Gene therapy clinical trials worldwide to 2007-an update. J Gene Med 2007;9:833-842.
58. Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, Breakefield XO, Snyder EY. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 2000;97: 12846-12851.
59. Brown AB, Yang W, Schmidt NO, Carroll R, Leishear KK, Rainov NG, Black PM, Breakefield XO, Aboody KS. Intravascular delivery of neural stem cell lines to target intracranial and extracranial tumors of neural and non-neural origin. Hum Gene Ther 2003;14:1777-1785.
60. Schmidt NO, Przylecki W, Yang W, Ziu M, Teng Y, Kim SU, Black PM, Aboody KS, Carroll RS. Brain tumor tropism of transplanted human neural stem cells is induced by vascular endothelial growth factor. Neoplasia 2005;7:623-629.
61. Kendall SE, Najbauer J, Johnston HF, Metz MZ, Li S, Bowers M, Garcia E, Kim SU, Barish ME, Aboody KS, Glackin CA. Neural stem cell targeting of glioma is dependent on phosphoinositide 3-kinase signaling. Stem Cells 2008;26:1575-1586.
62. Najbauer J, Danks MK, Schmidt NO, Kim SU, Aboody KS. Neural stem cell-mediated therapy of primary and metastatic solid tumors. In: Bertolotti R, Ozawa K, editors. Progress in Gene Therapy, Autologous and Cancer Stem Cell Gene Therapy. Vol 3: World Scientific; 2007.
63. Lin D, Najbauer J, Salvaterra PM, Mamelak AN, Barish ME, Garcia E, Metz MZ, Kendall SE, Bowers M, Kateb B, Kim SU, Johnson M, Aboody KS. Novel method for visualizing and modeling the spatial distribution of neural stem cells within intracranial glioma. Neuroimage 2007;37 suppl 1:S18-S26.
64. Aboody KS, Bush RA, Garcia E, Metz MZ, Najbauer J, Justus KA, Phelps DA, Remack JS, Yoon KJ, Gillespie S, Kim SU, Glackin CA, Potter PM, Danks MK. Development of a tumor-selective approach to treat metastatic cancer. PLoS ONE 2006;1/e23:1-8.
65. Danks MK, Yoon KJ, Bush RA, Remack JS, Wierdl M, Tsurkan L, Kim SU, Garcia E, Metz MZ, Najbauer J, Potter PM, Aboody KS. Tumor-targeted enzyme/prodrug therapy mediates long-term disease-free survival of mice bearing disseminated neuroblastoma. Cancer Res 2007;67:22-25.
66. Shimato S, Natsume A, Takeuchi H, Wakabayashi T, Fujii M, Ito M, Ito S, Park IH, Bang JH, Kim SU, Yoshida J. Human neural stem cells target and deliver therapeutic gene to experimental leptomeningeal medulloblastoma. Gene Ther 2007;14:1132-1142.
67. Kim SK, Kim SU, Park IH, Bang JH, Aboody KS, Wang KC, Cho BK, Kim M, Menon LG, Black PM, Carroll RS. Human neural stem cells target experimental intracranial medulloblastoma and deliver a therapeutic gene leading to tumor regression. Clin Cancer Res 2006;12:5550-5556.
68. Kim SK, Cargioli TG, Machluf M, Yang W, Sun Y, Al-Hashem R, Kim SU, Black PM, Carroll RS. PEX-producing human neural stem cells inhibit tumor growth in a mouse glioma model. Clin Cancer Res 2005;11:5965-5970.
69. Dickson PV, Hamner JB, Burger RA, Garcia E, Ouma AA, Kim SU, Ng CY, Gray JT, Aboody KS, Danks MK, Davidoff AM. Intravascular administration of tumor tropic neural progenitor cells permits targeted delivery of IFN-β and restricts tumor growth in a murine model of disseminated neuroblastoma. J Ped Surg 2007;42:48-53.
70. Moolten FL, Wells JM. Curability of tumors bearing hepes simplex thymidine kinase genes transferred by retroviral vectors. J Natl Cancer Inst 1990;82:297-300.
71. Culver KW, Ram Z, Wallbridge S, Ishii H, Oldfield EH, Blaese RM. In vivo gene transfer with retroviral vector producing cells for treatment of experimental brain tumors. Science 1992;256:1550-1552.
72. Huber BE, Austin EA, Richards CA, Davis S, Good SS. Metabolism of 5-FC to 5-FU in human colorectal tumor cells transduced with the cytosine deaminase gene: significant antitumor effects when only a small percentage of tumor cells express cytosine deaminase. Proc Natl Acad Sci USA 1994;91:8302-8306.
73. Li Z, Shanmugam N, Katayose D, Huber B, Srivastava S, Cowan K, Seth P. Enzyme/prodrug gene therapy approach for breast cancer using a recombinant adenovirus expressing E coli cytosine deaminase. Cancer Gene Ther 1997;4:113-117.
74. Danks MK, Morton CI, Pawlik CA, Potter CM. Overexpression of a rabbit liver carboxylesterase sensitizes human tumor cells to CPT-11. Cancer Res 1998;58:20-22.
75. Bello L, Lucini V, Carrabba G, Giussani C, Machluf M, Pluderi M, Nikas D, Zhang J, Tomei G, Villani RM, Carroll RS, Bikfalvi A, Black PM. Simultaneous inhibition of glioma angiogenesis, cell proliferation, and invasion by a naturally occurring fragment of human metaloproteinase-2. Cancer Res 2001;61:8730-8736.
76. Ostrand-Rosenberg S, GuntherVS, Armstrong TA, et al. Immunologic targets for the gene therapy of cancer. In: Lattime FC, Gerson SL, editors. Gene Therapy of Cancer. San Diego: Academic Press; 1999. 33-48.
77. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biocehm 1998;67:227-264.
78. Streck CJ, Dickson PV, Ng CY, Zhou J, Hall MM, Gray JT, Nathwani AC, Davidoff AM. Antitumor efficacy of AAVmediated delivery of Interferon-beta. Cancer Gene Ther 2006;13:99-106.
79. Yoshida J, Mizuno M, Wakabayashi T. Interferon-β gene therapy for cancer: Basic research to clinical application. Cancer Sci 2004;95:858-865.
80. Najbauer J, Danks MK, Kim SU, Metz M, Garcia E, Aramburo S, Valenzuela V, Gutova M, Zhao D, Thu M, Frank R, Bowers M, Laszlo S, Barish M, Glackin C, Aboody KS. Neural stem cell mediated tumor-selective gene delivery: towards high grade glioma clinical trials. Mol Ther 2008;16 Suppl 1:S136.