Gene transfer mediated by stem cell grafts to treat CNS injury

Expert Opinion on Biological Therapy

Volumn 11, Issue 12, 2011, Pages 1599-1610

  Hwang, Dong H ^a   Jeong, Soo R ^a   Kim, Byung G ^a,b  

^a Ajou University School of Medicine   (South Korea)

^b Department of Neurology ^*  (South Korea)

Author keywords

CNS injury; gene transfer; neurotrophic factor; stem cell

Indexed keywords

GROWTH FACTOR; NEUROTROPHIC FACTOR;

BIOLOGICAL ACTIVITY; CENTRAL NERVOUS SYSTEM DISEASE; CLINICAL EFFECTIVENESS; GENE DELIVERY SYSTEM; GENE INTERACTION; GENE TARGETING; GENE TRANSFER; MICROENVIRONMENT; NEUROPROTECTION; REVIEW; RISK ASSESSMENT; STEM CELL GENE THERAPY; STEM CELL TRANSPLANTATION;

ANIMALS; BRAIN INJURIES; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; NERVE GROWTH FACTORS; NERVE REGENERATION; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; TREATMENT OUTCOME;

EID: 80555144185     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.2011.631908     Document Type: Review

References (98)

1. Auriel E, Bornstein NM. Neuroprotection in acute ischemic stroke-current status. J Cell Mol Med 2010;14:2200-2
2. Nesathurai S. Steroids and spinal cord injury: revisiting the NASCIS 2 and NASCIS 3 trials. J Trauma 1998;45:1088-93
3. Jain KK. Neuroprotection in traumatic brain injury. Drug Discov Today 2008;13:1082-9
4. Fisher M. New approaches to neuroprotective drug development. Stroke 2011;42:S24-7
5. Shuaib A, Hussain MS. The past and future of neuroprotection in cerebral ischaemic stroke. Eur Neurol 2008;59:4-14
6. Lu P, Jones LL, Snyder EY, Tuszynski MH. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 2003;181:115-29
7. Tang Y, Yasuhara T, Hara K, et al. Transplantation of bone marrow-derived stem cells: a promising therapy for stroke. Cell Transplant 2007;16:159-69
8. Park KI, Teng YD, Snyder EY. The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue. Nat Biotechnol 2002;20:1111-17
9. Cao Q, He Q, Wang Y, et al. Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 2010;30:2989-3001
10. Yamashita T, Deguchi K, Nagotani S, et al. Gene and stem cell therapy in ischemic stroke. Cell Transplant 2009;18:999-1002
11. Blesch A, Lu P, Tuszynski MH. Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair. Brain Res Bull 2002;57:833-8
12. Taha MF. Cell based-gene delivery approaches for the treatment of spinal cord injury and neurodegenerative disorders. Curr Stem Cell Res Ther 2010;5:23-36
13. Blits B, Boer GJ, Verhaagen J. Pharmacological, cell, and gene therapy strategies to promote spinal cord regeneration. Cell Transplant 2002;11:593-613
14. Park IH, Zhao R, West JA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008;451:141-6
15. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-72
16. Naegele JR, Maisano X, Yang J, et al. Recent advancements in stem cell and gene therapies for neurological disorders and intractable epilepsy. Neuropharmacology 2010;58:855-64
17. Wright KT, El Masri W, Osman A, et al. Concise review: bone marrow for the treatment of spinal cord injury: mechanisms and clinical applications. Stem Cells 2011;29:169-78
18. Naldini L. Ex vivo gene transfer and correction for cell-based therapies. Nat Rev Genet 2011;5:301-15
19. Imitola J, Raddassi K, Park KI, et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci USA 2004;101:18117-22
20. Benedetti S, Pirola B, Pollo B, et al. Gene therapy of experimental brain tumors using neural progenitor cells. Nat Med 2000;6:447-50
21. Aboody KS, Brown A, Rainov NG, et al. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci USA 2000;97:12846-51
22. Sykova E, Jendelova P. In vivo tracking of stem cells in brain and spinal cord injury. Prog Brain Res 2007;161:367-83
23. Rosenkranz K, Kumbruch S, Lebermann K, et al. The chemokine SDF-1/CXCL12 contributes to the homing' of umbilical cord blood cells to a hypoxic-ischemic lesion in the rat brain. J Neurosci Res 2010;88:1223-33
24. Ahmed AU, Tyler MA, Thaci B, et al. A comparative study of neural and mesenchymal stem cell-based carriers for oncolytic adenovirus in a model of malignant glioma. Mol Pharm 2011;8:1559-72
25. Wang JM, Zeng YS, Wu JL, et al. Cograft of neural stem cells and Schwann cells overexpressing TrkC and neurotrophin-3 respectively after rat spinal cord transection. Biomaterials 2011;32:7454-68
26. Bonner JF, Connors TM, Silverman WF, et al. Grafted neural progenitors integrate and restore synaptic connectivity across the injured spinal cord. J Neurosci 2011;31:4675-86
27. 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
28. Hwang DH, Kim HM, Kang YM, et al. Combination of multifaceted strategies to maximize the therapeutic benefits of neural stem cell transplantation for spinal cord repair. Cell Transplant 2011;published online 1 July 2011; doi: 10.3727/096368910X557155
29. Lee SI, Kim BG, Hwang DH, et al. Overexpression of Bcl-XL in human neural stem cells promotes graft survival and functional recovery following transplantation in spinal cord injury. J Neurosci Res 2009;87:3186-97
30. Lee HJ, Park IH, Kim HJ, Kim SU. Human neural stem cells overexpressing glial cell line-derived neurotrophic factor in experimental cerebral hemorrhage. Gene Ther 2009;16:1066-76
31. Kurozumi K, Nakamura K, Tamiya T, et al. Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model. Mol Ther 2005;11:96-104
32. Kurozumi K, Nakamura K, Tamiya T, et al. BDNF gene-modified mesenchymal stem cells promote functional recovery and reduce infarct size in the rat middle cerebral artery occlusion model. Mol Ther 2004;9:189-97
33. Lu P, Jones LL, Tuszynski MH. BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury. Exp Neurol 2005;191:344-60
34. Sasaki M, Radtke C, Tan AM, et al. BDNF-hypersecreting human mesenchymal stem cells promote functional recovery, axonal sprouting, and protection of corticospinal neurons after spinal cord injury. J Neurosci 2009;29:14932-41
35. Romero MI, Rangappa N, Li L, et al. Extensive sprouting of sensory afferents and hyperalgesia induced by conditional expression of nerve growth factor in the adult spinal cord. J Neurosci 2000;20:4435-45
36. Totoiu MO, Keirstead HS. Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol 2005;486:373-83
37. Keirstead HS, Nistor G, Bernal G, et al. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 2005;25:4694-705
38. Kim HM, Hwang DH, Lee JE, et al. Ex vivo VEGF delivery by neural stem cells enhances proliferation of glial progenitors, angiogenesis, and tissue sparing after spinal cord injury. PLoS One 2009;4:e4987
39. Bradbury EJ, Moon LD, Popat RJ, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002;416:636-40
40. Hellal F, Hurtado A, Ruschel J, et al. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 2011;331:928-31
41. Asher RA, Morgenstern DA, Fidler PS, et al. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 2000;20:2427-38
42. Logan A, Green J, Hunter A, et al. Inhibition of glial scarring in the injured rat brain by a recombinant human monoclonal antibody to transforming growth factor-beta2. Eur J Neurosci 1999;11:2367-74
43. Moon LD, Fawcett JW. Reduction in CNS scar formation without concomitant increase in axon regeneration following treatment of adult rat brain with a combination of antibodies to TGFbeta1 and beta2. Eur J Neurosci 2001;14:1667-77
44. Jeong SR, Jang DY, Kim SS, et al. Hepatocyte growth factor inhibits glial scar formation and decreases production of chondroitin sulfate proteoglycans after spinal cord injury. Program No. 365.5/ CC74. 2009 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009
45. Iannotti CA, Clark M, Horn KP, et al. A combination immunomodulatory treatment promotes neuroprotection and locomotor recovery after contusion SCI. Exp Neurol 2011;1:3-15
46. Pluchino S, Zanotti L, Rossi B, et al. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 2005;436:266-71
47. Ben-Hur T. Immunomodulation by neural stem cells. J Neurol Sci 2008;265:102-4
48. Madri JA. Modeling the neurovascular niche: implications for recovery from CNS injury. J Physiol Pharmacol 2009;60(Suppl 4):95-104
49. Shyu WC, Lin SZ, Yen PS, et al. Stromal cell-derived factor-1alpha promotes neuroprotection, angiogenesis, and mobilization/homing of bone marrow-derived cells in stroke rats. J Pharmacol Exp Ther 2008;324:834-49
50. Makri G, Lavdas AA, Katsimpardi L, et al. Transplantation of embryonic neural stem/precursor cells overexpressing BM88/Cend1 enhances the generation of neuronal cells in the injured mouse cortex. Stem Cells 2010;28:127-39
51. Papastefanaki F, Chen J, Lavdas AA, et al. Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 2007;130:2159-74
52. Hargus G, Cui Y, Schmid JS, et al. Tenascin-R promotes neuronal differentiation of embryonic stem cells and recruitment of host-derived neural precursor cells after excitotoxic lesion of the mouse striatum. Stem Cells 2008;26:1973-84
53. Chen J, Bernreuther C, Dihne M, Schachner M. Cell adhesion molecule L1-transfected embryonic stem cells with enhanced survival support regrowth of corticospinal tract axons in mice after spinal cord injury. J Neurotrauma 2005;22:896-906
54. Miki Y, Nonoguchi N, Ikeda N, et al. Vascular endothelial growth factor gene-transferred bone marrow stromal cells engineered with a herpes simplex virus type 1 vector can improve neurological deficits and reduce infarction volume in rat brain ischemia. Neurosurgery 2007;61:586-94
55. Rosenstein JM, Krum JM. New roles for VEGF in nervous tissue - beyond blood vessels. Exp Neurol 2004;187:246-53
56. Jin K, Zhu Y, Sun Y, et al. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 2002;99:11946-50
57. Onda T, Honmou O, Harada K, et al. Therapeutic benefits by human mesenchymal stem cells (hMSCs) and Ang-1 gene-modified hMSCs after cerebral ischemia. J Cereb Blood Flow Metab 2008;28:329-40
58. Liu H, Honmou O, Harada K, et al. Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain 2006;129:2734-45
59. Toyama K, Honmou O, Harada K, et al. Therapeutic benefits of angiogenetic gene-modified human mesenchymal stem cells after cerebral ischemia. Exp Neurol 2009;216:47-55
60. Maina F, Klein R. Hepatocyte growth factor, a versatile signal for developing neurons. Nat Neurosci 1999;2:213-17
61. Zhao MZ, Nonoguchi N, Ikeda N, et al. Novel therapeutic strategy for stroke in rats by bone marrow stromal cells and ex vivo HGF gene transfer with HSV-1 vector. J Cereb Blood Flow Metab 2006;26:1176-88
62. Shi E, Jiang X, Wang L, et al. Intrathecal injection of hepatocyte growth factor gene-modified marrow stromal cells attenuates neurologic injury induced by transient spinal cord ischemia in rabbits. Anesthesiology 2010;113:1109-17
63. Liu JP, Baker J, Perkins ASL, et al. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r).Cell 1993;75:59-72
64. Ozdinler PH, Macklis JD. IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat Neurosci 2006;9:1371-81
65. Hollis ER II, Lu P, Blesch A, Tuszynski MH. IGF-I gene delivery promotes corticospinal neuronal survival but not regeneration after adult CNS injury. Exp Neurol 2009;215:53-9
66. Rabinovich GA, Baum LG, Tinari N, et al. Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends Immunol 2002;23:313-20
67. Ishibashi S, Kuroiwa T, Sakaguchi M, et al. Galectin-1 regulates neurogenesis in the subventricular zone and promotes functional recovery after stroke. Exp Neurol 2007;207:302-13
68. Horie H, Kadoya T, Hikawa N, et al. Oxidized galectin-1 stimulates macrophages to promote axonal regeneration in peripheral nerves after axotomy. J Neurosci 2004;24:1873-80
69. Yamane J, Nakamura M, Iwanami A, et al. Transplantation of galectin-1-expressing human neural stem cells into the injured spinal cord of adult common marmosets. J Neurosci Res 2010;88:1394-405
70. Kim BG, Hwang DH, Lee SI, et al. Stem cell-based cell therapy for spinal cord injury. Cell Transplant 2007;16:357-66
71. Snyder EY, Park KI. Limitations in brain repair. Nat Med 2002;8:928-30
72. Okada S, Ishii K, Yamane J, et al. In vivo imaging of engrafted neural stem cells: its application in evaluating the optimal timing of transplantation for spinal cord injury. FASEB J 2005;19:1839-41
73. Hill CE, Guller Y, Raffa SJ, et al. A calpain inhibitor enhances the survival of Schwann cells in vitro and after transplantation into the injured spinal cord. J Neurotrauma 2010;27:1685-95
74. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, et al. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 2006;26:3377-89
75. Ikegami T, Nakamura M, Yamane J, et al. Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur J Neurosci 2005;22:3036-46
76. Kim BG, Dai HN, Lynskey JV, et al. Degradation of chondroitin sulphate proteoglycans potentiates transplant-mediated axonal remodelling and functional recovery after spinal cord injury in adult rats. J Comp Neurol 2006;497:182-98
77. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, et al. Synergistic effects of transplanted adult neural stem/ progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci 2010;30:1657-76
78. Nomura H, Tator CH, Shoichet MS. Bioengineered strategies for spinal cord repair. J Neurotrauma 2006;23:496-507
79. Teng YD, Lavik EB, Qu X, et al. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci USA 2002;99:3024-9
80. Kim BG, Kang YM, Phi JH, et al. Implantation of polymer scaffolds seeded with neural stem cells in a canine spinal cord injury model. Cytotherapy 2010;12:841-5
81. Hanna J, Wernig M, Markoulaki S, et al. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 2007;318:1920-3
82. Okita K, Nakagawa M, Hyenjong H, et al. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008;322:949-53
83. Stadtfeld M, Nagaya M, Utikal J, et al. Induced pluripotent stem cells generated without viral integration. Science 2008;322:945-9
84. Gutierrez-Aranda I, Ramos-Mejia V, Bueno C, et al. Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells 2010;28:1568-70
85. Straley KS, Foo CW, Heilshorn SC. Biomaterial design strategies for the treatment of spinal cord injuries. J Neurotrauma 2009;27:1-19
86. Potter W, Kalil RE, Kao WJ. Biomimetic material systems for neural progenitor cell-based therapy. Front Biosci 2008;13:806-21
87. Silva GA, Czeisler C, Niece KL, et al. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2004;303:1352-5
88. Tuszynski MH, Thal L, Pay M, et al. A phase I clinical trial of nerve growthfactor gene therapy for Alzheimer disease.Nat Med 2005;11:551-5
89. Tuszynski MH, Roberts J, Senut MC, et al. Gene therapy in the adult primate brain: intraparenchymal grafts of cells genetically modified to produce nerve growth factor prevent cholinergic neuronal degeneration. Gene Ther 1996;3:305-14
90. Conner JM, Darracq MA, Roberts J, Tuszynski MH. Nontropic actions of neurotrophins: subcortical nerve growth factor gene delivery reverses age-related degeneration of primate cortical cholinergic innervation. Proc Natl Acad Sci USA 2001;98:1941-6
91. Lindholm P, Voutilainen MH, Lauren J, et al. Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 2007;448:73-7
92. Honma Y, Araki T, Gianino S, et al. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 2002;35:267-82
93. Yabe T, Sanagi T, Yamada H. The neuroprotective role of PEDF: implication for the therapy of neurological disorders. Curr Mol Med 2010;10:259-66
94. Ruff CA, Wilcox JT, Fehlings MG. Cell-based transplantation strategies to promote plasticity following spinal cord injury. Exp Neurol 2011;published online 17 February 2011; doi:10.1016/j.expneurol.2011.02.010
95. Hacein-Bey-Abina S, Hauer J, Lim A, et al. Efficacy of gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2010;363:355-64
96. Aiuti A, Cattaneo F, Galimberti S, et al. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N Engl J Med 2009;360:447-58
97. Howe SJ, Mansour MR, Schwarzwaelder K, et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest 2008;118:3143-50
98. Cartier N, Hacein-Bey-Abina S, Bartholomae CC, et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 2009;326:818-23