Intraspinal delivery of neurotrophin-3 using neural stem cells genetically modified by recombinant retrovirus

Experimental Neurology

Volumn 158, Issue 1, 1999, Pages 9-26

  Liu, Y ^a   Himes, B T ^a,b   Solowska, J ^a   Moul, J ^a   Chow, S Y ^a   Park, K I ^c   Tessler, A ^a,b   Murray, M ^a   Snyder, E Y ^c   Fischer, I ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Gene therapy; Immunosuppression; Neurotransplantation; Spinal cord injury; Xenograft

Indexed keywords

NEUROTROPHIN 3; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE THERAPY; GRAFT SURVIVAL; HISTOPATHOLOGY; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT; RETROVIRUS; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; TREATMENT OUTCOME;

EID: 0032818773     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7079     Document Type: Article

References (67)

1. Acheson A., Conover J. C., Fandl J. P., DeChiara T. M., Russell M., Thadani A., Squinto S. P., Yancopoulos G. D., Lindsay R. M. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature. 374:1995;450-453.
2. Aebischer P., Tresco P. A., Winn S. R., Greene L. A., Jaeger C. B. Long-term cross-species brain transplantation of a polymer-encapsulated dopamine-secreting cell line. Exp. Neurol. 111:1991;269-275.
3. Anton R., Kordower J. H., Maidment N. T., Manaster J. S., Kane D. J., Rabizadeh S., Schueller S. B., Yang J., Rabizadeh S., Edwards R. H. Neural-targeted gene therapy for rodent and primate hemiparkinsonism. Exp. Neurol. 127:1994;207-218.
4. Archer D. R., Leven S., Duncan I. D. Myelination by cryopreserved xenografts and allografts in the myelin-deficient rat. Exp. Neurol. 125:1994;268-277.
5. Bjorklund A., Stenevi U., Dunnett S. B., Gage F. H. Cross-species neural grafting in a rat model of Parkinson's disease. Nature. 298:1982;652-654.
6. Boyne L., Martin K., Hockfield S., Fischer I. Expression and distribution of phosphorylated MAP1B in growing axons of cultured hippocampal neurons. J. Neurosci. Res. 40:1995;439-450.
7. Bregman B. S., Broude E., McAtee M., Kelley M. S. Transplants and neurotrophic factors prevent atrophy of mature CNS neurons after spinal cord injury. Exp. Neurol. 149:1998;13-27.
8. Bregman B. S., McAtee M., Dal H. N., Kuhn P. L. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp. Neurol. 148:1997;475-494.
9. Brundin P., Nilsson O. G., Gage F. H., Bjorklund A. Cyclosporin A increases survival of cross-species intrastriatal grafts of embryonic dopamine-containing neurons. Exp. Brain Res. 60:1985;204-208.
10. Brundin P., Widner H., Nilsson O. G., Strecker R. E., Bjorklund A. Intracerebral xenografts of dopamine neurons: the role of immunosuppression and the blood-brain barrier. Exp. Brain Res. 75:1989;195-207.
11. Cattaneo E., Magrassi L., Butti G., Santi L., Giavazzi A., Pezzotta S. A short term analysis of the behaviour of conditionally immortalized neuronal progenitors and primary neuroepithelial cells implanted into the fetal rat brain. Brain Res. Dev. Brain Res. 83:1994;197-208.
12. Cattaneo E., McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature. 347:1990;762-765.
13. Dahlstrand J., Lardelli M., Lendahl U. Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system. Brain Res. Dev. Brain Res. 84:1995;109-129.
14. Diener P. S., Bregman B. S. Fetal spinal cord transplants support growth of supraspinal and segmental projections after cervical spinal cord hemisection in the neonatal rat. J. Neurosci. 18:1998;779-793.
15. Diener P. S., Bregman B. S. Fetal spinal cord transplants support the development of target reaching and coordinated postural adjustments after neonatal cervical spinal cord injury. J. Neurosci. 18:1998;763-778.
16. Eaton M. J., Santiago D. I., Dancausse H. A., Whittemore S. R. Lumbar transplants of immortalized serotonergic neurons alleviate chronic neuropathic pain. Pain. 72:1997;59-69.
17. Finsen B., Poulsen P. H., Zimmer J. Xenografting of fetal mouse hippocampal tissue to the brain of adult rats: Effects of cyclosporin A treatment. Exp. Brain Res. 70:1988;117-133.
18. Fischer I., Romano-Clarke G. Association of microtubule-associated protein (MAP1B) with growing axons in cultured hippocampal neurons. Mol. Cell. Neurosci. 2:1991;39-51.
19. Friedman B., Hockfield S., Black J. A., Woodruff K. A. In situ demonstration of mature oligodendrocytes and their processes: An immunocytochemical study with a new monoclonal antibody, rip. Glia. 2:1989;380-390.
20. Ghattas I. R., Sanes J. R., Majors J. E. The encephalomyocarditis virus internal ribosome entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and in embryos. Mol. Cell. Biol. 11:1991;5848-5859.
21. Grill R., Murai K., Blesch A., Gage F. H., Tuszynski M. H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17:1997;5560-5572.
22. Himes B. T., Solowska-Baird J., Boyne L., Snyder E. Y., Tessler A., Fischer I. Grafting of genetically modified cells that produce neurotrophins in order to rescue axotomized neurons in rat spinal cord. Soc. Neurosci. Abstr. 537:1995.
23. Ibarra A., Guizar-Sahagun G., Correa D., Kretschmer R., Grijalva I. Alteration of cyclosporin-A pharmacokinetics after experimental spinal cord injury. J. Neurotrauma. 13:1996;267-272.
24. Jang S. K., Wimmer E. Cap-independent translation of encephalomyocarditis virus RNA: Structural elements of the internal ribosomal entry site and involvement of a cellular 57-kD RNA-binding protein. Genes Dev. 4:1990;1560-1572.
25. Kim D. G., Kang H. M., Jang S. K., Shin H. S. Construction of a bifunctional mRNA in the mouse by using the internal ribosomal entry site of the encephalomyocarditis virus. Mol. Cell. Biol. 12:1992;3636-3643.
26. Kitchens D. L., Snyder E. Y., Gottlieb D. I. FGF and EGF are mitogens for immortalized neural progenitors. J. Neurobiol. 25:1994;797-807.
27. Lacorazza H. D., Flax J. D., Snyder E. Y., Jendoubi M. Expression of human beta-hexosaminidase alpha-subunit gene (the gene defect of Tay-Sachs disease) in mouse brains upon engraftment of transduced progenitor cells. Nature Med. 2:1996;424-429.
28. Liu Y., Himes B. T., Moul J., Huang W. L., Chow S. Y., Tessler A., Fischer I. Application of recombinant adenovirus for in vivo gene delivery to spinal cord. Brain Res. 768:1997;19-29.
29. Liu Y., Himes B. T., Tryon B., Moul J., Chow S. Y., Jin H., Murray M., Tessler A., Fischer I. Intraspinal grafting of fibroblasts genetically modified by recombinant adenoviruses. NeuroReport. 9:1998;1075-1079.
30. Liu Y., Xia J., Ma D. L., Faber D. S., Fischer I. Tau-like proteins in the nervous system of goldfish. Neurochem. Res. 22:1997;1511-1516.
31. Lundberg C., Field P. M., Ajayi Y. O., Raisman G., Bjorklund A. Conditionally immortalized neural progenitor cell lines integrate and differentiate after grafting to the adult rat striatum: A combined autoradiographic and electron microscopic study. Brain Res. 737:1996;295-300.
32. Lundberg C., Martinez-Serrano A., Cattaneo E., McKay R. D., Bjorklund A. Survival, integration, and differentiation of neural stem cell lines after transplantation to the adult rat striatum. Exp. Neurol. 145:1997;342-360.
33. Mann R., Mulligan R. C., Baltimore D. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell. 33:1983;153-159.
34. Martinez-Serrano A., Bjorklund A. Immortalized neural progenitor cells for CNS gene transfer and repair. Trends Neurosci. 20:1997;530-538.
35. Martinez-Serrano A., Bjorklund A. Protection of the neostriatum against excitotoxic damage by neurotrophin-producing, genetically modified neural stem cells. J. Neurosci. 16:1996;4604-4616.
36. Martinez-Serrano A., Fischer W., Bjorklund A. Reversal of age-dependent cognitive impairments and cholinergic neuron atrophy by NGF-secreting neural progenitors grafted to the basal forebrain. Neuron. 15:1995;473-484.
37. Martinez-Serrano A., Fischer W., Soderstrom S., Ebendal T., Bjorklund A. Long-term functional recovery from age-induced spatial memory impairments by nerve growth factor gene transfer to the rat basal forebrain. Proc. Natl. Acad. Sci. USA. 93:1996;6355-6360.
38. Martinez-Serrano A., Hantzopoulos P. A., Bjorklund A. Ex vivo gene transfer of brain-derived neurotrophic factor to the intact rat forebrain: Neurotrophic effects on cholinergic neurons. Eur. J. Neurosci. 8:1996;727-735.
39. Martinez-Serrano A., Lundberg C., Horellou P., Fischer W., Bentlage C., Campbell K., McKay R. D., Mallet J., Bjorklund A. CNS-derived neural progenitor cells for gene transfer of nerve growth factor to the adult rat brain: Complete rescue of axotomized cholinergic neurons after transplantation into the septum. J. Neurosci. 15:1995;5668-5680.
40. McTigue D. M., Horner P. J., Stokes B. T., Gage F. H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18:1998;5354-5365.
41. Miller A. D. Retrovirus packaging cells. Hum. Gene Ther. 1:1990;5-14.
42. Miya D., Giszter S., Mori F., Adipudi V., Tessler A., Murray M. Fetal transplants alter the development of function after spinal cord transection in newborn rats. J. Neurosci. 17:1997;4856-4872.
43. Morgan R. A., Couture L., Elroy-Stein O., Ragheb J., Moss B., Anderson W. F. Retroviral vectors containing putative internal ribosome entry sites: Development of a polycistronic gene transfer system and applications to human gene therapy. Nucleic Acids Res. 20:1992;1293-1269.
44. Onifer S. M., Whittemore S. R., Holets V. R. Variable morphological differentiation of a raphe-derived neuronal cell line following transplantation into the adult rat CNS. Exp. Neurol. 122:1993;130-142.
45. Ortega J. D., Sagen J., Pappas G. D. Survival and integration of bovine chromaffin cells transplanted into rat central nervous system without exogenous trophic factors. J. Comp. Neurol. 323:1992;13-24.
46. Park K. I., Jensen P. E., Himes T., Fischer I., Snyder E. Y. Transplantation of neurotrophin-3 (NT-3) expressing neural stem-like cells into hypoxic-ischemic (HI) brain injury. Soc. Neurosci. Abstr. 23:1997;140.10.
47. Reid L. C. M. Cloning. Jakoby W. B., Pastan I. H. Cell Culture. 1979;152-164 Academic Press, San Diego.
48. Renfranz P. J., Cunningham M. G., McKay R. D. Region-specific differentiation of the hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell. 66:1991;713-729.
49. Rosario C. M., Yandava B. D., Kosaras B., Zurakowski D., Sidman R. L., Snyder E. Y. Differentiation of engrafted multipotent neural progenitors towards replacement of missing granule neurons in meander tail cerebellum may help determine the locus of mutant gene action. Development. 124:1997;4213-4224.
50. Ryder E. F., Snyder E. Y., Cepko C. L. Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J. Neurobiol. 21:1990;356-375.
51. Safaei R., Fischer I. Molecular cloning of MAP1B cDNA: Regulation of mRNA levels during brain development. J. Neurochem. 52:1989;1871-1879.
52. Sagen J., Wang H., Tresco P. A., Aebischer P. Transplants of immunologically isolated xenogeneic chromaffin cells provide a long-term source of pain-reducing neuroactive substances. J. Neurosci. 13:1993;2415-2423.
53. Shihabuddin L. S., Hertz J. A., Holets V. R., Whittemore S. R. The adult CNS retains the potential to direct region-specific differentiation of a transplanted neuronal precursor cell line. J. Neurosci. 15:1995;6666-6678.
54. Shimohama S., Rosenberg M. B., Fagan A. M., Wolff J. A., Short M. P., Breakefield X. O., Friedmann T., Gage F. H. Grafting genetically modified cells into the rat brain: Characteristics of E. coli β-galactosidase as a reporter gene. Mol. Brain Res. 5:1989;271-278.
55. Snyder E. Y., Deitcher D. L., Walsh C., Arnold-Aldea S., Hartwieg E. A., Cepko C. L. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell. 68:1992;33-51.
56. Snyder E. Y., Macklis J. D. Multipotent neural progenitor or stem-like cells may be uniquely suited for therapy for some neurodegenerative conditions. Clin. Neurosci. 3:1995;310-316.
57. Snyder E. Y., Park K. I., Flax J. D., Liu S., Rosario C. M., Yandava B. D., Aurora S. Potential of neural "stem-like" cells for gene therapy and repair of the degenerating central nervous system. Adv. Neurol. 72:1997;121-132.
58. Snyder E. Y., Taylor R. M., Wolfe J. H. Neural progenitor cell engraftment corrects lysosomal storage throughout the MPS VII mouse brain. Nature. 374:1995;367-370.
59. Snyder E. Y., Wolfe J. H. Central nervous system cell transplantation: A novel therapy for storage diseases. Curr. Opin. Neurol. 9:1996;126-136.
60. Snyder E. Y., Yoon C., Flax J. D., Macklis J. D. Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proc. Natl. Acad. Sci. USA. 94:1997;11663-11668.
61. Sommer I., Schachner M. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: An immunocytological study in the central nervous system. Dev. Biol. 83:1981;311-327.
62. Taylor R. M., Snyder E. Y. Widespread engraftment of neural progenitor and stem-like cells throughout the mouse brain. Transplant. Proc. 29:1997;845-847.
63. Tessler A., Fischer I., Giszter S., Himes B. T., Miya D., Mori F., Murray M. Seil F. J. Embryonic Spinal Cord Transplants Enhance Locomotor Performance in Spinalized Newborn Rats. 1997;Raven Press, New York.
64. Tessler A., Murray M. Neural Transplantation: Spinal Cord. 1996;Kluwer, Dordrecht.
65. White L. A., Eaton M. J., Castro M. C., Klose K. J., Globus M. Y., Shaw G., Whittemore S. R. Distinct regulatory pathways control neurofilament expression and neurotransmitter synthesis in immortalized serotonergic neurons. J. Neurosci. 14:1994;6744-6753.
66. Whittemore S. R., Snyder E. Y. Physiological relevance and functional potential of central nervous system-derived cell lines. Mol. Neurobiol. 12:1996;13-38.
67. Whittemore S. R., White L. A. Target regulation of neuronal differentiation in a temperature-sensitive cell line derived from medullary raphe. Brain Res. 615:1993;27-40.