Adult neural progenitor cell grafts survive after acute spinal cord injury and integrate along axonal pathways

European Journal of Neuroscience

Volumn 18, Issue 4, 2003, Pages 743-751

  Vroemen, Maurice ^a   Aigner, Ludwig ^a   Winkler, Juergen ^a,b   Weidner, Norbert ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axon; CNS; Glia; Rat; Regeneration; Retroviral; Transplantation

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; MACROGLIA; NERVE CELL DIFFERENTIATION; NERVE FIBER REGENERATION; NERVE SPROUTING; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; REMYELINIZATION; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELL DIVISION; CELLS, CULTURED; FEMALE; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; NERVE REGENERATION; NEURONS; OLIGODENDROGLIA; RATS; RATS, INBRED F344; SPINAL CORD; SPINAL CORD INJURIES; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSDUCTION, GENETIC;

EID: 0041317188     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02804.x     Document Type: Article

References (39)

1. Aigner, L., Arber, S., Kapfhammer, J.P., Laux, T., Schneider, C., Botteri, F., Brenner, H.R. & Caroni, P. (1995) Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system. Cell, 83, 269-278.
2. Ben-Hur, T., Einstein, O., Mizrachi-Kol, R., Ben-Menachem., O., Reinhartz, E., Karussis, D. & Abramsky, O. (2003) Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia, 41, 73-80.
3. Blesch, A., Grill, R.J. & Tuszynski, M.H. (1998) Neurotrophin gene therapy in CNS models of trauma and degeneration. Prog. Brain Res., 117, 473-484.
4. Blesch, A., Uy, H.S., Grill, R.J., Cheng, J.G., Patterson, P.H. & Tuszynski, M.H. (1999) Leukemia inhibitory factor augments neurotrophin expression and corticospinal axon growth after adult CNS injury. J. Neurosci., 19, 3556-3566.
5. Cao, Q.L., Howard, R.M., Dennison, J.B. & Whittemore, S.R. (2002) Differentiation of engrafted neuronal-restricted precursor cells is inhibited in the traumatically injured spinal cord. Exp. Neurol., 177, 349-359.
6. Cao, Q.L., Zhang, Y.P., Howard, R.M., Walters, W.M., Tsoulfas, P. & Whittemore, S.R. (2001) Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp. Neurol., 167, 48-58.
7. Englund, U., Ericson, C., Rosenblad, C., Mandel, R.J., Trono, D., Wictorin, K. & Lundberg, C. (2000) The use of a recombinant lentiviral vector for ex vivo gene transfer into the rat CNS. Neuroreport, 11, 3973-3977.
8. Falk, A., Holmstrom, N., Carlen, M., Cassidy, R., Lundberg, C. & Frisen, J. (2002) Gene delivery to adult neural stem cells. Exp. Cell Res., 279, 34-39.
9. Gaiano, N., Kohtz, J.D., Turnbull, D.H. & Fishell, G. (1999) A method for rapid gain-of-function studies in the mouse embryonic nervous system. Nat. Neurosci., 2, 812-819.
10. Grill, R., Murai, K., Blesch, A., Gage, F.H. & Tuszynski, M.H. (1997) Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci., 17, 5560-5572.
11. Grimpe, B. & Silver, J. (2002) The extracellular matrix in axon regeneration. Prog. Brain Res., 137, 333-349.
12. Han, S.S., Kang, D.Y., Mujtaba, T., Rao, M.S. & Fischer, I. (2002) Grafted lineage-restricted precursors differentiate exclusively into neurons in the adult spinal cord. Exp. Neurol., 177, 360-375.
13. Horky, L.L., Horner, P.J., Van Praag, H., Shihabuddin, L.S. & Gage, F.H. (2000) Proliferating and quiescent CNS progenitors respond differently to injury in the adult mammalian spinal cord. Soc. Neurosci. Abstr., 26, 124.6.
14. Horner, P.J., Power, A.E., Kempermann, G., Kuhn, H.G., Palmer, T.D., Winkler, J., Thal, L.J. & Gage, F.H. (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci., 20, 2218-2228.
15. Kojima, A. & Tator, C.H. (2000) Epidermal growth factor and fibroblast growth factor 2 cause proliferation of ependymal precursor cells in the adult rat spinal cord in vivo. J. Neuropathol. Exp. Neurol., 59, 687-697.
16. Kojima, A. & Tator, C.H. (2002) Intrathecal administration of epidermal growth factor and fibroblast growth factor 2 promotes ependymal proliferation and functional recovery after spinal cord injury in adult rats. J. Neurotrauma, 19, 223-238.
17. Li, Y., Field, P.M. & Raisman, G. (1997) Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science, 277, 2000-2002.
18. Liu, Y., Kim, D., Himes, B.T., Chow, S.Y., Schallert, T., Murray, M., Tessler, A. & Fischer, I. (1999) Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J. Neurosci., 19, 4370-4387.
19. Martens, D.J., Seaberg, R.M. & Van Der Kooy, D. (2002) In vivo infusions of exogenous growth factors into the fourth ventricle of the adult mouse brain increase the proliferation of neural progenitors around the fourth ventricle and the central canal of the spinal cord. Eur. J. Neurosci., 16, 1045-1057.
20. McDonald, J.W., Liu, X.Z., Qu, Y., Liu, S., Mickey, S.K., Turetsky, D., Gottlieb, D.I. & Choi, D.W. (1999) Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nature Med., 5, 1410-1412.
21. Pannell, D. & Ellis, J. (2001) Silencing of gene expression: implications for design of retrovirus vectors. Rev. Med. Virol., 11, 205-217.
22. Pfeifer, A., Ikawa, M., Dayn, Y. & Verma, I.M. (2002) Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. USA, 99, 2140-2145.
23. Ramon-Cueto, A., Cordero, M.I., Santos-Benito, F.F. & Avila, J. (2000) Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron, 25, 425-435.
24. Reynolds, B.A. & Weiss, S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255, 1707-1710.
25. Schwab, M.E. (2002) Repairing the injured spinal cord. Science, 295, 1029-1031.
26. Shihabuddin, L.S., Horner, P.J., Ray, J. & Gage, F.H. (2000) Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J. Neurosci., 20, 8727-8735.
27. Shihabuddin, L.S., Ray, J. & Gage, F.H. (1997) FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp. Neurol., 148, 577-586.
28. Song, H., Stevens, C.F. & Gage, F.H. (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature, 417, 39-44.
29. Suda, Y., Suzuki, M., Ikawa, Y. & Aizawa, S. (1987) Mouse embryonic stem cells exhibit indefinite proliferative potential. J. Cell Physiol., 133, 197-201.
30. Svendsen, C.N., Caldwell, M.A., Shen, J., ter Borg, M.G., Rosser, A.E., Tyers, P., Karmiol, S. & Dunnett, S.B. (1997) Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease. Exp. Neurol., 148, 135-146.
31. Svendsen, C.N., ter Borg, M.G., Armstrong, R.J., Rosser, A.E., Chandran, S., Ostenfeld, T. & Caldwell, M.A. (1998) A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Meth., 85, 141-152.
32. Teng, Y.D., Lavik, E.B., Qu, X., Park, K.I., Ourednik, J., Zurakowski, D., Langer, R. & Snyder, E.Y. (2002) Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl. Acad. Sci. USA, 99, 3024-3029.
33. Tuszynski, M.H. & Kordower, J. (1999) CNS Regeneration. Academic Press, San Diego, CA, USA.
34. Wachs, F.P., Couillard-Despres, S., Engelhardt, M., Wilhelm, D., Ploetz, S., Vroemen, M., Kaesbauer, J., Uyanik, G., Klucken, J., Karl, C., Tebbing, J., Svendsen, C., Weidner, N., Kuhn, H.G., Winkler, J. & Aigner, L. (2003) High efficacy of clonal growth and expansion of adult neural stem cells. Lab. Invest., 83, 949-962.
35. Weidner, N., Blesch, A., Grill, R.J. & Tuszynski, M.H. (1999a) NGF-hyperpsecreting Schwann cell grafts augment and guide spinal cord axonal growth, and remyelinate CNS axons in a phenotypically appropriate manner that correlates with expression of L1. J. Comp. Neurol., 413, 495-506.
36. Weidner, N., Grill, R.J. & Tuszynski, M.H. (1999b) Elimination of basal lamina and the collagen 'scar' after spinal cord injury fails to augment corticospinal tract regeneration. Exp. Neurol., 160, 40-50.
37. Weidner, N., Ner, A., Salimi, N. & Tuszynski, M.H. (2001) Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. USA, 98, 3513-3518.
38. Weiss, S., Dunne, C., Hewson, J., Wohl, C., Wheatley, M., Peterson, A.C. & Reynolds, B.A. (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci., 16, 7599-7609.
39. Xu, X.M., Guenard, V., Kleitman, N. & Bunge, M.B. (1995) Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol., 351, 145-160.