Alginate encapsulated BDNF-producing fibroblast grafts permit recovery of function after spinal cord injury in the absence of immune suppression

Journal of Neurotrauma

Volumn 22, Issue 1, 2005, Pages 138-156

  Tobias, Christopher A ^a   Han, Steve S W ^a   Shumsky, Jed S ^a   Kim, Duckhyun ^b   Tumolo, Maureen ^a   Dhoot, Nikhil O ^c   Wheatley, Margaret A ^c,d   Fischer, Itzhak ^a   Tessler, Alan ^a,e   Murray, Marion ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b MB Research Laboratories   (United States)

^c Drexel University   (United States)

^d DREXEL UNIVERSITY   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Alginate; Axonal growth; Encapsulation; Functional recovery; Spinal cord injury; Transplantation

Indexed keywords

ALGINIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCITONIN GENE RELATED PEPTIDE; NEUROMODULIN; SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CELL ENCAPSULATION; CELL REGENERATION; CELL TRANSPLANTATION; CONTROLLED STUDY; CONVALESCENCE; DRUG DELIVERY SYSTEM; FEMALE; FIBROBLAST; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOCYTOCHEMISTRY; IMMUNOMODULATION; LOCOMOTION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; OPEN FIELD BEHAVIOR; RAT; RUBROSPINAL TRACT; SPINAL CORD INJURY;

EID: 19944433307     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2005.22.138     Document Type: Article

References (56)

1. ARCHELOS, J.J., ROGGENBUCK, K., SCHNEIDER-SCHAULIES, J., LININGTON, C., TOYKA, K.V., and HARTUNG, H.P. (1993). Production and characterization of monoclonal antibodies to the extracellular domain of P0. J. Neurosci. Res. 35, 46-53.
2. BAREYRE, F.M., KERSCHENSTEINER, M., RAINETEAU, O., METTENLEITER, T.C., WEINMANN, O., and SCHWAB, M.E. (2004). The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 7, 269-277.
3. BASSO, D.M., BEATTIE, M.S., and BRESNAHAN, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma. 12, 1-21.
4. BRADBURY, E.J., MOON, L.D., POPAT, R.J., et al. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640.
5. BREGMAN, B.S., MCATEE, M., DAI, H.N., and KUHN, P.L. (1997). Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp. Neurol. 148, 475-494.
6. BREGMAN, B.S., KUNKEL-BAGDEN, E., REIER, P.J., DAI, H.N., MCATEE, M., and GAO, D. (1993). Recovery of function after spinal cord injury: mechanisms underlying transplant-mediated recovery of function differ after spinal cord injury in newborn and adult rats. Exp. Neurol. 123, 3-16.
7. BROWN, L.T. (1974). Rubrospinal projections in the rat. J. Comp. Neurol. 154, 169-187.
8. CHANG, P.L., HORTELANO, G., TSE, M., and AWREY, D.E. (1994). Growth of recombinant fibroblasts in alginate microcapsules. Biotechnol. Bioeng. 43, 925-933.
9. CHENG, W.T., CHEN, B.C., CHIOU, S.T., and CHEN, C.M. (1998). Use of nonautologous microencapsulated fibroblasts in growth hormone gene therapy to improve growth of midget swine. Hum. Gene Ther. 9, 1995-2003.
10. CHOW, S.Y., MOUL, J., TOBIAS, C.A., et al. (2000). Characterization and intraspinal grafting of EGF/bFGF-dependent neurospheres derived from embryonic rat spinal cord. Brain Res. 874, 87-106.
11. COHEN, S.M. (2002). Current immunosuppression in liver transplantation. Am. J. Ther. 9, 119-125.
12. CONDIC, M.L., and LEMONS, M.L. (2002). Extracellular matrix in spinal cord regeneration: getting beyond attraction and inhibition. Neuroreport 13, A37-A48.
13. DERGHAM, P., ELLEZAM, B., ESSAGIAN, C., AVEDISSIAN, H., LUBELL, W.D., and MCKERRACHER, L. (2002). Rho signaling pathway targeted to promote spinal cord repair. J. Neurosci. 22, 6570-6577.
14. DIAZ-RUIZ, A., RIOS, C., DUARTE, I., et al. (1999). Cyclosporin-A inhibits lipid peroxidation after spinal cord injury in rats. Neurosci. Lett. 266, 61-64.
15. DIAZ-RUIZ, A., RIOS, C., DUARTE, I., et al. (2000). Lipid peroxidation inhibition in spinal cord injury: cyclosporin-A vs methylprednisolone. Neuroreport 11, 1765-1767.
16. FAWCETT, J.W., and ASHER, R.A. (1999). The glial scar and central nervous system repair. Brain Res. Bull. 49, 377-391.
17. FISCHER, I., RICHTER-LANDSBERG, C., and SAFAEI, R. (1991). Regulation of microtubule associated protein 2 (MAP2) expression by nerve growth factor in PC12 cells. Exp. Cell. Res. 194, 195-201.
18. GRILL, R., MURAI, K., BLESCH, A., GAGE, F.H., and TUSZYNSKI, M.H. (1997a). Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17, 5560-5572.
19. GRILL, R.J., BLESCH, A., and TUSZYNSKI, M.H. (1997b). Robust growth of chronically injured spinal cord axons induced by grafts of genetically modified NGF-secreting cells. Exp. Neurol. 148, 444-452.
20. HAYASHI, Y., SHUMSKY, J.S., CONNORS, T., et al. (2005). Immunosuppression with either cyclosporine A or FK 506 promotes repair processes after spinal cord injury. J. Neurotrauma (submitted).
21. HIMES, B.T., and TESSLER, A. (2001) Neuroprotection from cell death following axotomy, in: Axonal Regeneration in the Central Nervous System. N. Ingoglia and M. Murray (eds), Marcel Dekker: New York, pps. 477-504.
22. HIMES, B.T., COLEMAN, C., KUSHNER, R., et al. (2005). Recovery of function following grafting of human bone marrow stromal cells into the injured spinal cord. Exp. Neurol. (submitted).
23. HIRAI, S., KASAI, S., and MITO, M. (1993). Encapsulated hepatocyte transplantation for the treatment of D-galactosamine-induced acute hepatic failure in rats. Eur. Surg. Res. 25, 193-202.
24. HOFSTETTER, C.P., SCHWARZ, E.J., HESS, D., et al. (2002). Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA 99, 2199-2204.
25. HORTELANO, G., AL-HENDY, A., OFOSU, F.A., and CHANG, P.L. (1996). Delivery of human factor IX in mice by encapsulated recombinant myoblasts: a novel approach towards allogeneic gene therapy of hemophilia B. Blood. 87, 5095-5103.
26. JEFFERY, N.D., and FITZGERALD, M. (2001). Effects of red nucleus ablation and exogenous neurotrophin-3 on corticospinal axon terminal distribution in the adult rat. Neuroscience 104, 513-521.
27. JOKI, T., MACHLUF, M., ATALA, A., et al. (2001). Continuous release of endostatin from microencapsulated engineered cells for tumor therapy. Nat. Biotechnol. 19, 35-39.
28. KATAOKA, K., SUZUKI, Y., KITADA, M., et al. (2001). Alginate, a bioresorbable material derived from brown seaweed, enhances elongation of amputated axons of spinal cord in infant rats. J. Biomed. Mater. Res. 54, 373-384.
29. KIM, D., SCHALLERT, T., LIU, Y., et al. (2001). Transplantation of genetically modified fibroblasts expressing BDNF in adult rats with a subtotal hemisection improves specific motor and sensory functions. Neurorehabil. Neural. Repair. 15, 141-150.
30. LEPORE, A.C., HAN, S.S.W., TYLER-POLSZ, C.J., CAI, J., RAO, M.S., and FISCHER, I. (2004). Differential fate of multipotent and lineage-restricted neural precursors following transplantation into the adult CNS. Neuron Glia Biol. 1, 113-126.
31. LIU, H.W., OFOSU, F.A., and CHANG, P.L. (1993). Expression of human factor IX by microencapsulated recombinant fibroblasts. Hum Gene Ther. 4, 291-301.
32. LIU, Y., HIMES, B.T., MURRAY, M., TESSLER, A., and FISCHER, I. (2002). Grafts of BDNF-producing fibroblasts rescue axotomized rubrospinal neurons and prevent their atrophy. Exp. Neurol. 178, 150-164.
33. LIU, Y., KIM, D., HIMES, B.T., et al. (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.
34. MCDONALD, J.W., LIU, X.Z., QU, Y., et al. (1999). Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat. Med. 5, 1410-1412.
35. MURRAY, M. (2001) Therapies to promote CNS repair, in: Axonal Regeneration in the Central Nervous System. N. Ingoglia and M. Murray (eds), Marcel Dekker: New York, pps. 649-673.
36. MURRAY, M., and TOBIAS, C.A. (2003). Regeneration and sprouting in the injured spinal cord: a decade of growth. Top. Spinal Cord Inj. Rehab. 8, 37-51.
37. NEUMANN, S., BRADKE, F., TESSIER-LAVIGNE, M., and BASBAUM, A.I. (2002). Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron. 34, 885-893.
38. PALLADINI, G., CARONTI, B., POZZESSERE, G., et al. (1996). Treatment with cyclosporine A promotes axonal regeneration in rats submitted to transverse section of the spinal cord. II. Recovery of function. J. Hirnforsch. 37, 145-153.
39. PLUNET, W., KWON, B.K., and TETZLAFF, W. (2002). Promoting axonal regeneration in the central nervous system by enhancing the cell body response to axotomy. J. Neurosci. Res. 68, 1-6.
40. RABCHEVSKY, A.G., FUGACCIA, I., SULLIVAN, P.G., and SCHEFF, S.W. (2001). Cyclosporin A treatment following spinal cord injury to the rat: behavioral effects and stereological assessment of tissue sparing. J. Neurotrauma 18, 513-522.
41. RAMON-CUETO, A., CORDERO, M.I., SANTOS-BENITO, F.F., and AVILA, J. (2000). Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25, 425-435.
42. REIER, P.J., BREGMAN, B.S., and WUJEK, J.R. (1986). Intraspinal transplantation of embryonic spinal cord tissue in neonatal and adult rats. J. Comp. Neurol. 247, 275-296.
43. SCHWARTZ, E.D., SHUMSKY, J.S., WEHRLI, S., TESSLER, A., MURRAY, M., HACKNEY, D.B. (2003). Ex vivo MR determined apparent diffusion coefficients correlate with motor recovery mediated by intraspinal transplants of fibroblasts genetically modified to express BDNF. Exp. Neurol. 182, 42-63.
44. SIMPSON, D. (2001). New developments in the prophylaxis and treatment of graft versus host disease. Expert Opin. Pharmacother. 2, 1109-1117.
45. SUN, Y., MA, X., ZHOU, D., VACEK, I., and SUN, M. (1996). Normalization of diabetes in spontaneously diabetic cynomologous monkeys by xenografts of microencapsulated porcine islets without immunosuppression. J. Clin. Invest. 98, 1417-1422.
46. SUZUKI, K., SUZUKI, Y., OHNISHI, K., ENDO, K., TANIHARA, M., and NISHIMURA, Y. (1999a). Regeneration of transected spinal cord in young adult rats using freeze-dried alginate gel. Neuroreport 10, 2891-2894.
47. SUZUKI, Y., TANIHARA, M., OHNISHI, K., SUZUKI, K., ENDO, K., and NISHIMURA, Y. (1999b). Cat peripheral nerve regeneration across 50-mm gap repaired with a novel nerve guide composed of freeze-dried alginate gel. Neurosci. Lett. 259, 75-78.
48. SUZUKI, Y., KITAURA, M., WU, S., et al. (2002). Electrophysiological and horseradish peroxidase-tracing studies of nerve regeneration through alginate-filled gap in adult rat spinal cord. Neurosci. Lett. 318, 121-124.
49. SUZUKI, Y., KATAOKA, K., KITADA, M., et al. (2001). Alginate, a bioresorbable material, enhances elongation of amputated axons of rat spinal cord. Soc. Neurosci. Abst. 27, program no. 367, 313.
50. TESSLER, A., FISCHER, I., GISZTER, S., et al. (1997). Embryonic spinal cord transplants enhance locomotor performance in spinalized newborn rats. Adv. Neurol. 72, 291-303.
51. TOBIAS, C.A., DHOOT, N.O., WHEATLEY, M.A., TESSLER, A., MURRAY, M., and FISCHER, I. (2001). Grafting of encapsulated BDNF-producing fibroblasts into the injured spinal cord without immune suppression in adult rats. J. Neurotrauma. 18, 287-301.
52. TOBIAS, C.A., SHUMSKY, J.S., SHIBATA, M., et al. (2003). Delayed grafting of BDNF and NT-3 producing fibroblasts into the injured spinal cord stimulates sprouting, partially rescues axotomized red nucleus neurons from loss and atrophy, and provides limited regeneration. Exp. Neurol. 184, 97-113.
53. WEIDNER, N., NER, A., SALIMI, N., and 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.
54. XU, X.M., CHEN, A., GUENARD, V., KLEITMAN, N., and BUNGE, M.B. (1997). Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J. Neurocytol. 26, 1-16.
55. XUE, Y., GAO, J., XI, Z., et al. (2001). Microencapsulated bovine chromaffin cell xenografts into hemiparkinsonian rats: a drug-induced rotational behavior and histological changes analysis. Artif. Organs. 25, 131-135.
56. YE, J.H., and HOULE, J.D. (1997). Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143, 70-81.