FGF-2-responsive and spinal cord-resident cells improve locomotor function after spinal cord injury

Journal of Neurotrauma

Volumn 31, Issue 18, 2014, Pages 1584-1598

  Kasai, Masaki ^a   Jikoh, Takahiro ^a   Fukumitsu, Hidefumi ^a   Furukawa, Shoei ^a  

^a GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

axonal regeneration; cell transplantation; growth factors; locomotor function; spinal cord injury

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBRONECTIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; NERVE GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; NEUROMODULIN; NEUROTROPHIC FACTOR; THROMBOMODULIN; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL INFILTRATION; CELL LABELING; CELL STRUCTURE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LOCOMOTION; MESENCHYMAL STEM CELL; NERVE FIBER; NERVE FIBER REGENERATION; NONHUMAN; RAT; RETROGRADE NERVE FIBER TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; SPINAL CORD TRANSSECTION; ANIMAL; CELL TRANSPLANTATION; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; INJECTION; METABOLISM; MOTOR ACTIVITY; MOUSE; SPINAL CORD; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; WISTAR RAT;

ANIMALS; CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLAST GROWTH FACTOR 2; FIBRONECTINS; INJECTIONS; MICE; MOTOR ACTIVITY; RATS; RATS, WISTAR; SPINAL CORD; SPINAL CORD INJURIES; SPINAL CORD REGENERATION;

EID: 84907042347     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2009.1108     Document Type: Article

References (49)

1. Nathan, P.W. (1994). Effects on movement of surgical incisions into the human spinal cord. Brain 117 (Pt. 2), 337-346.
2. Iannotti, C., Zhang, Y.P., Shields, L.B., Han, Y., Burke, D.A., Xu, X.M., and Shields, C.B. (2006). Dural repair reduces connective tissue scar invasion and cystic cavity formation after acute spinal cord laceration injury in adult rats. J. Neurotrauma 23, 853-865.
3. Fitch, M.T., and Silver, J. (2008). CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp. Neurol. 209, 294-301.
4. Yiu, G., and He, Z. (2006). Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617-627.
5. He, Z., and Koprivica, V. (2004). The Nogo signaling pathway for regeneration block. Annu. Rev. Neurosci. 27, 341-368.
6. Schwab, M.E. (2004). Nogo and axon regeneration. Curr. Opin. Neurobiol. 14, 118-124.
7. Bulsara, K.R., Iskandar, B.J., Villavicencio, A.T., and Skene, J.H. (2002). A new millennium for spinal cord regeneration: growthassociated genes. Spine 27, 1946-1949.
8. Harel, N.Y., and Strittmatter, S.M. (2006). Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat. Rev. Neurosci. 7, 603-616.
9. Hashimoto, M., Nitta, A., Fukumitsu, H., Nomoto, H., Shen, L., and Furukawa, S. (2005a). Inflammation-induced GDNF improves locomotor function after spinal cord injury. Neuroreport 16, 99-102.
10. Hashimoto, M., Nitta, A., Fukumitsu, H., Nomoto, H., Shen, L., and Furukawa, S. (2005b). Involvement of glial cell line-derived neurotrophic factor in activation processes of rodent macrophages. J. Neurosci. Res. 79, 476-487.
11. Schnell, L., Schneider, R., Kolbeck, R., Barde, Y.A., and Schwab, M.E. (1994). Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173.
12. Widenfalk, J., Lundstromer, K., Jubran, M., Brene, S., and Olson, L. (2001). Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J. Neurosci. 21, 3457-3475.
13. Presta., M,, Dell'Era, P., Mitola, S., Moroni, E., Ronca, R., and Rusnati, M. (2005). Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 16, 159-178.
14. Greenberg, D.A., and Jin, K. (2005). From angiogenesis to neuropathology. Nature 438, 954-959.
15. Nakatomi, H., Kuriu, T., Okabe, S., Yamamoto, S., Hatano, O., Kawahara, N., Tamura, A., Kirino, T., and Nakafuku, M. (2002). Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429-441.
16. Ohori, Y., Yamamoto, S., Nagao, M., Sugimori, M., Yamamoto, N., Nakamura, K., and Nakafuku, M. (2006). Growth factor treatment and genetic manipulation stimulate neurogenesis and oligodendrogenesis by endogenous neural progenitors in the injured adult spinal cord. J. Neurosci. 26, 11948-11960.
17. Yoshimura, S., Teramoto, T., Whalen, M.J., Irizarry, M.C., Takagi, Y., Qiu, J., Harada, J., Waeber, C., Breakefield, X.O., and Moskowitz, M.A. (2003). FGF-2 regulates neurogenesis and degeneration in the dentate gyrus after traumatic brain injury in mice. J. Clin. Invest. 112, 1202-1210.
18. Abe, K., and Saito, H. (2001). Effects of basic fibroblast growth factor on central nervous system functions. Pharmacol. Res. 43, 307-312.
19. Bansal, R. (2002). Fibroblast growth factors and their receptors in oligodendrocyte development: implications for demyelination and remyelination. Dev. Neurosci. 24, 35-46.
20. Rabchevsky, A.G., Fugaccia, I., Fletcher-Turner, A., Blades, D.A., Mattson, M.P., and Scheff, S.W. (1999). Basic fibroblast growth factor (bFGF) enhances tissue sparing and functional recovery following moderate spinal cord injury. J. Neurotrauma 16, 817-830.
21. Rabchevsky, A.G., Fugaccia, I., Turner, A.F., Blades, D.A., Mattson, M.P., and Scheff, S.W. (2000). Basic fibroblast growth factor (bFGF) enhances functional recovery following severe spinal cord injury to the rat. Exp. Neurol. 164, 280-291.
22. Ibarra, A., Hernández, E., Lomeli, J., Pineda, D., Buenrostro, M., Martiñón, S., Garcia, E., Flores, N., Guizar-Sahagun, G., Correa, D., and Madrazo, I. (2007). Cyclosporin-A enhances non-functional axonal growing after complete spinal cord transection. Brain Res. 1149, 200-209.
23. Gómez-Pinilla, F, Vu, L, and Cotman, C.W. (1995). Regulation of astrocyte proliferation by FGF-2 and heparan sulfate in vivo. J. Neurosci. 15, 2021-2029.
24. Walz, A., McFarlane, S, Brickman, Y.G., Nurcombe, V., Bartlett, P.F., and Holt, C.E. (1997). Essential role of heparan sulfates in axon navigation and targeting in the developing visual system. Development 124, 2421-2430.
25. Squires, C.H., Childs, J., Eisenberg, S.P., Polverini, P.J., and Sommer, A. (1988). Production and characterization of human basic fibroblast growth factor from Escherichia coli. J. Biol. Chem. 263, 16297-16302.
26. 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
27. Nitta, A., Ito, M., Fukumitsu, H., Ohmiya, M., Ito, H., Sometani, A., Nomoto, H., Furukawa, Y., and Furukawa, S. (1999). 4-Methylcatechol increases brain-derived neurotrophic factor content and mRNA expression in cultured brain cells and in rat brain in vivo. J. Pharmacol. Exp. Ther. 291, 1276-1283.
28. Ito, H., Nakajima, A., Nomoto, H., and Furukawa, S. (2003). Neurotrophins facilitate neuronal differentiation of cultured neural stem cells via induction of mRNA expression of basic helix-loop-helix transcription factors Mash1 and Math1. J. Neurosci. Res. 71, 648-658.
29. Furukawa, S., and Furukawa, Y. (2007). FGF-2-treatment improves locomotor function via axonal regeneration in the transected rat spinal cord. Brain Nerve 59, 1333-1339.
30. Niclou, S.P., Franssen, E.H., Ehlert, E.M., Taniguchi, M., and Verhaagen, J. (2003). Meningeal cell-derived semaphorin 3A inhibits neurite outgrowth. Mol. Cell Neurosci. 24, 902-912.
31. Riehl, R., Johnson, K., Bradley, R., Grunwald, G.B., Cornel, E., Lilienbaum, A., and Holt, C.E. (1996). Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17, 837-848.
32. Tomaselli, K.J., Neugebauer, K.M., Bixby, J.L., Lilien, J., and Reichardt, L.F. (1988). N-cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron 1, 33-43.
33. Jimenez Hamann, M.C., Tator, C.H., and Shoichet, M.S. (2005). Injectable intrathecal delivery system for localized administration of EGF and FGF-2 to the injured rat spinal cord. Exp. Neurol. 194, 106-119.
34. Kojima, A., and 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.
35. Gonzalez, A.M., Carman, L.S., Ong, M., Ray, J., Gage, F.H., Shults, C.W., and Baird, A. (1994). Storage, metabolism, and processing of 125I-fibroblast growth factor-2 after intracerebral injection. Brain Res. 665, 285-292.
36. De Winter, F., Oudega, M., Lankhorst, A.J., Hamers, F.P., Blits, B., Ruitenberg, M.J., Pasterkamp, R.J., Gispen, W.H., and Verhaagen, J. (2002). Injury-induced class 3 semaphorin expression in the rat spinal cord. Exp. Neurol. 175, 61-75.
37. Grill, R., Murai, K., Blesch, A., Gage, F.H., and 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.
38. Liu, Y., Kim, D., Himes, B.T., Chow, S.Y., Schallert, T., Murray, M., Tessler, A., and 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.
39. Tetzlaff, W., Alexander, S.W., Miller, F.D., and Bisby, M.A. (1991). Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J. Neurosci. 11, 2528-2544.
40. Kuchler, M., Fouad, K., Weinmann, O., Schwab, M.E., and Raineteau, O. (2002). Red nucleus projections to distinct motor neuron pools in the rat spinal cord. J. Comp. Neurol. 448, 349-359.
41. Muir, G.D., and Whishaw, I.Q. (2000). Red nucleus lesions impair overground locomotion in rats: a kinetic analysis. Eur. J. Neurosci. 12, 1113-1122.
42. Cizkova, D., Rosocha, J., Vanicky, I., Jergova, S., and Cizek, M. (2006). Transplants of human mesenchymal stem cells improve functional recovery after spinal cord injury in the rat. Cell Mol. Neurobiol. 26, 1167-1180.
43. Dasari, V.R., Spomar, D.G., Cady, C., Gujrati, M., Rao, J.S., and Dinh, D.H. (2007). Mesenchymal stem cells from rat bone marrow downregulate caspase-3-mediated apoptotic pathway after spinal cord injury in rats. Neurochem. Res. 32, 2080-2093.
44. De Ugarte, D.A., Alfonso, Z., Zuk, P.A., Elbarbary, A., Zhu, M., Ashjian, P., Benhaim, P., Hedrick, M.H., and Fraser, J.K. (2003). Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. Immunol. Lett. 89, 267-270.
45. Miyazaki, T., Kitagawa, Y., Toriyama, K., Kobori, M., and Torii, S. (2005). Isolation of two human fibroblastic cell populations with multiple but distinct potential of mesenchymal differentiation by ceiling culture of mature fat cells from subcutaneous adipose tissue. Differentiation 73, 69-78.
46. Uccelli, A., Moretta, L., and Pistoia, V. (2008). Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 8, 726-736.
47. Kaneko, S., Iwanami, A., Nakamura, M., Kishino, A., Kikuchi, K., Shibata, S., Okano, H.J., Ikegami, T., Moriya, A., Konishi, O., Nakayama, C., Kumagai, K., Kimura, T., Sato, Y., Goshima, Y., Taniguchi, M., Ito, M., He, Z., Toyama, Y., and Okano, H. (2006). A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat. Med. 12, 1380-1389.
48. Rapalino, O., Lazarov-Spiegler, O., Agranov, E., Velan, G.J., Yoles, E., Fraidakis, M., Solomon, A., Gepstein, R., Katz, A., Belkin, M., Hadani, M., and Schwartz, M. (1998). Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat. Med. 4, 814-821.
49. Moalem, G., Leibowitz-Amit, R., Yoles, E., Mor, F., Cohen, I.R., and Schwartz, M. (1999). Autoimmune T cells protect neurons from secondary degeneration after central nervous system axotomy. Nat. Med. 5, 49-55