Advertisement

Opportunities for Axon Repair in the CNS: Use of Microglia and Biopolymer Compositions

  • Joshua B. Stopek
  • Wolfgang J. Streit
  • Eugene P. Goldberg

Abstract

The failure of severed CNS axons to regenerate and to reconnect after injury is thought to be due to both insufficient expression of pro-regenerative genes by central neurons, and to an inhibitory microenvironment at the lesion site. Regarding the latter, astroglial scarring and presence of inhibitory myelin proteins are believed to represent major obstacles to axon regeneration. In addition, the inflammatory response within the CNS white matter is slow to develop, especially with regard to macrophage recruitment, and it is likely too weak to trigger sufficient local production of required growth-promoting molecules (Perry et al. (1987); Schwartz et al. (1999)). Transplantation of fetal neural tissue has been studied as one method for filling cystic spinal cord lesions, and has shown some promise for promoting functional recovery (Diener and Bregman (1998); Bregman et al. (1997); Anderson et al. (1995), Reier et al. (1994); Bregman et al. (1989)). However, while fetal tissue transplantation may allow filling of a lesion cavity, host fibers in adult animals tend to terminate within fetal transplants, rather than grow across them (Reier et al. (1983)). The same problem may also arise with neural stem cell transplants, which are increasingly being investigated for their benefit in spinal cord repair (Cao et al. (2001); Liu et al. (2000)).

Keywords

Schwann Cell Silk Fibroin Injured Spinal Cord Biomed Mater Peripheral Nerve Regeneration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Anderson, DK, Howland, DR and Reier, PJ (1995). Fetal neural grafts and repair of the injured spinal cord. Brain Pathol 5:451–457.PubMedCrossRefGoogle Scholar
  2. Archibald, SJ, Krarup, C, Shefner, J, Li, ST, Madison, RD (1991). A collagen-based nerve conduit for peripheral nerve repair, an electrophysiological study of nerve regeneration in rodents and nonhuman primates. J Comp Neurol 4:685–696.CrossRefGoogle Scholar
  3. Bellakonda, R, Ranieri, JP, Bouche, N, Aebischer (1995). Hydrogel-based threedimensional matrix for neural cells. J Biomed Mater Res 5:663–71.CrossRefGoogle Scholar
  4. Borkenhagen, M, Stoll, RC, Neunschwander, P, Suter, UW, Aebischer, P (1998). In vivo performance of a new biodegradable polyester urethane system used as a nerve guidance channel. Biomaterials 23:2155–65.CrossRefGoogle Scholar
  5. Bregman, BS, Kunkel, B, McAtee, EM and O’Neill, A (1989). Extension of the critical period for developmental plasticity of the corticospinal pathway. J Comp Neurol 282:355–370.PubMedCrossRefGoogle Scholar
  6. Bregman, BS, Diener, PS, McAtee, M, Dai, HN and James, C (1997). Intervention strategies to enhance anatomical plasticity and recovery of function after spinal cord injury. Adv Neurol 72:257–275.PubMedGoogle Scholar
  7. Burns, JW, Skinner, K, Colt, J, Sheidlin, A, Bronson, R, Yaacobi, Y, Goldberg, EP (1995). Prevention of Tissue Injury and Postsurgical Adhesions by Precoating Tissues with Hyaluronic Acid J Surg Res 59:644–652.PubMedCrossRefGoogle Scholar
  8. Burns, JW, Colt, MJ, Burgess, LS, Skinner, KC (1997). Preclinical evaluation of seprafilm bioresorbable membrane. Eur J Surg 577:40–48.Google Scholar
  9. Cao QI, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR (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.PubMedCrossRefGoogle Scholar
  10. Chamak B, Morandi V and Mallat M (1994). Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J Neurosci Res 38:221–233.PubMedCrossRefGoogle Scholar
  11. Cuadros, CL, Grantatir, CE (1987). Nerve regeneration through a synthetic microporous tube (expanded polytetrafluoroethylene): Experimental study in the sciatic nerve of the rat. Microsurgery 8:41–46.PubMedCrossRefGoogle Scholar
  12. Cook, AD, Hrkach, JS, Gao, NN, Johnson, IM, Pajvani, UB, Cannizzaro, SM, Langer, R (1997). Characterization and development of RGD-peptide-modified poly (lactic acidco-lysine) as an interactive, resorbable biomaterial. J Biomed Mater Res 35:513–523.PubMedCrossRefGoogle Scholar
  13. DeFife, KM, Yun, JK, Azeez, A, Stack, S, Ishihara, K, Nakabayashi, N, Colton, E, Anderson, JM (1995). Adhesion and cytokine production of monocytes on poly(2-methacrylolyoxyethyl phosphocholine-co-alkyl methacrylate)-coated polymers. J Bio Mat Res 29:431–439.CrossRefGoogle Scholar
  14. Diener, PS and Bregman, BS (1998). Fetal spinal cord transplants support growth of supraspinal and segmental projections after cervical spinal cord hemisection in the neonatal rat. J Neurosci 18:779–793.PubMedGoogle Scholar
  15. Drumheller, PD, Hubbell, JA (1994). Polymer networks with grafted cell-adhesion peptides for highly biospecific cell adhesive substrates. Anal Biochem 222:380–388.PubMedCrossRefGoogle Scholar
  16. Dunnen, den WFA, Van der Lei, B, Robinson, PH, Holwerda, A, Pennings, AJ, Schakenraad, JM (1995). The Biological performance of a degradable poly(lactic acid-∈-caprolactone) nerve guide: influence of tube dimensions. J Biomed Mater Res 29:757–766.CrossRefGoogle Scholar
  17. Dunnen, den WFA, Stokroos, I, Blaauw, EH, Holwerda, A, Pennings, AJ, Robinson, PH, Schakenraad, JM (1996). Light-microscopic and electron-microscopic evaluation of short-term nerve regeneration using a biodegradable poly(DL-lactid-∈-caprolactone) nerve guide. J Biomed Mater Res 31: 105–115.CrossRefGoogle Scholar
  18. Elkabes, S, DiCicco-Bloom, EM and Black, IB (1996). Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16:2508–2521.PubMedGoogle Scholar
  19. Fields, RD, Le Beau, JM, Longo, FM, Ellisman, MH (1989). Nerve regeneration through artificial tubular implants. Progr Neurobiol 33:87–134.CrossRefGoogle Scholar
  20. Fields, RD, Ellisman, MH (1986). Axons regenerated through silicone tube splices. I. Conduction properties. Exp Neurol 92:48–60.PubMedCrossRefGoogle Scholar
  21. Furuzono, T, Ishihara, K, Nakabayashi, N, Tamada, Y (2000). Chemical modification of silk fibroin with 2-methacryloyloxyethyl phosphorylcholine. II. Graft-polymerization onto fabric through 2-methacryloyloxyethyl isocyanate and interaction between fabric and platelets. Biomaterials 21:327–333.PubMedCrossRefGoogle Scholar
  22. Franzen, R, Schoenen, J, Leprince, P, Joosten, E, Moonen, G and Martin, D (1998). Effects of macrophage transplantation in the injured adult rat spinal cord: a combined immunocytochemical and biochemical study. J Neurosci Res 51:316–327.PubMedCrossRefGoogle Scholar
  23. Goldberg, EP, Sheets, JW, Habal, M (1980). Peritoneal Adhesions: Prevention with the use of Hydrophilic Polymer Coatings. Arch Surg 115:776–780.PubMedCrossRefGoogle Scholar
  24. Goldberg, EP, Burns, JW, Yaacobi, Y (1993). Prevention of postoperative adhesions by precoating tissues with dilute sodium hyaluronate solutions. Prog Clin Biol Res 381:191–204.PubMedGoogle Scholar
  25. Goldberg, EP (1997a). Pelvic Surgery: Adhesion Formation and Prevention. New York: Springer-Verlag.Google Scholar
  26. Goldberg, EP (1997b). Advances in Biomedical Polymers: Problems and Opportunities for Ophthalmic, Cardiovascular and Mammary Implants, and Tissue Protective Surgical Devices. Soc of Plastics EngGoogle Scholar
  27. Goldberg, EP (1997c). Protection of Tissues during Surgery with Polymer Solution Coatings: A New Concept. Intnl Congress-Peritoneal Tissue Repair.Google Scholar
  28. Goldberg, EP (1998). Polydimethylsiloxane (PDMS) coatings for stainless steel endovascular stents: uniform, stable, highly adherent coatings for reduced thrombogenicity and drug delivery. Soc for Biomaterials.Google Scholar
  29. Goldberg, EP (1999). Medical device surface modification by pulsed laser ablation deposition (PLAD) of silicone onto stainless steel. Soc for Biomaterials.Google Scholar
  30. Goldberg, EP (2000). Phospholipid and silicone modification of metal implant surfaces by electropolymerization. Soc for Biomaterials, 6th World Congress.Google Scholar
  31. Griffin, JW, George, R and Ho, T (1993). Macrophage systems in peripheral nerves. A review. JNeuropath Exp Neurol 52:553–560.CrossRefGoogle Scholar
  32. Hadlock, T, Sunback, C, Hunter, D, Cheney, M and Vacanti, JP (2000). A polymer foam conduit seeded with schwann cells promotes guided peripheral nerve regeneration. Tissue Eng 6:119–27.PubMedCrossRefGoogle Scholar
  33. Heese, K, Fiebich, BL, Bauer, J and Otten, U (1998). NF-kappa B modulates lipopolysaccharide-induced microglial nerve growth factor expression. Glia 22:401–407.PubMedCrossRefGoogle Scholar
  34. Hetier, E, Ayala, J, Denèfle, P, Bousseau, A, Rouget, P, Mallat, M and Prochiantz, A (1988). Brain macrophages synthesize interleukin-1 and interleukin-1 mRNAs in vitro. J Neurosci Res 21:391–397.PubMedCrossRefGoogle Scholar
  35. Hoppen, HJ, Leenslag, JW, Pennings, AJ, Van Der Lei, B, Robinson, PH (1990). Two-ply biodegradable nerve guide: Basic aspects of design, construction and biological performance. Biomaterials 11:286–290.PubMedCrossRefGoogle Scholar
  36. Houle, JD and Zeigler, MK (1994). Bridging a complete transection lesion of adult rat spinal cord with growth factor-treated nitrocellulose implants. J Neural Transplant Plast 5:115–24.PubMedCrossRefGoogle Scholar
  37. Houweling, DA, Lankhorst, AJ, Gispen, WH, Bar, PR and Joosten, PA (1998). Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in adult rat spinal cord and promotes partial functional recovery. Exp Neurol 153:49–59.PubMedCrossRefGoogle Scholar
  38. Hubbell, JA (1995). Biomaterials in tissue engineering. Bio-technology 13:565–576.PubMedGoogle Scholar
  39. Ishihara, K, Ziats, NP, Tierney, BP, Nakabayashi, N, Anderson, JM (1991). J Bio Mat Res 25:1397–1407.CrossRefGoogle Scholar
  40. Ishihara, K, Iwasaki, Y, Nakabayashi, N (1998). Novel biomedical polymers for regulating serious biological reactions. Mats Sci & Eng C6:253–259.CrossRefGoogle Scholar
  41. Ishihara, K, Nomura, H, Mihara, T, Kurita, K, Iwasaki, Y, Nakabayashi, N (1998b). Why do phospholipid polymers reduce protein adsorption? J Biomed Mater Res 39:323–330.PubMedCrossRefGoogle Scholar
  42. Ishihara, K (2000). Chemistry of Phospholipid Polymers as Biomaterials. Phospholipid Biomaterials Soc for Biomaterials.Google Scholar
  43. Iwasaki, Y, Ijuin, M, Mikami, A, Nakabayashi, N, Ishihara, K (1999). Behavior of blood cells in contact with water soluble phospholipid polymer. J Biomed Mater Res 46:360–367.PubMedCrossRefGoogle Scholar
  44. Iwasaki, Y, Sawada, S, Nakabayashi, N, Khang, G, Lee, HB, Ishihara, K (1999b). The effect of the chemical structure of the phospholipid polymer on fibronectin adsorption and fibroblast adhesion on the gradient phospholipid surface. Biomaterials 20:2185–2191.PubMedCrossRefGoogle Scholar
  45. Joosten, EA, Bar, PR, Gispen, WH (1995). Collagen implants and cortico-spinal axonal growth after mid-thoracic spinal cord lesion in the adult rat. J Neurosci Res 41:481–90.PubMedCrossRefGoogle Scholar
  46. Kojima, M, Ishihara, K, Watanabe, A, Nakabayashi, N (1991). Interaction between biocompatible phospholipid polymer and phospholipids. Biomaterials. 12:121–124.PubMedCrossRefGoogle Scholar
  47. LaBerge, M (2000). Investigation of the tribological properties of phospholipid polymers. Phospholipid Polymer Biomaterials, Society of Biomaterials 42–104.Google Scholar
  48. Lazarov-Spiegler, O, Soloman, AS, Zeev-Brann, AB, Hirschberg, DL, Lavie, V and Schwartz, M (1996). Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J 10:1296–1302.PubMedGoogle Scholar
  49. Lazarov-Spiegler, O, Solomon, AS and Schwartz, M (1998). Peripheral nerve-stimulated macrophages stimulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia 24:329–337.PubMedCrossRefGoogle Scholar
  50. Lee, J, Kaibara, M, Iwaki, M, Sasabe, H, Suszuki, Y, Kusakabe, M (1993). Selective adhesion and proliferation of cells on ion-implanted polymer domains. Biomaterials 14:958–960.PubMedCrossRefGoogle Scholar
  51. Lindholm, D, Heumann, R, Meyer, M and Thoenen, H (1987). Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve. Nature 330:658–659.PubMedCrossRefGoogle Scholar
  52. Lindholm, D, Heumann, R, Meyer M and Thoenen, H (1990). Transforming growth factorβ1 stimulates expression of nerve growth factor in the rat CNS. Neuroreport 1:9–12.PubMedCrossRefGoogle Scholar
  53. Liu, S, Peulve, P, Jin, O, Boisset, N, Tollier, J, Said, G and Tadie, M (1997). Axonal regrowth through collagen tubes bridging the spinal cord to nerve roots. JNeurosci Res 49:425–432.CrossRefGoogle Scholar
  54. Liu, S, Qu, Y, Steward TJ, Howard MJ, Chakrabortty, S, Holekamp, TF, McDonald, JW (2000). Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc Natl Acad Sci USA 97:6126–6131.PubMedCrossRefGoogle Scholar
  55. Mallat, M, Houlgatte, R, Brachet, P, and Prochiantz, A (1989). Lipopolysaccharidestimulated rat brain macrophages release NGF in vitro. Dev Biol 133:309–311.PubMedCrossRefGoogle Scholar
  56. Maquet, V, Martin, D, Malgrange, B, Franzen, R, Schoenen, J, Moonen, G and Jerome, R (2000). Peripheral nerve regeneration using bioresorbable macroporous polylactide scaffolds. J Biomed Mater Res 52:639–651.PubMedCrossRefGoogle Scholar
  57. Masuda-Nakagawa, LM, Muller, KJ and Nicholls, JG (1993). Axonal sprouting and laminin appearance after destruction of glial sheaths. Proc Natl Acad Sci USA 90:4966–4970.PubMedCrossRefGoogle Scholar
  58. Molander, H, Olsson, Y, Engkvist, O (1982). Regeneration of peripheral nerve through a polylactin tube. Muscle Nerve 5:54–57.PubMedCrossRefGoogle Scholar
  59. Mrak, RE and Griffin, WS (2000). Interleukin-1 and the immunogenetics of Alzheimer disease, J Neuropathol Exp Neurol, 59:471–476.PubMedGoogle Scholar
  60. Müller, JC, Klein, MA, Haas, S, Jones, L, Kreutzberg, GW, Raivich G. (1996). Regulation of thrombospondin in the regenerating mouse facial motor nucleus. Glia 17:121–132.CrossRefGoogle Scholar
  61. Nagata, K, Takei, N, Nakajima K, Saito H and Kohsaka S. (1993). Microglial conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J Neurosci Res 34:357–363.PubMedCrossRefGoogle Scholar
  62. Nakabayashi, N (2000). Concept and history of phospholipid polymer biomaterials. Phospholipid Polymer Biomaterials, Society of Biomaterials 6–14.Google Scholar
  63. Neugebauer, KM, Emmett, CJ, Venstrom, KA and Reichardt, LF (1991). Vitronectin and thrombospondin promote retinal neurite outgrowth: developmental regulation and role of integrins. Neuron 6:345–358.PubMedCrossRefGoogle Scholar
  64. O’Shea, KS, Liu, LH and Dixit, VM (1991). Thrombospondin and a 140 kd fragment promote adhesion and neurite outgrowth from embryonic central and peripheral neurons and from PC12 cells. Neuron 7:231–237.PubMedCrossRefGoogle Scholar
  65. Pearson, VL, Rothwell, NJ and Toulmond, S (1999). Excitotoxic brain damage in the rat induces interleukin-1 β protein in microglia and astrocytes: correlation with the progression of cell death. Glia 25:311–323.PubMedCrossRefGoogle Scholar
  66. Perry, VH, Brown, MC, Gordon, S (1987). The macrophage response to central and peripheral nerve injury. J Exp Med 165:1218–1223.PubMedCrossRefGoogle Scholar
  67. Plant, GW and Harvery, AR (2000). A new type of biocompatible bridging structure supports axon regrowth after implantation into lesioned rat optic tract. Cell Transplant 9:759–772.PubMedGoogle Scholar
  68. Plant, GW, Harvey, AR, Chirila, TV (1995). Axonal growth within poly (2-hydroxyethyl methacrylate) sponges infiltrated with Schwann cells and implanted into the lesioned rat optic tract. Brain Res 671:119–130.PubMedCrossRefGoogle Scholar
  69. Posse de Chaves, EI, Rusinol, AE, Vance, DE, Campenot, RB, Vance, JE (1997). Role of lipoproteins in the delivery of lipids to axons during axonal regeneration. J Biol Chem 49:30766–30773.CrossRefGoogle Scholar
  70. Prewitt, CM, Niesman, IR, Kane, CJ. and Houlé, JD (1997). Activated macrophage/microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp Neurol 148:433–443.PubMedCrossRefGoogle Scholar
  71. Rabchevsky, AG and Streit, WJ (1997). Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 47:34–48.PubMedCrossRefGoogle Scholar
  72. Rabchevsky, AG and Streit, WJ (1998). Role of microglia in post-injury repair and regeneration of the CNS. Mental Retard Develop Disab Res Rev 4:187–192.CrossRefGoogle Scholar
  73. Rapalino, O, Lazarov-Spiegler, O, Agranov, E, Velan, GJ, 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. Nature Med 4:814–821.PubMedCrossRefGoogle Scholar
  74. Reier, PJ, Stensaas, LJ and Guth, L (1983). The astrocytic scar as an impediment to regeneration in the central nervous system. In Spinal Cord Reconstruction, eds. CC Kao, RP Bunge and PJ Reier, pp. 163–195. New York: Raven Press.Google Scholar
  75. Reier, PJ, Anderson, DK, Schrimsher, GW, Bao, J, Friedman, RM, Ritz, LA and Stokes, BT (1994). Neural cell grafting: Anatomical and functional repair of the spinal cord. In The neurobiology of central nervous system trauma, eds. SK Salzman and AI Faden, pp. 288–311. New York: Oxford University Press.Google Scholar
  76. Rieske, E, Graeber, MB, Tetzlaff, W, Czlonkowska, A, Streit, WJ and Kreutzberg GW (1989). Microglia and microglia derived brain macrophages in culture: generation from axotomized facial nuclei, identification and characterization in vitro. Brain Res 492:1–14.PubMedCrossRefGoogle Scholar
  77. Schwartz, M, Moalem, G, Leibowitz-Amit, R, Cohen, IR (1999). Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci 22:295–299.PubMedCrossRefGoogle Scholar
  78. Schugens, CH, Grandfils, CH, Jerome, R, Teyssie, PH, Delree, P, Martin, D, Malgrange, B, Moonen, G (1995). Preparation of a macroporous biodegradable polylactide implant for neuronal transplantation J Biomed Biomat Res 29:1349–1362.CrossRefGoogle Scholar
  79. Seckel, BR, Chiu, TH, Nylias, E, Sidman, RL (1983). Nerve regeneration through synthetic biodegradable nerve guides: Regulation by the target organ. Plastic Reconstr Surg 74:173–181.CrossRefGoogle Scholar
  80. Seeger, JM, Kaelin, LD, Staples, EM, Yaacobi, Y, Bailey, JC, Normann, S, Burns, JW, Goldberg, EP (1996). Prevention of postoperative pericardial adhesions using tissueprotective solutions. J Surg Res 68:63–66.CrossRefGoogle Scholar
  81. Shimojo, M, Nakajima, K, Takei, N, Hamanoue, M, and Kohsaka, S (1991). Production of basic fibroblast growth factor in cultured rat brain microglia. Neurosci Lett 123:229–231.PubMedCrossRefGoogle Scholar
  82. Streit, WJ, Semple-Rowland, SL, Hurley, SD, Miller, RC, Popovich, PG, and Stokes, BT (1998). Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp Neurol 152:74–87.PubMedCrossRefGoogle Scholar
  83. Takahashi, M, Satou, T, Hashimoto, S (1988). In vivo regeneration of peripheral nerve axons and perineurium guided by resorbable collagen film. Acta Pathol Jpn 38:1489–1502.PubMedGoogle Scholar
  84. Tong, X, Hirai, K, Shimada, H (1994). Sciatic nerve regeneration navigated by lamininfibronectin double coated biodegradable collagen grafts in rats. Brain Res 663:155–162.PubMedCrossRefGoogle Scholar
  85. Widenhouse, CW (1996). Surface Modification of Vascular Prosthesis and Intracorneal Lens Polymers. Ph.D. dissertation, University of Florida.Google Scholar
  86. Woerly, S, Maghami, G, Duncan, R, Subr, V, Ulbrich, K (1993). Synthetic polymer derivatives as substrata for neuronal adhesion and growth. Brain Res Bull 30:423–432.PubMedCrossRefGoogle Scholar
  87. Yaacobi, Y, Israel, AA, Goldberg, EP (1993). Prevention of postoperative abdominal adhesions by tissue precoating with polymer solutions. J Surg Res 55:422.PubMedCrossRefGoogle Scholar
  88. Yaacobi, Y, Latif, MH, Kaul, K, Maher, MF (1992). Reduction of postoperative adhesions secondary to strabismus surgery in rabbits. Ophthalmic Surg 23:123.PubMedGoogle Scholar
  89. Yao, J, Keri, JE, Taffs, RE, Colton, CA (1992). Characterization of interleukin-1 production by microglia in culture. Brain Research 591:88–93.PubMedCrossRefGoogle Scholar
  90. Yoneyama, T, Ishihara, K, Nakabayashi, N, Ito, M, Mishima, Y (1998). Chemical modification of silk fibroin with 2-methacryloyloxyethyl phosphorylcholine. II. Graftpolymerization onto fabric through 2-methacryloyloxyethyl isocyanate and interaction between fabric and platelets. J Biomed Mater Res 43:15–20.PubMedCrossRefGoogle Scholar
  91. Yoshida K and Gage FH (1992). Cooperative regulation of nerve growth factor synthesis and secretion in fibroblasts and astrocytes by fibroblast growth factor and other cytokines. Brain Res 569:14–25.PubMedCrossRefGoogle Scholar
  92. Young, BL, Begovac, DG, Stuart, DG, Goslow, GE (1984). An effective sleeving technique in nerve repair. J Neurosci Meth 10:51–58.CrossRefGoogle Scholar
  93. Yu, X, Dillon, GP, Bellamkonda, RB (1999). A laminin and nerve growth factor-laden three-dimensional scaffold for enhanced neurite extension. Tissue Eng 4:291–304.CrossRefGoogle Scholar
  94. Zhang, SF, Rolfe, P, Wright, G, Lian, W, Milling, AJ, Tanaka, S, Ishihara, K (1998). Physical and biological properties of compound membranes incorporating a copolymer with a phosphorycholine head group. Biomaterials 19:691–700.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Joshua B. Stopek
  • Wolfgang J. Streit
  • Eugene P. Goldberg

There are no affiliations available

Personalised recommendations