Relationship between scaffold channel diameter and number of regenerating axons in the transected rat spinal cord

Acta Biomaterialia

Volumn 5, Issue 7, 2009, Pages 2551-2559

  Krych, Aaron J ^a   Rooney, Gemma E ^a,b   Chen, Bingkun ^a,b   Schermerhorn, Thomas C ^a   Ameenuddin, Syed ^a,b   Gross, LouAnn ^a,b   Moore, Michael J ^a   Currier, Bradford L ^a   Spinner, Robert J ^a   Friedman, Jonathan A ^a   Yaszemski, Michael J ^a   Windebank, Anthony J ^a,b  

^a Mayo Clinic   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Biomedical engineering; Central nervous system; Polymeric scaffolds; Tissue development and growth

Indexed keywords

FUNCTIONAL POLYMERS; ION IMPLANTATION; POLYMERIC IMPLANTS; PROFESSIONAL ASPECTS; RATS; SCAFFOLDS (BIOLOGY); TISSUE; TISSUE REGENERATION;

AXONAL REGENERATION; CENTRAL NERVOUS SYSTEMS; CHANNEL DIAMETERS; FIBROUS RIM; POLYMERIC SCAFFOLD; RAT SPINAL CORD; SCAFFOLD CHANNELS; SCHWANN CELLS; TISSUE DEVELOPMENT; TISSUE GROWTH;

NEURONS;

NEUROFILAMENT PROTEIN; POLYGLACTIN; TISSUE SCAFFOLD;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SIZE; CELL TYPE; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; NERVE FIBER REGENERATION; NONHUMAN; PHYSICAL PARAMETERS; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN EXPRESSION; RAT; SCHWANN CELL; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; TISSUE ENGINEERING;

ANIMALIA; RATTUS;

EID: 68949140667     PISSN: 17427061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actbio.2009.03.021     Document Type: Article

References (58)

1. Network. SCII: Spinal cord injury: facts and figures at a glance. 2001. Available from: www.spinalcorduabedu.
2. DeVivo M.J. Causes and costs of spinal cord injury in the United States. Spinal Cord 35 (1997) 809-813
3. Blesch A., Uy H.S., Grill R.J., Cheng J.G., Patterson P.H., and Tuszynski M.H. Leukemia inhibitory factor augments neurotrophin expression and corticospinal axon growth after adult cns injury. J Neurosci 19 (1999) 3556-3566
4. Liu Y., Kim D., Himes B.T., Chow S.Y., Schallert T., Murray M., et al. Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 19 (1999) 4370-4387
5. Ramer M.S., Priestly J.V., and McMahon S.B. Functional regeneration of sensory axons into the adult spinal cord. Nature 403 (2000) 312-316
6. Blesch A., and Tuszynski M.H. Cellular gdnf delivery promotes growth of motor and dorsal column sensory axons after partial and complete spinal cord transections and induces remyelination. J Comp Neurol 467 (2003) 403-417
7. Blesch A., and Tuszynski M.H. Transient growth factor delivery sustains regenerated axons after spinal cord injury. J Neurosci 27 (2007) 10535-10545
8. Buffo A., Zagrebelsky M., Huber A.B., Skerra A., Schwab M.E., and Strata P. Application of neutralizing antibodies against Ni-35/250 myelin-associated neurite growth inhibitory proteins to the adult rat cerebellum induces sprouting of uninjured Purkinje cell axons. J Neurosci 20 (2000) 2275-2286
9. Kyoto A., Hata K., and Yamashita T. Synapse formation of the cortico-spinal axons is enhanced by RGMa inhibition after spinal cord injury. Brain Res 1186 (2007) 74-86
10. Yu P., Huang L., Zou J., Zhu H., Wang X., Yu Z., et al. DNA vaccine against NgR promotes functional recovery after spinal cord injury in adult rats. Brain Res 1147 (2007) 66-76
11. Guest J.D., Rao A., Olsen L., Bunge M.B., and Bunge R.P. The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp Neurol 148 (1997) 502-522
12. Li Y., and Raisman G. Integration of transplanted cultured Schwann cells into the long myelinated fiber tracts of the adult spinal cord. Exp Neurol 145 (1997) 397-411
13. McDonald J.W., Liu X.Z., Qu Y., Liu S., Mickey S.K., Turetsky D., et al. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat Med 5 (1999) 1410-1412
14. Tuszynski M.H., Peterson D.A., Ray J., Baird A., Nakahara Y., and Gage F.H. Fibroblasts genetically modified to produce nerve growth factor induce robust neuritic growth after grafting to the spinal cord. Exp Neurol 126 (1994) 1-14
15. Parr A.M., Tator C.H., and Keating A. Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant 40 (2007) 609-619
16. Parr A.M., Kulbatski I., Zahir T., Wang X., Yue C., Keating A., et al. Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155 (2008) 760-770
17. Guest J.D., Herrera L., Margitich I., Oliveria M., Marcillo A., and Casas C.E. Xenografts of expanded primate olfactory ensheathing glia support transient behavioral recovery that is independent of serotonergic or corticospinal axonal regeneration in nude rats following spinal cord transection. Exp Neurol 212 (2008) 261-274
18. Bamber N., Li H., Lu X., Oudega M., Aebischer P., and Xu X. Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur J Neurosci 13 (2001) 257-268
19. Brook G., Lawrence J., and Raisman G. Columns of Schwann cells extruded into the CNS induce in-growth of astrocytes to form organized new glial pathways. Glia 33 (2001) 118-130
20. Chen A., Xu X., Kleitman N., and Bunge M. Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp Neurol 138 (1996) 261-276
21. Kuhlengel K., Bunge M., Bunge R., and Burton H. Implantation of cultured sensory neurons and Schwann cells into lesioned neonatal rat spinal cord. Part II. Implant characteristics and examination of corticospinal tract growth. J Comp Neurol 293 (1990) 74-91
22. Li Y., and Raisman G. Schwann cells induce sprouting in motor and sensory axons in the adult rat spinal cord. J Neurosci 14 (1994) 4050-4063
23. Plant G., Harvey A., and Chirila T. Axonal growth within poly(2-hydroxyethyl methacrylate) sponges infiltrated with Schwann cells and implanted into the lesioned rat optic tract. Brain Res 671 (1995) 119-130
24. Stichel C., Hermanns S., Lausberg F., and Muller H. Effects of Schwann cell suspension grafts on axon regeneration in subacute and chronic CNS traumatic injuries. Glia 28 (1999) 156-165
25. Xu X., Zhang S., Li H., Aebischer P., and Bunge M. Regrowth of axons into the distal spinal cord through a Schwann-cell-seeded mini-channel implanted into hemisected adult rat spinal cord. Eur J Neurosci 11 (1999) 1723-1740
26. Agudo M., Woodhoo A., Webber D., Mirsky R., Jessen K.R., and McMahon S.B. Schwann cell precursors transplanted into the injured spinal cord multiply, integrate and are permissive for axon growth. Glia 56 (2008) 1263-1270
27. Golden K.L., Pearse D.D., Blits B., Garg M.S., Oudega M., Wood P.M., et al. Transduced Schwann cells promote axon growth and myelination after spinal cord injury. Exp Neurol 207 (2007) 203-217
28. Luis A.L., Rodrigues J.M., Amado S., Veloso A.P., Armada-Da-Silva P.A., Raimondo S., et al. PLGA 90/10 and caprolactone biodegradable nerve guides for the reconstruction of the rat sciatic nerve. Microsurgery 27 (2007) 125-137
29. Someya Y., Koda M., Dezawa M., Kadota T., Hashimoto M., Kamada T., et al. Reduction of cystic cavity, promotion of axonal regeneration and sparing and functional recovery with transplanted bone marrow stromal cell-derived Schwann cells after contusion injury to the adult rat spinal cord. J Neurosurg 9 (2008) 600-610
30. Zhang X., Zeng Y., Zhang W., Wang J., Wu J., and Li J. Co-transplantation of neural stem cells and NT-3-overexpressing Schwann cells in transected spinal cord. J Neurotrauma 24 (2007) 1863-1877
31. Novikova L.N., Pettersson J., Brohlin M., Wiberg M., and Novikov L.N. Biodegradable poly-beta-hydroxybutyrate scaffold seeded with Schwann cells to promote spinal cord repair. Biomaterials 29 (2008) 1198-1206
32. Ban DX, Kong XH, Feng SQ, Ning GZ, Chen JT, Guo SF. Intraspinal cord graft of autologous activated Schwann cells efficiently promotes axonal regeneration and functional recovery after rat's spinal cord injury. Brain Res 2009;1256:149.
33. Murphy W., Peters M., Kohn D., and Mooney D. Sustained release of vascular endothelial growth factor from mineralized poly(lactide-co-glycolide) scaffolds for tissue engineering. Biomaterials 21 (2000) 2521-2527
34. Lu L., Zhu X., Valenzuela R., Currier B., and Yaszemski M. Biodegradable polymer scaffolds for cartilage tissue engineering. Clin Orthop 391 (2001) S251-S270
35. Maquet V., Martin D., Scholtes F., Franzen R., Schoenen J., Moonen G., et al. Poly(d,l-lactide) foams modified by poly(ethylene oxide)-block-poly(d,l-lactide) copolymers and a-FGF: in vitro and in vivo evaluation for spinal cord regeneration. Biomaterials 22 (2001) 1137-1146
36. Jain R. The manufacturing techniques of various drug loaded biodegradable poly(lactide-co-glycolide) (PLGA) devices. Biomaterials 21 (2000) 2475-2490
37. Eliaz R., Wallach D., and Kost J. Delivery of soluble tumor necrosis factor receptor from in-situ forming PLGA implants: in-vivo. Pharm Res 17 (2000) 1546-1550
38. Gumusderelioglu M., and Deniz G. Sustained release of mitomycin-C from poly(d,l-lactide)/poly(d,l-lactide-co-glycolide) films. J Biomater Sci Polym Ed 11 (2000) 1039-1050
39. Xu X., Yee W.C., Hwang P.Y., Yu H., Wan A.C., Gao S., et al. Peripheral nerve regeneration with sustained release of poly(phosphoester) microencapsulated nerve growth factor within nerve guide conduits. Biomaterials 24 (2003) 2405-2412
40. Friedman J., Windebank A., Moore M., Spinner R., Currier B., and Yazemski M. Biodegradable polymer grafts for surgical repair of the injured spinal cord. Neurosurgery 51 (2002) 742-752
41. Bunge M. Bridging areas of injury in the spinal cord. Neuroscientist 7 (2001) 325-339
42. Bunge M. Bridging the transected or contused adult rat spinal cord with Schwann call and olfactory ensheathing glia transplants. Prog Brain Res 137 (2002) 275-282
43. Takami T., Oudega M., Bates M., Wood P., Kleitman N., and MB B. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22 (2002) 6670-6681
44. Novikova L.N., Novikov L.N., and Kellerth J.O. Biopolymers and biodegradable smart implants for tissue regeneration after spinal cord injury. Curr Opin Neurol 16 (2003) 711-715
45. Xu X., Guenard V., Kleitman N., and Bunge M. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J Comp Neurol 351 (1995) 145-160
46. Nomura H., Baladie B., Katayama Y., Morshead C.M., Shoichet M.S., and Tator C.H. Delayed implantation of intramedullary chitosan channels containing nerve grafts promotes extensive axonal regeneration after spinal cord injury. Neurosurgery 63 (2008) 127-141 discussion 141-123
47. Moore M.J., Friedman J.A., Lewellyn E.B., Mantila S.M., Krych A.J., Ameenuddin S., et al. Multiple-channel scaffolds to promote spinal cord axon regeneration. Biomaterials 27 (2006) 419-429
48. Brunden K.R., Windebank A.J., and Poduslo J.F. Role of axons in the regulation of P0 biosynthesis by schwann cells. J Neurosci Res 26 (1990) 135-143
49. Bunge M., Wood P., Tynan L., Bates M., and Sanes J. Perineurium originates from fibroblasts: demonstration in vitro with a retroviral marker. Science 243 (1989) 229-231
50. Dyck P., Dyck P., Giannini C., Sahenk Z., and Windebank A. Peripheral nerves. In: Graham D.I., and Lantos P.L. (Eds). Greenfield's neuropathology (2002), Arnold, London 551-675
51. Fitch M.T., Doller C., Combs C.K., Landreth G.E., and Silver J. Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 19 (1999) 8182-8198
52. McKeon R., Schreiber R., Rudge J., and Silver J. Reduction of neurite outgrowth in a model of glial scarring following cns injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11 (1991) 3398-3411
53. Puchala E., and Windle W. The possibility of structural and functional restitution after spinal cord injury. A review. Exp Neurol 55 (1977) 1-42
54. Ramon y Cajal S. Degeneration and regeneration of the nervous system [Engl. transl. and reprint, 1959]. New York: Hafner; 1928.
55. Reier P., Eng L., and Jakeman L. Reactive astrocyte and axonal outgrowth in the injured CNS: is gliosis really an impediment to regeneration?. In: Seil F.J. (Ed). Neural regeneration and transplantation (1989), Alan R Liss, New York 183-209
56. den Dunnen W., van der Lei B., Robinson P., Holwerda A., Pennings A., and Schakenraad J. Biological performance of a degradable poly(lactic acid-epsilon-caprolactone) nerve guide: influence of tube dimensions. J Biomed Mater Res 29 (1995) 757-766
57. Ekholm M., Hietanen J., Tulamo R., Muhonen J., Lindqvist C., Kellomaki M., and Rasfds S. Tissue reactions of subcutaneously implanted mixture of epsilon-caprolactone-lactide copolymer and tricalcium phosphate. An electron microscopic evaluation in sheep. J Mater Sci Mater Med 14 10 (2003) 913-918
58. Chen BK, Gross L, de Ruiter GC, Knight AM, Nesbitt JJ, Podratz JL, et al. Axon regeneration through scaffold into distal spinal cord after transection. J Neurotrauma, in press.