Mats made from fibronectin support oriented growth of axons in the damaged spinal cord of the adult rat

Experimental Neurology

Volumn 182, Issue 2, 2003, Pages 383-398

  King, Von R ^a,d   Henseler, Manuel ^b   Brown, Robert A ^c   Priestley, John V ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Fibronectin; Neurotrophins; Regeneration; Schwann cells; Spinal cord; Synthetic implant

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALPHA ADRENERGIC RECEPTOR; BIOMATERIAL; CALCITONIN GENE RELATED PEPTIDE; CHOLERA TOXIN; FIBRONECTIN; GLUTAMATE RECEPTOR; GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; SUBSTANCE P;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL TRANSPLANTATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; INCUBATION TIME; NERVE FIBER; NERVE FIBER REGENERATION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; SCHWANN CELL; SENSORY NERVE; SPINAL CORD LESION;

EID: 0042665647     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00033-5     Document Type: Article

References (57)

1. Ahmed Z., Brown R.A. Adhesion, alignment, and migration of cultured Schwann cells on ultrathin fibronectin fibres. Cell Motil. Cytoskelton. 42:1999;331-343.
2. Bailey S.B., Eichler M.E., Villadiego A., Rich K.M. The influence of fibronectin and laminin during Schwann cell migration and peripheral nerve regeneration through silicon chambers. J. Neurocytol. 22:1993;176-184.
3. Blesch A., Tuszynski M.H. Robust growth of chronically injured spinal cord axons induced by grafts of genetically modified NGF secreting cells. Exp. Neurol. 148:1997;444-452.
4. Bradbury E.J., Khemani S., King V.R., Priestley J.V., McMahon S.B. NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur. J. Neurosci. 11:1999;3873-3883.
5. Bradbury E.J., King V.R., Simmons L.J., Priestley J.V., McMahon S.B. NT-3, but not BDNF, prevents atrophy and death of axotomized spinal cord projection neurons. Eur. J. Neurosci. 10:1998;3058-3068.
6. Bregman B.S., McAtee M., Dai H.N., Kuhn P.L. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp. Neurol. 148:1997;475-494.
7. Brook G.A., Plate D., Franzen R., Martin D., Moonen G., Schoenen J., Schmitt A.B., Noth J., Nacimiento W. Spontaneous longitudinally oriented axonal regeneration is associated with the Schwann cell framework within the lesion site following spinal cord compression injury of the rat. J. Neurosci. Res. 53:1998;51-65.
8. Brown R.A., Blunn G.W., Ejim O.S. Preparation of orientated fibrous mats from fibronectin: composition and stability. Biomaterials. 15:1994;457-464.
9. Cai D., Shen Y., De Bellard M., Tang S., Filbin M.T. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron. 22:1999;89-101.
10. Chauhan N.B., Figlewicz H.M., Khan T. Carbon filaments direct the growth of postlesional plastic axons after spinal cord injury. Int. J. Dev. Neurosci. 17:1999;255-264.
11. Ejim O.S., Blunn G.W., Brown R.A. Production of artificial-orientated mats and strands from plasma fibronectin: a morphological study. Biomaterials. 14:1993;743-748.
12. Gautier S.E., Oudega M., Fragoso M., Chapon P., Plant G.W., Bunge M.B., Parel J.M. Poly(alpha-hydroxyacids) for application in the spinal cord: resorbability and biocompatibility with adult rat Schwann cells and spinal cord. J. Biomed. Mater. Res. 42:1998;642-654.
13. Giehl K.M., Tetzlaff W. BDNF and NT-3, but not NGF prevent axotomy-induced cell death of rat corticospinal neurones in vivo. Eur. J. Neurosci. 8:1996;1167-1175.
14. Goldberg J.L., Barres B.A. The relationship between neuronal survival and regeneration. Annu. Rev. Neurosci. 23:2000;579-612.
15. Grill R., Murai D., Blesch A., Gage F.H., Tuszynski M.H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial function recovery after spinal cord injury. J. Neurosci. 17:1997;5560-5572.
16. Horner P.J., Gage F.H. Regenerating the damaged central nervous system. Nature. 407:2000;963-970.
17. Houle J.D., Ziegler M.K. Bridging a complete transection lesion of adult rat spinal cord with growth factor-treated nitrocellulose paper. J. Neural Trans. Plas. 5:1994;115-124.
18. Houweling D.A., Lankhorst A.J., Gispen W.H., Bär P.R., Joosten E.A.J. Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery. Exp. Neurol. 153:1998;49-59.
19. Ide C. Peripheral nerve regeneration. Neurosci. Res. 25:1996;101-121.
20. Jessen K.R., Mirsky R. Schwann cell precursors and their development. Glia. 4:1991;185-194.
21. Kashiba H., Noguchi K., Ueda Y., Senba E. Coexpression of trk family members and low-affinity neurotrophin receptors in rat dorsal-root ganglion neurons. Mol. Brain Res. 30:1995;158-164.
22. King V.R., Bradbury E.J., McMahon S.B., Priestley J.V. Changes in truncated trkB and p75 receptor expresssion in the rat spinal cord following spinal cord hemisection and spinal cord hemisection plus neurotrophin treatment. Exp. Neurol. 165:2000;327-341.
23. King V.R., McBride A., Priestley J.V. Immunohistochemical expression of the α5 integrin subunit in the normal adult rat nervous system. J. Neurocytol. 30:2001;243-252.
24. King V.R., Michael G.J., Joshi R.K., Priestley J.V. TrkA, trkB, and trkC messenger RNA expression by bulbospinal cells of the rat. Neuroscience. 92:1999;935-944.
25. King V.R., Priestley J.V., Hunt-Grubbe H., Brown R. Glial, macrophage and blood vessel infiltration into fibronectin mats implanted into the injured rat spinal cord. Soc. Neurosci. Abstr. 26:2000;864.
26. Kobayashi N.R., Fan D.P., Giehl K.M., Bedard A.M., Wiegand S.J., Tetzlaff W. BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and T-Alpha1 tubulin mRNA expression, and promote axonal regeneration. J. Neurosci. 17:1997;9583-9595.
27. Li Y., Raisman G. Schwann cells induce sprouting in motor and sensory axons in the adult rat spinal cord. J. Neurosci. 14:1994;4050-4063.
28. Li Y., Raisman G. Integration of transplanted cultured Schwann cells in the long myelinated fiber tracts of the adult spinal cord. Exp. Neurol. 145:1997;397-411.
29. Liu Y., Kim D., Himes B.T., Chow S.Y., Schallert T., Murray M., Tessler A., Fischer I. 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.
30. McMahon S.B., Armanini M.P., Ling L.H., Phillips H.S. Expression and coexpression of trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron. 12:1994;1161-1171.
31. Menei P., Montero-Menei C., Whittemore S.R., Bunge R.P., Bunge M.B. Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. Eur. J. Neurosci. 10:1998;607-621.
32. Milner R., Wilby M., Nishimura S., Boylen K., Edwards G., Fawcett J., Streuli C., Pytella R., ffrench-Constant C. Division of labor of Schwann cell integrins during migration on peripheral nerve extracellular matrix ligans. Dev. Biol. 185:1997;215-228.
33. Neumann S., Woolf C.J. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron. 23:1999;83-91.
34. Prewitt C.M., Niesman I.R., Kane C.J., Houle J.D. Activated macrophage/microglial cells can promote the regeneration of sensory axons into the injured spinal cord. Exp. Neurol. 148:1997;433-443.
35. Priestley, J.V., Alvarez, F.J., Averill, S., 1992. Pre-embedding electron microscopic immunocytochemistry, in: Polak, J.M., Priestley, J.V. (Eds.), Electron Microscopic Immunocytochemistry, Oxford University Press, Oxford, UK, pp. 89-121.
36. Proudfit H.K., Clark F.M. The projections of locus coeruleus neurons to the spinal cord. Prog. Brain Res. 88:1991;123-141.
37. Rabchevsky A.G., Streit W.J. Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J. Neurosci. Res. 47:1997;4-48.
38. Ramer M.S., Duraisingam I., Priestley J.V., McMahon S.B. Two-tiered inhibition of axonal regeneration at the dorsal root entry zone. J. Neurosci. 21:2001;2560-2651.
39. Ramer M.S., Priestley J.V., McMahon S.B. Functional regeneration of sensory axons into the adult spinal cord. Nature. 403:2000;312-316.
40. Reichardt L.F., Tomaselli K.J. Extracellular matrix molecules and their receptors: functions in neural development. Annu. Rev. Neurosci. 14:1991;531-570.
41. Richardson P.M., Issa V.M. Peripheral injury enhances central regeneration of primary sensory neurones. Nature. 309:1984;791-793.
42. Rogers S.L., Letourneau P.C., Peterson B.A., Furcht L.T., McCarthy J.B. Selective interaction of peripheral and central nervous system cells with two distinct cell binding domains of fibronectin. J. Cell Biol. 105:1987;1435-1442.
43. Schnell L., Schneider R., Kolbeck R., Barde Y.A., Schwab M.E. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature. 367:1994;170-173.
44. Sensenbrenner M., Lucas M., Deloulme J.C. Expression of two neuronal markers, growth-associated protein 43 and neuron-specific enolase, in rat glial cells. J. Mol. Med. 75:1997;653-663.
45. Sterne G.D., Brown R.A., Green C.J., Terenghi G. Neurotrophin-3 delivered locally via fibronectin mats enhances peripheral nerve regeneration. Eur. J. Neurosci. 9:1997;1388-1396.
46. Terenghi G. Peripheral nerve regeneration and neurotrophic factors. J. Anat. 194:1999;1-14.
47. Weidner N., Blesch A., Grill R.J., Tuszynski M.H. Nerve-growth factor hypersecreting Schwann cells grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with the expression of L1. J. Comp. Neurol. 413:1999;495-506.
48. Whitworth I.H., Brown R.A., Dore C.J., Anand P., Green C.J., Terenghi G. Nerve growth factor enhances nerve regeneration through fibronectin grafts. J. Hand Surg. 21:1996;514-522.
49. Whitworth I.H., Terenghi G., Green C.J., Brown R.A., Stevens E., Tomlinson D.R. Target delivery of nerve growth factor via fibronectin conduit assists nerve regeneration in control and diabetic rats. Eur. J. Neurosci. 7:1995;2220-2225.
50. Wilson P.O.G., Barber P.C., Hamid Q.A., Power B.F., Dhillon A.P., Rode J., Day I.N., Thompson R.J., Polak J.M. The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br. J. Exp. Pathol. 69:1988;91-104.
51. Woerly S., Petrov P., Sykova E., Roitbak T., Simonova Z., Harvey A.R. Neural tissue formation within porous hydrogels implanted in brain and spinal cord lesions: ultrastructural, immunohistochemical, and diffusion studies. Tissue Eng. 5:1999;467-488.
52. Woerly S., Pinet E., DeRobertis L., Bousmina M., Laroche G., Roitback T., Vargova L., Sykov E. Heterogenous PHPMA hydrogels for tissue repair and axonal regeneration in the injured spinal cord. J. Biomater. Sci. Polym. Ed. 9:1998;681-711.
53. Wright D.E., Snider W.D. Neurotrophin receptor mRNA expression defines distinct subpopulations of neurons in rat dorsal root ganglia. J. Comp. Neurol. 351:1995;329-338.
54. Xu X.M., Guènard V., Kleitman N., Bunge M.B. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 351:1995;145-160.
55. Xu X.M., Zhan S.-X., Li H., Aebischer P., Bunge M.B. 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.
56. Yanagida H., Tanaka J., Maruo S. Immunocytochemical localization of a cell adhesion molecule, integrin alpha5beta1, in nerve growth cones. J. Orthop. Sci. 4:1999;353-360.
57. Ye J.H., Houle J.D. Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143:1997;70-81.