Directed nerve outgrowth is enhanced by engineered glial substrates

Experimental Neurology

Volumn 184, Issue 1, 2003, Pages 141-152

  Biran, Roy ^a   Noble, Mark D ^b   Tresco, Patrick A ^a,c  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c University of Utah   (United States)

Author keywords

Astrocyte; Axon; Biomaterial; Engineer; Extracellular matrix; Glia; Guidance; Neurite; Neurite outgrowth; Oriented

Indexed keywords

FIBRONECTIN; LAMININ; NERVE CELL ADHESION MOLECULE; PROTEOCHONDROITIN SULFATE;

ANIMAL CELL; ARTICLE; ASTROCYTE; BIOENGINEERING; CELL CULTURE; CELL GROWTH; CELL SURFACE; GLIA; IN VITRO STUDY; NERVE FIBER; NERVE FIBER REGENERATION; NERVE REGENERATION; NEURITE; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL GANGLION;

EID: 0345689366     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00253-X     Document Type: Article

References (79)

1. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., Watson, J., 1994. Cell junctions, cell adhesion, and the extracellular matrix, in: Molecular Biology of the Cell, Garland Publishing Inc., New York, pp. 984-999.
2. Anderson P.N., Turmaine M. Axonal regeneration through arterial grafts. J. Anat. 147:1986;73-82.
3. Bandtlow C.E., Schwab M.E. NI-35/250/nogo-a a neurite growth inhibitor restricting structural plasticity and regeneration of nerve fibers in the adult vertebrate CNS. Glia. 29:2000;175-181.
4. Barrett C.P., Guth L., Donati E.J., Krikorian J.G. Astroglial reaction in the gray matter lumbar segments after midthoracic transection of the adult rat spinal cord. Exp. Neurol. 73:1981;365-377.
5. Bernstein J.J., Getz R., Jefferson M., Kelemen M. Astrocytes secrete basal lamina after hemisection of rat spinal cord. Brain Res. 327:1985;135-141.
6. Berry M., Maxwell W.L., Logan A., Mathewson A., McConnell P., Ashhurst D.E., Thomas G.H. Deposition of scar tissue in the central nervous system. Acta Neurochir. Suppl. 32:1983;31-53.
7. Biran R., Webb K., Noble M.D., Tresco P.A. Surfactant-immobilized fibronectin enhances bioactivity and regulates sensory neurite outgrowth. J. Biomed. Mater. Res. 55:2001;1-12.
8. Bohn R.C., Reier P.J., Sourbeer E.B. Axonal interactions with connective tissue and glial substrata during optic nerve regeneration in Xenopus larvae and adults. Am. J. Anat. 165:1982;397-419.
9. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature. 416:2002;636-640.
10. Brook G., Lawrence J., 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.
11. Brook G.A., Lawrence J.M., Shah B., Raisman G. Extrusion transplantation of Schwann cells into the adult rat thalamus induces directional host axon growth. Exp. Neurol. 126:1994;31-43.
12. Brook G.A., Plate D., Franzen R., Martin D., Moonen G., Schoenen J., Schmitt A.B., Noth J., Nacimiento W. Spontaneous longitudinally orientated 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.
13. Bunge M.B. Bridging areas of injury in the spinal cord. Neuroscientist. 7:2001;325-339.
14. Bungner O. Die degenerations-und regenerationvorganange am nerven nach verletzungen. Beitr. Pathol. Anal. 10:1891;321-393.
15. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ F., Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature. 403:2000;434-439.
16. Chiu D.T., Janecka I., Krizek T.J., Wolff M., Lovelace R.E. Autogenous vein graft as a conduit for nerve regeneration. Surgery. 91:1982;226-233.
17. Clemente C. Structural regeneration in the mammalian central nervous system and the role of neuroglia and connective tissue. Windle W. Regeneration in the Nervous System. 1955;147-161 Thomas, Springfield, IL.
18. David S., Aguayo A.J. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science. 214:1981;931-933.
19. Davies S.J., Fitch M.T., Memberg S.P., Hall A.K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature. 390:1997;680-683.
20. Davies S.J., Goucher D.R., Doller C., Silver J. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 19:1999;5810-5822.
21. Del Rio Hortega P., Penfield W. Cerebral cicatrix; the reaction of neuroglia and microglia to brain wounds. Bull, Johns Hopkins Hosp. 41:1927;278-303.
22. den Braber E.T., de Ruijter J.E., Ginsel L.A., von Recum A.F., Jansen J.A. Orientation of ECM protein deposition, fibroblast cytoskeleton, and attachment complex components on silicone microgrooved surfaces. J. Biomed. Mater. Res. 40:1998;291-300.
23. Eddleston M., Mucke L. Molecular profile of reactive astrocytes - implications for their role in neurologic disease. Neuroscience. 54:1993;15-36.
24. Faissner A., Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron. 5:1990;627-637.
25. Fitch M.T., Silver J. Glial cell extracellular matrix boundaries for axon growth in development and regeneration. Cell Tissue Res. 290:1997;379-384.
26. Flemming R.G., Murphy C.J., Abrams G.A., Goodman S.L., Nealey P.F. Effects of synthetic micro- and nano-structured surfaces on cell behavior. Biomaterials. 20:1999;573-588.
27. Frisen J., Haegerstrand A., Risling M., Fried K., Johansson C.B., Hammarberg H., Elde R., Hokfelt T., Cullheim S. Spinal axons in central nervous system scar tissue are closely related to laminin-immunoreactive astrocytes. Neuroscience. 65:1995;293-304.
28. Geller H.M., Fawcett J.W. Building a bridge engineering spinal cord repair. Exp. Neurol. 174:2002;125-136.
29. Glasby M.A., Gschmeissner S.G., Hitchcock R.J., Huang C.L. The dependence of nerve regeneration through muscle grafts in the rat on the availability and orientation of basement membrane. J. Neurocytol. 15:1986;497-510.
30. Gomez T.M., Letourneau P.C. Filopodia initiate choices made by sensory neuron growth cones at laminin/fibronectin borders in vitro. J. Neurosci. 14:1994;5959-5972.
31. Grierson J.P., Petroski R.E., Ling D.S., Geller H.M. Astrocyte topography and tenascin cytotactin expression correlation with the ability to support neuritic outgrowth. Brain Res. Dev. Brain Res. 55:1990;11-19.
32. Grill R., Murai K., Blesch A., Gage F.H., Tuszynski M.H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17:1997;5560-5572.
33. Grimpe B., Dong S., Doller C., Temple K., Malouf A.T., Silver J. The critical role of basement membrane-independent laminin gamma 1 chain during axon regeneration in the CNS. J. Neurosci. 22:2002;3144-3160.
34. Hammarback J.A., Palm S.L., Furcht L.T., Letourneau P.C. Guidance of neurite outgrowth by pathways of substratum-adsorbed laminin. J. Neurosci. Res. 13:1985;213-220.
35. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El Manira A., Prockop D.J., Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. USA. 99:2002;2199-2204.
36. Kawaja M.D., Gage F.H. Reactive astrocytes are substrates for the growth of adult CNS axons in the presence of elevated levels of nerve growth factor. Neuron. 7:1991;1019-1030.
37. Keynes R.J., Hopkins W.G., Huang L.H. Regeneration of mouse peripheral nerves in degenerating skeletal muscle guidance by residual muscle fibre basement membrane. Brain Res. 295:1984;275-281.
38. Leavitt B.R., Hernit-Grant C.S., Macklis J.D. Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp. Neurol. 157:1999;43-57.
39. Li Y., Field P.M., Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J. Neurosci. 18:1998;10514-10524.
40. Liesi P. Laminin-immunoreactive glia distinguish regenerative adult CNS systems from non-regenerative ones. EMBO J. 4:1985;2505-2511.
41. Liesi P., Dahl D., Vaheri A. Laminin is produced by early rat astrocytes in primary culture. J. Cell Biol. 96:1983;920-924.
42. Liesi P., Silver J. Is astrocyte laminin involved in axon guidance in the mammalian CNS. Dev. Biol. 130:1988;774-785.
43. McCarthy K.D., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85:1980;890-902.
44. McKeon R.J., Schreiber R.C., Rudge J.S., 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.
45. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron. 13:1994;805-811.
46. Meiners S., Powell E.M., Geller H.M. A distinct subset of tenascin/CS-6-PG-rich astrocytes restricts neuronal growth in vitro. J. Neurosci. 15:1995;8096-8108.
47. Miller C., Jeftinija S., Mallapragada S. Micropatterned Schwann cell-seeded biodegradable polymer substrates significantly enhance neurite alignment and outgrowth. Tissue Eng. 7:2001;705-715.
48. Neugebauer K.M., Tomaselli K.J., Lilien J., Reichardt L.F. N-cadherin, NCAM, and integrins promote retinal neurite outgrowth on astrocytes in vitro. J. Cell Biol. 107:1988;1177-1187.
49. Nguyen Q.T., Sanes J.R., Lichtman J.W. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5:2002;861-867.
50. Noble M., Albrechtsen M., Moller C., Lyles J., Bock E., Goridis C., Watanabe M., Rutishauser U. Glial cells express N-CAM/D2-CAM-like polypeptides in vitro. Nature. 316:1985;725-728.
51. Noble M., Fok-Seang J., Cohen J. Glia are a unique substrate for the in vitro growth of central nervous system neurons. J. Neurosci. 4:1984;1892-1903.
52. Pettigrew D.B., Crutcher K.A. White matter of the CNS supports or inhibits neurite outgrowth in vitro depending on geometry. J. Neurosci. 19:1999;8358-8366.
53. Pettigrew D.B., Crutcher K.A. Myelin contributes to the parallel orientation of axonal growth on white matter in vitro. BMC Neurosci. 2:2001;9.
54. Pettigrew D.B., Shockley K.P., Crutcher K.A. Disruption of spinal cord white matter and sciatic nerve geometry inhibits axonal growth in vitro in the absence of glial scarring. BMC Neurosci. 2:2001;8.
55. Powell E.M., Meiners S., DiProspero N.A., Geller H.M. Mechanisms of astrocyte-directed neurite guidance. Cell Tissue Res. 290:1997;385-393.
56. Powell E.M., Mercado M.L., Calle-Patino Y., Geller H.M. Protein kinase C mediates neurite guidance at an astrocyte boundary. Glia. 33:2001;288-297.
57. Price J., Hynes R.O. Astrocytes in culture synthesize and secrete a variant form of fibronectin. J. Neurosci. 5:1985;2205-2211.
58. Reier P.J., Houle J.D. The glial scar its bearing on axonal elongation and transplantation approaches to CNS repair. Adv. Neurol. 47:1988;87-138.
59. Richardson P.M., McGuinness U.M., Aguayo A.J. Axons from CNS neurons regenerate into PNS grafts. Nature. 284:1980;264-265.
60. Risling M., Fried K., Linda H., Carlstedt T., Cullheim S. Regrowth of motor axons following spinal cord lesions distribution of laminin and collagen in the CNS scar tissue. Brain Res. Bull. 30:1993;405-414.
61. Rudge J.S., Silver J. Inhibition of neurite outgrowth on astroglial scars in vitro. J. Neurosci. 10:1990;3594-3603.
62. Schachner M., Kim S.K., Zehnle R. Developmental expression in central and peripheral nervous system of oligodendrocyte cell surface antigens (O antigens) recognized by monoclonal antibodies. Dev. Biol. 83:1981;328-338.
63. Silver J., Edwards M.A., Levitt P. Immunocytochemical demonstration of early appearing astroglial structures that form boundaries and pathways along axon tracts in the fetal brain. J. Comp. Neurol. 328:1993;415-436.
64. Singhvi R., Stephanopoulos G., Wang D.I.C. Review effects of substratum morphology on cell physiology. Biotechnol. Bioengin. 43:1994;764-771.
65. Snow D.M., Lemmon V., Carrino D.A., Caplan A.I., Silver J. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 109:1990;111-130.
66. Steindler D.A., O'Brien T.F., Cooper N.G. Glycoconjugate boundaries during early postnatal development of the neostriatal mosaic. J. Comp. Neurol. 267:1988;357-369.
67. Stensaas S.S., Stensaas L.J. The reaction of the cerebral cortex to chronically implanted plastic needles. Acta Neuropathol. 35:1976;187-203.
68. Stensaas S.S., Stensaas L.J. Histopathological evaluation of materials implanted in the cerebral cortex. Acta Neuropathol. (Berl.). 41:1978;145-155.
69. Sung J.H. Tangled masses of regenerated central nerve fibers (non-myelinated central neuromas) in the central nervous system. J. Neuropathol. Exp. Neurol. 40:1981;645-657.
70. Tello F. La influencia del neurotropismo en la regeneracion de los centros nerviosos. Trab. Lab. Invest. Biol. 9:1911;123-159.
71. Teng Y.D., Lavik E.B., Qu X., Park K.I., Ourednik J., Zurakowski D., Langer R., Snyder E.Y. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl. Acad. Sci. USA. 99:2002;3024-3029.
72. Tomaselli K.J., Neugebauer K.M., Bixby J.L., Lilien J., Reichardt L.F. N-Cadherin and integrins two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron. 1:1988;33-43.
73. Tresco P.A. Tissue engineering strategies for nervous system repair. Prog. Brain Res. 128:2000;349-363.
74. van Kooten T.G., von Recum A.F. Cell adhesion to textured silicone surfaces the influence of time of adhesion and texture on focal contact and fibronectin fibril formation. Tissue Eng. 5:1999;223-240.
75. Webb A., Clark P., Skepper J., Compston A., Wood A. Guidance of oligodendrocytes and their progenitors by substratum topography. J. Cell Sci. 108:1995;2747-2760.
76. Winn S.R., Aebischer P., Galletti P.M. Brain tissue reaction to permselective polymer capsules. J. Biomed. Mater. Res. 23:1989;31-44.
77. Woerly S., Marchand R., Lavallee C. Interactions of copolymeric poly(glyceryl methacrylate)-collagen hydrogels with neural tissue effects of structure and polar groups. Biomaterials. 12:1991;197-203.
78. Wrede L. Ueberbruckung eines nervendefektes mittels seidennhat und lebenden venenstuckes. Dtsch. Med. Wochenschr. 35:1909;1125.
79. Xu X.M., Zhang 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.