Long-term characterization of axon regeneration and matrix changes using multiple channel bridges for spinal cord regeneration

Tissue Engineering - Part A

Volumn 20, Issue 5-6, 2014, Pages 1027-1037

  Tuinstra, Hannah M ^a   Margul, Daniel J ^a   Goodman, Ashley G ^a   Boehler, Ryan M ^a   Holland, Samantha J ^a   Zelivyanskaya, Marina L ^a   Cummings, Brian J ^b,c   Anderson, Aileen J ^b,c   Shea, Lonnie D ^a,d,e  

^a Northwestern University   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; DEGRADATION; NEURONS; REPAIR;

AXON REGENERATION; BRIDGE STRUCTURES; CELL INFILTRATION; CHONDROITIN SULFATES; DEGREE OF CONNECTIVITY; MICROENVIRONMENTS; MULTIPLE CHANNELS; SPINAL CORD INJURIES (SCI);

DEPOSITION;

COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBRONECTIN; LAMININ; POLYGLACTIN; PROTEOCHONDROITIN SULFATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; MEDICAL DEVICE; MULTIPLE CHANNEL BRIDGE; MYELINATION; NERVE FIBER; NERVE FIBER REGENERATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SCHWANN CELL; SPINAL CORD INJURY; SPINAL CORD REGENERATION;

ACETYLCHOLINESTERASE; ANIMALS; AXONS; CALCITONIN GENE-RELATED PEPTIDE; CHONDROITIN SULFATES; COLLAGEN TYPE I; COLLAGEN TYPE IV; EXTRACELLULAR MATRIX; FEMALE; FIBRONECTINS; LAMININ; MYELIN SHEATH; RATS; RATS, LONG-EVANS; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; TIME FACTORS;

EID: 84896843874     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0111     Document Type: Article

References (72)

1. Richardson, P.M., McGuinness, U.M., and Aguayo, A.J. Axons from CNS neurons regenerate into PNS grafts. Nature 284, 264, 1980
2. David, S., and Aguayo, A.J. Axonal elongation into peripheral nervous system ''bridges'' after central nervous system injury in adult rats. Science 214, 931, 1981
3. Geller, H.M., and Fawcett, J.W. Building a bridge: Engineering spinal cord repair. Exp Neurol 174, 125, 2002
4. Joosten, E.A. Biodegradable biomatrices and bridging the injured spinal cord: The corticospinal tract as a proof of principle. Cell Tissue Res 349, 375, 2012
5. Wang, M., Zhai, P., Chen, X., Schreyer, D.J., Sun, X., and Cui, F. Bioengineered scaffolds for spinal cord repair. Tissue Eng Part B Rev 17, 177, 2011
6. Lonjon, N., Kouyoumdjian, P., Prieto, M., Bauchet, L., Haton, H., Gaviria, M., et al. Early functional outcomes and histological analysis after spinal cord compression injury in rats. J Neurosurg Spine 12, 106, 2010
7. Martin, D., Schoenen, J., Delree, P., Gilson, V., Rogister, B., Leprince, P., et al. Experimental acute traumatic injury of the adult rat spinal cord by a subdural inflatable balloon: Methodology, behavioral analysis, and histopathology. J Neurosci Res 32, 539, 1992
8. Vanicky, I., Urdzikova, L., Saganova, K., Cizkova, D., and Galik, J. A simple and reproducible model of spinal cord injury induced by epidural balloon inflation in the rat. J Neurotrauma 18, 1399, 2001
9. Young, W. Spinal cord contusion models. Prog Brain Res 137, 231, 2002
10. Schwab, M.E., and Bartholdi, D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76, 319, 1996
11. Zhang, S.X., Huang, F., Gates, M., White, J., and Holmberg, E.G. Histological repair of damaged spinal cord tissue from chronic contusion injury of rat: A LM observation. Histol Histopathol 26, 45, 2011
12. Beattie, M.S. Anatomic and behavioral outcome after spinal cord injury produced by a displacement controlled impact device. J Neurotrauma 9, 157-9; discussion 9-60, 1992
13. Zhang, S.X., Geddes, J.W., Owens, J.L., and Holmberg, E.G. X-irradiation reduces lesion scarring at the contusion site of adult rat spinal cord. Histol Histopathol 20, 519, 2005
14. Gledhill, R.F., Harrison, B.M., and McDonald, W.I. Demyelination and remyelination after acute spinal cord compression. Exp Neurol 38, 472, 1973
15. Zhang, S.X., Huang, F., Gates, M., and Holmberg, E.G. Scar ablation combined with LP/OEC transplantation promotes anatomical recovery and P0-positive myelination in chronically contused spinal cord of rats. Brain Res 1399, 1, 2011
16. Beattie, M.S., Bresnahan, J.C., Komon, J., Tovar, C.A., Van Meter, M., Anderson, D.K., et al. Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148, 453, 1997
17. Behrmann, D.L., Bresnahan, J.C., Beattie, M.S., and Shah, B.R. Spinal cord injury produced by consistent mechanical displacement of the cord in rats: Behavioral and histologic analysis. J Neurotrauma 9, 197, 1992
18. Wong, D.Y., Leveque, J.C., Brumblay, H., Krebsbach, P.H., Hollister, S.J., and Lamarca, F. Macro-Architectures in spinal cord scaffold implants influence regeneration. J Neurotrauma 25, 1027, 2008
19. De Laporte, L., Yang, Y., Zelivyanskaya, M.L., Cummings, B.J., Anderson, A.J., and Shea, L.D. Plasmid releasing multiple channel bridges for transgene expression after spinal cord injury. Mol Ther 17, 318, 2009
20. Yao, L., de Ruiter, G.C., Wang, H., Knight, A.M., Spinner, R.J., Yaszemski, M.J., et al. Controlling dispersion of axonal regeneration using a multichannel collagen nerve conduit. Biomaterials 31, 5789, 2010
21. De Laporte, L., Yan, A.L., and Shea, L.D. Local gene delivery from ECM-coated poly(lactide-co-glycolide) multiple channel bridges after spinal cord injury. Biomaterials 30, 2361, 2009
22. Yang, Y., De Laporte, L., Zelivyanskaya, M.L., Whittlesey, K.J., Anderson, A.J., Cummings, B.J., et al. Multiple channel bridges for spinal cord injury: Cellular characterization of host response. Tissue Eng Part A 15, 3283, 2009
23. Tuinstra, H.M., Aviles, M.O., Shin, S., Holland, S.J., Zelivyanskaya, M.L., Fast, A.G., et al. Multifunctional, multichannel bridges that deliver neurotrophin encoding lentivirus for regeneration following spinal cord injury. Biomaterials 33, 1618, 2012
24. Fawcett, J.W. Overcoming inhibition in the damaged spinal cord. J Neurotrauma 23, 371, 2006
25. Fitch, M.T., and Silver, J. CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol 209, 294, 2008
26. Silver, J., and Miller, J.H. Regeneration beyond the glial scar. Nat Rev Neurosci 5, 146, 2004
27. Avnur, Z., and Geiger, B. Immunocytochemical localization of native chondroitin-sulfate in tissues and cultured cells using specific monoclonal antibody. Cell 38, 811, 1984
28. Loy, D.N., Crawford, C.H., Darnall, J.B., Burke, D.A., Onifer, S.M., and Whittemore, S.R. Temporal progression of angiogenesis and basal lamina deposition after contusive spinal cord injury in the adult rat. J Comp Neurol 445, 308, 2002
29. Cholas, R.H., Hsu, H.P., and Spector, M. The reparative response to cross-linked collagen-based scaffolds in a rat spinal cord gap model. Biomaterials 33, 2050, 2012
30. Bixby, J.L., and Harris, W.A. Molecular mechanisms of axon growth and guidance. Annu Rev Cell Biol 7, 117, 1991
31. Patist, C.M., Mulder, M.B., Gautier, S.E., Maquet, V., Jerome, R., and Oudega, M. Freeze-dried poly(D,L-lactic acid) macroporous guidance scaffolds impregnated with brain-derived neurotrophic factor in the transected adult rat thoracic spinal cord. Biomaterials 25, 1569, 2004
32. Hurtado, A., Moon, L.D., Maquet, V., Blits, B., Jerome, R., and Oudega, M. Poly (D,L-lactic acid) macroporous guidance scaffolds seeded with Schwann cells genetically modified to secrete a bi-functional neurotrophin implanted in the completely transected adult rat thoracic spinal cord. Biomaterials 27, 430, 2006
33. Friedman, J.A., Windebank, A.J., Moore, M.J., Spinner, R.J., Currier, B.L., and Yaszemski, M.J. Biodegradable polymer grafts for surgical repair of the injured spinal cord. Neurosurgery 51, 742, 2002
34. 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, 419, 2006
35. Chen, B.K., Knight, A.M., de Ruiter, G.C.W., Spinner, R.J., Yaszemski, M.J., Currier, B.L., et al. Axon regeneration through scaffold into distal spinal cord after transection. J Neurotrauma 26, 1759, 2009
36. Krych, A.J., Rooney, G.E., Chen, B., Schermerhorn, T.C., Ameenuddin, S., Gross, L., et al. Relationship between scaffold channel diameter and number of regenerating axons in the transected rat spinal cord. Acta Biomater 5, 2551, 2009
37. Olson, H.E., Rooney, G.E., Gross, L., Nesbitt, J.J., Galvin, K.E., Knight, A., et al. Neural stem cell- And Schwann cellloaded biodegradable polymer scaffolds support axonal regeneration in the transected spinal cord. Tissue Eng Part A 15, 1797, 2009
38. Chen, B.K., Knight, A.M., Madigan, N.N., Gross, L.A., Dadsetan, M., Nesbitt, J.J., et al. Comparison of polymer scaffolds in rat spinal cord: A step toward quantitative assessment of combinatorial approaches to spinal cord repair. Biomaterials 32, 8077, 2011
39. Stokols, S., Sakamoto, J., Breckon, C., Holt, T., Weiss, J., and Tuszynski, M.H. Templated agarose scaffolds support linear axonal regeneration. Tissue Eng 12, 2777, 2006
40. Stokols, S., and Tuszynski, M.H. Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. Biomaterials 27, 443, 2006
41. Stokols, S., and Tuszynski, M.H. The fabrication and characterization of linearly oriented nerve guidance scaffolds for spinal cord injury. Biomaterials 25, 5839, 2004
42. Yu, T.T., and Shoichet, M.S. Guided cell adhesion and outgrowth in peptide-modified channels for neural tissue engineering. Biomaterials 26, 1507, 2005
43. Eyre, J.A. Corticospinal tract development and its plasticity after perinatal injury. Neurosci Biobehav Rev 31, 1136, 2007
44. 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, 127; discussion 41, 2008
45. Richardson, P.M., McGuinness, U.M., and Aguayo, A.J. Peripheral nerve autografts to the rat spinal cord: Studies with axonal tracing methods. Brain Res 237, 147, 1982
46. Hiruma, H., Saito, A., Ichikawa, T., Kiriyama, Y., Hoka, S., Kusakabe, T., et al. Effects of substance P and calcitonin gene-related peptide on axonal transport in isolated and cultured adult mouse dorsal root ganglion neurons. Brain Res 883, 184, 2000
47. Weidner, N., Ner, A., Salimi, N., and Tuszynski, M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci U S A 98, 3513, 2001
48. Zhou, L., Baumgartner, B.J., Hill-Felberg, S.J., McGowen, L.R., and Shine, H.D. Neurotrophin-3 expressed in situ induces axonal plasticity in the adult injured spinal cord. J Neurosci 23, 1424, 2003
49. Smith, K.J., Blakemore, W.F., and McDonald, W.I. Central remyelination restores secure conduction. Nature 280, 395, 1979
50. Blight, A.R., and Young, W. Central axons in injured cat spinal cord recover electrophysiological function following remyelination by Schwann cells. J Neurol Sci 91, 15, 1989
51. Zawadzka, M., Rivers, L.E., Fancy, S.P., Zhao, C., Tripathi, R., Jamen, F., et al. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6, 578, 2010
52. Nave, K.A., and Trapp, B.D. Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31, 535, 2008
53. Weidner, N., Blesch, A., Grill, R.J., and Tuszynski, M.H. Nerve growth factor-hypersecreting Schwann cell grafts augment and guide spinal cord axonal growth and remyelinate central nervous system axons in a phenotypically appropriate manner that correlates with expression of L1. J Comp Neurol 413, 495, 1999
54. Tuszynski, M.H., Weidner, N., McCormack, M., Miller, I., Powell, H., and Conner, J. Grafts of genetically modified Schwann cells to the spinal cord: Survival, axon growth, and myelination. Cell Transplant 7, 187, 1998
55. Cummings, B.J., Uchida, N., Tamaki, S.J., Salazar, D.L., Hooshmand, M., Summers, R., et al. Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci U S A 102, 14069, 2005
56. Keirstead, H.S., Morgan, S.V., Wilby, M.J., and Fawcett, J.W. Enhanced axonal regeneration following combined demyelination plus schwann cell transplantation therapy in the injured adult spinal cord. Exp Neurol 159, 225, 1999
57. Camand, E., Morel, M.P., Faissner, A., Sotelo, C., and Dusart, I. Long-Term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur J Neurosci 20, 1161, 2004
58. Khaing, Z.Z., Milman, B.D., Vanscoy, J.E., Seidlits, S.K., Grill, R.J., and Schmidt, C.E. High molecular weight hyaluronic acid limits astrocyte activation and scar formation after spinal cord injury. J Neural Eng 8, 046033, 2011
59. Asher, R.A., Morgenstern, D.A., Shearer, M.C., Adcock, K.H., Pesheva, P., and Fawcett, J.W. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J Neurosci 22, 2225, 2002
60. Asher, R.A., Morgenstern, D.A., Fidler, P.S., Adcock, K.H., Oohira, A., Braistead, J.E., et al. Neurocan is upregulated in injured brain and in cytokine-Treated astrocytes. J Neurosci 20, 2427, 2000
61. Moon, L.D., Asher, R.A., Rhodes, K.E., and Fawcett, J.W. Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience 109, 101, 2002
62. Tang, X., Davies, J.E., and Davies, S.J. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 71, 427, 2003
63. Stichel, C.C., andMuller,H.W. TheCNS lesion scar: Newvistas on an old regeneration barrier. Cell Tissue Res 294, 1, 1998
64. Houweling, D.A., Lankhorst, A.J., Gispen, W.H., Bar, P.R., and Joosten, E.A. 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, 49, 1998
65. Yoshii, S., Oka, M., Shima, M., Taniguchi, A., Taki, Y., and Akagi, M. Restoration of function after spinal cord transection using a collagen bridge. J Biomed Mater Res A 70, 569, 2004
66. Cheng, H., Huang, Y.C., Chang, P.T., and Huang, Y.Y. Laminin-incorporated nerve conduits made by plasma treatment for repairing spinal cord injury. Biochem Biophys Res Commun 357, 938, 2007
67. King, V.R., Henseler, M., Brown, R.A., and Priestley, J.V. Mats made from fibronectin support oriented growth of axons in the damaged spinal cord of the adult rat. Exp Neurol 182, 383, 2003
68. Phillips, J.B., King, V.R., Ward, Z., Porter, R.A., Priestley, J.V., and Brown, R.A. Fluid shear in viscous fibronectin gels allows aggregation of fibrous materials for CNS tissue engineering. Biomaterials 25, 2769, 2004
69. King, V.R., Phillips, J.B., Hunt-Grubbe, H., Brown, R., and Priestley, J.V. Characterization of non-neuronal elements within fibronectin mats implanted into the damaged adult rat spinal cord. Biomaterials 27, 485, 2005
70. Okada, M., Miyamoto, O., Shibuya, S., Zhang, X., Yamamoto, T., and Itano, T. Expression and role of type I collagen in a rat spinal cord contusion injury model. Neurosci Res 58, 371, 2007
71. Sroga, J.M., Jones, T.B., Kigerl, K.A., McGaughy, V.M., and Popovich, P.G. Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J CompNeurol 462, 223, 2003
72. Bregman, B.S., Kunkel-Bagden, E., Schnell, L., Dai, H.N., Gao, D., and Schwab, M.E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378, 498, 1995