Biomaterials combined with cell therapy for treatment of spinal cord injury

Regenerative Medicine

Volumn 7, Issue 2, 2012, Pages 207-224

  Kubinová, Šárka ^a   Syková, Eva ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

Author keywords

biomaterial; cell therapy; scaffold; spinal cord injury; stem cell; tissue engineering

Indexed keywords

BIOMATERIAL; BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; METHYLPREDNISOLONE; N ACETYLGALACTOSAMINE 4 SULFATASE; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; POLYMER; SCAVENGER; TISSUE SCAFFOLD;

ASTROCYTE; BIOCOMPATIBILITY; CELL ADHESION; CELL GROWTH; CELL MIGRATION; CHRONIC DISEASE; CLINICAL EFFECTIVENESS; CONTROLLED DRUG RELEASE; DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; HUMAN; HYDROGEL; MESENCHYMAL STEM CELL; MICROENCAPSULATION; NERVE CELL DIFFERENTIATION; NERVE FIBER REGENERATION; NEURAL STEM CELL; NONHUMAN; PATIENT SAFETY; PHYSICAL CHEMISTRY; POROSITY; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; THERAPY EFFECT; TISSUE ENGINEERING; TREATMENT PLANNING;

ANIMALS; BIOCOMPATIBLE MATERIALS; DRUG DELIVERY SYSTEMS; HUMANS; POLYMERS; SPINAL CORD INJURIES; TISSUE SCAFFOLDS; TISSUE THERAPY;

EID: 84858252039     PISSN: 17460751     EISSN: 1746076X     Source Type: Journal    
DOI: 10.2217/rme.11.121     Document Type: Review

References (129)

1. Thuret S, Moon LD, Gage FH. Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 7, 628-643 (2006). (Pubitemid 44106745)
2. Hulsebosch CE. Recent advances in pathophysiology and treatment of spinal cord injury. Adv. Physiol. Educ. 26, 238-255 (2002).
3. Silver J, Miller JH. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146-156 (2004). (Pubitemid 38160289)
4. Sandvig A, Berry M, Barrett LB, Butt A, Logan A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 46, 225-251 (2004). (Pubitemid 38679204)
5. Baptiste DC, Fehlings MG. Update on the treatment of spinal cord injury. Prog. Brain Res. 161, 217-233 (2007). (Pubitemid 47017406)
6. Kadoya K, Tsukada S, Lu P et al. Combined intrinsic and extrinsic neuronal mechanisms facilitate bridging axonal regeneration one year after spinal cord injury. Neuron 64, 165-172 (2009).
7. Sykova E, Homola A, Mazanec R et al. Autologous bone marrow transplantation in patients with subacute and chronic spinal cord injury. Cell Transplant. 15, 675-687 (2006). (Pubitemid 46095251)
8. Willerth SM, Sakiyama-Elbert SE. Cell therapy for spinal cord regeneration. Adv. Drug Deliv. Rev. 60, 263-276 (2008). (Pubitemid 350236403)
9. Harkema S, Gerasimenko Y, Hodes J et al. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 377, 1938-1947 (2011).
10. Rossi SL, Keirstead HS. Stem cells and spinal cord regeneration. Curr. Opin. Biotechnol. 20, 552-562 (2009).
11. Urdzikova L, Jendelova P, Glogarova K, Burian M, Hajek M, Sykova E. Transplantation of bone marrow stem cells as well as mobilization by granulocyte-colony stimulating factor promotes recovery after spinal cord injury in rats. J. Neurotrauma 23, 1379-1391 (2006). (Pubitemid 46489623)
12. Sykova E, Jendelova P. Magnetic resonance tracking of transplanted stem cells in rat brain and spinal cord. Neurodegener. Dis. 3, 62-67 (2006). (Pubitemid 43760370)
13. Tetzlaff W, Okon EB, Karimi-Abdolrezaee S et al. A systematic review of cellular transplantation therapies for spinal cord injury. J. Neurotrauma 28, 1611-1682 (2011).
14. Xu XM, Onifer SM. Transplantation-mediated strategies to promote axonal regeneration following spinal cord injury. Respir. Physiol. Neurobiol. 169, 171-182 (2009).
15. Coutts M, Keirstead HS. Stem cells for the treatment of spinal cord injury. Exp. Neurol. 209, 368-377 (2008). (Pubitemid 351181429)
16. Amemori T, Jendelova P, Ruzickova K, Arboleda D, Sykova E. Co-transplantation of olfactory ensheathing glia and mesenchymal stromal cells does not have synergistic effects after spinal cord injury in the rat. Cytotherapy 12, 212-225 (2010).
17. Straley KS, Foo CW, Heilshorn SC. Biomaterial design strategies for the treatment of spinal cord injuries. J. Neurotrauma 27, 1-19 (2010).
18. Chan G, Mooney DJ. New materials for tissue engineering: towards greater control over the biological response. Trends Biotechnol. 26, 382-392 (2008).
19. Wang M, Zhai P, Chen X, Schreyer DJ, Sun X, Cui F. Bioengineered scaffolds for spinal cord repair. Tissue Eng. Part B Rev. 17, 177-194 (2011).
20. Fournier E, Passirani C, Montero-Menei CN, Benoit JP. Biocompatibility of implantable synthetic polymeric drug carriers: focus on brain biocompatibility. Biomaterials 24, 3311-3331 (2003). (Pubitemid 36577679)
21. Jones KS. Effects of biomaterial-induced inflammation on fibrosis and rejection. Semin. Immunol. 20, 130-136 (2008).
22. Gal P, Kravcukova P, Mokry M, Kluchova D. Chemokines as possible targets in modulation of the secondary damage after acute spinal cord injury: a review. Cell. Mol. Neurobiol. 29, 1025-1035 (2009).
23. Chen BK, Knight AM, Madigan NN et al. Comparison of polymer scaffolds in rat spinal cord: a step toward quantitative assessment of combinatorial approaches to spinal cord repair. Biomaterials 32, 8077-8086 (2011).
24. Kubinova S, Horak D, Hejcl A, Plichta Z, Kotek J, Sykova E. Highly superporous cholesterol-modified poly(2-hydroxyethyl methacrylate) scaffolds for spinal cord injury repair. J. Biomed. Mater. Res. A 99, 618-629 (2011).
25. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006). (Pubitemid 44233625)
26. Leach JB, Brown XQ, Jacot JG, Dimilla PA, Wong JY. Neurite outgrowth and branching of PC12 cells on very soft substrates sharply decreases below a threshold of substrate rigidity. J. Neural Eng. 4, 26-34 (2007). (Pubitemid 46603794)
27. Bakshi A, Fisher O, Dagci T, Himes BT, Fischer I, Lowman A. Mechanically engineered hydrogel scaffolds for axonal growth and angiogenesis after transplantation in spinal cord injury. J. Neurosurg. Spine 1, 322-329 (2004).
28. Gopferich A. Mechanisms of polymer degradation and erosion. Biomaterials 17, 103-114 (1996). (Pubitemid 26031366)
29. Tysseling-Mattiace VM, Sahni V, Niece KL et al. Self-assembling nanofibers inhibit glial scar formation and promote axon elongation after spinal cord injury. J. Neurosci. 28, 3814-3823 (2008).
30. Oudega M, Gautier SE, Chapon P et al. Axonal regeneration into Schwann cell grafts within resorbable poly(alpha-hydroxyacid) guidance channels in the adult rat spinal cord. Biomaterials 22, 1125-1136 (2001). (Pubitemid 32229937)
31. Teng YD, Lavik EB, Qu X et al. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc. Natl Acad. Sci. USA 99, 3024-3029 (2002). (Pubitemid 34240579)
32. Maquet V, Martin D, Scholtes F 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, 1137-1146 (2001). (Pubitemid 32229938)
33. Moore MJ, Friedman JA, Lewellyn EB et al. Multiple-channel scaffolds to promote spinal cord axon regeneration. Biomaterials 27, 419-429 (2006). (Pubitemid 41457245)
34. Itosaka H, Kuroda S, Shichinohe H et al. Fibrin matrix provides a suitable scaffold for bone marrow stromal cells transplanted into injured spinal cord: a novel material for CNS tissue engineering. Neuropathology 29, 248-257 (2009).
35. Huang J, Hu X, Lu L, Ye Z, Zhang Q, Luo Z. Electrical regulation of Schwann cells using conductive polypyrrole/chitosan polymers. J. Biomed. Mater. Res. A 93, 164-174 (2010).
36. Kubinova S, Sykova E. Nanotechnology for treatment of stroke and spinal cord injury. Nanomedicine 5, 99-108 (2010).
37. Nomura H, Tator CH, Shoichet MS. Bioengineered strategies for spinal cord repair. J. Neurotrauma 23, 496-507 (2006). (Pubitemid 43726324)
38. Nisbet DR, Crompton KE, Horne MK, Finkelstein DI, Forsythe JS. Neural tissue engineering of the CNS using hydrogels. J. Biomed. Mater. Res. B 87, 251-263 (2008).
39. Madigan NN, McMahon S, OBrien T, Yaszemski MJ, Windebank AJ. Current tissue engineering and novel therapeutic approaches to axonal regeneration following spinal cord injury using polymer scaffolds. Respir. Physiol. Neurobiol. 169, 183-199 (2009).
40. Cheung H-Y, Lau K-T, Lu T-P, Hui D. A critical review on polymer-based bio-engineered materials for scaffold development. Composites Part B Eng. 38, 291-300 (2007). (Pubitemid 46149453)
41. Tsai EC, Dalton PD, Shoichet MS, Tator CH. Synthetic hydrogel guidance channels facilitate regeneration of adult rat brainstem motor axons after complete spinal cord transection. J. Neurotrauma 21, 789-804 (2004). (Pubitemid 38880249)
42. Hejcl A, Lesny P, Pradny M et al. Biocompatible hydrogels in spinal cord injury repair. Physiol. Res. 57(Suppl. 3), S121-S132 (2008).
43. Woerly S, Fort S, Pignot-Paintrand I, Cottet C, Carcenac C, Savasta M. Development of a sialic acid-containing hydrogel of poly[N-(2- hydroxypropyl) methacrylamide]: characterization and implantation study. Biomacromolecules 9, 2329-2337 (2008).
44. Xu XM, Guenard V, Kleitman N, Bunge MB. Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J. Comp. Neurol. 351, 145-160 (1995).
45. Hejcl A, Sedy J, Kapcalova M et al. HPMA-RGD hydrogels seeded with mesenchymal stem cells improve functional outcome in chronic spinal cord injury. Stem Cells Dev. 19, 1535-1546 (2010).
46. Woerly S, Pinet E, de Robertis L, Van Diep D, Bousmina M. Spinal cord repair with PHPMA hydrogel containing RGD peptides (NeuroGel). Biomaterials 22, 1095-1111 (2001). (Pubitemid 32229935)
47. Silva NA, Salgado AJ, Sousa RA et al. Development and characterization of a novel hybrid tissue engineering-based scaffold for spinal cord injury repair. Tissue Eng. Part A 16, 45-54 (2010).
48. Tsai EC, Dalton PD, Shoichet MS, Tator CH. Matrix inclusion within synthetic hydrogel guidance channels improves specific supraspinal and local axonal regeneration after complete spinal cord transection. Biomaterials 27, 519-533 (2006). (Pubitemid 41457254)
49. Yua L, Deana K, Lib L. Polymer blends and composites from renewable resources. Prog. Polym. Sci. 31, 576-602 (2006).
50. Schlosshauer B, Dreesmann L, Schaller HE, Sinis N. Synthetic nerve guide implants in humans: a comprehensive survey. Neurosurgery 59, 740-747; discussion 7-8 (2006). (Pubitemid 44579574)
51. Mollers S, Heschel I, Damink LH et al. Cytocompatibility of a novel, longitudinally microstructured collagen scaffold intended for nerve tissue repair. Tissue Eng. Part A 15, 461-472 (2009).
52. Prang P, Muller R, Eljaouhari A et al. The promotion of oriented axonal regrowth in the injured spinal cord by alginate-based anisotropic capillary hydrogels. Biomaterials 27, 3560-3569 (2006).
53. Stokols S, Tuszynski MH. Freeze-dried agarose scaffolds with uniaxial channels stimulate and guide linear axonal growth following spinal cord injury. Biomaterials 27, 443-451 (2006). (Pubitemid 41457247)
54. Hurtado A, Moon LD, Maquet V, Blits B, Jerome R, 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, 430-442 (2006). (Pubitemid 41457246)
55. Xu XM, Guenard V, Kleitman N, Aebischer P, Bunge MB. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 134, 261-272 (1995).
56. Bamber NI, Li H, Lu X, Oudega M, Aebischer P, Xu XM. 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, 257-268 (2001). (Pubitemid 32142470)
57. Krych AJ, Rooney GE, Chen B et al. Relationship between scaffold channel diameter and number of regenerating axons in the transected rat spinal cord. Acta Biomater. 5, 2551-2559 (2009).
58. Wong DY, Leveque JC, Brumblay H, Krebsbach PH, Hollister SJ, Lamarca F. Macro-architectures in spinal cord scaffold implants influence regeneration. J. Neurotrauma 25, 1027-1037 (2008).
59. Jimenez Hamann MC, Tator CH, Shoichet MS. Injectable intrathecal delivery system for localized administration of EGF and FGF-2 to the injured rat spinal cord. Exp. Neurol. 194, 106-119 (2005). (Pubitemid 40719747)
60. Jain A, Kim YT, McKeon RJ, Bellamkonda RV. In situ gelling hydrogels for conformal repair of spinal cord defects, and local delivery of BDNF after spinal cord injury. Biomaterials 27, 497-504 (2006). (Pubitemid 41457252)
61. Piantino J, Burdick JA, Goldberg D, Langer R, Benowitz LI. An injectable, biodegradable hydrogel for trophic factor delivery enhances axonal rewiring and improves performance after spinal cord injury. Exp. Neurol. 201, 359-367 (2006). (Pubitemid 44344229)
62. Guo J, Su H, Zeng Y et al. Reknitting the injured spinal cord by self-assembling peptide nanofiber scaffold. Nanomedicine 3, 311-321 (2007). (Pubitemid 350199643)
63. Tysseling VM, Sahni V, Pashuck ET et al. Self-assembling peptide amphiphile promotes plasticity of serotonergic fibers following spinal cord injury. J. Neurosci. Res. 88, 3161-3170 (2010).
64. Cigognini D, Satta A, Colleoni B et al. Evaluation of early and late effects into the acute spinal cord injury of an injectable functionalized self-assembling scaffold. PLoS One 6, E19782 (2011).
65. Kubinova S, Sykova E. Nanotechnologies in regenerative medicine. Minim. Invasive Ther. Allied Technol. 19, 144-156 (2010).
66. Cao H, Liu T, Chew SY. The application of nanofibrous scaffolds in neural tissue engineering. Adv. Drug Deliv. Rev. 61, 1055-1064 (2009).
67. Gelain F, Panseri S, Antonini S et al. Transplantation of nanostructured composite scaffolds results in the regeneration of chronically injured spinal cords. ACS Nano 5, 227-236 (2011).
68. Xie J, MacEwan MR, Schwartz AG, Xia Y. Electrospun nanofibers for neural tissue engineering. Nanoscale 2, 35-44 (2010).
69. Hurtado A, Cregg JM, Wang HB et al. Robust CNS regeneration after complete spinal cord transection using aligned poly-l-lactic acid microfibers. Biomaterials 32, 6068-6079 (2011).
70. Huveneers S, Danen EH. Adhesion signaling - crosstalk between integrins, Src and Rho. J. Cell Sci. 122, 1059-1069 (2009).
71. Kubinova S, Horak D, Sykova E. Cholesterol-modified superporous poly(2- hydroxyethyl methacrylate) scaffolds for tissue engineering. Biomaterials 30, 4601-4609 (2009).
72. Kubinova S, Horak D, Kozubenko N et al. The use of superporous Ac-CGGASIKVAVS-OH-modified PHEMA scaffolds to promote cell adhesion and the differentiation of human fetal neural precursors. Biomaterials 31, 5966-5975 (2010).
73. Gunn JW, Turner SD, Mann BK. Adhesive and mechanical properties of hydrogels influence neurite extension. J. Biomed. Mater. Res. A 72, 91-97 (2005). (Pubitemid 39628337)
74. Nguyen EH, Schwartz MP, Murphy WL. Biomimetic approaches to control soluble concentration gradients in biomaterials. Macromol. Biosci. 11, 483-492 (2011).
75. Adams DN, Kao EY, Hypolite CL, Distefano MD, Hu WS, Letourneau PC. Growth cones turn and migrate up an immobilized gradient of the laminin IKVAV peptide. J. Neurobiol. 62, 134-147 (2005). (Pubitemid 39636384)
76. Musoke-Zawedde P, Shoichet MS. Anisotropic three-dimensional peptide channels guide neurite outgrowth within a biodegradable hydrogel matrix. Biomed. Mater. 1, 162-169 (2006). (Pubitemid 44529342)
77. Dodla MC, Bellamkonda RV. Differences between the effect of anisotropic and isotropic laminin and nerve growth factor presenting scaffolds on nerve regeneration across long peripheral nerve gaps. Biomaterials 29, 33-46 (2008). (Pubitemid 47599652)
78. Wei YT, He Y, Xu CL et al. Hyaluronic acid hydrogel modified with Nogo-66 receptor antibody and poly-l-lysine to promote axon regrowth after spinal cord injury. J. Biomed. Mater. Res. B 95, 110-117 (2010).
79. Bunge MB. Novel combination strategies to repair the injured mammalian spinal cord. J. Spinal Cord Med. 31, 262-269 (2008).
80. Nomura H, Baladie B, Katayama Y, Morshead CM, Shoichet MS, Tator CH. Delayed implantation of intramedullary chitosan channels containing nerve grafts promotes extensive axonal regeneration after spinal cord injury. Neurosurgery 63, 127-141; discussion 41-43 (2008).
81. Hejcl A, Urdzikova L, Sedy J et al. Acute and delayed implantation of positively charged 2-hydroxyethyl methacrylate scaffolds in spinal cord injury in the rat. J. Neurosurg. Spine 8, 67-73 (2008).
82. Okada S, Ishii K, Yamane J et al. In vivo imaging of engrafted neural stem cells: its application in evaluating the optimal timing of transplantation for spinal cord injury. FASEB J. 19, 1839-1841 (2005). (Pubitemid 41598768)
83. Hill CE, Moon LD, Wood PM, Bunge MB. Labeled Schwann cell transplantation: cell loss, host Schwann cell replacement, and strategies to enhance survival. Glia 53, 338-343 (2006). (Pubitemid 43221355)
84. Iannotti C, Li H, Yan P, Lu X, Wirthlin L, Xu XM. Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp. Neurol. 183, 379-393 (2003). (Pubitemid 37205080)
85. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead CM, Fehlings MG. Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J. Neurosci. 26, 3377-3389 (2006).
86. Nandoe Tewarie RD, Hurtado A, Ritfeld GJ et al. Bone marrow stromal cells elicit tissue sparing after acute but not delayed transplantation into the contused adult rat thoracic spinal cord. J. Neurotrauma 26, 2313-2322 (2009).
87. Oudega M, Xu XM. Schwann cell transplantation for repair of the adult spinal cord. J. Neurotrauma 23, 453-467 (2006). (Pubitemid 43726321)
88. Aghayan HR, Arjmand B, Norouzi-Javidan A et al. Clinical grade cultivation of human Schwann cell, by the using of human autologous serum instead of fetal bovine serum and without growth factors. Cell Tissue Bank. (2011) (In press).
89. Ramer MS, Priestley JV, McMahon SB. Functional regeneration of sensory axons into the adult spinal cord. Nature 403, 312-316 (2000). (Pubitemid 30062387)
90. Fortun J, Hill CE, Bunge MB. Combinatorial strategies with Schwann cell transplantation to improve repair of the injured spinal cord. Neurosci. Lett. 456, 124-132 (2009).
91. Chen A, Xu XM, Kleitman N, Bunge MB. Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp. Neurol. 138, 261-276 (1996). (Pubitemid 26132713)
92. Xu XM, Chen A, Guenard V, Kleitman N, Bunge MB. Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J. Neurocytol. 26, 1-16 (1997). (Pubitemid 27186757)
93. Novikova LN, Pettersson J, Brohlin M, Wiberg M, Novikov LN. Biodegradable poly-beta-hydroxybutyrate scaffold seeded with Schwann cells to promote spinal cord repair. Biomaterials 29, 1198-1206 (2008).
94. Olson HE, Rooney GE, Gross L et al. Neural stem cell- and Schwann cell-loaded biodegradable polymer scaffolds support axonal regeneration in the transected spinal cord. Tissue Eng. Part A 15, 1797-1805 (2009).
95. Chen BK, Knight AM, de Ruiter GC et al. Axon regeneration through scaffold into distal spinal cord after transection. J. Neurotrauma 26, 1759-1771 (2009).
96. Afshari FT, Kwok JC, Fawcett JW. Astrocyte-produced ephrins inhibit schwann cell migration via VAV2 signaling. J. Neurosci. 30, 4246-4255 (2010).
97. Chau CH, Shum DK, Li H et al. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. FASEB J. 18, 194-196 (2004).
98. Bradbury EJ, Carter LM. Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Res. Bull. 84, 306-316 (2011).
99. Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW. Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J. Neurosci. 31, 9332-9344 (2011).
100. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, Pearse DD. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J. Neurosci. 25, 1169-1178 (2005). (Pubitemid 40268958)
101. Vavrek R, Pearse DD, Fouad K. Neuronal populations capable of regeneration following a combined treatment in rats with spinal cord transection. J. Neurotrauma 24, 1667-1673 (2007). (Pubitemid 350035836)
102. Gros T, Sakamoto JS, Blesch A, Havton LA, Tuszynski MH. Regeneration of long-tract axons through sites of spinal cord injury using templated agarose scaffolds. Biomaterials 31, 6719-6729 (2010).
103. Uccelli A, Benvenuto F, Laroni A, Giunti D. Neuroprotective features of mesenchymal stem cells. Best Pract. Res. Clin. Haematol. 24, 59-64 (2011).
104. Wright KT, Masri WE, Osman A, Chowdhury J, Johnson WE. Concise review: bone marrow for the treatment of spinal cord injury: mechanisms and clinical applications. Stem Cells 29, 169-178 (2011).
105. Zeng X, Zeng YS, Ma YH et al. Bone marrow mesenchymal stem cells in a three dimensional gelatin sponge scaffold attenuate inflammation, promote angiogenesis and reduce cavity formation in experimental spinal cord injury. Cell Transplant. (2011) (In press).
106. Kang KN, Lee JY, Kim da Y et al. Regeneration of completely transected spinal cord using scaffold of poly(d,l-lactide-co-glycolide)/small intestinal submucosa seeded with rat bone marrow stem cells. Tissue Eng. Part A 17, 2143-2152 (2011).
107. Martino G, Pluchino S. The therapeutic potential of neural stem cells. Nat. Rev. Neurosci. 7, 395-406 (2006).
108. Parr AM, Kulbatski I, Zahir T et al. Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155, 760-770 (2008).
109. Romanyuk N, Amemori T, Turnovcova K et al. Using human fetal neural stem cells or human induced pluripotent stem cell-derived neural precursors for the treatment of experimental spinal cord injury. Presented at: 8th IBRO World Congress of Neuroscience. Florence, Italy, 14-18 July 2011.
110. Nomura H, Zahir T, Kim H et al. Extramedullary chitosan channels promote survival of transplanted neural stem and progenitor cells and create a tissue bridge after complete spinal cord transection. Tissue Eng. Part A 14, 649-665 (2008). (Pubitemid 351684737)
111. Yu D, Neeley WL, Pritchard CD et al. Blockade of peroxynitrite-induced neural stem cell death in the acutely injured spinal cord by drug-releasing polymer. Stem Cells 27, 1212-1222 (2009).
112. Kozubenko N, Hejcl A, Hrubý M et al. Treating spinal cord injury with a combination of human fetal neural stem cells and hydroxyethyl methacrylate hydrogels modified with serotonin agonists. Presented at: 7th FENS Forum of European Neuroscience. Amsterdam, The Netherlands, 3-7 July 2010.
113. Hwang DH, Kim HM, Kang YM et al. Combination of multifaceted strategies to maximize the therapeutic benefits of neural stem cell transplantation for spinal cord repair. Cell Transplant. 20, 1361-1379 (2011).
114. Enzmann GU, Benton RL, Woock JP, Howard RM, Tsoulfas P, Whittemore SR. Consequences of noggin expression by neural stem, glial, and neuronal precursor cells engrafted into the injured spinal cord. Exp. Neurol. 195, 293-304 (2005). (Pubitemid 41297782)
115. Cloutier F, Siegenthaler MM, Nistor G, Keirstead HS. Transplantation of human embryonic stem cell-derived oligodendrocyte progenitors into rat spinal cord injuries does not cause harm. Regen. Med. 1, 469-479 (2006).
116. Kozubenko N, Turnovcova K, Kapcalova M et al. Analysis of in vitro and in vivo characteristics of human embryonic stem cell-derived neural precursors. Cell Transplant. 19, 471-486 (2010).
117. Keirstead HS, Nistor G, Bernal G et al. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J. Neurosci. 25, 4694-4705 (2005). (Pubitemid 40664118)
118. Johnson PJ, Tatara A, Shiu A, Sakiyama-Elbert SE. Controlled release of neurotrophin-3 and platelet-derived growth factor from fibrin scaffolds containing neural progenitor cells enhances survival and differentiation into neurons in a subacute model of SCI. Cell Transplant. 19, 89-101 (2010).
119. Hatami M, Mehrjardi NZ, Kiani S et al. Human embryonic stem cell-derived neural precursor transplants in collagen scaffolds promote recovery in injured rat spinal cord. Cytotherapy 11, 618-630 (2009).
120. Joosten EA, Veldhuis WB, Hamers FP. Collagen containing neonatal astrocytes stimulates regrowth of injured fibers and promotes modest locomotor recovery after spinal cord injury. J. Neurosci. Res. 77, 127-142 (2004). (Pubitemid 38850063)
121. Willerth SM, Sakiyama-Elbert SE. Approaches to neural tissue engineering using scaffolds for drug delivery. Adv. Drug Deliv. Rev. 59, 325-338 (2007). (Pubitemid 46879972)
122. Lee H, McKeon RJ, Bellamkonda RV. Sustained delivery of thermostabilized chABC enhances axonal sprouting and functional recovery after spinal cord injury. Proc. Natl Acad. Sci. USA 107, 3340-3345.
123. Katz JS, Burdick JA. Hydrogel mediated delivery of trophic factors for neural repair. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 1, 128-139 (2009).
124. Xu XM, Zhang SX, Li H, Aebischer P, Bunge MB. 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, 1723-1740 (1999). (Pubitemid 29192248)
125. Hsu JY, Xu XM. Early profiles of axonal growth and astroglial response after spinal cord hemisection and implantation of Schwann cell-seeded guidance channels in adult rats. J. Neurosci. Res. 82, 472-483 (2005).
126. Chen G, Hu YR, Wan H et al. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells and Schwann cells. Chin. Med. J. (Engl.) 123, 2424-2431 (2010).
127. Sykova E, Jendelova P. Magnetic resonance tracking of implanted adult and embryonic stem cells in injured brain and spinal cord. Ann. NY Acad. Sci. 1049, 146-160 (2005). (Pubitemid 40967582)
128. Kang KN, Lee JY, Kim DY et al. Regeneration of completely transected spinal cord using scaffold of poly(d,l-lactide-co-glycolide)/small intestinal submucosa seeded with rat bone marrow stem cells. Tissue Eng. Part A 17, 2143-2152 (2011).
129. Min SH, Lee SH, Shim H et al. Development of complete thoracic spinal cord transection model in rats for delayed transplantation of stem cells. Spine 36, E155-E163 (2011).