Cell therapy for spinal cord repair: Optimization of biologic scaffolds for survival and neural differentiation of human bone marrow stromal cells

Cytotherapy

Volumn 12, Issue 4, 2010, Pages 522-537

  Zurita, Mercedes ^a   Otero, Laura ^a   Aguayo, Concepción ^a   Bonilla, Celia ^a   Ferreira, Edgar ^a   Parajón, Avelino ^a   Vaquero, Jesús ^a  

^a HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

Author keywords

Bone marrow stromal cells; Cell therapy; Central nervous system repair; Spinal cord injury

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHLORIDE; FIBRIN; FIBRINOGEN; NERVE GROWTH FACTOR; RETINOIC ACID; THROMBIN;

APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL THERAPY; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; SPINAL CORD INJURY;

EID: 77954454266     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.3109/14653241003615164     Document Type: Article

References (72)

1. Gospodarowicz D . , Tauber JP. Growth factors and the extracellular matrix. Endocr Rev. 1980;1:201-227
2. Engbring JA, Kleinman HK. The basement membrane matrix in malignancy. J Pathol. 2003;200:465-470
3. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer. 2001;1:46-54.
4. Gilmore AP. Anoikis. Cell Death Differ. 2005;12(Suppl 2): 1473-1477
5. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol. 1994;124:619-626
6. Valentinis B, Morrione A, Peruzzi F, Prisco M, Reiss K, Baserga R. Anti-apoptotic signaling of the IGF-1 receptor in fibloblasts following loss of matrix adhesion. Oncogene. 1999;18:1827-1836
7. Sakai H, Kobayashi E, Sakai E, Shibata M, Kato Y. Cell adhesion is a prerequisite for osteoclast survival. Biochem Biophys Res Commun. 2000;270:550-556
8. Marchionini DM, Collier TJ, Camargo M, McGuire S, Pitzer M, Sortwell CE. Interference with anoikis induced cell death of dopamine neurons: implications for augmenting embryonic graft survival in a rat model of Parkinson's disease. J Comp Neurol. 2003;464:172-179
9. Koda M, Someya Y, Nishio Y, Kadota R, Mannoji C, Miyashita T, et al. Brain-derived neurotrophic factor suppresses anoikis induced death of Schwann cells. Neurosci Lett. 2008;444:143-147
10. Robey TE, Saiget MK, Reinecke H, Murry CE. Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol. 2008;45:567-581
11. Vaquero J, Zurita M. Bone marrow stromal cells for spinal cord repair: a challenge for contemporary neurobiology. Histol Histopathol. 2009;24:107-116
12. Okada S, Ishii K, Yamane J, Iwanami A, Ikegami T, Katoh H, et al. In vivo imaging of transplantation for spinal cord injury. FASEB J. 2005;19:1839-1841
13. Levenberg S, Burdick JA, Kraehenbuchl T, Langer R. Neurotrophin-induced differentiation of human embryonic stem cells on three-dimensional polymeric scaffold. Tissue Eng. 2005;11:506-512
14. Harrinson J, Pattanawong S, Forsythe JS, Gross KA, Nisbet DR, Beh H et al. Colonization and maintenance of murine embryonic stem cells on poly(alpha-hydroxy esters). Biomaterials. 2004;25:4963-4970
15. Ma W, Fitzgerald W, Liu QY, O'Shaughnessy TJ, Maric D, Lin HJ, et al. CNS stem and progenitor cell differentiation into functional neuronal circuits in three-dimensional collagen gels. Exp Neurol. 2004;190:276-288
16. Jost M, Huggett TM, Kari C, Rodeck U. Matrix-independent survival of human keratinocytes through an EGF receptor/ MAPK-kinase-dependent pathway. Mol Biol Cell. 2001;12: 1519-1527
17. Silva GA, Czeisler C, Niece KL, Beniash E, Harrington DA, Kessler JA, et al. Selective differentiation of neural progenitor cells by high epitope density nanofibers. Science. 2004;303: 1352-1355
18. Liu S, Said G, Tadie M. Regrowth of the rostral spinal axons into the caudal ventral roots through a collagen tube implanted into hemisected adult rat spinal cord. Neurosurgery. 2001;49: 143-150
19. Goldsmith HS, Fonseca A Jr, Porter J. Spinal cord separation: MRI evidence of healing after omentum-collagen reconstruction. Neurol Res. 2005;27:115-123
20. Kataoka K, Suzuki Y, Kitada M, Ohnishi K, Suzuki K, Tanihara M, et al. Alginate, a bioresorbable material derived from brown seaweed, enhances elongation of amputated axons of spinal cord in infant rats. J Biomed Mater Res. 2001;54:373-384
21. Suzuki Y, Kitaura M, Wu S, Kataoka K, Suzuki K, Endo K, et al. Electrophysiological and horseradish peroxidise-tracing studies of nerve regeneration through alginate-filled gap in adult rat spinal cord. Neurosci Lett. 2002;318:121-124
22. Blacher S, Maquet V, Schils F, Martin D, Schoenen J, Moonen G, et al. Image analysis of the axonal ingrowth into poly(D,L-lactide) porous scaffolds in relation to the 3D porous structure. Biomaterials. 2003;24:1033-1040
23. Patist CM, Mulder MB, Gautier SE, Maquet V, Jerome R, 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. 2004;25:1569-1582
24. 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. 2004;1:322-329
25. Shi R, Borgens RB, Blight AR. Functional reconnection of severed mammalian spinal cord axons with polyethylene glycol. J Neurotrauma. 1999;16:727-738
26. Novikova LN, Mosahebi A, Wiberg M, Terenghi G, Kellerth JO, Novikov LN. Alginate hydrogel and matrigel as potential cell carriers for neurotransplantation. J Biomed Mater Res A. 2006;77:242-252
27. Xiao M, Klueber KM, Lu C, Guo Z, Marshall CT, Wang H, et al. Human adult olfactory neural progenitors rescue axotomized rodent rubrospinal neurons and promote functional recovery. Exp Neurol. 2005;194:12-30.
28. Facchiano F, Fernandez E, Mancarella S, Maira G, Miscusi M, D'Arcangelo D, et al. Promotion of regeneration of corticospinal tract axons in rats with recombinant vascular endothelial growth factor alone and combined with adenovirus coding for this factor. J Neurosurg. 2002; 97:161-168
29. Ahmed Z, Underwood S, Brown RA. Nerve guide material made from fibronectin: assessment of in vitro properties. Tissue Eng. 2003;9:219-231
30. Christman KL, Vardanian AJ, Fang Q, Sievers RE, Fok HH, Lee RJ. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion and induces neovasculature formation in ischemic myocardium. J Am Coll Cardiol. 2004;44:654-660
31. Laurens N, Koolwijk P, De Maat MP. Fibrin structure and wound healing. J Thromb Haemost. 2006;4:932-939
32. Falanga V, Iwamoto S, Chartier M, Yufit T, Butmarc J, Kouttab N, et al. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng. 2007;13:1299-1312.
33. Taylor SJ, McDonald JW 3rd, Sakiyama-Elbert SE. Controlled release of neurotrophin-3 from fibrin gels for spinal cord injury. J Control Release. 2004;98:281-294
34. Gille J, Meisner U, Ehlers EM, Müller A, Russlies M, Behrens P. Migration pattern, morphology and viability of cells suspended in or sealed with fibrin blue: A histomorphologic study. Tissue Cell. 2005;37:339-348
35. Le Guéhennec L, Layrolle P, Daculsi G. A review of bioceramics and fibrin sealant. Eur Cell Mater. 2004;8:1-10.
36. Matras H. [Effect of various fibrin preparations on reimplantations in the rat skin.] Osterr Z Stomatol. 1970;67:338-359
37. Wakitani S, Kimura T, Hirooka A. Repair of rabbit articular surfaces with allograft chondrocytes embedded in collagen gel. J Bone Joint Surg Br. 1989;71:74-80.
38. Boo JS, Yamada Y, Okazaki Y, Okada K, Hata K, Yoshikawa T, et al. Tissue engineered bone using mesenchymal stem cells and a biodegradable scaffold. J Craniofac Surg. 2002;13: 231-239
39. Weilbrich G, Kleis WK, Buch R, Hitzler WE, Hafner G. The Harvest smart PrePTM system versus the Friadent-Schütze platelet-rich plasma kit. Clin Oral Implants Res. 2003;14:233-239
40. Eby BW. Platelet-rich plasma: harvesting with a single-spin centrifuge. J Oral Implantol. 2002;28:297-301.
41. Anitua E, Andia I, Ardanza B, Nurden P, Nurden AT. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb Haemost. 2004;91:4-15. (Pubitemid 38111215)
42. Harrison P, Cramer EM. Platelet granules. Blood Rev. 1993;7:52-62.
43. Van den Dolder J, Mooren R, Vloon AP, Stoelinga PJ, Jansen JA. Platelet-rich plasma: quantification of growth factor levels and the effect on growth and differentiation of rat bone marrow cells. Tissue Eng. 2006;12:3067-3073
44. Zurita M, Vaquero J, Bonilla C, Santos M, De Haro J, Oya S, et al. Functional recovery of chronic paraplegic pigs after autologous transplantation of bone marrow stromal cells. Transplantation. 2008;86:845-853
45. Willerth SM, Arendas KJ, Gottlieb DI, Sakiyama-Elbert SE. Optimization of fibrin scaffolds for differentiation of murine embryonic stem cells into neural lineage cells. Biomaterials. 2006;27:5990-6003.
46. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, et al. Cardoimyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol. 2007;25: 1015-1024
47. Yamada Y, Boo JS, Ozawa R, Nagasaka T, Okazaki Y, Hata K, et al. Bone regeneration following injection of mesenchymal stem cells and fibrin glue with a biodegradable scaffold. J Craniomaxillofac Surg. 2003;31:27-33.
48. Geffner LF, Santacruz P, Izurieta M, Flor L, Maldonado B, Auad AH, et al. Administration of autologous bone marrow stem cells into spinal cord injury patients via multiple routes is safe and improves their quality of life: comprehensive case studies. Cell Transplant. 2008;17:1277-1293
49. Samadikuchaksaraei A. An overview of tissue engineering approaches for management of spinal cord injury. J Neuroeng Rehabil. 2007;4:1-16.
50. Sakiyama-Elbert SE, Panitch A, Hubbell JA. Development of growth factor fusion proteins for cell-triggered drug delivery. FASEB J. 2001;15:1300-1302
51. Ruszymah BH. Autologous human fibrin as the biomaterial for tissue engineering. Med J Malaysia. 2004;59(Suppl B): 30-31
52. Schmoekel HG, Weber FE, Schense JC, Grätz KW, Schawalder P, Hubbell JA. Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol Bioeng. 2005;89:253-262
53. Herbert CB, Bittner GD, Hubbell JA. Effects of fibrinolysis on neurite growth from dorsal root ganglia cultured in two-and three dimensional fibrin gels. J Comp Neurol. 1996;365:380-391
54. Cox S, Cole M, Tawil B. Behavior of human dermal fibroblasts in three dimensional fibrin clots: dependence on fibrinogen and thrombin concentration. Tissue Eng. 2004; 10:942-954
55. Bensaid W, Triffitt JT, Blanchat C, Oudina K, Sedel L, Petite H. A biodegradable fibrin scaffold for mesen chymal stem cells transplantation. Biomaterials. 2003;24:2497-2502
56. Wolberg AS. Thrombin generation and fibrin clot structure. Blood Rev. 2007;21:131-142
57. Cervelli V, Gentile P, Scioli MG, Grimaldi M, Casciani CU, Spagnoli LG, Orlandi A. Application of platelet-rich plasma in plastic surgery: clinical and in vitro evaluation. Tissue Eng Part C Methods. 2009;15:625-634
58. Sunitha RV, Muniratham EN. Platelet-rich fibrin: evolution of a second-generation platelet concentrate. Indian J Dent Res. 2008;19:42-46
59. Marx RE, Carlson ER, Eichstaedt RM, Schimmele SR, Strauss JE, Georgeff KR. Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surg Oral Med O. 1998; 85:638-646
60. Lu HH, Vo JM, Chin HS, Lin J, Cozin M, Tsay R, et al. Controlled delivery of platelet-rich plasma derived growth factors for bone formation. J Biomed Mater Res A. 2008; 86:1128-1136
61. Lucarelli E, Beccheroni A, Donati D, Sangiorgi L, Cennachi A, Del Vento AM, et al. Platelet-derived growth factors enhance proliferation of human stromal stem cells. Biomaterials. 2003;24:3095-3100
62. G arg AK. The use of platelet-rich plasma to enhance the success of bone grafts around dental implants. Dental Implantol Update. 2000;11:17-21.
63. Yamada Y, Ueda M, Naiki T, Takahashi M, Hata K, Nagasaka T. Autogenous injectable bone for regeneration with mesenchymal stem cells and platelet-rich plasma: tissue engineered bone regeneration. Tissue Eng. 2004;10: 955-964
64. Zurita M, Vaquero J, Oya S, Miguel M. Schwann cells induce neuronal differentiation of bone marrow stromal cells. Neuroreport. 2005;16:505-508 (Pubitemid 40477557)
65. Zurita M, Vaquero J, Oya S, Bonilla C, Aguayo C. Neurotrophic Schwann-cell factors induce neural differentiation of bone marrow stromal cells. Neuroreport. 2007;18:1713-1717
66. Zurita M, Bonilla C, Otero L, Aguayo, C, Vaquero J. Neural transdifferentiation of bone marrow stromal cells obtained by chemical agents is a short-time reversible phenomenon. Neurosci Res. 2008;60:275-280
67. Zurita M, Vaquero J. Bone marrow stromal cells can achieve cure of chronic paraplegic rats: functional and morphological outcome one year after transplantation. Neurosci Lett. 2006; 402:51-56
68. Maden M. Retinoids and spinal cord development. J Neurobiol. 2006;66:726-738
69. Leng SL, Fan WG, Qu HG, Xu SC, Zhong WY, Zhang WY, et al. Transplantation of bone mesenchymal stem cells containing the nerve growth factor gene in adult rat brain with Fimbria Fornix lesion. Brain Res. 2009; in press.
70. Leng J, Jiang L, Hengsheng C, Zhang X. Brain derived neurotrophic factor and electrophysiological properties of voltage-gated ion channels during neuronal stem cell development. Brain Res. 2009;1272:14-24.
71. Kim HJ, Lee JH, Kim SH. Therapeutic effects of human mesenchymal stem cells for traumatic brain injury in rats: secretion of neurotrophic factors and inhibition of apoptosis. J Neurotrauma. 2010;27:131-138
72. Wang Z, Deng Q, Zhang X, Zhang J. Treatment of injured neurons with bone marrow stem cells cotransfected by hTERT and Ad-BDNF in vitro. J Mol Neurosci. 2009;38: 265-272