Delivery of Alginate Scaffold Releasing Two Trophic Factors for Spinal Cord Injury Repair

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Grulova, I ^a   Slovinska, L ^a   Blasko J ^a   Devaux, S ^a,b   Wisztorski, M ^b   Salzet, M ^b   Fournier, I ^b   Kryukov, O ^c   Cohen, S ^c   Cizkova, D ^a,b  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b INSERM   (France)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; ALGINIC ACID; CALCITONIN GENE RELATED PEPTIDE; CALCIUM BINDING PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCURONIC ACID; HEXURONIC ACID; NERVE GROWTH FACTOR; PROTEOME;

ANGIOGENESIS; ANIMAL; AXON; BIOSYNTHESIS; CHEMISTRY; CLUSTER ANALYSIS; CONVALESCENCE; DISEASE MODEL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOTONEURON; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; PROTEOMICS; RAT; SPINAL CORD INJURIES; SYNAPSE VESICLE; TISSUE SCAFFOLD;

ALGINATES; ANIMALS; AXONS; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM-BINDING PROTEINS; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCURONIC ACID; HEXURONIC ACIDS; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; MICROFILAMENT PROTEINS; MOTOR ACTIVITY; MOTOR NEURONS; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE GROWTH FACTORS; PROTEOME; PROTEOMICS; RATS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; SYNAPTIC VESICLES; TISSUE SCAFFOLDS;

EID: 84941082609     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13702     Document Type: Article

References (76)

1. Rowland, J. W., Hawryluk, G. W., Kwon, B., Fehlings, M. G. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg Focus 25, E2 (2008).
2. Kakulas, B. A. A review of the neuropathology of human spinal cord injury with emphasis on special features. J Spinal Cord Med 22, 119-124 (1999).
3. Kwon, B. K., Tetzlaff, W., Grauer, J. N., Beiner, J., Vaccaro, A. R. Pathophysiology and pharmacologic treatment of acute spinal cord injury. Spine J 4, 451-464 (2004).
4. Norenberg, M. D., Smith, J., Marcillo, A. The pathology of human spinal cord injury: defining the problems. J Neurotrauma 21, 429-440 (2004).
5. Fitch, M. T., Silver, J. CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol 209, 294-301 (2008).
6. Ha, K. Y., Kim, Y. H. Neuroprotective effect of moderate epidural hypothermia after spinal cord injury in rats. Spine (Phila Pa 1976) 33, 2059-2065 (2008).
7. Cafferty, W. B. et al. Chondroitinase ABC-mediated plasticity of spinal sensory function. J Neurosci 28, 11998-12009 (2008).
8. Galtrey, C. M., Asher, R. A., Nothias, F., Fawcett, J. W. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 130, 926-939 (2007).
9. Galtrey, C. M., Fawcett, J. W. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54, 1-18 (2007).
10. Andrade, M. S., Mendonca, L. M., Chadi, G. Treadmill running protects spinal cord contusion from secondary degeneration. Brain Res 1346, 266-278 (2010).
11. Cizkova, D. et al. Response of ependymal progenitors to spinal cord injury or enhanced physical activity in adult rat. Cell Mol Neurobiol 29, 999-1013 (2009).
12. Thuret, S., Moon, L. D., Gage, F. H. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7, 628-643 (2006).
13. Gupta, D., Tator, C. H., Shoichet, M. S. Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. Biomaterials 27, 2370-2379 (2006).
14. Jain, A., Kim, Y. T., McKeon, R. J., Bellamkonda, R. V. 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).
15. Piantino, J., Burdick, J. A., Goldberg, D., Langer, R., Benowitz, L. I. An injectable, biodegradable hydrogel for trophic factor delivery enhances axonal rewiring and improves performance after spinal cord injury. Exp Neurol 201, 359-367 (2006).
16. Williams, D. F. On the nature of biomaterials. Biomaterials 30, 5897-5909 (2009).
17. Garbayo, E. et al. Effective GDNF brain delivery using microspheres-a promising strategy for Parkinson's disease. J Control Release 135, 119-126 (2009).
18. Wang, Y. C. et al. Sustained intraspinal delivery of neurotrophic factor encapsulated in biodegradable nanoparticles following contusive spinal cord injury. Biomaterials 29, 4546-4553 (2008).
19. Gutowska, A., Jeong, B., Jasionowski, M. Injectable gels for tissue engineering. Anat Rec 263, 342-349 (2001).
20. Tan, L. P., Hidayat, A., Lao, L. L., Quah, L. F. Release of hydrophilic drug from biodegradable polymer blends. J Biomater Sci Polym Ed 20, 1381-1392 (2009).
21. Nomura, H., Tator, C. H., Shoichet, M. S. Bioengineered strategies for spinal cord repair. J Neurotrauma 23, 496-507 (2006).
22. Sugahara, K. et al. Structural studies on the chondroitinase ABC-resistant sulfated tetrasaccharides isolated from various chondroitin sulfate isomers. Carbohydr Res 255, 145-163 (1994).
23. Suzuki, Y. et al. Electrophysiological and horseradish peroxidase-tracing studies of nerve regeneration through alginate-filled gap in adult rat spinal cord. Neurosci Lett 318, 121-124 (2002).
24. Prang, P. et al. The promotion of oriented axonal regrowth in the injured spinal cord by alginate-based anisotropic capillary hydrogels. Biomaterials 27, 3560-3569 (2006).
25. Cizkova, D. et al. The influence of sustained dual-factor presentation on the expansion and differentiation of neural progenitors in affinity-binding alginate scaffolds. J Tissue Eng Regen Med doi: 10.1002/term.1797 (2013).
26. Lee, K., Silva, E. A., Mooney, D. J. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J R Soc Interface 8, 153-170 (2011).
27. Perale, G. et al. Hydrogels in spinal cord injury repair strategies. ACS Chem Neurosci 2, 336-345 (2011).
28. Shanbhag, M. S. et al. Neural progenitor cells grown on hydrogel surfaces respond to the product of the transgene of encapsulated genetically engineered fibroblasts. Biomacromolecules 11, 2936-2943 (2010).
29. Lam, H. J., Patel, S., Wang, A., Chu, J., Li, S. In vitro regulation of neural differentiation and axon growth by growth factors and bioactive nanofibers. Tissue Eng Part A 16, 2641-2648 (2010).
30. Cizkova, D. et al. Alterations of protein composition along the rostro-caudal axis after spinal cord injury: proteomic, in vitro and in vivo analyses. Front Cell Neurosci 8, 105 (2014).
31. Vanicky, I., Urdzikova, L., Saganova, K., Cizkova, D., Galik, J. A simple and reproducible model of spinal cord injury induced by epidural balloon inflation in the rat. J Neurotrauma 18, 1399-1407 (2001).
32. Cizkova, D. et al. Modulation properties of factors released by bone marrow stromal cells on activated microglia: an in vitro study. Sci Rep 4, 7514 (2014).
33. Cox, J., Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26, 1367-1372 (2008).
34. Cox, J. N. N., Michalski, A.; Scheltema, R. A., Olsen, J. V., Mann, M. Andromeda: a peptide search engine integrated into the MaxQuant environment. . J. Proteome Res. 10, 1794-1805 (2011).
35. Cox, J. et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics 13, 2513-2526 (2014).
36. Vizcaino, J. A. et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 32, 223-226 (2014).
37. Vizcaino, J. A. et al. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 41, D1063-1069 (2013).
38. Tsur-Gang, O. et al. The effects of peptide-based modification of alginate on left ventricular remodeling and function after myocardial infarction. Biomaterials 30, 189-195 (2009).
39. Basso, D. M., Beattie, M. S., Bresnahan, J. C. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12, 1-21 (1995).
40. Grulova, I., Slovinska, L., Nagyova, M., Cizek, M., Cizkova, D. The effect of hypothermia on sensory-motor function and tissue sparing after spinal cord injury. Spine J 13, 1881-1891 (2013).
41. Cizkova, D. et al. Enrichment of rat oligodendrocyte progenitor cells by magnetic cell sorting. J Neurosci Methods 184, 88-94 (2009).
42. Jones, L. L., Tuszynski, M. H. Spinal cord injury elicits expression of keratan sulfate proteoglycans by macrophages, reactive microglia, and oligodendrocyte progenitors. J Neurosci 22, 4611-4624 (2002).
43. Novotna, I. et al. IT delivery of ChABC modulates NG2 and promotes GAP-43 axonal regrowth after spinal cord injury. Cell Mol Neurobiol 31, 1129-1139 (2011).
44. Nadelhaft, I., Booth, A. M. The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: a horseradish peroxidase study. J Comp Neurol 226, 238-245 (1984).
45. Cizkova, D. et al. Functional recovery in rats with ischemic paraplegia after spinal grafting of human spinal stem cells. Neuroscience 147, 546-560 (2007).
46. Bareyre, F. M. Neuronal repair and replacement in spinal cord injury. J Neurol Sci 265, 63-72 (2008).
47. Hejcl, A. 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).
48. Pachence, J. M. Collagen-based devices for soft tissue repair. J Biomed Mater Res 33, 35-40 (1996).
49. Schwab, M. E. Repairing the injured spinal cord. Science 295, 1029-1031 (2002).
50. Urdzikova, L. M. et al. Human mesenchymal stem cells modulate inflammatory cytokines after spinal cord injury in rat. Int J Mol Sci 15, 11275-11293.
51. Jahn, R., Schiebler, W., Ouimet, C., Greengard, P. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci USA 82, 4137-4141 (1985).
52. Wiedenmann, B., Franke, W. W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41, 1017-1028 (1985).
53. Nudo, R. J., Masterton, R. B. Descending pathways to the spinal cord: a comparative study of 22 mammals. J Comp Neurol 277, 53-79 (1988).
54. Nudo, R. J., Masterton, R. B. Descending pathways to the spinal cord, IV: Some factors related to the amount of cortex devoted to the corticospinal tract. J Comp Neurol 296, 584-597 (1990).
55. Bareyre, F. M. et al. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7, 269-277 (2004).
56. Cizkova, D. et al. Repetitive intrathecal catheter delivery of bone marrow mesenchymal stromal cells improves functional recovery in a rat model of contusive spinal cord injury. J Neurotrauma 9, 1951-1961 (2011).
57. Karimi-Abdolrezaee, S., Eftekharpour, E., Wang, J., Schut, D., Fehlings, M. G. Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci 30, 1657-1676 (2010).
58. Maier, I. C. et al. Constraint-induced movement therapy in the adult rat after unilateral corticospinal tract injury. J Neurosci 28, 9386-9403 (2008).
59. Carbonetto, S., Gruver, M. M., Turner, D. C. Nerve fiber growth in culture on fibronectin, collagen, and glycosaminoglycan substrates. J Neurosci 3, 2324-2335 (1983).
60. Carbonetto, S. T., Gruver, M. M., Turner, D. C. Nerve fiber growth on defined hydrogel substrates. Science 216, 897-899 (1982).
61. Zhong, Y., Yu, X., Gilbert, R., Bellamkonda, R. V. Stabilizing electrode-host interfaces: a tissue engineering approach. J Rehabil Res Dev 38, 627-632 (2001).
62. Kataoka, K. 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 54, 373-384 (2001).
63. Suzuki, K. et al. Regeneration of transected spinal cord in young adult rats using freeze-dried alginate gel. Neuroreport 10, 2891-2894 (1999).
64. Joosten, E. A., Bar, P. R., Gispen, W. H. Collagen implants and cortico-spinal axonal growth after mid-thoracic spinal cord lesion in the adult rat. J Neurosci Res 41, 481-490 (1995).
65. Olson, H. E. 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).
66. Plate, K. H. Mechanisms of angiogenesis in the brain. J Neuropathol Exp Neurol 58, 313-320 (1999).
67. Sobue, K. et al. Induction of blood-brain barrier properties in immortalized bovine brain endothelial cells by astrocytic factors. Neurosci Res 35, 155-164 (1999).
68. Bird, G. C. et al. Pain-related synaptic plasticity in spinal dorsal horn neurons: role of CGRP. Mol Pain 2, 31 (2006).
69. Keast, J. R., De Groat, W. C. Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J Comp Neurol 319, 615-623 (1992).
70. Ji, R. R., Kohno, T., Moore, K. A., Woolf, C. J. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26, 696-705 (2003).
71. Minami, T. et al. Involvement of primary afferent C-fibres in touch-evoked pain (allodynia) induced by prostaglandin E2. Eur J Neurosci 11, 1849-1856 (1999).
72. Samad, T. A. et al. Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410, 471-475 (2001).
73. Hua, X. Y., Chen, P., Marsala, M., Yaksh, T. L. Intrathecal substance P-induced thermal hyperalgesia and spinal release of prostaglandin E2 and amino acids. Neuroscience 89, 525-534 (1999).
74. Ferrari, D. et al. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J Immunol 159, 1451-1458 (1997).
75. Svensson, C. I. et al. Prostaglandin E2 release evoked by intrathecal dynorphin is dependent on spinal p38 mitogen activated protein kinase. Neuropeptides 39, 485-494 (2005).
76. Silver, J., Miller, J. H. Regeneration beyond the glial scar. Nat Rev Neurosci 5, 146-156 (2004).