Evaluation of early and late effects into the acute spinal cord injury of an injectable functionalized self-assembling scaffold

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Cigognini, Daniela ^a,b   Satta, Alessandro ^a   Colleoni, Bianca ^a   Silva, Diego ^a,b   Donegà, Matteo ^a   Antonini, Stefania ^a,b   Gelain, Fabrizio ^a,b,c  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b OSPEDALE NIGUARDA CA GRANDA   (Italy)

^c CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; GROWTH FACTOR; NANOMATERIAL; RADA16 I 4G BONE MARROW HOMING PEPTIDE 1; UNCLASSIFIED DRUG; PEPTIDE; RADA16 I; RADA16-I; TISSUE SCAFFOLD;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CELL SURVIVAL; CLINICAL EVALUATION; CONTROLLED STUDY; FEMALE; FORELIMB; GENE EXPRESSION REGULATION; HINDLIMB; HISTOPATHOLOGY; IN VITRO STUDY; MOTOR COORDINATION; MOTOR PERFORMANCE; NERVE REGENERATION; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROCESS OPTIMIZATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; THERAPY EFFECT; ACUTE DISEASE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHRONIC DISEASE; DRUG EFFECT; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; INJECTION; METABOLISM; MOLECULAR GENETICS; MOTOR ACTIVITY; NEOVASCULARIZATION (PATHOLOGY); NERVE FIBER; PATHOLOGY; PATHOPHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

RATTUS;

ACUTE DISEASE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CHRONIC DISEASE; EXTRACELLULAR MATRIX; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; INJECTIONS; MOLECULAR SEQUENCE DATA; MOTOR ACTIVITY; NEOVASCULARIZATION, PATHOLOGIC; NERVE FIBERS; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPINAL CORD INJURIES; TISSUE SCAFFOLDS;

EID: 79956206107     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019782     Document Type: Article

References (69)

1. Anderson KD, (2004) Targeting Recovery: Priorities of the Spinal Cord-Injured Population. J Neurotrauma 21: 1371-1383.
2. ICCP,International Campaign for Cures of spinal cord injury Paralysis (2007) Experimental treatments for spinal cord injury. A guide for people with spinal cord injury Available: http://icord.org/documents/iccp-clinical-trials-information/ via the Internet.
3. Baptiste DC, Fehlings MG, (2007) Update on the treatment of spinal cord injury. Prog Brain Res 161: 217-233.
4. Hamid S, Hayek R, (2008) Role of electrical stimulation for rehabilitation and regeneration after spinal cord injury: an overview. Eur Spine J 17: 1256-1269.
5. Thuret S, Moon LD, Gage FH, (2006) Therapeutic interventions after spinal cord injury. Nature 7: 628-643.
6. Hagg T, Oudega M, (2006) Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 23: 264-280.
7. Fitch MT, Silver J, (2008) CNS injury, glial scars, and inflammation: Inhibitory extracellular matrices and regeneration failure. Exp Neurol 209: 294-301.
8. Madigan NN, McMahon S, O'Brien T, Yaszemski MJ, Windebank AJ, (2009) Current tissue engineering and novel therapeutic approaches to axonal regeneration following spinal cord injury using polymer scaffolds. Respir Physiol Neurobiol 169: 183-199.
9. Andrade MS, Mendonça LM, Chadi G, (2010) Treadmill running protects spinal cord contusion from secondary degeneration. Brain Res 1346: 266-278.
10. Sahni V, Kessler JA, (2010) Stem cell therapies for spinal cord injury. Nat Rev Neurol 6: 363-372.
11. Hu R, Zhou J, Luo C, Lin J, Wang X, et al. (2010) Glial scar and neuroregeneration: histological, functional, and magnetic resonance imaging analysis in chronic spinal cord injury. J Neurosurg Spine 13: 169-180.
12. Straley KS, Foo CW, Heilshorn SC, (2010) Biomaterial design strategies for the treatment of spinal cord injuries. J Neurotrauma 27: 1-19.
13. Hejcl A, Lesný P, Prádný M, Michálek J, Jendelová P, et al. (2008) Biocompatible hydrogels in spinal cord injury repair. Physiol Res 57 (Suppl 3): S121-S132.
14. Joosten EA, Bär PR, Gispen WH, (1995) Collagen implants and cortico-spinal axonal growth after mid-thoracic spinal cord lesion in the adult rat. J Neurosci Res 41: 481-490.
15. Cui FZ, Tian WM, Hou SP, Xu QY, Lee IS, (2006) Hyaluronic acid hydrogel immobilized with RGD peptides for brain tissue engineering. J Mater Sci Mater Med 17: 1393-1401.
16. Gupta D, Tator CH, Shoichet MS, (2006) Fast-gelling injectable blend of hyaluronan and methylcellulose for intrathecal, localized delivery to the injured spinal cord. Biomaterials 27: 2370-2379.
17. Gros T, Sakamoto JS, Blesch A, Havton LA, Tuszynski MH, (2010) Regeneration of long-tract axons through sites of spinal cord injury using templated agarose scaffolds. Biomaterials 31: 6719-6729.
18. Yao L, Damodaran G, Nikolskaya N, Gorman AM, Windebank A, et al. (2010) The effect of laminin peptide gradient in enzymatically cross-linked collagen scaffolds on neurite growth. J Biomed Mater Res A 92: 484-492.
19. Yu TT, Shoichet MS, (2005) Guided cell adhesion and outgrowth in peptide-modified channels for neural tissue engineering. Biomaterials 26: 1507-1514.
20. Gelain F, Unsworth LD, Zhang S, (2010) Slow and sustained release of active cytokines from self-assembling peptide scaffolds. J Control Release 145: 231-239.
21. Nuttelman CR, Tripodi MC, Anseth KS, (2006) Dexamethasone-functionalized gels induce osteogenic differentiation of encapsulated hMSCs. J Biomed Mater Res A 76: 183-195.
22. Saha K, Pollock JF, Schaffer DV, Healy KE, (2007) Designing synthetic materials to control stem cell phenotype. Curr Opin Chem Biol 11: 381-7.
23. Mapili G, Lu Y, Chen S, Roy K, (2005) Laser-layered microfabrication of spatially patterned functionalized tissue-engineering scaffolds. J Biomed Mater Res B Appl Biomater 75: 414-424.
24. Arcaute K, Mann B, Wicker R, (2010) Stereolithography of spatially controlled multi-material bioactive poly(ethylene glycol) scaffolds. Acta Biomater 6: 1047-1054.
25. Rao SS, Winter JO, (2009) Adhesion molecule-modified biomaterials for neural tissue engineering. Front Neuroengineering 2: 6.
26. Shin H, Jo S, Mikos AG, (2003) Biomimetic materials for tissue engineering. Biomaterials 24: 4353-4364.
27. Ye Z, Zhang H, Luo H, Wang S, Zhou Q, et al. (2008) Temperature and pH effects on biophysical and morphological properties of self-assembling peptide RADA16-I. J Pept Sci 14: 152-162.
28. Zhang S, (2003) Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol 21: 1171-1178.
29. Gelain F, Horii A, Zhang S, (2007) Designer self-assembling peptide scaffolds for 3-d tissue cell cultures and regenerative medicine. Macromol Biosci 7: 544-551.
30. Kyle S, Aggeli A, Ingham E, McPherson MJ, (2009) Production of self-assembling biomaterials for tissue engineering. Trends Biotechnol 27: 423-433.
31. Ellis-Behnke RG, Liang YX, You SW, Tay DK, Zhang S, et al. (2006) Nano neuro knitting: peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proc Natl Acad Sci U S A 103: 5054-5059.
32. Guo J, Su H, Zeng Y, Liang YX, Wong WM, et al. (2007) Reknitting the injured spinal cord by self-assembling peptide nanofiber scaffold. Nanomedicine 3: 311-321.
33. Gelain F, Bottai D, Vescovi A, Zhang S, (2006) Designer self-assembling peptide nanofiber scaffolds for adult mouse neural stem cell 3-dimensional cultures. PLoS One 1: e119.
34. Nowakowski GS, Dooner MS, Valinski HM, Mihaliak AM, Quesenberry PJ, et al. (2004) A specific heptapeptide from a phage display peptide library homes to bone marrow and binds to primitive hematopoietic stem cells Stem Cells 22: 1030-1038.
35. Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL, (1999) Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 283: 534-537.
36. Gelain F, Panseri S, Antonini S, Cunha C, Donega M, et al. (2011) Transplantation of nanostructured composite scaffolds results in the regeneration of chronically injured spinal cords. ACS Nano 5: 227-236.
37. Taraballi F, Natalello A, Campione M, Villa O, Doglia SM, et al. (2010) Glycine-spacers influence functional motifs exposure and self-assembling propensity of functionalized substrates tailored for neural stem cell cultures. Front Neuroengineering 3: 1.
38. Hsu JY, Xu XM, (2005) 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.
39. Fernandes KJ, Fan DP, Tsui BJ, Cassar SL, Tetzlaff W, (1999) Influence of the axotomy to cell body distance in rat rubrospinal and spinal motoneurons: differential regulation of GAP-43, tubulins, and neurofilament-M. J Comp Neurol 414: 495-510.
40. Ruff RL, McKerracher L, Selzer ME, (2008) Repair and neurorehabilitation strategies for spinal cord injury. Ann N Y Acad Sci 1142: 1-20.
41. Ye J, Cao L, Cui R, Huang A, Yan Z, et al. (2004) The effects of ciliary neurotrophic factor on neurological function and glial activity following contusive spinal cord injury in the rats. Brain Res 997: 30-39.
42. Xiao Q, Du Y, Wu W, Yip HK, (2010) Bone morphogenetic proteins mediate cellular response and, together with Noggin, regulate astrocyte differentiation after spinal cord injury. Exp Neurol 221: 353-366.
43. Kim HM, Hwang DH, Lee JE, Kim SU, Kim BG, (2009) Ex vivo VEGF delivery by neural stem cells enhances proliferation of glial progenitors, angiogenesis, and tissue sparing after spinal cord injury. PLoS One 4: e4987.
44. Rosenberg GA, (2002) Matrix metalloproteinases in neuroinflammation. Glia 39: 279-291.
45. Sinescu C, Popa F, Grigorean VT, Onose G, Sandu AM, et al. (2010) Molecular basis of vascular events following spinal cord injury. J Med Life 3: 254-261.
46. Pizzi MA, Crowe MJ, (2007) Matrix metalloproteinases and proteoglycans in axonal regeneration. Exp Neurol 204: 496-511.
47. Stamenkovic I, (2003) Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 200: 448-464.
48. Mahad DJ, Ziabreva I, Campbell G, Lax N, White K, et al. (2009) Mitochondrial changes within axons in multiple sclerosis. Brain 132: 1161-1174.
49. Haynes RL, Borenstein NS, Desilva TM, Folkerth RD, Liu LG, et al. (2005) Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol 484: 156-167.
50. Beattie MS, Bresnahan JC, Komon J, Tovar CA, Van Meter M, et al. (1997) Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 148: 453-463.
51. Basso DM, Beattie MS, Bresnahan JC, (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 2: 1-21.
52. King VR, Alovskaya A, Wei DY, Brown RA, Priestley JV, (2010) The use of injectable forms of fibrin and fibronectin to support axonal ingrowth after spinal cord injury. Biomaterials 31: 4447-4456.
53. Nakamura M, Houghtling RA, MacArthur L, Bayer BM, Bregman BS, (2003) Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp Neurol 184: 313-325.
54. Lü HZ, Hu JG, (2009) Expression of bone morphogenetic proteins-2/4 in neural stem cells and their lineages. Acta Neurobiol Exp (Wars) 69: 441-447.
55. Beck KD, Nguyen HX, Galvan MD, Salazar DL, Woodruff TM, et al. (2010) Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain 133: 433-447.
56. Mautes AE, Weinzierl MR, Donovan F, Noble LJ, (2000) Vascular events after spinal cord injury: contribution to secondary pathogenesis Phys Ther.
57. Heissig B, Nishida C, Tashiro Y, Sato Y, Ishihara M, et al. (2010) Role of neutrophil-derived matrix metalloproteinase-9 in tissue regeneration. Histol Histopathol 25: 765-770.
58. Klapka N, Hermanns S, Straten G, Masanneck C, Duis S, (2005) Suppression of fibrous scarring in spinal cord injury of rat promotes long-distance regeneration of corticospinal tract axons, rescue of primary motoneurons in somatosensory cortex and significant functional recovery. Eur J Neurosci 22: 3047-3058.
59. Buss A, Pech K, Kakulas BA, Martin D, Schoenen J, et al. (2007) Growth-modulating molecules are associated with invading Schwann cells and not astrocytes in human traumatic spinal cord injury. Brain 130: 940-953.
60. King VR, Phillips JB, Hunt-Grubbe H, Brown R, Priestley JV, (2006) Characterization of non-neuronal elements within fibronectin mats implanted into the damaged adult rat spinal cord. Biomaterials 27: 485-496.
61. Tsiper MV, Yurchenco PD, (2002) Laminin assembles into separate basement membrane and fibrillar matrices in Schwann cells. J Cell Sci 115: 1005-1015.
62. Kawasaki T, Nishio T, Kawaguchi S, Kurosawa H, (2001) Spatiotemporal distribution of GAP-43 in the developing rat spinal cord: a histological and quantitative immunofluorescence study. Neurosci Res 39: 347-358.
63. McTigue DM, Wei P, Stokes BT, (2001) Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci 21: 3392-3400.
64. Agrawal G, Kerr C, Thakor NV, All AH, (2010) Characterization of graded multicenter animal spinal cord injury study contusion Spinal Cord Injury Using Somatosensory-Evoked Potentials. Spine 35: 1122-1127.
65. Holguin A, O'Connor KA, Biedenkapp J, Campisi J, Wieseler-Frank J, et al. (2004) HIV-1 gp120 stimulates proinflammatory cytokine-mediated pain facilitation via activation of nitric oxide synthase-I (nNOS). Pain 110: 517-530.
66. Hajebrahimi Z, Mowla SJ, Movahedin M, Tavallaei M, (2008) Gene expression alterations of neurotrophins, their receptors and prohormone convertases in a rat model of spinal cord contusion. Neurosci Lett 441: 261-266.
67. Bonefeld BE, Elfving B, Wegener G, (2008) Reference genes for normalization: a study of rat brain tissue. Synapse 62: 302-309.
68. Ringhoffer M, Schmitt M, Karbach J, Jäger E, Oesch F, et al. (2001) Quantitative assessment of the expression of melanoma-associated antigens by non-competitive reverse transcription polymerase chain reaction. Int J Oncol 19: 983-989.
69. Wrenzycki C, Lucas-Hahn A, Herrmann D, Lemme E, Korsawe K, et al. (2002) In vitro production and nuclear transfer affect dosage compensation of the X-linked gene transcripts G6PD, PGK, and Xist in preimplantation bovine embryos. Biol Reprod 66: 127-134.