Effects of collagen membranes enriched with in vitro-differentiated N1E-115 cells on rat sciatic nerve regeneration after end-to-end repair

Journal of NeuroEngineering and Rehabilitation

Volumn 7, Issue 1, 2010, Pages

  Amado, Sandra ^b   Rodrigues, Jorge M ^a   Luís, Ana L ^a   Armada Da Silva, Paulo A S ^b   Vieira, Mrcia ^a   Gartner, Andrea ^a   Simes, Maria J ^a   Veloso, Antánio P ^b   Fornaro, Michele ^c   Raimondo, Stefania ^c   Varejo, Artur S P ^d   Geuna, Stefano ^c   Maurício, Ana C ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSIDADE DE LISBOA   (Portugal)

^c UNIVERSITY OF TURIN   (Italy)

^d UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 3;

ANASTOMOSIS; ANIMAL; ARTICLE; CELL DIFFERENTIATION; CONVALESCENCE; CYTOLOGY; IN VITRO STUDY; INJURY; MALE; METHODOLOGY; NERVE CELL; NERVE FIBER TRANSECTION; NERVE REGENERATION; PHYSIOLOGY; RAT; SCIATIC NERVE; SPRAGUE DAWLEY RAT; TISSUE ENGINEERING; TRANSPLANTATION;

ANASTOMOSIS, SURGICAL; ANIMALS; AXOTOMY; CELL DIFFERENTIATION; COLLAGEN TYPE III; MALE; NERVE REGENERATION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SCIATIC NERVE; TISSUE ENGINEERING;

EID: 77649195488     PISSN: None     EISSN: 17430003     Source Type: Journal    
DOI: 10.1186/1743-0003-7-7     Document Type: Article

References (75)

1. Bridging nerve defects: the role of tissue interpositioning. G Lundborg, Severe Traumatic Defects of the Upper Limb London: Martin Dunitz, Masquelet AC, Ferreira AC, 2003 153 167
2. Peripheral nerve repair and grafting techniques: a review. T Matsuyama M Mackay R Midha, Neurol Med Chir 2000 40 187 199 10.2176/nmc.40.187
3. Current techniques and concepts in peripheral nerve repair. M Siemionow G Brzezicki, Int Rev Neurobiol 2009 87 139 170
4. Electrical Stimulation for Improving Nerve Regeneration: Where do we stand? T Gordon OA Sulaiman A Ladak, Int Rev Neurobiol 2009 87 433 444 full-text 19682653
5. The Role of Conduits in Nerve Repair, a Review. VB Doolabh MC Hertl SE Mackinnon, Rev Neurosci 1996 7 47 84 8736678
6. Use of anti-CD40 ligand Monoclonal Antibody as Antirejection Therapy in a Murine Peripheral Nerve Allograft Model. JN Jensen TH Tung SE Mackinnon MJ Brenner DA Hunter, Microsurgery 2004 24 309 315 10.1002/micr.20028 15274190
7. Alternatives to Autologous Nerve Grafts. G Lundborg, Handchir, Mikrochir, Plast Chir 2004 36 1 7 10.1055/s-2004-820870 (Pubitemid 38470243)
8. End-to-side (Terminolateral) Nerve Regeneration: a Challenge for Neuroscientists Coming from an Intriguing Nerve Repair Concept. S Geuna I Papalia P Tos, Brain Res Rev 2006 52 381 388 10.1016/j.brainresrev.2006.05.002 16766038
9. Peripheral nerve regeneration using silicone rubber chambers filled with collagen, laminin and fibronectin. YS Chen CL Hsieh CC Tsai TH Chen WC Cheng CL Hu CH Yao, Biomaterials 2000 21 1541 1547 10.1016/S0142-9612(00)00028-4 10885726
10. Long-term evaluation of degradation and foreign body reaction of subcutaneously implanted poly (DL-lactide - caprolactone). WFA Den Dunnen R Van Wessel AJ Pennings PH Robinson MBM Van Leeuwen JM Schakenraad, J Biomed Mater Sci 1997 36 337 346 10.1002/(SICI)1097-4636(19970905)36:3<337::AID-JBM93.0. CO;2-F
11. Neural Tissue Engineering: Strategies for repair and regeneration. CE Schmidt JB Leach, Annu Rev Biomed Eng 2003 5 293 347 10.1146/annurev.bioeng.5. 011303.120731 14527315
12. Use of PLGA 90:10 scafolds enriched with in vitro-differentiated neural cells for repairing rat sciatic nerve defects. AL Luís JM Rodrigues S Geuna S Amado Y Shirosaki JM Lee F Fregnan MA Lopes AP Veloso AJ Ferreira JD Santos PAS Armada-da-Silva ASP Varejo AC Maurício, Tissue Engineering Part A 2008 14 6 979 993 10.1089/ten.tea.2007.0273 18447635
13. Neural cell transplantation effects on sciatic nerve regeneration after standardized crush injury in the rat. AL Luís JM Rodrigues S Geuna S Amado MJ Simes F Fregnan AJ Ferreira AP Veloso PAS Armada-da-Silva ASP Varejo AC Maurício, Microsurgery 2008 28 6 458 470 10.1002/micr.20524 18623156
14. Use of hybrid chitosan membranes and N1E-115 cells for promoting nerve regeneration in an axonotmesis rat model. S Amado MJ Simes PAS Armada-da-Silva AL Luís Y Shirosaki MA Lopes JD Santos F Fregnan G Gambarotta S Raimondo M Fornaro AP Veloso ASP Varejo AC Maurício S Geuna, Biomaterials 2008 29 33 4409 4419 10.1016/j.biomaterials.2008.07.043 18723219
15. Tissue engineering of peripheral nerves. B Battiston S Raimondo P Tos V Gaidano C Audisio A Scevola I Perroteau S Geuna, Int Rev Neurobiol 2009 87 225 250
16. Comparison of regeneration results of prefabricated nerve graft, autogenous nerve graft, and vein graft in repair of nerve defects. H Karagoz E Ulkur F Uygur MG Senol M Yapar P Turan B Celikoz, Microsurgery 2009 29 138 143 10.1002/micr.20586 18942646
17. Gene therapy perspectives for nerve repair. S Zacchigna M Giacca, Int Rev Neurobiol 2009 87 381 392 full-text 19682649
18. A Laminin graft replaces neurorrhaphy in the restorative surgery of the rat sciatic nerve. T Kauppila E Jyvasjarvi T Huopaniemi E Hujanen P Liesi, Exp Neurol 1993 123 181 191 10.1006/exnr.1993.1151 8405284
19. Adhesion molecules of the nervous system. U Rutishauser, Curr Opin Neurobiol 1993 3 709 715 10.1016/0959-4388(93)90142-L 8260819
20. Sciatic nerve regeneration navigated by laminin-fibronectin double coated biodegradable collagen grafts in rats. XJ Tong K Hirai H Shimada Y Mizutani T Izumi N Toda P Yu, Brain Res 1994 663 155 162 10.1016/0006-8993(94)90473-1 7850464
21. Orientated mats of fibronectin as a conduit material for use in peripheral nerve repair. IH Whitworth RA Brown C Dore CJ Green G Terenghi, J Hand Surg (Br) 1995 20 429 36 7594978
22. Adhesion, alignment, and migration of cultured Schwann cells on ultrathin fibronectin fibres. Z Ahmed RA Brown, Cell Motil Cytoskelet 1999 42 331 343 10.1002/(SICI)1097-0169(1999)42:4<331::AID-CM63.0.CO;2-7
23. Peripheral Nerve Regeneration along Collagen Filaments. S Yoshii M Oka, Brain Res 2001 888 158 162 10.1016/S0006-8993(00)03025-0 11146062 (Pubitemid 32056272)
24. The extracellular matrix in axon regeneration. B Grimpe J Silver, Prog Brain Res 2002 137 333 349 full-text 12440376
25. Evaluation of peripheral nerve regeneration across an 80-mm gap using a polyglycolic acid (PGA)-collagen nerve conduit filled with laminin-soaked collagen sponge in dogs. T Toba T Nakamura AK Lynn K Matsumoto S Fukuda M Yoshitami Y Hori Y Shimizu, Int J Artif Organs 2002 25 230 237 11999196
26. Evaluation of crosslinking procedures of collagen tubes used in peripheral nerve repair. S Itoh K Takakuda S Kawabata Y Aso K Kasai, Biomaterials 2002 23 4475 4481 10.1016/S0142-9612(02)00166-7 12322967
27. Regeneration of rat sciatic nerve along collagen filaments. S Yoshii M Oka M Shima A Taniguchi M Akagi, Brain Res 2002 949 202 208 10.1016/S0006- 8993(02)03149-9 12213317
28. Magnetically aligned collagen gel filling a collagen nerve guide improves peripheral nerve regeneration. D Ceballos X Navarro N Dubey G Wendelschafer-Crabb WR Kennedy RT Tranquillo, Exp Neurol 1999 158 290 300 10.1006/exnr.1999.7111 10415137
29. Guided Neurite Elongation and Schwann Cell Invasion Into Magnetically Aligned Collagen in Simulated Peripheral Nerve Regeneration. N Dubey PC Letourneau RT Tranquillo, Exp Neurol 1999 158 338 350 10.1006/exnr.1999.7095 10415141 (Pubitemid 29382825)
30. Monkey median nerve repaired by nerve graft or collagen nerve guide tube. SJ Archibald J Shefner C Krarup RD Madison, J Neurosci 1995 15 4109 4123 7751969
31. Collagen- GAG substrate enhances the quality of nerve regeneration through collagen tubes up to level of autograft. LJ Chamberlain IV Yannas HP Hsu G Strichartz M Spector, Exp Neurol 1998 154 315 329 10.1006/exnr.1998.6955 9878170
32. Near-terminus axonal structure and function following rat sciatic nerve regeneration through a collagen-GAG matrix in a ten millimeter gap. LJ Chamberlain IV Yannas HP Hsu GR Strichartz M Spector, J Neurosci Res 2000 60 666 677 10.1002/(SICI)1097-4547(20000601)60:5<666::AID-JNR123.0.CO;2-0 10820438
33. The cellular and molecular basis of peripheral nerve regeneration. SY Fu T Gordon, Mol Neurobiol 1997 14 67 116 10.1007/BF02740621 9170101
34. Pharmacokinetics of nerve growth factor (NGF) following different routes of administration to adult rats. MA Tria M Fusco G Vantini R Mariot, Exp Neurol 1994 127 178 183 10.1006/exnr.1994.1093 8033961
35. Neurotransmitter synthesis by neuroblastoma clones (neuroblast differentiation-cell culture-choline acetyltransferase-acetylcholinesterase- tyrosine hydroxylase-axons-dendrites). TER Amano M Niremberg, Proc Natl Acad Sci (USA) 1972 69 258 263 10.1073/pnas.69.1.258
36. 2+ concentration in the N1E-115 neuronal cell line and its use for peripheric nerve regeneration. JM Rodrigues AL Luís JV Lobato MV Pinto A Faustino N Sooraj Hussain MA Lopes AP Veloso M Freitas S Geuna JD Santos AC Maurício, Acta Med Portug 2005 18 323 328
37. 2+ concentration in the N1E-115 neuronal cell line in perspective of its use for peripheric nerve regeneration. JM Rodrigues AL Luís JV Lobato MV Pinto MA Lopes AP Veloso M Freitas S Geuna JD Santos AC Maurício, J Bio-Medical Mat Eng 2005 15 455 465
38. Maturation of neuroblastoma cells in the presence of dimethylsulfoxide. Y Kimhy I Spector Y Barak UZ Littauer, Proc Natl Acad Sci (USA) 1976 73 462 466 10.1073/pnas.73.2.462
39. The plasma membrane as a regulatory site in growth and differentiation of neuroblastoma cells. SL De Laat PT van der Saag, Int Rev Cyt 1982 74 1 7 full-text
40. Up-regulation of angiotensin II receptors by in vitro differentiation of murine N1E-115 neuroblastoma cells. LP Reagan X Ye R Mir R DePalo J Fluharty, Mol Pharmacol 1990 38 878 886 2123521
41. Growth Inhibition of N1E-115 Mouse Neuroblastoma Cells by C-myc or N-myc Antisense Oligodeoxynucleotides Causes Limited Differentiation but is not Coupled to Neurite Formation. Biochem. JC Larcher M Basseville JL Vaysierre L Cordeau-Lossouarn B Croizat F Gros, Biophys Res Comun 1992 185 915 924 10.1016/0006-291X(92)91714-2
42. Differentiation of neuroblastoma cells: a useful model for neurobiology and cancer. KN Prasad, Biol Rev Camb Philos Soc 1991 66 431 451 10.1111/j.1469-185X.1991.tb01148.x 1801947
43. Modification of the expression of adenosine 3', 5'-cyclic monophosphate-induced differentiated functions in neuroblastoma cells by beta-carotene and D-alpha-tocopheryl succinate. KN Prasad S Kentroti J Edwards-Prasad A Vernadakis M Imam E Carvalho S Kumar, J Am Coll Nutr 1994 13 298 303 7915734
44. A comparison of cryoprobe and crush lesions in the rat sciatic nerve. JM Kerns B Braverman A Mathew C Lucchinetti AD Ivankovich, Pain 1991 47 31 39 10.1016/0304-3959(91)90008-L 1771091
45. A simple method for reducing autotomy in rats with peripheral nerve lesions. ME Sporel-Ozakat PM Edwards KT Hepgul A Savas WH Gispen, J Neurosci Méthodes 1991 36 263 265 10.1016/0165-0270(91)90052-2
46. Neurologic evaluation of the rat during sciatic nerve block with lidocaine. JG Thalhammer M Vladimirova B Bershad-Sky GR Strichartz, Anaesthesiology 1995 82 1013 1025 10.1097/00000542-199504000-00026
47. Quantification of functional recovery following rat sciatic nerve transection. R Koka TA Hadlock, Exp Neurol 2001 168 192 195 10.1006/exnr.2000. 7600 11170734
48. Prolonged regional nerve blockade by controlled release of local anesthetic from a biodegradable polymer matrix. DB Masters CB Berge SK Dutta CT Griggs D Hu W Kupsky R Langer, Anesthesiology 1993 79 340 346 10.1097/00000542-199308000-00020 8342843 (Pubitemid 23224847)
49. Neurologic evaluation of infant and adult rats before and after sciatic nerve blockade. D Hu R Hu CB Berde, Anaesthesiology 1997 86 957 965 10.1097/00000542-199704000-00026 (Pubitemid 27174736)
50. Nerve lesions and the generation of pain. JN Campbell, Muscle Nerve 2001 24 1261 1273 10.1002/mus.1143 11562904
51. The Correlation between Dietary Soy Phytoestrogens and Neuropathic Pain Behavior in Rats after Partial Denervation. Y Shir JN Campbell SN Raja Z Seltzer, Anesth Analg 2002 94 2 421 426 10.1097/00000539-200202000-00037 11812712
52. Toe Out Angle: a functional index for the evaluation of sciatic nerve recovery in the rat model. ASP Varejo AM Cabrita S Geuna P Melo-Pinto VM Filipe A Gramsbergen MF Meek, Exp Neurol 2003 183 695 699 10.1016/S0014-4886(03)00208-5 14552911
53. Motion of the foot and ankle during the stance phase in rats. ASP Varejo AM Cabrita MF Meek J Bulas-Cruz RC Gabriel VM Filipe P Melo-Pinto DA Winter, Muscle Nerve 2002 26 630 635 10.1002/mus.10242 12402284
54. Ankle kinematics to evaluate functional recovery in crushed rat sciatic nerve. ASP Varejo AM Cabrita MF Meek J Bulas-Cruz VM Filipe RC Gabriel AJ Ferreira S Geuna D Winter, Muscle Nerve 2003 27 706 714 10.1002/mus.10374 12766982 (Pubitemid 36667480)
55. Long-term functional and morphological assessment of a standardized rat sciatic nerve crush injury with a non-serrated clamp. AL Luís S Amado S Geuna JM Rodrigues MJ Simes JD Santos F Fregman S Raimondo AP Veloso AJA Ferreira PAS Armada-da-Silva ASP Varejo AC Maurício, J Neurosci Methods 2007 163 92 104 10.1016/j.jneumeth.2007.02.017 17397932
56. A simple protocol for paraffin-embedded myelin sheath staining with osmium tetroxide for light microscope observation. F Di Scipio S Raimondo P Tos S Geuna, Microsc Res Tech 2008 71 497 502 10.1002/jemt.20577 18320578
57. Methods and protocols in peripheral nerve regeneration experimental research: Part II - morphological techniques. S Raimondo M Fornaro F Di Scipio G Ronchi MG Giacobini-Robecchi S Geuna, Int Rev Neurobiol 2009 87 79 101
58. Verification of the two-dimensional disector, a method for the unbiased estimation of density and number of myelinated nerve fibers in peripheral nerves. S Geuna P Tos B Battiston R Guglielmone, Ann Anat 2000 182 23 34 10.1016/S0940-9602(00)80117-X 10668555
59. Methodological issues in size estimation of myelinated nerve fibers in peripheral nerves. S Geuna P Tos R Guglielmone B Battiston MG Giacobini-Robecchi, Anat Embryol 2001 204 1 10 10.1007/s004290100188 11506429
60. On sampling and sampling errors in histomorphometry of peripheral nerve fibers. S Geuna D Gigo-Benato AC Rodrigues, Microsurgery 2004 24 72 76 10.1002/micr.10199 14748030
61. The revolution of counting "Tops": two decades of the disector principle in morphological research. S Geuna, Microsc Res Tech 2005 66 270 274 10.1002/jemt.20167 15940681
62. Enhancement of peripheral nerve regeneration. BR Seckel, Muscle Nerve 1990 13 785 800 10.1002/mus.880130904 2233865
63. Peripheral nerve regeneration. C Ide, Neurosci Res 1996 25 101 121 8829147
64. Use of stem cells for improving nerve regeneration. G Terenghi M Wiberg PJ Kingham, Int Rev Neurobiol 2009 87 393 403 full-text 19682650
65. Enhancing posttraumatic nerve regeneration. G Lundborg, J Periph Nerv Syst 2002 7 139 140 10.1046/j.1529-8027.2002.02019.x
66. Tissue engineered nerve constructs: where do we stand? CT Chalfoun GA Wirth GRJ Evans, J Cell Mol Med 2006 10 309 317 10.1111/j.1582-4934.2006. tb00401.x 16796801
67. Stem-cell plasticity and therapy for injuries of the peripheral nervous system. M Tohill G Terenghi, Biotechnol Appl Biochem 2004 40 17 24 10.1042/BA20030173 15270703
68. Nerve conduits and growth factor delivery in peripheral nerve repair. LA Pfister M Papalozos HP Merkle B Gander, J Peripher Nerv Syst 2007 12 65 82 10.1111/j.1529-8027.2007.00125.x 17565531
69. Long nerve gaps limit the regenerative potential of bioartificial nerve conduits filled with Schwann cells. N Sinis HE Schaller ST Becker B Schlosshauer M Doser H Roesner S Oberhoffner HW Müller M Haerle, Restor Neurol Neurosci 2007 25 131 141 17726272
70. Future perspective in peripheral nerve reconstruction. L Dahlin F Johansson C Lindwall M Kanje, Int Rev Neurobiol 2009 87 507 530 full-text 19682657
71. Luminal fillers in nerve conduits for peripheral nerve repair. MB Chen F Zhang WC Lineaweaver, Ann Plast Surg 2006 57 462 471 10.1097/01.sap.0000237577. 07219.b6 16998343
72. Nestin expression in hair follicle sheath progenitor cells. L Li J Mignone M Yang M Matic S Penman G Enikolopov RM Hoffman, Proceedings of the National Academy of Sciences USA 2003 100 9958 9961 10.1073/pnas.1733025100 (Pubitemid 37087050)
73. Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Y Amoh L Li K Katsuoka S Penman RM Hoffman, Proceedings of the National Academy of Sciences USA 2005 102 5530 5534 10.1073/pnas. 0501263102 (Pubitemid 40530292)
74. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Y Amoh L Li R Campillo K Kawahara K Katsuoka S Penman RM Hoffman, Proceedings of the National Academy of Sciences USA 2005 102 17734 17738 10.1073/pnas.0508440102 (Pubitemid 41803566)
75. Human hair follicle pluripotent stem (hfPS) cells promote regeneration of peripheral-nerve injury: an advantageous alternative to ES and iPS cells. Y Amoh M Kanoh S Niiyama Y Hamada K Kawahara Y Sato RM Hoffman K Katsuoka, Journal of Cellular Biochemistry 2009 107 1016 1020 10.1002/jcb.22204 19507228