Comparison of schwann cells and olfactory ensheathing cells for peripheral nerve gap bridging

Cells Tissues Organs

Volumn 196, Issue 6, 2012, Pages 534-542

  Penna, Vincenzo ^a   Stark, G Bjoern ^a   Wewetzer, Konstantin ^b,d,e   Radtke, Christine ^c   Lang, Eva M ^a,f  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Departments of Functional and Applied Anatomy   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^e CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^f EVANGELISCHES KRANKENHAUS   (Germany)

Author keywords

Biogenic conduit; Nerve conduit; Nerve gap; Olfactory ensheathing cell; Schwann cell; Sciatic functional index

Indexed keywords

FIBRIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSPLANTATION; CONTROLLED STUDY; FEMALE; GLIA CELL; HISTOLOGY; MOTOR PERFORMANCE; MYELINATION; NERVE FIBER; NERVE FIBER REGENERATION; NONHUMAN; OLFACTORY ENSHEATHING CELL; PERIPHERAL NERVE; PRIORITY JOURNAL; RAT; SCHWANN CELL; SCIATIC NERVE;

ANIMALS; CELL CULTURE TECHNIQUES; FEMALE; NERVE REGENERATION; NEUROGLIA; OLFACTORY NERVE; PERIPHERAL NERVES; RATS; RATS, INBRED LEW; SCHWANN CELLS; TRANSFECTION;

RATTUS;

EID: 84870236082     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000338059     Document Type: Article

References (68)

1. Acheson, A., P.A. Barker, R.F. Alderson, F.D. Miller, R.A. Murphy (1991) Detection of brain-derived neurotrophic factor-like activity in fibroblasts and Schwann cells: Inhibition by antibodies to NGF. Neuron 7: 265-275.
2. Anderson, P.N., M. Turmaine (1986) Axonal regeneration through arterial grafts. J Anat 147: 73-82. (Pubitemid 16051848)
3. Ansselin, A.D., T. Fink, D.F. Davey (1997) Peripheral nerve regeneration through nerve guides seeded with adult Schwann cells. Neuropathol Appl Neurobiol 23: 387-398. (Pubitemid 27440479)
4. Babiarz, J., N. Kane-Goldsmith, S. Basak, K. Liu, W. Young, M. Grumet (2011) Juvenile and adult olfactory ensheathing cells bundle and myelinate dorsal root ganglion axons in culture. Exp Neurol 229: 72-79.
5. Bach, A.D., H. Bannasch, T.J. Galla, K.M. Bittner, G.B. Stark (2001) Fibrin glue as matrix for cultured autologous urothelial cells in urethral reconstruction. Tissue Eng 7: 45-53. (Pubitemid 32175961)
6. Bandtlow, C.E., R. Heumann, M.E. Schwab, H. Thoenen (1987) Cellular localization of nerve growth factor synthesis by in situ hybridization. EMBO J 6: 891-899.
7. Battiston, B., P. Tos, S. Geuna, M.G. Giacobini-Robecchi, R. Guglielmone (2000) Nerve repair by means of vein filled with muscle grafts. 2. Morphological analysis of regeneration. Microsurgery 20: 37-41. (Pubitemid 30053972)
8. Belkas, J.S., M.S. Shoichet, R. Midha (2004) Peripheral nerve regeneration through guidance tubes. Neurol Res 26: 151-160. (Pubitemid 38419098)
9. Best, T.J., S.E. Mackinnon (1994) Peripheral nerve revascularization: A current literature review. J Reconstr Microsurg 10: 193-204. (Pubitemid 24151359)
10. Boyd, J.G., R. Doucette, M.D. Kawaja (2005) Defining the role of olfactory ensheathing cells in facilitating axon remyelination following damage to the spinal cord. Faseb J 19: 694-703. (Pubitemid 40617374)
11. Brandes, G., M. Khayami, C.T. Peck, W. Baumgartner, H. Bugday, K. Wewetzer (2011) Cell surface expression of 27C7 by neonatal rat olfactory ensheathing cells in situ and in vitro is independent of axonal contact. Histochem Cell Biol 135: 397-408.
12. Brockes, J.P., K.L. Fields, M.C. Raff (1979) Studies on cultured rat Schwann cells. 1. Establishment of purified populations from cultures of peripheral nerve. Brain Res 165: 105-118. (Pubitemid 9148699)
13. Bryan, D.J., A.H. Holway, K.K. Wang, A.E. Silva, D.J. Trantolo, D. Wise, I.C. Summerhayes (2000) Influence of glial growth factor and Schwann cells in a bioresorbable guidance channel on peripheral nerve regeneration. Tissue Eng 6: 129-138. (Pubitemid 30227169)
14. Bunge, R.P. (1994) The role of the Schwann cell in trophic support and regeneration. J Neurol 242 (suppl 1): s19-S21. (Pubitemid 24367035)
15. Devon, R., R. Doucette (1992) Olfactory ensheathing cells myelinate dorsal root ganglion neurites. Brain Res 589: 175-179.
16. Doolabh, V.B., M.C. Hertl, S.E. Mackinnon (1996) The role of conduits in nerve repair: A review. Rev Neurosci 7: 47-84. (Pubitemid 26161452)
17. Fansa, H., W. Schneider, G. Keilhoff (2001) Revascularization of tissue-engineered nerve grafts and invasion of macrophages. Tissue Eng 7: 519-524. (Pubitemid 33032375)
18. Franklin, R.J., S.C. Barnett (2000) Olfactory ensheathing cells and CNS regeneration: The sweet smell of success? Neuron 28: 15-18.
19. Franssen, E.H., F.M. De Bree, A.H. Essing, A. Ramon-Cueto, J. Verhaagen (2008) Comparative gene expression profiling of olfactory ensheathing glia and Schwann cells indicates distinct tissue repair characteristics of olfactory ensheathing glia. Glia 56: 1285-1298.
20. Friedman, B., S.S. Scherer, J.S. Rudge, M. Helgren, D. Morrisey, J. McClain, D.Y. Wang, S.J. Wiegand, M.E. Furth, R.M. Lindsay, et al. (1992) Regulation of ciliary neurotrophic factor expression in myelin-related Schwann cells in vivo. Neuron 9: 295-305.
21. Galla, T.J., S.V. Vedecnik, J. Halbgewachs, S. Steinmann, C. Friedrich, G.B. Stark (2004) Fibrin/Schwann cell matrix in poly-epsiloncaprolactone conduits enhances guided nerve regeneration. Int J Artif Organs 27: 127-136. (Pubitemid 38444420)
22. Grant, G.A., R. Goodkin, M. Kliot (1999) Evaluation and surgical management of peripheral nerve problems. Neurosurgery 44: 825-839, discussion 839-840.
23. Guerout, N., C. Duclos, L. Drouot, O. Abramovici, N. Bon-Mardion, Y. Lacoume, L. Jean, O. Boyer, J.P. Marie (2011a) Transplantation of olfactory ensheathing cells promotes axonal regeneration and functional recovery of peripheral nerve lesion in rats. Muscle Nerve 43: 543-551.
24. Guerout, N., A. Paviot, N. Bon-Mardion, C. Duclos, D. Genty, L. Jean, O. Boyer, J.P. Marie (2011b) Co-transplantation of olfactory ensheathing cells from mucosa and bulb origin enhances functional recovery after peripheral nerve lesion. PLoS One 6: E22816.
25. Guntinas-Lichius, O., D.N. Angelov, T.L. Tomov, J. Dramiga, W.F. Neiss, K. Wewetzer (2001) Transplantation of olfactory ensheathing cells stimulates the collateral sprouting from axotomized adult rat facial motoneurons. Exp Neurol 172: 70-80. (Pubitemid 33141155)
26. Guntinas-Lichius, O., K. Wewetzer, T.L. Tomov, N. Azzolin, S. Kazemi, M. Streppel, W.F. Neiss, D.N. Angelov (2002) Transplantation of olfactory mucosa minimizes axonal branching and promotes the recovery of vibrissae motor performance after facial nerve repair in rats. J Neurosci 22: 7121-7131. (Pubitemid 35379167)
27. Hobson, M.I., R. Brown, C.J. Green, G. Terenghi (1997) Inter-relationships between angiogenesis and nerve regeneration: A histochemical study. Br J Plast Surg 50: 125-131. (Pubitemid 27107462)
28. Hobson, M.I., C.J. Green, G. Terenghi (2000) VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy. J Anat 197: 591-605. (Pubitemid 32051540)
29. Hood, B., H.B. Levene, A.D. Levi (2009) Transplantation of autologous Schwann cells for the repair of segmental peripheral nerve defects. Neurosurg Focus 26: e4.
30. Horch, R.E., H. Bannasch, J. Kopp, C. Andree, G.B. Stark (1998) Single-cell suspensions of cultured human keratinocytes in fibrin-glue reconstitute the epidermis. Cell Transplant 7: 309-317. (Pubitemid 28280859)
31. Imaizumi, T., K.L. Lankford, J.D. Kocsis (2000) Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res 854: 70-78. (Pubitemid 30067662)
32. Kalbermatten, D.F., P.J. Kingham, D. Mahay, C. Mantovani, J. Pettersson, W. Raffoul, H. Balcin, G. Pierer, G. Terenghi (2008) Fibrin matrix for suspension of regenerative cells in an artificial nerve conduit. J Plast Reconstr Aesthet Surg 61: 669-675. (Pubitemid 351680445)
33. Kim, D.H., S.E. Connolly, D.G. Kline, R.M. Voorhies, A. Smith, M. Powell, T. Yoes, J.K. Daniloff (1994) Labeled Schwann cell transplants versus sural nerve grafts in nerve repair. J Neurosurg 80: 254-260. (Pubitemid 24036496)
34. Lakatos, A., R.J. Franklin, S.C. Barnett (2000) Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 32: 214-225.
35. Lin, H., F. Liu, C. Zhang, Z. Zhang, Z. Kong, X. Zhang, R.M. Hoffman (2011) Characterization of nerve conduits seeded with neurons and Schwann cells derived from hair follicle neural crest stem cells. Tissue Eng Part A 17: 1691-1698.
36. Lundborg, G. (1982) Regeneration after peripheral nerve injury - a biological and clinical problem. Lakartidningen 79: 2013-2017. (Pubitemid 12128566)
37. Mackinnon, S.E., A.L. Dellon (1990) A study of nerve regeneration across synthetic (Maxon) and biologic (collagen) nerve conduits for nerve gaps up to 5 cm in the primate. J Reconstr Microsurg 6: 117-121. (Pubitemid 20171339)
38. Meek, M.F., J.H. Coert (2008) US Food and Drug Administration/Conformit Europeapproved absorbable nerve conduits for clinical repair of peripheral and cranial nerves. Ann Plast Surg 60: 466-472.
39. Meyer, M., I. Matsuoka, C. Wetmore, L. Olson, H. Thoenen (1992) Enhanced synthesis of brainderived neurotrophic factor in the lesioned peripheral nerve: Different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119: 45-54.
40. Penna, V., B. Munder, G.B. Stark, E.M. Lang (2011) An in vivo engineered nerve conduit - fabrication and experimental study in rats. Microsurgery 31: 395-400.
41. Penna, V., G.B. Stark, E.M. Lang (2012) Longterm evaluation of the biogenic conduit for nerve gap bridging. Microsurgery, accepted.
42. Radtke, C., A.A. Aizer, S.K. Agulian, K.L. Lankford, P.M. Vogt, J.D. Kocsis (2009a) Transplantation of olfactory ensheathing cells enhances peripheral nerve regeneration after microsurgical nerve repair. Brain Res 1254: 10-17.
43. Radtke, C., Y. Akiyama, J. Brokaw, K.L. Lankford, K. Wewetzer, W.L. Fodor, J.D. Kocsis (2004) Remyelination of the nonhuman primate spinal cord by transplantation of Htransferase transgenic adult pig olfactory ensheathing cells. FASEB J 18: 335-337.
44. Radtke, C., J.D. Kocsis, P.M. Vogt (2009b) Chapter 22: Transplantation of olfactory ensheathing cells for peripheral nerve regeneration. Int Rev Neurobiol 87: 405-415.
45. Radtke, C., K.L. Lankford, K. Wewetzer, T. Imaizumi, W.L. Fodor, J.D. Kocsis (2010) Impaired spinal cord remyelination by longterm cultured adult porcine olfactory ensheathing cells correlates with altered in vitro phenotypic properties. Xenotransplantation 17: 71-80.
46. Radtke, C., K. Wewetzer (2009) Translating basic research into clinical practice or what else do we have to learn about olfactory ensheathing cells? Neurosci Lett 456: 133-136.
47. Radtke, C., K. Wewetzer, K. Reimers, P.M. Vogt (2011) Transplantation of olfactory ensheathing cells as adjunct cell therapy for peripheral nerve injury. Cell Transplant 20: 145-152.
48. Ramon-Cueto, A., J. Avila (1998) Olfactory ensheathing glia: Properties and function. Brain Res Bull 46: 175-187. (Pubitemid 28293162)
49. Rende, M., D. Muir, E. Ruoslahti, T. Hagg, S. Varon, M. Manthorpe (1992) Immunolocalization of ciliary neuronotrophic factor in adult rat sciatic nerve. Glia 5: 25-32.
50. Roet, K.C., K. Bossers, E.H. Franssen, M.J. Ruitenberg, J. Verhaagen (2011) A meta-analysis of microarray-based gene expression studies of olfactory bulb-derived olfactory ensheathing cells. Exp Neurol 229: 10-45.
51. Sasaki, M., K.L. Lankford, M. Zemedkun, J.D. Kocsis (2004) Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J Neurosci 24: 8485-8493. (Pubitemid 39313771)
52. Schroder, J.M., R. May, J. Weis (1993) Perineurial cells are the first to traverse gaps of peripheral nerves in silicone tubes. Clin Neurol Neurosurg 95 (suppl): s78-S83. (Pubitemid 23091677)
53. Sinis, N., H.E. Schaller, S.T. Becker, B. Schlosshauer, M. Doser, H. Roesner, S. Oberhoffner, H.W. Muller, M. Haerle (2007) Long nerve gaps limit the regenerative potential of bioartificial nerve conduits filled with Schwann cells. Restor Neurol Neurosci 25: 131-141. (Pubitemid 47290441)
54. Sinis, N., H.E. Schaller, C. Schulte-Eversum, B. Schlosshauer, M. Doser, K. Dietz, H. Rosner, H.W. Muller, M. Haerle (2005) Nerve regeneration across a 2-cm gap in the rat median nerve using a resorbable nerve conduit filled with Schwann cells. J Neurosurg 103: 1067-1076. (Pubitemid 43194556)
55. Smith, P.M., F.J. Sim, S.C. Barnett, R.J. Franklin (2001) SCIP/Oct-6, Krox-20, and desert hedgehog mRNA expression during CNS remyelination by transplanted olfactory ensheathing cells. Glia 36: 342-353. (Pubitemid 34010062)
56. Takami, T., M. Oudega, M.L. Bates, P.M. Wood, N. Kleitman, M.B. Bunge (2002) Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22: 6670-6681. (Pubitemid 35386423)
57. Tarlov, I.M., J.A. Epstein (1945) Nerve grafts: The importance of an adequate blood supply. Brain 68: 49-71.
58. Terzis, J.K., T.G. Skoulis, P.N. Soucacos (1995) Vascularized nerve grafts. A review. Int Angiol 14: 264-277.
59. Terzis, J.K., D.D. Sun, P.K. Thanos (1997) Historical and basic science review: Past, present, and future of nerve repair. J Reconstr Microsurg 13: 215-225. (Pubitemid 127795161)
60. Varejao, A.S., A.M. Cabrita, M.F. Meek, M. Fornaro, S. Geuna, M.G. Giacobini-Robecchi (2003) Morphology of nerve fiber regeneration along a biodegradable poly (DLLAepsilon-CL) nerve guide filled with fresh skeletal muscle. Microsurgery 23: 338-345. (Pubitemid 37093601)
61. Verdú, E., X. Navarro, G. Gudino-Cabrera, F.J. Rodriguez, D. Ceballos, A. Valero, M. Nieto-Sampedro (1999) Olfactory bulb ensheathing cells enhance peripheral nerve regeneration. Neuroreport 10: 1097-1101. (Pubitemid 29317995)
62. Wewetzer, K., G. Brandes (2006) Axonal signalling and the making of olfactory ensheathing cells: A hypothesis. Neuron Glia Biol 2: 217-224. (Pubitemid 46360169)
63. Wewetzer, K., C. Grothe, P. Claus (2001) In vitro expression and regulation of ciliary neurotrophic factor and its alpha receptor subunit in neonatal rat olfactory ensheathing cells. Neurosci Lett 306: 165-168. (Pubitemid 32530825)
64. Wewetzer, K., C. Heiniger, B. Seilheimer (1996) An improved cell-ELISA for the differential screening of antibodies against cell surface molecules of viable adherent Schwann cells. J Immunol Methods 191: 171-178. (Pubitemid 26173519)
65. Wewetzer, K., C. Radtke, J. Kocsis, W. Baumgartner (2011) Species-specific control of cellular proliferation and the impact of large animal models for the use of olfactory ensheathing cells and Schwann cells in spinal cord repair. Exp Neurol 229: 80-87.
66. Wewetzer, K., E. Verdú, D.N. Angelov, X. Navarro (2002) Olfactory ensheathing glia and Schwann cells: Two of a kind? Cell Tissue Res 309: 337-345. (Pubitemid 34994871)
67. Widenfalk, J., K. Lundstromer, M. Jubran, S. Brene, L. Olson (2001) Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 21: 3457-3475. (Pubitemid 32422810)
68. Woodhall, E., A.K. West, M.I. Chuah (2001) Cultured olfactory ensheathing cells express nerve growth factor, brain-derived neurotrophic factor, glia cell line-derived neurotrophic factor and their receptors. Brain Res Mol Brain Res 88: 203-213. (Pubitemid 32274278)