Transplantation of olfactory ensheathing cells as adjunct cell therapy for peripheral nerve injury

Cell Transplantation

Volumn 20, Issue 2, 2011, Pages 145-152

  Radtke, Christine ^a   Wewetzer, Konstantin ^a,b,c   Reimers, Kerstin ^a   Vogt, Peter M ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^c CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

Cell expansion; Cell transplantation; Olfactory ensheathing cells (OECs); Regeneration; Remyelination; Wallerian degeneration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ADIPOSE TISSUE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; ELECTROSTIMULATION; HUMAN; MESENCHYMAL STEM CELL; NERVE FIBER REGENERATION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NOSE MUCOSA; OLFACTORY BULB; OLFACTORY ENSHEATHING CELL; OLFACTORY EPITHELIUM; PERIPHERAL NERVE INJURY; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; REVIEW; SCHWANN CELL;

ANIMALS; CELL TRANSPLANTATION; HUMANS; NERVE REGENERATION; OLFACTORY BULB; PERIPHERAL NERVES; WOUND HEALING;

WALLERIA;

EID: 79955432527     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X522081     Document Type: Review

References (85)

1. Amir, R.; Devor, M. Ongoing activity in neuroma afferents bearing retrograde sprouts. Brain Res. 630: 283-288; 1993.
2. Angelov, D. N.; Guntinas-Lichius, O.; Wewetzer, K.; Neiss, W. F.; Streppel, M. Axonal branching and recovery of coordinated muscle activity after transection of the facial nerve in adult rats. Adv. Anat. Embryol. Cell Biol. 180: 1-130; 2005.
3. Bacsi, A. M.; Kiernan, M. C. Changes in axonal excitability and burst pattern behaviour in synkinesis. J. Clin. Neurosci. 15: 1288-1290; 2008.
4. Bock, P.; Beineke, A.; Techangamsuwan, S.; Baumgärtner, W.; Wewetzer, K. Differential expression of HNK-1 and p75(NTR) in adult canine Schwann cells and olfactory ensheathing cells in situ but not in vitro. J. Comp. Neurol. 505: 572-585; 2007.
5. Bovolenta, P.; Wandosell, F.; Nieto-Sampedro, M. CNS glial scar tissue: A source of molecules which inhibit central neurite outgrowth. Prog. Brain Res. 94: 367-379; 1992.
6. Bretzner, F.; Liu, J.; Roskams, A. J.; Tetzlaff, W. Undesired effects of combinatorial treatment for spinal cord injury: Transplantation of olfactory ensheathing cells and BDNF infusion to the red nucleus. Eur. J. Neurosci. 28: 1795-1807; 2008.
7. Brösamle, C.; Halpern, M. E. Nogo-Nogo receptor signalling in PNS axon outgrowth and pathfinding. Mol. Cell. Neurosci. 40: 401-409; 2009.
8. Bunge, M. B. Novel combination strategies to repair the injured mammalian spinal cord. J. Spinal Cord Med. 31: 262-269; 2008.
9. Carr, V. M.; Farbman, A. I. Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp. Neurol. 115: 55-59; 1992.
10. Chen, L.; Huang, H.; Xi, H.; Xie, Z.; Liu, R.; Jiang, Z.; Zhang, F.; Liu, Y.; Chen, D.; Wang, Q.; Wang, H.; Ren, Y.; Zhou, C. Intracranial transplant of olfactory ensheathing cells in children and adolescents with cerebral palsy: A randomized controlled clinical trial. Cell Transplant. 19: 185-191; 2010.
11. Choi, D.; Raisman, G. Disorganization of the facial nucleus after nerve lesioning and regeneration in the rat: Effects of transplanting candidate reparative cells to the site of injury. Neurosurgery 56: 1093-1100; 2005.
12. Deumens, R.; Koopmans, G. C.; Lemmens, M.; Mollers, S.; Honig, W. M.; Steinbusch, H. W.; Brook, G.; Joosten, E. A. Neurite outgrowth promoting effects of enriched and mixed OEC/ONF cultures. Neurosci. Lett. 397: 20-24; 2006.
13. Devon, R.; Doucette, R. Olfactory ensheathing cells myelinate dorsal root ganglion neurites. Brain Res. 589: 175-179; 1992.
14. Devor, M. Response of nerves to injury in relation to neuropathic pain. In: McMahon, S. L.; Koltzenburg, M., eds. Wall and Melzack's textbook of pain, 5th ed. London, UK: Churchill Livingstone; 2006: 905-927.
15. Dombrowski, M. A.; Sasaki, M.; Lankford, K. L.; Kocsis, J. D.; Radtke, C. Myelination and nodal formation of regenerated peripheral nerve fibers following transplantation of acutely prepared olfactory ensheathing cells. Brain Res. 1125: 1-8; 2006.
16. Féron, F.; Perry, C.; Cochrane, J.; Licina, P.; Nowitzke, A.; Urquhart, S.; Geraghty, T.; Mackay-Sim, A. Autologous olfactory ensheathing cell transplantation in human spinal cord injury. Brain 128: 2951-2960; 2005.
17. Fouad, K.; Schnell, L.; Bunge, M. B.; Schwab, M. E.; Liebscher, T.; Pearse, D. D. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J. Neurosci. 25: 1169-1178; 2005.
18. Franklin, R. J.; Barnett, S. C. Do olfactory glia have advantages over Schwann cells for CNS repair? J. Neurosci. Res. 50: 665-672; 1997.
19. Fu, S. Y.; Gordon, T. Contributing factors to poor functional recovery after delayed nerve repair: Prolonged axotomy. J. Neurosci. 15: 3876-3885; 1995.
20. Fu, S. Y.; Gordon, T. The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 14: 67-116; 1997.
21. Furey, M.; Midha, R.; Xu, Q. B.; Belkas, J.; Gordon, T. Prolonged target deprivation reduces the capacity of injured motoneurons to regenerate. Neurosurgery 60: 723-732; 2007.
22. García-Escudero, V.; Garcia-Gomez, A.; Gargini, R.; Martin-Bermejo, M. J.; Langa, E.; de Yebenes, J. G.; Delicado, A.; Avila, J.; Moreno-Flores, M. T.; Lim, F. Prevention of senescence progression in reversibly immortalized human ensheathing glia permits their survival after deimmortalization. Mol. Ther. 18: 394-403; 2010.
23. Goméz, V. M.; Averill, S.; King, V.; Yang, Q.; Doncel Pérez, E.; Chacón, S. C.; Ward, R.; Nieto-Sampedro, M.; Priestley, J.; Taylor, J. Transplantation of olfactory ensheathing cells fails to promote significant axonal regeneration from dorsal roots into the rat cervical cord. J. Neurocytol. 32: 53-70; 2003.
24. Goodrum, J. F.; Bouldin, T. W. The cell biology of myelin degeneration and regeneration in the peripheral nervous system. J. Neuropathol. Exp. Neurol. 55: 943-953; 1996.
25. Gordon, T.; Amirjani, N.; Edwards, D. C.; Chan, K. M. Brief post-surgical electrical stimulation accelerates axon regeneration and muscle reinnervation without affecting the functional measures in carpal tunnel syndrome patients. Exp. Neurol. 223: 192-202; 2010.
26. Grant, G. A.; Goodkin, R.; Kliot, M. Evaluation and surgical management of peripheral nerve problems. Neurosurgery 44: 825-840; 1999.
27. Graziadei, P. P.; Graziadei, G. A. Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J. Neurocytol. 8: 1-18; 1979.
28. Guntinas-Lichius, O.; Angelov, D. N.; Tomov, T. L.; Dramiga, J.; Neiss, W. F.; Wewetzer, K. Transplantation of olfactory ensheathing cells stimulates the collateral sprouting from axotomized adult rat facial motoneurons. Exp. Neurol. 172: 70-80; 2001.
29. Guntinas-Lichius, O.; Wewetzer, K.; Tomov, T. L.; Azzolin, N.; Kazemi, S.; Streppel, M.; Neiss, W. F.; Angelov, D. N. 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; 2002.
30. Hofstetter, C. P.; Holmström, N. A.; Lilja, J. A.; Schweinhardt, P.; Hao, J.; Spenger, C.; Wiesenfeld-Hallin, Z.; Kurpad, S. N.; Frisen, J.; Olson, L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat. Neurosci. 8: 346-353; 2005.
31. Huang, H.; Chen, L.; Wang, H.; Xiu, B.; Li, B.; Wang, R.; Zhang, J.; Zhang, F.; Gu, Z.; Li, Y.; Song, Y.; Hao, W.; Pang, S.; Sun, J. Influence of patients' age on functional recovery after transplantation of olfactory ensheathing cells into injured spinal cord injury. Chin. Med. J. (Engl.). 116: 1488-1491; 2003.
32. Ibrahim, A. G.; Kirkwood, P. A.; Raisman, G.; Li, Y. Restoration of hand function in a rat model of repair of brachial plexus injury. Brain 132: 1268-1276; 2009.
33. Ibrahim, A.; Li, Y.; Li, D.; Raisman, G.; El Masry, W. S. Olfactory ensheathing cells: Ripples of an incoming tide? Lancet Neurol. 5: 453-457; 2006.
34. Imaizumi, T.; Lankford, K. L.; Kocsis, J. D. Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res. 854: 70-78; 2000.
35. Ito, D.; Ibanez, C.; Ogawa, H.; Franklin, R. J.; Jeffery, N. D. Comparison of cell populations derived from canine olfactory bulb and olfactory mucosal cultures. Am. J. Vet. Res. 67: 1050-1056; 2006.
36. Jacobs, J. J.; Kieboom, K.; Marino, S.; DePinho, R. A.; van Lohuizen, M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168; 1999.
37. Johnson, Jr., E. M.; Taniuchi, M.; DiStefano, P. S. Expression and possible function of nerve growth factor receptors on Schwann cells. Trends Neurosci. 11: 299-304; 1988.
38. Klinge, P.; Vafa, M. A.; Brinker, T.; Brandis, A.; Walter, G. F.; Stieglitz, T.; Samii, M.; Wewetzer, K. Immunohistochemical characterization of axonal sprouting and reactive tissue changes after long-term implantation of a polyimide sieve electrode to the transected adult rat sciatic nerve. Biomaterials 22: 2333-2343; 2001.
39. Lankford, K. L.; Sasaki, M.; Radtke, C.; Kocsis, J. D. Olfactory ensheathing cells exhibit unique migratory, phagocytic, and myelinating properties in the X-irradiated spinal cord not shared by Schwann cells. Glia 56: 1664-1678; 2008.
40. Li, Y.; Carlstedt, T.; Berthold, C. H.; Raisman, G. Interaction of transplanted olfactory-ensheathing cells and host astrocytic processes provides a bridge for axons to regenerate across the dorsal root entry zone. Exp. Neurol. 188: 300-308; 2004.
41. Li, Y.; Field, P. M.; Raisman, G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277: 2000-2002; 1997.
42. Li, Y.; Field, P. M.; Raisman, G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J. Neurosci. 18: 10514-10524; 1998.
43. Li, Y.; McIntosh, K.; Chen, J.; Zhang, C.; Gao, Q.; Borneman, J.; Raginski, K.; Mitchell, J.; Shen, L.; Zhang, J.; Lu, D.; Chopp, M. Allogeneic bone marrow stromal cells promote glial-axonal remodeling without immunologic sensitization after stroke in rats. Exp. Neurol. 198: 313-325; 2006.
44. Li, Y.; Yamamoto, M.; Raisman, G.; Choi, D.; Carlstedt, T. An experimental model of ventral root repair showing the benficial effect of transplanted olfactory ensheathing cells. Neurosurgery 60: 734-740; 2007.
45. Lim, F.; Martin-Bermejo, M. J.; Garcia-Escudero, V.; Gallego-Hernandez, M. T.; Garcia-Gomez, A.; Rabano, A.; Diaz-Nido, J.; Avila, J.; Moreno-Flores, M. T. Reversibly immortalized human olfactory ensheathing glia from an elderly donor maintain neuroregenerative capacity. Glia 58: 546-558; 2010.
46. Lima, C.; Pratas-Vital, J.; Escada, P.; Hasse-Ferreira, A.; Capucho, C.; Peduzzi, J. D. Olfactory mucosa autografts in human spinal cord injury: A pilot clinical study. J. Spinal Cord Med. 29: 191-206; 2006.
47. Liuzzi, F. J.; Lasek, R. J. Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway. Science 237: 642-645; 1987.
48. López-Vales, R.; García-Alías, G.; Forés, J.; Navarro, X.; Verdú, E. Increased expression of cyclo-oxygenase 2 and vascular endothelial growth factor in lesioned spinal cord by transplanted olfactory ensheathing cells. J. Neuro-trauma 21: 1031-1043; 2004.
49. Ma, Y. H.; Zhang, Y.; Cao, L.; Su, J. C.; Wang, Z. W.; Xu, A. B.; Zhang, S. C. Effect of neurotrophin-3 genetically modified olfactory ensheathing cells transplantation on spinal cord injury. Cell Transplant. 19: 167-177; 2010.
50. Mackay-Sim, A.; Feíron, F.; Cochrane, J.; Bassingthwaighte, L.; Bayliss, C.; Davies, W.; Fronek, P.; Gray, C.; Kerr, G.; Licina, P.; Nowitzke, A.; Perry, C.; Silburn, P. A.; Urquhart, S.; Geraghty, T. Autologous olfactory ensheathing cell transplantation in human paraplegia: A 3-year clinical trial. Brain 131: 2376-2386; 2008.
51. Marshall, C. T.; Lu, C.; Winstead, W.; Zhang, X.; Xiao, M.; Harding, G.; Klueber, K. M.; Roisen, F. J. The therapeutic potential of human olfactory-derived stem cells. Histol. Histopathol. 21: 633-643; 2006.
52. Moulton, D. G. Dynamics of cell populations in the olfactory epithelium. Ann. NY Acad. Sci. 237: 52-61; 1974.
53. Navarro, X.; Valero, A.; Gudiño, G.; Forés, J.; Rodríguez, F. J.; Verdú, E.; Pascual, R.; Cuadras, J.; Nieto-Sampedro, M. Ensheathing glia transplants promote dorsal root regeneration and spinal reflex restitution after multiple lumbar rhizotomy. Ann. Neurol. 45: 207-215; 1999.
54. Pearse, D. D.; Sanchez, A. R.; Pereira, F. C.; Andrade, C. M.; Puzis, R.; Pressman, Y.; Golden, K.; Kitay, B. M.; Blits, B.; Wood, P. M.; Bunge, M. B. Transplantation of Schwann cells and/or olfactory ensheathing glia into the contused spinal cord: Survival, migration, axon association, and functional recovery. Glia 55: 976-1000; 2007.
55. Plant, G. W.; Currier, P. F.; Cuervo, E. P.; Bates, M. L.; Pressman, Y.; Bunge, M. B.; Wood, P. M. Purified adult ensheathing glia fail to myelinate axons under culture conditions that enable Schwann cells to form myelin. J. Neurosci. 22: 6083-6091; 2002.
56. Radtke, C.; Aizer, A. A.; Agulian, S. K.; Lankford, K. L.; Vogt, P. M.; Kocsis, J. D. Transplantation of olfactory ensheathing cells enhances peripheral nerve regeneration after microsurgical nerve repair. Brain Res. 1254: 10-17; 2009.
57. Radtke, C.; Akiyama, Y.; Lankford, K. L.; Vogt, P. M.; Krause, D. S.; Kocsis, J. D. Integration of engrafted Schwann cells into injured peripheral nerve: Axonal association and nodal formation on regenerated axons. Neurosci. Lett. 387: 85-89; 2005.
58. Radtke, C.; Kocsis, J. D.; Vogt, P. M. Transplantation of olfactory ensheathing cells for peripheral nerve regeneration. Int. Rev. Neurobiol. 87: 405-415; 2009.
59. Radtke, C.; Lankford, K. L.; Wewetzer, K.; Imaizumi, T.; Fodor, W.; Kocsis, J. D. Impaired spinal cord remyelination by long term cultured adult porcine olfactory ensheathing cells correlates with altered in vitro phenotypic properties. Xenotransplantation 17: 71-80; 2010.
60. Radtke, C.; Schmitz, B.; Spies, M.; Kocsis, J. D.; Vogt, P. M. Peripheral glial cell differentiation from neurospheres derived from adipose mesenchymal stem cells. Int. J. Dev. Neurosci. 27: 817-823; 2009.
61. Radtke, C.; Vogt, P. M. Peripheral nerve regeneration: A current perspective. Eplasty 9: e47; 2009.
62. Radtke, C.; Vogt, P. M.; Devor, M.; Kocsis, J. D. Keratinocytes acting on injured afferents induce extreme neuronal hyperexcitability and chronic pain. Pain 148: 94-102; 2010.
63. Radtke, C.; Wewetzer, K. Translating basic research into clinical practice or what else do we have to learn about olfactory ensheathing cells? Neurosci. Lett. 456: 133-136; 2009.
64. Raisman, G. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14: 237-254; 1985.
65. Raisman, G.; Li, Y. Repair of neural pathways by olfactory ensheathing cells. Nat. Rev. Neurosci. 8: 312-319; 2007.
66. Ramer, L. M.; Au, E.; Richter, M. W.; Liu, J.; Tetzlaff, W.; Roskams, A. J. Peripheral olfactory ensheathing cells reduce scar and cavity formation and promote regeneration after spinal cord injury. J. Comp. Neurol. 473: 1-15; 2004.
67. Ramón-Cueto, A.; Nieto-Sampedro, M. Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp. Neurol. 127: 232-244; 1994.
68. Ramón-Cueto, A.; Plant, G. W.; Avila, J.; Bunge, M. B. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci. 18: 3803-3815; 1998.
69. Riddell, J. S.; Enriquez-Denton, M.; Toft, A.; Fairless, R.; Barnett, S. C. Olfactory ensheathing cell grafts have minimal influence on regeneration at the dorsal root entry zone following rhizotomy. Glia 47: 150-167; 2004.
70. Rudge, J. S.; Silver, J. Inhibition of neurite outgrowth on astroglial scars in vitro. J. Neurosci. 10: 3594-3603; 1990.
71. Sasaki, M.; Black, J. A.; Lankford, K. L.; Tokuno, H. A.; Waxman, S. G.; Kocsis, J. D. Molecular reconstruction of nodes of Ranvier after remyelination by transplanted olfactory ensheathing cells in the demyelinated spinal cord. J. Neurosci. 26: 1803-1812; 2006.
72. Sasaki, M.; Lankford, K. L.; Zemedkun, M.; Kocsis, J. D. Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J. Neurosci. 24: 8485-8493; 2004.
73. Sasaki, M.; Radtke, C.; Tan, A. M.; Zhao, P.; Hamada, H.; Houkin, K.; Honmou, O.; Kocsis, J. D. BDNF-hypersecreting human mesenchymal stem cells promote functional recovery, axonal sprouting, and protection of corticospinal neurons after spinal cord injury. J. Neurosci. 29: 14932-14941; 2009.
74. NTR prevents spontaneous sensory reinnervation of the adult spinal cord. Brain 133: 421-432; 2010.
75. Sulaiman, O. A.; Gordon, T. Role of chronic Schwann cell denervation in poor functional recovery after nerve injuries and experimental strategies to combat it. Neurosurgery 65 (Suppl.): 105-114; 2009.
76. Techangamsuwan, S.; Kreutzer, R.; Kreutzer, M.; Imbschweiler, I.; Rohn, K.; Wewetzer, K.; Baumgartner, W. Transfection of adult canine Schwann cells and olfactory ensheathing cells at early and late passage with human TERT differentially affects growth factor responsiveness and in vitro growth. J. Neurosci. Methods 176: 112-120; 2009.
77. Terzis, J. K. Clinical microsurgery of the peripheral nerve: The state of the art. Clin. Plast. Surg. 6: 247-267; 1979.
78. Ubink, R.; Halasz, N.; Zhang, X.; Dagerlind, A.; Hokfelt, T. Neuropeptide tyrosine is expressed in ensheathing cells around the olfactory nerves in the rat olfactory bulb. Neuroscience 60: 709-726; 1994.
79. Verdú, E.; Navarro, X.; Gudiño-Cabrera, G.; Rodríguez, F. J.; Ceballos, D.; Valero, A.; Nieto-Sampedro, M. Olfactory bulb ensheathing cells enhance peripheral nerve regeneration. Neuroreport 10: 1097-1101; 1999.
80. Wang, G.; Ao, Q.; Gong, K.; Gong, Y.; Zhang, X. Synergistic effect of neural stem cells and olfactory ensheathing cells on repair of adult rat spinal cord injury. Cell Transplant. 19(10): 1325-1337; 2010.
81. Wewetzer, K.; Brandes, G. Axonal signalling and the making of olfactory ensheathing cells: A hypothesis. Neuron Glia Biol. 2: 217-224; 2006.
82. Wewetzer, K.; Grothe, C.; Claus, P. In vitro expression and regulation of ciliary neurotrophic factor and its α receptor unit in neonatal rat olfactory ensheathing cells. Neurosci. Lett. 306: 192-193; 2001.
83. Wewetzer, K.; Kern, N.; Ebel, C.; Radtke, C.; Brandes, G. Phagocytosis of O4+ axonal fragments in vitro by p75-neonatal rat olfactory ensheathing cells. Glia 49: 577-587; 2005.
84. Wewetzer, K.; Verdu, E.; Angelov, D. N.; Navarro, X. Olfactory ensheathing glia and Schwann cells: Two of a kind? Cell Tissue Res. 309: 337-345; 2002.
85. Yang, Q. Cellular senescence, telomere recombination and maintenance. Cytogenet. Genome Res. 122: 211-218; 2008.