Clinical application of adult olfactory bulb ensheathing glia for nervous system repair

Experimental Neurology

Volumn 229, Issue 1, 2011, Pages 181-194

  Ramón Cueto, Almudena ^a   Muñoz Quiles, Cintia ^b,c  

^a INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^b Fundación Investigación en Regeneración Del Sistema Nervioso   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Advanced therapy; Cell therapy; Clinical trial; Legislation; Medicinal product; Paraplegia; Regeneration; Spinal cord injury; Transplantation

Indexed keywords

ADULT; AUTOTRANSPLANTATION; CELL CULTURE; CELL ELONGATION; CELL FUNCTION; CELL IMMORTALIZATION; CELL MANIPULATION; CELL TRANSFORMATION; CELL TRANSPLANTATION; CLINICAL EFFECTIVENESS; CONCEPTUAL FRAMEWORK; FEASIBILITY STUDY; FUNCTIONAL ASSESSMENT; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; OLFACTORY ENSHEATHING CELL; OLFACTORY ENSHEATHING CELL TRANSPLANTATION; PATIENT SAFETY; PRIORITY JOURNAL; RELIABILITY; REPRODUCIBILITY; REVIEW; SPINAL CORD INJURY; SPINAL CORD REGENERATION; TISSUE ENGINEERING; VALIDATION STUDY; WOUND HEALING;

AGE FACTORS; ANIMALS; CELLS, CULTURED; HUMANS; NERVE REGENERATION; NEUROGLIA; OLFACTORY BULB; SPINAL CORD INJURIES;

EID: 79955465441     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.10.001     Document Type: Review

References (174)

1. Adams M., Cavanagh J.F. International Campaign for Cures of Spinal Cord Injury Paralysis (ICCP): another step forward for spinal cord injury research. Spinal Cord 2004, 42:273-280.
2. Agrawal A.K., Shukla S., Chaturvedi R.K., Seth K., Srivastava N., Ahmad A., Seth P.K. Olfactory ensheathing cell transplantation restores functional deficits in rat model of Parkinson's disease: a cotransplantation approach with fetal ventral mesencephalic cells. Neurobiol. Dis. 2004, 16:516-526.
3. Akiyama Y., Lankford K., Radtke C., Greer C.A., Kocsis J.D. Remyelination of spinal cord axons by olfactory ensheathing cells and Schwann cells derived from a transgenic rat expressing alkaline phosphatase marker gene. Neuron Glia Biol. 2004, 1:47-55.
4. Amemori T., Jendelova P., Ruzickova K., Arboleda D., Sykova E. Co-transplantation of olfactory ensheathing glia and mesenchymal stromal cells does not have synergistic effects after spinal cord injury in the rat. Cytotherapy 2010, 12:212-225.
5. Andrews M.R., Stelzner D.J. Modification of the regenerative response of dorsal column axons by olfactory ensheathing cells or peripheral axotomy in adult rat. Exp. Neurol. 2004, 190:311-327.
6. Andrews M.R., Stelzner D.J. Evaluation of olfactory ensheathing and Schwann cells after implantation into a dorsal injury of adult rat spinal cord. J. Neurotrauma 2007, 24:1773-1792.
7. Babiarz, J., Kane-Goldsmith, N., Basak, S., Liu, K., Young, W., Grumet, M., 2011. Juvenile and adult olfactory ensheathing cells bundle and myelinate dorsal root ganglion axons in culture. Exp. Neurol. 229, 72--79.
8. Barakat D.J., Gaglani S.M., Neravetla S.R., Sanchez A.R., Andrade C.M., Pressman Y., Puzis R., Garg M.S., Bunge M.B., Pearse D.D. Survival, integration, and axon growth support of glia transplanted into the chronically contused spinal cord. Cell transplantation 2005, 14:225-240.
9. Barber P.C. Neurogenesis and regeneration in the primary olfactory pathway of mammals. Bibl. Anat. 1982, 23:12-25.
10. Barber P.C., Lindsay R.M. Schwann cells of the olfactory nerves contain glial fibrillary acidic protein and resemble astrocytes. Neuroscience 1982, 7:3077-3090.
11. Barnett S.C., Alexander C.L., Iwashita Y., Gilson J.M., Crowther J., Clark L., Dunn L.T., Papanastassiou V., Kennedy P.G., Franklin R.J. Identification of a human olfactory ensheathing cell that can effect transplant-mediated remyelination of demyelinated CNS axons. Brain 2000, 123:1581-1588.
12. Bianco J.I., Perry C., Harkin D.G., Mackay-Sim A., Feron F. Neurotrophin 3 promotes purification and proliferation of olfactory ensheathing cells from human nose. Glia 2004, 45:111-123.
13. Blanes T. Sobre algunos puntos dudosos de la estructura del bulbo olfatorio. Rev. Trim. Micrograf. 1898, 3:99-127.
14. Bohbot A. Olfactory ensheathing glia transplantation combined with LASERPONCTURE in human spinal cord injury: results measured by electromyography monitoring. Cell transplantation 2010, 19:179-184.
15. Boyd J.G., Lee J., Skihar V., Doucette R., Kawaja M.D. LacZ-expressing olfactory ensheathing cells do not associate with myelinated axons after implantation into the compressed spinal cord. Proc. Natl Acad. Sci. USA 2004, 101:2162-2166.
16. Bretzner F., Liu J., Currie E., Roskams A.J., Tetzlaff W. Undesired effects of a combinatorial treatment for spinal cord injury-transplantation of olfactory ensheathing cells and BDNF infusion to the red nucleus. Eur. J. Neurosci. 2008, 28:1795-1807.
17. Cao L., Liu L., Chen Z.Y., Wang L.M., Ye J.L., Qiu H.Y., Lu C.L., He C. Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 2004, 127:535-549.
18. Carlstedt T. Regenerating axons form nerve terminals at astrocytes. Brain Res. 1985, 347:188-191.
19. Carlstedt T., Cullheim S., Risling M., Ulfhake B. Nerve fibre regeneration across the PNS-CNS interface at the root-spinal cord junction. Brain Res. Bull. 1989, 22:93-102.
20. 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. 2010, 19:185-191.
21. Choi D., Li D., Law S., Powell M., Raisman G. A prospective observational study of the yield of olfactory ensheathing cells cultured from biopsies of septal nasal mucosa. Neurosurgery 2008, 62:1140-1144.
22. Chuah M.I., Choi-Lundberg D., Weston S., Vincent A.J., Chung R.S., Vickers J.C., West A.K. Olfactory ensheathing cells promote collateral axonal branching in the injured adult rat spinal cord. Exp. Neurol. 2004, 185:15-25.
23. Chuah, M.I., Hale, D.M., West, A.K., 2011. Interaction of olfactory ensheathing cells with other cell types in vitro and after transplantation: glial scars and inflammtion. Exp. Neurol. 229, 46--53.
24. Collazos-Castro J.E., Muneton-Gomez V.C., Nieto-Sampedro M. Olfactory glia transplantation into cervical spinal cord contusion injuries. J. Neurosurg. 2005, 3:308-317.
25. Courtine G., Bunge M.B., Fawcett J.W., Grossman R.G., Kaas J.H., Lemon R., Maier I., Martin J., Nudo R.J., Ramon-Cueto A., Rouiller E.M., Schnell L., Wannier T., Schwab M.E., Edgerton V.R. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans?. Nat. Med. 2007, 13:561-566.
26. Deng C., Gorrie C., Hayward I., Elston B., Venn M., Mackay-Sim A., Waite P. Survival and migration of human and rat olfactory ensheathing cells in intact and injured spinal cord. J. Neurosci. Res. 2006, 83:1201-1212.
27. Deng Y.B., Liu Y., Zhu W.B., Bi X.B., Wang Y.Z., Ye M.H., Zhou G.Q. The co-transplantation of human bone marrow stromal cells and embryo olfactory ensheathing cells as a new approach to treat spinal cord injury in a rat model. Cytotherapy 2008, 10:551-564.
28. Deumens R., Koopmans G.C., Honig W.M., Hamers F.P., Maquet V., Jerome R., Steinbusch H.W., Joosten E.A. Olfactory ensheathing cells, olfactory nerve fibroblasts and biomatrices to promote long-distance axon regrowth and functional recovery in the dorsally hemisected adult rat spinal cord. Exp. Neurol. 2006, 200:89-103.
29. Deumens R., Koopmans G.C., Honig W.M., Maquet V., Jerome R., Steinbusch H.W., Joosten E.A. Chronically injured corticospinal axons do not cross large spinal lesion gaps after a multifactorial transplantation strategy using olfactory ensheathing cell/olfactory nerve fibroblast-biomatrix bridges. J. Neurosci. Res. 2006, 83:811-820.
30. Dewar D., Bentley D., Barnett S.C. Implantation of pure cultured olfactory ensheathing cells in an animal model of parkinsonism. Acta Neurochir. 2007, 149:407-414.
31. 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. 2006, 1125:1-8.
32. Doucette J.R. The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat. Rec. 1984, 210:385-391.
33. Doucette R. Glial influences on axonal growth in the primary olfactory system. Glia 1990, 3:433-449.
34. Doucette J.R., Kiernan J.A., Flumerfelt B.A. The re-innervation of olfactory glomeruli following transection of primary olfactory axons in the central or peripheral nervous system. J. Anat. 1983, 137:1-19.
35. Fairless R., Barnett S.C. Olfactory ensheathing cells: their role in central nervous system repair. Int. J. Biochem. Cell Biol. 2005, 37:693-699.
36. Fawcett J.W., Curt A., Steeves J.D., Coleman W.P., Tuszynski M.H., Lammertse D., Bartlett P.F., Blight A.R., Dietz V., Ditunno J., Dobkin B.H., Havton L.A., Ellaway P.H., Fehlings M.G., Privat A., Grossman R., Guest J.D., Kleitman N., Nakamura M., Gaviria M., Short D. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 2007, 45:190-205.
37. Feron 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 2005, 128:2951-2960.
38. 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. 2005, 25:1169-1178.
39. Fouad K., Pearse D.D., Tetzlaff W., Vavrek R. Transplantation and repair: combined cell implantation and chondroitinase delivery prevents deterioration of bladder function in rats with complete spinal cord injury. Spinal Cord 2009, 47:727-732.
40. Franssen E.H., de Bree F.M., Verhaagen J. Olfactory ensheathing glia: their contribution to primary olfactory nervous system regeneration and their regenerative potential following transplantation into the injured spinal cord. Brain Res. Rev. 2007, 56:236-258.
41. Garcia-Alias G., Lopez-Vales R., Fores J., Navarro X., Verdu E. Acute transplantation of olfactory ensheathing cells or Schwann cells promotes recovery after spinal cord injury in the rat. J. Neurosci. Res. 2004, 75:632-641.
42. Giordana M.T., Grifoni S., Votta B., Magistrello M., Vercellino M., Pellerino A., Navone R., Valentini C., Calvo A., Chio A. Neuropathology of olfactory ensheathing cell transplantation into the brain of two amyotrophic lateral sclerosis (ALS) patients. Brain Pathol. (Zurich, Switzerland) 2010, 20:730-737.
43. Golgi C. Sulla fina anatomia del bulbi olfatorii 1875, Reggio-Emilia.
44. Gomez V.M., Averill S., King V., Yang Q., Doncel Perez E., Chacon 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. 2003, 32:53-70.
45. Gorrie C.A., Hayward I., Cameron N., Kailainathan G., Nandapalan N., Sutharsan R., Wang J., Mackay-Sim A., Waite P.M. Effects of human OEC-derived cell transplants in rodent spinal cord contusion injury. Brain Res. 2010, 1337:8-20.
46. 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. 1979, 8:1-18.
47. Graziadei P.P., Monti Graziadei G.A. Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J. Neurocytol. 1980, 9:145-162.
48. Guest J.D., Herrera L., Margitich I., Oliveria M., Marcillo A., Casas C.E. Xenografts of expanded primate olfactory ensheathing glia support transient behavioral recovery that is independent of serotonergic or corticospinal axonal regeneration in nude rats following spinal cord transection. Exp. Neurol. 2008, 212:261-274.
49. 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. 2001, 172:70-80.
50. 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. 2002, 22:7121-7131.
51. Higginson, J.R., Barnett, S.C., 2011. The culture of olfactory ensheathing cells (OECs)-a distinct glial cell type. Exp. Neurol. 229, 2--9.
52. Hill C.E., Beattie M.S., Bresnahan J.C. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp. Neurol. 2001, 171:153-169.
53. Huang H., Chen L., Xi H., Wang H., Zhang J., Zhang F., Liu Y. Fetal olfactory ensheathing cells transplantation in amyotrophic lateral sclerosis patients: a controlled pilot study. Clin. Transplant. 2008, 22:710-718.
54. 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 2009, 132:1268-1276.
55. Ibrahim A.G., Raisman G., Li Y. Permanent loss of fore-paw grasping requires complete deprivation of afferent input from a minimum of four dorsal roots of the rat brachial plexus. Exp. Neurol. 2009, 215:142-145.
56. Imaizumi T., Lankford K.L., Waxman S.G., Greer C.A., Kocsis J.D. Transplanted olfactory ensheathing cells remyelinate and enhance axonal conduction in the demyelinated dorsal columns of the rat spinal cord. J. Neurosci. 1998, 18:6176-6185.
57. Imaizumi T., Lankford K.L., Burton W.V., Fodor W.L., Kocsis J.D. Xenotransplantation of transgenic pig olfactory ensheathing cells promotes axonal regeneration in rat spinal cord. Nat. Biotechnol. 2000, 18:949-953.
58. 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. 2000, 854:70-78.
59. Ito D., Fujita N., Ibanez C., Sasaki N., Franklin R.J., Jeffery N.D. Serum-free medium provides a clinically relevant method to increase olfactory ensheathing cell numbers in olfactory mucosa cell culture. Cell Transplant. 2008, 16:1021-1027.
60. Iwatsuki K., Yoshimine T., Kishima H., Aoki M., Yoshimura K., Ishihara M., Ohnishi Y., Lima C. Transplantation of olfactory mucosa following spinal cord injury promotes recovery in rats. NeuroReport 2008, 19:1249-1252.
61. Jeffery N.D., Lakatos A., Franklin R.J. Autologous olfactory glial cell transplantation is reliable and safe in naturally occurring canine spinal cord injury. J. Neurotrauma 2005, 22:1282-1293.
62. Johansson S., Lee I.H., Olson L., Spenger C. Olfactory ensheathing glial co-grafts improve functional recovery in rats with 6-OHDA lesions. Brain 2005, 128:2961-2976.
63. Kato T., Honmou O., Uede T., Hashi K., Kocsis J.D. Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 2000, 30:209-218.
64. Kawaja M.D., Boyd J.G., Smithson L.J., Jahed A., Doucette R. Technical strategies to isolate olfactory ensheathing cells for intraspinal implantation. J. Neurotrauma 2009, 26:155-177.
65. Keyvan-Fouladi N., Raisman G., Li Y. Functional repair of the corticospinal tract by delayed transplantation of olfactory ensheathing cells in adult rats. J. Neurosci. 2003, 23:9428-9434.
66. Klapka N., Hermanns S., Straten G., Masanneck C., Duis S., Hamers F.P., Muller D., Zuschratter W., Muller H.W. 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. 2005, 22:3047-3058.
67. Komuta Y., Teng X., Yanagisawa H., Sango K., Kawamura K., Kawano H. Expression of transforming growth factor-beta receptors in meningeal fibroblasts of the injured mouse brain. Cell. Mol. Neurobiol. 2010, 30:101-111.
68. Krudewig C., Deschl U., Wewetzer K. Purification and in vitro characterization of adult canine olfactory ensheathing cells. Cell Tissue Res. 2006, 326:687-696.
69. Kubasak M.D., Jindrich D.L., Zhong H., Takeoka A., McFarland K.C., Munoz-Quiles C., Roy R.R., Edgerton V.R., Ramon-Cueto A., Phelps P.E. OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats. Brain 2008, 131:264-276.
70. Lakatos A., Franklin R.J., Barnett S.C. Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 2000, 32:214-225.
71. Lakatos A., Barnett S.C., Franklin R.J. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Exp. Neurol. 2003, 184:237-246.
72. Lakatos A., Smith P.M., Barnett S.C., Franklin R.J. Meningeal cells enhance limited CNS remyelination by transplanted olfactory ensheathing cells. Brain 2003, 126:598-609.
73. Lammertse D., Tuszynski M.H., Steeves J.D., Curt A., Fawcett J.W., Rask C., Ditunno J.F., Fehlings M.G., Guest J.D., Ellaway P.H., Kleitman N., Blight A.R., Dobkin B.H., Grossman R., Katoh H., Privat A., Kalichman M. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: clinical trial design. Spinal Cord 2007, 45:232-242.
74. 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 2008, 56:1664-1678.
75. Lee I.H., Bulte J.W., Schweinhardt P., Douglas T., Trifunovski A., Hofstetter C., Olson L., Spenger C. In vivo magnetic resonance tracking of olfactory ensheathing glia grafted into the rat spinal cord. Exp. Neurol. 2004, 187:509-516.
76. Li Y., Field P.M., Raisman G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 1997, 277:2000-2002.
77. Li Y., Field P.M., Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J. Neurosci. 1998, 18:10514-10524.
78. Li Y., Decherchi P., Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J. Neurosci. 2003, 23:727-731.
79. Li Y., Sauve Y., Li D., Lund R.D., Raisman G. Transplanted olfactory ensheathing cells promote regeneration of cut adult rat optic nerve axons. J. Neurosci. 2003, 23:7783-7788.
80. 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. 2004, 188:300-308.
81. Li Y., Field P.M., Raisman G. Olfactory ensheathing cells and olfactory nerve fibroblasts maintain continuous open channels for regrowth of olfactory nerve fibres. Glia 2005, 52:245-251.
82. Li Y., Yamamoto M., Raisman G., Choi D., Carlstedt T. An experimental model of ventral root repair showing the beneficial effect of transplanting olfactory ensheathing cells. Neurosurgery 2007, 60:734-740.
83. Li B.C., Jiao S.S., Xu C., You H., Chen J.M. PLGA conduit seeded with olfactory ensheathing cells for bridging sciatic nerve defect of rats. J. Biomed. Mater. Res. 2010, 94:769-780.
84. 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 2010, 58:546-558.
85. 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. 2006, 29:191-203.
86. Lindsay S.L., Riddell J.S., Barnett S.C. Olfactory mucosa for transplant-mediated repair: a complex tissue for a complex injury?. Glia 2010, 58:125-134.
87. Liu K., Li Y., Wang H., Jiang X., Zhao Y., Sun D., Chen L., Young W., Huang H., Zhou C. The immunohistochemical characterization of human fetal olfactory bulb and olfactory ensheathing cells in culture as a source for clinical CNS restoration. Anat. Rec. 2010, 293:359-369.
88. Llamusi, M.B., Ruibio, M.P., Ramón-Cueto A., 2011. Telomerase protects adult rodent olfactory ensheathing glia from early senescence. Exp. Neurol. 229, 54--64.
89. Lopez-Vales R., Garcia-Alias G., Fores J., Vela J.M., Navarro X., Verdu E. Transplanted olfactory ensheathing cells modulate the inflammatory response in the injured spinal cord. Neuron Glia Biol. 2004, 1:201-209.
90. Lopez-Vales R., Fores J., Verdu E., Navarro X. Acute and delayed transplantation of olfactory ensheathing cells promote partial recovery after complete transection of the spinal cord. Neurobiol. Dis. 2006, 21:57-68.
91. Lopez-Vales R., Garcia-Alias G., Guzman-Lenis M.S., Fores J., Casas C., Navarro X., Verdu E. Effects of COX-2 and iNOS inhibitors alone or in combination with olfactory ensheathing cell grafts after spinal cord injury. Spine 2006, 31:1100-1106.
92. Lopez-Vales R., Fores J., Navarro X., Verdu E. Olfactory ensheathing glia graft in combination with FK506 administration promote repair after spinal cord injury. Neurobiol. Dis. 2006, 24:443-454.
93. Lopez-Vales R., Fores J., Navarro X., Verdu E. Chronic transplantation of olfactory ensheathing cells promotes partial recovery after complete spinal cord transection in the rat. Glia 2007, 55:303-311.
94. Lu J., Feron F., Ho S.M., Mackay-Sim A., Waite P.M. Transplantation of nasal olfactory tissue promotes partial recovery in paraplegic adult rats. Brain Res. 2001, 889:344-357.
95. 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. 2010, 19:167-177.
96. Mackay-Sim, A., John, J.A., 2011. Olfactory ensheathing cells from the nose: Clinical application in human spinal cord injuries. Exp. Neurol. 229, 174--180.
97. Miedzybrodzki R., Tabakow P., Fortuna W., Czapiga B., Jarmundowicz W. The olfactory bulb and olfactory mucosa obtained from human cadaver donors as a source of olfactory ensheathing cells. Glia 2006, 54:557-565.
98. Morita E., Watanabe Y., Ishimoto M., Nakano T., Kitayama M., Yasui K., Fukada Y., Doi K., Karunaratne A., Murrell W.G., Sutharsan R., Mackay-Sim A., Hata Y., Nakashima K. A novel cell transplantation protocol and its application to an ALS mouse model. Exp. Neurol. 2008, 213:431-438.
99. Munoz-Quiles C., Santos-Benito F.F., Llamusi M.B., Ramon-Cueto A. Chronic spinal injury repair by olfactory bulb ensheathing glia and feasibility for autologous therapy. J. Neuropathol. Exp. Neurol. 2009, 68:1294-1308.
100. Murrell W., Feron F., Wetzig A., Cameron N., Splatt K., Bellette B., Bianco J., Perry C., Lee G., Mackay-Sim A. Multipotent stem cells from adult olfactory mucosa. Dev. Dyn. 2005, 233:496-515.
101. Murrell W., Wetzig A., Donnellan M., Feron F., Burne T., Meedeniya A., Kesby J., Bianco J., Perry C., Silburn P., Mackay-Sim A. Olfactory mucosa is a potential source for autologous stem cell therapy for Parkinson's disease. Stem Cells (Dayton, Ohio) 2008, 26:2183-2192.
102. Nash H.H., Borke R.C., Anders J.J. Ensheathing cells and methylprednisolone promote axonal regeneration and functional recovery in the lesioned adult rat spinal cord. J. Neurosci. 2002, 22:7111-7120.
103. Navarro X., Valero A., Gudino G., Fores J., Rodriguez F.J., Verdu 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. 1999, 45:207-215.
104. Negredo P., Rivero J.L., Gonzalez B., Ramon-Cueto A., Manso R. Slow- and fast-twitch rat hind limb skeletal muscle phenotypes 8months after spinal cord transection and olfactory ensheathing glia transplantation. J. Physiol. 2008, 586:2593-2610.
105. Niclou S.P., Franssen E.H., Ehlert E.M., Taniguchi M., Verhaagen J. Meningeal cell-derived semaphorin 3A inhibits neurite outgrowth. Mol. Cell. Neurosci. 2003, 24:902-912.
106. Novikova, L.N., Lobov, S., Wiberg, M., Novikov, L., 2011. Efficacy of olfactory ensheathing cells to support regeneration after spinal cord injury is influenced by method of culture preparation. Exp. Neurol. 229, 132--142.
107. Othman M., Lu C., Klueber K., Winstead W., Roisen F. Clonal analysis of adult human olfactory neurosphere forming cells. Biotech. Histochem. 2005, 80:189-200.
108. Pascual J.I., Gudino-Cabrera G., Insausti R., Nieto-Sampedro M. Spinal implants of olfactory ensheathing cells promote axon regeneration and bladder activity after bilateral lumbosacral dorsal rhizotomy in the adult rat. J. Urol. 2002, 167:1522-1526.
109. Pearse D.D., Marcillo A.E., Oudega M., Lynch M.P., Wood P.M., Bunge M.B. Transplantation of Schwann cells and olfactory ensheathing glia after spinal cord injury: does pretreatment with methylprednisolone and interleukin-10 enhance recovery?. J. Neurotrauma 2004, 21:1223-1239.
110. 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 2007, 55:976-1000.
111. Perez-Bouza A., Wigley C.B., Nacimiento W., Noth J., Brook G.A. Spontaneous orientation of transplanted olfactory glia influences axonal regeneration. NeuroReport 1998, 9:2971-2975.
112. Piepers S., van den Berg L.H. No benefits from experimental treatment with olfactory ensheathing cells in patients with ALS. Amyotroph. Lateral Scler. 2010, 11:328-330.
113. Pixley S.K. The olfactory nerve contains two populations of glia, identified both in vivo and in vitro. Glia 1992, 5:269-284.
114. Plant G.W., Christensen C.L., Oudega M., Bunge M.B. Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. J. Neurotrauma 2003, 20:1-16.
115. Plant, G.W., Harvey, A.R., Leaver, S.G., Lee, S.V., 2011. Olfactory ensheathing glia: repairing injury to the mammalian visual system. Exp. Neurol. 229, 99--108.
116. Polentes J., Stamegna J.C., Nieto-Sampedro M., Gauthier P. Phrenic rehabilitation and diaphragm recovery after cervical injury and transplantation of olfactory ensheathing cells. Neurobiol. Dis. 2004, 16:638-653.
117. Radtke C., Akiyama Y., Brokaw J., Lankford K.L., Wewetzer K., Fodor W.L., Kocsis J.D. Remyelination of the nonhuman primate spinal cord by transplantation of H-transferase transgenic adult pig olfactory ensheathing cells. FASEB J. 2004, 18:335-337.
118. Radtke C., Sasaki M., Lankford K.L., Vogt P.M., Kocsis J.D. Potential of olfactory ensheathing cells for cell-based therapy in spinal cord injury. J Rehabil. Res. Dev. 2008, 45:141-151.
119. 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. 2009, 1254:10-17.
120. Radtke, C., Wewetzer, K., Reimers, K., Vogt, P.M., 2010. Transplantatioin of olfactory ensheathing cells as adjunct cell-therapy for peripheral nerve injury. Cell Transplant.
121. Raisman G. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 1985, 14:237-254.
122. Raisman G., Li Y. Repair of neural pathways by olfactory ensheathing cells. Nat. Rev. 2007, 8:312-319.
123. Raisman, G., Carlstedt, T., Choi, D., Li, Y., 2011. Clinical prospects for transplantation of OECs in the repair of brachial and lumbosacral plexus injuries: opening a door. Exp. Neurol. 229, 168--173.
124. Ramón y Cajal S. Degeneration and regeneration of the nervous system 1991, Oxford University press, New York.
125. Ramon-Cueto A., Nieto-Sampedro M. Glial cells from adult rat olfactory bulb: immunocytochemical properties of pure cultures of ensheathing cells. Neuroscience 1992, 47:213-220.
126. Ramon-Cueto A., Nieto-Sampedro M. Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp. Neurol. 1994, 127:232-244.
127. Ramon-Cueto A., Valverde F. Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 1995, 14:163-173.
128. Ramon-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. 1998, 18:3803-3815.
129. Ramon-Cueto A., Cordero M.I., Santos-Benito F.F., Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000, 25:425-435.
130. Resnick D.K., Cechvala C.F., Yan Y., Witwer B.P., Sun D., Zhang S. Adult olfactory ensheathing cell transplantation for acute spinal cord injury. J. Neurotrauma 2003, 20:279-285.
131. Richter M.W., Fletcher P.A., Liu J., Tetzlaff W., Roskams A.J. Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J. Neurosci. 2005, 25:10700-10711.
132. Richter M., Westendorf K., Roskams A.J. Culturing olfactory ensheathing cells from the mouse olfactory epithelium. Meth. Mol. Biol. (Clifton NJ) 2008, 438:95-102.
133. 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 2004, 47:150-167.
134. Rubio M.P., Munoz-Quiles C., Ramon-Cueto A. Adult olfactory bulbs from primates provide reliable ensheathing glia for cell therapy. Glia 2008, 56:539-551.
135. Ruitenberg M.J., Plant G.W., Christensen C.L., Blits B., Niclou S.P., Harvey A.R., Boer G.J., Verhaagen J. Viral vector-mediated gene expression in olfactory ensheathing glia implants in the lesioned rat spinal cord. Gene Ther. 2002, 9:135-146.
136. Ruitenberg M.J., Plant G.W., Hamers F.P., Wortel J., Blits B., Dijkhuizen P.A., Gispen W.H., Boer G.J., Verhaagen J. Ex vivo adenoviral vector-mediated neurotrophin gene transfer to olfactory ensheathing glia: effects on rubrospinal tract regeneration, lesion size, and functional recovery after implantation in the injured rat spinal cord. J. Neurosci. 2003, 23:7045-7058.
137. Ruitenberg M.J., Levison D.B., Lee S.V., Verhaagen J., Harvey A.R., Plant G.W. NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration. Brain 2005, 128:839-853.
138. Salehi M., Pasbakhsh P., Soleimani M., Abbasi M., Hasanzadeh G., Modaresi M.H., Sobhani A. Repair of spinal cord injury by co-transplantation of embryonic stem cell-derived motor neuron and olfactory ensheathing cell. Iran. Biomed. J. 2009, 13:125-135.
139. Santos-Benito F.F., Munoz-Quiles C., Ramon-Cueto A. Long-term care of paraplegic laboratory mammals. J. Neurotrauma 2006, 23:521-536.
140. 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. 2004, 24:8485-8493.
141. 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. 2006, 26:1803-1812.
142. Sasaki M., Hains B.C., Lankford K.L., Waxman S.G., Kocsis J.D. Protection of corticospinal tract neurons after dorsal spinal cord transection and engraftment of olfactory ensheathing cells. Glia 2006, 53:352-359.
143. Schneider C.K., Salmikangas P., Jilma B., Flamion B., Todorova L.R., Paphitou A., Haunerova I., Maimets T., Trouvin J.H., Flory E., Tsiftsoglou A., Sarkadi B., Gudmundsson K., O'Donovan M., Migliaccio G., Ancans J., Maciulaitis R., Robert J.L., Samuel A., Ovelgonne J.H., Hystad M., Fal A.M., Lima B.S., Moraru A.S., Turcani P., Zorec R., Ruiz S., Akerblom L., Narayanan G., Kent A., Bignami F., Dickson J.G., Niederwieser D., Figuerola-Santos M.A., Reischl I.G., Beuneu C., Georgiev R., Vassiliou M., Pychova A., Clausen M., Methuen T., Lucas S., Schussler-Lenz M., Kokkas V., Buzas Z., MacAleenan N., Galli M.C., Line A., Gulbinovic J., Berchem G., Fraczek M., Menezes-Ferreira M., Vilceanu N., Hrubisko M., Marinko P., Timon M., Cheng W., Crosbie G.A., Meade N., di Paola M.L., VandenDriessche T., Ljungman P., D'Apote L., Oliver-Diaz O., Buttel I., Celis P. Challenges with advanced therapy medicinal products and how to meet them. Nat. Rev. Drug Discov. 2010, 9:195-201.
144. Shen Y., Qian Y., Zhang H., Zuo B., Lu Z., Fan Z., Zhang P., Zhang F., Zhou C. Guidance of olfactory ensheathing cell growth and migration on electrospun silk fibroin scaffolds. Cell Transplant. 2010, 19:147-157.
145. Shi X., Kang Y., Hu Q., Chen C., Yang L., Wang K., Chen L., Huang H., Zhou C. A long-term observation of olfactory ensheathing cells transplantation to repair white matter and functional recovery in a focal ischemia model in rat. Brain Res. 2010, 1317:257-267.
146. Shukla S., Chaturvedi R.K., Seth K., Roy N.S., Agrawal A.K. Enhanced survival and function of neural stem cells-derived dopaminergic neurons under influence of olfactory ensheathing cells in parkinsonian rats. J. Neurochem. 2009, 109:436-451.
147. Smale K.A., Doucette R., Kawaja M.D. Implantation of olfactory ensheathing cells in the adult rat brain following fimbria-fornix transection. Exp. Neurol. 1996, 137:225-233.
148. Smith P.M., Lakatos A., Barnett S.C., Jeffery N.D., Franklin R.J. Cryopreserved cells isolated from the adult canine olfactory bulb are capable of extensive remyelination following transplantation into the adult rat CNS. Exp. Neurol. 2002, 176:402-406.
149. Srivastava N., Seth K., Khanna V.K., Ansari R.W., Agrawal A.K. Long-term functional restoration by neural progenitor cell transplantation in rat model of cognitive dysfunction: co-transplantation with olfactory ensheathing cells for neurotrophic factor support. Int. J. Dev. Neurosci. 2009, 27:103-110.
150. Steeves J.D., Lammertse D., Curt A., Fawcett J.W., Tuszynski M.H., Ditunno J.F., Ellaway P.H., Fehlings M.G., Guest J.D., Kleitman N., Bartlett P.F., Blight A.R., Dietz V., Dobkin B.H., Grossman R., Short D., Nakamura M., Coleman W.P., Gaviria M., Privat A. Guidelines for the conduct of clinical trials for spinal cord injury (SCI) as developed by the ICCP panel: clinical trial outcome measures. Spinal Cord 2007, 45:206-221.
151. Takami T., Oudega M., Bates M.L., Wood P.M., Kleitman N., Bunge M.B. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J. Neurosci. 2002, 22:6670-6681.
152. Takeoka A., Kubasak M.D., Zhong H., Roy R.R., Phelps P.E. Serotonergic innervation of the caudal spinal stump in rats after complete spinal transection: effect of olfactory ensheathing glia. J. Comp. Neurol. 2009, 515:664-676.
153. Takeoka A., Kubasak M.D., Zhong H., Kaplan J., Roy R.R., Phelps P.E. Noradrenergic innervation of the rat spinal cord caudal to a complete spinal cord transection: effects of olfactory ensheathing glia. Exp. Neurol. 2010, 222:59-69.
154. Tang Z.P., Xie X.W., Shi Y.H., Liu N., Zhu S.Q., Li Z.W., Chen Y. Combined transplantation of neural stem cells and olfactory ensheathing cells improves the motor function of rats with intracerebral hemorrhage. Biomed. Environ. Sci. 2010, 23:62-67.
155. Techangamsuwan S., Imbschweiler I., Kreutzer R., Kreutzer M., Baumgartner W., Wewetzer K. Similar behaviour and primate-like properties of adult canine Schwann cells and olfactory ensheathing cells in long-term culture. Brain Res. 2008, 1240:31-38.
156. 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. Meth. 2009, 176:112-120.
157. Teng X., Nagata I., Li H.P., Kimura-Kuroda J., Sango K., Kawamura K., Raisman G., Kawano H. Regeneration of nigrostriatal dopaminergic axons after transplantation of olfactory ensheathing cells and fibroblasts prevents fibrotic scar formation at the lesion site. J. Neurosci. Res. 2008, 86:3140-3150.
158. Toft A., Scott D.T., Barnett S.C., Riddell J.S. Electrophysiological evidence that olfactory cell transplants improve function after spinal cord injury. Brain 2007, 130:970-984.
159. Tuszynski M.H., Steeves J.D., Fawcett J.W., Lammertse D., Kalichman M., Rask C., Curt A., Ditunno J.F., Fehlings M.G., Guest J.D., Ellaway P.H., Kleitman N., Bartlett P.F., Blight A.R., Dietz V., Dobkin B.H., Grossman R., Privat A. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP Panel: clinical trial inclusion/exclusion criteria and ethics. Spinal Cord 2007, 45:222-231.
160. Valverde F., Lopez-Mascaraque L. Neuroglial arrangements in the olfactory glomeruli of the hedgehog. J. Comp. Neurol. 1991, 307:658-674.
161. Valverde F., Santacana M., Heredia M. Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 1992, 49:255-275.
162. Vavrek R., Pearse D.D., Fouad K. Neuronal populations capable of regeneration following a combined treatment in rats with spinal cord transection. J. Neurotrauma 2007, 24:1667-1673.
163. Velardo M.J., Burger C., Williams P.R., Baker H.V., Lopez M.C., Mareci T.H., White T.E., Muzyczka N., Reier P.J. Patterns of gene expression reveal a temporally orchestrated wound healing response in the injured spinal cord. J. Neurosci. 2004, 24:8562-8576.
164. Verdu E., Navarro X., Gudino-Cabrera G., Rodriguez F.J., Ceballos D., Valero A., Nieto-Sampedro M. Olfactory bulb ensheathing cells enhance peripheral nerve regeneration. NeuroReport 1999, 10:1097-1101.
165. Verdu E., Garcia-Alias G., Fores J., Gudino-Cabrera G., Muneton V.C., Nieto-Sampedro M., Navarro X. Effects of ensheathing cells transplanted into photochemically damaged spinal cord. NeuroReport 2001, 12:2303-2309.
166. Verdu E., Garcia-Alias G., Fores J., Lopez-Vales R., Navarro X. Olfactory ensheathing cells transplanted in lesioned spinal cord prevent loss of spinal cord parenchyma and promote functional recovery. Glia 2003, 42:275-286.
167. Wang B., Han J., Gao Y., Xiao Z., Chen B., Wang X., Zhao W., Dai J. The differentiation of rat adipose-derived stem cells into OEC-like cells on collagen scaffolds by co-culturing with OECs. Neurosci. Lett. 2007, 421:191-196.
168. Wang, G., Ao, Q, Gong, K., Gong, Y., Zhang, X., 2010. Synergistic effect of neural stem cells and olfactory ensheathing cells on repair of adult rat spinal cord injury. Cell Transplant. 19, 1325--1337.
169. Wei Y., Miao X., Xian M., Zhang C., Liu X., Zhao H., Zhan X., Han D. Effects of transplanting olfactory ensheathing cells on recovery of olfactory epithelium after olfactory nerve transection in rats. Med. Sci. Monit. 2008, 14:BR198-BR204.
170. Wewetzer, K., Radtke, C., Kocsis, J., Baumgartner, W., 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.
171. Wu J., Sun T.S., Ren J.X., Wang X.Z. Ex vivo non-viral vector-mediated neurotrophin-3 gene transfer to olfactory ensheathing glia: effects on axonal regeneration and functional recovery after implantation in rats with spinal cord injury. Neurosci. Bull. 2008, 24:57-65.
172. Wu, A., Lauschke, J.L., Gorrie, C.A., Cameron, N., Hayward, Il, Mackay-Sim, A., Waite, P.M., 2011. Delayed olfactory ensheathing cell transplants reduce nociception after dorsal root injury. Exp. Neurol. 229, 143--157.
173. Yamamoto M., Raisman G., Li D., Li Y. Transplanted olfactory mucosal cells restore paw reaching function without regeneration of severed corticospinal tract fibres across the lesion. Brain Res. 2009, 1303:26-31.
174. You, H., Wei, L., Liu, Y., Oudega, M., Jiao, S.S., Feng, S.N., Chen, Y., Chen, J.M., Li, B.C. 2011. Olfactory ensheathing cells enhance Schwann cell-mediated anatomical and functional repair after sciatic nerve injury in adult rats. Exp. Neurol. 229, 158--167.