Repair of central nervous system lesions by transplantation of olfactory ensheathing cells

Handbook of Clinical Neurology

Volumn 109, Issue , 2012, Pages 541-549

  Raisman, Geoffrey ^a   Barnett, S C ^b   Ramón Cueto, Almudena ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84867836595     PISSN: 00729752     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-444-52137-8.00033-4     Document Type: Chapter

References (96)

1. Akiyama Y., Lankford K., Radtke C., et al. 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.
2. Alexander C.L., Fitzgerald U.F., Barnett S.C. Identification of growth factors that promote long-term proliferation of olfactory ensheathing cells and modulate their antigenic phenotype. Glia 2002, 37:349-364.
3. 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.
4. Barnett S.C. Olfactory ensheathing cells: unique glial cell types?. J Neurotrauma 2004, 21:375-382.
5. Barnett S.C., Riddell J.S. Olfactory ensheathing cell transplantation as a strategy for spinal cord repair - what can it achieve?. Nat Clin Pract Neurol 2007, 3:152-161.
6. Barnett S.C., Hutchins A.M., Noble M. Purification of olfactory nerve ensheathing cells from the olfactory bulb. Dev Biol 1993, 155:337-350.
7. Barnett S.C., Alexander C.L., Iwashita Y., et al. Identification of a human olfactory ensheathing cell that can effect transplant-mediated remyelination of demyelinated CNS axons. Brain 2000, 123:1581-1588.
8. Barnett S.C., Thompson R.J., Lakatos A., et al. Gap junctional communication and connexin expression in cultured olfactory ensheathing cells. J Neurosci Res 2001, 65:520-528.
9. Barraud P., Seferiadis A.A., Tyson L.D., et al. Neural crest origin of olfactory ensheathing glia. PNAS 2010, 107:21040-21045.
10. Bashkin P., Doctrow S., Klagsbrun M., et al. Basic fibroblast growth factor binds to subendothelial extracellular matrix and is released by heparitinase and heparin-like molecules. Biochemistry 1989, 28:1737-1743.
11. Blight A.R., Young W. Central axons in injured cat spinal cord recover electrophysiological function following remyelination by Schwann cells. J Neurol Sci 1989, 91:15-34.
12. Cao L., Liu L., Chen Z.Y., et al. Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 2004, 127:535-549.
13. Choi D., Li D., Law S., et al. A prospective observational study of the yield of olfactory ensheathing cells cultured from biopsies of septal nasal mucosa. Neurosurgery 2008, 62:1140-1144.
14. Choi D., Law S., Raisman G., et al. Olfactory ensheathing cells in the nasal mucosa of the rat and human. Br J Neurosurg 2008, 22:301-302.
15. Chuah M.I., Teague R. Basic fibroblast growth factor in the primary olfactory pathway: mitogenic effect on ensheathing cells. Neuroscience 1999, 88:1043-1050.
16. Chuah M.I., West A.K. Cellular and molecular biology of ensheathing cells. Microsc Res Tech 2002, 58:216-227.
17. Courtine G., Bunge M.B., Fawcett J.W., et al. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans?. Nat Med 2007, 13:561-566.
18. David S., Aguayo A.J. Axonal elongation into peripheral nervous system " bridges" after central nervous system injury in adult rats. Science 1981, 214:931-933.
19. Davis J.B., Stroobant P. Platelet-derived growth factors and fibroblast growth factors are mitogens for rat Schwann cells. J Cell Biol 1990, 110:1353-1360.
20. DeCarlos J., Lopez-Marcaraque L., Valverde F. The telencephalic vesicles are innervated by olfactory placode-derived cells: a possible mechanism to induce neocortical development. Neuroscience 1995, 68:1167-1178.
21. Delehedde M., Deudon E., Boilly B., et al. Heparan sulfate proteoglycans play a dual role in regulating fibroblast growth factor-2 mitogenic activity in human breast cancer cells. Exp Cell Res 1996, 229:398-406.
22. Doherty P., Cohen J., Walsh F.S. Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron 1990, 5:209-219.
23. Dombrowski M.A., Sasaki M., Lankford K.L., et al. Myelination and nodal formation of regenerated peripheral nerve fibers following transplantation of acutely prepared olfactory ensheathing cells. Brain Res 2006, 1125:1-8.
24. Doucette R. PNS-CNS transitional zone of the first cranial nerve. J Comp Neurol 1991, 312:451-466.
25. Doucette R. Olfactory ensheathing cells: potential for glial cell transplantation into areas of CNS injury. Histol Histopathol 1995, 10:503-507.
26. Fairless R., Frame M.C., Barnett S.C. N-cadherin differentially determines Schwann cell and olfactory ensheathing cell adhesion and migration responses upon contact with astrocytes. Mol Cell Neurosci 2005, 28:253-263.
27. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res Bull 1999, 49:377-391.
28. Franklin R.J., Gilson J.M., Franceschini I.A., et al. Schwann cell-like myelination following transplantation of an olfactory bulb-ensheathing cell line into areas of demyelination in the adult CNS. Glia 1996, 17:217-224.
29. Franklin R.J., Barnett S.C. Do olfactory glia have advantages over Schwann cells for CNS repair?. J Neurosci Res 1997, 50:665-672.
30. Franklin R.J., Barnett S.C. Olfactory ensheathing cells and CNS regeneration: the sweet smell of success?. Neuron 2000, 28:15-18.
31. 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 Brain Res Rev 2007, 56:236-258.
32. Franssen E.H., De Bree F.M., Essing A.H., et al. Comparative gene expression profiling of olfactory ensheathing glia and Schwann cells indicates distinct tissue repair characteristics of olfactory ensheathing glia. Glia 2008, 56:1285-1298.
33. Graziadei P.P., Monti Graziadei G.A. Neurogenesis and neuron regeneration in the olfactory system of mammals. 3. Deafferentation and reinnervation of the olfactory bulb following section of the fila-olfactoria in rat. J Neurocytol 1980, 9:145-162.
34. Guest J.D., Herrera L., Margitich I., et al. 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.
35. Imaizumi T., Lankford K.L., Waxman S.G., et al. 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.
36. Imaizumi T., Lankford K.L., Burton W.V., et al. Xenotransplantation of transgenic pig olfactory ensheathing cells promotes axonal regeneration in rat spinal cord. Nat Biotechnol 2000, 18:949-953.
37. Iwatsuki K., Yoshimine T., Kishima H., et al. Transplantation of olfactory mucosa following spinal cord injury promotes recovery in rats. Neuroreport 2008, 19:1249-1252.
38. Jessen K.R., Morgan L., Stewart H.J., et al. Three markers of adult non-myelin-forming Schwann cells, 217c (Ran-1), A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Development 1990, 109:91-103.
39. Kato T., Honmou O., Uede T., et al. Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 2000, 30:209-218.
40. Keyvan-Fouladi N., Raisman G., Li Y. Functional repair of the corticosponal tract by delayed transplantation of olfactory ensheathing cells in adult rats. J Neurosci 2003, 23:9428-9434.
41. Kubasak M.D., Jindrich D.L., Zhong H., et al. OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats. Brain 2008, 131:264-276.
42. Kuhlengel K.R., Bunge M.B., Bunge R.P., et al. Implantation of cultured sensory neurons and Schwann cells into lesioned neonatal rat spinal cord. II. Implant characteristics and examination of corticospinal tract growth. J Comp Neurol 1990, 293:74-91.
43. 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.
44. Lakatos A., Smith P.M., Barnett S.C., et al. Meningeal cells enhance limited CNS remyelination by transplanted olfactory ensheathing cells. Brain 2003, 126:598-609.
45. 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.
46. Le Douarin N.M. Cell line segregation during peripheral nervous system ontogeny. Science 1986, 231:1515-1522.
47. Li Y., Field P.M., Raisman G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 1997, 277:2000-2002.
48. 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.
49. 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.
50. López-Vales R., Forés J., Verdú E., et al. Acute and delayed transplantation of olfactory ensheathing cells promote partial recovery after complete transection of the spinal cord. Neurobiol Dis 2006, 21:57-68.
51. Lu J., Feron F., Ho S.M., et al. Transplantation of nasal olfactory tissue promotes partial recovery in paraplegic adult rats. Brain Res 2001, 889:344-357.
52. Lu J., Feron F., Mackay-Sim A., et al. Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain 2002, 125:14-21.
53. Lu P., Yang H., Culbertson M., et al. Olfactory ensheathing cells do not exhibit unique migratory or axonal growth-promoting properties after spinal cord injury. J Neurosci 2006, 26:11120-11130.
54. Lundin L., Larsson H., Kreuger J., et al. Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J Biol Chem 2000, 275:24653-24660.
55. Mackay-Sim A., Féron F., Cochrane J., et al. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 2008, 131:2376-2386.
56. Marin-Padilla M., Amieva M.R. Early neurogenesis of the mouse olfactory nerve: Golgi and electron microscopic studies. J Comp Neurol 1989, 288:339-352.
57. Mirsky R., Woodhoo A., Parkinson D.B., et al. Novel signals controlling embryonic Schwann cell development, myelination and dedifferentiation. J Peripher Nerv Syst 2008, 13:122-135.
58. Mundhenke C., Meyer K., Drew S., et al. Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 receptor binding in breast carcinoma. Am J Pathol 2002, 160:185-194.
59. 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.
60. Norgren R.B., Ratner N., Brackenbury R. Development of olfactory nerve glia defined by a monoclonal antibody specific for Schwann cells. Dev Dyn 1992, 194:231-238.
61. Oudega M., Xu X.M. Schwann cell transplantation for repair of the adult spinal cord. J Neurotrauma 2006, 23:453-467.
62. Plant G.W., Christensen C.L., Oudega M., et al. 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.
63. Pollock G.S., Franceschini I.A., Graham G., et al. Neuregulin is a mitogen and survival factor for olfactory bulb ensheathing cells and an isoform is produced by astrocytes. Eur J Neurosci 1999, 11:769-780.
64. Pringle N.P., Guthrie S., Lumsden A., et al. Dorsal spinal cord neuroepithelium generates astrocytes but not oligodendrocytes. Neuron 1998, 20:883-893.
65. Radtke C., Akiyama Y., Brokaw J., et al. Remyelination of the nonhuman primate spinal cord by transplantation of H-transferase transgenic pig olfactory ensheathing cells. FASEB J 2004, 18:335-337.
66. Raisman G. Neuronal plasticity in the septal nuclei of the adult rat. Brain Res 1969, 14:25-48.
67. Raisman G. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 1985, 14:237-254.
68. Raisman G. Olfactory ensheathing cells - another miracle cure for spinal cord injury?. Nat Rev Neurosci 2001, 2:369-375.
69. Raisman G., Li Y. Repair of neural pathways by olfactory ensheathing cells. Nat Rev Neurosci 2007, 8:312-319.
70. Ramer L.M., Au E., Richter M.W., et al. Peripheral olfactory ensheathing cells reduce scar and cavity formation and promote regeneration after spinal cord injury. J Comp Neurol 2004, 473:1-15.
71. Ramón-Cueto A., Avila J. Olfactory ensheathing glia: properties and function. Brain Res Bull 1998, 46:175-187.
72. Ramón-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.
73. Ramón-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.
74. Ramón-Cueto A., Valverde F. Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 1995, 14:163-173.
75. Ramón-Cueto A., Plant G.W., Avila J., et al. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci 1998, 18:3803-3815.
76. Ramón-Cueto A., Cordero M.I., Santos-Benito F.F., et al. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000, 25:425-435.
77. Richter M.W., Fletcher P.A., Liu J., et al. 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.
78. Rubio M.P., Muñoz-Quiles C., Ramón-Cueto A. Adult olfactory bulbs from primates provide reliable ensheathing glia for cell therapy. Glia 2008, 56:539-551.
79. Ruitenberg M.J., Levison D.B., Lee S.V., et al. NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration. Brain 2005, 128:839-853.
80. Santos-Benito F.F., Muñoz-Quiles C., Ramon-Cueto A. Long-term care of paraplegic laboratory mammals. J Neurotrauma 2006, 23:521-536.
81. Santos-Silva A., Fairless R., Frame M., et al. OECs lack a heparin sulphate proteoglycan that Schwann cells use to induce the astrocyte stress response mediated via FGFR1 activation. J Neurosci 2007, 27:7154-7167.
82. Sasaki M., Lankford K.L., Zemedkun, et al. Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J Neurosci 2004, 24:8485-8493.
83. Sasaki M., Black J.A., Lankford K.L., et al. Molecular reconstruction of nodes of Ranvier after remyelination by transplanted olfactory ensheathing cells in the demyelinated spinal cord. J Neurosci 2006, 26:1803-1812.
84. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat Rev Neurosci 2004, 5:146-156.
85. Smith P.M., Sim F.J., Barnett S.C., et al. SCIP/Oct-6, Krox-20, and desert hedgehog mRNA expression during CNS remyelination by transplanted olfactory ensheathing cells. Glia 2001, 36:342-353.
86. Steward O., Sharp K., Selvan G., et al. A re-assessment of the consequences of delayed transplantation of olfactory lamina propria following complete spinal cord transection in rats. Exp Neurol 2006, 198:483-499.
87. Thompson R.J., Roberts B., Alexander C.L., et al. Comparison of neuregulin-1 expression in olfactory ensheathing cells, Schwann cells and astrocytes. J Neurosci Res 2000, 61:172-185.
88. Toft A., Scott D.T., Barnett S.C., et al. Electrophysiological evidence that olfactory cell transplants improve function after spinal cord injury. Brain 2007, 130:970-984.
89. Verdu E., Garcia-Alias G., Fores J., et al. Olfactory ensheathing cells transplanted in lesioned spinal cord prevent loss of spinal cord parenchyma and promote functional recovery. Glia 2003, 42:275-286.
90. Villegas-Pérez M.P., Vidal-Sanz M., Bray G.M., et al. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci 1988, 8:265-280.
91. Vincent A.J., West A., Chuah M.I. Morphological and functional plasticity of olfactory ensheathing cells. J Neurocytol 2005, 34:65-85.
92. Wewetzer K., Verdu E., Angelov D.N., et al. Olfactory ensheathing glia and Schwann cells: two of a kind?. Cell Tissue Res 2002, 309:337-345.
93. Wilby M.J., Muir E.M., Fok-Seang J., et al. N-cadherin inhibits Schwann cell migration on astrocytes. Mol Cell Neurosci 1999, 14:66-84.
94. Woodhall E., West A.K., Chuah M.I. 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 2001, 88:203-213.
95. Yan H., Bunge M.B., Wood P.M., et al. Mitogenic response of adult rat olfactory ensheathing glia to four growth factors. Glia 2001, 33:334-342.
96. Yamamoto M., Raisman G., Li D.-Q., et al. Transplanted olfactory mucosal cells restore paw reaching function without regeneration of severed corticospinal tract fibers across the lesion. Brain Res 2009, 1303:26-31.