The culture of olfactory ensheathing cells (OECs)-a distinct glial cell type

Experimental Neurology

Volumn 229, Issue 1, 2011, Pages 2-9

  Higginson, Jennifer R ^a   Barnett, Susan C ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Culture; Maintenance; Molecular and cellular; Olfactory ensheathing cells; Properties; Purification

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR 2; FORSKOLIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE CELL ADHESION MOLECULE; NEUROTROPHIN RECEPTOR P75; PROTEIN S100B;

CELL CULTURE; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSPLANTATION; GENETIC MANIPULATION; GLIA CELL; HUMAN; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE INJURY; NERVE REGENERATION; OLFACTORY ENSHEATHING CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SCHWANN CELL;

ANIMALS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; HUMANS; NEUROGLIA; OLFACTORY BULB; OLFACTORY MUCOSA; SCHWANN CELLS;

EID: 79955477990     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.08.020     Document Type: Review

References (83)

1. Afshari F.T., Kwok J.C., Fawcett J.W. Astrocyte-produced ephrins inhibit Schwann cell migration via VAV2 signalling. J. Neurosci. 2010, 30:4246-4255.
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. Au E., Roskams A.J. Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 2003, 41:224-236.
4. Au W.W., Treloar H.B., Greer C.A. Sublaminar organisation of the mouse olfactory bulb nerve layer. J. Comp. Neurol. 2002, 46:68-80.
5. Au E., Richter M.W., Vincent A.J., Tetzlaff W., Aebersold R., Sage E.H., Roskams A.J. SPARC from olfactory ensheathing cells stimulates Schwann cells to promote neurite outgrowth and enhances spinal cord repair. J. Neurosci. 2007, 27:7208-7221.
6. Barber P.C., Lindsay R.M. Schwann cells of the olfactory nerves contain glial fibrillary acidic protein and resemble astrocytes. Neurosci. 1982, 7:3077-3090.
7. Barnett S.C., Chang L. Olfactory ensheathing cells and CNS repair: going solo or in need of a friend?. Trends Neurosci. 2004, 27:54-60.
8. Barnett S.C., Hutchins A.-M., Noble M. Purification of olfactory nerve ensheathing cells from the olfactory bulb. Dev. Biol. 1993, 55:337-350.
9. Barnett S.C., Alexander C.A., Gilson J., Clark L., Dunn L., Papanastassiou V., Kennedy P.G.E., Ishwashita Y., Franklin R.J.M. Identification of the human olfactory ensheathing cell (OEC) and demonstration of its ability to remyelinate experimentally-induced demyelinating lesions in the rat spinal cord. Brain 2000, 123:1581-1588.
10. Barnett S.C., Thompson R.J., Lakatos A.L., Pitts J. Gap junctional communication and connexin expression in cultured olfactory ensheathing Cells. J. Neurosci. Res. 2001, 65:520-528.
11. Bianco J.I., Perry C., Harkin D.G., Mackay-Sim A., Féron F. Neurotrophin 3 promotes purification and proliferation of olfactory ensheathing cells from human nose. Glia 2004, 45:111-123.
12. Blanes T. Sobre algunos puntos dudosos del la estructura del bulbo olfactorio. Rev. Trim. Micrograf. 1898, 3:99-127.
13. 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. 2007, 505:572-585.
14. Boyd J.G., Jahed A., McDonald T.G., Krol K.M., Van Eyk J.E., Doucette R., Kawaja M.D. Proteomic evaluation reveals that olfactory ensheathing cells but not Schwann cells express calponin. Glia 2006, 53:434-440.
15. Caubit X., Arsanto J.-P., Figarella-Branger D., Thouveny Y. Expression of polysialylated neural cell adhesion molecule (PSA-N-CAM) in developing, adult and regenerating caudal spinal cord of the urodele amphibians. In. J. Dev. Biol. 1993, 37:327-336.
16. Chuah M.I., Au C. Cultures of ensheathing cells from neonatal l rat olfactory bulbs. Brain Res. 1993, 601:213-220.
17. De Lorenzo A.J. Electron microscopic observations of the olfactory mucosa and olfactory nerve. J. Biophys. Biochem. Cytol. 1957, 3(6):839-850. Nov 25.
18. De Mello T.R., Busfield S., Dunlop S.A., Plant G.W. Culture conditions affect proliferative responsiveness of olfactory ensheathing glia to neuregulins. Glia 2007, 55:734-745.
19. Delorme B., Nivet E., Gaillard J., Haupl T., Ringe J., Devèze A., Magnan J., Sohier J., Khrestchatisky M., Roman F.S., Charbord P., Sensebe L., Layrolle P., Feron F. The human nose harbours a niche of olfactory ecto-mesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev. 2009, Epub ahead of print.
20. Den Pol Van, Santarelli J.G. Olfactory ensheathing cells: time lapse imaging of cellular interactions, axonal support, rapid morphologic shifts and mitosis. J. Comp. Neurol. 2003, 458:175-194.
21. Denis-Donini S., Stenoz M. Interneurons versus efferent neurons: heterogeneity in their neurite outgrowth response to glia from several brain regions. Dev. Biol. 1988, 130:237-249.
22. Doucette J.R. The glial cells in the nerve layer of the rat olfactory bulb. Anat. Rec. 1984, 210:385-391.
23. Doucette R. Glial influences on axonal growth in the primary olfactory system. Glia 1990, 3:433-449.
24. Doucette R. Glial progenitor cells of the nerve fiber layer of the olfactory bulb: effect of astrocyte growth media. J. Neurosci. Res. 1993, 35:274-287.
25. Fairless R., Frame M.C., Barnett S.C. N-cadherin differentially determines Schwann cell and olfactory ensheathing cell adhesion and migration upon contact with astrocytes. Mol. ell. Neurosci. 2005, 28:253-263.
26. Farbman I.A. Cell biology of olfaction 1992, Cambridge Univeristy Press.
27. 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 2005, 128:2951-2960.
28. Fraher J.P. The ultrastructure of sheath cells in developing rat vomeronasal nerve. J. Anat. 1982, 134:149-168.
29. Franceschini, Barnett S.C. Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol. 1996, 173:327-343.
30. Franklin R.J.M., Barnett S.C. Do olfactory glia have advantages over Schwann cells for CNS repair?. J. Neurosci. Res. 1997, 50:1-8.
31. Franklin R.J.M., Barnett S.C. Olfactory ensheathing cells and CNS regeneration-the sweet smell of success?. Neuron 2000, 28:1-4.
32. 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.
33. Franssen E.H., Riet K.L.C.D., de Bree F.M., Verhaagen J. Olfactory ensheathing glia and Schwann cells exhibit a distinct interaction behaviour with meningeal cells. J. Neurosci. Res. 2009, 87:1556-1564.
34. Fregien N.L., White L.A., Bunge M.B., Wood P.M. Forskolin increases neuregulin receptors in human Schwann cells without increasing receptor mRNA. Glia 2005, 49:24-35.
35. García-Escudero V., García-Gómez A., Gargini R., Martín-Bermejo M.J., Langa E., de Yébenes 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. 2010, 18:394-403.
36. Gasser H.S. Olfactory nerve fibres. J. Gen. Physiol. 1956, 39:483-496.
37. Golgi C. Sulla fina anatomia del bulbi olfactorii. Ti Rivista Sperimentale di Freniatria 1875, 1:403-425.
38. 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.
39. Graziadei P., Monti-Graziadei. The olfactory system: a model for the study of neurogenesis and axon regeneration in mammals. Neuronal plasticity 1978, 131-153. Raven Press, New York. C.W. Cotman (Ed.).
40. Grazaidei P.P.C., Monti-Graziadie 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.
41. Huang Z.H., Wang Y., Cao L., Su Z.D., Zhu Y.L., Chen Y.Z., Yuan X.B., He C. Migratory properties of cultured olfactory ensheathing cells by single-cell migration assay. Cell Res. 2008, 18:479-490.
42. Ibanez C., Ito D., Zawadzka M., Jeffery N.D., Franklin R.J.M. Calponin is expressed by fibroblasts and meningeal cells but not olfactory ensheathing cells in the adult peripheral olfactory system. Glia 2007, 55:144-151.
43. Jahed A., Rowland J.W., McDonald T., Boyd J.G., Doucette R., Kawaja M.D. Olfactory ensheathing cells express smooth muscle alpha-actin in vitro and in vivo. J. Comp. Neurol. 2007, 503:209-223.
44. Jani H.R., Raisman G. Ensheathing cell cultures from the olfactory bulb and mucosa. Glia 2004, 4:130-137.
45. Jessen K.R., Morgan L., Stewart H.J., Mirsky R. Three markers of adult non-myelin-forming Schwann cells, 217c(Ran-1), A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Dev. 1990, 109:91-103.
46. 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.
47. Kocsis J.D., Lankford K.L., Sasaki M., Radtke C. Unique in vivo properties of olfactory ensheathing cells that may contribute to neural repair and protection following spinal cord injury. Neurosci. Lett. 2009, 456:137-142.
48. Kumar R., Hayat S., Felts P., Bunting S., Wigley C. Functional differences and interactions between phenotypic subpopulations of olfactory cells in promoting CNS axonal regeneration. Glia 2005, 50:12-20.
49. Lakatos A., Franklin R.J.M., Barnett S.C. Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 2000, 32:214-225.
50. Lakatos A., Barnett S.C., Franklin R.J.M. 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.
51. 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.
52. Lim F., Martín-Bermejo M.J., García-Escudero V., Gallego-Hernández M.T., García-Gómez A., Rábano A., Díaz-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.
53. 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.
54. Mackay-Sim, Feron 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 2008, 131:2376-2386.
55. Miragall F., Kadmong G., Husmann M., Schachner M. Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of N-CAM. Dev. Biol. 1988, 129:516-531.
56. Monje P.V., Bartlett Bunge M., Wood P.M. Cyclic AMP synergistically enhances neuregulin-dependent ERK and Akt activation and cell cycle progression in Schwann cells. Glia 2006, 53:649-659.
57. Nash H.H., Borke R.C., Anders J.J. New Method of Purification for Establishing Primary Cultures of Ensheathing Cells From the Adult Olfactory Bulb. Glia 2001, 34:81-87.
58. Noble M., Murray K. Purified astrocytes promote the in vitro division of a bipotential glial progenitor cell. EMBO J. 1984, 3:2243-2247.
59. Pixley S.K. The olfactory nerve contains two populations of glia, identified both in vitro and in vivo. Glia 1992, 5:269-284.
60. Pollock G.S., Franceschini I.A., Graham G., Marchionni M.A., Barnett S.C. 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.
61. Radtke C., Lankford K.L., Wewetzer K., Imaizumi T., Fodor W.L., Kocsis J.D. Impaired spinal cord remyelination by long-term cultured adult porcine olfactory ensheathing cells correlates with altered in vitro phenotypic properties. Xenotransplantation 2010, 17:71-80.
62. Rahmatullah M., Schroering A., Rothblum K., Stahl R.C., Urban B., Carey D.J. Synergistic regulation of Schwann cell proliferation by heregulin and forskolin. Mol. Cell. Biol. 1998, 18:6245-6252.
63. Raisman G. Specialised neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neurosci. 1985, 14:237-254.
64. Ramón-Cueto A., Nieto-Sampedro M. Glial cells from the adult rat olfactory bulb, immunocytochemical properties of pure cultures of ensheathing cells. Neurosci. 1992, 47:213-220.
65. 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.
66. Ramón-Cueto A., Valverde F. Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 1994, 14:163-173.
67. Ramón-Cueto A., Pérez J., Nieto-Sampedro M. In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. Eur. J. Neurosci. 1993, 5:1172-1180.
68. Richter M., Westendorf K., Roskams A.J. Culturing olfactory ensheathing cells from the mouse olfactory epithelium. Methods Mol Biol. 2008, 438:95-102.
69. Rubio M.P., Munoz-Quiles C., Ramón-Cueto A. Adult olfactory bulbs from the primate provides reliable ensheathing glia for cell transplantation. Glia 2008, 56:539-551.
70. Santos-Silva A., Fairless R., Frame M., Montague P., Smith G.M., Toft A., Riddell J.S., Barnett S.C. 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.
71. Shields S.A., Blakemore W.F., Franklin R.J.M. Schwann cell remyelination is restricted to astrocyte-deficient areas after transplantation into demyelinated adult rat brain. J. Neurosci. Res. 2000, 60:571-578.
72. Techangamsuwan S., Imbschweiler I., Kreutzer R., Kreutzer M., Baumgärtner 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.
73. Techangamsuwan S., Haas L., Rohn K., Baumgärtner W., Wewetzer K. Distinct cell tropism of canine distemper virus strains to adult olfactory ensheathing cells and Schwann cells in vitro. Virus Res. 2009, 144:195-201.
74. Tetzlaff W., Okon E.B., Karimi-Abdolrezaee S., Hill C.E., Sparling J.S., Plemel J.R., Plunet W.T., Tsai E.C., Baptiste D., Smithson L.J., Kawaja M.D., Fehlings M.G., Kwon B.K. A systematic review of cellular transplantation therapies for spinal cord injury. J. Neurotrauma 2010, Apr 20. [Epub ahead of print].
75. Thompson R.J., Roberts B., Alexander C.L., Williams S.K., Barnett S.C. Comparison of neuregulin-1 expression in olfactory ensheathing cells, Schwann cells and astrocytes. J. Neurosci. Res. 2000, 61:172-185.
76. Toft A, Tome M, Barnett SC & Riddell JS. Cell transplant mediated spinal cord repair: Do purified glial cells have advantages over fibroblast or mixed cell cultures? Submitted to Glia.
77. Tomé M., Siladzic E., Santos-Silva A., Barnett S.C. Calponin is expressed by subpopulations of connective tissue cells but not olfactory ensheathing cells in the neonatal olfactory mucosa. BMC Neurosci. 2007, 8:74.
78. Tomé M., Lindsay S.L., Riddell J.S., Barnett S.C. Identification of nonepithelial multipotent cells in the embryonic olfactory mucosa. Stem Cells 2009, 27:2196-2208.
79. Vincent A.J., West A.K., Chuah M.I. Morphological plasticity of olfactory ensheathing cells in regulated by cAMP and endothelin-1. Glia 2003, 41:393-403.
80. Webster H.D., Martin J.R., O'Connell M.F. The relationship between interphase Schwann cells and axons before myelination; a quantitative electron microscopic study. Dev. Biol. 1973, 32:401-416.
81. Wewetzer K., Verdú E., Angelov D.N., Navarro X. Olfactory ensheathing glia and Schwann cells: two of a kind?. Cell Tissue Res. 2002, 309:337-345.
82. 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 2005, 49:577-587.
83. Yan H., Bunge M.B., Wood P.M., Plant G.W. Mitogenic response of adult rat olfactory ensheathing glia to four growth factors. Glia 2001, 33:334-342.