Axonal signalling and the making of olfactory ensheathing cells: A hypothesis

Neuron Glia Biology

Volumn 2, Issue 3, 2006, Pages 217-224

  Wewetzer, Konstantin ^a,b   Brandes, Gudrun ^b  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Differentiation; OEC; Phenotype; Schwann cell; Transplantation

Indexed keywords

PROTEIN P75;

ANTIGEN EXPRESSION; CELL PROLIFERATION; CELL TRANSPLANTATION; CELL ULTRASTRUCTURE; DOWN REGULATION; GLIA CELL; HUMAN; NERVE REGENERATION; NERVOUS SYSTEM; NONHUMAN; OLFACTORY ENSHEATHING CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION; SPINAL CORD LESION; UPREGULATION;

EID: 33847690237     PISSN: 1740925X     EISSN: 17410533     Source Type: Journal    
DOI: 10.1017/S1740925X06000305     Document Type: Review

References (112)

1. Akiyama Y., Lankford K.L., Radtke C., Greer C.A. and Kocsis J.D. (2004) Remyelination of spinal cord axons by olfactory ensheathing cells and Schwann cells derived from a transgenic rat expressing alkaline phosphatase marker gene. Neuron Glia Biology 1, 47-55.
2. Alexander C.L., Fitzgerald U.F. and Barnett S.C. (2002) Identification of growth factors that promote long-term proliferation of olfactory ensheathing cells and modulate their antigenic phenotype. Glia 37, 349-364.
3. Au E. and Roskams A.J. (2003) Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 41, 224-236.
4. Au W.W., Treloar H.B. and Greer C.A. (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. Journal of Comparative Neurology 446, 68-80.
5. Barber P.C. (1982) Neurogenesis and regeneration in the primary olfactory pathway of mammals. Bibliotheca Anatomica 23, 12-25.
6. Bartolomei J.C. and Greer C.A. (2000) Olfactory ensheathing cells: bridging the gap in spinal cord injury. Neurosurgery 47, 1057-1069.
7. Bailey M.S., Puche A.C. and Shipley M.T. (1999) Development of the olfactory bulb: evidence for glia-neuron interactions in glomerular formation. Journal of Comparative Neurology 415, 423-448.
8. Barnett S.C., Alexander C.L., Iwashita Y., Gilson J.M., Crowther J., Clark L. et al. (2000) Identification of a human olfactory ensheathing cell that can effect transplant-mediated remyelination of demyelinated CNS axons. Brain 123, 1581-1588.
9. Barnett S.C. and Chang L. (2004) Olfactory ensheathing cells and CNS repair: going solo or in need of a friend? Trends in Neurosciences 27, 54-60.
10. Boyd J.G., Doucette R. and Kawaja M.D. (2005) Defining the role of olfactory ensheathing cells in facilitating axon remyelination following damage to the spinal cord. FASEB Journal 19, 694-703.
11. Boyd J.G., Jahed A., McDonald T.G., Krol K.M., Van Eyk J.E., Doucette R. et al. (2006) Proteomic evaluation reveals that olfactory ensheathing cells but not Schwann cells express calponin. Glia 53, 434-440.
12. Boyd J.G., Skihar V., Kawaja M. and Doucette R. (2003) Olfactory ensheathing cells: historical perspective and therapeutic potential. Anatomical Record 271B, 49-60.
13. Calof A.L., Hagiwara N., Holcomb J.D., Mumm J.S. and Shou J. (1996) Neurogenesis and cell death in olfactory epithelium. Journal of Neurobiology 30, 67-81.
14. Chen S., Rio S., Ji R.R., Dikes P., Coggeshall R.E., Woolf C.J. et al. (2003) Disruption of ErbB receptor signaling in adult nonmyelinating Schwann cells causes progressive sensory loss. Nature Neuroscience 6, 1186-1193.
15. Chen S., Velardez M.O., Warot X., Yu Z.X., Miller S.J. and Corfas G. (2006) Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. Journal of Neuroscience 26, 3079-3086.
16. Chen J.K., Yao L.L. and Jenq C.B. (1991) Mitogenic response of rat Schwann cells to fibroblast growth factors is potentiated by increased intracellular cyclic AMP levels. Journal of Neuroscience Research 30, 321-327.
17. Chuah M.I., Cossins J., Woodhall E., Tennent R., Nash G. and West A.K. (2000) Glial growth factor 2 induces proliferation and structural changes in ensheathing cells. Brain Research 857, 265-274.
18. Chuah M.I. and Teague R. (1999) Basic fibroblast growth factor in the primary olfactory pathway: mitogenic effect on ensheathing cells. Neuroscience 88, 1043-1050.
19. Chuah M.I. and West A.K. (2002) Cellular and molecular biology of ensheathing cells. Microscopy Research and Technique 58, 216-227.
20. Chung R.S., Woodhouse A., Fung S., Dickinson T.C., West A.K., Vickers C. et al. (2004) Olfactory ensheathing cells promote neurite sprouting of injured axons in vitro by direct cellular contact and secretion of soluble factors. Cellular and Molecular Life Sciences 61, 1238-1245.
21. Corfas G., Velardez M.O., Ko C.P., Ratner N. and Peles E. (2004) Mechanisms and roles of axon-Schwann cell interactions. Journal of Neuroscience 24, 9250-9260.
22. Davis J.B. and Stroobant P. (1990) Platelet-derived growth factors and fibroblast growth factors are mitogens for rat Schwann cells. Journal of Cell Biology 110, 1353-1360.
23. Devon R. and Doucette R. (1992) Olfactory ensheathing cells myelinate dorsal root ganglion neurites. Brain Research 589, 175-179.
24. Devon R. and Doucette R. (1995) Olfactory ensheathing cells do not require L-ascorbic acid in vitro to assemble a basal lamina or to myelinate dorsal root ganglion neurites. Brain Research 688, 223-229.
25. Doucette J.R. (1984) The glial cells in the nerve fiber layer of the rat olfactory bulb. Anatomical Record 210, 385-391.
26. Doucette J.R. (1993) Glial cells in the nerve fiber layer of the main olfactory bulb of embryonic and adult mammals. Microscopy and Research Technique 24, 113-130.
27. Doucette R. and Devon R. (1995) Elevated intracellular levels of cAMP induce olfactory ensheathing cells to express GAL-C and GFAP but not MBP. Glia 13, 130-140.
28. Fairless R., Frame M.C. and Barnett S.C. (2005) N-cadherin differentially determines Schwann cell and olfactory ensheathing cell adhesion and migration responses upon contact with astrocytes. Molecular and Cellular Neuroscience 28, 253-263.
29. Field P., Li Y. and Raisman G. (2003) Ensheathment of the olfactory nerves in the adult rat. Journal of Neurocytology 32, 317-324.
30. Franceschini I.A. and Barnett S.C. (1996) Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Developmental Biology 173, 327-343.
31. Franklin R.J. (2003) Remyelination by transplanted olfactory ensheathing cells. Anatomical Record 271B, 71-76.
32. Franklin R.J. and Barnett S.C. (1997) Do olfactory glia have advantages over Schwann cells for CNS repair? Journal of Neuroscience Research 50, 665-672.
33. Franklin R.J. and Barnett S.C. (2000) Olfactory ensheathing cells and CNS regeneration: the sweet smell of success? Neuron 28, 15-18.
34. Franklin R.J., Gilson J.M., Franceschini I.A. and Barnett S.C. (1996) Schwann cell-like myelination following transplantation of an olfactory bulb-ensheathing cell line into areas of demyelination in the adult CNS. Glia 17, 217-224.
35. Gong Q., Bailey M.S., Pixley S.K., Ennis M., Liu W. and Shipley M.T. (1994) Localization and regulation of low affinity nerve growth factor receptor expression in the rat olfactory system during development and regeneration. Journal of Comparative Neurology 344, 336-348.
36. Graziadei P.P. and Monti-Graziadei G.A. (1985) Neurogenesis and plasticity of the olfactory sensory neurons. Annals of the New York Academy of Sciences 457, 127-142.
37. Gupta S.K., Pringle J., Poduslo J.F. and Mezei C. (1993) Induction of myelin genes during peripheral myelination requires a continous signal from the ingrowing axon. Journal of Neuroscience Research 34, 14-23.
38. Imaizumi T., Lankford K.L., Waxman S.G., Greer C.A. and Kocsis J.D. (1998) Transplanted olfactory ensheathing cells remyelinate and enhance axonal conduction in the demyelinated dorsal columns of the rat spinal cord. Journal of Neuroscience 18, 6176-6185.
39. Itoh K., Stevens B., Schachner M. and Fields R.D. (1995) Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science 270, 1369-1372.
40. Jessen K.R., Mirsky R. and Morgan L. (1987) Axonal signals regulate the differentiation of non-myelin-forming Schwann cells: an immunohistochemical study of galactocerebroside in transected and regenerating nerves. Journal of Neuroscience 7, 3362-3369.
41. Jessen K.R. and Mirsky R. (1991) Schwann cell precursor and their development. Glia 4, 185-194.
42. Jessen K.R. and Mirsky R. (2002) Signals that determine Schwann cell identity. Journal of Anatomy 200, 367-376.
43. Jessen K.R. and Mirsky R. (2004) Schwann cell development. In, Lazzarini R.A., ed. Myelin Biology and Disorders. Elsevier Academic Press, 329-370.
44. Jessen K.R. and Mirsky R. (2005) The origin and development of glial cells in peripheral nerves. Nature Reviews Neuroscience 6, 671-682.
45. Jessen K.R., Mirsky R. and Morgan L. (1991) Role of cyclic AMP and proliferation controls in Schwann cell differentiation. Annals of the New York Academy of Sciences 633, 78-89.
46. Jessen K.R., Morgan L., Stewart H.J. and Mirsky R. (1990) Three markers of adult non-myelin-forming Schwann cells, 217c(Ran-1), A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Development 109, 91-103.
47. Jirounek P., Bretton C. and Dalle C. (2002) Axon-glia interactions modulate axonal excitability in mammalian unmyelinated nerves. Journal of Physiology Paris 96, 237-241.
48. Kafitz K.W. and Greer C.A. (1997) Role of laminin in axonal extension from olfactory receptor cells. Journal of Neurobiology 32, 298-310.
49. Keyvan-Fouladi N., Raisman G. and Li Y. (2003) Functional repair of the corticospinal tract by delayed transplantation of olfactory ensheathing cells in adult rats. Journal of Neuroscience 23, 9428-9434.
50. 2 dopamine receptors. Journal of Comparative Neurology 411, 666-673.
51. Krudewig C., Deschl U. and Wewetzer K. (2006) Purification and in vitro characterization of adult canine olfactory ensheathing cells. Cell and Tissue Research 326, 687-696.
52. Kumar R., Hayat S., Felts P., Bunting S. and Wigley C. (2005) Functional differences and interactions between phenotypic subpopulations of olfactory ensheathing cells in promoting CNS axonal regeneration. Glia 50, 12-20.
53. Lakatos A., Barnett S.C. and Franklin R.J. (2003a) Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than Schwann cells following transplantation into adult CNS white matter. Experimental Neurology 184, 237-246.
54. Lakatos A., Franklin R.J. and Barnett S.C. (2000) Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 32, 214-225.
55. Lakatos A., Smith P.M., Barnett S.C. and Franklin R.J. (2003b) Meningeal cells enhance limited CNS remyelination by transplanted olfactory ensheathing cells. Brain 126, 598-609.
56. LeBlanc A.C., Windenbank A.C. and Poduslo J.F. (1992) PO expression in Schwann cells is modulated by an increase of cAMP which is dependent on the presence of axons. Brain Research Molecular Brain Research 12, 31-38.
57. Lee M., Brennan A., Blanchard A., Zoidl G., Dong Z., Tabernero A. et al. (1997) P0 is constitutively expressed in the rat neural crest and embryonic nerves and is negatively and positively regulated by axons to generate non-myelin-forming and myelin-forming Schwann cells, respectively. Molecular and Cellular Neuroscience 8, 336-350.
58. Lemke G. (2006) Neuregulin-1 and myelination. Science's Signal Transduction Knowledge Environment 325, pe11.
59. Li Y., Decherchi P. and Raisman G. (2003a) Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. Journal of Neuroscience 23, 727-731.
60. Li Y., Field P.M. and Raisman G. (1998) Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. Journal of Neuroscience 18, 10514-10524.
61. Li Y., Sauve Y., Li D., Lund R.D. and Raisman G. (2003b) Transplanted olfactory ensheathing cells promote regeneration of cut adult rat optic nerve axons. Journal of Neuroscience 23, 7783-7788.
62. Lim J.H. and Brunjes P.C. (1999) Activity-dependent regulation of interleukin-1 beta immunoreactivity in the developing rat olfactory bulb. Neuroscience 93, 371-374.
63. Mackay-Sim A. (2005) Olfactory ensheathing cells and spinal cord repair. Keio Journal of Medicine 54, 8-14.
64. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeier C. et al. (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304, 700-703.
65. Mirsky R. and Jessen K.R. (1999) The neurobiology of Schwann cells. Brain Pathology 9, 293-311.
66. Morgan L., Jessen K.R. and Mirsky R. (1991) The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelin phenotype (P0+, GFAP-, N-CAM-, NGF-receptor-) depends on growth inhibition. Journal of Cell Biology 112, 457-467.
67. Parkinson D.B., Bhaskaran A., Droggiti A., Dickinson S., D'Antonio M., Mirsky R. et al. (2004) Krox-20 inhibits Jun-NH2-terminal kinase/c-Jun to control Schwann cell proliferation and death. Journal of Cell Biology 164, 385-394.
68. Parmantier E., Lynn B., Lawson D., Turmaine M., Namini S.S., Chakrabarti L. et al. (1999) Schwann cell-derived Desert hedgehog controls the development of peripheral nerve sheaths. Neuron 23, 713-724.
69. Pixley S.K. (1992) The olfactory nerve contains two populations of glia, identified both in vivo and in vitro. Glia 5, 269-284.
70. Pixley S.K. (1996) Characterization of olfactory receptor neurons and other cell types in dissociated rat olfactory cell cultures. International Journal of Developmental Neuroscience 14, 823-839.
71. Poduslo J.F. (1993) Regulation of myelin gene expression in the peripheral nervous system. In, Dyck P.J., Low P.A. and Poduslo J.F., eds. Peripheral Neuropathy. Saunders, 282-289.
72. Pollock G.S., Franceschini I.A., Grahma G., Marchionni M.A. and Barnett S.C. (1999) Neuregulin is a mitogen and survival factor for olfactory bulb ensheathing cells and an isoform is produced by astrocytes. European Journal of Neuroscience 11, 769-780.
73. Radtke C., Akiyama Y., Brokaw J., Lankford K.L., Wewetzer K., Fodor W.L. et al. (2004) Remyelination of the nonhuman primate spinal cord by transplantation of H-transferase transgenic adult pig olfactory ensheathing cells. FASEB Journal 18, 335-337.
74. Raisman G. (1985) Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14, 237-254.
75. Raisman G. (2001) Olfactory ensheathing cells - another miracle cure for spinal cord injury? Nature Reviews Neuroscience 2, 369-375.
76. Ramón-Cueto A. and Avila J. (1998) Olfactory ensheathing glia: properties and function. Brain Research Bulletin 46, 175-187.
77. Ramón-Cueto A., Perez J. and Nieto-Sampedro M. (1993) In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. European Journal of Neuroscience 5, 1172-1180.
78. Ramón-Cueto A. and Valverde F. (1995) Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 14, 163-173.
79. Richter M.W., Fletcher P.A., Liu J., Tetzlaff W. and Roskams A.J. (2005) Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. Journal of Neuroscience 16, 10700-10711.
80. Ronnett G.V., Hester L.D. and Snyder S.H. (1991) Primary culture of neonatal rat olfactory neurons. Journal of Neuroscience 11, 1243-1255.
81. Santos-Benito F.F. and Ramón-Cueto A. (2003) Olfactory ensheathing glia transplantation: a therapy to promote repair in the mammalian central nervous system. Anatomical Record 271B, 77-85.
82. Sasaki M., Black J.A., Lankford K.L., Tokuno H.A., Waxman S.G. and Kocsis J.D. (2006) Molecular reconstruction of nodes of Ranvier after remyelination by transplanted olfactory ensheathing cells in the demyelinated spinal cord. Journal of Neuroscience 26, 1803-1812.
83. Sasaki M., Lankford K.L., Zemedkun M. and Kocsis J.D. (2004) Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. Journal of Neuroscience 24, 8485-8493.
84. Sherman D.L. and Brophy P.J. (2005) Mechanisms of axon ensheathment and myelin growth. Nature Reviews Neuroscience 6, 683-690.
85. Shuman S., Hardy M., Sobue G. and Pleasure D. (1988) A cyclic AMP analogue induces synthesis of a myelin-specific glycoprotein by cultured Schwann cells. Journal of Neurochemistry 50, 190-194.
86. Smith P.M., Sim F.J., Barnett S.C. and Franklin R.J. (2001) SCIP/Oct-6, Krox-20, and desert hedgehog mRNA expression during CNS remyelination by transplanted olfactory ensheathing cells. Glia 36, 342-353.
87. Sobue G., Shuman S. and Pleasure D. (1986) Schwann cell responses to cyclic AMP: proliferation, change in shape, and appearance of surface galactocerebroside. Brain Research 362, 23-32.
88. Stemple D.L. and Anderson D.J. (1991) A Schwann cell antigen recognized by monoclonal antibody 217c is the rat low-affinity nerve growth factor receptor. Neuroscience Letters 124, 57-60.
89. Stevens B. and Fields R.D. (2000) Response of Schwann cells to action potentials in development. Science 287, 2267-2271.
90. Stewart H.J., Eccleston P.A., Jessen K.R. and Mirsky R. (1991) Interaction between cAMP elevation, identified growth factors, and serum components in regulating Schwann cell growth. Journal of Neuroscience Research 30, 346-352.
91. Takami T., Oudega M., Bates M.L., Wood P.M., Kleitman N. and Bunge M.B. (2002) Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. Journal of Neuroscience 22, 6670-6681.
92. Taveggia C., Zanazzi G., Petrylak A., Yano H., Rosenbluth J., Einheber S. et al. (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47, 681-694.
93. Taylor V. and Suter U. (1997) Molecular biology of axon-glia interactions in the peripheral nervous system. Progress in Nucleic Acid Research and Molecular Biology 56, 225-256.
94. Thomas P.K., Berthold C.H. and Ochoa J. (1993) Microscopic anatomy of the peripheral nervous system. In, Dyck P.J., Low P.A. and Poduslo J.F., eds. Peripheral Neuropathy. Saunders, 28-73.
95. Tisay K.T., Bartlett P.F. and Key B. (2000) Primary olfactory axons form ectopic glomeruli in mice lacking p75NTR. Journal of Comparative Neurology 428, 656-670.
96. Treloar H.B., Bartolomei J.C., Lipscomb B.W. and Greer C.A. (2001) Mechanisms of axonal plasticity: lessons from the olfactory pathway. Neuroscientist 7, 55-63.
97. Tucker E.S., Oland L.A. and Tolbert L.P. (2004) In vitro analyses of interactions between olfactory receptor growth cones and glial cells that mediate axon sorting and glomerulus formation. Journal of Comparative Neurology 472, 478-495.
98. Turner C.P. and Perez-Polo J.R. (1993) Expression of p75NGFR in the olfactory system following peripheral deafferentation. Neuroreport 4, 1023-1026.
99. Turner C.P. and Perez-Polo J.R. (1994) Changes in expression of the low affinity receptor for neurotrophins, p75NGFR, in the regenerating olfactory system. International Journal of Developmental Neuroscience 12, 767-773.
100. Vincent A.J., Taylor J.M., Choi-Lundberg D.L., West A.K. and Chuah M.I. (2005a) Genetic expression profile of olfactory ensheathing cells is distinct from that of Schwann cells and astrocytes. Glia 51, 132-147.
101. Vincent A.J., West A.K. and Chuah M.I. (2001) Morphological plasticity of olfactory ensheathing cells is regulated by cAMP and endothelin-1. Glia 41, 393-403.
102. Vincent A.J., West A.K. and Chuah M.I. (2005b) Morphological and functional plasticity of olfactory ensheathing cells. Journal of Neurocytology 34, 65-80.
103. Vroemen M. and Weidner N. (2003) Purification of Schwann cells by selection of p75 low affinity nerve growth factor receptor expressing cells fromadult peripheral nerve. Journal of Neuroscience Methods 124, 135-143.
104. Wegner M. (2000) Transcriptional control in myelinating glia: flavors and spices. Glia 31, 1-14.
105. Wewetzer K., Grothe C., Christ B. and Seilheimer B. (1997) Identification and characterization of differentiation-dependent Schwann cell surface antigens by novel monoclonal antibodies: introduction of a marker common to the non-myelin-forming phenotype. Glia 19, 213-226.
106. Wewetzer K., Grothe C. and Claus P. (2001) In vitro expression and regulation of ciliary neurotrophic factor and its alpha receptor subunit in neonatal rat olfactory ensheathing cells. Neuroscience Letters 306, 165-168.
107. - neonatal olfactory ensheathing cells. Glia 49, 557-587.
108. Wewetzer K., Verdú E., Angelov D.N. and Navarro X. (2002) Olfactory ensheathing glia and Schwann cells: two of a kind? Cell and Tissue Research 309, 337-345.
109. Woodhall E., West A.K., Vickers J.C. and Chuah M.I. (2003) Olfactory ensheathing cell phenotype following implantation in the lesioned spinal cord. Cellular and Molecular Life Sciences 60, 2241-2253.
110. Yan H., Bunge M.B., Wood P.M. and Plant G.W. (2001) Mitogenic response of adult rat olfactory ensheathing glia to four growth factors. Glia 33, 334-342.
111. Yasuda T., Sobue G., Mokuno K., Kreider B. and Pleasure D. (1987) Cultured rat Schwann cells express low affinity receptors for nerve growth factor. Brain Research 436, 113-119.
112. Zorick T.S. and Lemke G. (1996) Schwann cell differentiation. Current Opinion in Cell Biology 8, 870-876.