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

Experimental Neurology

Volumn 229, Issue 1, 2011, Pages 80-87

  Wewetzer, Konstantin ^a,b,c   Radtke, Christine ^b   Kocsis, Jeffery ^d   Baumgärtner, Wolfgang ^a,c  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autologous transplantation; Cell transplantation; Immortalization; OECs; Regeneration; SCs; Spinal cord injury; Translational research

Indexed keywords

CYCLIC AMP;

AUTOTRANSPLANTATION; CELL EXPANSION; CELL IMMORTALIZATION; CELL PROLIFERATION; CELL TRANSPLANTATION; DOG; HAPLORHINI; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IN VITRO STUDY; IN VIVO STUDY; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE FIBER REGENERATION; NONHUMAN; OLFACTORY ENSHEATHING CELL; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; SPECIES DIFFERENCE; SPINAL CORD INJURY; SPINAL CORD REGENERATION; SWINE;

ANIMALS; CELL PROLIFERATION; CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; DOGS; HAPLORHINI; HUMANS; OLFACTORY BULB; SCHWANN CELLS; SPECIES SPECIFICITY; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; SWINE;

EID: 79955476564     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.08.029     Document Type: Review

References (104)

1. 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.
2. Angelov D.N., Guntinas-Lichius O., Wewetzer K., Neiss W.F., Streppel M. Axonal branching and recovery of coordinated muscle activity after transection of the facial nerve in adult rats. Adv. Anat. Embryol. Cell Biol. 2005, 180:1-130.
3. Avellana-Adalid V., Bachelin C., Lachapelle F., Escriou C., Ratzkin B., Baron-Van Evercooren A. In vitro and in vivo behaviour of NDF-expanded monkey Schwann cells. Eur. J. Neurosci. 1998, 10:291-300.
4. Bachelin C., Lachapelle F., Girard C., Moissonnier P., Serguera-Lagache C., Mallet J., Fontaine D., Chojnowski A., Le Guern E., Nait-Oumesmar B., Baron-Van Evercooren A. Efficient myelin repair in the macaque spinal cord by autologous grafts of Schwann cells. Brain 2005, 128:540-549.
5. Bachelin C., Zujovic V., Buchet D., Mallet J., Baron-Van Evercooren A. Ecoptic expression of the polysialylated neural cell adhesion molecule in adult macaque Schwann cells promotes their migration and remyelination potential in the central nervous system. Brain 2010, 133:406-420.
6. 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.
7. Bianco J.I., Perry C., Harkin D.G., Mackay-Sim A., Féron F. Neurotrophin-3 promotes proliferation of olfactory ensheathing cells from human nose. Glia 2004, 45:111-123.
8. 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.
9. Bolin L.M., Iisma T.P., Shooter E.M. Isolation of activated adult Schwann cells and a spontaneous immortal Schwann cell clone. J. Neurosci. Res. 1992, 33:231-238.
10. Boyd J.G., Jahed A., McDonald T.G., Krol K.M., VanEyk 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.
11. Brockes J.P., Lemke G.E., Balzer D.R. Purification and preliminary characterization of a glial growth factor from the bovine pituitary. J. Biol. Chem. 1980, 255:8374-8377.
12. Calancie B., Madsen P.W., Marcillo A.E., Levi A.D., Bunge R.P. A guidance channel seeded with autologous Schwann cells for repair of cauda equine injury in a primate model. J. Spinal Cord Med. 2009, 32:379-388.
13. Casella G.T., Wieser R., Bunge R.P., Margitich I.S., Katz J., Olson L., Wood P.M. Density dependent regulation of human Schwann cell proliferation. Glia 2000, 30:165-177.
14. Chen J.K., Yao L.L., Jenq C.B. Mitogenic response of rat Schwann cells to fibroblast growth factors is potentiated by increased intracellular cyclic AMP levels. J. Neurosci. Res. 1991, 30:321-327.
15. Chu L., Norota I., Yomogida S., Ishii K., Endoh M. Differential inotropic effects of endothelin-1, angiotensin II, and phenylephrine induced by crosstalk with cAMP-mediated signaling process in dog ventricular myocardium. J. Pharmacol. Sci. 2004, 96:199-207.
16. Chuah M.I., Teague R. Basic fibroblast growth factor in the primary olfactory pathway: mitogenic effect on ensheathing cells. Neuroscience 1999, 88:1043-1050.
17. Courtine G., Bunge M.B., Fawcett J.W., Grossman R.G., Kaas J.H., Lemon R., Maier I., Martin J., Nudo R.J., Ramón-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.
18. 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.
19. 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.
20. Eccleston P.A., Mirsky R., Jessen K.R. Spontaneous immortalisation of Schwann cells in culture: short-term cultured Schwann cells secrete growth inhibitory activity. Development 1991, 112:33-42.
21. Emery E., Li X., Brunschwig J.P., Olson L., Levi A.D. Assessment of the malignant potential of mitogen stimulated human Schwann cells. J. Peripher. Nerv. Syst. 1999, 4:107-116.
22. 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.
23. Franklin R.J., Barnett S.C. Do olfactory glia have advantages over Schwann cells for CNS repair?. J. Neurosci. Res. 1997, 50:665-672.
24. 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.
25. Franssen E.H., De Bree F.M., Essing A.H., Ramón-Cueto A., Verhaagen J. 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.
26. Franssen E.H., Roet K.C., de Bree F.M., Verhaagen J. Olfactory ensheathing glia and Schwann cells exhibit a distinct interaction behavior with meningeal cells. J. Neurosci. Res. 2009, 87:1556-1564.
27. Fregien N.L., White L.A., Bunge M.B., Wood P. Forskolin increases neuregulin receptors in human Schwann cells without increasing receptor mRNA. Glia 2004, 49:24-35.
28. Girard C., Bemelmans A.-P., Dufour N., Mallet J., Bachelin C., Nait-Oumesmar B., Baron-van Evercooren A., Lachapelle F. Grafts of brain-derived neurotrophic factor and neurotrophin 3-transduced primate Schwann cells lead to functional recovery of the demyelinated mouse spinal cord. J. Neurosci. 2005, 25:7924-7933.
29. Goda S., Hammer J., Kobiler D., Quarles R.H. Expression of the myelin-associated glycoprotein in cultures of immortalized Schwann cells. J. Neurochem. 1991, 56:1354-1361.
30. Goméz V.M., Averill S., King V., Yang Q., Doncel-Pérez E., Chacón S.C., Ward R., Nieto-Sampedro M., Priestley J., Taylor J. Transplantation of olfactory ensheathing cells fails to promote significant axonal regeneration from dorsal roots into the cervical cord. J. Neurocytol. 2003, 32:53-70.
31. 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, 1337C:8-20.
32. Graziadei P.P., Monti Graziadei G.A. Neurogenesis and plasticity of the olfactory sensory neurons. Ann. NY Acad. Sci. 1985, 457:127-142.
33. 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.
34. Haastert K., Seef P., Stein V.M., Tipold A., Grothe C. A new cell culture protocol for enrichment and genetic modification of adult canine Schwann cells suitable for peripheral nerve tissue engineering. Res. Vet. Sci. 2009, 87:140-142.
35. Hanemann C.O., Rosenbaum C., Kupfer S., Wosch S., Stoegbauer F., Müller H.W. Improved culture methods to expand Schwann cells with altered growth behaviour from CMT1A patients. Glia 1998, 23:89-98.
36. Harvey A.R., Plant G.W. Olfactory ensheathing glia and spinal cord injury: basic mechanisms to transplantation. Future Neurol. 2006, 1:453-463.
37. 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.
38. 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.
39. Jeffery N.D., Smith P.M., Lakatos A., Ibanez C., Ito D., Franklin R.J. Clinical canine spinal cord injury provides an opportunity to examine the issues in translating laboratory techniques into practical therapy. Spinal Cord 2006, 44:584-593.
40. Jessen K.R., Mirsky R., Morgan L. Role of cyclic AMP and proliferation controls in Schwann cell differentiation. Ann. NY Acad. Sci. 1991, 633:78-89.
41. Kastner A., Gauthier P. Are rodents an appropriate pre-clinical model for treating spinal cord injury? Examples from the respiratory system?. Exp. Neurol. 2008, 213:249-256.
42. 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.
43. 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, 26:1-24.
44. Kocsis J.D. Restoration of function by glial cell transplantation into demyelinated spinal cord. J. Neurotrauma 1999, 16:695-703.
45. 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.
46. Kohama I., Lankford K.L., Preiningerova J., White F.A., Vollmer T.L., Kocsis J.D. Transplantation of cryopreserved adult human Schwann cells enhances axonal conduction in demyelinated spinal cord. J. Neurosci. 2001, 21:944-950.
47. Krudewig C., Deschl U., Wewetzer K. Purification and in vitro characterization of adult canine olfactory ensheathing cells. Cell Tissue Res. 2006, 26:687-696.
48. Langford L.A., Porter S., Bunge R.P. Immortalized rat Schwann cells produce tumours in vivo. J. Neurocytol. 1988, 17:521-529.
49. Lankford K.L., Imaizumi T., Honmou O., Kocsis J.D. A quantitative morphometric analysis of rat spinal cord remyelination following transplantation of allogeneic Schwann cells. J. Comp. Neurol. 2002, 443:259-274.
50. 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.
51. Lavdas A.A., Papastefanaki F., Thomaidou D., Matsas R. Schwann cell transplantation for CNS repair. Curr. Med. Chem. 2008, 15:151-160.
52. Lemke G.E., Brockes J.P. Identification and purification of glial growth factor. J. Neurosci. 1984, 4:75-83.
53. Levi A.D., Bunge R.P., Lofgren J.A., Meima L., Hefti F., Nikolics K., Sliwkowski M.X. The influence of heregulins on human Schwann cell proliferation. J. Neurosci. 1995, 15:1329-1340.
54. Li Y., Raisman G. Schwann cells induce sprouting in motor and sensory axons in the adult spinal cord. J. Neurosci. 1994, 14:4050-4063.
55. Li Y., Field P.M., Raisman G. Repair of adult corticospinal tract by transplants of olfactory ensheathing cells. Science 1997, 277:2000-2002.
56. 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, 29:191-206.
57. Lima C., Escada P., Pratas-Vital J., Branco C., Arcangeli C.A., Lazzeri G., Maia C.A., Capucho C., Hasse-Ferreira A., Peduzzi J.D. Olfactory mucosal autografts and rehabilitation for chronic traumatic spinal cord injury. Neurorehabil. Neural Repair 2010, 24:10-22.
58. Luo S.F., Chiu C.T., Tsao H.L., Fan L.W., Tsai C.T., Pan S.L., Yang C.M. Effect of forskolin on bradykinin-induced calcium mobilization in cultured canine tracheal smooth muscle cells. Cell. Signal. 1997, 9(2):159-167. Feb.
59. Mackay-Sim A., Féron 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.
60. Monje P.V., Bunge M.B., 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.
61. Moretto G., Kim S.U., Shin D.H., Pleasure D.E., Rizzuro N. Long-term cultures of human adult Schwann cells isolated from autopsy materials. Acta Neuropathol. 1984, 64:15-21.
62. Morgan L., Jessen K.R., Mirsky R. 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. J. Cell Biol. 1991, 112:457-467.
63. Morrissey T.K., Bunge R.P., Kleitman N. Human Schwann cells in vitro. I. Failure to differentiate and support neuronal health under co-culture conditions that promote full function of rodent cells. J. Neurobiol. 1995, 28:171-189.
64. Navarro X., Valero A., Gudiño G., Fores J., Rodriquez 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.
65. Ohsawa M., Kotani M., Tajima Y., Tsuji D., Ishibashi Y., Kuroki A., Itoh K., Watabe K., Sango K., Yamanaka S., Sakuraba H. Establishment of immortalized Schwann cellls from Sandhoff mice and corrective effect of recombinant human β-hexoaminidase A on the accumulated GM2 ganglioside. J. Hum. Genet. 2005, 50:460-467.
66. Pauls J., Nolte C., Forterre F., Brunnberg L. Cultivation and expansion of canine Schwann cells using reexplantation. Berl. Münch. Tierärztl. Wochenschr. 2004, 117:341-352.
67. 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.
68. Porter S., Clark M.B., Glaser L., Bunge R.P. Schwann cells stimulated to proliferate in the absence of neurons retain full functional capability. J. Neurosci. 1986, 6:3070-3078.
69. Porter S., Glaser L., Bunge R.P. Release of autocrine growth factor by primary and immortalized Schwann cells. Proc. Natl Acad. Sci. USA 1987, 87:7768-7772.
70. Radtke C., Wewetzer K. Translating basic research into clinical practice or what else do we have to learn about olfactory ensheathing cells?. Neurosci. Lett. 2009, 456:133-136.
71. 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.
72. 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 properties. Xeno transplantation 2010, 17:71-80.
73. Radtke C., Wewetzer K., Reimers K., Vogt P.M. Transplantation of olfactory ensheathing cells as adjunct cell therapy for peripheral nerve injury. Cell Transplant 2010b; accepted.
74. Raff M.C., Hornby-Smith A., Brockes J.P. Cyclic AMP as a mitogenic signal for cultured rat Schwann cells. Nature 1978, 273:672-673.
75. Raisman G. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 1985, 14:237-254.
76. Ramer L.M., Richter M.W., Roskams A.J., Tetzlaff W., Ramer M.S. Peripherally-derived olfactory ensheathing cells do not promote primary afferent regeneration following dorsal root injury. Glia 2004, 47:189-206.
77. 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.
78. Ramón-Cueto A., Valverde F. Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 1995, 14:163-173.
79. Ramón-Cueto A., Cordero I.M., Santos-Benito F.F., Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensgheathing glia. Neuron 2000, 25:425-435.
80. 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.
81. 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.
82. Rutkowski J.L., Kirk C.J., Lerner M.A., Tennekoon G.I. Purification and expansion of human Schwann cells in vitro. Nat. Med. 1995, 1:80-83.
83. Saberi H., Moshayedi P., Aghayan H.R., Arjmand B., Hosseini S.K., Emami-Razavi S.H., Rahimi-Movaghar V., Raza M., Firouzi M. Treatment of chronic thoracic spinal cord injury patients with autologous Schwann cell transplantation: an interim report on safety considerations and possible outcomes. Neurosci. Lett. 2008, 443:46-50.
84. Santos-Benito F.F., Ramón-Cueto A. Olfactory ensheathing glia transplantation: a therapy to promote repair in the mammalian central nervous system. Anat. Rec. 2003, 271B:77-85.
85. Saravanan K., Büssow H., Weiler N., Gieselmann V., Franken S. A spontaneously immortalized Schwann cell line to study the molecular aspects of metachromatic leukodystrophy. J. Neurosci. Methods 2007, 161:223-233.
86. Schmitte R., Tipold A., Stein V.M., Schenk H., Flieshardt C., Grothe C., Haastert K. Genetically modified canine Schwann cells - in vitro and in vivo evaluation of their suitability for peripheral nerve tissue engineering. J. Neurosci. Methods 2009, Epub ahead of print, Dec 3, 2009.
87. Schubert D. Synergistic interactions between transforming growth factor beta and fibroblast growth factor regulate Schwann cell mitosis. J. Neurobiol. 1992, 23:143-148.
88. Shen J.S., Watabe K., Meng X.L., Ida H., Ohashi T., Eto Y. Establishment and characterization of spontaneously immortalized Schwann cells from murine model of globoid cell leukodystrophy (twicher). J. Neurosci. Res. 2002, 68:588-594.
89. Shyu W.-C., Liu D.D., Lin S.-Z., Li W.-W., Su C.-Y., Chang Y.-C., Wang H.-J., Wang H.-W., Tsai C.-H., Li H. Implantation of olfactory ensheathing cells promotes neuroplasticity in murine models of stroke. J. Clin. Investig. 2008, 118:2482-2495.
90. 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.
91. Sobue G., Shuman S., Pleasure D. Schwann cell responses to cyclic AMP: proliferation, change in shape, and appearance of surface galactocerebroside. Brain Res. 1986, 362:23-32.
92. Sonigra R.J., Kandiah S.S., Wigley C.B. Spontaneous immortalisation of ensheathing cells from adult rat olfactory nerve. Glia 1996, 16:247-256.
93. Stewart H.J., Eccleston P.A., Jessen K.R., Mirsky R. Interaction between cAMP elevation, identified growth factors, and serum components in regulating Schwann cell growth. J. Neurosci. Res. 1991, 30:346-352.
94. 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 enheathing cells in long-term culture. Brain Res. 2008, 1240:31-38.
95. Techangamsuwan S., Kreutzer R., Kreutzer M., Imbschweiler I., Rohn K., Wewetzer K., Baumgärtner W. Transfection of adult canine Schwann cells and olfactory ensheathing cells at early and late passage with human TERT differentially affects growth factor responsiveness and in vitro growth. J. Neurosci. Methods 2009, 176:112-120.
96. Van den Berg L.H., Bär P.R., Sodaar P., Mollee I., Wokke J.J., Logtenberg T. Selective expansion and long-term culture of human Schwann cells from sural nerve biopsies. Ann. Neurol. 1995, 38:674-678.
97. Vincent A.J., Taylor J.M., Choi-Lundberg D.L., West A.K., Chuah M.I. Genetic expression profile of olfactory ensheathing cells is distinct from that of Schwann cells. Glia 2005, 51:132-147.
98. Watabe K., Fukuda T., Tanaka J., Honda H., Toyohara K., Sakai O. Spontaneously immortalized adult mouse Schwann cells secrete autocrine and paracrine growth-promoting activities. J. Neurosci. Res. 1995, 41:279-290.
99. Wewetzer K., Brandes G. Axonal signalling and the making of olfactory ensheathing cells: a hypothesis. Neuron Glia Biol. 2006, 2:217-224.
100. Wewetzer K., Grothe C., Claus P. In vitro expression and regulation of ciliary neurotrophic factor and its alpha receptor subunit in neonatal rat olfactory ensheathing cells. Neurosci. Lett. 2001, 306:165-168.
101. 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.
102. Wood P.M., Bunge R.P. Evidence that sensory axons are mitogenic for Schwann cells. Nature 1975, 256:662-664.
103. 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.
104. Zhang M., Schleicher R.L., Fink A.S., Gunter-Smith P., Savard C., Nguyen T., Lee S.P. Growth and function of isolated canine pancreatic ductal cells. Pancreas 2000, 20:67-76.