Comparison of bulbar and mucosal olfactory ensheathing cells using FACS and simultaneous antigenic bivariate cell cycle analysis

GLIA

Volumn 59, Issue 11, 2011, Pages 1658-1671

  Kueh, Jacqueline Li Ling ^a,b   Raisman, Geoffrey ^a   Li, Ying ^a   Stevens, Robert ^b   Li, Daqing ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b RUTHERFORD APPLETON LABORATORY   (United Kingdom)

Author keywords

Adult; Culture; Flow cytometry; P75; Repair; Stem cells; Thy1; Transplant

Indexed keywords

FIBRONECTIN; PROTEIN P75;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIVARIATE ANALYSIS; CELL CULTURE; CELL CYCLE; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; MOUSE; NONHUMAN; OLFACTORY ENSHEATHING CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; FIBROBLASTS; FLOW CYTOMETRY; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; OLFACTORY BULB; OLFACTORY MUCOSA; RATS; RECEPTOR, NERVE GROWTH FACTOR;

EID: 80052791749     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21213     Document Type: Article

References (64)

1. Au E, Roskams AJ. 2002. Culturing olfactory ensheathing glia from the mouse olfactory epithelium. Methods Mol Biol 198: 49-54.
2. Au E, Roskams AJ. 2003. Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 41: 224-236.
3. Au WW, Treloar HB, Greer CA. 2002. Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446: 68-80.
4. Barnett SC, Alexander CL, Iwashita Y, Gilson JM, Crowther J, Clark L, Dunn LT, Papanastassiou V, Kennedy PG, Franklin RJ. 2000. Identification of a human olfactory ensheathing cell that can effect transplant-mediated remyelination of demyelinated CNS axons. Brain 123: 1581-1588.
5. Barnett SC, Chang L. 2004. Olfactory ensheathing cells and CNS repair: Going solo or in need of a friend? Trends Neurosci 27: 54-60.
6. Barnett SC, Roskams AJ. 2008. Olfactory ensheathing cells: Isolation and culture from the neonatal olfactory bulb. Methods Mol Biol 438: 85-94.
7. Bianco JI, Perry C, Harkin DG, Mackay-Sim A, Féron F. 2004. Neurotrophin 3 promotes purification and proliferation of olfactory ensheathing cells from human nose. Glia 45: 111-123.
8. Booth BW, Mack DL, Androutsellis-Theotokis A, McKay RD, Boulanger CA, Smith GH. 2008. The mammary microenvironment alters the differentiation repertoire of neural stem cells. Proc Natl Acad Sci USA 105: 14891-14896.
9. Carter LA, MacDonald JL, Roskams AJ. 2004. Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci 24: 5670-5683.
10. Choi D, Law S, Raisman G, Li D. 2008. Olfactory ensheathing cells in the nasal mucosa of the rat and human. Br J Neurosurg 22: 301-302.
11. Chuah MI, Au C. 1993. Cultures of ensheathing cells from neonatal rat olfactory bulbs. Brain Res 601: 213-220.
12. Chuah MI, Choi-Lundberg D, Weston S, Vincent AJ, Chung RS, Vickers JC, West AK. 2004. Olfactory ensheathing cells promote collateral axonal branching in the injured adult rat spinal cord. Exp Neurol 185: 15-25.
13. Chuah MI, Hale DM, West AK. 2010. Interaction of olfactory ensheathing cells with other cell types in vitro and after transplantation: Glial scars and inflammation. Exp Neurol 229:46-53.
14. Delorme B, Nivet E, Gaillard J, Haupl T, Ringe J, Deveze A, Magnan J, Sohier J, Khrestchatisky M, Roman FS, Charbord P, Sensebe L, Layrolle P, Feron F. 2010. The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev 19: 853-866.
15. Deumens R, Koopmans GC, Honig WM, Hamers FP, Maquet V, Jerome R, Steinbusch HW, Joosten EA. 2006. 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 200: 89-103.
16. Doucette JR. 1984. The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat Rec 210: 385-391.
17. Feron F, Mackay-Sim A, Andrieu JL, Matthaei KI, Holley A, Sicard G. 1999. Stress induces neurogenesis in non-neuronal cell cultures of adult olfactory epithelium. Neuroscience 88: 571-583.
18. Féron F, Perry C, McGrath JJ, Mackay-Sim A. 1998. New techniques for biopsy and culture of human olfactory epithelial neurons. Arch Otolaryngol Head Neck Surg 124: 861-866.
19. Franssen EH, De Bree FM, Essing AH, Ramon-Cueto A, Verhaagen J. 2008. Comparative gene expression profiling of olfactory ensheathing glia and Schwann cells indicates distinct tissue repair characteristics of olfactory ensheathing glia. Glia 56: 1285-1298.
20. Garcia-Escudero V, Garcia-Gomez A, Gargini R, Martin-Bermejo MJ, Langa E, de Yebenes JG, Delicado A, Avila J, Moreno-Flores MT, Lim F. 2010a. Prevention of senescence progression in reversibly immortalized human ensheathing glia permits their survival after deimmortalization. Mol Ther 18: 394-403.
21. Garcia-Escudero V, Gargini R, Gallego-Hernandez MT, Garcia-Gomez A, Martin-Bermejo MJ, Simon D, Delicado A, Moreno-Flores MT, Avila J, Lim F. 2010b. A neuroregenerative human ensheathing glia cell line with conditional rapid growth. Cell Transplant 20:153-166.
22. Gong Q, Bailey MS, Pixley SK, Ennis M, Liu W, Shipley MT. 1994. Localization and regulation of low affinity nerve growth factor receptor expression in the rat olfactory system during development and regeneration. J Comp Neurol 344: 336-348.
23. Guerout N, Derambure C, Drouot L, Bon-Mardion N, Duclos C, Boyer O, Marie JP. 2010. Comparative gene expression profiling of olfactory ensheathing cells from olfactory bulb and olfactory mucosa. Glia 58: 1570-1580.
24. Guest JD, Herrera L, Margitich I, Oliveria M, Marcillo A, Casas CE. 2008. 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 212: 261-274.
25. Hai M, Muja N, DeVries GH, Quarles RH, Patel PI. 2002. Comparative analysis of Schwann cell lines as model systems for myelin gene transcription. J Neurosci Res 69: 497-508.
26. Harper LJ, Costea DE, Gammon L, Fazil B, Biddle A, Mackenzie IC. 2010. Normal and malignant epithelial cells with stem-like properties have an extended G2 cell cycle phase that is associated with apoptotic resistance. BMC Cancer 10: 166.
27. Holbrook EH, Szumowski KEM, Schwob JE. 1995. An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium. J Comp Neurol 363: 129-146.
28. Huang H, Chen L, Xi H, Wang H, Zhang J, Zhang F, Liu Y. 2008. Fetal olfactory ensheathing cells transplantation in amyotrophic lateral sclerosis patients: A controlled pilot study. Clin Transplant 22: 710-718.
29. Ito D, Ibanez C, Ogawa H, Franklin RJ, Jeffery ND. 2006. Comparison of cell populations derived from canine olfactory bulb and olfactory mucosal cultures. Am J Vet Res 67: 1050-1056.
30. Jani HR, Raisman G. 2004. Ensheathing cell cultures from the olfactory bulb and mucosa. Glia 47: 130-137.
31. Jessen KR, Mirsky R. 1997. Embryonic Schwann cell development: The biology of Schwann cell precursors and early Schwann cells. J Anat 191: 501-505.
32. Li Y, Field PM, Raisman G. 1997. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277: 2000-2002.
33. Li Y, Field PM, Raisman G. 1998. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 18: 10514-10524.
34. Li Y, Decherchi P, Raisman G. 2003. Transplantation of Olfactory Ensheathing Cells into Spinal Cord Lesions Restores Breathing and Climbing. J Neurosci 23: 727-731.
35. Li Y, Li D, Khaw PT, Raisman G. 2008. Transplanted olfactory ensheathing cells incorporated into the optic nerve head ensheathe retinal ganglion cell axons: possible relevance to glaucoma. Neurosci Lett 440: 251-254.
36. Lindsay SL, Riddell JS, Barnett SC. 2010. Olfactory mucosa for transplant-mediated repair: A complex tissue for a complex injury? Glia 58: 125-134.
37. Llamusi MB, Rubio MP, Ramon-Cueto A. 2010. Telomerase protects adult rodent olfactory ensheathing glia from early senescence. Exp Neurol 229:54-64.
38. Mackay-Sim A, St. John JA. 2010. Olfactory ensheathing cells from the nose: Clinical application in human spinal cord injuries. Exp Neurol 229: 174-180.
39. Murrell W, Féron F, Wetzig A, Cameron N, Splatt K, Bellette B, Bianco J, Perry C, Lee G, Mackay-Sim A. 2005. Multipotent stem cells from adult olfactory mucosa. Dev Dyn 233: 496-515.
40. Nash HH, Borke RC, Anders JJ. 2001. New method of purification for establishing primary cultures of ensheathing cells from the adult olfactory bulb. Glia 34: 81-87.
41. Novikova LN, Lobov S, Wiberg M, Novikov LN. 2010. Efficacy of olfactory ensheathing cells to support regeneration after spinal cord injury is influenced by method of culture preparation. Exp Neurol 229: 132-142.
42. Novikova LN, Lobov S, Wiberg M, Novikov LN. 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.
43. Pollock GS, Franceschini IA, Graham G, Marchionni MA, Barnett SC. 1999. Neuregulin is a mitogen and survival factor for olfactory bulb ensheathing cells and an isoform is produced by astrocytes. Eur J Neurosci 11: 769-780.
44. Pool M, Thiemann J, Bar-Or A, Fournier AE. 2008. NeuriteTracer: A novel ImageJ plugin for automated quantification of neurite outgrowth. J Neurosci Meth 168: 134-139.
45. Radtke C, Akiyama Y, Brokaw J, Lankford KL, Wewetzer K, Fodor WL, Kocsis JD. 2004. Remyelination of the nonhuman primate spinal cord by transplantation of H-transferase transgenic adult pig olfactory ensheathing cells. FASEB J 18: 335-337.
46. Raisman G. 1985. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14: 237-254.
47. Raisman G, Li Y. 2007. Repair of neural pathways by olfactory ensheathing cells. Nat Rev Neurosci 8: 312-319.
48. Ramón-Cueto A, Plant GW, Avila J, Bunge MB. 1998. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci 18: 3803-3815.
49. Richter M, Westendorf K, Roskams AJ. 2008. Culturing olfactory ensheathing cells from the mouse olfactory epithelium. Methods Mol Biol 438: 95-102.
50. Richter MW, Fletcher PA, Liu J, Tetzlaff W, Roskams AJ. 2005. Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J Neurosci 25: 10700-10711.
51. Richter MW, Roskams AJ. 2008. Olfactory ensheathing cell transplantation following spinal cord injury: Hype or hope? Exp Neurol 209: 353-367.
52. Rubio MP, Munoz-Quiles C, Ramon-Cueto A. 2008. Adult olfactory bulbs from primates provide reliable ensheathing glia for cell therapy. Glia 56: 539-551.
53. Santos-Benito FF, Ramon-Cueto A. 2003. Olfactory ensheathing glia transplantation: A therapy to promote repair in the mammalian central nervous system. Anat Rec B New Anat 271: 77-85.
54. Soleimani M, Nadri S, Salehi M, Sobhani A, Hajarizadeh A. 2008. Characterization of fibroblast-like cells from the rat olfactory bulb. Int J Dev Biol 52: 979-984.
55. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB. 2002. Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22: 6670-6681.
56. Tomé M, Lindsay SL, Riddell JS, Barnett SC. 2009. Identification of nonepithelial multipotent cells in the embryonic olfactory mucosa. Stem Cells 27: 2196-2208.
57. Turner CP, Perez-Polo JR. 1992. Regulation of the low affinity receptor for nerve growth factor, p75NGFR, in the olfactory system of neonatal and adult rat. Int J Dev Neurosci 10: 343-359.
58. Turner CP, Perez-Polo JR. 1994. Changes in expression of the low affinity receptor for neurotrophins, p75NGFR, in the regenerating olfactory system. Int J Dev Neurosci 12: 767-773.
59. Werbowetski-Ogilvie TE, Bosse M, Stewart M, Schnerch A, Ramos-Mejia V, Rouleau A, Wynder T, Smith MJ, Dingwall S, Carter T, Williams C, Harris C, Dolling J, Wynder C, Boreham D, Bhatia M. 2009. Characterization of human embryonic stem cells with features of neoplastic progression. Nat Biotechnol 27: 91-97.
60. Wewetzer K, Brandes G. 2007. Axonal signalling and the making of olfactory ensheathing cells: A hypothesis. Neuron Glia Biol 2: 217-224.
61. Wewetzer K, Radtke C, Kocsis J, Baumgartner W. 2010. 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.
62. Windus LC, Lineburg KE, Scott SE, Claxton C, Mackay-Sim A, Key B, St. John JA. 2010. Lamellipodia mediate the heterogeneity of central olfactory ensheathing cell interactions. Cell Mol Life Sci 67: 1735-1750.
63. Yamamoto M, Raisman G, Li D, Li Y. 2009. Transplanted olfactory mucosal cells restore paw reaching function without regeneration of severed corticospinal tract fibres across the lesion. Brain Res 1303: 26-31.
64. Yui S, Ito D, Fujita N, Nishimura R. 2011. Effects of fibroblasts derived from the olfactory bulb and nasal olfactory mucosa on proliferation of olfactory ensheathing cells harvested from the olfactory bulb. J Vet Med Sci 73: 133-137.