Transplantation of olfactory ensheathing cells promotes axonal regeneration and functional recovery of peripheral nerve lesion in rats

Muscle and Nerve

Volumn 43, Issue 4, 2011, Pages 543-551

  Guérout, Nicolas ^a   Duclos, Célia ^a   Drouot, Laurent ^a   Abramovici, Olivia ^a   Bon Mardion, Nicolas ^a,b   Lacoume, Yann ^a   Jean, Laetitia ^a   Boyer, Olivier ^a   Marie, Jean Paul ^a,b  

^a UNIVERSITÉ DE ROUEN   (France)

^b HÔPITAL CHARLES NICOLLE   (France)

Author keywords

Axonal regrowth; Neurotrophic factors; Olfactory ensheathing cells; Peripheral nerve; Regeneration

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; GASTROCNEMIUS MUSCLE; MUSCLE STRENGTH; NERVE REGENERATION; NONHUMAN; OLFACTORY BULB; PERIPHERAL NERVE INJURY; PERIPHERAL NERVE LESION; PHENOTYPE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE CULTURE; ANIMAL; CELL CULTURE; CELL TRANSPLANTATION; COMPARATIVE STUDY; CONVALESCENCE; CYTOLOGY; FISCHER 344 RAT; MALE; NERVE FIBER; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SCIATIC NEUROPATHY; TRANSPLANTATION;

ANIMALS; AXONS; CELL TRANSPLANTATION; CELLS, CULTURED; MALE; MUSCLE STRENGTH; NERVE REGENERATION; OLFACTORY BULB; RATS; RATS, INBRED F344; RECOVERY OF FUNCTION; SCIATIC NEUROPATHY;

EID: 79151469143     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.21907     Document Type: Article

References (45)

1. Graziadei GA, Graziadei PP. Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol 1979;8:197-213. (Pubitemid 9175213)
2. Graziadei PP, Graziadei GA. 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.
3. Calof AL, Chikaraishi DM. Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 1989;3:115-127.
4. Mackay-Sim A, Kittel P. Cell dynamics in the adult mouse olfactory epithelium: a quantitative autoradiographic study. J Neurosci 1991;11:979-984.
5. Devon R, Doucette R. Olfactory ensheathing cells myelinate dorsal root ganglion neurites. Brain Res 1992;589:175-179.
6. Ramon-Cueto A, Avila J. Olfactory ensheathing glia: properties and function. Brain Res Bull 1998;46:175-187. (Pubitemid 28293162)
7. Li Y, Field PM, Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 1998;18:10514-10524. (Pubitemid 29016571)
8. Choi D, Raisman G. Disorganization of the facial nucleus after nerve lesioning and regeneration in the rat: effects of transplanting candidate reparative cells to the site of injury. Neurosurgery 2005;56:1093-1100.
9. Franklin RJ, Barnett SC. Olfactory ensheathing cells and CNS regeneration: the sweet smell of success? Neuron 2000;28:15-18.
10. Franceschini IA, Barnett SC. Low-affinity NGF-receptor and E-NCAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol 1996;173:327-343. (Pubitemid 26063429)
11. Boyd JG, Doucette R, Kawaja MD. Defining the role of olfactory ensheathing cells in facilitating axon remyelination following damage to the spinal cord. FASEB J 2005;19:694-703. (Pubitemid 40617374)
12. Chung RS, Woodhouse A, Fung S, Dickson TC, West AK, Vickers JC, et al. Olfactory ensheathing cells promote neurite sprouting of injured axons in vitro by direct cellular contact and secretion of soluble factors. Cell Mol Life Sci 2004;61:1238-1245. (Pubitemid 38703753)
13. Franklin RJ. Remyelination by transplanted olfactory ensheathing cells. Anat Rec B New Anat 2003;271:71-76. (Pubitemid 37248096)
14. Moreno-Flores MT, Diaz-Nido J, Wandosell F, Avila J. Olfactory ensheathing glia: drivers of axonal regeneration in the central nervous system? J Biomed Biotechnol 2002;2:37-43.
15. Lipson AC, Widenfalk J, Lindqvist E, Ebendal T, Olson L. Neurotrophic properties of olfactory ensheathing glia. Exp Neurol 2003;180:167-171. (Pubitemid 36398171)
16. Boruch AV, Conners JJ, Pipitone M, Deadwyler G, Storer PD, Devries GH, et al. Neurotrophic and migratory properties of an olfactory ensheathing cell line. Glia 2001;33:225-229. (Pubitemid 32219131)
17. Woodhall E, West AK, Chuah MI. 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. (Pubitemid 32274278)
18. 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.
19. Lakatos A, Smith PM, Barnett SC, Franklin RJ. Meningeal cells enhance limited CNS remyelination by transplanted olfactory ensheathing cells. Brain 2003;126:598-609. (Pubitemid 36240861)
20. Guntinas-Lichius O, Wewetzer K, Tomov TL, Azzolin N, Kazemi S, Streppel M, et al. Transplantation of olfactory mucosa minimizes axonal branching and promotes the recovery of vibrissae motor performance after facial nerve repair in rats. J Neurosci 2002;22:7121-7131. (Pubitemid 35379167)
21. Guntinas-Lichius O, Angelov DN, Tomov TL, Dramiga J, Neiss WF, Wewetzer K. Transplantation of olfactory ensheathing cells stimulates the collateral sprouting from axotomized adult rat facial motoneurons. Exp Neurol 2001;172:70-80. (Pubitemid 33141155)
22. Radtke C, Aizer AA, Agulian SK, Lankford KL, Vogt PM, Kocsis JD. Transplantation of olfactory ensheathing cells enhances peripheral nerve regeneration after microsurgical nerve repair. Brain Res 2009;1254:10-17.
23. Hood B, Levene HB, Levi AD. Transplantation of autologous Schwann cells for the repair of segmental peripheral nerve defects. Neurosurg Focus 2009;26:E4.
24. Ramon-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.
25. Laquerriere A, Peulve P, Jin O, Tiollier J, Tardy M, Vaudry H, et al. Effect of basic fibroblast growth factor and alpha-melanocytic stimulating hormone on nerve regeneration through a collagen channel. Microsurgery 1994;15:203-210. (Pubitemid 24153068)
26. Franssen EH, de Bree FM, 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. (Pubitemid 350100870)
27. Dombrowski MA, Sasaki M, Lankford KL, Kocsis JD, Radtke C. Myelination and nodal formation of regenerated peripheral nerve fibers following transplantation of acutely prepared olfactory ensheathing cells. Brain Res 2006;1125:1-8. (Pubitemid 44838544)
28. Li Y, Sauve Y, Li D, Lund RD, Raisman G. Transplanted olfactory ensheathing cells promote regeneration of cut adult rat optic nerve axons. J Neurosci 2003;23:7783-7788. (Pubitemid 37052346)
29. Franklin RJ, Gilson JM, Franceschini IA, Barnett SC. Schwann celllike myelination following transplantation of an olfactory bulbensheathing cell line into areas of demyelination in the adult CNS. Glia 1996;17:217-224. (Pubitemid 26309432)
30. Imaizumi T, Lankford KL, Waxman SG, Greer CA, Kocsis JD. 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. (Pubitemid 28373225)
31. Ramon-Cueto A, Plant GW, Avila J, Bunge MB. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci 1998;18: 3803-3815. (Pubitemid 28225687)
32. Sasaki M, Black JA, Lankford KL, Tokuno HA, Waxman SG, Kocsis JD. Molecular reconstruction of nodes of Ranvier after remyelination by transplanted olfactory ensheathing cells in the demyelinated spinal cord. J Neurosci 2006;26:1803-1812. (Pubitemid 43236993)
33. Deumens R, Koopmans GC, Honig WM, Hamers FP, Maquet V, Jerome R, et al. 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 2006;200:89-103. (Pubitemid 44080749)
34. 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.
35. Pellitteri R, Spatuzza M, Russo A, Zaccheo D, Stanzani S. Olfactory ensheathing cells represent an optimal substrate for hippocampal neurons: an in vitro study. Int J Dev Neurosci 2009;27:453-458.
36. Runyan SA, Phelps PE. Mouse olfactory ensheathing glia enhance axon outgrowth on a myelin substrate in vitro. Exp Neurol 2009;216:95-104.
37. Doncel-Perez E, Caballero-Chacon S, Nieto-Sampedro M. Neurosphere cell differentiation to aldynoglia promoted by olfactory ensheathing cell conditioned medium. Glia 2009.
38. Shukla S, Chaturvedi RK, Seth K, Roy NS, Agrawal AK. Enhanced survival and function of neural stem cells-derived dopaminergic neurons under influence of olfactory ensheathing cells in parkinsonian rats. J Neurochem 2009;109:436-451.
39. Agrawal AK, Shukla S, Chaturvedi RK, Seth K, Srivastava N, Ahmad A, et al. Olfactory ensheathing cell transplantation restores functional deficits in rat model of Parkinson's disease: a cotransplantation approach with fetal ventral mesencephalic cells. Neurobiol Dis 2004;16:516-526. (Pubitemid 38942984)
40. Srivastava N, Seth K, Khanna VK, Ansari RW, Agrawal AK. Long-term functional restoration by neural progenitor cell transplantation in rat model of cognitive dysfunction: co-transplantation with olfactory ensheathing cells for neurotrophic factor support. Int J Dev Neurosci 2009;27:103-110.
41. Pan HC, Cheng FC, Chen CJ, Lai SZ, Lee CW, Yang DY, et al. Postinjury regeneration in rat sciatic nerve facilitated by neurotrophic factors secreted by amniotic fluid mesenchymal stem cells. J Clin Neurosci 2007;14:1089-1098.
42. Stoll G, Muller HW. Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol 1999;9:313-325. (Pubitemid 29157718)
43. Streppel M, Azzolin N, Dohm S, Guntinas-Lichius O, Haas C, Grothe C, et al. Focal application of neutralizing antibodies to soluble neurotrophic factors reduces collateral axonal branching after peripheral nerve lesion. Eur J Neurosci 2002;15:1327-1342. (Pubitemid 35477994)
44. Araki T, Milbrandt J. Ninjurin, a novel adhesion molecule, is induced by nerve injury and promotes axonal growth. Neuron 1996; 17:353-361. (Pubitemid 26296161)
45. Cao L, Zhu YL, Su Z, Lv B, Huang Z, He C, et al. Olfactory ensheathing cells promote migration of Schwann cells by secreted nerve growth factor. Glia 2007;55:897-904. (Pubitemid 46903990)