Olfactory ensheathing cell-neurite alignment enhances neurite outgrowth in scar-like cultures

Experimental Neurology

Volumn 269, Issue , 2015, Pages 93-101

  Khankan, Rana R ^a   Wanner, Ina B ^a   Phelps, Patricia E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocytes; Cell adhesion; Meningeal fibroblasts; Neurite outgrowth; OEC; Reactive astrocytes; Spinal cord injury

Indexed keywords

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL CONTACT; CELL ELONGATION; CONTROLLED STUDY; FIBROBLAST; NERVE CELL CULTURE; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; OLFACTORY ENSHEATHING CELL; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; ANIMAL; BRAIN CORTEX; CELL CULTURE; COCULTURE; CYTOLOGY; NERVE CELL; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURITE; OLFACTORY BULB; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SCAR;

ANIMALS; ASTROCYTES; CELLS, CULTURED; CEREBRAL CORTEX; CICATRIX; COCULTURE TECHNIQUES; NERVE REGENERATION; NEURITES; NEUROGENESIS; NEURONS; OLFACTORY BULB; RATS; SPINAL CORD INJURIES;

EID: 84927761267     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.03.025     Document Type: Article

References (65)

1. Akins M.R., Benson D.L., Greer C.A. Cadherin expression in the developing mouse olfactory system. J. Comp. Neurol. 2007, 501:483-497.
2. Barnabé-Heider F., Göritz C., Sabelström H., Takebayashi H., Pfrieger F.W., Meletis K., Frisén J. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 2010, 7:470-482.
3. Barrett C.P., Guth L., Donati E.J. Astroglial reaction in the gray matter of lumbar segments after midthoracic transection of the adult rat spinal cord. Exp. Neurol. 1981, 73:365-377.
4. Bixby J.L., Zhang R. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J. Cell Biol. 1990, 110:1253-1260.
5. Bradbury E.J., Moon L.D.F., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
6. Burda J., Ao Y., Gao F., Coppola G., Sofroniew M. Defining the astrocyte CSPG and ECM transcriptome in vivo by cell-type specific analysis of actively translated mRNA. Program No. 705.21. Neuroscience 2014 Abstracts 2014, Society for Neuroscience, Washington, D.C., (Online).
7. Buss A., Pech K., Kakulas B.A., Martin D., Schoenen J., Noth J., Brook G.A. NG2 and phosphacan are present in the astroglial scar after human traumatic spinal cord injury. BMC Neurol. 2009, 9:32.
8. Castellani V., Chédotal A., Schachner M., Faivre-Sarrailh C., Rougon G. Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 2000, 27:237-249.
9. Chandler C.E., Parsons L.M., Hosang M., Shooter E.M. A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J. Biol. Chem. 1984, 259:6882-6889.
10. Chung R.S., Woodhouse A., Fung S., Dickson T.C., West A.K., Vickers J.C., Chuah M.I. 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.
11. Crandall J.E., Dibble C., Butler D., Pays L., Ahmad N., Kostek C., Püschel A.W., Schwarting G.A. Patterning of olfactory sensory connections is mediated by extracellular matrix proteins in the nerve layer of the olfactory bulb. J. Neurobiol. 2000, 45:195-206.
12. Davies S.J., Fitch M.T., Memberg S.P., Hall A.K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997, 390:680-683.
13. De Wit J., De Winter F., Klooster J., Verhaagen J. Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix. Mol. Cell. Neurosci. 2005, 29:40-55.
14. Doucette R. Glial influences on axonal growth in the primary olfactory system. Glia 1990, 3:433-449.
15. Doucette R. PNS-CNS transitional zone of the first cranial nerve. J. Comp. Neurol. 1991, 312:451-466.
16. Ellis E.F., McKinney J.S., Willoughby K.A., Liang S., Povlishock J.T. A new model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J. Neurotrauma 1995, 12:325-339.
17. Fairless R., Frame M.C., Barnett S.C. N-cadherin differentially determines Schwann cell and olfactory ensheathing cell adhesion and migration responses upon contact with astrocytes. Mol. Cell. Neurosci. 2005, 28:253-263.
18. Fitch M.T., Silver J. CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp. Neurol. 2008, 209:294-301.
19. Göritz C., Dias D.O., Tomilin N., Barbacid M., Shupliakov O., Frisén J. A pericyte origin of spinal cord scar tissue. Science 2011, 333:238-242.
20. Graziadei P.P., Monti Graziadei G.A. Neurogenesis and plasticity of the olfactory sensory neurons. Ann. N. Y. Acad. Sci. 1985, 457:127-142.
21. Grimpe B., Pressman Y., Lupa M.D., Horn K.P., Bunge M.B., Silver J. The role of proteoglycans in Schwann cell/astrocyte interactions and in regeneration failure at PNS/CNS interfaces. Mol. Cell. Neurosci. 2005, 28:18-29.
22. Guérout N., Derambure C., Drouot L., Bon-Mardion N., Duclos C., Boyer O., Marie J.-P. Comparative gene expression profiling of olfactory ensheathing cells from olfactory bulb and olfactory mucosa. Glia 2010, 58:1570-1580.
23. Hu R., Zhou J., Luo C., Lin J., Wang X., Li X., Bian X., Li Y., Wan Q., Yu Y., Feng H. Glial scar and neuroregeneration: histological, functional, and magnetic resonance imaging analysis in chronic spinal cord injury. J. Neurosurg. Spine 2010, 13:169-180.
24. Imai T., Yamazaki T., Kobayakawa R., Kobayakawa K., Abe T., Suzuki M., Sakano H. Pre-target axon sorting establishes the neural map topography. Science 2009, 325:585-590.
25. Kafitz K.W., Greer C.A. Olfactory ensheathing cells promote neurite extension from embryonic olfactory receptor cells in vitro. Glia 1999, 25:99-110.
26. Kiryushko D., Berezin V., Bock E. Regulators of neurite outgrowth: role of cell adhesion molecules. Ann. N. Y. Acad. Sci. 2004, 1014:140-154.
27. Kubasak M.D., Jindrich D.L., Zhong H., Takeoka A., McFarland K.C., Muñoz-Quiles C., Roy R.R., Edgerton V.R., Ramón-Cueto A., Phelps P.E. OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats. Brain 2008, 131:264-276.
28. 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.
29. Li Y., Li D., Raisman G. Interaction of olfactory ensheathing cells with astrocytes may be the key to repair of tract injuries in the spinal cord: the "pathway hypothesis". J. Neurocytol. 2005, 34:343-351.
30. Li Y., Li D., Ibrahim A., Raisman G. Repair involves all three surfaces of the glial cell. Prog. Brain Res. 2012, 201:199-218.
31. Lipson A.C., Widenfalk J., Lindqvist E., Ebendal T., Olson L. Neurotrophic properties of olfactory ensheathing glia. Exp. Neurol. 2003, 180:167-171.
32. López-Vales R., Forés J., Navarro X., Verdú E. Olfactory ensheathing glia graft in combination with FK506 administration promote repair after spinal cord injury. Neurobiol. Dis. 2006, 24:443-454.
33. Lu J., Féron F., Mackay-Sim A., Waite P.M.E. Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain 2002, 125:14-21.
34. McKeon R.J., Höke A., Silver J. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp. Neurol. 1995, 136:32-43.
35. Miragall F., Kadmon 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.
36. Morgenstern D.A., Asher R.A., Fawcett J.W. Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 2002, 137:313-332.
37. Niclou S.P., Franssen E.H.P., Ehlert E.M.E., Taniguchi M., Verhaagen J. Meningeal cell-derived semaphorin 3A inhibits neurite outgrowth. Mol. Cell. Neurosci. 2003, 24:902-912.
38. Pasterkamp R.J., De Winter F., Holtmaat A.J., Verhaagen J. Evidence for a role of the chemorepellent semaphorin III and its receptor neuropilin-1 in the regeneration of primary olfactory axons. J. Neurosci. 1998, 18:9962-9976.
39. Pasterkamp R.J., Anderson P.N., Verhaagen J. Peripheral nerve injury fails to induce growth of lesioned ascending dorsal column axons into spinal cord scar tissue expressing the axon repellent Semaphorin3A. Eur. J. Neurosci. 2001, 13:457-471.
40. 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.
41. Ramón-Cueto A., Valverde F. Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 1995, 14:163-173.
42. Ramón-Cueto A., Plant G.W., Avila J., Bunge M.B. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci. 1998, 18:3803-3815.
43. Ramón-Cueto A., Cordero M.I.I., Santos-Benito F.F., Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000, 25:425-435.
44. Reier P.J., Houle J.D. The glial scar: its bearing on axonal elongation and transplantation approaches to CNS repair. Adv. Neurol. 1988, 47:87-138.
45. Roet K.C.D., Franssen E.H.P., de Bree F.M., Essing A.H.W., Zijlstra S.-J.J., Fagoe N.D., Eggink H.M., Eggers R., Smit A.B., van Kesteren R.E., Verhaagen J. A multilevel screening strategy defines a molecular fingerprint of proregenerative olfactory ensheathing cells and identifies SCARB2, a protein that improves regenerative sprouting of injured sensory spinal axons. J. Neurosci. 2013, 33:11116-11135.
46. Ruitenberg M.J., Plant G.W., Hamers F.P.T., Wortel J., Blits B., Dijkhuizen P.A., Gispen W.H., Boer G.J., Verhaagen J. Ex vivo adenoviral vector-mediated neurotrophin gene transfer to olfactory ensheathing glia: effects on rubrospinal tract regeneration, lesion size, and functional recovery after implantation in the injured rat spinal cord. J. Neurosci. 2003, 23:7045-7058.
47. Runyan S.A., Phelps P.E. Mouse olfactory ensheathing glia enhance axon outgrowth on a myelin substrate in vitro. Exp. Neurol. 2009, 216:95-104.
48. Schwarting G.A., Kostek C., Ahmad N., Dibble C., Pays L., Püschel A.W. Semaphorin 3A is required for guidance of olfactory axons in mice. J. Neurosci. 2000, 20:7691-7697.
49. Shearer M.C., Niclou S.P., Brown D., Asher R.A., Holtmaat A.J.G.D., Levine J.M., Verhaagen J., Fawcett J.W. The astrocyte/meningeal cell interface is a barrier to neurite outgrowth which can be overcome by manipulation of inhibitory molecules or axonal signalling pathways. Mol. Cell. Neurosci. 2003, 24:913-925.
50. Shields S.D., Moore K.D., Phelps P.E., Basbaum A.I. Olfactory ensheathing glia express aquaporin 1. J. Comp. Neurol. 2010, 518:4329-4341.
51. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
52. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009, 32:638-647.
53. Sonigra R.J., Brighton P.C., Jacoby J., Hall S., Wigley C.B. Adult rat olfactory nerve ensheathing cells are effective promoters of adult central nervous system neurite outgrowth in coculture. Glia 1999, 25:256-269.
54. Tabakow P., Raisman G., Fortuna W., Czyz M., Huber J., Li D., Szewczyk P., Okurowski S., Miedzybrodzki R., Czapiga B., Salomon B., Halon A., Li Y., Lipiec J., Kulczyk A., Jarmundowicz W. Functional regeneration of supraspinal connections in a patient with transected spinal cord following transplantation of bulbar olfactory ensheathing cells with peripheral nerve bridging. Cell Transplant. 2014, 23:1631-1655.
55. Takeoka A., Jindrich D.L., Muñoz-Quiles C., Zhong H., van den Brand R., Pham D.L., Ziegler M.D., Ramón-Cueto A., Roy R.R., Edgerton V.R., Phelps P.E. Axon regeneration can facilitate or suppress hindlimb function after olfactory ensheathing glia transplantation. J. Neurosci. 2011, 31:4298-4310.
56. Wanner I.B. An in vitro trauma model to study rodent and human astrocyte reactivity. Methods Mol. Biol. 2012, 814:189-219.
57. Wanner I.B., Wood P.M. N-cadherin mediates axon-aligned process growth and cell-cell interaction in rat Schwann cells. J. Neurosci. 2002, 22:4066-4079.
58. Wanner I.B., Guerra N.K., Mahoney J., Wood P.M., Mirsky R., Jessen K.R. The role of glial N-cadherin in Schwann cell precursors of growing nerves. Glia 2006, 54:439-459.
59. Wanner I.B., Deik A., Torres M., Rosendahl A., Neary J.T., Lemmon V.P., Bixby J.L. A new in vitro model of the glial scar inhibits axon growth. Glia 2008, 56:1691-1709.
60. Wanner I.B., Anderson M.A., Song B., Levine J., Fernandez A., Gray-Thompson Z., Ao Y., Sofroniew M.V. Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal cord injury. J. Neurosci. 2013, 33:12870-12886.
61. Witheford M., Westendorf K., Roskams A.J. Olfactory ensheathing cells promote corticospinal axonal outgrowth by a L1 CAM-dependent mechanism. Glia 2013, 61:1873-1889.
62. Woodhall E., West A.K., Chuah M.I. 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.
63. Yoshida K., Rutishauser U., Crandall J.E., Schwarting G.A. Polysialic acid facilitates migration of luteinizing hormone-releasing hormone neurons on vomeronasal axons. J. Neurosci. 1999, 19:794-801.
64. Ziegler M.D., Hsu D., Takeoka A., Zhong H., Ramón-Cueto A., Phelps P.E., Roy R.R., Edgerton V.R. Further evidence of olfactory ensheathing glia facilitating axonal regeneration after a complete spinal cord transection. Exp. Neurol. 2011, 229:109-119.
65. Zuo J., Neubauer D., Dyess K., Ferguson T.A., Muir D. Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp. Neurol. 1998, 154:654-662.