Olfactory ensheathing cells, but not schwann cells, proliferate and migrate extensively within moderately X-Irradiated juvenile rat brain

GLIA

Volumn 62, Issue 1, 2014, Pages 52-63

  Lankford, Karen L ^a,b   Brown, Robert J ^a,b   Sasaki, Masanori ^a,b,c   Kocsis, Jeffery D ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cell migration; CNS; Hippocampus; X irradiation

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN; BRAIN CORTEX; BRAIN STEM; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSPLANTATION; CEREBELLUM; CHOROID PLEXUS; CONTROLLED STUDY; CORPUS CALLOSUM; DENTATE GYRUS; DISPERSION; FEMALE; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; JUVENILE ANIMAL; LATERAL BRAIN VENTRICLE; MALE; MICROGLIA; NONHUMAN; OLFACTORY BULB; OLFACTORY ENSHEATHING CELL; PERICYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; SPINAL CORD; STEREOLOGY; SUBVENTRICULAR ZONE; X IRRADIATION;

CELL MIGRATION; CNS; HIPPOCAMPUS; X-IRRADIATION;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS; ANTIGENS, CD11B; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; MALE; NEUROGLIA; OLFACTORY MUCOSA; OLIGODENDROGLIA; PROTEOGLYCANS; RADIATION INJURIES, EXPERIMENTAL; RATS; RATS, SPRAGUE-DAWLEY; SCHWANN CELLS; STEM CELL TRANSPLANTATION;

EID: 84888132955     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22583     Document Type: Article

References (53)

1. Andrews MR, Stelzner DJ. 2007. Evaluation of olfactory ensheathing and Schwann cells after implantation into a dorsal injury of adult rat spinal cord. J Neurotrauma 24:1773-1792.
2. Atkinson SL, Li YQ, Wong CS. 2005. Apoptosis and proliferation of oligodendrocyte progenitor cells in the irradiated rodent spinal cord. Int J Radiat Oncol Biol Phys 62:535-544.
3. Bachelin C, Zujovic V, Buchet D, Mallet J, Baron-Van Evercooren A. 2010. Ectopic expression of polysialylated neural cell adhesion molecule in adult macaque Schwann cells promotes their migration and remyelination potential in the central nervous system. Brain 133:406-420.
4. Bambakidis NC, Miller RH. 2004. Transplantation of oligodendrocyte precursors and sonic hedgehog results in improved function and white matter sparing in the spinal cords of adult rats after contusion. Spine J 4:16-26.
5. Barakat DJ, Gaglani SM, Neravetla SR, Sanchez AR, Andrade CM, Pressman Y, Puzis R, Garg MS, Bunge MB, Pearse, DD. 2005. Survival, integration, and axon growth support of glia transplanted into the chronically contused spinal cord. Cell Transplant 14:225-240.
6. Baron-Van Evercooren A, Clerin-Duhamel E, Lapie P, Gansmüller A, Lachapelle F, Gumpel M. 1992 The fate of Schwann cells transplanted in the brain during development. Dev Neurosci 14:73-84.
7. Baron-Van Evercooren A, Duhamel-Clerin E, Boutry JM, Hauw J.J, Gumpel M. 1993. Pathways of migration of transplanted Schwann cells in the demyelinated mouse spinal cord. J Neurosci Res 35:428-438.
8. Boruch AV, Conners JJ, Pipitone M, Deadwyler G, Storer PD, Devries GH, Jones KJ. 2001. Neurotrophic and migratory properties of an olfactory ensheathing cell line. Glia 33:225-229.
9. Brush J, Lipnick SL, Phillips T, Sitko J, McDonald JT, McBride WH. 2007. Molecular mechanisms of late normal tissue injury. Semin Radiat Oncol 17:121-130.
10. Chari DM, Blakemore WF. 2002. Efficient recolonisation of progenitor-depleted areas of the CNS by adult oligodendrocyte progenitor cells. Glia 37:307-313.
11. Chuah MI, Tennent R, Jacobs I. 1995. Response of olfactory Schwann cells to intranasal zinc sulfate irrigation. J Neurosci Res 42:470-478.
12. Coderre JA, Morris GM, Micca PL, Hopewell JW, Verhagen I, Kleiboer BJ, van der Kogel AJ. 2006. Late effects of radiation on the central nervous system: Role of vascular endothelial damage and glial stem cell survival. Radiat Res 166:495-503.
13. Ferrer I, Olive M, Blanco R, Ballabriga J, Cinós C, Planas AM. 1995. Amoeboid microglial response following X-ray-induced apoptosis in the neonatal rat brain. Neurosci Lett 193:109-112.
14. Franklin RJ, Bayley SA, Blakemore WF. 1996. Transplanted CG4 cells (an oligodendrocyte progenitor cell line survive, migrate, and contribute to repair of areas of demyelination in X-irradiated and damaged spinal cord but not in normal spinal cord. Exp Neurol 137:263-276.
15. Ghosh M, Tuesta LM, Puentes R, Patel S, Melendez K, El Maarouf A, Rutishauser U, Pearse DD. 2012. Extensive cell migration, axon regeneration, and improved function with polysialic acid-modified Schwann cells after spinal cord injury. Glia 60:979-992.
16. Gorrie CA, Hayward I, Cameron N, Kailainathan G, Nandapalan N, Sutharsan R, Wang J, Mackay-Sim A, Waite PM. 2010. Effects of human OEC-derived cell transplants in rodent spinal cord contusion injury. Brain Res 1337:8-20.
17. Gutin PH, McDermott MW, Ross G, Chan PH, Chen SF, Levin KJ, Babuna O, Marton LJ. 1990. Polyamine accumulation and vasogenic oedema in the genesis of late delayed radiation injury of the central nervous system (CNS). Acta Neurochir Suppl (Wien) 51:372-374.
18. Hellstrom NA, Björk-Eriksson T, Blomgren K, Kuhn HG. 2009. Differential recovery of neural stem cells in the subventricular zone and dentate gyrus after ionizing radiation. Stem Cells 27:634-641.
19. Hinks GL, Chari DM, O'Leary MT, Zhao C, Keirstead HS, Blakemore WF, Franklin RJ. 2001. Depletion of endogenous oligodendrocyte progenitors rather than increased availability of survival factors is a likely explanation for enhanced survival of transplanted oligodendrocyte progenitors in X-irradiated compared with normal CNS. Neuropathol Appl Neurobiol 27:59-67.
20. Hwang SY, Jung JS, Kim TH, Lim SJ, Oh ES, Kim JY, Ji KA, Joe EH, Cho KH, Han IO. 2006. Ionizing radiation induces astrocyte gliosis through microglia activation. Neurobiol Dis 21:457-467.
21. Irvine KA, Blakemore WF. 2007. A different regional response by mouse oligodendrocyte progenitor cells (OPCs) to high-dose X-irradiation has consequences for repopulating OPC-depleted normal tissue. Eur J Neurosci 25:417-424.
22. Imaizumi T, Lankford KL, Kocsis JD. 2000. Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res 854:70-78.
23. Iwashita Y, Blakemore WF. 2000. Areas of demyelination do not attract significant numbers of Schwann cells transplanted into normal white matter. Glia 31:232-240.
24. Kocsis JD, Lankford, KL, Sasaki M, Radtke C. 2009, Unique in vivo properties of olfactory ensheathing cells that may contribute to neural repair and protection following spinal cord injury. Neurosci Lett 456:137-142.
25. Lakatos A, Franklin RJ, Barnett SC. 2000. Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 32:214-225.
26. Lavdas AA, Franceschini I, Dubois-Dalcq M, Matsas R. 2006. Schwann cells genetically engineered to express PSA show enhanced migratory potential without impairment of their myelinating ability in vitro. Glia 53:868-878.
27. Lankford KL, Imaizumi T, Honmou O, Kocsis JD. 2002. A quantitative morphometric analysis of rat spinal cord remyelination following transplantation of allogenic Schwann cells. J Comp Neurol 443:259-274.
28. Lankford KL, Sasaki M, Radtke C, Kocsis JD. 2008. Olfactory ensheathing cells exhibit unique migratory, phagocytic, and myelinating properties in the X-irradiated spinal cord not shared by Schwann cells. Glia 56:1664-1678.
29. Li Y, Field PM, and Raisman G. 1998. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 18:10514-10524.
30. Li BC, Li Y, Chen LF, Chang JY, Duan ZX. 2011. Olfactory ensheathing cells can reduce the tissue loss but not the cavity formation in contused spinal cords of rats. J Neurol Sci 303:67-74.
31. Lu P, Yang H, Culbertson M, Graham L, Roskams AJ, Tuszynski MH. 2006. Olfactory ensheathing cells do not exhibit unique migratory or axonal growth-promoting properties after spinal cord injury. J Neurosci 26:11120-11130.
32. Manda K, Ueno M, Anzai K. 2009. Cranial irradiation-induced inhibition of neurogenesis in hippocampal dentate gyrus of adult mice: Attenuation by melatonin pretreatment. J Pineal Res 46:71-78.
33. McGinn MJ, Sun D, Colello RJ. 2008. Utilizing X-irradiation to selectively eliminate neural stem/progenitor cells from neurogenic regions of the mammalian brain. J Neurosci Methods 170:9-15.
34. Naylor AS, Bull C, Nilsson MK, Zhu C, Björk-Eriksson T, Eriksson PS, Blomgren K, Kuhn HG. 2008. Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain. Proc Natl Acad Sci USA 105:14632-14637.
35. Noble M, and Dietrich J. 2002. Intersections between neurobiology and oncology: Tumor origin, treatment and repair of treatment-associated damage. Trends Neurosci 25:103-107.
36. Papastefanaki F, Chen J, Alexandros A. Lavdas AA, Thomaidou D, Schachner M, Matsas R. 2007. Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain 130:2159-2174.
37. Perry A, Schmidt RE. 2006. Cancer therapy-associated CNS neuropathology: An update and review of the literature. Acta Neuropathol 111:197-212.
38. Peterson K, Rosenblum MK, Powers JM, Alvord E, Walker RW, Posner JB. 1993. Effect of brain irradiation on demyelinating lesions. Neurology 43:2105-2112.
39. Pinjuh D, Bedi KS. 2003. X-irradiation of adult spinal cord increases its capacity to support neurite regeneration in vitro. Int J Dev Neurosci 21:409-416.
40. Plant GW, Christensen CL, Oudega M, Bunge MB. 2003. Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. J Neurotrauma 20:1-16.
41. Ramon-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.
42. Sasaki M, Lankford KL, Radtke C, Honmou O, Kocsis JD. 2011. Remyelination after olfactory ensheathing cell transplantation into diverse demyelinating environments. Exp Neurol l229:88-98.
43. Sasaki, M, Black JA, Lankford KL, Tokuno HA, Waxman SG, Kocsis JD. 2006. Molecular reconstruction of nodes of Ranvier after remyelination by transplanted olfactory ensheathing cells in the demyelinated spinal cord. J Neurosci 26:1803-1812.
44. Sasaki, M, Lankford KL, Zemedkun M, Kocsis JD. 2004. Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J Neurosci 24:8485-84993.
45. Schultheiss TE, Stephens LC. 1992. Permanent radiation myelopathy. British J Radiol 65:737-753.
46. Shi L, Molina DP, Robbins ME, Wheeler KT, Brunso-Bechtold JK. 2008. Hippocampal neuron number is unchanged 1 year after fractionated whole-brain irradiation at middle age. Int J Radiat Oncol Biol Phys 71:526-532.
47. Stamegna JC, Felix MS, Roux-Peyronnet J, Rossi V, Féron F, Gauthier P, Matarazzo V. 2011. Nasal OEC transplantation promotes respiratory recovery in a subchronic rat model of cervical spinal cord contusion. Exp Neurol 229:120-131.
48. Su Z, Yuan Y, Chen J, Cao L, Zhu Y, Gao L, Qiu Y, He C. 2009. Reactive astrocytes in glial scar attract olfactory ensheathing cells migration by secreted TNF-alpha in spinal cord lesion of rat. PLoS One 4:e8141.
49. Vincent AJ, Choi-Lundberg DL, Harris JA, West AK, Chuah MI. 2007. Bacteria and PAMPs activate nuclear factor kappaB and Gro production in a subset of olfactory ensheathing cells and astrocytes but not in Schwann cells. Glia 55:905-916.
50. Wewetzer K, Kern N, Ebel C, Radtke C, Brandes G. 2005. Phagocytosis of O4+ axonal fragments in vitro by p75- neonatal rat olfactory ensheathing cells. Glia 49:577-587.
51. Woodhall E, West AK, Chuah MI. 2001. 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 88:203-213.
52. Woodhoo A, Sahni V, Gilson J, Setzu A, Franklin RJ, Blakemore WF, Mirsky R, Jessen KR. 2007. Schwann cell precursors: A favourable cell for myelin repair in the central nervous system. Brain 130:2175-2185.
53. Zujovic V, Bachelin C, Baron-Van Evercooren A. 2007. Remyelination of the central nervous system: A valuable contribution from the periphery. Neuroscientist 3:383-391.