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
Deumens, R.; Koopmans, G. C.; Honig, W. M. M.et al.
2006 • In Experimental Neurology, 200 (1), p. 89-103
[en] Cellular transplantation, including olfactory ensheathing cells (OEC) and olfactory nerve fibroblasts (ONF), after experimental spinal cord injury in the rat has previously resulted in regrowth of severed corticospinal (CS) axons across small lesion gaps and partial functional recovery. In order to stimulate CS axon regrowth across large lesion gaps, we used a multifactorial transplantation strategy to create an OEC/ONF continuum in spinal cords with a 2-mm-long dorsal hemisection lesion gap. This strategy involved the use of aligned OEG/ONF-poly(D,L)-lactide biomatrix bridges within the lesion gap and OEC/ONF injections at I mm rostral and caudal to the lesion gap. In order to test the effects of this complete strategy, control animals only received injections with culture medium rostral and caudal to the lesion gap. Anatomically, our multifactorial intervention resulted in an enhanced presence of injured CS axons directly rostral to the lesion gap (65.0 +/- 12.8% in transplanted animals versus 13.1 +/- 3.9% in control animals). No regrowth of these axons was observed through the lesion site, which may be related to a lack of OEC/ONF survival on the biomatrices. Furthermore, a 10-fold increase of neurofilament-positive axon ingrowth into the lesion site as compared to untreated control animals was observed. With the use of quantitative gait analysis, a modest recovery in stride length and swing speed of the hind limbs was observed. Although multifactorial strategies may be needed to stimulate repair of large spinal lesion gaps, we conclude that the combined use of OEC/ONF and poly(D,L)-lactide biomatrices is rather limited.
Research Center/Unit :
Center for Education and Research on Macromolecules (CERM)
Deumens, R.; University of Maastricht > Department of Psychiatry and Neuropsychology > Division Neuroscience
Koopmans, G. C.; University of Maastricht > Department of Psychiatry and Neuropsychology > Division Neuroscience
Honig, W. M. M.; Academic Hospital Maastricht > Department of Anesthesiology
Hamers, F. P. T.; University Medical Center Utrecht, Rudolf Magnus Institute for Neuroscience > Department of Physical Medicine and Rehabilitation
Maquet, Véronique; Université de Liège - ULiège > Department of Chemistry > Center for Education and Research on Macromolecules (CERM)
Jérôme, Robert ; Université de Liège - ULiège > Department of Chemistry > Center for Education and Research on Macromolecules (CERM)
Steinbusch, H. W. M.; University of Maastricht > Department of Psychiatry and Neuropsychology > Division Neuroscience
Joosten, E. A. J.; Academic Hospital Maastricht > Department of Anesthesiology
Language :
English
Title :
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
Publication date :
July 2006
Journal title :
Experimental Neurology
ISSN :
0014-4886
eISSN :
1090-2430
Publisher :
Academic Press Inc Elsevier Science, San Diego, United States - California
Bareyre F.M., Kerschensteiner M., Raineteau O., Mettenleiter T.C., Weinmann O., and Schwab M.E. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 7 (2004) 269-277
Barnett S.C., and Chang L. Olfactory ensheathing cells and CNS repair: going solo or in need of a friend?. Trends Neurosci. 27 (2004) 54-60
Basso D.M., Beattie M.S., and Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12 (1995) 1-21
Bregman B.S., Kunkel-Bagden E., Schnell L., Dai H.N., Gao D., and Schwab M.E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378 (1995) 498-501
Brook G.A., Houweling D.A., Gieling R.G., Hermanns T., Joosten E.A., Bar D.P., Gispen W.H., Schmitt A.B., Leprince P., Noth J., and Nacimiento W. Attempted endogenous tissue repair following experimental spinal cord injury in the rat: involvement of cell adhesion molecules L1 and NCAM?. Eur. J. Neurosci. 12 (2000) 3224-3238
Bunge R.P., Puckett W.R., and Hiester E.D. Observations on the pathology of several types of human spinal cord injury, with emphasis on the astrocyte response to penetrating injuries. Adv. Neurol. 72 (1997) 305-315
Bunn H.J., Woltmann G., and Grigg J. Applicability of laser scanning cytometry to study paediatric alveolar macrophages. Eur. Respir. J. 20 (2002) 1437-1443
Chuah M.I., Choi-Lundberg D., Weston S., Vincent A.J., Chung R.S., Vickers J.C., and West A.K. Olfactory ensheathing cells promote collateral axonal branching in the injured adult rat spinal cord. Exp. Neurol. 185 (2004) 15-25
Coumans J.V., Lin T.T., Dai H.N., MacArthur L., McAtee M., Nash C., and Bregman B.S. Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J. Neurosci. 21 (2001) 9334-9344
Deumens R., Koopmans G.C., Den Bakker C.G., Maquet V., Blacher S., Honig W.M., Jerome R., Pirard J.P., Steinbusch H.W., and Joosten E.A. Alignment of glial cells stimulates directional neurite growth of CNS neurons in vitro. Neuroscience 125 (2004) 591-604
Deumens R., Koopmans G.C., and Joosten E.A. Regeneration of descending axon tracts after spinal cord injury. Prog. Neurobiol. 77 (2005) 57-89
Dusart I., and Schwab M.E. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6 (1994) 712-724
Fawcett J.W. Astrocytic and neuronal factors affecting axon regeneration in the damaged central nervous system. Cell Tissue Res. 290 (1997) 371-377
Franceschini I.A., and Barnett S.C. Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev. Biol. 173 (1996) 327-343
Goldshmit Y., Galea M.P., Wise G., Bartlett P.F., and Turnley A.M. Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J. Neurosci. 24 (2004) 10064-10073
GrandPre T., Li S., and Strittmatter S.M. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417 (2002) 547-551
Grill R., Blesch A., Gage F.H., and Tuszynski M.H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17 (1997) 5560-5572
Hamers F.P., Lankhorst A.J., van Laar T.J., Veldhuis W.B., and Gispen W.H. Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J. Neurotrauma 18 (2001) 187-201
Imaizumi T., Lankford K.L., and Kocsis J.D. Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res. 854 (2000) 70-78
Iwashita Y., Crang A.J., and Blakemore W.F. Redistribution of bisbenzimide Hoechst 33342 from transplanted cells to host cells. NeuroReport 11 (2000) 1013-1016
Joosten E.A., and Gribnau A.A. Astrocytes and guidance of outgrowing corticospinal tract axons in the rat. An immunocytochemical study using anti-vimentin and anti-glial fibrillary acidic protein. Neuroscience 31 (1989) 439-452
Joosten E.A., Veldhuis W.B., and Hamers F.P. Collagen containing neonatal astrocytes stimulates regrowth of injured fibers and promotes modest locomotor recovery after spinal cord injury. J. Neurosci. Res. 77 (2004) 127-142
Koopmans G.C., Deumens R., Honig W.M., Hamers F.P., Steinbusch H.W., and Joosten E.A. The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J. Neurotrauma 22 (2005) 214-225
Li Y., Field P.M., and Raisman G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277 (1997) 2000-2002
Li Y., Field P.M., and Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J. Neurosci. 18 (1998) 10514-10524
Li Y., Decherchi P., and Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J. Neurosci. 23 (2003) 727-731
Li Y., Field P.M., and Raisman G. Olfactory ensheathing cells and olfactory nerve fibroblasts maintain continuous open channels for regrowth of olfactory nerve fibres. Glia 52 (2005) 245-251
Lu J., Feron F., Ho S.M., Mackay-Sim A., and Waite P.M. Transplantation of nasal olfactory tissue promotes partial recovery in paraplegic adult rats. Brain Res. 889 (2001) 344-357
Mainil-Varlet P., Curtis R., and Gogolewski S. Effect of in vivo and in vitro degradation on molecular and mechanical properties of various low-molecular-weight polylactides. J. Biomed. Mater. Res. 36 (1997) 360-380
Maquet V., Martin D., Scholtes F., Franzen R., Schoenen J., Moonen G., and Jerme R. Poly(d,l-lactide) foams modified by poly(ethylene oxide)-block-poly(d,l-lactide) copolymers and a-FGF: in vitro and in vivo evaluation for spinal cord regeneration. Biomaterials 22 (2001) 1137-1146
Nash H.H., Borke R.C., and Anders J.J. Ensheathing cells and methylprednisolone promote axonal regeneration and functional recovery in the lesioned adult rat spinal cord. J. Neurosci. 22 (2002) 7111-7120
Oudega M., Vargas C.G., Weber A.B., Kleitman N., and Bunge M.B. Long-term effects of methylprednisolone following transection of adult rat spinal cord. Eur. J. Neurosci. 11 (1999) 2453-2464
Pallini R., Fernandez E., and Sbriccoli A. Retrograde degeneration of corticospinal axons following transection of the spinal cord in rats. A quantitative study with anterogradely transported horseradish peroxidase. J. Neurosurg. 68 (1988) 124-128
Pasterkamp R.J., Giger R.J., Ruitenberg M.J., Holtmaat A.J., De Wit J., De Winter F., and Verhaagen J. Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol. Cell. Neurosci. 13 (1999) 143-166
Perez-Bouza A., Wigley C.B., Nacimiento W., Noth J., and Brook G.A. Spontaneous orientation of transplanted olfactory glia influences axonal regeneration. NeuroReport 9 (1998) 2971-2975
Plant G.W., Christensen C.L., Oudega M., and Bunge M.B. Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. J. Neurotrauma 20 (2003) 1-16
Raisman G. Olfactory ensheathing cells-Another miracle cure for spinal cord injury?. Nat. Rev., Neurosci. 2 (2001) 369-375
Ramon-Cueto A., and Avila J. Olfactory ensheathing glia: properties and function. Brain Res. Bull. 46 (1998) 175-187
Ramon-Cueto A., and Nieto-Sampedro M. Glial cells from adult rat olfactory bulb: immunocytochemical properties of pure cultures of ensheathing cells. Neuroscience 47 (1992) 213-220
Ramon-Cueto A., Cordero M.I., Santos-Benito F.F., and Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25 (2000) 425-435
Richardson P.M., Issa V.M., and Aguayo A.J. Regeneration of long spinal axons in the rat. J. Neurocytol. 13 (1984) 165-182
Sasaki M., Lankford K.L., Zemedkun M., and Kocsis J.D. Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J. Neurosci. 24 (2004) 8485-8493
Schnell L., and Schwab M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343 (1990) 269-272
Schnell L., and Schwab M.E. Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur. J. Neurosci. 5 (1993) 1156-1171
Schnell L., Schneider R., Kolbeck R., Barde Y.A., and Schwab M.E. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367 (1994) 170-173
Starkey M.L., Hamers F.F., Doherty P., McMahon S.B., and Bradbury E.J. Assessing behavioural function following unilateral lesion of the corticospinal tract in adult mice. Program No 43102004 Abstract Viewer/Itinerary Planner (2004), Society for Neuroscience, Washington, DC
von Meyenburg J., Brosamle C., Metz G.A., and Schwab M.E. Regeneration and sprouting of chronically injured corticospinal tract fibers in adult rats promoted by NT-3 and the mAb IN-1, which neutralizes myelin-associated neurite growth inhibitors. Exp. Neurol. 154 (1998) 583-594
Wagner Jr. F.C., VanGilder J.C., and Dohrmann G.J. Pathological changes from acute to chronic in experimental spinal cord trauma. J. Neurosurg. 48 (1978) 92-98
Woodhouse A., Vincent A.J., Kozel M.A., Chung R.S., Waite P.M., Vickers J.C., West A.K., and Chuah M.I. Spinal cord tissue affects ensheathing cell proliferation and apoptosis. NeuroReport 16 (2005) 737-740
