Clinical prospects for transplantation of OECs in the repair of brachial and lumbosacral plexus injuries: Opening a door

Experimental Neurology

Volumn 229, Issue 1, 2011, Pages 168-173

  Raisman, Geoffrey ^a   Carlstedt, Thomas ^a,b   Choi, David ^a   Li, Ying ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Adult regeneration; Motor; Sensory; Spinal roots; Translation

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE;

BRACHIAL PLEXUS; BRACHIAL PLEXUS INJURY; CELL ADHESION; CELL MIGRATION; CELL TRANSPLANTATION; DEAFFERENTATION PAIN; DORSAL ROOT; HUMAN; LUMBOSACRAL PLEXUS; LUMBOSACRAL PLEXUS INJURY; MOTONEURON; MUSCLE INNERVATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE INJURY; NERVE SPROUTING; NEUROPATHIC PAIN; NONHUMAN; OLFACTORY ENSHEATHING CELL TRANSPLANTATION; PRIORITY JOURNAL; PROPRIOCEPTION; REVIEW; SPINAL CORD REGENERATION; SYNKINESIS; TOUCH; VENTRAL ROOT;

ANIMALS; AXONS; BRACHIAL PLEXUS; CELL TRANSPLANTATION; HUMANS; LUMBOSACRAL PLEXUS; OLFACTORY BULB; SPINAL NERVE ROOTS;

EID: 79151479159     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.05.007     Document Type: Review

References (56)

1. Berman J., Anand P., Chen L., Taggart M., Birch R. Pain relief from preganglionic injury to the brachial plexus by late intercostal nerve transfer. J. Bone Joint Surg. Br. 1996, 78:759-760.
2. Blits B., Carlstedt T.P., Ruitenberg M.J., W.F.de., Hermens W.T., Dijkhuizen P.A., Claasens J.W., Eggers R., van der S.R., Tenenbaum L., Boer G.J., Verhaagen J. Rescue and sprouting of motoneurons following ventral root avulsion and reimplantation combined with intraspinal adeno-associated viral vector-mediated expression of glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor. Exp. Neurol. 2004, 189:303-316.
3. Bostock H. U-turns in rat ventral roots. J. Physiol. 1981, 312:49-50.
4. Cajal S.R. Degeneration and regeneration of the nervous system 1928, Hafner, New York.
5. Carlstedt T. Central nerve plexus injury 2007, Imperial College Press, London.
6. Carlstedt T. Nerve root replantation. Neurosurg. Clin. N. Am. 2009, 20:39-50. vi.
7. Carlstedt T., Hultgren T., Nyman T., Hansson T. Cortical activity and hand function restoration in a patient after spinal cord surgery. Nat. Rev. Neurol. 2009, 5:571-574.
8. Chew D.J., Leinster V.H., Sakthithasan M., Robson L.G., Carlstedt T., Shortland P.J. Cell death after dorsal root injury. Neurosci. Lett. 2008, 433:231-234.
9. Choi D., Li D., Law S., Powell M., Raisman G. A prospective observational study of the yield of olfactory ensheathing cells cultured from biopsies of septal nasal mucosa. Neurosurgery 2008, 62:1140-1144.
10. Choi D., Raisman G. Immune rejection of a facial nerve xenograft does not prevent regeneration and the return of function: an experimental study. Neuroscience 2003, 121:501-507.
11. 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.
12. Chong M.S., Woolf C.J., Haque N.S.K., Anderson P.N. Axonal regeneration from injured dorsal roots into the spinal cord of adult rats. J. Comp. Neurol. 1999, 410:42-54.
13. David, S. and Aguayo, A. J., 1981. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats Sci 214, 931-933.
14. Doucette J.R. The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat. Rec. 1984, 210:385-391.
15. Fraher J.P. The CNS-PNS transitional zone of the rat. Morphometric studies at cranial and spinal levels. Prog. Neurobiol. 1992, 38:261-316.
16. Graziadei P.P.C., Levine R.R., Montigraziadei G.A. Plasticity of connections of the olfactory sensory neuron: regeneration into the forebrain following bulbectomy in the neonatal mouse. Neuroscience 1979, 4:713-727.
17. Graziadei P.P.C., Montigraziadei G.A. Neurogenesis and neuron regeneration in the olfactory system of mammals. 3. Deafferentation and reinnervation of the olfactory bulb following section of the fila-olfactoria in rat. J. Neurocytol. 1980, 9:145-162.
18. Guntinas-Lichius O., Wewetzer K., Tomov T.L., Azzolin N., Kazemi S., Streppel M., Neiss W.F., Angelov D.N. 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.
19. Gutmann E., Young J.Z. The re-innervation of muscle after various periods of atrophy. J. Anat. 1944, 78:15-43.
20. Hallin R.G., Carlstedt T., Nilsson-Remahl I., Risling M. Spinal cord implantation of avulsed ventral roots in primates; correlation between restored motor function and morphology. Exp. Brain Res. 1999, 124:304-310.
21. Havton L.A., Carlstedt T. Repair and rehabilitation of plexus and root avulsions in animal models and patients. Curr. Opin. Neurol. 2009, 22:570-574.
22. Hoang T.X., Nieto J.H., Dobkin B.H., Tillakaratne N.J., Havton L.A. Acute implantation of an avulsed lumbosacral ventral root into the rat conus medullaris promotes neuroprotection and graft reinnervation by autonomic and motor neurons. Neuroscience 2006, 138:1149-1160.
23. Hoang T.X., Nieto J.H., Tillakaratne N.J., Havton L.A. Autonomic and motor neuron death is progressive and parallel in a lumbosacral ventral root avulsion model of cauda equina injury. J. Comp. Neurol. 2003, 467:477-486.
24. Htut M., Misra P., Anand P., Birch R., Carlstedt T. Pain phenomena and sensory recovery following brachial plexus avulsion injury and surgical repairs. J. Hand Surg. Br. 2006, 31:596-605.
25. Huang H., Chen L., Xi H., Wang H., Zhang J., Zhang F., Liu Y. Fetal olfactory ensheathing cells transplantation in amyotrophic lateral sclerosis patients: a controlled pilot study. Clin. Transplant. 2008, 22:710-718.
26. Huard J.M.T., Youngentob S.L., Goldstein B.J., Luskin M.B., Schwob J.E. Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J. Comp. Neurol. 1998, 400:469-486.
27. Ibrahim A., Raisman G., Li Y. Permanent loss of fore-paw grasping requires complete deprivation of afferent input from a minimum of four dorsal roots of the rat brachial plexus. Exp. Neurol. 2009, 215:142-145.
28. Ibrahim A.G., Kirkwood P.A., Raisman G., Li Y. Restoration of hand function in a rat model of repair of brachial plexus injury. Brain 2009, 132:1268-1276.
29. Kaas J.H., Merzenich M.M., Killackey H.P. The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Annu. Rev. Neurosci. 1983, 6:325-356.
30. Kliot M., Smith G.M., Siegal J.D., Silver J. Astrocyte-polymer implants promote regeneration of dorsal root fibers into the adult mammalian spinal cord. Exp. Neurol. 1990, 109:57-69.
31. Li Y., Carlstedt T., Berthold C.-H., Raisman G. Interaction of transplanted olfactory-ensheathing cells and host astrocytic processes provides a bridge for axons to regenerate across the dorsal root entry zone. Exp. Neurol. 2004, 188:300-308.
32. Li Y., Decherchi P., Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J. Neurosci. 2003, 23:727-731.
33. Li Y., Field P.M., Raisman G. Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J. Neurosci. 1998, 18:10514-10524.
34. Li Y., Yamamoto M., Raisman G., Choi D., Carlstedt T. An experimental model of ventral root repair showing the beneficial effect of transplanting olfactory ensheathing cells. Neurosurgery 2007, 60:734-740.
35. Linda H., Risling M., Cullheim S. 'Dendraxons' in regenerating motoneurons in the cat: do dendrites generate new axons after central axotomy?. Brain Res. 1985, 358:329-333.
36. Lindsay S.L., Riddell J.S., Barnett S.C. Olfactory mucosa for transplant-mediated repair: a complex tissue for a complex injury?. Glia 2010, 58:125-134.
37. Liu C.N., Chambers W.W. Intraspinal sprouting of dorsal root axons; development of new collaterals and preterminals following partial denervation of the spinal cord in the cat AMA. Arch. Neurol. Psychiatry 1958, 79:46-61.
38. Lundborg G., Rosén B. Hand function after nerve repair. Acta Physiol. 2007, 189:207-217. Oxf.
39. Mackay-Sim A., Feron F., Cochrane J., Bassingthwaighte L., Bayliss C., Davies W., Fronek P., Gray C., Kerr G., Licina P., Nowitzke A., Perry C., Silburn P.A., Urquhart S., Geraghty T. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 2008, 131:2376-2386.
40. Mackay-Sim A., Kittel P.W. On the life span of olfactory receptor neurons. Eur. J. Neurosci. 1991, 3:209-215.
41. McMahon S.B., Kett-White R. Sprouting of peripherally regenerating primary sensory neurones in the adult central nervous system. J. Comp. Neurol. 1991, 304:307-315.
42. Raisman G. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 1985, 14:237-254.
43. Ramer L.M., Richter M.W., Roskams A.J., Tetzlaff W., Ramer M.S. Peripherally-derived olfactory ensheathing cells do not promote primary afferent regeneration following dorsal root injury. Glia 2004, 47:189-206.
44. Ramer M.S., Bishop T., Dockery P., Mobarak M.S., O'Leary D., Fraher J.P., Priestley J.V., McMahon S.B. Neurotrophin-3-mediated regeneration and recovery of proprioception following dorsal rhizotomy. Mol. Cell. Neurosci. 2002, 19:239-249.
45. Ramón-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.
46. Ramón-Cueto A., Nieto-Sampedro M. Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp. Neurol. 1994, 127:232-244.
47. Richardson P.M., McGuinness U.M., Aguayo A.J. Peripheral nerve autografts to the rat spinal cord: studies with axonal tracing methods. Brain Res. 1982, 237:147-162.
48. Richter M.W., Fletcher P.A., Liu J., Tetzlaff W., Roskams A.J. Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J. Neurosci. 2005, 25:10700-10711.
49. Riddell J.S., Enriquez-Denton M., Toft A., Fairless R., Barnett S.C. Olfactory ensheathing cell grafts have minimal influence on regeneration at the dorsal root entry zone following rhizotomy. Glia 2004, 47:150-167.
50. Shortland P., Woolf C.J. Chronic peripheral nerve section results in a rearrangement of the central axonal arborizations of axotomized A beta primary afferent neurons in the rat spinal cord. J. Comp. Neurol. 1993, 330:65-82.
51. Sulaiman O.A., Gordon T. Role of chronic Schwann cell denervation in poor functional recovery after nerve injuries and experimental strategies to combat it. Neurosurgery 2009, 65:105-114.
52. Toft A., Scott D.T., Barnett S.C., Riddell J.S. Electrophysiological evidence that olfactory cell transplants improve function after spinal cord injury. Brain 2007, 130:970-984.
53. Valverde F., Lopez-Mascaraque L. Neuroglial arrangements in the olfactory glomeruli of the hedgehog. J. Comp. Neurol. 1991, 307:658-674.
54. Wang R., King T., Ossipov M.H., Rossomando A.J., Vanderah T.W., Harvey P., Cariani P., Frank E., Sah D.W., Porreca F. Persistent restoration of sensory function by immediate or delayed systemic artemin after dorsal root injury. Nat. Neurosci. 2008, 11:488-496.
55. Windus L.C., Lineburg K.E., Scott S.E., Claxton C., Mackay-Sim A., Key B., St John J.A. Lamellipodia mediate the heterogeneity of central olfactory ensheathing cell interactions. Cell. Mol. Life Sci. 2010, 67:1735-1750.
56. Yamamoto M., Raisman G., Li D.Q., Li Y. Transplanted olfactory mucosal cells restore paw reaching function without regeneration of severed corticospinal tract fibres across the lesion. Brain Res. 2009, 1303:26-31.