Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants

Journal of Neuroscience

Volumn 18, Issue 10, 1998, Pages 3803-3815

  Ramón Cueto, Almudena ^a,b   Plant, Giles W ^a   Avila, Jesus ^b   Bunge, Mary Bartlett ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Axonal regeneration; Immunohistochemistry; Olfactory ensheathing glia; Spinal cord injury; Transplantation; WGA HRP

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NEUROFILAMENT PROTEIN; NEUROMODULIN; SEROTONIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GLIA CELL; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; OLFACTORY EPITHELIUM; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; SPINAL CORD TRANSSECTION; TISSUE TRANSPLANTATION;

AGE FACTORS; ANIMALS; AXONS; CELL MOVEMENT; CELLS, CULTURED; CORDOTOMY; DENERVATION; FEMALE; MYELIN SHEATH; NERVE REGENERATION; NEUROGLIA; OLFACTORY BULB; RATS; RATS, INBRED F344; SCHWANN CELLS; SCIATIC NERVE; SPINAL CORD; SPINAL CORD INJURIES; WHEAT GERM AGGLUTININ-HORSERADISH PEROXIDASE CONJUGATE;

EID: 0000635530     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Baird A, Klagsbrun M (1991) The fibroblast growth factor family. Ann NY Acad Sci 638:239-243.
2. Bandtlow C, Zachleder T, Schwab ME (1990) Oligodendrocytes arrest neurite growth by contact inhibition. J Neurosci 10:3837-3848.
3. Baron-Van Evercooren A, Gansmuller A, Clerin E, Gumpel M (1991) Hoechst 33342 a suitable fluorescent marker for Schwann cells after transplantation in the mouse spinal cord. Neurosci Lett 131:241-244.
4. Bixby JL, Lilien J, Reichardt LF (1988) Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J Cell Biol 107:353-361.
5. Bovolenta P, Wandosell F, Nieto-Sampedro M (1992) CNS glial scar tissue: a source of molecules which inhibit central neurite outgrowth. Prog Brain Res 94:367-379.
6. Bregman BS, Kunkel-Bagden E, Schnell L, Dai HN, Gao D, Schwab ME (1995) Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378:498-501.
7. Caroni P, Schwab ME (1988) Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J Cell Biol 106:1281-1288.
8. Chen A, Xu XM, Kleitman N, Bunge M (1996) Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp Neurol 138:261-276.
9. Cheng H, Cao Y, Oison L (1996) Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273:510-513.
10. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76.
11. Cummings DM, Brunjes PC (1995) Migrating luteinizing hormone-releasing hormone (LHRH) neurons and processes are associated with a substrate that expresses S100. Dev Brain Res 88:148-157.
12. David S, Aguayo AJ (1981) Axonal elongation into peripheral nervous system bridges after central nervous system injury in adult rats. Science 214:931-933.
13. Doucette JR, Kiernan JA, Flumerfelt BA (1983) The re-innervation of olfactory glomeruli following transection of primary olfactory axons in the central or peripheral nervous system. J Anat 137:1-19.
14. Doucette R (1091) PNS-CNS transitional zone of the first cranial nerve. J Comp Neurol 312:451-466.
15. Eaton MJ, Whittemore SR (1996) Autocrine BDNF secretion enhances the survival and serotonergic differentiation of raphe neuronal precursor cells grafted into the adult rat CNS. Exp Neurol 140:105-114.
16. Fawcett JW, Keynes RJ (1990) Peripheral nerve regeneration. Annu Rev Neurosci 13:43-60.
17. Fernaud-Espinosa I. Nieto-Sampedro M, Bovolenta P (1993) Differential activation of microglia and astrocytes in aniso- and isomorphic gliotic tissue. Glia 8:277-291.
18. Franceschini IA, Barnett SC (1996) Low-affinity NGF-receptor and E-N-CAM expression define two types of olfactory nerve ensheathing cells that share a common lineage. Dev Biol 173:327-343.
19. Gibson S, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, McGregor GP, Morrison JFB, Kelly JS, Evans RM, Rosenfeld MG (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4:3101-3111.
20. Giulian D (1993) Reactive glia as rivals in regulating neuronal survival. Glia 7:102-110.
21. Graziadei P, Monti Graziadei G (1980) Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria in rat. J Neurocytol 9:145-162.
22. Guénard VN, Xu XM, Bunge MB (1993) The use of Schwann cell transplantation to foster central nervous system repair. Semin Neurosci 5:401-411.
23. Guest JD, Rao A, Olson E, Bunge MB, Bunge RP (1997) The ability of human Schwann cell grafts to promote regeneration in the transected nude rat spinal cord. Exp Neurol 148:502-522.
24. Hagg T, Vahlsing HL, Manthorpe M, Varon S (1990) Septohippocampal cholinergic axonal regeneration through peripheral nerve bridges: quantification and temporal development. Exp Neurol 109:153-163.
25. Harvey AR, Chen M, Plant GW, Dyson SE (1994) Regrowth of axons within Schwann cell-filled polycarbonate tubes implanted into the damaged optic tract and cerebral cortex of rats. Rest Neurol Neurosci 6:221-237.
26. Hatten ME, Liem RKH, Shelanski ME, Mason C (1991) Astroglia in CNS injury. Glia 4:233-243.
27. Kalderon N, Fuks Z (1996) Severed corticospinal axons recover electrophysiologic control of muscle activity after x-ray therapy in lesioned adult spinal cord. Proc Natl Acad Sci USA 93:11185-11190.
28. Kott JN, Westrum EE, Raines EW, Sasahara M, Ross R (1994) Olfactory ensheathing glia and platelet-derived growth factor B-chain reactivity in the transplanted rat olfactory bulb. Int J Dev Neurosci 12:315-323.
29. Kromer LF, Cornbrooks CJ (1985) Transplants of Schwann cell cultures promote axonal regeneration in the adult mammalian brain. Proc Natl Acad Sci USA 82:6330-6334.
30. Li Y, Field PM, Raisman G (1997) Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277:2000-2002.
31. Liesi P (1985) Eaminin immunoreactive glia distinguish regenerative adult CNS systems from non-regenerative ones. EMBO J 4:2505-2511.
32. Liuzzi FJ, Lasek RJ (1987) Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway. Science 237:642-645.
33. Menei P, Montero-Menei C, Whittemore SR, Bunge RP, Bunge MB (1998) Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. Eur J Neurosci 10:607-621.
34. Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106-117.
35. Miragall F, Kadmon G, Husmann M, Schachner M (1988) Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of N-CAM. Dev Biol 129:516-531.
36. Mocchetti I, Rabin SJ, Colangelo AM, Whittemore SR, Wrathall JR (1996) Increased basic fibroblast growth factor expression following contusive spinal cord injury. Exp Neurol 141:154-164.
37. Montgomery CT, Robson JA (1993) Implants of cultured Schwann cells support axonal growth in the central nervous system of adult rats. Exp Neurol 122:107-124.
38. Morrissey TK, Kleitman N, Bunge RP (1991) Isolation and functional characterization of Schwann cells isolated from adult peripheral nerves. J Neurosci 11:2433-2442.
39. Nakahara Y, Gage FH, Tuszynski MH (1996) Grafts of fibroblasts genetically modified to secrete NGF, BDNF, NT-3, or basic FGF elicit differential responses in the adult spinal cord. Cell Transplant 5:191-204.
40. Newton BW, Hamill RW (1988) The morphology and distribution of rat serotoninergic intraspinal neurons: an immunohistochemical study. Brain Res Bull 20:349-360.
41. Newton BW, Hamill RW (1989) Immunohistochemical distribution of serotonin in spinal autonomic nuclei. I. Fiber patterns in the adult rat. J Comp Neurol 279:68-81.
42. Onno T, Saito H, Kishimoto T, Okumoto T, Miyamoto K (1991) Stimulation of biosynthesis of nerve growth factor by acidic fibroblast growth factor in cultured mouse astrocytes. Neurosci Lett 126:18-20.
43. Oudega M, Hagg T (1996) Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp Neurol 140:218-229.
44. Petroski RE, Grierson JP, Choi-Kwon S, Geller HM (1991) Basic fibroblast growth factor regulates the ability of astrocytes to support hypothalamic neuronal survival. Dev Biol 147:1-13.
45. Raivich G, Kreutzberg GW (1993) Peripheral nerve regeneration: role of growth factors and their receptors. Int J Dev Neurosci 11:311-324.
46. Ramón-Cueto A, Avila J (1998) Olfactory ensheathing glia: properties and function. Brain Res Bull, in press.
47. Ramón-Cueto A, Nieto-Sampedro M (1992) Glial cells from adult rat olfactory bulb: immunocytochemical properties of pure cultures of ensheathing cells. Neuroscience 47:213-220.
48. Ramón-Cueto A, Nieto-Sampedro M (1994) Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp Neurol 127:232-244.
49. Ramón-Cueto A, Valverde F (1995) Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 14:163-173.
50. Ramón-Cueto A, Pérez J, Nieto-Sampedro M (1993) In vitro enfolding of olfactory neurites by p75 NGF receptor positive ensheathing cells from adult rat olfactory bulb. Eur J Neurosci 5:1172-1180.
51. Ramón y Cajal S (1928) Degeneration and regeneration of the nervous system (May RM, translator). New York: Oxford UP.
52. Reier PJ, Stensaas LJ, Guth L (1983) The astrocytic scar as an impediment to regeneration in the central nervous system. In: Spinal cord reconstruction (Cao CC, Bunge RP, Reier PJ, eds), pp 163-198. New York: Raven.
53. Reinhard E, Meier R, Halfter W, Rovelli G, Monrad D (1988) Detection of glia-derived nexin in the olfactory system of the rat. Neuron 1:387-394.
54. Sauve Y, Sawai H, Rasminsky M (1995) Functional synaptic connections made by regenerated retinal ganglion cell axons in the superior colliculus of adult hamsters. J Neurosci 15:665-675.
55. Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME (1994) Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367:170-173.
56. Schwab ME, Kapfhammer JP, Bandtlow CE (1993) Inhibitors of neurite growth. Annu Rev Neurosci 16:565-595.
57. Smith GM, Rutishauser U, Silver J, Miller RH (1990) Maturation of astrocytes in vitro alters the extent and molecular basis of neurite outgrowth. Dev Biol 138:377-390.
58. Son YJ, Trachtenberg JT, Thompson WJ (1996) Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci 19:280-284.
59. Tracey DJ (1985) Ascending and descending pathways in the spinal cord. In: The rat nervous system: hindbrain and spinal cord, Vol 2 (Paxinos G, ed), pp 311-324. Sydney: Australia: Academic.
60. Tuszynski MH, Peterson DA, Ray J, Baird A, Nakahara Y, Gage FH (1994) Fibroblasts genetically modified to produce nerve growth factor induce robust neuritic ingrowth after grafting to the spinal cord. Exp Neurol 126:1-14.
61. Ubink R, Halasz N, Zhang X, Dagerlind A, Hokfelt T (1994) Neuropeptide tyrosine is expressed in ensheathing cells around the olfactory nerves in the rat olfactory bulb. Neuroscience 60:709-726.
62. Unsicker K, Grothe C, Westermann R, Wewetzer K (1992) Cytokines in neural regeneration. Curr Opin Neurobiol 2:671-678.
63. Vergara J, Medina L, Maulen J, Inestrosa NC, Alvarez J (1993) Nerve regeneration is improved by insulin-like growth factor I (IGF-I) and basic fibroblast growth factor (bFGF). Rest Neurol Neurosci 5:181-189.
64. Xu XM, Guénard V, Kleitman N, Bunge MB (1995a) Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J Comp Neurol 351:145-160.
65. Xu XM, Guénard V, Kleitman N, Aebischer P, Bunge MB (1995b) A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp Neurol 134:261-272.
66. Xu XM, Chen A, Guénard V, Kleitman N, Bunge MB (1997) Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J Neurocytol 26:1-16.
67. Ye JH, Houle JD (1997) Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp Neurol 143:70-81.