Grafts of brain-derived neurotrophic factor and neurotrophin 3-transduced primate Schwann cells lead to functional recovery of the demyelinated mouse spinal cord

Journal of Neuroscience

Volumn 25, Issue 35, 2005, Pages 7924-7933

  Girard, Christelle ^a   Bemelmans, Alexis Pierre ^a,b   Dufour, Noëlle ^a,c   Mallet, Jacques ^a   Bachelin, Corinne ^a   Nait Oumesmar, Brahim ^a   Baron Van Evercooren, Anne ^a   Lachapelle, François ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b JULES GONIN EYE HOSPITAL   (Switzerland)

^c SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

Author keywords

Astrogliosis; Neuroprotection; Neurotrophins; Primate; Remyelination; Schwann cell

Indexed keywords

GREEN FLUORESCENT PROTEIN; GROWTH FACTOR; MYELIN; NEUROTROPHIN 3; RECOMBINANT BRAIN DERIVED NEUROTROPHIC FACTOR; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; AUTOTRANSPLANTATION; BRAIN FUNCTION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CONVALESCENCE; DEMYELINATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; GLIA CELL; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; MACACA; MALE; MOUSE; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION; SCHWANN CELL; SPINAL CORD DISEASE; STEM CELL; SUPERNATANT; TREATMENT OUTCOME;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL TRANSPLANTATION; CELLS, CULTURED; DEMYELINATING DISEASES; FEMALE; HUMANS; MACACA FASCICULARIS; MALE; MICE; MICE, NUDE; NERVE FIBERS, MYELINATED; NEUROTROPHIN 3; RECOVERY OF FUNCTION; SCHWANN CELLS; SPINAL CORD; TRANSDUCTION, GENETIC; TRANSPLANTS;

EID: 24344453717     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4890-04.2005     Document Type: Article

References (81)

1. Abnet K, Fawcett JW, Dunnett SB (1991) Interactions between meningeal cells and astrocytes in vivo and in vitro. Brain Res Dev Brain Res 59:187-196.
2. Acheson A, Barker PA, Alderson RF, Miller FD, Murphy RA (1991) Detection of brain-derived neurotrophic factor-like activity in fibroblasts and Schwann cells: inhibition by antibodies to NGF. Neuron 7:265-275.
3. Anderson TJ, Montague P, Nadon N, Nave KA, Griffiths IR (1997) Modification of Schwann cell phenotype with Plp transgenes: evidence that the PLP and DM20 isoproteins are targeted to different cellular domains. J Neurosci Res 50:13-22.
4. Avellana-Adalid V, Bachelin C, Lachapelle F, Escriou C, Ratzkin B, Baron-Van Evercooren A (1998) In vitro and in vivo behaviour of NDF-expanded monkey Schwann cells. Eur J Neurosci 10:291-300.
5. Bachelin C, Lachapelle F, Girard C, Moissonnier P, Serguera-Lagache C, Mallet J, Fontaine D, Chojnowski A, Le Guern E, Nait-Oumesmar B, Baron-Van Evercooren A (2005) Efficient myelin repair in the macaque spinal cord by autologous grafts of Schwann cells. Brain 128:540-549.
6. Baron-Van Evercooren A, Blakemore W (2004) Remyelination through engraftment. In: Myelin biology and disorders, Chap 6 (Lazzarini R, Griffin J, Lassmann H, Nave K-A, Miller R, Trapp B, eds), pp 143-172. San Diego: Elsevier.
7. Baron-Van Evercooren A, Kleinman HK, Ohno S, Marangos P, Schwartz JP, Dubois-Dalcq ME (1982) Nerve growth factor, laminin, and fibronectin promote neurite growth in human fetal sensory ganglia cultures. J Neurosci Res 8:179-193.
8. Baron-Van Evercooren A, Gansmuller A, Duhamel E, Pascal F, Gumpel M (1992) Repair of a myelin lesion by Schwann cells transplanted in the adult mouse spinal cord. J Neuroimmunol 40:235-242.
9. Barres BA, Schmid R, Sendnter M, Raff MC (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118:283-295.
10. Barres BA, Raff MC, Gaese F, Bartke I, Dechant G, Barde YA (1994) A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 367:371-375.
11. Blakemore WF, Crang AJ (1985) The use of cultured autologous Schwann cells to remyelinate areas of persistent demyelination in the central nervous system. J Neurol Sci 70:207-223.
12. Blakemore WF, Patterson RC (1975) Observations on the interactions of Schwann cells and astrocytes following X-irradiation of neonatal rat spinal cord. J Neurocytol 4:573-585.
13. Blakemore WF, Eames RA, Smith KJ, McDonald WI (1977) Remyelination in the spinal cord of the cat following intraspinal injections of lysolecithin. J Neurol Sci 33:31-43.
14. Blakemore WF, Gilson JM, Crang AJ (2003) The presence of astrocytes in areas of demyelination influences remyelination following transplantation of oligodendrocyte progenitors. Exp Neurol 184:955-963.
15. Bottenstein JE, Sato GH (1979) Growth of a rat neuroblastoma cell line i serum-free supplemented medium. Proc Natl Acad Sci USA:514-517.
16. Cao L, Liu L, Chen ZY, Wang LM, Ye JL, Qiu HY, Lu CL, He C (2004) Olfactory ensheathing cells genetically modified to secrete GDNF to promote spinal cord repair. Brain 127:535-549.
17. Carroll WM, Jennings AR (1994) Early recruitment of oligodendrocyte precursors in CNS demyelination. Brain 117:563-578.
18. Chan J, Cosgaya J, Wu Y, Shooter E (2001) Neurotrophins are key mediators of the myelination program in the peripheral nervous system. Proc Natl Acad Sci USA 98:14661-14668.
19. Charneau P, Alizon M, Clavel F (1992) A second origin of DNA plus-strand synthesis is required for optimal human immunodeficiency virus replication. J Virol 66:2814-2820.
20. Cosgaya JM, Chan JR, Shooter EM (2002) The neurotrophin receptor p75NTR as a positive modulator of myelination. Science 298:1245-1248.
21. Duncan ID, Aguayo AJ, Bunge RP, Wood PM (1981) Transplantation of rat Schwann cells grown in tissue culture into the mouse spinal cord. J Neurol Sci 49:241-252.
22. Dunham NW, Miya TS (1957) A note on a simple apparatus for detecting neurological deficit in rats and mice. J Am Pharm Assoc 46:208-209.
23. Dusart I, Marty S, Peschanski M (1991) Glial changes following an excitotoxic lesion in the CNS-II. Astrocytes. Neuroscience 45:541-549.
24. 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.
25. Fitch MT, Silver J (1997) Activated macrophages and the blood-brain barrier: inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp Neurol 148:587-603.
26. Franklin RJ (2002) Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 3:705-714.
27. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O, Verge VM, Persson H (1993) Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123:455-465.
28. Ghirnikar RS, Eng LF (1995) Chondroitin sulfate proteoglycan staining in astrocyte-Schwann cell co-cultures. Glia 14:145-152.
29. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH (1997) Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17:5560-5572.
30. Grimpe B, Silver J (2004) A novel DNA enzyme reduces glycosaminoglycan chains in the glial scar and allows microtransplanted dorsal root ganglia axons to regenerate beyond lesions in the spinal cord. J Neurosci 24:1393-1397.
31. Honmou O, Felts PA, Waxman SG, Kocsis JD (1996) Restoration of normal conduction properties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. J Neurosci 16:3199-3208.
32. Houweling DA, Lankhorst AJ, Gispen WH, Bar PR, Joosten EA (1998) Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery. Exp Neurol 153:49-59.
33. Jean I, Lavialle C, Barthelaix-Pouplard A, Fressinaud C (2003) Neurotrophin-3 specifically increases mature oligodendrocyte population and enhances remyelination after chemical demyelination of adult rat CNS. Brain Res 972:110-118.
34. Jiang H, Duchala CS, Awatramani R, Shumas S, Carlock L, Kamholz J, Garbern J, Scherer SS, Shy ME, Macklin WB (2000) Proteolipid protein mRNA stability is regulated by axonal contact in the rodent peripheral nervous system. J Neurobiol 44:7-19.
35. Jones LL, Sajed D, Tuszynski MH (2003) Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci 23:9276-9288.
36. Keirstead HS, Levine JM, Blakemore WF (1998) Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 22:161-170.
37. Kerschensteiner M, Stadelmann C, Buddeberg BS, Merkler D, Bareyre FM, Anthony DC, Linington C, Bruck W, Schwab ME (2004) Targeting experimental autoimmune encephalomyelitis lesions to a predetermined axonal tract system allows for refined behavioral testing in an animal model of multiple sclerosis. Am J Pathol 164:1455-1469.
38. Kiernan BW, Gotz B, Faissner A, ffrench-Constant C (1996) Tenascin-C inhibits oligodendrocvte precursor cell migration by both adhesion-dependent and adhesion-independent mechanisms. Mol Cell Neurosci 7:322-335.
39. Kim DH, Gutin PH, Noble LJ, Nathan D, Yu JS, Nockels RP (1996) Treatment with genetically engineered fibroblasts producing NGF or BDNF can accelerate recovery from traumatic spinal cord injury in the adult rat. NeuroReport 7:2221-2225.
40. Klinguer C, Trifilieff E (1994) Characterization and comparison of the polyclonal immune response to purified PLP and DM-20 in the Lewis rat: determination of a new antigenic determinant. Neurochem Int 25:433-440.
41. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
42. 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.
43. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH (2004) Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 24:6402-6409.
44. Manthorpe M, Engvall E, Ruoslahti E, Longo FM, Davis GE, Varon S (1983) Laminin promotes neuritic regeneration from cultured peripheral and central neurons. J Cell Biol 97:1882-1890.
45. Mathisen PM, Kawczak JA, Yu M, Johnson JM, Tuohy VK (2001) Differential DM20 mRNA expression distinguishes two distinct patterns of spontaneous recovery from murine autoimmune encephalomyelitis. J Neurosci Res 64:542-551.
46. McGavern DB, Murray PD, Rodriguez M (1999) Quantitation of spinal cord demyelination, remyelination, atrophy, and axonal loss in a model of progressive neurologic injury. J Neurosci Res 58:492-504.
47. McMorris FA, McKinnon RD (1996) Regulation of oligodendrocyte development and CNS myelination by growth factors: prospects for therapy of demyelinating disease. Brain Pathol 6:313-329.
48. McTigue DM, Horner PJ, Stokes BT, Gage FH (1998) Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 18:5354-5365.
49. Meier C, Parmantier E, Brennan A, Mirsky R, Jessen KR (1999) Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J Neurosci 19:3847-3859.
50. 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.
51. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H (1992) Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119:45-54.
52. Morgan L, Jessen K, Mirsky R (1991) The effects of cAMP on differentiation of cultured Schwann cells: progression from an early phenotype (04+) to a myelinphenotype (P0+, GFAP-, N-CAM-, NGF-receptor-)dependson growth inhibition. J Cell Biol 112:457-467.
53. Morrissey TK, Kleitman N, Bunge RP (1995) Human Schwann cells in vitro. II. Myelination of sensory axons following extensive purification and heregulin-induced expansion. J Neurobiol 28:190-201.
54. Murray PD, McGavern DB, Sathornsumetee S, Rodriguez M (2001) Spontaneous remyelination following extensive demyelination is associated with improved neurological function in a viral model of multiple sclerosis. Brain 124:1403-1416.
55. 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.
56. Nishiyama A, Lin XH, Giese N, Heldin CH, Stallcup WB (1996) Colocalization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 43:299-314.
57. Oudega M, Gautier SE, Chapon P, Fragoso M, Bates ML, Parel JM, Bunge MB (2001) Axonal regeneration into Schwann cell grafts within resorbable poly(alpha-hydroxyacid) guidance channels in the adult rat spinal cord. Biomaterials 22:1125-1136.
58. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB (2004) cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10:610-616.
59. Pham-Dinh D, Birling MC, Roussel G, Dautigny A, Nussbaum JL (1991) Proteolipid DM-20 predominates over PLP in peripheral nervous system. NeuroReport 2:89-92.
60. Plant GW, Bates ML, Bunge MB (2001) Inhibitory proteoglycan immunoreactivity is higher at the caudal than the rostral Schwann cell graft-transected spinal cord interface. Mol Cell Neurosci 17:471-487.
61. Ranscht B, Clapshaw PA, Price I, Noble M, Seifert W (1982) Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc Natl Acad Sci USA 79:2709-2713.
62. Redwine JM, Armstrong RC (1998) In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J Neurobiol 37:413-428.
63. Reynolds R, Cenci di Bello I, Dawson M, Levine J (2001) The response of adult oligodendrocyte progenitors to demyelination in EAE. Prog Brain Res 132:165-174.
64. Rodriguez-Tebar A, Dechant G, Gotz R, Barde Y (1992) Binding of neurotrophin-3 to its neuronal receptors and interactions with nerve growth factor and brain-derived neurotrophic factor. EMBO J 11:917-922.
65. Rubio N, Rodriguez R, Arevalo MA (2004) In vitro myelination by oligodendrocyte precursor cells transfected with the neurotrophin-3 gene. Glia 47:78-87.
66. Schinstine M, Fiore DM, Winn SR, Emerich DF (1995) Polymer-encapsulated Schwannoma cells expressing human nerve growth factor promote the survival of cholinergic neurons after a fimbria-fornix transection. Cell Transplant 4:93-102.
67. Schmidt C, Ohlemeyer C, Labrakakis C, Walter T, Kettenmann H, Schnitzer J (1997) Analysis of motile oligodendrocyte precursor cells in vitro and in brain slices. Glia 20:284-298.
68. 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.
69. Shields SA, Blakemore WF, Franklin RJ (2000) Schwann cell remyelination is restricted to astrocyte-deficient areas after transplantation into demyelinated adult rat brain. J Neurosci Res 60:571-578.
70. Tolwani R, Cosgaya J, Varma S, Jacob R, Kuo L, Shooter E (2004) BDNF overexpression produces a long-term increase in myelin formation in the peripheral nervous system. J Neurosci Res 77:662-669.
71. 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.
72. Tuszynski MH, Weidner N, McCormack M, Miller I, Powell H, Conner J (1998) Grafts of genetically modified Schwann cells to the spinal cord: survival, axon growth, and myelination. Cell Transplant 7:187-196.
73. Wilby MJ, Muir EM, Fok-Seang J, Gour BJ, Blaschuk OW, Fawcett JW (1999) N-Cadherin inhibits Schwann cell migration on astrocytes. Mol Cell Neurosci 14:66-84.
74. Xu X, Zhang S, Li H, Aebischer P, Bunge M (1999) Regrowth of axons into the distal spinal cord through a Schwann-cell-seeded mini-channel implanted into hemisected adult rat spinal cord. Eur J Neurosci 11:1723-1740.
75. Yamauchi J, Chan J, Shooter E (2004) Neurotrophins regulate Schwann cell migration by activating divergent signaling pathways dependent on Rho GTPases. Proc Natl Acad Sci USA 101:8774-8779.
76. Yan H, Wood PM (2000) NT-3 weakly stimulates proliferation of adult rat O1(-)O4(+)oligodendrocyte-lineage cells and increases oligodendrocyte myelination in vitro. J Neurosci Res 62:329-335.
77. Yoshimoto Y, Lin Q, Collier TJ, Frim DM, Breakefield XO, Bohn MC (1995) Astrocytes retrovirally transduced with BDNF elicit behavioral improvement in a rat model of Parkinson's disease. Brain Res 691:25-36.
78. Yoshimura K, Negishi T, Kaneko A, Sakamoto Y, Kitamura K, Hosokawa T, Hamaguchi K, Nomura M (1996) Monoclonal antibodies specific to the integral membrane protein P0 of bovine peripheral nerve myelin. Neurosci Res 25:41-49.
79. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, Charneau P (2000) HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101:173-185.
80. Zennou V, Serguera C, Sarkis C, Colin P, Perret E, Mallet J, Charneau P (2001) The HIV-1 DNA flap stimulates HIV vector-mediated cell transduction in the brain. Nat Biotechnol 19:446-450.
81. Zhang J, Luo X, Xian C, Liu Z, Zhou X (2000) Endogenous BDNF is required for myelination and regeneration of injured sciatic nerve in rodents. Eur J Neurosci 12:4171-4180.