Adeno-associated viral vector-mediated neurotrophin gene transfer in the injured adult rat spinal cord improves hind-limb function

Neuroscience

Volumn 118, Issue 1, 2003, Pages 271-281

  Blits, B ^c   Oudega, M ^a,b   Boer, G J ^c   Bunge, M Bartlett ^a,b   Verhaagen, J ^c  

^a UNIVERSITY OF MIAMI   (United States)

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

^c VU University   (Netherlands)

Author keywords

AAV vectors; BDNF; Injury; NT 3; Transplantation; Viral vectors

Indexed keywords

ADENOVIRUS VECTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; NEUROTROPHIN; NEUROTROPHIN 3; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LINE; CONTROLLED STUDY; DRUG ACTIVITY; EMBRYO; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TRANSFER; GENETIC TRANSDUCTION; HINDLIMB; HUMAN; HUMAN CELL; IMPLANTATION; IN VITRO STUDY; KIDNEY CELL; LOCOMOTION; LUMBAR SPINAL CORD; MOTOR PERFORMANCE; NERVE CELL; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GRAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SCHWANN CELL; SPINAL CORD INJURY; TRANSGENE; VIRAL GENE THERAPY;

EID: 0037466249     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00970-3     Document Type: Article

References (60)

1. Altar C.A., Boylan C.B., Fritsche M., Jackson C., Hyman C., Lindsay R.M. The neurotrophins NT-4/5 and BDNF augment serotonin, dopamine, and GABAergic systems during behaviorally effective infusions to the substantia nigra. Exp Neurol. 130:1994;31-40.
2. Anderson K.D., Alderson R.F., Altar C.A., DiStefano P.S., Corcoran T.L., Lindsay R.M., Wiegand S.J. Differential distribution of exogenous BDNF, NGF, and NT-3 in the brain corresponds to the relative abundance and distribution of high-affinity and low-affinity neurotrophin receptors. J Comp Neurol. 357:1995;296-317.
3. Ankeny D.P., McTigue D.M., Guan Z., Yan Q., Kinstler O., Stokes B.T., Jakeman L.B. Pegylated brain-derived neurotrophic factor shows improved distribution into the spinal cord and stimulates locomotor activity and morphological changes after injury. Exp Neurol. 170:2001;85-100.
4. Armanini M.P., McMahon S.B., Sutherland J., Shelton D.L., Phillips H.S. Truncated and catalytic isoforms of trkB are co-expressed in neurons of rat and mouse CNS. Eur J Neurosci. 7:1995;1403-1409.
5. Arvanov V.L., Seebach B.S., Mendell L.M. NT-3 evokes an LTP-like facilitation of AMPA/kainate receptor-mediated synaptic transmission in the neonatal rat spinal cord. J Neurophysiol. 84:2000;752-758.
6. Bamber N., Li H., Lu X., Oudega M., Aebischer P., Xu X.M. Neurotrophins BDNF and NT-3 promote axonal re-entry into the caudal host spinal cord through Schwann cell-seeded mini-channels. Eur J Neurosci. 13:2001;257-268.
7. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma. 12:1995;1-21.
8. Blesch A., Uy H.S., Grill R.J., Cheng J.G., Patterson P.H., Tuszynski M.H. Leukemia inhibitory factor augments neurotrophin expression and corticospinal axon growth after adult CNS injury. J Neurosci. 19:1999;3556-3566.
9. Blits B., Dijkhuizen P.A., Boer G.J., Verhaagen J. Adenoviral vector-mediated gene delivery in the injured spinal cord effects of post-lesion injection time on transduction efficiency . Soc Neurosci Abst. 25:1999;2280.
10. Blits B., Dijkhuizen P.A., Boer G.J., Verhaagen J. Intercostal nerve implants transduced with an adenoviral vector encoding neurotrophin-3 promote regrowth of injured rat corticospinal tract fibers and improve hindlimb function. Exp Neurol. 164:2000;25-37.
11. Bunge M.B. Bridging areas of injury in the spinal cord. Neuroscientist. 7:2001;325-339.
12. Cai D., Shen Y., De Bellard M., Tang S., Filbin M.T. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a camp-dependent mechanism. Neuron. 22:1999;89-101.
13. Chen A., Xu X.M., Kleitman N., Bunge M.B. Methylprednisolone administration improves axonal regeneration into Schwann cell bridges in transected adult rat thoracic spinal cord. Exp Neurol. 138:1996;261-276.
14. Davies A.M. Neurotrophins neurotrophic modulation of neurite growth . Curr Biol. 10:2000;R198-R200.
15. Dijkhuizen P.A., Pasterkamp R.J., Hermens W.T., de Winter F., Giger R.J., Verhaagen J. Adenoviral vector-mediated gene delivery to injured rat peripheral nerve. J Neurotrauma. 15:1998;387-397.
16. Dijkhuizen P.A., Hermens W.T., Teunis M.A., Verhaagen J. Adenoviral vector-directed expression of neurotrophin-3 in rat dorsal root ganglion explants results in a robust neurite outgrowth response. J Neurobiol. 33:1997;172-184.
17. Dijkhuizen P.A., Verhaagen J. The use of neurotrophic factors to treat spinal cord injury advantages and disadvantages of different delivery methods . Neurosci Res Comm. 24:1999;1-11.
18. Dittrich F., Ochs G., Grosse-Wilde A., Berweiler U., Yan Q., Miller J.A., Toyka K.V., Sendtner M. Pharmacokinetics of intrathecally applied BDNF and effects on spinal motoneurons. Exp Neurol. 41:1996;225-239.
19. Edgerton V.R., Leon R.D., Harkema S.J., Hodgson J.A., London N., Reinkensmeyer D.J., Roy R.R., Talmadge R.J., Tillakaratne N.J., Timoszyk W., Tobin A. Retraining the injured spinal cord. J Physiol. 533:2001;15-22.
20. Eriksdotter J.M., Nordberg A., Amberla K., Backman L., Ebendal T., Meyerson B., Olson L., Seiger ÅShigeta M., Theodorsson E., Viitanen M., Winblad B., Wahlund L.O. Intracerebroventricular infusion of nerve growth factor in three patients with Alzheimer's disease. Dement Geriatr Cogn Disord. 9:1998;246-257.
21. Frerking M., Malenka R.C., Nicoll R.A. Brain-derived neurotrophic factor (BDNF) modulates inhibitory, but not excitatory, transmission in the CA1 region of the hippocampus. J Neurophysiol. 80:1998;3383-3386.
22. Frisen J., Verge V.M., Fried K., Risling M., Persson H., Trotter J., Hokfelt T., Lindholm D. Characterization of glial trkB receptors differential response to injury in the central and peripheral nervous systems . Proc Natl Acad Sci USA. 90:1993;4971-4975.
23. Grill R., Murai K., Blesch A., Gage F.H., 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.
24. Guest J.D., Rao A., Olson L., Bunge M.B., Bunge R.P. The ability of human Schwann cell bridges to promote regeneration in the transected nude rat spinal cord. Exp Neurol. 148:1997;502-522.
25. Hermens W.T., ter Brake O., Dijkhuizen P.A., Sonnemans M.A., Grimm D., Kleinschmidt J.A., Verhaagen J. Purification of recombinant adeno-associated virus by iodixanol gradient ultracentrifugation allows rapid and reproducible preparation of vector stocks for gene transfer in the nervous system. Hum Gene Ther. 10:1999;1885-1891.
26. Hermens W.T., Verhaagen J. Suppression of inflammation by dexamethasone prolongs adenoviral vector-mediated transgene expression in the facial nucleus of the rat. Brain Res Bull. 47:1998;133-140.
27. Hermens W.T., Verhaagen J. Viral vectors, tools for gene transfer in the nervous system. Prog Neurobiol. 55:1998;399-432.
28. Horner P.J., Gage F.H. Regenerating the damaged central nervous system. Nature. 407:2000;963-970.
29. Houweling D.A., Lankhorst A.J., Gispen W.H., Bar P.R., Joosten E.A. Collagen containing neurotrophin-3 (NT-3) attracts regrowing injured corticospinal axons in the adult rat spinal cord and promotes partial functional recovery. Exp Neurol. 153:1998;49-59.
30. Houweling D.A., van Asseldonk J.T., Lankhorst A.J., Hamers F.P., Martin D., Bar P.R., Joosten E.A. Local application of collagen containing brain-derived neurotrophic factor decreases the loss of function after spinal cord injury in the adult rat. Neurosci Lett. 251:1998;193-196.
31. Jakeman L.B., Wei P., Guan Z., Stokes B.T. Brain-derived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury. Exp Neurol. 154:1998;170-184.
32. Kafitz K.W., Rose C.R., Thoenen H., Konnerth A. Neurotrophin-evoked rapid excitation through TrkB receptors. Nature. 401:1999;918-921.
33. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
34. Klein R.L., McNamara R.K., King M.A., Lenox R.H., Muzyczka N., Meyer E.M. Generation of aberrant sprouting in the adult rat brain by GAP-43 somatic gene transfer. Brain Res. 832:1999;136-144.
35. Kozak M. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J Mol Biol. 196:1987;947-950.
36. Loeb J.E., Cordier W.S., Harris M.E., Weitzman M.D., Hope T.J. Enhanced expression of transgenes from adeno-associated virus vectors with the woodchuck hepatitis virus posttranscriptional regulatory element implications for gene therapy . Hum Gene Ther. 10:1999;2295-2305.
37. McTigue D.M., Horner P.J., Stokes B.T., Gage F.H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci. 18:1998;5354-5365.
38. Mendell L.M., Munson J.B., Arvanian V.L. Neurotrophins and synaptic plasticity in the mammalian spinal cord. J Physiol. 533:2001;91-97.
39. Moon L.D., Asher R.A., Rhodes K.E., Fawcett J.W. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci. 4:2001;465-466.
40. Morrissey T.K., Kleitman N., Bunge R.P. Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J Neurosci. 11:1991;2433-2442.
41. Muir G.D., Steeves J.D. Sensorimotor stimulation to improve locomotor recovery after spinal cord injury. Trends Neurosci. 20:1997;72-77.
42. Nordberg A. Pharmacological treatment of cognitive dysfunction in dementia disorders. Acta Neurol Scand Suppl. 168:1996;87-92.
43. Oudega M., Xu X.M., Guenard V., Kleitman N., Bunge M.B. A combination of insulin-like growth factor-I and platelet-derived growth factor enhances myelination but diminishes axonal regeneration into Schwann cell grafts in the adult rat spinal cord. Glia. 19:1997;247-258.
44. Oudega M., Rosano C., Sadi D., Wood P.M., Schwab M.E., Hagg T. Neutralizing antibodies against neurite growth inhibitor NI-35/250 do not promote regeneration of sensory axons in the adult rat spinal cord. Neuroscience. 100:2000;873-883.
45. Oudega M., Hagg T. Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp Neurol. 140:1996;218-229.
46. Oudega M., Hagg T. Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res. 818:1999;431-438.
47. Paterna J.C., Moccetti T., Mura A., Feldon J., Bueler H. Influence of promoter and WHV post-transcriptional regulatory element on AAV-mediated transgene expression in the rat brain. Gene Ther. 7:2000;1304-1311.
48. Peel A.L., Zolotukhin S., Schrimsher G.W., Muzyczka N., Reier P.J. Efficient transduction of green fluorescent protein in spinal cord neurons using adeno-associated virus vectors containing cell type-specific promoters. Gene Ther. 4:1997;16-24.
49. Qiu J., Cai D., Dai H., McAtee M., Hoffman P.N., Bregman B.S., Filbin M.T. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron. 34:2002;895-903.
50. Schnell L., 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.
51. Schnell L., Schwab M.E. Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur J Neurosci. 5:1993;1156-1171.
52. Schwab M.E. Neurobiology finding the lost target . Nature. 403:2000;257-260.
53. Siuciak J.A., Boylan C., Fritsche M., Altar C.A., Lindsay R.M. BDNF increases monoaminergic activity in rat brain following intracerebroventricular or intraparenchymal administration. Brain Res. 710:1996;11-20.
54. Thoenen H. Neurotrophins and neuronal plasticity. Science. 270:1995;593-598.
55. von Meyenburg J., Brosamle C., Metz G.A., 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.
56. Xu X.M., Guénard V., Kleitman N., Bunge M.B. Axonal regeneration into Schwann cell-seeded guidance channels bridged into transected adult rat spinal cord. J Comp Neurol. 351:1995;145-160.
57. Xu X.M., Guénard V., Kleitman N., Aebischer P., Bunge M.B. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp Neurol. 134:1995;261-272.
58. Xu X.M., Chen A., Guenard V., Kleitman N., Bunge M.B. Bridging Schwann cell transplants promote axonal regeneration from both the rostral and caudal stumps of transected adult rat spinal cord. J Neurocytol. 26:1997;1-16.
59. Yick L.W., Wu W., So K.F., Yip H.K., Shum D.K. Chondroitinase ABC promotes axonal regeneration of Clarke's neurons after spinal cord injury. Neuroreport. 11:2000;1063-1067.
60. Zhang G., Gurtu V., Kain S.R. An enhanced green fluorescent protein allows sensitive detection of gene transfer in mammalian cells. Biochem Biophys Res Commun. 227:1996;707-711.