Muscle injection of AAV-NT3 promotes anatomical reorganization of CST axons and improves behavioral outcome following SCI

Journal of Neurotrauma

Volumn 26, Issue 7, 2009, Pages 941-953

  Fortun, Jenny ^a   Puzis, Raisa ^a   Pearse, Damien D ^a   Gage, Fred H ^b   Bunge, Mary Bartlett ^a,c  

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

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF MIAMI   (United States)

Author keywords

Adeno associated virus; Axon growth sprouting; Corticospinal tract; Neurotrophin 3; Retrograde transport

Indexed keywords

BETA GALACTOSIDASE; BUPRENORPHINE; GENTAMICIN; GREEN FLUORESCENT PROTEIN; NEUROTROPHIN 3; PARVOVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOSIS; BEHAVIOR; CERVICAL SPINAL CORD INJURY; CONTROLLED STUDY; EMBRYO; FEMALE; GENE TARGETING; GENE THERAPY; GRIP STRENGTH; HANGING; HUMAN; HUMAN CELL; NERVE CELL; NERVE FIBER; NERVE FIBER GROWTH; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PYRAMIDAL TRACT; RAT; SEROTYPE; SPINAL CORD MOTONEURON; TRICEPS BRACHII MUSCLE; VIRAL GENE DELIVERY SYSTEM; ANIMAL; CERVICAL SPINE; CONVALESCENCE; DEPENDOPARVOVIRUS; FISCHER 344 RAT; GENETICS; HAND STRENGTH; INTRAMUSCULAR DRUG ADMINISTRATION; METABOLISM; MOTONEURON; NERVE REGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD INJURIES; TREATMENT OUTCOME;

ANIMALS; AXONS; CERVICAL VERTEBRAE; DEPENDOVIRUS; FEMALE; HAND STRENGTH; INJECTIONS, INTRAMUSCULAR; MOTOR NEURONS; NERVE REGENERATION; NEUROTROPHIN 3; PYRAMIDAL TRACTS; RATS; RATS, INBRED F344; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; TREATMENT OUTCOME;

EID: 69249124531     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0807     Document Type: Article

References (52)

1. Andres, R., Herraez-Baranda, L.A., Thompson, J., Wyatt, S., and Davies, A.M. (2008). Regulation of sympathetic neuron differentiation by endogenous nerve growth factor and neurotrophin-3. Neurosci. Lett. 431, 241-246.
2. Bradbury, E.J., Khemani, S., King, V.R., Priestley, J.V., and McMahon, S.B. (1999). NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur. J. Neurosci. 11, 3873-3883.
3. Bradbury, E.J., King, V., Simmons, L.J., Priestley, J.V., and McMahon, S.B. (1998). NT-3, but not BDNF, prevents atrophy and death of axotomized spinal cord projection neurons. Eur. J. Neurosci. 10, 3058-3068.
4. Bregman, B.S., Kunkelbagden, E., McAtee, M., and Oneill, A. (1989). Extension of the critical period for developmental plasticity of the corticospinal pathway. J. Comp. Neurol. 282, 355-370.
5. Brodski, C., Schnurch, H., and Dechant, G. (2000). Neurotrophin-3 promotes the cholinergic differentiation of sympathetic neurons. Proc. Natl. Acad. Sci. USA 97, 9683-9688.
6. Burger, C., Gorbatyuk, O.S., Velardo, M.J., Peden, C.S., Williams, P., Zolotukhin, S., Reier, P.J., Mandel, R.J., and Muzyczka, N. (2004). Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol. Ther. 10, 302-317.
7. Chen, H.H., Tourtellotte, W.G., and Frank, E. (2002). Muscle spindle-derived neurotrophin 3 regulates synaptic connectivity between muscle sensory and motor neurons. J. Neurosci. 22, 3512-3519.
8. Chen, Q., Smith, G., and Shine, H.D. (2008). Immune activation is required for NT-3-induced neuroplasticity in injured spinal cord. Exp. Neurol. 209, 497-509.
9. Girard, C., Bemelmans, A.P., Dufour, N., Mallet, J., Bachelin, C., Nait-Oumesmar, B., Baron-Van Evercooren, A., and Lachapelle, F. (2005). Grafts of brain-derived neurotrophic factor and neurotrophin 3-transduced primate Schwann cells lead to functional recovery of the demyelinated mouse spinal cord. J. Neurosci. 25, 7924-7933. (Pubitemid 41254395)
10. Golden, K.L., Pearse, D.D., Blits, B., Garg, M.S., Oudega, M., Wood, P.M., and Bunge, M.B. (2007). Transduced Schwann cells promote axon growth and myelination after spinal cord injury. Exp. Neurol. 207, 203-217.
11. Grill, R., Murai, K., Blesch, A., Gage, F.H., and Tuszynski, M.H. (1997). Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 17, 5560-5572. (Pubitemid 127777377)
12. Henderson, C.E., Camu, W., Mettling, C., Gouin, A., Poulsen, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S.B., Armanini, M.P., Berkemeier, L., Phillips, H.S., and Rosenthal, A. (1993). Neurotrophins promote motor-neuron survival and are present in embryonic limb bud. Nature 363, 266-270. (Pubitemid 23158531)
13. Hollis, E.R., Kadoya, K., Hirsch, M., Samulski, R.J., and Tuszynski, M.H. (2008). Efficient retrograde neuronal transduction utilizing self-complementary AAV1. Mol. Ther. 16, 296-301.
14. Howard, D.B., Powers, K., Wang, Y., and Harvey, B.K. (2008). Tropism and toxicity of adeno-associated viral vector serotypes 1, 2, 5, 6, 7, 8, and 9 in rat neurons and glia in vitro. Virology 372, 24-34.
15. Hu, X.H., Jin, L., and Feng, L.Y. (2004). Erk1/2 but not PI3K pathway is required for neurotrophin 3-induced oligodendrocyte differentiation of post-natal neural stem cells. J. Neurochem. 90, 1339-1347. (Pubitemid 39223638)
16. Iarikov, D.E., Kim, B.G., Dai, H.N., McAtee, M., Kuhn, P.L., and Bregman, B.S. (2007). Delayed transplantation with exogenous neurotrophin administration enhances plasticity of corticofugal projections after spinal cord injury. J. Neurotrauma 24, 690-702. (Pubitemid 46996028)
17. Kamei, N., Tanaka, N., Oishi, Y., Hamasaki, T., Nakanishi, K., Sakai, N., and Ochi, M. (2007). BDNF, NT-3, and NGF released from transplanted neural progenitor cells promote corticospinal axon growth in organotypic cocultures. Spine 32, 1272-1278. (Pubitemid 46791444)
18. Kaspar, B.K., Erickson, D., Schaffer, D., Hinh, L., Gage, F.H., and Peterson, D.A. (2002). Targeted retrograde gene delivery for neuronal protection. Mol. Ther. 5, 50-56.
19. Kaspar, B.K., Llado, J., Sherkat, N., Rothstein, J.D., and Gage, F.H. (2003). Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301, 839-842. (Pubitemid 36962626)
20. Kelkar, S., De, B.P., Gao, G.P., Wilson, J.M., Crystal, R.G., and Leopold, P.L. (2006). A common mechanism for cytoplasmic dynein-dependent microtubule binding shared among adeno-associated virus and adenovirus serotypes. J. Virol. 80, 7781-7785. (Pubitemid 44092599)
21. Kim, D.H., Zhao, X.R., Tu, C.H., Casaccia-Bonnefil, P., and Chao, M.V. (2004). Prevention of apoptotic but not necrotic cell death following neuronal injury by neurotrophins signaling through the tyrosine kinase receptor. J. Neurosurg. 100, 79-87. (Pubitemid 38017819)
22. Krimm, R.F., Davis, B.M., and Albers, K.M. (2000). Cutaneous overexpression of neurotrophin-3 (NT3) selectively restores sensory innervation in NT3 gene knockout mice. J. Neurobiol. 43, 40-49.
23. Kruttgen, A., Moller, J.C., Heymach, J.V., and Shooter, E.M. (1998). Neurotrophins induce release of neurotrophins by the regulated secretory pathway. Proc. Natl. Acad. Sci. USA 95, 15867.
24. Liang, F., Moret, V., Wiesendanger, M., and Rouiller, E.M. (1991). Corticomotoneuronal connections in the rat-evidence from double-labeling of motoneurons and corticospinal axon arborizations. J. Comp. Neurol. 311, 356-366.
25. Lohof, A.M., Ip, N.Y., and Poo, M.M. (1993). Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350-353. (Pubitemid 23161530)
26. Martinov, V.N., Sefland, I., Walaas, S.I., Lomo, T., Nja, A., and Hoover, F. (2002). Targeting functional subtypes of spinal motoneurons and skeletal muscle fibers in vivo by intramuscular injection of adenoviral and adeno-associated viral vectors. Anat. Embryol. 205, 215-221.
27. McKenna, J.E., Prusky, G.T., and Whishaw, I.Q. (2000). Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: A retrograde carbocyanine dye analysis. J. Comp. Neurol. 419, 286-296.
28. McTigue, D.M., Horner, P.J., Stokes, B.T., and Gage, F.H. (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.
29. Mendell, L.M., and Arvanian, V.L. (2002). Diversity of neurotrophin action in the postnatal spinal cord. Brain Res. Rev. 40, 230-239.
30. Mendell, L.M., Munson, J.B., and Arvanian, V.L. (2001). Neurotrophins and synaptic plasticity in the mammalian spinal cord. J. Physiol. 533, 91-97. (Pubitemid 32499361)
31. Pearse, D.D., Lo, T.P., Cho, K.S., Lynch, M.P., Garg, M.S., Marcillo, A.E., Sanchez, A.R., Cruz, Y., and Dietrich, W.D. (2005). Histopathological and behavioral characterization of a novel cervical spinal cord displacement contusion injury in the rat. J. Neurotrauma 22, 680-702. (Pubitemid 40840383)
32. Pearse, D.D., Sanchez, A.R., Pereira, F.C., Andrade, C.M., Puzis, R., Pressman, Y., Golden, K., Kitay, B.M., Blits, B., Wood, P.M., and Bunge, M.B. (2007). Transplantation of Schwann cells and=or olfactory ensheathing glia into the contused spinal cord: survival, migration, axon association, and functional recovery. Glia 55, 976-1000. (Pubitemid 46903998)
33. Pirozzi, M., Quattrini, A., Andolfi, G., Dina, G., Malaguti, M.C., Auricchio, A., and Rugarli, E.I. (2006). Intramuscular viral delivery of paraplegin rescues peripheral axonopathy in a model of hereditary spastic paraplegia. J. Clin. Invest. 116, 202-208.
34. Ramer, M.S., Bishop, T., Dockery, P., Mobarak, M.S., O'Leary, D., Fraher, J.P., Priestley, J.V., and McMahon, S.B. (2002). Neurotrophin-3-mediated regeneration and recovery of proprioception following dorsal rhizotomy. Mol. Cell Neurosci. 19, 239-249.
35. Ruitenberg, M.J., Levison, D.B., Lee, S.V., Verhaagen, J., Harvey, A.R., and Plant, G.W. (2005). NT-3 expression from engineered olfactory ensheathing glia promotes spinal sparing and regeneration. Brain 128, 839-853. (Pubitemid 40516921)
36. Ruitenberg, M.J., Plant, G.W., Hamers, F.P.T., Wortel, J., Blits, B., Dijkhuizen, P.A., Gispen, W.H., Boer, G.J., and Verhaagen, J. (2003). Ex vivo adenoviral vector-mediated neurotrophin gene transfer to olfactory ensheathing glia: Effects on rubrospinal tract regeneration, lesion size, and functional recovery after implantation in the injured rat spinal cord. J. Neurosci. 23, 7045-7058. (Pubitemid 36975870)
37. Schnell, L., Schneider, R., Kolbeck, R., Barde, Y.A., and Schwab, M.E. (1994). Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173. (Pubitemid 24031697)
38. Schnell, L., and Schwab, M.E. (1990). Axonal regeneration in the rat spinal-cord produced by an antibody against myelin-associated neurite growth-inhibitors. Nature 343, 269-272. (Pubitemid 20030644)
39. Schucht, P., Raineteau, O., Schwab, M.E., and Fouad, K. (2002). Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp. Neurol. 176, 143-153.
40. Sharma, H.S. (2007). A select combination of neurotrophins enhances neuroprotection and functional recovery following spinal cord injury. Ann. N. Y. Acad. Sci. 1122, 95-111.
41. Taylor, L., Jones, L., Tuszynski, M.H., and Blesch, A. (2006a). Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord. J. Neurosci. 26, 9713-9721. (Pubitemid 44427710)
42. Taylor, S.J., Rosenzweig, E.S., McDonald, J.W., and Sakiyama-Elbert, S.E. (2006b). Delivery of neurotrophin-3 from fibrin enhances neuronal fiber sprouting after spinal cord injury. J. Control Release 113, 226-235. (Pubitemid 43963190)
43. Taymans, J.M., Vandenberghe, L.H., Van Den Haute, C., Thiry, I., Deroose, C.M., Mortelmans, L., Wilson, J.M., Debyser, Z., and Baekelandt, V. (2007). Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum. Gene Ther. 18, 195-206.
44. Vasileva, A., and Jessberger, R. (2005). Precise hit: adeno-associated virus in gene targeting. Nat. Rev. Microbiol. 3, 837-847.
45. Vavrek, R., Girgis, J., Tetzlaff, W., Hebert, G.W., and Fouad, K. (2006). BDNF promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats. Brain 129, 1534-1545. (Pubitemid 43999385)
46. Wang, L., Muramatsu, S., Lu, Y., Ikeguchi, K., Fujimoto, K., Okada, T., Mizukami, H., Hanazono, Y., Kume, A., Urano, F., Ichinose, H., Nagatsu, T., Nakano, I., and Ozawa, K. (2002). Delayed delivery of AAV-GDNF prevents nigral neurodegeneration and promotes functional recovery in a rat model of Parkinson's disease. Gene Ther. 9, 381-389. (Pubitemid 34414036)
47. Wang, Z., Li, L.Y., Taylor, M.D., Wright, D.E., and Frank, E. (2007). Prenatal exposure to elevated NT3 disrupts synaptic selectivity in the spinal cord. J. Neurosci. 27, 3686-3694. (Pubitemid 46557669)
48. Wright, D.E., Zhou, L., Kucera, J., and Snider, W.D. (1997). Introduction of a neurotrophin-3 transgene into muscle selectively rescues proprioceptive neurons in mice lacking endogenous neurotrophin-3. Neuron 19, 503-517. (Pubitemid 27430740)
49. Xu, J.F., Ma, C.Y., Bass, C., and Terwilliger, E.F. (2005). A combination of mutations enhances the neurotropism of AAV-2. Virology 341, 203-214. (Pubitemid 41416730)
50. Yamauchi, J., Miyamoto, Y., Tanoue, A., Shooter, E.M., and Chan, J.R. (2005). Ras activation of a Rac1 exchange factor, Tiam1, mediates neurotrophin-3-induced Schwann cell migration. Proc. Natl. Acad. Sci. USA 102, 14889-14894.
51. Yan, H.L., and Wood, P.M. (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.
52. Zhou, L., Baumgartner, B.J., Hill-Felberg, S.J., McGowen, L.R., and Shine, H.D. (2003). Neurotrophin-3 expressed in situ induces axonal plasticity in the adult injured spinal cord. J. Neurosci. 23, 1424-1431. (Pubitemid 36258921)