Combination of chondroitinase ABC and AAV-NT3 promotes neural plasticity at descending spinal pathways after thoracic contusion in rats

Journal of Neurophysiology

Volumn 110, Issue 8, 2013, Pages 1782-1792

  Hunanyan, Arsen S ^a,b   Petrosyan, Hayk A ^a,b   Alessi, Valentina ^a,b   Arvanian, Victor L ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

5 HT; AAV NT3; Chondroitinase ABC; Contusion injury; Detour connections

Indexed keywords

CHONDROITIN ABC LYASE; NEUROTROPHIN 3; PARVOVIRUS VECTOR; PROTEOCHONDROITIN SULFATE; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; GAIT; GRAY MATTER; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; INTRACELLULAR RECORDING; MALE; MOTONEURON; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; QUANTITATIVE ANALYSIS; RAT; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; SPINAL CORD VENTRAL HORN; WHITE MATTER;

5-HT; AAV-NT3; CHONDROITINASE ABC; CONTUSION INJURY; DETOUR CONNECTIONS;

ANIMALS; CHONDROITIN ABC LYASE; CONTUSIONS; DEPENDOVIRUS; FEMALE; GENETIC THERAPY; INTERNEURONS; LOCOMOTION; MOTOR NEURONS; NEURONAL PLASTICITY; NEUROTROPHIN 3; PYRAMIDAL TRACTS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; SYNAPSES; THORACIC INJURIES;

EID: 84885623692     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00427.2013     Document Type: Article

References (81)

1. Alilain WJ, Horn KP, Hu H, Dick TE, Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 475: 196-200, 2011.
2. Alstermark B, Ogawa J, Isa T. Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J Neurophysiol 91: 1832-1839, 2004.
3. Arvanian V. Role of neurotrophins in spinal plasticity and locomotion. Curr Pharm Des 19: 4509-4516, 2013.
4. Arvanian VL, Bowers WJ, Anderson A, Horner PJ, Federoff HJ, Mendell LM. Combined delivery of neurotrophin-3 and NMDA receptors 2D subunit strengthens synaptic transmission in contused and staggered double hemisected spinal cord of neonatal rat. Exp Neurol 197: 347-352, 2006.
5. Arvanian VL, Horner PJ, Gage FH, Mendell LM. Chronic neurotrophin-3 strengthens synaptic connections to motoneurons in the neonatal rat. J Neurosci 23: 8706-8712, 2003.
6. Arvanian VL, Schnell L, Lou L, Golshani R, Hunanyan A, Ghosh A, Pearse DD, Robinson JK, Schwab ME, Fawcett JW, Mendell LM. Chronic spinal hemisection in rats induces a progressive decline in transmission in uninjured fibers to motoneurons. Exp Neurol 216: 471-480, 2009.
7. Arvanov VL, Seebach BS, Mendell LM. NT-3 evokes an LTP-like facilitation of AMPA/kainate receptor-mediated synaptic transmission in the neonatal rat spinal cord. J Neurophysiol 84: 752-758, 2000.
8. Babalian A, Liang F, Rouiller EM. Cortical influences on cervical motoneurons in the rat: recordings of synaptic responses from motoneurons and compound action potential from corticospinal axons. Neurosci Res 16: 301-310, 1993.
9. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7: 269-277, 2004.
10. Barritt AW, Davies M, Marchand F, Hartley R, Grist J, Yip P, McMahon SB, Bradbury EJ. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 26: 10856-10867, 2006.
11. Blits B, Carlstedt TP, Ruitenberg MJ, de Winter F, Hermens WT, Dijkhuizen PA, Claasens JW, Eggers R, van der Sluis R, Tenenbaum L, Boer GJ, Verhaagen J. Rescue and sprouting of motoneurons following ventral root avulsion and reimplantation combined with intraspinal adenoassociated viral vector-mediated expression of glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor. Exp Neurol 189: 303-316, 2004.
12. Blits B, Oudega M, Boer GJ, Bartlett Bunge M, Verhaagen J. Adenoassociated viral vector-mediated neurotrophin gene transfer in the injured adult rat spinal cord improves hind-limb function. Neuroscience 118: 271-281, 2003.
13. Bogatyreva ES, Shapavalov AI. Synaptic processes evoked by intracortical microstimulation in the lumbar motor neurons of rats. Neirofiziologiia 15: 174-180, 1973.
14. Boyce VS, Park J, Gage FH, Mendell LM. Differential effects of brainderived neurotrophic factor and neurotrophin-3 on hindlimb function in paraplegic rats. Eur J Neurosci 35: 221-232, 2012.
15. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416: 636-640, 2002.
16. Bresnahan JC, Beattie MS, Stokes BT, Conway KM. Three-dimensional computer-assisted analysis of graded contusion lesions in the spinal cord of the rat. J Neurotrauma 8: 91-101, 1991.
17. Caggiano AO, Zimber MP, Ganguly A, Blight AR, Gruskin EA. Chondroitinase ABCI improves locomotion and bladder function following contusion injury of the rat spinal cord. J Neurotrauma 22: 226-239, 2005.
18. Cao Q, Zhang YP, Iannotti C, DeVries WH, Xu XM, Shields CB, Whittemore SR. Functional and electrophysiological changes after graded traumatic spinal cord injury in adult rat. Exp Neurol Suppl 1: S3-S16, 2005.
19. Carmel JB, Berrol LJ, Brus-Ramer M, Martin JH. Chronic electrical stimulation of the intact corticospinal system after unilateral injury restores skilled locomotor control and promotes spinal axon outgrowth. J Neurosci 30: 10918-10926, 2010.
20. Cearley CN, Wolfe JH. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther 13: 528-537, 2006.
21. Dou CL, Levine JM. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 14: 7616-7628, 1994.
22. Eaton MJ, Blits B, Ruitenberg MJ, Verhaagen J, Oudega M. Amelioration of chronic neuropathic pain after partial nerve injury by adeno-associated viral (AAV) vector-mediated over-expression of BDNF in the rat spinal cord. Gene Ther 9: 1387-1395, 2002.
23. Edgley SA, Eyre JA, Lemon RN, Miller S. Comparison of activation of corticospinal neurons and spinal motor neurons by magnetic and electrical transcranial stimulation in the lumbosacral cord of the anaesthetized monkey. Brain 120: 839-853, 1997.
24. Fortun J, Puzis R, Pearse DD, Gage FH, Bunge MB. Muscle injection of AAV-NT3 promotes anatomical reorganization of CST axons and improves behavioral outcome following SCI. J Neurotrauma 26: 941-953, 2009.
25. Fouad K, Pedersen V, Schwab ME, Brösamle C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol 11: 1766-1770, 2001.
26. Fouad K, Schnell L, Bunge MB, Schwab ME, Liebscher T, Pearse DD. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J Neurosci 25: 1169-1178, 2005.
27. Galtrey CM, Fawcett JW. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 54: 1-18, 2007.
28. García-Alías G, Petrosyan HA, Schnell L, Horner PJ, Bowers WJ, Mendell LM, Fawcett JW, Arvanian VL. Chondroitinase ABC combined with neurotrophin NT-3 secretion and NR2D expression promotes axonal plasticity and functional recovery in rats with lateral hemisection of the spinal cord. J Neurosci 31: 17788-17799, 2011.
29. Ghosh A, Haiss F, Sydekum E, Schneider R, Gullo M, Wyss MT, Mueggler T, Baltes C, Rudin M, Weber B, Schwab ME. Rewiring of hindlimb corticospinal neurons after spinal cord injury. Nat Neurosci 13: 97-104, 2010.
30. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17: 5560-5572, 1997.
31. Hamers FP, Lankhorst AJ, van Laar TJ, Veldhuis WB, Gispen WH. Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J Neurotrauma 18: 187-201, 2001.
32. Harris NG, Mironova YA, Hovda DA, Sutton RL. Chondroitinase ABC enhances pericontusion axonal sprouting but does not confer robust improvements in behavioral recovery. J Neurotrauma 27: 1971-1982, 2010.
33. Hendriks WT, Eggers R, Ruitenberg MJ, Blits B, Hamers FP, Verhaagen J, Boer GJ. Profound differences in spontaneous long-term functional recovery after defined spinal tract lesions in the rat. J Neurotrauma 23: 18-35, 2006.
34. Hill CE, Beattie MS, Bresnahan JC. Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol 171: 153-169, 2001.
35. Hori N, Carp JS, Carpenter DO, Akaike N. Corticospinal transmission to motoneurons in cervical spinal cord slices from adult rats. Life Sci 72: 389-396, 2002.
36. Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J Neurosci 26: 7405-7415, 2006.
37. Hunanyan AS, García-Alías G, Alessi V, Levine JM, Fawcett JW, Mendell LM, Arvanian VL. Role of chondroitin sulfate proteoglycans in axonal conduction in mammalian spinal cord. J Neurosci 30: 7761-7769, 2010.
38. Hunanyan AS, Petrosyan HA, Alessi V, Arvanian VL. Detour synaptic connections from the motor cortex (MC) to individual neurons in lumbar dorsal and ventral horns after mid-thoracic contusion injury. Strengthening of novel connections by chondroitinase ABC and neurotrophin NT-3 (Abstract). Neuroscience Meeting Planner 2012: 270-03, 2012a.
39. Hunanyan AS, Petrosyan HA, Alessi V, Arvanian VL. Repetitive spinal electromagnetic stimulation opens a window of synaptic plasticity in damaged spinal cord: role of NMDA receptors. J Neurophysiol 107: 3027-3039, 2012b.
40. Iseda T, Okuda T, Kane-Goldsmith N, Mathew M, Ahmed S, Chang YW, Young W, Grumet M. Single, high-dose intraspinal injection of chondroitinase reduces glycosaminoglycans in injured spinal cord and promotes corticospinal axonal regrowth after hemisection but not contusion. J Neurotrauma 25: 334-349, 2008.
41. James ND, Bartus K, Grist J, Bennett DL, McMahon SB, Bradbury EJ. Conduction failure following spinal cord injury: functional and anatomical changes from acute to chronic stages. J Neurosci 31: 18543-18555, 2011.
42. Jankowska E, Hammar I, Chojnicka B, Heden CH. Effects of monoamines on interneurons in four spinal reflex pathways from group I and/or group II muscle afferents. Eur J Neurosci 12: 701-714, 2000.
43. Jankowska E, Hammar I, Djouhri L, Heden C, Szabo Lackberg Z, Yin XK. Modulations of responses of four types of feline ascending tract neurons by serotonin and noradrenaline. Eur J Neurosci 9: 1375-1387, 1997.
44. Jankowska E, Riddell JS, Skoog B, Noga BR. Gating of transmission to motoneurones by stimuli applied in the locus coeruleus and raphe nuclei of the cat. J Physiol 461: 705-722, 1993.
45. Kim BG, Dai HN, Lynskey JV, McAtee M, Bregman BS. Degradation of chondroitin sulfate proteoglycans potentiates transplant-mediated axonal remodeling and functional recovery after spinal cord injury in adult rats. J Comp Neurol 497: 182-198, 2006.
46. Koopmans GC, Deumens R, Honig WM, Hamers FP, Steinbusch HW, Joosten EA. The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J Neurotrauma 22: 214-225, 2005.
47. Lee H, McKeon RJ, Bellamkonda RV. Sustained delivery of thermostabilized chABC enhances axonal sprouting and functional recovery after spinal cord injury. Proc Natl Acad Sci USA 107: 3340-3345, 2010.
48. Lemon RN. Descending pathways in motor control. Annu Rev Neurosci 31: 195-218, 2008.
49. Loy DN, Talbott JF, Onifer SM, Mills MD, Burke DA, Dennison JB, Fajardo LC, Magnuson DS, Whittemore SR. Both dorsal and ventral spinal cord pathways contribute to overground locomotion in the adult rat. Exp Neurol 177: 575-580, 2002.
50. Martin JH. The corticospinal system: from development to motor control. Neuroscientist 11: 161-173, 2005.
51. Massey JM, Amps J, Viapiano MS, Matthews RT, Wagoner MR, Whitaker CM, Alilain W, Yonkof AL, Khalyfa A, Cooper NG, Silver J, Onifer SM. Increased chondroitin sulfate proteoglycan expression in denervated brainstem targets following spinal cord injury creates a barrier to axonal regeneration overcome by chondroitinase ABC and neurotrophin-3. Exp Neurol 209: 426-445, 2008.
52. Mendell LM, Munson JB, Arvanian VL. Neurotrophins and synaptic plasticity in the mammalian spinal cord. J Physiol 533: 91-97, 2001.
53. Metz GA, Curt A, van de Meent H, Klusman I, Schwab ME, Dietz V. Validation of the weight-drop contusion model in rats: a comparative study of human spinal cord injury. J Neurotrauma 17: 1-17, 2000.
54. Moon LD, Asher RA, Rhodes KE, Fawcett JW. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci 4: 465-466, 2001.
55. Mountney A, Zahner MR, Lorenzini I, Oudega M, Schramm LP, Schnaar RL. Sialidase enhances recovery from spinal cord contusion injury. Proc Natl Acad Sci USA 107: 11561-11566, 2010.
56. Mountney A, Zahner MR, Sturgill ER, Riley CJ, Aston JW, Oudega M, Schramm LP, Hurtado A, Schnaar RL. Sialidase, chondroitinase ABC, and combination therapy after spinal cord contusion injury. J Neurotrauma 30: 181-190, 2013.
57. Norenberg MD, Smith J, Marcillo A. The pathology of human spinal cord injury: defining the problems. J Neurotrauma 21: 429-440, 2004.
58. Oatway MA, Chen Y, Bruce JC, Dekaban GA, Weaver LC. Anti-CD11d integrin antibody treatment restores normal serotonergic projections to the dorsal, intermediate, and ventral horns of the injured spinal cord. J Neurosci 25: 637-647, 2005.
59. Onifer SM, Smith GM, Fouad K. Plasticity after spinal cord injury: relevance to recovery and approaches to facilitate it. Neurotherapeutics 8: 283-293, 2011.
60. Petrosyan HA, Hunanyan AS, Alessi V, Singh V, Matar N, Shaikh N, Levine J, Arvanian VL. A comparison of the transduction efficiency of neurons and glial cells in adult rat spinal cord by AAV-1, 2, 5, 9, rh10 and hu11 serotypes following mid-thoracic contusion injury (Abstract). Neuroscience Meeting Planner 2012: 165-01, 2012.
61. Petrosyan HA, Hunanyan AS, Alessi V, Schnell L, Levine J, Arvanian VL. Neutralization of inhibitory molecule NG2 improves synaptic transmission, retrograde transport, and locomotor function after spinal cord injury in adult rats. J Neurosci 33: 4032-4043, 2013.
62. Pinco M, Lev-Tov A. Synaptic transmission between ventrolateral funiculus axons and lumbar motoneurons in the isolated spinal cord of the neonatal rat. J Neurophysiol 72: 2406-2419, 1994.
63. Porter R, Lemon R. Corticospinal Function and Voluntary Movement. Oxford, UK: Oxford Univ. Press, 1993.
64. Reed WR, Shum-Siu A, Whelan A, Onifer SM, Magnuson DS. Anterograde labeling of ventrolateral funiculus pathways with spinal enlargement connections in the adult rat spinal cord. Brain Res 1302: 76-84, 2009.
65. Ruitenberg MJ, Blits B, Dijkhuizen PA, te Beek ET, Bakker A, van Heerikhuize JJ, Pool CW, Hermens WT, Boer GJ, Verhaagen J. Adeno-associated viral vector-mediated gene transfer of brain-derived neurotrophic factor reverses atrophy of rubrospinal neurons following both acute and chronic spinal cord injury. Neurobiol Dis 15: 394-406, 2004.
66. Saruhashi Y, Young W, Perkins R. The recovery of 5-HT immunoreactivity in lumbosacral spinal cord and locomotor function after thoracic hemisection. Exp Neurol 139: 203-213, 1996.
67. Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JE Jr. Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J Neurotrauma 20: 179-193, 2003.
68. Schmidt BJ, Jordan LM. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53: 689-710, 2000.
69. Schnell L, Hunanyan AS, Bowers WJ, Horner PJ, Federoff HJ, Gullo M, Schwab ME, Mendell LM, Arvanian VL. Combined delivery of Nogo-A antibody, neurotrophin-3 and the NMDA-NR2d subunit establishes a functional "detour" in the hemisected spinal cord. Eur J Neurosci 34: 1256-1267, 2011.
70. Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367: 170-173, 1994.
71. Schucht P, Raineteau O, Schwab ME, Fouad K. Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp Neurol 176: 143-153, 2002.
72. Sherrington CS. The Integrative Action of the Nervous System. New Haven, CT: Yale Univ. Press, 1906.
73. Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci 5: 146-156, 2004.
74. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109: 111-130, 1990.
75. Soleman S, Yip PK, Duricki DA, Moon LD. Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats. Brain 135: 1210-1223, 2012.
76. Starkey ML, Bartus K, Barritt AW, Bradbury EJ. Chondroitinase ABC promotes compensatory sprouting of the intact corticospinal tract and recovery of forelimb function following unilateral pyramidotomy in adult mice. Eur J Neurosci 36: 3665-3678, 2012.
77. Steencken AC, Siebert JR, Stelzner DJ. Lack of axonal sprouting of spared propriospinal fibers caudal to spinal contusion injury is attributed to chronic axonopathy. J Neurotrauma 26: 2279-2297, 2009.
78. Tom VJ, Kadakia R, Santi L, Houlé JD. Administration of chondroitinase ABC rostral or caudal to a spinal cord injury site promotes anatomical but not functional plasticity. J Neurotrauma 26: 2323-2333, 2009.
79. Vinukonda G, Zia MT, Bhimavarapu BB, Hu F, Feinberg M, Bokhari A, Ungvari Z, Fried VA, Ballabh P. Intraventricular hemorrhage induces deposition of proteoglycans in premature rabbits, but their in vivo degradation with chondroitinase does not restore myelination, ventricle size and neurological recovery. Exp Neurol (Mar 6, 2013). doi:10.1016/j.expneurol. 2013.02.018.
80. Weidner N, Ner A, Salimi N, Tuszynski MH. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci USA 98: 3513-3518, 2001.
81. Yang HW, Lemon RN. An electron microscopic examination of the corticospinal projection to the cervical spinal cord in the rat: lack of evidence for cortico-motoneuronal synapses. Exp Brain Res 149: 458-469, 2003.