Chondroitinase enhances cortical map plasticity and increases functionally active sprouting axons after brain injury

Journal of Neurotrauma

Volumn 30, Issue 14, 2013, Pages 1257-1269

  Harris, Neil G ^a   Nogueira, Marcia S M ^a   Verley, Derek R ^a   Sutton, Richard L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

axonal sprouting; c Fos; cortex; CSPG; perineuronal net; plasticity

Indexed keywords

N ACETYLGALACTOSAMINE 4 SULFATASE; NEUROMODULIN; PROTEIN C FOS; PROTEOCHONDROITIN SULFATE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; FORELIMB; GLIA CELL; NERVE CELL PLASTICITY; NERVE FIBER; NERVE SPROUTING; NONHUMAN; PHENOTYPE; RAT;

ANIMALS; ATROPHY; AXONS; BRAIN INJURIES; CELL COUNT; CEREBRAL CORTEX; CHONDROITIN ABC LYASE; ELECTRIC STIMULATION; FORELIMB; GAP-43 PROTEIN; IMMUNOHISTOCHEMISTRY; MALE; NERVE NET; NEURAL PATHWAYS; NEUROGLIA; NEURONAL PLASTICITY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84880382150     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2737     Document Type: Article

References (57)

1. Harris, N., Mironova, Y.A., Hovda, D., and Sutton, R.L. (2010). Chondroitinase ABC enhances pericontusion axonal sprouting but does not confer robust improvements in behavioral recovery. J. Neurotrauma 27, 1-12.
2. Yi, J.-H., Katagiri, Y., Susarla, B., Figge, D., Symes, A.J., and Geller, H.M. (2012). Alterations in sulfated chondroitin glycosaminoglycans following controlled cortical impact injury in mice. J. Comp. Neurol. 520, 3295-3313.
3. Harris, N.G., Carmichael, S.T., Hovda, D.A., and Sutton, R.L. (2009). Traumatic brain injury results in disparate regions of chondroitin sulfate proteoglycan expression that are temporally limited. J. Neurosci. Res. 87, 2937-2950.
4. Barritt, A.W., Davies, M., Marchand, F., Hartley, R., Grist, J., Yip, P., McMahon, S.B., and Bradbury, E.J. (2006). Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J. Neurosci. 26, 10856-10867.
5. Bowes, C., Massey, J.M., Burish, M., Cerkevich, C.M., and Kaas, J.H. (2012). Chondroitinase ABC promotes selective reactivation of somatosensory cortex in squirrel monkeys after a cervical dorsal column lesion. Proc. Natl. Acad. Sci. U. S. A. 109, 2595-2600.
6. Bradbury, E.J., Moon, L.D., Popat, R.J., King, V.R., Bennett, G.S., Patel, P.N., Fawcett, J.W., and McMahon, S.B. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640. (Pubitemid 34406764)
7. Cafferty, W.B.J., Yang, S.-H., Duffy, P.J., Li, S., and Strittmatter, S.M. (2007). Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J. Neurosci. 27, 2176-2185. (Pubitemid 46340954)
8. Garcia-Alias, G., Petrosyan, H.A., Schnell, L., Horner, P.J., Bowers, W.J., Mendell, L.M., Fawcett, J.W., and Arvanian, V.L. (2011). 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.
9. Grimpe, B., and 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. (Pubitemid 38222990)
10. Houle, J.D., Tom, V.J., Mayes, D., Wagoner, G., Phillips, N., and Silver, J. (2006). 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. (Pubitemid 44315209)
11. Ikegami, T., Nakamura, M., Yamane, J., Katoh, H., Okada, S., Iwanami, A., Watanabe, K., Ishii, K., Kato, F., Fujita, H., Takahashi, T., Okano, H.J., Toyama, Y., and Okano, H. (2005). Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur. J. Neurosci. 22, 3036-3046. (Pubitemid 43001987)
12. Karimi-Abdolrezaee, S., Eftekharpour, E., Wang, J., Schut, D., and Fehlings, M.G. (2010). Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J. Neurosci. 30, 1657-1676.
13. Mingorance, A., Sol, S., Eftekharpour, E., Wang, J., Schut, D., and Fehlings, M.G. (2010). Synergistic effects of traneration of lesioned entorhino-hippocampal axons in vitro by combined degradation of inhibitory proteoglycans and blockade of Nogo-66/NgR signaling. FASEB J. 20, 491-493. (Pubitemid 46671226)
14. Moon, L.D., Asher, R.A., Rhodes, K.E., and Fawcett, J.W. (2001). Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci 4, 465-466. (Pubitemid 32397182)
15. Steinmetz, M.P., Horn, K.P., Tom, V.J., Miller, J.H., Busch, S.A., Nair, D., Silver, D.J., and Silver, J. (2005). Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J. Neurosci. 25, 8066-8076. (Pubitemid 41254410)
16. Tropea, D., Caleo, M., and Maffei, L. (2003). Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. J. Neurosci. 23, 7034-7044. (Pubitemid 36975869)
17. Wang, D., Ichiyama, R.M., Zhao, R., Andrews, M.R., and Fawcett, J.W. (2011). Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J. Neurosci. 31, 9332-9344.
18. Yick, L.W., Cheung, P.T., So, K.F., and Wu, W. (2003). Axonal regeneration of Clarke's neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC. Exp. Neurol. 182, 160-168. (Pubitemid 36776259)
19. Zhao, R.-R., Muir, E.M., Alves, J.N., Rickman, H., Allan, A.Y., Kwok, J.C., Roet, K.C.D., Verhaagen, J., Schneider, B.L., Bensadoun, J.-C., Ahmed, S.G., Yáñez-Muñoz, R.J., Keynes, R.J., Fawcett, J.W., and Rogers, J.H. (2011). Lentiviral vectors express chondroitinase ABC in cortical projections and promote sprouting of injured corticospinal axons. J. Neurosci. Methods 201, 228-238.
20. Soleman, S., Yip, P.K., Duricki, D.A., and Moon, L.D.F. (2012). Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats. Brain 135, 1210-1223.
21. Castro-Alamancos, M.A., and Borrell, J. (1995). Functional recovery of forelimb response capacity after forelimb primary motor cortex damage in the rat is due to the reorganization of adjacent areas of cortex. Neuroscience 68, 793-805.
22. Asikainen, I., Kaste, M., and Sarna, S. (1999). Early and late posttraumatic seizures in traumatic brain injury rehabilitation patients: brain injury factors causing late seizures and influence of seizures on long-term outcome. Epilepsia 40, 584-589. (Pubitemid 29207322)
23. Harris, N.G., Mironova, Y.A., Hovda, D.A., and Sutton, R.L. (2010). Pericontusion axon sprouting is spatially and temporally consistent with a growth-permissive environment after traumatic brain injury. J. Neuropathol. Exp. Neurol. 69, 139-154.
24. Chen S., Richards, H.K., Smielewski, P., Pickard, J.D., and Harris N.G. (2002). Preventing flow-Metabolism uncoupling acutely reduces evolving axonal injury after traumatic brain injury. J. Neurotrauma 19, 1300.
25. Chen, S., Pickard, J.D., and Harris, N.G. (2003). Time course of cellular pathology after controlled cortical impact injury. Exp. Neurol. 182, 87-102. (Pubitemid 36776252)
26. Chen, S.F., Richards, H.K., Smielewski, P., Johnstrom, P., Salvador, R., Pickard, J.D., and Harris, N.G. (2004). Relationship between flowmetabolism uncoupling and evolving axonal injury after experimental traumatic brain injury. J. Cereb. Blood Flow Metab. 24, 1025-1036. (Pubitemid 39223626)
27. Harris, N.G., Mironova, Y.A., Chen, S.-F., Richards, H.K., and Pickard, J.D. (2012). Preventing flow-metabolism uncoupling acutely reduces axonal injury after traumatic brain injury. J. Neurotrauma 29, 1469-1482.
28. Pawela, C.P., Biswal, B.B., Hudetz, A.G., Schulte, M.L., Li, R., Jones, S.R., Cho, Y.R., Matloub, H.S., and Hyde, J.S. (2009). A protocol for use of medetomidine anesthesia in rats for extended studies using taskinduced BOLD contrast and resting-state functional connectivity. Neuroimage 46, 1137-1147.
29. Verley, D., Hovda, D.A., Sutton, R.L., and Harris, N.G. (2011). Timecourse of sensorimotor brain activation after traumatic brain injury in the rat. J. Neurotrauma 28, A-81,P220.
30. Lowe, A.S., Beech, J.S., and Williams, S.C.R. (2007). Small animal, whole brain fMRI: innocuous and nociceptive forepaw stimulation. Neuroimage 35, 719-728. (Pubitemid 46420429)
31. Ghosh, A., Haiss, F., Sydekum, E., Schneider, R., Gullo, M., Wyss, M.T., Mueggler, T., Baltes, C., Rudin, M., Weber, B., and Schwab, M.E. (2010). Rewiring of hindlimb corticospinal neurons after spinal cord injury. Nat. Neurosci. 13, 97-104.
32. Bullitt, E., Lee, C.L., Light, A.R., and Willcockson, H. (1992). The effect of stimulus duration on noxious-stimulus induced c-fos expression in the rodent spinal cord. Brain Res. 580, 172-179.
33. Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J.W., and Maffei, L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251. (Pubitemid 35285495)
34. Pyka, M., Wetzel, C., Aguado, A., Geissler, M., Hatt, H., and Faissner, A. (2011). Chondroitin sulfate proteoglycans regulate astrocyte-dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons. Eur. J. Neurosci. 33, 2187-2202.
35. Massey, J.M., Hubscher, C.H., Wagoner, M.R., Decker, J.A., Amps, J., Silver, J., and Onifer, S.M. (2006). Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J. Neurosci. 26, 4406-4414. (Pubitemid 44315399)
36. Dityatev, A., Bruckner, G., Dityateva, G., Grosche, J., Kleene, R., and Schachner, M. (2007). Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev. Neurobiol. 67, 570-588. (Pubitemid 47066941)
37. Yang, L., Afroz, S., Michelson, H.B., Goodman, J.H., Valsamis, H.A., and Ling, D.S.F. (2010). Spontaneous epileptiform activity in rat neocortex after controlled cortical impact injury. J. Neurotrauma 27, 1541-1548.
38. Papadopoulos, C.M., Tsai, S.Y., Cheatwood, J.L., Bollnow, M.R., Kolb, B.E., Schwab, M.E., Kartje, G.L. (2005) Dendritic plasticity in the adult rat following middle cerebral artery occlusion and Nogo-A neutralization. Cereb. Cortex 16, 529-536.
39. Karetko-Sysa, M., Skangiel-Kramska, J., and Nowicka, D. (2011). Disturbance of perineuronal nets in the perilesional area after photothrombosis is not associated with neuronal death. Exp. Neurol. 231, 113-126.
40. Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C.I., Choquet, D., and Gundelfinger, E.D. (2009). Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat, Neurosci. 12, 897-904.
41. Clarkson, A.N., Huang, B.S., MacIsaac, S.E., Mody, I., and Carmichael, S.T. (2010). Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468, 305-309.
42. Wegner, F., Hartig, W., Bringmann, A., Grosche, J., Wohlfarth, K., Zuschratter, W., and Bruckner, G. (2003). Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABAA receptor [alpha]1 subunit form a unique entity in rat cerebral cortex. Exp. Neurol. 184, 705-714. (Pubitemid 38182799)
43. Carulli, D., Pizzorusso, T., Kwok, J.C.F., Putignano, E., Poli, A., Forostyak, S., Andrews, M.R., Deepa, S.S., Glant, T., and Fawcett, J.W. (2010). Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133, 2331-2347
44. Saghatelyan, A.K., Dityatev, A., Schmidt, S., Schuster, T., Bartsch, U., and Schachner, M. (2001). Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol. Cell. Neurosci. 17, 226-240. (Pubitemid 32113549)
45. Gentet, L.J., Kremer, Y., Taniguchi, H., Huang, Z.J., Staiger, J.F., and Petersen, C.C.H. (2012). Unique functional properties of somatostatinexpressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607-612.
46. Benali, A., Weiler, E., Benali, Y., Dinse, H.R., and Eysel, U.T. (2008). Excitation and inhibition jointly regulate cortical reorganization in adult rats. J. Neurosci. 28, 12284-12293.
47. Hermann, G.E., Rogers, R.C., Bresnahan, J.C., and Beattie, M.S. (2001). Tumor necrosis factor-alpha induces cFOS and strongly potentiates glutamate-mediated cell death in the rat spinal cord. Neurobiol. Dis. 8, 590-599. (Pubitemid 32758663)
48. Hermann, G.E., and Rogers, R.C. (2009). TNF activates astrocytes and catecholaminergic neurons in the solitary nucleus: implications for autonomic control. Brain Res. 1273, 72-82.
49. Su, C.-K., Ho, C.-M., Kuo, H.-H., Wen, Y.-C., and Chai, C.-Y. (2009). Sympathetic-correlated c-Fos expression in the neonatal rat spinal cord in vitro. J. Biomed Sci. 16, 44.
50. Stevens, B., and Fields, R. (2000). Response of Schwann cells to action potentials in development. Science 287, 2267-2271. (Pubitemid 30177032)
51. Goldenberg-Cohen, N., Guo, Y., Margolis, F., Cohen, Y., Miller, N.R., and Bernstein, S.L. (2005). Oligodendrocyte dysfunction after induction of experimental anterior optic nerve ischemia. Invest. Ophthalmol. Vis. Sci. 46, 2716-2725. (Pubitemid 43086691)
52. Nedergaard, M., and Verkhratsky, A. (2012). Artifact versus reality-how astrocytes contribute to synaptic events. Glia 60, 1013-1023.
53. Rusakov, D.A. (2001). The role of perisynaptic glial sheaths in glutamate spillover and extracellular Ca(2 + ) depletion. Biophys. J. 81, 1947-1959. (Pubitemid 32917147)
54. Hrabetov, D.A. (2001). The role of perisynaptic glial sheaths in glu. Calcium diffusion enhanced after cleavage of negatively charged components of brain extracellular matrix by chondroitinase ABC. J. Physiol 587, 4029-4049.
55. Lloyd, E., Somera-Molina, K., Van Eldik, L.J., Watterson, D.M., and Wainwright, M.S. (2008). Suppression of acute proinflammatory cytokine and chemokine upregulation by post-injury administration of a novel small molecule improves long-term neurologic outcome in a mouse model of traumatic brain injury. J. Neuroinflammation 5, 28.
56. Carter, L.M., Starkey, M.L., Akrimi, S.F., Davies, M., McMahon, S.B., and Bradbury, E.J. (2008). The yellow fluorescent protein (YFPH) mouse reveals neuroprotection as a novel mechanism underlying chondroitinase ABC-mediated repair after spinal cord injury. J. Neurosci. 28, 14107-14120.
57. Rolls, A., Cahalon, L., Bakalash, S., Avidan, H., Lider, O., and Schwartz, M. (2006). A sulfated disaccharide derived from chondroitin sulfate proteoglycan protects against inflammation-associated neurodegeneration. FASEB J. 20, 547-549. (Pubitemid 46671245)