Chondroitin Sulfate Proteoglycans in the Nervous System: Inhibitors to Repair

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Siebert, Justin R ^a   Conta Steencken, Amanda ^b   Osterhout, Donna J ^b  

^a LAKE ERIE COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

^b SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN ABC LYASE; PROTEOCHONDROITIN SULFATE;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN DAMAGE; CENTRAL NERVOUS SYSTEM FUNCTION; HUMAN; INFLAMMATION; MODULATION; MULTIPLE SCLEROSIS; NERVOUS SYSTEM; NONHUMAN; OLIGODENDROGLIA; PARKINSON DISEASE; PROTEIN EXPRESSION; REVIEW; ANIMAL; DRUG EFFECTS; INJURY; METABOLISM; NERVE DEGENERATION; NERVE REGENERATION; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CHONDROITIN SULFATE PROTEOGLYCANS; HUMANS; INFLAMMATION; NERVE DEGENERATION; NERVE REGENERATION; NERVOUS SYSTEM; WOUNDS AND INJURIES;

EID: 84920930485     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/845323     Document Type: Review

References (174)

1. I. M. Elatorai, "History of spinal cord medicine," in Spinal Cord Medicine: Principles & Practice, V. W. Lin, Ed., pp. 3-14,Demos Medical, New York, NY, USA, 2003.
2. S. David and A. J. Aguayo, "Axonal elongation into peripheral nervous systembridges after central nervous systeminjury in adult rats," Science, vol. 214, no. 4523, pp. 931-933, 1981.
3. M. Benfey and A. J. Aguayo, "Extensive elongation of axons fromrat brain into peripheral nerve grafts," Nature, vol. 296, no. 5853, pp. 150-152, 1982.
4. K. J. L. Fernandes, D. P. Fan, B. J. Tsui, S. L. Cassar, and W. Tetzlaff, "Influence of the axotomy to cell body distance in rat rubrospinal and spinal motor neurons: Differential regulation of GAP-43, Tubulins, and Neurofilament-M," Journal of Comparative Neurology, vol. 414, pp. 494-510, 1999.
5. M. K. Hossain-Ibrahim, K. Rezajooi, J. K. MacNally, M. R. J. Mason, A. R. Lieberman, and P. N. and erson, "Effects of lipopolysaccharide-induced inflammation on expression of growth-associated genes by corticospinal neurons," BMC Neuroscience, vol. 7, article 8, 2006.
6. M. R. J. Mason, A. R. Lieberman, and P. N. and erson, "Corticospinal neurons up-regulate a range of growth-associated genes following intracortical, but not spinal, axotomy," European Journal of Neuroscience, vol. 18, no. 4, pp. 789-802, 2003.
7. Injury Prevention & Control: Traumatic Brain Injury, "Centers for Disease Control and Prevention," http://www.cdc.gov/TraumaticBrainInjury.
8. SCI Information Network, University of Alabama at Birmingham, 2013, https://www.nscisc.uab.edu/.
9. W. Young, "Spinal cord contusion models," Progress in Brain Research, vol. 137, pp. 231-255, 2002.
10. C. Profyris, S. S. Cheema, D. Zang, M. F. Azari, K. Boyle, and S. Petratos, "Degenerative and regenerative mechanisms governing spinal cord injury," Neurobiology of Disease, vol. 15, no. 3, pp. 415-436, 2004.
11. S. T. Dawodu, Traumatic Brain Injury (TBI)-Definition, Epidemiology, Pathophysiology, Medscape, 2014, http://emedicine .medcape.com/article/326510-overview#aw2aab6b4.
12. J. R. Faulkner, J. E. Herrmann, M. J. Woo, K. E. Tansey, N. B. Doan, and M. V. Sofroniew, "Reactive astrocytes protect tissue and preserve function after spinal cord injury," The Journal of Neuroscience, vol. 24, no. 9, pp. 2143-2155, 2004.
13. D. J. Myer, G. G. Gurkoff, S. M. Lee, D. A. Hovda, and M. V. Sofroniew, "Essential protective roles of reactive astrocytes in traumatic brain injury," Brain, vol. 129, no. 10, pp. 2761-2772, 2006.
14. A. Rolls, R. Shechter, and M. Schwartz, "The bright side of the glial scar in CNS repair," Nature Reviews Neuroscience, vol. 10, no. 3, pp. 235-241, 2009.
15. M. V. Sofroniew, "Molecular dissection of reactive astrogliosis and glial scar formation," Trends in Neurosciences, vol. 32, no. 12, pp. 638-647, 2009.
16. C. E. Bandtlow and D. E. Zimmermann, "Proteoglycans in the developing brain: New conceptual insights for old proteins," Physiological Reviews, vol. 80, no. 4, pp. 1267-1291, 2000.
17. M. S. Viapiano and R. T. Matthews, "From barriers to bridges: Chondroitin sulfate proteoglycans in neuropathology," Trends in Molecular Medicine, vol. 12, no. 10, pp. 488-496, 2006.
18. C. M. Galtrey and J.W. Fawcett, "The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system," Brain Research Reviews, vol. 54, no. 1, pp. 1-18, 2007.
19. A. Nishiyama, K. J. Dahlin, J. T. Prince, S. R. Johnstone, and W. B. Stallcup, "The primary structure of NG2, a novelmembranespanning proteoglycan," Journal of Cell Biology, vol. 114, no. 2, pp. 359-371, 1991.
20. R. Lin, T. W. Rosahl, P. J. Whiting, J. W. Fawcett, and J. C. F. Kwok, "6-Sulphated chondroitins have a positive influence on axonal regeneration," PLoS ONE, vol. 6, no. 7,Article ID e21499, 2011.
21. H. Wang, Y. Katagiri, T. E. McCann et al., "Chondroitin-4-sulfation negatively regulates axonal guidance and growth," Journal of Cell Science, vol. 121, no. 15, pp. 3083-3091, 2008.
22. J.H. Yi, Y. Katagiri, B. Susarla,D. Figge, A. J. Symes, and H.M. Geller, "Alterations in sulfated chondroitin glycosaminoglycans following controlled cortical impact injury in mice," TheJournal of Comparative Neurology, vol. 520, no. 15, pp. 3295-3313, 2012.
23. D. M. Snow, V. Lemmon, D. A. Carrino, A. I. Caplan, and J. Silver, "Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro," Experimental Neurology, vol. 109, no. 1, pp. 111-130, 1990.
24. A. M. Clement, S. Nadanaka, K. Masayama, C. Mandl, K. Sugahara, and A. Faissner, "The DSD-1 carbohydrate epitope depends on sulfation, correlates with chondroitin sulfate D motifs, and is sufficient to promote neurite outgrowth," The Journal of Biological Chemistry, vol. 273, no. 43, pp. 28444-28453, 1998.
25. A. M. Clement, K. Sugahara, and A. Faissner, "Chondroitin sulfate E promotes neurite outgrowth of rat embryonic day 18 hippocampal neurons," Neuroscience Letters, vol. 269, no. 3, pp. 125-128, 1999.
26. S. A. Busch and J. Silver, "Therole of extracellular matrix in CNS regeneration," Current Opinion in Neurobiology, vol. 17,no. 1, pp. 120-127, 2007.
27. K. E. Rhodes and J. W. Fawcett, "Chondroitin sulphate proteoglycans: Preventing plasticity or protecting the CNS?" Journal of Anatomy, vol. 204, no. 1, pp. 33-48, 2004.
28. S.Thuret, L. D. F.Moon, and F. H. Gage, "Therapeutic interventions after spinal cord injury," Nature Reviews Neuroscience, vol. 7, no. 8, pp. 628-643, 2006.
29. J.W. Fawcett and R. A.Asher, "The glial scar and central nervous system repair," Brain Research Bulletin, vol. 49, no. 6, pp. 377-391, 1999.
30. M. D. Norenberg, J. Smith, and A. Marcillo, "The pathology of human spinal cord injury: Defining the Problems," Journal of Neurotrauma, vol. 21, no. 4, pp. 429-440, 2004.
31. G. Stoll, B. D. Trapp, and J. W. Griffin, "Macrophage function during Wallerian degeneration of rat optic nerve: Clearance of degeneratingmyelin and Ia expression," Journal ofNeuroscience, vol. 9, no. 7, pp. 2327-2335, 1989.
32. V. H. Perry, M. C. Brown, and S. Gordon, "The macrophage response to central and peripheral nerve injury: A possible role for macrophages in regeneration," Journal of Experimental Medicine, vol. 165, no. 4, pp. 1218-1223, 1987.
33. J. C. Fleming, M. D. Norenberg, D. A. Ramsay et al., "The cellular inflammatory response in human spinal cords after injury," Brain, vol. 129, no. 12, pp. 3249-3269, 2006.
34. K. A. Kigerl, J. C. Gensel, D. P. Ankeny, J. K. Alexander, D. J. Donnelly, and P. G. Popovich, "Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injuredmouse spinal cord," Journal of Neuroscience, vol. 29, no. 43, pp. 13435-13444, 2009.
35. K. D. Barron, "The microglial cell. A historical review," Journal of the Neurological Sciences, vol. 134, no. 1, pp. 57-68, 1995.
36. F. Aloisi, "Immune function of microglia," Glia, vol. 36, no. 2, pp. 165-179, 2001.
37. R. B. Rock, G. Gekker, S. Hu et al., "Role of microglia in central nervous system infections," Clinical Microbiology Reviews, vol. 17, no. 4, pp. 942-964, 2004.
38. P.G. Popovich, P. Wei, and B. T. Stokes, "Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats," Journal of Comparative Neurology, vol. 377, pp. 443-464, 1997.
39. C. E. Bandtlow, M. F. Schmidt, T. D. Hassinger, M. E. Schwab, and S. B. Kater, "Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones," Science, vol. 259, no. 5091, pp. 80-83, 1993.
40. G. Yiu and Z. He, "Glial inhibition of CNS axon regeneration," Nature Reviews Neuroscience, vol. 7, no. 8, pp. 617-627, 2006.
41. C. L. Masters and K. Beyreuther, "Neuronal origin of cerebral amyloidogenic proteins: Their role in Alzheimers disease and unconventional virus diseases of the nervous system," Ciba Foundation Symposium, vol. 126, pp. 49-64, 1987.
42. H. Braak, E. Braak, and M. Strothjohann, "Abnormally phosphorylated tau protein related to the formation of neurofibrillary tangles and neuropil threads in the cerebral cortex of sheep and goat," Neuroscience Letters, vol. 171, no. 1-2, pp. 1-4, 1994.
43. I. S. Coraci, J. Husemann, J. W. Berman et al., "CD36, a class B scavenger receptor, is expressed on microglia in Alzheimers disease brains and can mediate production of reactive oxygen species in response to β-amyloid fibrils," The American Journal of Pathology, vol. 160, no. 1, pp. 101-112, 2002.
44. J. T. Jarrett, E. P. Berger, and P. T. Lansbury Jr., "The C-terminus of the βprotein is critical inamyloidogenesis," Annals of the New York Academy of Sciences, vol. 695, pp. 144-148, 1993.
45. S. Itagaki, P. L. McGeer, H. Akiyama, S. Zhu, and D. Selkoe, "Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease," Journal of Neuroimmunology, vol. 24, no. 3, pp. 173-182, 1989.
46. P. L. McGeer, H. Akiyama, S. Itagaki, and E. G. McGeer, "Activation of the classical complement pathway in brain tissue of Alzheimer patients," Neuroscience Letters, vol. 107, no. 1-3, pp. 341-346, 1989.
47. P. L. McGeer, H. Akiyama, S. Itagaki, and E. G. McGeer, "Immune system response in Alzheimers disease," Canadian Journal of Neurological Sciences, vol. 16, no. 4, pp. 516-527, 1989.
48. P. L. McGeer and E. G. McGeer, "Autotoxicity and Alzheimer disease," Archives of Neurology, vol. 57, no. 6, pp. 789-790, 2000.
49. H. Akiyama, S. Barger, S. Barnum et al., "Inflammation and Alzheimers disease," Neurobiology of Aging, vol. 21, no. 3, pp. 383-421, 2000.
50. A. Gupta and K. Pansari, "Inflammation and Alzheimers disease," International Journal of Clinical Practice, vol. 57, no. 1, pp. 36-39, 2003.
51. P. L. McGeer and E. G. McGeer, "Inflammation, autotoxicity and Alzheimer disease," Neurobiology of Aging, vol. 22, no. 6, pp. 799-809, 2001.
52. P. L.McGeer and E. G.McGeer, "Local neuroinflammation and the progression of Alzheimers disease," Journal of NeuroVirology, vol. 8, no. 6, pp. 529-538, 2002.
53. P. L. McGeer, E. G. McGeer, and K. Yasojima, "Alzheimer disease and neuroinflammation," Journal of Neural Transmission, Supplement, no. 59, pp. 53-57, 2000.
54. P.Teismann, K.Tieu,D.Choi et al., "Cyclooxygenase-2 is instrumental in Parkinsons disease neurodegeneration," Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5473-5478, 2003.
55. S. Fahn, "Description of Parkinsons disease as a clinical syndrome," Annals of the New York Academy of Sciences, vol. 991, pp. 1-14, 2003.
56. S. Hunot and E. C. Hirsch, "Neuroinflammatory processes in Parkinsons disease," Annals of Neurology, vol. 53,no. 3, pp. S49-S60, 2003.
57. C. F. Orr, D. B. Rowe, and G. M. Halliday, "An inflammatory review of Parkinson's disease," Progress in Neurobiology, vol. 68, no. 5, pp. 325-340, 2002.
58. D. C. Wu, V. Jackson-Lewis, M. Vila et al., "Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease," Journal of Neuroscience, vol. 22, no. 5, pp. 1763-1771, 2002.
59. B. Liu, L. Du, and J.Hong, "Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation," Journal of Pharmacology and ExperimentalTherapeutics, vol. 293, no.2,pp. 607-617, 2000.
60. E. Grünblatt, S. Mandel, and M. B. H. Youdim, "Neuroprotective strategies in Parkinsons disease using the models of 6-hydroxydopamine and MPTP," Annals of the New York Academy of Sciences, vol. 899, pp. 262-273, 2000.
61. G.T.Liberatore,V. Jackson-Lewis, S.Vukosavic et al., "Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease," Nature Medicine, vol. 5, no. 12, pp. 1403-1409, 1999.
62. P.L.McGeer, S. Itagaki,H. Tago, and E.G.McGeer, "Occurrence of HLA-DR reactive microglia in Alzheimers disease," Annals of the New York Academy of Sciences, vol. 540, pp. 319-323, 1988.
63. M. Mogi, M. Harada, T. Kondo, P. Riederer, and T. Nagatsu, "Brain β2-microglobulin levels are elevated in the striatum in Parkinsons diseaselevels are elevated in the striatum in Parkinsons disease," Journal of Neural Transmission: Parkinsons Disease and Dementia Section, vol. 9, no. 1, pp. 87-92, 1995.
64. M. Rodríguez, P. Barroso-Chinea, P. Abdala, J. Obeso, and T. González-Hernández, "Dopamine cell degeneration induced by intraventricular administration of 6-hydroxydopamine in the rat: Similarities with cell loss in Parkinsons disease," Experimental Neurology, vol. 169, no. 1, pp. 163-181, 2001.
65. G. Martino, E. Clementi, E. Brambilla et al., "γ interferon activates a previously undescribed Ca2+ influx in T lymphocytes from patients with multiple sclerosis," Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 11, pp. 4825-4829, 1994.
66. J. Correale and M. De los Milagros Bassani Molinas, "Oligoclonal bands and antibody responses in multiple sclerosis," Journal of Neurology, vol. 249, no. 4, pp. 375-389, 2002.
67. H. Lassmann, W. Brück, and C. Lucchinetti, "Heterogeneity of multiple sclerosis pathogenesis: Implications for diagnosis and therapy," Trends in Molecular Medicine, vol. 7, no. 3, pp. 115-121, 2001.
68. M. A. Proescholdt, S. Jacobson, N. Tresser, E. H. Oldfield, and M. J. Merrill, "Vascular endothelial growth factor is expressed in multiple sclerosis plaques and can induce inflammatory lesions in experimental allergic encephalomyelitis rats," Journal of Neuropathology & Experimental Neurology, vol. 61, no. 10, pp. 914-925, 2002.
69. K. W. Selmaj, M. Farooq, W. T. Norton, C. S. Raine, and C. F. Brosnan, "Proliferation of astrocytes in vitro in response to cytokines. A primary role for tumor necrosis factor," Journal of Immunology, vol. 144, no. 1, pp. 129-135, 1990.
70. F. Aloisi, A. Giampaolo, G. Russo, C. Peschle, and G. Levi, "Developmental appearance, antigenic profile, and proliferation of glial cells of the human embryonic spinal cord: An immunocytochemical study using dissociated cultured cells," Glia, vol. 5, no. 3, pp. 171-181, 1992.
71. K. Frei, K. Nohava, U. V. Malipiero, C. Schwerdel, and A. Fontana, "Production ofmacrophage colony-stimulating factor by astrocytes and brain macrophages," Journal of Neuroimmunology, vol. 40, no. 2-3, pp. 189-195, 1992.
72. D. Giulian and J. F. Ingeman, "Colony-stimulating factors as promoters of ameboid microglia," Journal of Neuroscience, vol. 8, no. 12, pp. 4707-4717, 1988.
73. P. C. Wong, H. Cai, D. R. Borchelt, and D. L. Price, "Genetically engineered mouse models of neurodegenerative diseases," Nature Neuroscience, vol. 5, no. 7, pp. 633-639, 2002.
74. F. Torreilles, S. Salman-Tabcheh, M. Guérin, and J. Torreilles, "Neurodegenerative disorders: The role of peroxynitrite," Brain Research Reviews, vol. 30, no. 2, pp. 153-163, 1999.
75. P. L. McGeer and E. G. McGeer, "Inflammatory processes in amyotrophic lateral sclerosis," Muscle and Nerve, vol. 26, no. 4, pp. 459-470, 2002.
76. K. Hensley, R. A. Floyd, B. Gordon et al., "Temporal patterns of cytokine and apoptosis-related gene expression in spinal cords of the G93A-SOD1 mouse model of amyotrophic lateral sclerosis," Journal of neurochemistry, vol. 82, pp. 365-374, 2002.
77. H. Akiyama and P. L. McGeer, "Brain microglia constitutively express β-2 integrins," Journal of Neuroimmunology, vol. 30, no. 1, pp. 81-93, 1990.
78. T. Kawamata, H. Akiyama, T. Yamada, and P. L. McGeer, "Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue," The American Journal of Pathology, vol. 140, no. 3, pp. 691-707, 1992.
79. D. Troost, J. J. van den Oord, and J. M. B. Vianney de Jong, "Immunohistochemical characterization of the inflammatory infiltrate in amyotrophic lateral sclerosis," Neuropathology and Applied Neurobiology, vol. 16, no. 5, pp. 401-410, 1990.
80. P. G. Popovich, B. T. Stokes, and C. C. Whitacre, "Concept of autoimmunity following spinal cord injury: Possible roles for T lymphocytes in the traumatized central nervous system," Journal of Neuroscience Research, vol. 45, pp. 349-363, 1996.
81. Y. Gasche, P. M. Soccal, M. Kanemitsu, and J. Copin, "Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain," Frontiers in Bioscience, vol. 11, no. 2, pp. 1289-1301, 2006.
82. N.Weiss,F.Miller, S. Cazaubon, and P.O.Couraud, "The bloodbrain barrier in brain homeostasis and neurological diseases," Biochimica et BiophysicaActa, vol. 1788,no. 4, pp.842-857, 2009.
83. B. Obermeier, R. Daneman, and R. M. Ransohoff, "Development maintenance and disruption of the blood-brain barrier," Nature Medicine, vol. 19, no. 12, pp. 1584-1596, 2013.
84. B. O. Popescu, E. C. Toescu, L. M. Popescu et al., "Bloodbrain barrier alterations in ageing and dementia," Journal of the Neurological Sciences, vol. 283, no. 1-2, pp. 99-106, 2009.
85. R. M. Friedlander and J. Yuan, "ICE, neuronal apoptosis and neurodegeneration," Cell Death and Differentiation, vol. 5, no. 10, pp. 823-831, 1998.
86. G. Kim, J. Xu, S. Song et al., "Tumor necrosis factor receptor deletion reduces nuclear factor-κB activation, cellular inhibitor of apoptosis protein 2 expression, and functional recovery after traumatic spinal cord injury," Journal of Neuroscience, vol. 21,no. 17, pp. 6617-6625, 2001.
87. K. Selmaj, A. Walczak, M. Mycko, T. Berkowicz, T. Kohno, and C. S. Raine, "Suppression of experimental autoimmune encephalomyelitis with a TNF binding protein (TNFbp) correlates with down-regulation of VCAM-1/VLA-4," European Journal of Immunology, vol. 28, pp. 2035-2044, 1998.
88. K.W. Selmaj, "Tumour necrosis factor and anti-tumour necrosis factor approach to inflammatory demyelinating diseases of the central nervous system," Annals of the Rheumatic Diseases, vol. 59, supplement 1, pp. i94-i102, 2000.
89. W. J. Streit, S. A.Walter, and N. A. Pennell, "Reactivemicrogliosis," Progress in Neurobiology, vol. 57, no. 6, pp. 563-581, 1999.
90. M.Tuna, S. Polat, T. Erman et al., "Effect of anti-rat interleukin-6 antibody after spinal cord injury in the rat: Inducible nitric oxide synthase expression, sodium-and potassium-activated, magnesium-dependent adenosine-5′-triphosphatase and superoxide dismutase activation, and ultrastructural changes," Journal of Neurosurgery, vol. 95, no. 1, pp. 64-73, 2001.
91. K. G. Kahl, N. Kruse, K. V. Toyka, and P. Rieckmann, "Serial analysis of cytokine mRNA profiles in whole blood samples from patients with early multiple sclerosis," Journal of the Neurological Sciences, vol. 200, no. 1-2, pp. 53-55, 2002.
92. P.G.Popovich, Z. Guan,P.Wei, I.Huitinga, N. VanRooijen, and B. T. Stokes, "Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury," Experimental Neurology, vol. 158, no. 2, pp. 351-365, 1999.
93. V. Balasingam, T. Tejada-Berges, E. Wright, R. Bouckova, and V. W. Yong, "Reactive astrogliosis in the neonatal mouse brain and its modulation by cytokines," Journal of Neuroscience, vol. 14, no. 2, pp. 846-856, 1994.
94. D. Giulian, J. Woodward, D. G. Young, J. F. Krebs, and L. B. Lachman, "Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization," Journal of Neuroscience, vol. 8, no. 7, pp. 2485-2490, 1988.
95. R. Shechter, C. Raposo, A. London, I. Sagi, and M. Schwartz, "The glial scar-monocyte interplay: A pivotal resolution phase in spinal cord repair," PLoS ONE, vol. 6, no. 12, Article IDe27969, 2011.
96. V. W. Yong, R. Moumdjian, F. P. Young et al., "γ-Interferon promotes proliferation of adult human astrocytes in vitro and reactive gliosis in the adult mouse brain in vivo," Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 16, pp. 7016-7020, 1991.
97. W. Liu, Y. Tang, and J. Feng, "Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system," Life Sciences, vol. 89, no. 5-6, pp. 141-146, 2011.
98. J. A. Smith, A. Das, S. K. Ray, and N. L. Banik, "Role of proinflammatory cytokines released from microglia in neurodegenerative diseases," Brain Research Bulletin, vol. 87, no. 1, pp. 10-20, 2012.
99. F. Properzi, D. Carulli, R. A. Asher et al., "Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axon-growth inhibitory glia," European Journal of Neuroscience, vol. 21, no. 2, pp. 378-390, 2005.
100. U. Hanisch, "Microglia as a source and target of cytokines," GLIA, vol. 40, no. 2, pp. 140-155, 2002.
101. L. Uhlin-Hansen, T. Wik, L. Kjellen, E. Berg, F. Forsdahl, and S. O. Kolset, "Proteoglycan metabolism in normal and inflammatory human macrophages," Blood, vol. 82, no. 9, pp. 2880-2889, 1993.
102. R. A. Asher, D. A. Morgenstern, M. C. Shearer, K. H. Adcock, P. Pesheva, and J. W. Fawcett, "Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells," Journal of Neuroscience, vol. 22, no. 6, pp. 2225-2236, 2002.
103. L. L. Jones, R. U. Margolis, and M. H. Tuszynski, "The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury," Experimental Neurology, vol. 182, no. 2, pp. 399-411, 2003.
104. S. Imagama, K. Sakamoto, R. Tauchi et al., "Keratan sulfate restricts neural plasticity after spinal cord injury," Journal of Neuroscience, vol. 31, no. 47, pp. 17091-17102, 2011.
105. E. M. andrews, R. J. Richards, F. Q. Yin, M. S. Viapiano, and L. B. Jakeman, "Alterations in chondroitin sulfate proteoglycan expression occur both at and far from the site of spinal contusion injury," Experimental Neurology, vol. 235, no. 1, pp. 174-187, 2012.
106. P. L. McGeer and E. G. McGeer, "The inflammatory response systemof brain: Implications for therapy of Alzheimer and other neurodegenerative diseases," Brain Research Reviews, vol. 21,no. 2, pp. 195-218, 1995.
107. D. Bonneh-Barkay and C. A.Wiley, "Brain extracellular matrix in neurodegeneration," Brain Pathology, vol. 19, no. 4, pp. 573-585, 2009.
108. R. A. Sobel and A. S. Ahmed, "White matter extracellular matrix chondroitin sulfate/dermatan sulfate proteoglycans in multiple sclerosis," Journal of Neuropathology and Experimental Neurology, vol. 60, no. 12, pp. 1198-1207, 2001.
109. M. L. Fuller, A. K. DeChant, B. Rothstein et al., "Bone morphogenetic proteins promote gliosis in demyelinating spinal cord lesions," Annals of Neurology, vol. 62, no. 3, pp. 288-300, 2007.
110. G. Barreto, R. E. White, Y. Ouyang, L. Xu, and R. G. Giffard, "Astrocytes: Targets for neuroprotection in stroke," Central Nervous System Agents in Medicinal Chemistry, vol. 11, no. 2, pp. 164-173, 2011.
111. H.Mizuno, H.Warita, M. Aoki, and Y. Itoyama, "Accumulation of chondroitin sulfate proteoglycans in the microenvironment of spinal motor neurons in amyotrophic lateral sclerosis transgenic rats," Journal of Neuroscience Research, vol. 86, no. 11, pp. 2515-2523, 2008.
112. M.G.Tansey,M. K.McCoy, and T.C.Frank-Cannon, "Neuroinflammatory mechanisms in Parkinsons disease: Potential environmental triggers, pathways, and targets for early therapeutic intervention," Experimental Neurology, vol. 208, no. 1, pp. 1-25, 2007.
113. T. Town, V. Nikolic, and J. Tan, "The microglial activation continuum: From innate to adaptive responses," Journal of Neuroinflammation, vol. 2, article 24, 2005.
114. D. R. Friedlander, P. Milev, L. Karthikeyan, R. K. Margolis, R. U. Margolis, and M. Grumet, "The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth," Journal of Cell Biology, vol. 125, no. 3, pp. 669-680, 1994.
115. B. A.Walker, S. Ji, and S. R. Jaffrey, "Intra-axonal translation of RhoA promotes axon growth inhibition by CSPG," Journal of Neuroscience, vol. 32, no. 41, pp. 14442-14447, 2012.
116. K. E. Dow and W. Wang, "Cell biology of astrocyte proteoglycans," Cellular and Molecular Life Sciences, vol. 54, no. 6, pp. 567-581, 1998.
117. K.-H. Braunewell, P. Pesheva, J. B. McCarthy, L. T. Furcht, B. Schmitz, and M. Schachner, "Functional involvement of sciatic nerve-derived versican and decorin-like molecules and other chondroitin sulphate proteoglycans in ECM-mediated cell adhesion and neurite outgrowth," European Journal of Neuroscience, vol. 7, no. 4, pp. 805-814, 1995.
118. P.S.Fidler,K.Schuette, R. A. Asher et al., "Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: The major axon-inhibitory proteoglycan is NG2," Journal of Neuroscience, vol. 19, no. 20, pp. 8778-8788, 1999.
119. A. M. Tan, W. Zhang, and J. M. Levine, "NG2: A component of the glial scar that inhibits axon growth," Journal of Anatomy, vol. 207, no. 6, pp. 717-725, 2005.
120. D. M. McTigue, R. Tripathi, and P. Wei, "NG2 colocalizes with axons and is expressed by a mixed cell population in spinal cord lesions," Journal ofNeuropathology and ExperimentalNeurology, vol. 65, no. 4, pp. 406-420, 2006.
121. Z. Yang, R. Suzuki, S. B. Daniels, C. B. Brunquell, C. J. Sala, and A.Nishiyama, "NG2 glial cells provide a favorable substrate for growing axons," Journal of Neuroscience, vol. 26, no. 14, pp. 3829-3839, 2006.
122. S. A. Busch, K. P. Horn, F. X. Cuascut et al., "Adult NG2+cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury," Journal of Neuroscience, vol. 30, no. 1, pp. 255-265, 2010.
123. S. Henke-Fahle, K. Wild, A. Sierra, and P. P. Monnier, "Characterization of a new brain-derived proteoglycan inhibiting retinal ganglion cell axon outgrowth," Molecular and Cellular Neuroscience, vol. 18, no. 5, pp. 541-556, 2001.
124. P. P. Monnier, A. Sierra, J. M. Schwab, S. Henke-Fahle, and B. K. Mueller, "The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar," Molecular and Cellular Neuroscience, vol. 22, no. 3, pp. 319-330, 2003.
125. J. R. Siebert and D. J. Osterhout, "The inhibitory effects of chondroitin sulfate proteoglycans on oligodendrocytes," Journal of Neurochemistry, vol. 119, no. 1, pp. 176-188, 2011.
126. L. W. Lau, M. B. Keough, S.Haylock-Jacobs et al., "Chondroitin sulfate proteoglycans in demyelinated lesions impair remyelination," Annals of Neurology, vol. 72, no. 3, pp. 419-432, 2012.
127. J. C. Pendleton, M. J. Shamblott, D. S. Gary et al., "Chondroitin sulfate proteoglycans inhibit oligodendrocyte myelination through PTP," Experimental Neurology, vol. 247, pp. 113-121, 2013.
128. J. M. Levine, R. Reynolds, and J. W. Fawcett, "The oligodendrocyte precursor cell in health and disease," Trends in Neurosciences, vol. 24, no. 1, pp. 39-47, 2001.
129. R. B.Tripathi and D. M.McTigue, "Chronically increased ciliary neurotrophic factor and fibroblast growth factor-2 expression after spinal contusion in rats," Journal of Comparative Neurology, vol. 510, no. 2, pp. 129-144, 2008.
130. J. R. Siebert, D. J. Stelzner, and D. J. Osterhout, "Chondroitinase treatment following spinal contusion injury increases migration of oligodendrocyte progenitor cells," Experimental Neurology, vol. 231, no. 1, pp. 19-29, 2011.
131. M. J. Crowe, J. C. Bresnahan, S.l. Shuman, J. N.Masters, and M. S. Beattie, "Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys," Nature Medicine, vol. 3, no. 1, pp. 73-76, 1997.
132. H. M. Bramlett and W. D. Dietrich, "Progressive damage after brain and spinal cord injury: Pathomechanisms and treatment strategies," Progress in Brain Research, vol. 161, pp. 125-141, 2007.
133. S. A. Back, T. M. F. Tuohy, H. Chen et al., "Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitormaturation," Nature Medicine, vol. 11, no. 9, pp. 966-972, 2005.
134. M. Bugiani, N. Postma, E. Polder et al., "Hyaluronan accumulation and arrested oligodendrocyte progenitor maturation in vanishing white matter disease," Brain, vol. 136, no. 1, pp. 209-222, 2013.
135. D. E. Harlow and W. B. Macklin, "Inhibitors of remyelination: ECM changes, SPGs and PTPs," Experimental Neurology, vol. 251, pp. 39-46, 2014.
136. D. Fisher, B. Xing, J. Dill et al., "Leukocyte common antigenrelated phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors," Journal of Neuroscience, vol. 31, no. 40, pp. 14051-14066, 2011.
137. T. L. Dickendesher, K. T. Baldwin, Y. A. Mironova et al., "NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans," Nature Neuroscience, vol. 15, no. 5, pp. 703-712, 2012.
138. D. Crespo, R. A. Asher, R. Lin, K. E. Rhodes, and J.W. Fawcett, "How does chondroitinase promote functional recovery in the damaged CNS?" Experimental Neurology, vol. 206, no. 2, pp. 159-171, 2007.
139. J. Zuo, D. Neubauer, K. Dyess, T. A. Ferguson, and D. Muir, "Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue," Experimental Neurology, vol. 154, no. 2, pp. 654-662, 1998.
140. L. Yick,W.Wu, K. So,H.K. Yip, and D. K. Shum, "Chondroitinase ABC promotes axonal regeneration of Clarkes neurons after spinal cord injury," NeuroReport, vol. 11, no. 5, pp. 1063-1067, 2000.
141. E. J. Bradbury, L.D. F.Moon, R. J. Popat et al., "Chondroitinase ABC promotes functional recovery after spinal cord injury," Nature, vol. 416, no. 6881, pp. 636-640, 2002.
142. L. Yick, P. Cheung, K. So, and W. Wu, "Axonal regeneration of Clarkes neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC," Experimental Neurology, vol. 182, no. 1, pp. 160-168, 2003.
143. A. W. Barritt, M. Davies, F. Marchand et al., "Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury," Journal of Neuroscience, vol. 26, no. 42, pp. 10856-10867, 2006.
144. V. J. Tom, R. Kadakia, L. Santi, and J.D.Houlé, "Administration of chondroitinase ABC rostral or caudal to a spinal cord injury site promotes anatomical but not functional plasticity," Journal of Neurotrauma, vol. 26, no. 12, pp. 2323-2333, 2009.
145. S. Soleman, P. K. Yip, D. A. Duricki, and L.D.F.Moon, "Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats," Brain, vol. 135, no. 4, pp. 1210-1223, 2012.
146. J. J. Hill, K. Jin, X. O. Mao, L. Xie, and D. A. Greenberg, "Intracerebral chondroitinase ABC and heparan sulfate proteoglycan glypican improve outcome from chronic stroke in rats," Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 23, pp. 9155-9160, 2012.
147. N. G. Harris, Y. A. Mironova, D. A. Hovda, and R. L. Sutton, "Chondroitinase ABC enhances pericontusion axonal sprouting but does not confer robust improvements in behavioral recovery," Journal of Neurotrauma, vol. 27, no. 11, pp. 1971-1982, 2010.
148. N. J. Tester, A. H. Plaas, and D. R.Howland, "Effect of body temperature on chondroitinase ABCs ability to cleave chondroitin sulfate glycosaminoglycans," Journal of Neuroscience Research, vol. 85, no. 5, pp. 1110-1118, 2007.
149. G. García-Alías, R. Lin, S. F. Akrimi, D. Story, E. J. Bradbury, and J.W. Fawcett, "Therapeutic time window for the application of chondroitinase ABC after spinal cord injury," Experimental Neurology, vol. 210, no. 2, pp. 331-338, 2008.
150. M. Nazari-Robati, K. Khajeh, M. Aminian, N. Mollania, and A. Golestani, "Enhancement of thermal stability of chondroitinase ABC i by site-directed mutagenesis: An insight from Ramachandran plot," Biochimica et Biophysica Acta -Proteins and Proteomics, vol. 1834, no. 2, pp. 479-486, 2013.
151. G. M. Curinga, D. M. Snow, C. Mashburn et al., "Mammalianproduced chondroitinase AC mitigates axon inhibition by chondroitin sulfate proteoglycans," Journal of Neurochemistry, vol. 102, no. 1, pp. 275-288, 2007.
152. Y. Jin, A. Ketschek, Z. Jiang, G. Smith, and I. Fischer, "Chondroitinase activity can be transduced by a lentiviral vector in vitro and in vivo," Journal of Neuroscience Methods, vol. 199, no. 2, pp. 203-213, 2011.
153. R. Zhao, E. M. Muir, J. N. Alves et al., "Lentiviral vectors express chondroitinase ABC in cortical projections and promote sprouting of injured corticospinal axons," Journal of Neuroscience Methods, vol. 201, no. 1, pp. 228-238, 2011.
154. H. Kanno, Y. Pressman, A. Moody et al., "Combination of engineered Schwann cell grafts to secrete neurotrophin and chondroitinase promotes axonal regeneration and locomotion after spinal cord injury," The Journal of Neuroscience, vol. 34, no. 5, pp. 1838-1855, 2014.
155. K. Bartus, N. D. James, A. Didangelos et al., "Large-scale chondroitin sulfate proteoglycan digestion with chondroitinase gene therapy leads to reduced pathology and modulatesmacrophage phenotype following spinal cord contusion injury," Journal of Neuroscience, vol. 34, no. 14, pp. 4822-4836, 2014.
156. J.D. Lannu, R.Choi,A.Au et al., "Chondroitinase activity is protected for extended times when incorporated into nanospheres for time release delivery," Neuroscience, abstracts,Washington, DC, USA, Society for Neuroscience, 2007.
157. D. J. Osterhout, P. D. Garma, A. Au et al., "Chondroitinase release from nanospheres induces axonal sprouting after spinal cord injury," Submitted.
158. F. M. Bareyre, M. Kerschensteiner, O. Raineteau, T. C. Mettenleiter, O.Weinmann, and M. E. Schwab, "The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats," Nature Neuroscience, vol. 7, no. 3, pp. 269-277, 2004.
159. I. C. Maier and M. E. Schwab, "Sprouting, regeneration, and circuit formation in the injured spinal cord: Factors and activity," Nature Medicine, vol. 12, pp. 790-792, 2006.
160. G. Courtine, B. Song, R. R. Roy et al., "Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury," Nature Medicine, vol. 14, no. 1, pp. 69-74, 2008.
161. E. J. Bradbury and S. B. McMahon, "Spinal cord repair strategies: Why do they work?" Nature Reviews Neuroscience, vol. 7, no. 8, pp. 644-653, 2006.
162. S. Karimi-Abdolrezaee, D. Schut, J. Wang, and M. G. Fehlings, "Chondroitinase and growth factors enhance activation and oligodendrocyte differentiation of endogenous neural precursor cells after spinal cord injury," PLoS ONE, vol. 7, no. 5,Article ID e37589, 2012.
163. G.K.Matsushima and P.Morell, "Theneurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system," Brain Pathology, vol. 11, no. 1, pp. 107-116, 2001.
164. T. L. Laabs, H. Wang,Y.Katagiri, T. McCann, J.W. Fawcett, and H. M. Geller, "Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans," Journal of Neuroscience, vol. 27, no. 52, pp. 14494-14501, 2007.
165. B. Grimpe and J. Silver, "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," Journal of Neuroscience, vol. 24, no. 6, pp. 1393-1397, 2004.
166. M. L. Lemons, J. D. Sandy, D. K. and erson, and D. R. Howland, "Intact aggrecan and chondroitin sulfate-depleted aggrecan core glycoprotein inhibit axon growth in the adult rat spinal cord," Experimental Neurology, vol. 184, no. 2,pp. 981-990, 2003.
167. J. Silver and J. H. Miller, "Regeneration beyond the glial scar," Nature Reviews Neuroscience, vol. 5, no. 2, pp. 146-156, 2004.
168. M. Grumet, P. Milev, T. Sakurai et al., "Interactions with tenascin and differential effects on cell adhesion of neurocan and phosphacan, two major chondroitin sulfate proteoglycans of nervous tissue," The Journal of Biological Chemistry, vol. 269, no. 16, pp. 12142-12146, 1994.
169. R. K. Margolis, U. W. E. Rauch, P. Maurel, and R. U. Margolis, "Neurocan and phosphacan: Two major nervous tissue-specific chondroitin sulfate proteoglycans," Perspectives onDevelopmental Neurobiology, vol. 3, no. 4, pp. 273-290, 1996.
170. L. L. Jones and M. H. Tuszynski, "Spinal cord injury elicits expression of keratan sulfate proteoglycans by macrophages, reactive microglia, and oligodendrocyte progenitors," The Journal of Neuroscience, vol. 22, no. 11, pp. 4611-4624, 2002.
171. L. L. Jones, Y. Yamaguchi, W. B. Stallcup, and M. H. Tuszynski, "NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors," Journal of Neuroscience, vol. 22, no. 7, pp. 2792-2803, 2002.
172. L. Zhu, J. Lu, S. S. W. Tay, H. Jiang, and B. P. He, "Induced NG2 expressing microglia in the facialmotor nucleus after facial nerve axotomy," Neuroscience, vol. 166, no. 3, pp. 842-851, 2010.
173. J. Bu,N. Akhtar, and A.Nishiyama, "Transient expression of the NG2 proteoglycan by a subpopulation of activatedmacrophages in an excitotoxic hippocampal lesion," GLIA, vol. 34, no. 4, pp. 296-310, 2001.
174. L. Zhu, P. Xiang, K. Guo et al., "Microglia/monocytes with NG2 expression have no phagocytic function in the cortex after LPS focal injection into the rat brain," GLIA, vol. 60, no. 9, pp. 1417-1426, 2012.