Neural ECM in regeneration and rehabilitation

Progress in Brain Research

Volumn 214, Issue , 2014, Pages 179-192

  Kwok, Jessica C F ^a   Yang, Sujeong ^a   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Chondroitin sulfate proteoglycans; Perineuronal nets; Plasticity; Regeneration; Rehabilitation

Indexed keywords

PROTEOCHONDROITIN SULFATE;

ARTICLE; BRAIN INJURY; BRAIN TUMOR; CELL COMPOSITION; CELL REGENERATION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; DEGENERATIVE DISEASE; EXTRACELLULAR MATRIX; HUMAN; MEMORY; NERVE CELL; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECOGNITION; SOMATOSENSORY CORTEX; VISUAL CORTEX;

EID: 84922275011     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/B978-0-444-63486-3.00008-6     Document Type: Chapter

References (91)

1. Asher R.A., Morgenstern D.A., Fidler P.S., Adcock K.H., Oohira A., Braistead J.E., Levine J.M., Margolis R.U., Rogers J.H., Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 2000, 20:2427-2438.
2. Asher R.A., Morgenstern D.A., Shearer M.C., Adcock K.H., Pesheva P., Fawcett J.W. Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J. Neurosci. 2002, 22:2225-2236.
3. Baig S., Wilcock G.K., Love S. Loss of perineuronal net N-acetylgalactosamine in Alzheimer's disease. Acta Neuropathol. 2005, 110:393-401.
4. Bandtlow C.E., Zimmermann D.R. Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 2000, 80:1267-1290.
5. Bartko S.J., Winters B.D., Cowell R.A., Saksida L.M., Bussey T.J. Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations. J. Neurosci. 2007, 27:2548-2559.
6. Bellail A.C., Hunter S.B., Brat D.J., Tan C., van Meir E.G. Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int. J. Biochem. Cell Biol. 2004, 36:1046-1069.
7. Berardi N., Pizzorusso T., Ratto G.M., Maffei L. Molecular basis of plasticity in the visual cortex. Trends Neurosci. 2003, 26:369-378.
8. Berzin T.M., Zipser B.D., Rafii M.S., Kuo-Leblanc V., Yancopoulos G.D., Glass D.J., Fallon J.R., Stopa E.G. Agrin and microvascular damage in Alzheimer's disease. Neurobiol. Aging 2000, 21:349-355.
9. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
10. Bruckner G., Hausen D., Hartig W., Drlicek M., Arendt T., Brauer K. Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer's disease. Neuroscience 1999, 92:791-805.
11. Cabungcal J.H., Steullet P., Morishita H., Kraftsik R., Cuenod M., Hensch T.K., Do K.Q. Perineuronal nets protect fast-spiking interneurons against oxidative stress. PNAS 2013, 110:9130-9135.
12. Carmichael S.T., Archibeque I., Luke L., Nolan T., Momiy J., Li S. Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp. Neurol. 2005, 193:291-311.
13. Carulli D., Rhodes K.E., Fawcett J.W. Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum. J. Comp. Neurol. 2007, 501:83-94.
14. Carulli D., Pizzorusso T., Kwok J.C., Putignano E., Poli A., Forostyak S., Andrews M.R., Deepa S.S., Glant T.T., Fawcett J.W. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 2010, 133:2331-2347.
15. Castillo G.M., Ngo C., Cummings J., Wight T.N., Snow A.D. Perlecan binds to the beta-amyloid proteins (A beta) of Alzheimer's disease, accelerates A beta fibril formation, and maintains A beta fibril stability. J. Neurochem. 1997, 69:2452-2465.
16. Cotman S.L., Halfter W., Cole G.J. Agrin binds to beta-amyloid (Abeta), accelerates abeta fibril formation, and is localized to Abeta deposits in Alzheimer's disease brain. Mol. Cell. Neurosci. 2000, 15:183-198.
17. Crespo D., Asher R.A., Lin R., Rhodes K.E., Fawcett J.W. How does chondroitinase promote functional recovery in the damaged CNS?. Exp. Neurol. 2007, 206:159-171.
18. Deepa S.S., Carulli D., Galtrey C., Rhodes K., Fukuda J., Mikami T., Sugahara K., Fawcett J.W. Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J. Biol. Chem. 2006, 281:17789-17800.
19. Delpech B., Maingonnat C., Girard N., Chauzy C., Maunoury R., Olivier A., Tayot J., Creissard P. Hyaluronan and hyaluronectin in the extracellular matrix of human brain tumour stroma. Eur. J. Cancer 1993, 29A:1012-1017.
20. Dewitt D.A., Silver J., Canning D.R., Perry G. Chondroitin sulphate proteoglycans are associated with the lesions of Alzheimer's disease. Exp. Neurol. 1993, 121:149-152.
21. Dewitt D.A., Richey P.L., Praprotnik D., Silver J., Perry G. Chondroitin sulphate proteoglycans are a common component of neuronal inclusions and astrocytic reaction in neurodegenerative diseases. Brain Res. 1994, 656:205-209.
22. Donahue J.E., Berzin T.M., Rafii M.S., Glass D.J., Yancopoulos G.D., Fallon J.R., Stopa E.G. Agrin in Alzheimer's disease: altered solubility and abnormal distribution within microvasculature and brain parenchyma. PNAS 1999, 96:6468-6472.
23. Erzurumlu R.S., Gaspar P. Development and critical period plasticity of the barrel cortex. Eur. J. Neurosci. 2012, 35:1540-1553.
24. Fagiolini M., Pizzorusso T., Berardi N., Domenici L., Maffei L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 1994, 34:709-720.
25. Fawcett J.W. Molecular control of brain plasticity and repair. Prog. Brain Res. 2009, 175:501-509.
26. Galtrey C.M., Fawcett J.W. The role of chondroitin sulphate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res. Rev. 2007, 54:1-18.
27. Galtrey C.M., Kwok J.C., Carulli D., Rhodes K.E., Fawcett J.W. Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord. Eur. J. Neurosci. 2008, 27:1373-1390.
28. Garcia-Alias G., Barkhuysen S., Buckle M., Fawcett J.W. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat. Neurosci. 2009, 12:1145-1151.
29. Giamanco K.A., Morawski M., Matthews R.T. Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience 2010, 170:1314-1327.
30. Gogolla N., Caroni P., Luthi A., Herry C. Perineuronal nets protect fear memories from erasure. Science 2009, 325:1258-1261.
31. Golembieski W.A., Ge S., Nelson K., Mikkelsen T., Rempel S.A. Increased SPARC expression promotes U87 glioblastoma invasion in vitro. Int. J. Dev. Neurosci. 1999, 17:463-472.
32. Haddock G., Cross A.K., Allan S., Sharrack B., Callaghan J., Bunning R.A., Buttle D.J., Woodroofe M.N. Brevican and phosphacan expression and localization following transient middle cerebral artery occlusion in the rat. Biochem. Soc. Trans. 2007, 35:692-694.
33. Happel M.F., Niekisch H., Castiblanco Rivera L.L., Ohl F.W., Deliano M., Frischknecht R. Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex. PNAS 2014, 111:2800-2805.
34. Hartig W., Derouiche A., Welt K., Brauer K., Grosche J., Mader M., Reichenbach A., Bruckner G. Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res. 1999, 842:15-29.
35. Hartig W., Klein C., Brauer K., Schuppel K.F., Arendt T., Bigl V., Bruckner G. Hyperphosphorylated protein tau is restricted to neurons devoid of perineuronal nets in the cortex of aged bison. Neurobiol. Aging 2001, 22:25-33.
36. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005, 6:877-888.
37. Hobohm C., Gunther A., Grosche J., Rossner S., Schneider D., Bruckner G. Decomposition and long-lasting downregulation of extracellular matrix in perineuronal nets induced by focal cerebral ischemia in rats. J. Neurosci. Res. 2005, 80:539-548.
38. Iozzo R.V. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 1998, 67:609-652.
39. Jones L.L., Yamaguchi Y., Stallcup W.B., Tuszynski M.H. NG2 is a major chondroitin sulphate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 2002, 22:2792-2803.
40. Jones L.L., Margolis R.U., Tuszynski M.H. The chondroitin sulphate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp. Neurol. 2003, 182:399-411.
41. Karetko-Sysa M., Skangiel-Kramska J., Nowicka D. Disturbance of perineuronal nets in the perilesional area after photothrombosis is not associated with neuronal death. Exp. Neurol. 2011, 231:113-126.
42. Kim J.H., McNally G.P., Richardson R. Recovery of fear memories in rats: role of gamma-amino butyric acid (GABA) in infantile amnesia. Behav. Neurosci. 2006, 120:40-48.
43. Kobayashi K., Emson P.C., Mountjoy C.Q. Vicia villosa lectin-positive neurones in human cerebral cortex. Loss in Alzheimer-type dementia. Brain Res. 1989, 498:170-174.
44. Köppe G., Brückner G., Härtig W., Delpech B., Bigl V. Characterization of proteoglycan-containing perineuronal nets by enzymatic treatments of rat brain sections. Histochem. J. 1997, 29:11-20.
45. Kwok J.C., Afshari F., Garcia-Alias G., Fawcett J.W. Proteoglycans in the central nervous system: plasticity, regeneration and their stimulation with chondroitinase ABC. Restor. Neurol. Neurosci. 2008, 26:131-145.
46. Kwok J.C.F., Carulli D., Fawcett J.W. In vitro modeling of perineuronal nets: the role of cartilage link protein and hyaluronan synthase in its formation and integrity. J. Neurochem. 2010, 114:1447-1459.
47. Kwok J.C., Dick D., Wang D., Fawcett J.W. Extracellular matrix and perineuronal nets in CNS repair. Dev. Neurobiol. 2011, 71:1073-1089.
48. Kwok J.C., Tan C.L., Wang D., Heller J., Fawcett J.W. Chondroitin sulphates in axon regeneration and plasticity. Trends Glycosci. Glyc. 2011, 133:201-211.
49. Kwok J.C., Warren P., Fawcett J.W. Chondroitin sulphate: a key molecule in the brain matrix. Int. J. Biochem. Cell Biol. 2012, 44:582-586.
50. Lander C., Kind P., Maleski M., Hockfield S. A family of activity-dependent neuronal cell-surface chondroitin sulphate proteoglycans in cat visual cortex. J. Neurosci. 1997, 17:1928-1939.
51. Li S., Overman J.J., Katsman D., Kozlov S.V., Donnelly C.J., Twiss J.L., Giger R.J., Coppola G., Geschwind D.H., Carmichael S.T. An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke. Nat. Neurosci. 2010, 13:1496-1504.
52. Madinier A., Quattromani M.J., Sjolund C., Ruscher K., Wieloch T. Enriched housing enhances recovery of limb placement ability and reduces aggrecan-containing perineuronal nets in the rat somatosensory cortex after experimental stroke. PLoS One 2014, 9:e93121.
53. Maresh G.A., Erezyilmaz D., Murry C.E., Nochlin D., Snow A.D. Detection and quantitation of perlecan mRNA levels in Alzheimer's disease and normal aged hippocampus by competitive reverse transcription-polymerase chain reaction. J. Neurochem. 1996, 67:1132-1144.
54. Matthews R.T., Kelly G.M., Zerillo C.A., Gray G., Tiemeyer M., Hockfield S. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 2002, 22:7536-7547.
55. McRae P.A., Rocco M.M., Kelly G., Brumberg J.C., Matthews R.T. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J. Neurosci. 2007, 27:5405-5413.
56. 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. 2001, 4:465-466.
57. Morawski M., Bruckner M.K., Riederer P., Bruckner G., Arendt T. Perineuronal nets potentially protect against oxidative stress. Exp. Neurol. 2004, 188:309-315.
58. Morawski M., Bruckner G., Jager C., Seeger G., Arendt T. Neurons associated with aggrecan-based perineuronal nets are protected against tau pathology in subcortical regions in Alzheimer's disease. Neuroscience 2010, 169:1347-1363.
59. Morawski M., Pavlica S., Seeger G., Grosche J., Kouznetsova E., Schliebs R., Bruckner G., Arendt T. Perineuronal nets are largely unaffected in Alzheimer model Tg2576 mice. Neurobiol. Aging 2010, 31:1254-1256.
60. Morawski M., Bruckner G., Jager C., Seeger G., Matthews R.T., Arendt T. Involvement of perineuronal and perisynaptic extracellular matrix in Alzheimer's disease neuropathology. Brain Pathol. 2012, 22:547-561.
61. Morgenstern D.A., Asher R.A., Fawcett J.W. Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 2002, 137:313-332.
62. Mumby D.G., Pinel J.P. Rhinal cortex lesions and object recognition in rats. Behav. Neurosci. 1994, 108:11-18.
63. Nakamura M., Nakano K., Morita S., Nakashima T., Oohira A., Miyata S. Expression of chondroitin sulphate proteoglycans in barrel field of mouse and rat somatosensory cortex. Brain Res. 2009, 1252:117-129.
64. Novak U., Kaye A.H. Extracellular matrix and the brain: components and function. J. Clin. Neurosci. 2000, 7:280-290.
65. Perry G., Richey P., Siedlak S.L., Galloway P., Kawai M., Cras P. Basic fibroblast growth factor binds to filamentous inclusions of neurodegenerative diseases. Brain Res. 1992, 579:350-352.
66. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298:1248-1251.
67. Properzi F., Asher R.A., Fawcett J.W. Chondroitin sulphate proteoglycans in the central nervous system: changes and synthesis after injury. Biochem. Soc. Trans. 2003, 31:335-336.
68. Pyka M., Busse C., Seidenbecher C., Gundelfinger E.D., Faissner A. Astrocytes are crucial for survival and maturation of embryonic hippocampal neurons in a neuron-glia cell-insert coculture assay. Synapse 2011, 65:41-53.
69. Quirk G.J., Pare D., Richardson R., Herry C., Monfils M.H., Schiller D., Vicentic A. Erasing fear memories with extinction training. J. Neurosci. 2010, 30:14993-14997.
70. Reilly C.E. Crucial role of heparan sulphate proteoglycan (agrin) in beta-amyloid formation in Alzheimer's disease. J. Neurol. 2000, 247:663-664.
71. Rempel S.A., Golembieski W.A., Ge S., Lemke N., Elisevich K., Mikkelsen T., Gutierrez J.A. SPARC: a signal of astrocytic neoplastic transformation and reactive response in human primary and xenograft gliomas. J. Neuropathol. Exp. Neurol. 1998, 57:1112-1121.
72. Rempel S.A., Ge S., Gutierrez J.A. SPARC: a potential diagnostic marker of invasive meningiomas. Clin. Cancer Res. 1999, 5:237-241.
73. Rempel S.A., Golembieski W.A., Fisher J.L., Maile M., Nakeff A. SPARC modulates cell growth, attachment and migration of U87 glioma cells on brain extracellular matrix proteins. J. Neuro-Oncol. 2001, 53:149-160.
74. Rolls A., Shechter R., Schwartz M. The bright side of the glial scar in CNS repair. Nat. Rev. Neurosci. 2009, 10:235-241.
75. Romberg C., Yang S., Melani R., Andrews M.R., Horner A.E., Spillantini M.G., Bussey T.J., Fawcett J.W., Pizzorusso T., Saksida L.M. Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex. J. Neurosci. 2013, 33:7057-7065.
76. Rosenmann H., Meiner Z., Kahana E., Aladjem Z., Friedman G., Ben-Yehuda A., Grenader T., Wertman E., Abramsky O. An association study of a polymorphism in the heparan sulphate proteoglycan gene (perlecan, HSPG2) and Alzheimer's disease. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2004, 128B:123-125.
77. Ruoslahti E. Brain extracellular matrix. Glycobiology 1996, 6:489-492.
78. Schultz C., Lemke N., Ge S., Golembieski W.A., Rempel S.A. Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res. 2002, 62:6270-6277.
79. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
80. Snow A.D., Mar H., Nochlin D., Kimata K., Kato M., Suzuki S., Hassell J., Wight T.N. The presence of heparan sulphate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease. Am. J. Pathol. 1988, 133:456-463.
81. Snow A.D., Wight T.N., Nochlin D., Koike Y., Kimata K., DeArmond S.J., Prusiner S.B. Immunolocalization of heparan sulphate proteoglycans to the prion protein amyloid plaques of Gerstmann-Straussler syndrome, Creutzfeldt-Jakob disease and scrapie. Lab. Invest. 1990, 63:601-611.
82. Sugiyama S., Di Nardo A.A., Aizawa S., Matsuo I., Volovitch M., Prochiantz A., Hensch T.K. Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 2008, 134:508-520.
83. Suttkus A., Rohn S., Jager C., Arendt T., Morawski M. Neuroprotection against iron-induced cell death by perineuronal nets - an in vivo analysis of oxidative stress. Am. J. Neurodegener. Dis. 2012, 1:122-129.
84. Suttkus A., Rohn S., Weigel S., Glockner P., Arendt T., Morawski M. Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress. Cell Death Dis. 2014, 5:e1119.
85. Van Gool D., David G., Lammens M., Baro F., Dom R. Heparan sulphate expression patterns in the amyloid deposits of patients with Alzheimer's and Lewy body type dementia. Dementia 1993, 4:308-314.
86. van Horssen J., Wilhelmus M.M., Heljasvaara R., Pihlajaniemi T., Wesseling P., de Waal R.M., Verbeek M.M. Collagen XVIII: a novel heparan sulphate proteoglycan associated with vascular amyloid depositions and senile plaques in Alzheimer's disease brains. Brain Pathol. 2002, 12:456-462.
87. Verbeek M.M., Otte-Holler I., van den Born J., van den Heuvel L.P., David G., Wesseling P., de Waal R.M. Agrin is a major heparan sulphate proteoglycan accumulating in Alzheimer's disease brain. Am. J. Pathol. 1999, 155:2115-2125.
88. Vorobyov V., Kwok J.C., Fawcett J.W., Sengpiel F. Effects of digesting chondroitin sulphate proteoglycans on plasticity in cat primary visual cortex. J. Neurosci. 2013, 33:234-243.
89. Wang D., Ichiyama R.M., Zhao R., Andrews M.R., Fawcett J.W. Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J. Neurosci. 2011, 31:9332-9344.
90. Winters B.D., Forwood S.E., Cowell R.A., Saksida L.M., Bussey T.J. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J. Neurosci. 2004, 24:5901-5908.
91. Zimmermann D.R., Dours-Zimmermann M.T. Extracellular matrix of the central nervous system: from neglect to challenge. Histochem. Cell Biol. 2008, 130:635-653.