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

Volumn 109, Issue 23, 2012, Pages 9155-9160

  Hill, Justin J ^a   Jin, Kunlin ^a,b   Mao, Xiao Ou ^a   Xie, Lin ^a   Greenberg, David A ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Astrocyte; Astrogliosis; Glia

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHONDROITIN ABC LYASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYPICAN; MICROTUBULE ASSOCIATED PROTEIN 2; NEUROCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN NERVE CELL; CONTROLLED STUDY; EMBRYO; HISTOLOGY; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STROKE; TREATMENT OUTCOME; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHONDROITIN ABC LYASE; FIBROBLAST GROWTH FACTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYPICANS; IMMUNOHISTOCHEMISTRY; INFUSIONS, INTRA-ARTERIAL; MICROTUBULE-ASSOCIATED PROTEINS; NEURITES; NEUROCAN; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; STROKE;

RATTUS;

EID: 84861884705     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1205697109     Document Type: Article

References (48)

1. Fawcett JW, Asher RA (1999) The glial scar and central nervous system repair. Brain Res Bull 49:377-391. (Pubitemid 29385505)
2. Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7: 617-627. (Pubitemid 44106744)
3. Deguchi K, et al. (2005) Expression of neurocan after transient middle cerebral artery occlusion in adult rat brain. Brain Res 1037:194-199. (Pubitemid 40362396)
4. Rhodes KE, Fawcett JW (2004) Chondroitin sulphate proteoglycans: Preventing plasticity or protecting the CNS? J Anat 204:33-48. (Pubitemid 38128573)
5. Rolls A, Shechter R, Schwartz M (2009) The bright side of the glial scar in CNS repair. Nat Rev Neurosci 10:235-241.
6. Fitch MT, Silver J (1997) Activated macrophages and the blood-brain barrier: Inflammation after CNS injury leads to increases in putative inhibitory molecules. Exp Neurol 148:587-603. (Pubitemid 28068851)
7. Panickar KS, Norenberg MD (2005) Astrocytes in cerebral ischemic injury: Morphological and general considerations. Glia 50:287-298. (Pubitemid 40780835)
8. Properzi F, Asher RA, Fawcett JW (2003) Chondroitin sulphate proteoglycans in the central nervous system: Changes and synthesis after injury. Biochem Soc Trans 31: 335-336. (Pubitemid 36520669)
9. Coles CH, et al. (2011) Proteoglycan-specific molecular switch for RPTPó clustering and neuronal extension. Science 332:484-488.
10. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5: 146-156. (Pubitemid 38160289)
11. Galtrey CM, Fawcett JW (2007) The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Brain Res Rev 54: 1-18. (Pubitemid 46498163)
12. Nakamae T, et al. (2010) The effects of combining chondroitinase ABC and NEP1-40 on the corticospinal axon growth in organotypic co-cultures. Neurosci Lett 476: 14-17.
13. Moon LD, Asher RA, Rhodes KE, Fawcett JW (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)
14. Corvetti L, Rossi F (2005) Degradation of chondroitin sulfate proteoglycans induces sprouting of intact purkinje axons in the cerebellum of the adult rat. J Neurosci 25: 7150-7158. (Pubitemid 41113931)
15. Bradbury EJ, et al. (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640. (Pubitemid 34406764)
16. García-Alías G, Barkhuysen S, Buckle M, Fawcett JW (2009) Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12:1145-1151.
17. Nandini CD, et al. (2004) Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish. Neuritogenic and binding activities for growth factors and neurotrophic factors. J Biol Chem 279:50799-50809. (Pubitemid 40017818)
18. Properzi F, et al. (2008) Heparan sulphate proteoglycans in glia and in the normal and injured CNS: Expression of sulphotransferases and changes in sulphation. Eur J Neurosci 27:593-604. (Pubitemid 351239298)
19. Tisay KT, Key B (1999) The extracellular matrix modulates olfactory neurite outgrowth on ensheathing cells. J Neurosci 19:9890-9899. (Pubitemid 30226662)
20. Jain A, McKeon RJ, Brady-Kalnay SM, Bellamkonda RV (2011) Sustained delivery of activated Rho GTPases and BDNF promotes axon growth in CSPG-rich regions following spinal cord injury. PLoS ONE 6:e16135.
21. Kurihara D, Yamashita T (2012) Chondroitin sulfate proteoglycans downregulate spine formation in cortical neurons by targeting tropomyosin-related kinase B (TrkB). J Biol Chem 287:13822-13828.
22. Nurcombe V, Ford MD, Wildschut JA, Bartlett PF (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science 260: 103-106. (Pubitemid 23122755)
23. Su G, et al. (2006) Glypican-1 is frequently overexpressed in human gliomas and enhances FGF-2 signaling in glioma cells. Am J Pathol 168:2014-2026. (Pubitemid 43825320)
24. Jin K, Mao XO, Greenberg DA (2006) Vascular endothelial growth factor stimulates neurite outgrowth from cerebral cortical neurons via Rho kinase signaling. J Neurobiol 66:236-242. (Pubitemid 43202761)
25. Smit M, Leng J, Klemke RL (2003) Assay for neurite outgrowth quantification. Biotechniques 35:254-256. (Pubitemid 36994323)
26. Harris NG, Mironova YA, Hovda DA, Sutton RL (2010) Chondroitinase ABC enhances pericontusion axonal sprouting but does not confer robust improvements in behavioral recovery. J Neurotrauma 27:1971-1982.
27. Soleman S, Yip PK, Duricki DA, Moon LD (2012) Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats. Brain 135:1210-1223.
28. Hunanyan AS, et al. (2010) Role of chondroitin sulfate proteoglycans in axonal conduction in Mammalian spinal cord. J Neurosci 30:7761-7769.
29. Massey JM, et al. (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)
30. Sato Y, et al. (2008) Reduction of brain injury in neonatal hypoxic-ischemic rats by intracerebroventricular injection of neural stem/progenitor cells together with chondroitinase ABC. Reprod Sci 15:613-620. (Pubitemid 351875962)
31. McKeon RJ, Schreiber RC, Rudge JS, Silver J (1991) Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411.
32. Kirkham DL, et al. (2006) Neural stem cells from protein tyrosine phosphatase sigma knockout mice generate an altered neuronal phenotype in culture. BMC Neurosci 7: 50.
33. Shen Y, et al. (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592-596.
34. Meathrel K, Adamek T, Batt J, Rotin D, Doering LC (2002) Protein tyrosine phosphatase sigma-deficient mice show aberrant cytoarchitecture and structural abnormalities in the central nervous system. J Neurosci Res 70:24-35.
35. Xu J, et al. (2010) Effect of chondroitinase ABC on growth associated protein 43 and glial fibrillary acidic protein after spinal cord injury in rats. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 24:1212121-1212126.
36. Nudo RJ (2007) Postinfarct cortical plasticity and behavioral recovery. Stroke 38(2 Suppl):840-845.
37. Walicke P, Cowan WM, Ueno N, Baird A, Guillemin R (1986) Fibroblast growth factor promotes survival of dissociated hippocampal neurons and enhances neurite extension. Proc Natl Acad Sci USA 83:3012-3016. (Pubitemid 16041791)
38. Irving EA, et al. (2005) Identification of neuroprotective properties of anti-MAG antibody: A novel approach for the treatment of stroke? J Cereb Blood Flow Metab 25: 98-107. (Pubitemid 40096901)
39. Seymour AB, et al. (2005) Delayed treatment with monoclonal antibody IN-1 1 week after stroke results in recovery of function and corticorubral plasticity in adult rats. J Cereb Blood Flow Metab 25:1366-1375. (Pubitemid 41348738)
40. Suzuki T, et al. (2007) Chondroitinase ABC treatment enhances synaptogenesis between transplant and host neurons in model of retinal degeneration. Cell Transplant 16:493-503. (Pubitemid 351448285)
41. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Schut D, Fehlings MG (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.
42. Jin K, et al. (2010) Transplantation of human neural precursor cells in Matrigel scaffolding improves outcome from focal cerebral ischemia after delayed postischemic treatment in rats. J Cereb Blood Flow Metab 30:534-544.
43. Nawashiro H, Tasaki K, Ruetzler CA, Hallenbeck JM (1997) TNF-alpha pretreatment induces protective effects against focal cerebral ischemia in mice. J Cereb Blood Flow Metab 17:483-490. (Pubitemid 27250974)
44. Bacigaluppi M, et al. (2009) Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132: 2239-2251.
45. Metz GA, Whishaw IQ (2002) Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: A new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 115:169-179. (Pubitemid 34461965)
46. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39: 777-787. (Pubitemid 30103682)
47. Jin K, et al. (2001) Caspase-3 and the regulation of hypoxic neuronal death by vascular endothelial growth factor. Neuroscience 108:351-358. (Pubitemid 33152975)
48. Jin KL, Mao XO, Greenberg DA (2000) Vascular endothelial growth factor: Direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci USA 97:10242-10247.