Keratan sulfate restricts neural plasticity after spinal cord injury

Journal of Neuroscience

Volumn 31, Issue 47, 2011, Pages 17091-17102

  Imagama, Shiro ^a   Sakamoto, Kazuma ^a   Tauchi, Ryoji ^a   Shinjo, Ryuichi ^a   Ohgomori, Tomohiro ^a   Ito, Zenya ^a   Zhang, Haoqian ^a,b   Nishida, Yoshihiro ^a   Asami, Nagamasa ^c   Takeshita, Sawako ^c   Sugiura, Nobuo ^d   Watanabe, Hideto ^d   Yamashita, Toshihide ^e   Ishiguro, Naoki ^a   Matsuyama, Yukihiro ^a,f   Kadomatsu, Kenji ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SEIKAGAKU CORPORATION   (Japan)

^d AICHI MEDICAL UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CHONDROITIN ABC LYASE; CHONDROITIN SULFATE; CORE PROTEIN; KERATAN SULFATE; KERATANASE II; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ALKYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME DENATURATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL PLASTICITY; NERVE FIBER REGENERATION; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR FUNCTION; SPINAL CORD INJURY;

ACETYLGLUCOSAMINIDASE; ANIMALS; FEMALE; KERATAN SULFATE; NERVE REGENERATION; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; THORACIC VERTEBRAE;

EID: 81855193754     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5120-10.2011     Document Type: Article

References (47)

1. Asher RA, Scheibe RJ, Keiser HD, Bignami A (1995) On the existence of a cartilage-like proteoglycan and link proteins in the central nervous system. Glia 13:294-308
2. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21
3. Berardi N, Pizzorusso T, Maffei L (2004) Extracellular matrix and visual cortical plasticity: freeing the synapse. Neuron 44:905-908
4. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640
5. Butler CD, Schnetz SA, Yu EY, Davis JB, Temple K, Silver J, Malouf AT (2004) Keratan sulfate proteoglycan phosphacan regulates mossy fiber outgrowth and regeneration. J Neurosci 24:462-473
6. Celio MR, Blümcke I (1994) Perineuronal nets-a specialized form of extracellular matrix in the adult nervous system. Brain Res Brain Res Rev 19:128-145
7. Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21:510-515
8. Cole GJ, McCabe CF (1991) Identification of a developmentally regulated keratan sulfate proteoglycan that inhibits cell adhesion and neurite outgrowth. Neuron 7:1007-1018
9. Coles CH, Shen Y, Tenney AP, Siebold C, Sutton GC, Lu W, Gallagher JT, Jones EY, Flanagan JG, Aricescu AR (2011) Proteoglycan-specific molecular switch for RPTPσ clustering and neuronal extension. Science 332:484-488
10. Davies SJ, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822
11. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12:897-904
12. Funderburgh JL (2000) Keratan sulfate: structure, biosynthesis, and function. Glycobiology 10:951-958
13. Funderburgh JL (2002) Keratan sulfate biosynthesis. IUBMB Life 54:187-194
14. 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
15. Geisert EE Jr, Bidanset DJ, Del Mar N, Robson JA (1996) Up-regulation of a keratan sulfate proteoglycan following cortical injury in neonatal rats. Int J Dev Neurosci 14:257-267
16. Gogolla N, Caroni P, Lüthi A, Herry C (2009) Perineuronal nets protect fear memories from erasure. Science 325:1258-1261
17. Grimpe B, 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
18. Hutchinson KJ, Gómez-Pinilla F, Crowe MJ, Ying Z, Basso DM (2004) Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats. Brain 127:1403-1414
19. Ito Z, Sakamoto K, Imagama S, Matsuyama Y, Zhang H, Hirano K, Ando K, Yamashita T, Ishiguro N, Kadomatsu K (2010) N-acetylglucosamine 6-O-sulfotransferase-1-deficient mice show better functional recovery after spinal cord injury. J Neurosci 30:5937-5947
20. John N, Krügel H, Frischknecht R, Smalla KH, Schultz C, Kreutz MR, Gundelfinger ED, Seidenbecher CI (2006) Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Mol Cell Neurosci 31:774-784
21. Johnson WE, Caterson B, Eisenstein SM, Hynds DL, Snow DM, Roberts S (2002) Human intervertebral disc aggrecan inhibits nerve growth in vitro. Arthritis Rheum 46:2658-2664
22. Jones LL, Tuszynski MH (2002) Spinal cord injury elicits expression of keratan sulfate proteoglycans by macrophages, reactive microglia, and oligodendrocyte progenitors. J Neurosci 22:4611-4624
23. Kiani C, Chen L, Wu YJ, Yee AJ, Yang BB (2002) Structure and function of aggrecan. Cell Res 12:19-32
24. Krautstrunk M, Scholtes F, Martin D, Schoenen J, Schmitt AB, Plate D, Nacimiento W, Noth J, Brook GA (2002) Increased expression of the putative axon growth-repulsive extracellular matrix molecule, keratan sulphate proteoglycan, following traumatic injury of the adult rat spinal cord. Acta Neuropathol 104:592-600
25. Margolis RK, Margolis RU (1993) Nervous tissue proteoglycans. Experientia 49:429-446
26. Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, Onifer SM (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
27. 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
28. Moon LD, Asher RA, Rhodes KE, Fawcett JW (2002) Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience 109:101-117
29. Oray S, Majewska A, Sur M (2004) Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44:1021-1030
30. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248-1251
31. Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L (2006) Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci U S A 103:8517-8522
32. Powell EM, Fawcett JW, Geller HM (1997) Proteoglycans provide neurite guidance at an astrocyte boundary. Mol Cell Neurosci 10:27-42
33. Properzi F, Carulli D, Asher RA, Muir E, Camargo LM, van Kuppevelt TH, ten Dam GB, Furukawa Y, Mikami T, Sugahara K, Toida T, Geller HM, Fawcett JW (2005) Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axongrowth inhibitory glia. Eur J Neurosci 21:378-390
34. Pumphrey CY, Theus AM, Li S, Parrish RS, Sanderson RD (2002) Neoglycans, carbodiimide-modified glycosaminoglycans: a new class of anticancer agents that inhibit cancer cell proliferation and induce apoptosis. Cancer Res 62:3722-3728
35. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Hadani M, Schwartz M (1998) Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4:814-821
36. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG (2009) PTPσ is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592-596
37. Shinmei M, Miyauchi S, Machida A, Miyazaki K (1992) Quantitation of chondroitin 4-sulfate and chondroitin 6-sulfate in pathologic joint fluid. Arthritis Rheum 35:1304-1308
38. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156
39. Sivasankaran R, Pei J, Wang KC, Zhang YP, Shields CB, Xu XM, He Z (2004) PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci 7:261-268
40. Snow DM, Steindler DA, Silver J (1990a) Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in the development of an axon barrier. Dev Biol 138:359-376
41. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J (1990b) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111-130
42. Sutter M, Deletis V, Dvorak J, Eggspuehler A, Grob D, Macdonald D, Mueller A, Sala F, Tamaki T (2007) Current opinions and recommendations on multimodal intraoperative monitoring during spine surgeries. Eur Spine J 16 [Suppl 2]:S232-S237.
43. Takahashi-Iwanaga H, Murakami T, Abe K (1998) Three-dimensional microanatomy of perineuronal proteoglycan nets enveloping motor neurons in the rat spinal cord. J Neurocytol 27:817-827
44. Tamaki T, Kubota S (2007) History of the development of intraoperative spinal cord monitoring. Eur Spine J 16 [Suppl 2]:S140-S146.
45. Tom VJ, Steinmetz MP, Miller JH, Doller CM, Silver J (2004) Studies on the development and behavior of the dystrophic growth cone, the hallmark of regeneration failure, in an in vitro model of the glial scar and after spinal cord injury. J Neurosci 24:6531-6539
46. Yamagishi K, Suzuki K, Imai K, Mochizuki H, Morikawa K, Kyogashima M, Kimata K, Watanabe H (2003) Purification, characterization, and molecular cloning of a novel keratan sulfate hydrolase, endo-β-Nacetylglucosaminidase, from Bacillus circulans. J Biol Chem 278: 25766-25772
47. Zhang H, Muramatsu T, Murase A, Yuasa S, Uchimura K, Kadomatsu K (2006) N-Acetylglucosamine 6-O-sulfotransferase-1 is required for brain keratan sulfate biosynthesis and glial scar formation after brain injury. Glycobiology 16:702-710.