N-acetylglucosamine 6-O-sulfotransferase-1-deficient mice show better functional recovery after spinal cord injury

Journal of Neuroscience

Volumn 30, Issue 17, 2010, Pages 5937-5947

  Ito, Zenya ^a   Sakamoto, Kazuma ^a   Imagama, Shiro ^a   Matsuyama, Yukihiro ^a   Zhang, Haoqian ^a   Hirano, Kenichi ^a   Ando, Kei ^a   Yamashita, Toshihide ^b   Ishiguro, Naoki ^a   Kadomatsu, Kenji ^a,c  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHONDROITIN SULFATE; KERATAN SULFATE; N ACETYLGLUCOSAMINE; N ACETYLGLUCOSAMINE 6 O SULFOTRANSFERASE 1; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATLANTOOCCIPITAL JOINT; CELL ASSAY; CEREBELLUM; CLINICAL ASSESSMENT; CONTROLLED STUDY; CONTUSION; CONVALESCENCE; ELECTROSTIMULATION; FEMALE; FOOTFALL TEST; FOOTPRINT TEST; GENE EXPRESSION; IN VITRO STUDY; INFLAMMATORY CELL; LAMINECTOMY; LOCOMOTION; MOTOR PERFORMANCE; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NEUROMUSCULAR SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PYRAMIDAL TRACT; RAPHE MAGNUS NUCLEUS; SCORING SYSTEM; SPINAL CORD INJURY; THORACIC CAVITY; WILD TYPE;

ANIMALS; ANTIGENS, CD11B; AXONS; BRAIN; CELLS, CULTURED; CHONDROITIN SULFATES; FEMALE; KERATAN SULFATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NERVE REGENERATION; NEURAL PATHWAYS; NEURITES; NEUROMUSCULAR JUNCTION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; SULFOTRANSFERASES;

EID: 77951658160     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2570-09.2010     Document Type: Article

References (46)

1. Akama TO, Nishida K, Nakayama J, Watanabe H, Ozaki K, Nakamura T, Dota A, Kawasaki S, Inoue Y, Maeda N, Yamamoto S, Fujiwara T, Thonar EJ, Shimomura Y, Kinoshita S, Tanigami A, Fukuda MN (2000) Macular corneal dystrophy type I and type II are caused by distinct mutations in a new sulphotransferase gene. Nat Genet 26:237-241.
2. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, Mctigue DM, Popovich PG (2006) Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23:635-659.
3. Biffi A, De Palma M, Quattrini A, Del Carro U, Amadio S, Visigalli I, Sessa M, Fasano S, Brambilla R, Marchesini S, Bordignon C, Naldini L (2004) Correction of metachromatic leukodystrophy in the mouse model by transplantation of genetically modified hematopoietic stem cells. J Clin Invest 113:1108-1110. (Pubitemid 38544097)
4. Borisoff JF, Chan CC, Hiebert GW, Oschipok L, Robertson GS, Zamboni R, Steeves JD, Tetzlaff W (2003) Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates. Mol Cell Neurosci 2:405-416. (Pubitemid 36407602)
5. 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. (Pubitemid 34406764)
6. Bush TG, Puvanachandra N, Horner CH, Polito A, Ostenfeld T, Svendsen CN, Mucke L, Johnson MH, Sofroniew MV (1999) Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scarforming, reactive astrocytes in adult transgenic mice. Neuron 23:297-308. (Pubitemid 29315725)
7. Buss A, Pech K, Kakulas BA, Martin D, Schoenen J, Noth J, Brook GA (2007) Growth-modulating molecules are associated with invading Schwann cells and not astrocytes in human traumatic spinal cord injury Brain 130:940-953.
8. Condic ML, Lemons ML (2002) Extracellular matrix in spinal cord regeneration: getting beyond attraction and inhibition. Neuroreport 13:37-48.
9. De Winter F, Holtmaat AJ, Verhaagen J (2002) Neuropilin and class 3 semaphorins in nervous system regeneration. Adv Exp Med Biol 515:115-139. (Pubitemid 36324186)
10. Faulkner RJ, Julia E. Herrmann, Michael J. Woo, Keith E. Tansey, Ngan B. Doan, Michael V. Sofroniew (2004) Reactive Astrocytes Protect Tissue and Preserve Function after Spinal Cord Injury. J Neurosci 24:2143-2155.
11. Fawcett JW, Asher RA (1999) The glial scar and central nervous system repair. Brain Res Bull 49:377-391. (Pubitemid 29385505)
12. Filbin MT (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4:703-713.
13. Geisert EE Jr, Bidanset DJ (1993) A central nervous system keratan sulfate proteoglycan: localization to boundaries in the neonatal rat brain. Brain Res Dev Brain Res 75:163-173.
14. Grimpe B, Silver J (2004) 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)
15. Habuchi H, Habuchi O, Uchimura K, Kimata K, Muramatsu T (2006) Determination of substrate specificity of sulfotransferases and glycosyltransferases (proteoglycans). Methods Enzymol 416:225-243.
16. Hemmerich S, Bistrup A, Singer MS, van Zante A, Lee JK, Tsay D, Peters M, Carminati JL, Brennan TJ, Carver-Moore K, Leviten M, Fuentes ME, Ruddle NH, Rosen SD (2001) Sulfation of L-selectin ligands by an HEV-restricted sulfotransferase regulates lymphocyte homing to lymph nodes. Immunity 15:237-247.
17. 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.
18. Kaneko M, Kubo T, Hata K, Yamaguchi A, Yamashita T (2007) Repulsion of cerebellar granule neurons by chondroitin sulfate proteoglycans is mediated by MAPK pathway. Neurosci Lett 423:62-67.
19. Kawashima H, Petryniak B, Hiraoka N, Mitoma J, Huckaby V, Nakayama J, Uchimura K, Kadomatsu K, Muramatsu T, Lowe JB, Fukuda M (2005) N-acetylglucosamine-6-O-sulfotransferases 1 and 2 cooperatively control lymphocyte homing through L-selectin ligand biosynthesis in high endothelial venules. Nat Immunol 6:1096-1104.
20. Kim JE, Liu BP, Park JH, Strittmatter SM (2004) Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 44:439-451.
21. King CE, Canty AJ, Vickers JC (2001) Alterations in neurofilaments associated with reactive brain changes and axonal sprouting following acute physical injury to the rat neocortex. Neuropathol Appl Neurobiol 27: 115-126.
22. Kitayama K, Hayashida Y, Nishida K, Akama TO (2007) Enzymes responsible for synthesis of corneal keratan sulfate glycosaminoglycans. J Biol Chem 282:30085-30096.
23. Liesi P, Kauppila T (2002) Induction of type IV collagen and other basement-membrane-associated proteins after spinal cord injury of the adult rat may participate in formation of the glial scar. Exp Neurol 173:31-45.
24. 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.
25. McGee AW, Strittmatter SM (2003) The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci 26:193-198.
26. Menet V, M. Prieto, A. Privat, M. Giménez y Ribotta (2003) Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentin genes. Proc Natl Acad Sci U S A 100:8999-9004.
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. Mueller BK, Mack H, Teusch N (2005) Rho kinase, a promising drug target for neurological disorders. Nat Rev Drug Discov 4:387-398.
30. Neumann S, Woolf CJ (1999) Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 23:83-91.
31. Okada S, Nakamura M, Katoh H, Miyao T, Shimazaki T, Ishii K, Yamane J, Yoshimura A, Iwamoto Y, Toyama Y, Okano H (2006) Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat Med 12:829-834.
32. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi G, Vescovi AL, Martino G (2003) Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422:688-694.
33. Ruoslahti E (1996) Brain extracellular matrix. Glycobiology 6:489-492.
34. Schwab ME (2004) Nogo and axon regeneration. Curr Opin Neurobiol 14:118-124.
35. Schwab ME, Bartholdi D (1996) Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76:319-370.
36. Shiga T, Oppenheim RW (1991) Immunolocalization studies of putative guidance molecules used by axons and growth cones of intersegemental interneurons in the chick embryo spinal cord. J Comp Neurol 310:234-252.
37. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
38. Stichel CC, Hermanns S, Luhmann HJ, Lausberg F, Niermann H, D'Urso D, Servos G, Hartwig HG, Müller HW (1999) Inhibition of collagen IV deposition promotes regeneration of injured CNS axons. Eur J Neurosci 11:632-646.
39. Tetzlaff W, Bisby MA (1989) Neurofilament elongation into regenerating facial nerve axons. Neuroscience 29:659-666.
40. Uchimura K, Kadomatsu K, El-Fasakhany FM, Singer MS, Izawa M, Kannagi R, Takeda N, Rosen SD, Muramatsu T (2004) N-acetylglucosamine 6-O-sulfotransferase- 1 regulates expression of L-selectin ligands and lymphocyte homing. J Biol Chem 279:35001-35008.
41. Uchimura K, Gauguet JM, Singer MS, Tsay D, Kannagi R, Muramatsu T, von Andrian UH, Rosen SD (2005) A major class of L-selectin ligands is eliminated in mice deficient in two sulfotransferases expressed in high endothelial venules. Nat Immunol 6:1105-1113.
42. Ughrin YM, Chen ZJ, Levine JM (2003) Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci 23:175-186.
43. Weidner N, Grill RJ, Tuszynski MH (1999) Elimination of basal lamina and the collagen "scar" after spinal cord injury fails to augment corticospinal tract regeneration. Exp Neurol 160:40-50.
44. Widenfalk J, Lundströmer K, Jubran M, Brene S, Olson L (2001) Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J Neurosci 21:3457-3475.
45. Yin J, Sakamoto K, Zhang H, Ito Z, Imagama S, Kishida S, Natori T, Sawada M, Matsuyama Y, Kadomatsu K (2009) Transforming growth factor-beta1 upregulates keratan sulfate and chondroitin sulfate biosynthesis in microglia after brain injury. Brain Res 1263:10-22.
46. 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 biosynthesisandglial scar formation after brain injury. Glycobiology 16:702-710.