An in vitro model of the inhibition of axon growth in the lesion scar formed after central nervous system injury

Molecular and Cellular Neuroscience

Volumn 43, Issue 2, 2010, Pages 177-187

  Kimura Kuroda, Junko ^a   Teng, Xichuan ^a,b   Komuta, Yukari ^a   Yoshioka, Nozomu ^a   Sango, Kazunori ^a   Kawamura, Koki ^a   Raisman, Geoffrey ^c   Kawano, Hitoshi ^a  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b EASTERN LIAONING UNIVERSITY   (China)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Astrocyte; Chondroitin sulfate; Fibroblast; Fibrotic scar; Neurite outgrowth; TGF

Indexed keywords

CHONDROITIN SULFATE; COLLAGEN TYPE 4; EPHRIN B2; EPHRIN RECEPTOR B2; LAMININ; NG2 PROTEOGLYCAN; PROTEOGLYCAN; SEMAPHORIN 3A; TENASCIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIOACCUMULATION; CELL ADHESION; CELL AGGREGATION; CELL PROLIFERATION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM DISEASE; CEREBELLUM CORTEX; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE TECHNIQUE; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROSIS; GROWTH INHIBITION; IN VITRO STUDY; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NEURITE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCAR FORMATION; TRAUMATIC BRAIN INJURY; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANTIGENS; ANTIGENS, CD31; ASTROCYTES; AXONS; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CELLS, CULTURED; CEREBELLUM; CEREBRAL CORTEX; CHONDROITIN SULFATES; COCULTURE TECHNIQUES; FIBROBLASTS; FIBRONECTINS; GENE EXPRESSION REGULATION; MENINGES; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURITES; NEURONS; PROTEOGLYCANS; PYRAZOLES; PYRROLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPHB2; SEMAPHORIN-3A; TENASCIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 73049106964     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.10.008     Document Type: Article

References (64)

1. Abnet K., Fawcett J.W., and Dunnett S.B. Interactions between meningeal cells and astrocytes in vivo and in vitro. Brain Res. Dev. Brain Res. 59 (1991) 187-196
2. Alonso G. NG2 proteoglycan-expressing cells of the adult rat brain: possible involvement in the formation of glial scar astrocytes following stab wound. Glia 49 (2005) 318-338
3. Ard M.D., Bunge M.B., Wood P.M., Schachner M., and Bunge R.P. Retinal neurite growth on astrocytes is not modified by extracellular matrix, anti-L1 antibody, or oligodendrocytes. Glia 4 (1991) 70-82
4. 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., and Fawcett J.W. Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J. Neurosci. 20 (2000) 2427-2438
5. Asher R.A., Morgenstern D.A., Moon L.D., and Fawcett J.W. Chondroitin sulphate proteoglycans: inhibitory components of the glial scar. Prog. Brain Res. 132 (2001) 611-619
6. Bassols A., and Massagué J. Transforming growth factor beta regulates the expression and structure of extracellular matrix chondroitin/dermatan sulfate proteoglycans. J. Biol. Chem. 263 (1988) 3039-3045
7. Berry M., Maxwell W.L., Logan A., Mathewson A., McConnell P., Ashhurst D.E., and Thomas G.H. Deposition of scar tissue in the central nervous system. Acta. Neurochir. Suppl. (Wien). 32 (1983) 31-53
8. Border W.A., Okuda S., Languino L.R., and Ruoslahti E. Transforming growth factor-beta regulates production of proteoglycans by mesangial cells. Kidney. Int. 37 (1990) 689-695
9. Bundesen L.Q., Scheel T.A., Bregman B.S., and Kromer L.F. Ephrin-B2 and EphB2 regulation of astrocyte-meningeal fibroblast interactions in response to spinal cord lesions in adult rats. J. Neurosci. 23 (2003) 7789-7800
10. Cutroneo K.R. TGF-beta-induced fibrosis and SMAD signaling: oligo decoys as natural therapeutics for inhibition of tissue fibrosis and scarring. Wound Repair Regen. 15 Suppl. 1 (2007) S54-60
11. Davies J.E., Tang X., Denning J.W., Archibald S.J., and Davies S.J. Decorin suppresses neurocan, brevican, phosphacan and NG2 expression and promotes axon growth across adult rat spinal cord injuries. Eur. J. Neurosci. 19 (2004) 1226-1242
12. Fallon J.R. Preferential outgrowth of central nervous system neurites on astrocytes and Schwann cells as compared with nonglial cells in vitro. J. Cell. Biol. 100 (1985) 198-207
13. Haas C.A., Rauch U., Thon N., Merten T., and Deller T. Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J. Neurosci. 19 (1999) 9953-9963
14. Hirsch S., and Bahr M. Growth promoting and inhibitory effects of glial cells in the mammalian nervous system. Adv. Exp. Med. Biol. 468 (1999) 199-205
15. Homma A., Li H.P., Hayashi K., Kawano Y., and Kawano H. Differential response of arcuate proopiomelanocortin- and neuropeptide Y-containing neurons to the lesion produced by gold thioglucose administration. J. Comp. Neurol. 499 (2006) 120-131
16. Ignotz R.A., and Massagué J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261 (1986) 4337-4345
17. Jones L.L., Yamaguchi Y., Stallcup W.B., and Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 22 (2002) 2792-2803
18. Kähäri V.M., Larjava H., and Uitto J. Differential regulation of extracellular matrix proteoglycan (PG) gene expression. Transforming growth factor-beta 1 up-regulates biglycan (PGI), and versican (large fibroblast PG) but down-regulates decorin (PGII) mRNA levels in human fibroblasts in culture. J. Biol. Chem. 266 (1991) 10608-10615
19. Kawano H., Li H.P., Sango K., Kawamura K., and Raisman G. Inhibition of collagen synthesis overrides the age-related failure of regeneration of nigrostriatal dopaminergic axons. J. Neurosci. Res. 80 (2005) 191-202
20. Kawano H., Li H.P., and Kawamura K. Central nervous system injury and chondroitin sulfate proteoglycans. In: Maeda N. (Ed). Neural Proteoglycans (2007), Research Signpost, Kerala, India 216-228
21. Kisseleva T., and Brenner D.A. Mechanisms of fibrogenesis. Exp. Biol. Med. (Maywood) 233 (2008) 109-122
22. Klapka N., and Müller H.W. Collagen matrix in spinal cord injury. J. Neurotrauma. 23 (2006) 422-435
23. Klapka N., Hermanns S., Straten G., Masanneck C., Duis S., Hamers F.P., Muller D., Zuschratter W., and Muller H.W. Suppression of fibrous scarring in spinal cord injury of rat promotes long-distance regeneration of corticospinal tract axons, rescue of primary motoneurons in somatosensory cortex and significant functional recovery. Eur. J. Neurosci. 22 (2005) 3047-3058
24. Komuta, Y., Teng, X., Yanagisawa, H., Sango, K., Kawamura, K., Kawano, H., in press. Expression of transforming growth factor-β receptors in meningeal fibroblasts of the injured mouse brain. Cell Mol Neurobiol.
25. Lagord C., Berry M., and Logan A. Expression of TGFbeta2 but not TGFbeta1 correlates with the deposition of scar tissue in the lesioned spinal cord. Mol. Cell. Neurosci. 20 (2002) 69-92
26. Lastres P., Almendro N., Bellon T., Lopez-Guerrero J.A., Eritja R., and Bernabeu C. Functional regulation of platelet/endothelial cell adhesion molecule-1 by TGF-beta 1 in promonocytic U-937 cells. J. Immunol. 153 (1994) 4206-4218
27. Laywell E.D., Dorries U., Bartsch U., Faissner A., Schachner M., and Steindler D.A. Enhanced expression of the developmentally regulated extracellular matrix molecule tenascin following adult brain injury. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 2634-2638
28. Le R., and Esquenazi S. Astrocytes mediate cerebral cortical neuronal axon and dendrite growth, in part, by release of fibroblast growth factor. Neurol. Res. 24 (2002) 81-92
29. Li H.P., Homma A., Sango K., Kawamura K., Raisman G., and Kawano H. Regeneration of nigrostriatal dopaminergic axons by degradation of chondroitin sulfate is accompanied by elimination of the fibrotic scar and glia limitans in the lesion site. J. Neurosci. Res. 85 (2007) 536-547
30. Lindholm D., Castren E., Kiefer R., Zafra F., and Thoenen H. Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J. Cell. Biol. 117 (1992) 395-400
31. Logan A., Berry M., Gonzalez A.M., Frautschy S.A., Sporn M.B., and Baird A. Effects of transforming growth factor beta 1 on scar production in the injured central nervous system of the rat. Eur. J. Neurosci. 6 (1994) 355-363
32. Logan A., Green J., Hunter A., Jackson R., and Berry M. Inhibition of glial scarring in the injured rat brain by a recombinant human monoclonal antibody to transforming growth factor-beta2. Eur. J. Neurosci. 11 (1999) 2367-2374
33. Maniscalco W.M., and Campbell M.H. Transforming growth factor-beta induces a chondroitin sulfate/dermatan sulfate proteoglycan in alveolar type II cells. Am. J. Physiol. 266 (1994) L672-680
34. Matsui F., and Oohira A. Proteoglycans and injury of the central nervous system. Congenit. Anom. (Kyoto) 44 (2004) 181-188
35. McKeon R.J., Schreiber R.C., Rudge J.S., and Silver J. 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 (1991) 3398-3411
36. McKeon R.J., Jurynec M.J., and Buck C.R. The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J. Neurosci. 19 (1999) 10778-10788
37. Merrill J.E., and Benveniste E.N. Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci. 19 (1996) 331-338
38. Morgenstern D.A., Asher R.A., and Fawcett J.W. Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 137 (2002) 313-332
39. Moses H.L., Coffey Jr. R.J., Leof E.B., Lyons R.M., and Keski-Oja J. Transforming growth factor beta regulation of cell proliferation. J. Cell. Physiol. Suppl. Suppl 5 (1987) 1-7
40. Müller H.W., Junghans U., and Kappler J. Astroglial neurotrophic and neurite-promoting factors. Pharmacol. Ther. 65 (1995) 1-18
41. Nagata I., Ono K., Kawana A., and Kimura-Kuroda J. Aligned neurite bundles of granule cells regulate orientation of Purkinje cell dendrites by perpendicular contact guidance in two-dimensional and three-dimensional mouse cerebellar cultures. J. Comp. Neurol. 499 (2006) 274-289
42. Noble M., Fok-Seang J., and Cohen J. Glia are a unique substrate for the in vitro growth of central nervous system neurons. J. Neurosci. 4 (1984) 1892-1903
43. Pasterkamp R.J., Giger R.J., Ruitenberg M.J., Holtmaat A.J., De Wit J., De Winter F., and Verhaagen J. Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol. Cell. Neurosci. 13 (1999) 143-166
44. Popovich P.G., and Longbrake E.E. Can the immune system be harnessed to repair the CNS?. Nat. Rev. Neurosci. 9 (2008) 481-493
45. Romaris M., Bassols A., and David G. Effect of transforming growth factor-beta 1 and basic fibroblast growth factor on the expression of cell surface proteoglycans in human lung fibroblasts. Enhanced glycanation and fibronectin-binding of CD44 proteoglycan, and down-regulation of glypican. Biochem. J. 310 Pt. 1 (1995) 73-81
46. Rudge J.S., and Silver J. Inhibition of neurite outgrowth on astroglial scars in vitro. J. Neurosci. 10 (1990) 3594-3603
47. Rudge J.S., Smith G.M., and Silver J. An in vitro model of wound healing in the CNS: analysis of cell reaction and interaction at different ages. Exp. Neurol. 103 (1989) 1-16
48. Sawyer J.S., Anderson B.D., Beight D.W., Campbell R.M., Jones M.L., Herron D.K., Lampe J.W., McCowan J.R., McMillen W.T., Mort N., Parsons S., Smith E.C., Vieth M., Weir L.C., Yan L., Zhang F., and Yingling J.M. Synthesis and activity of new aryl- and heteroaryl-substituted pyrazole inhibitors of the transforming growth factor-beta type I receptor kinase domain. J. Med. Chem. 46 (2003) 3953-3956
49. Shearer M.C., and Fawcett J.W. The astrocyte/meningeal cell interface-a barrier to successful nerve regeneration?. Cell. Tissue Res. 305 (2001) 267-273
50. Shearer M.C., Niclou S.P., Brown D., Asher R.A., Holtmaat A.J., Levine J.M., Verhaagen J., and Fawcett J.W. The astrocyte/meningeal cell interface is a barrier to neurite outgrowth which can be overcome by manipulation of inhibitory molecules or axonal signalling pathways. Mol. Cell. Neurosci. 24 (2003) 913-925
51. Silver J., and Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5 (2004) 146-156
52. Smith G.M., and Hale J.H. Macrophage/microglia regulation of astrocytic tenascin: synergistic action of transforming growth factor-beta and basic fibroblast growth factor. J. Neurosci. 17 (1997) 9624-9633
53. Stichel C.C., Hermanns S., Luhmann H.J., Lausberg F., Niermann H., D'Urso D., Servos G., Hartwig H.G., and Muller H.W. Inhibition of collagen IV deposition promotes regeneration of injured CNS axons. Eur. J. Neurosci. 11 (1999) 632-646
54. Struckhoff G. Cocultures of meningeal and astrocytic cells-a model for the formation of the glial-limiting membrane. Int. J. Dev. Neurosci. 13 (1995) 595-606
55. Tang X., Davies J.E., and Davies S.J. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J. Neurosci. Res. 71 (2003) 427-444
56. Teng X., Nagata I., Li H.P., Kimura-Kuroda J., Sango K., Kawamura K., Raisman G., and Kawano H. Regeneration of nigrostriatal dopaminergic axons after transplantation of olfactory ensheathing cells and fibroblasts prevents fibrotic scar formation at the lesion site. J. Neurosci. Res. 86 (2008) 3140-3150
57. Wanner I.B., Deik A., Torres M., Rosendahl A., Neary J.T., Lemmon V.P., and Bixby J.L. A new in vitro model of the glial scar inhibits axon growth. Glia 56 (2008) 1691-1709
58. Wise G.E., Lin F., and Fan W. Effects of transforming growth factor-beta 1 on cultured dental follicle cells from rat mandibular molars. Arch. Oral Biol. 37 (1992) 471-478
59. Wynn T.A. Cellular and molecular mechanisms of fibrosis. J. Pathol. 214 (2008) 199-210
60. Xu Q., Norman J.T., Shrivastav S., Lucio-Cazana J., and Kopp J.B. In vitro models of TGF-beta-induced fibrosis suitable for high-throughput screening of antifibrotic agents. Am. J. Physiol. Renal. Physiol. 293 (2007) F631-F640
61. Yiu G., and He Z. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7 (2006) 617-627
62. Yoshida M., Saito H., and Katsuki H. Neurotrophic effects of conditioned media of astrocytes isolated from different brain regions on hippocampal and cortical neurons. Experientia 51 (1995) 133-136
63. Zhang Y., Anderson P.N., Campbell G., Mohajeri H., Schachner M., and Lieberman A.R. Tenascin-C expression by neurons and glial cells in the rat spinal cord: changes during postnatal development and after dorsal root or sciatic nerve injury. J. Neurocytol. 24 (1995) 585-601
64. Zhu X., Bergles D.E., and Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135 (2008) 145-157