Neurite outgrowth inhibitor of gliotic brain tissue. Mode of action and cellular localization, studied with specific monoclonal antibodies

European Journal of Neuroscience

Volumn 9, Issue 5, 1997, Pages 977-989

  Bovolenta, P ^a   Fernaud Espinosa, I ^a   Mendez Otero, R ^a   Nieto Sampedro, M ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

Brain damage; Glial cells; Neuritogenesis; Proteoglycan; Rat; Regeneration

Indexed keywords

GROWTH INHIBITOR; MONOCLONAL ANTIBODY; PROTEOCHONDROITIN SULFATE; PROTEOHEPARAN SULFATE;

ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN MEMBRANE; CELLULAR DISTRIBUTION; FEMALE; GLIA CELL; GROWTH CONE; IMMUNOBLOTTING; MOLECULAR WEIGHT; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL;

EID: 0030927538     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.1997.tb01448.x     Document Type: Article

References (69)

1. Ard, M. D. and Bunge, R. P. (1988) Heparan sulfate proteoglycan and laminin immunoreactivity on cultured astrocytes: relationship to differentiation and neurite growth. J. Neurosci., 8, 2844–2858.
2. Bovolenta, P., Wandosell, F. and Nieto‐Sampedro, M. (1992) Glial scar tissue: a source of molecules which inhibit central neurite outgrowth. Prog. Brain Res., 94, 367–379.
3. Bovolenta, P., Wandosell, E and Nieto‐Sampedro, M. (1993a) Characterization of a neurite outgrowth inhibitor expressed after CNS injury. Eur. J. Neurosci., 5, 454–465.
4. Bovolenta, P., Wandosell, F., and Nieto‐Sampedro, M. (1993b) Neurite outgrowth inhibitors associated with glial cells and glial cell lines. NeuroReport, 5, 345–348.
5. Brauker, J. H., Trautman, M. S. and Berfield, M. (1991) Syndecan, a cell surface proteoglycan, exhibits a molecular polymorphism during lung development. Dev. Biol., 147, 285–292.
6. Bicknese, A. R., Sheppard, A. M., O'Leary, D. D. M. and Perlman, A. L. (1994) Thalamocortical axons extend along a chondroitin sulfate proteoglycan‐enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J. Neurosci., 14, 3500–3510.
7. Brittis, P. A., Canning, D. R. and Silver, J. (1992) Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science, 255, 733–736.
8. Cajal, S. R. (1928) Degeneration and Regeneration of the Nervous System. Oxford University Press, Oxford.
9. Carbonetto, S. (1991) Facilitatory and inhibitory effects of glial cells and extracellular matrix in axonal regeneration. Curr: Opin. Neurobiol., 1, 507–413.
10. Carey, D. J., Evans, D. M., Stahl, R. C., Asundi, V. K., Conner, K. J., Garbes, P. and Cizmeci‐Smith, G. (1992) Molecular cloning and characterization of N‐syndecan, a novel transmembrane heparan sulphate proteoglycan. J. Cell Biol 117, 191–201.
11. Caroni, P. and Schwab, M. E. (1988) Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J. Cell Biol., 106, 1281–1288.
12. Castellot, J. J., Wong, K., Herman, B., Hoover, R. L., Albertini, D. F., Wright, T. C., Caleb, B. L. and Karnovsky, M. J. (1985) Binding and internalization of heparin by vascular smooth muscle cells. J. Cell. Physiol., 124, 13–20.
13. Choung, C. M. and Edelman, G. M. (1984) Alteration in cell adhesion molecules during development of different regions of the nervous system. J. Neurosci., 4, 2354–2368.
14. Cole, G. J. and McCabe, C. F. (1991) Identification of a developmentally regulated keratan sulfate proteoglycan that inhibit cell adhesion and neurite outgrowth. Neuron, 7, 1007–1018.
15. Cole, G. J., Loewy, A., Cross, N. V., Akerson, R. and Glaser, L. (1986) Topographic localization of the heparin‐binding domain of the neural cell adhesion molecule N‐CAM. J. Cell Biol., 103, 1739–1744.
16. Dou, C. L. and Levine, J. M. (1994) Inhibition of neurite outgrowth by the NG2 chondroitin sulfate proteoglycan. J. Neurosci., 14, 7616–7628.
17. Faissner, A., Clement, A., Lochter, A., Streit, A., Mandl, C. and Schachner, M. (1994) Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties. J. Cell Biol., 126, 783–799.
18. Fernand‐Espinosa, I., Nieto‐Sampedro, M. and Bovolenta, P. (1993) Differential activation of microglia and astrocytes in aniso‐ and isomorphic gliotic tissue. Glia, 8, 277–291.
19. Fernaud‐Espinosa, I., Nieto‐Sampedro, M. and Bovolenta, P. (1994) Differential effects of glycosaminoglycans on neurite outgrowth from hippocampal and thalamic neurons. J. Cell Sci., 107, 1437–1448.
20. Fernaud‐Espinosa, I., Nieto‐Sampedro, M. and Bovolenta, P. (1996) Developmental distribution of glycosaminoglycans in the embryonic rat brain: relationship to axonal tract formation. J. Neurobiol., 30, 410–424.
21. Fichard, A., Verna, J. M. and Saxod, R. (1991) Involvement of a chondroitin sulfate proteoglycan in the avoidance of chick epidermis by dorsal root ganglia fibers: a study using β‐D‐xyloside. Dev. Biol., 148, 1–9.
22. Friedlander, D. R., Milev, P., Karthikeyan, L., Margolis, R. K., Margolis, R. U. and Grumet, M. (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng‐CAM/L1/NILE and N‐CAM, and inhibits neuronal adhesion and neurite outgrowth. J. Cell Biol, 125, 699–680.
23. Grumet, M. (1991) Cell adhesion molecules and their subgroups in the nervous system. Curr. Opin. Neurobiol., 1, 370–376.
24. Grumet, M., Flaccus, A. and Margolis, R. U. (1993) Functional characterization of chondroitin sulfate proteoglycans of brains: interaction with neurons and neural cell adhesion molecules. J. Cell Biol., 120, 815–824.
25. Halfter, W. and Schurer, B. (1994) A new heparan sulfate proteoglycan in the extracellular matrix of the developing chick embryo. Exp. Cell Res., 214, 285–296.
26. Harlow, E. and Lane, D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp. 521–524.
27. Herndon, M. E. and Lander, A. D. (1990) A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron, 4, 945–961.
28. Ishihara, M., Fedarko, N. S. and Conrad H. E. (1986) Transport of heparan sulfate into the nuclei of hepatocytes. J. Bid. Chem., 261, 13575–13580.
29. Kapfhammer, J. P., Grunewald, B. E. and Raper, J. A. (1986) The selective inhibition of growth cone advancement of specific neurites in cultures. J. Neurosci., 6, 2521–2534.
30. Kater, S. B. and Mills, L. R. (1991) Regulation of growth cone behaviour by calcium. J. Neurosci. 11, 891–899.
31. Kennedy, T. E. and Tessier‐Lavigne, M. (1995) Guidance and induction of branch formation in developing axons by target‐derived diffusible factors. Curr Opin. Neurobiol., 5, 83–90.
32. Keynes, R. J. and Cook, G. M. W. (1995) Repulsive and inhibitory signals. Curr Opin. Neurobiol., 5, 75–82.
33. Lafont, F., Rouget, M., Triller, A., Prochiantz, A. and Rousselet, A. (1992) In vitro control of neuronal polarity by glycosaminoglycans. Development, 114, 17–29.
34. Lafont, F., Prochiantz, A., Valenza, C., Petitou, M., Pascal, M., Rouget, M. and Rousselet, A. (1994) Defined glycosaminoglycans motifs have opposite effects on neuronal polarity in vitro. Dev. Biol., 165, 453–468.
35. Landolt, R. M., Vaughan, L., Winterhalter, K. H. and Zimmermann, D. R. (1995) Versican is selectively expressed in embryonic tissues that act as barriers to neural crest cell migration and axon outgrowth. Development, 121, 2303–2312.
36. LeGal LeSalle, G., Rougon, G. and Valin, A. (1992) The embryonic form of neural cell surface molecule (E‐NCAM) in the rat hippocampus and its reexpression on glial cells following kainic acid ‐induced status epilepticus. J. Neurosci., 12, 872–882.
37. Letourneau, P. C., Condic, M. L. and Snow, D. M. (1994) Interactions of developing neurons with the extracellular matrix. J. Neurosci., 14, 915–928.
38. Levine, J. M. (1994) Increased expression of the NG2 chondroitin sulfate proteoglycan after brain injury. J. Neurosci., 14, 4716–4730.
39. Lochter, A., Vaughan, L., Kaplony, A., Prochiantz, A., Schachner, M. and Faissner, A. (1991) JI/Tenascin in substrate‐bound and soluble form display contrary effects on neurite outgrowth. J. Cell Biol, 113, 1159–1171.
40. Luo, Y. and Raper, J. A. (1994) Inhibitory factors controlling growth cone motility and guidance: Curr: Opin. Neurobiol., 4, 648–654.
41. Luo, Y., Raible, D. Raper, J. A. (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell, 75, 217–227.
42. Maeda, N. and Noda, M. (1996) 6B4 proteoglycan/phosphacan is a repulsive substratum but promotes morphological differentiation of cortical neurons. Development, 122, 647–658.
43. Margolis, R. K. and Margolis, R. U. (1989) Structure and localization of glycoproteins and proteoglycans. In Margolis, R. U. and Margolis, R. K., (eds), Neurobiology of Glycoconjugates. Plenum Press, New York, pp. 85–126.
44. McKeon, R. J., Schreiber, R. C., Rudge, J. S. and 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.
45. McKeon, R. J., Hoke, A. and Silver, J. (1995) Injury‐induced proteoglycans inhibit the potential for laminin‐mediated axon growth on astrocytic scars. Exp. Neurol., 136, 3243.
46. McKerracher, L., Davis, S., Jackson, D. L., Kottis, V., Dunn, R. J. and Braun, P. E. (1994) Identification of myelin‐associated glycoprotein as a major myelin‐derived inhibitor of neurite outgrowth. Neuron, 13, 805–811.
47. McMillian, M. K., Thai, L., Hong, J. S., O'Callaghan, J. P. and Pennypacker, K. R. (1994) Brain injury in a dish: a model for reactive gliosis. Trends Neurosci., 17, 138–142.
48. Messersmith, E. K., Leonardo, E. D., Shatz, C. J., Tessier‐Lavigne, M., Goodman, C. S. and Kolodkin, A. L. (1995) Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron, 14, 949–959.
49. Morrisey, J. H. (1981) Modified silver stain for proteins in polyacrylamide gels. And. Biochem., 117, 307–310.
50. Muir, D., Engvall, E., Varon, S. and Manthorpe, M. (1989) Schwannoma cellderived inhibitor of neurite‐promoting activity of laminin. J. Cell Biol., 109, 2353–2362.
51. Mukhopadhyay, G., Doherty, P., Walsh, F. S., Crocker, P. R. and Fibin, M. T. (1994) Recombinant MAG expressed by CHO cells is shown to stimulate axonal extension by neonatal sensory neurons, but to inhibit extension by adult neurons. Neuron, 13, 757–767.
52. Nadler, J. V., Perry, B. W. and Cotman, C. W. (1978) Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature, 271, 676–677.
53. Nieto‐Sampedro, M. and Mora, F. (1994) Active microglia, sick astroglia and Alzheimer's type dementias. NeuroReport, 5, 375–380.
54. Oakley, R. and Tosney, K. W. (1991) Peanut agglutinin and chondroitin‐6‐sulfate are molecular markers for tissues that act as barriers to axon advance in the avian embryo. Dew. Biol., 147, 187–206.
55. Perry, G., Siedlak, S., Richey, P., Kawai, M., Cras, P., Kalaria, R., Galloway, P., Scardina, J., Cordell, B., Greenberg, B., Ledbetter, S. and Gambetti, P. (1991) Association of heparan sulfate proteoglycan with the neurofibrillary tangles of Alzheimer disease. J. Neurosci., 11, 3679–3683.
56. Pini, A. (1993) Chemorepulsion of axons in the developing mammalian central nervous system. Science, 261, 95–98.
57. Püschel, A. W., Adams, R. H. and Betz, H. (1995) Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron, 14, 941–948.
58. Raper, J. A. and Kapfhammer, J. P. (1990) The enrichment of a neuronal growth cone collapsing activity from embryonic chick brain. Neuron, 4, 21–29.
59. Reichardt, L. F. and Tomaselli, K. J. (1991) Extracellular matrix molecules and their receptors: functions in neural development. Annu. Rev. Neurosci., 14, 531–570.
60. Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M. and Sunshine, J. (1988) The neural cell adhesion molecule (NCAM) as a regulator of cell‐cell interactions. Science, 240, 53–57.
61. Schwab, M. E., Kapfhammer, J. P. and Bandtlow, C. E. (1993) Inhibitors of neurite growth. Annu. Rev. Neurosci., 16, 565–595.
62. Sheppard A. M., Hamilton, S. K. and Pearlman, A. L. (1991) Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J. Neurosci., 11, 3928–3942.
63. Siman, R., Card, J. P., Nelson, R. B. and Davis, L. G. (1989) Expression of P‐amyloid precursor protein in reactive astrocytes following neuronal damage. Neuron, 3, 275–285.
64. Snow, D. and Letourneau, P. C. (1992) Neurite outgrowth on a step gradient of chondroitin sulfate proteoglycan (CS‐PG). J. Neurobiol., 23, 322–336.
65. Snow, D., Lemmon, V., Camno, D. A., Caplan, A. I. and Silver, J. (1990) Sulfate proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol., 109, 111–130.
66. Snow, D., Watanabe, M., Letourneau, P. and Silver, J. (1991) A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development, 113, 1473–1485.
67. Snow, D., Atkinson, P. B., Hassinger, T. D., Letourneau, P. C. and Kater, S. B. (1994a) Chondroitin sulfate proteoglycan elevates cytoplasmic calcium in DRG neurons. Dev. Biol, 166, 87–100.
68. Snow, A., Sekiguchi, R., Nochlin, D., Frase, P., Kimata, K., Mizutani, A., Arai, M., Schreirer, W. and Morgan, D. (1994b) An important role of heparan sulfate proteoglycan (perlcan) in a model system for the deposition and persistence of fibrillar β‐amyloid in rat brain. Neurol, 12, 219–234.
69. Su, J. H., Cummings, B. J. and Cotman C. W. (1992) Localization of heparan sulfate glycosaminoglycans and proteoglycan core protein in aged brain and Alheimer's disease. Neuroscience, 51, 801–813.