Blockage of 9-O-acetyl gangliosides induces microtubule depolymerization in growth cones and neurites

European Journal of Cell Biology

Volumn 72, Issue 3, 1997, Pages 202-213

  Araujo, Helena ^a   Menezes, Meiga ^a   Mendez Otero, Rosália ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Axonal navigation; Cytoskeleton; Gangliosides; Growth cones; Neural development

Indexed keywords

GANGLIOSIDE; GANGLIOSIDE ANTIBODY; MONOCLONAL ANTIBODY;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; DEPOLYMERIZATION; EMBRYO; GROWTH CONE; MICROFILAMENT; MICROTUBULE ASSEMBLY; MOUSE; NERVE CELL CULTURE; NERVE CELL GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; SPINAL GANGLION;

EID: 0030967477     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Abotomey, C., W. D. Cowden, C. E. Hill: Carbohydrates play a role in neurite outgrowth in vitro during development and regeneration. Dev. Brain Res. 79, 101-114 (1994).
2. Ahmad, F. J., T. P. Pienkowski, M. Baas: Regional differences in microtubule dynamics in the axon. J. Neurosci. 13, 856-866 (1993).
3. Araujo, H., R. Mendez-Otero: Cytoskeletal dynamics in growth cone retraction induced by the mAb JONES. Neurosci. Abstr. 21, 1038 (1995).
4. Baas, P. W., M. M. Black: Individual microtubules in the axon consist of domains that differ in both composition and stability. J. Cell Biol. 111, 495-509 (1990).
5. Bantlow, C., M. Schmidt, T. Hassinger, M. Schwab, S. Kater: Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. Science 259, 80-83 (1993).
6. Bassi, R., V. Chigorno, A. Fiorilli, S. Sonnino, G. Tettamanti: Exogenous gangliosides GD1b and GD1b-lactone, stably associated to rat brain P2 subcellular fraction, modulate differently the process of protein phosphorylation. J. Neurochem. 57, 1207-1211 (1991).
7. Blum, A. S., C. J. Barnstable: O-acetylation of a cell-surface carbohydrate creates discrete molecular patterns during neuronal development. Proc. Natl. Acad. Sci. USA 84, 8716-8720 (1987).
8. Bonafede, D. M., L. J. Macala, M. Constantine-Paton, R. K. Yu: Isolation and characterization of ganglioside 9-O-acetyl GD3 from bovine buttermilk. Lipids 24, 680-684 (1989).
9. Bray, D., C. Thomas, G. Shaw: Growth cone formation in cultures of sensory neurons. Proc. Natl. Acad. Sci. USA 75, 5226-5229 (1978).
10. Brown, A., Y. Li, T. Slaughter, M. Black: Composite microtubules of the axon: quantitative analysis of tyrosinated and acetylated tubulin along individual axonal microtubules. J. Cell Sci. 104, 339-352 (1993).
11. Burden-Guley, S. M., H. R. Payneand, V. Lemmon: Growth cones are actively influenced by substrate-bound adhesion molecules. J. Neurosci. 15, 4370-4381 (1995).
12. Cheresh, D. A., R. Pytela, M. D. Pierschbacher, F. G. Klier, E. Ruoslahti, A. R. Reisfeld: An Arg-Gly-Asp-directed receptor on human melanoma cells exist in a calcium-dependent functional complex with the disialoganglioside GD2. In: R. W. Ledeen, E. L. Hogan, G. Tettamati, A. J. Yates, R. K. Yu (eds.): New Trends in Ganglioside Research: Neurochemical and Neurodegenerative Aspects, pp. 203-217. Liviana Press. Padova 1987.
13. Clark, E. A., J. S. Brugge: Integrins and signal transduction pathways: the road taken. Science 268, 233-238 (1995).
14. Constantine-Paton, M., A. S. Blum, R. Mendez-Otero, C. J. Barnstable: A cell surface molecule distributed in a dorsal-ventral gradient in the perinatal rat retina. Nature 324, 459-462 (1986).
15. Davis, L, V. Rehder, S. B. Kater: Autonomous activities of the neuronal growth cone. In: P. C. Letourneau, S. B. Kater, E. R. Macagno (eds.): The Nerve Growth Cone. Raven Press. New York 1992.
16. Di Tella, M., F. Felguin, G. Mortini, A. Cáceres: Microfilament-associated growth cone component depends upon tau for its intracellular localization. Cell Motil. Cytoskel. 29, 117-130 (1994).
17. Dodd, J., T. Jessel: Axon guidance and the patterning of neuronal projections in vertebrates. Science 242, 692-699 (1988).
18. Fan, J., G. Mansfield, T. Redmond: P. Gordon-Weeks, J. Raper: The organization of F-actin and microtubules in growth cones exposed to a brain-derived collapsing factor. J. Cell Biol. 121, 867-878 (1993).
19. Finnegan, S. G., V. P. Lemon, E. Koenig: Characterization of the retraction response of goldfish retinal ganglion cell axons induced by monoclonal antibody 8A2 in vitro. Cell Motil. Cytoskel. 23, 279-301 (1992).
20. Finnegan, S. G., V. P. Lemon, E. Koenig: Monoclonal antibody 8A2-induced retraction appears to be mediated by protein phosphorylation in goldfish retinal ganglion cell axons. Dev. Biol. 156, 230-242 (1993).
21. Fishman, P.: Recent advances in identifying the functions of gangliosides. Chem. Phys. Lipids 42, 137-151 (1989).
22. Friedman, J. E., S. M. Fortune, M. Constantine-Paton: Antibodies to 9-O-acetylated gangliosides causes retraction of neuroblastoma and DRG glial process. Soc. Neurosci. Abstr. 16, 151 (1990).
23. Griffin, C. G., P. C. Letourneau: Rapid retraction of neurites by sensory neurons in response to increased concentrations of nerve growth factor. J. Cell Biol. 86, 156-161 (1980).
24. Grumet, M., D. R. Friedlander, G. Edelman: Evidence for the binding of Ng-CAM to laminin. Cell Adhesion and Commun. 1, 177-190 (1993).
25. Igarashi, M., S. Strittmater, T. Vartanian, M. Fishman: Mediation by G proteins of signals that cause collapse of growth cones. Science 259, 77-79 (1993).
26. Igarashi, M., H. Waki, M. Hirota, Y. Hirabayashi, K. Obata, S. Ando: Differences in lipid composition between isolated growth cones from the forebrain and those from the brainstem in the fetal brain. Dev. Brain Res. 51, 1-9 (1990).
27. Igarashi, M., H. Waki, S. Saito, Y. Komiya, S. Ando: Characteristics of gangliosides including O-acetylated species in growth cone membranes at several developmental stages in rat forebrain. Dev. Brain Res. 78, 17-24 (1994).
28. Jacobs, J. R., J. K. Stevens: Experimental modification of PC12 neurite shape with the microtubule-depolymerizing drug nocodazole: a serial microscope study of neurite shape control. J. Cell Biol. 103, 907-915 (1986).
29. Joshi, H. C., P. Baas, D. T. Chu, S. R. Heideman: The cytoskeleton of neurites after microtubule depolymerization. Exp. Cell Res. 163, 233-245 (1986).
30. Joshi, H. C., D. T. Chu, R. Buxbaum, S. R. Heideman: Tension and compression in the cytoskeleton of PC12 neurites. J. Cell Biol. 101, 697-705 (1985).
31. Laitinen, J., R. Lopponen, J. Merenmies, H. Ravala: Binding of laminin to brain gangliosides and inhibition of laminin-neuron interaction by the gangliosides. FEBS Lett. 217, 94-100 (1987).
32. Ledeen, R.: Gangliosides of the neuron. Trends Neurosci. 8, 169-174 (1985).
33. Ledeen, R. W.: Biosynthesis, metabolism, and biological effects of gangliosides. In: R. U. Margolis, R. K. Margolis (eds.): Neurobiology of Glycoconjugates. pp. 43-69. Plenum Press. New York 1989.
34. Letourneau, P.: Integrins and N-cadherin are adhesive molecules involved in growth cone migration. In: P. C. Letourneau, S. B. Kater, E. R. Macagno (eds.): The Nerve Growth Cone. pp. 181-193. Raven Press. New York 1991.
35. Letourneau, P., M. L. Condic, D. M. Snow: Interactions of developing neurons with the extracellular matrix. J. Neurosci. 14, 915-928 (1994).
36. Luo, Y., D. Raible, J. Raper: Collapsin: a protein m brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227 (1993).
37. Mendez-Otero, R., L. Cavalcante: Expression of 9-O-acetylated gansliosides is correlated with tangential cell migration in the rat brain. Neurosci. Lett. 204, 97-100 (1996).
38. Mendez-Otero, R., M. Constantine-Paton: Granule cell induction of 9-O-acetylated gangliosides on cerebellar glia in microcultures. Dev. Biol. 138, 400-409 (1990).
39. Mendez-Otero, R., J. E. Friedrnan: Role of acetylated gangliosides on neurite extension. Eur. J. Cell Biol. 71, 192-198 (1996).
40. Mendez-Otero, R., A. Ramon-Cueto: Expression of 9-O-acetylated gangliosides during development of the rat olfactory system. Neuroreport 5, 1755-1759 (1994).
41. Mendez-Otero, R., B. Schlosshauer, C. J. Barnstable, M. Constantine-Paton: A developmentally regulated antigen associated with neural cell and process migration. J. Neurosci. 8, 564-579 (1988.)
42. Mendez-Otero, R., B. Schlosshauer, M. Constantine-Paton: Role of acetylated gangliosides on neuronal migration and axonal out-growth. In: R. Lent (ed.): The Visual System from Genesis to Maturity. pp. 49-62. Birkhäuser. Boston 1992.
43. Mitchison, T., M. Kirschner: Cytoskeletal dynamics and nerve growth. Neuron 1, 761-772 (1988).
44. Mugnai, G., K. Lewandowska, H. U. Chui, L. C. Rosenberg, L. A. Clup: Ganglioside-dependent adhesion events of human neuroblastema cells regulated by the RGDS-dependent fibronectin receptor and proteoglycans. Exp. Cell Res. 175, 229-247 (1988).
45. Neeley, M. D., M. Gesemann: Disruption of microfilaments in growth cones following depolarization and calcium influx. J. Neurosci. 14, 7511-7520 (1994).
46. Pini, A.: Chemorepulsion of axons in the developing central nervous system. Science 261, 95-98 (1993).
47. Quaranta, V., J. R. Jones: The internal affairs of an integrin. Trends Cell Biol. 1, 2-4 (1991).
48. Rakic, P., R. S. Cameron, H. Komuro: Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr. Op. Neurobiol. 4, 63-69 (1994).
49. Raper, J. A., J. P. Kapfammer: The enrichment of a neuronal growth cone collapsing activity from embryonic chick brain. Neuron 4, 21-29 (1990).
50. Reichardt, L. F., K. J. Tomaselli: Extracellular matrix molecules and their receptors: functioning neural development. Annu. Rev. Neurosci. 14, 531-570 (1991).
51. Rivas, R. J., D. W. Burmeister, P. J. Goldberg: Rapid effects of laminin on the growth cone. Neuron 8, 107-115 (1992).
52. Robson, S., R. Burgoyne: Differential localization of tyrosinated, detyrosinated and acetylated α-tubulin in neuntes and growth cones of dorsal root neurons. Cell Motil. Cytoskel. 12, 273-282 (1989).
53. Roisen, E. S. G. Matta, M. M. Rapport: The role of gangliosides in neurotrophic interaction in vitro. In: G. Tettamati, R. W. Ledeen, K. Sadhoff, Y. G. Nagaiand Toffano (eds.): Gangliosides and Neuronal Plasticity. pp. 281-293. Liviana Press. Padova 1986.
54. Rösner, H., M. Al-Aqtum, H. Rahman: Gangliosides and neuronal differentiation. Neurochem. Int. 20, 339-351 (1992).
55. Rutishauser, U.: Adhesion molecules of the nervous system. Curr. Op. Neurobiol. 3, 709-715 (1993).
56. Sabel, B.: Anatomic mechanisms whereby ganglioside treatment induces brain repair. In: D. G. Stein, B. Sabel (eds.): Pharmacological Approaches to Treatment of Brain and Spinal Cord Injury. pp. 167-194. Plenum Press. New York 1988.
57. Sariola, H., E. Aufderheide, H. Bernard, S. Henke-Fahle, W. Dippold, P. Ekbolm: Antibodies to cell surface ganglioside GD3 perturb inductive epithelial-mesenchymal interactions. Cell 54, 235-245 (1988).
58. Schliwa, M.: Action of cytochalasin D on cytoskeletal networks. J. Cell Biol. 92, 79-91 (1982).
59. Schlosshauer, B., A. B. Blum, R. Mendez-Otero, C. Barnstable, M. Constantine-Paton: Developmental regulation of ganglioside antigens recognized by JONES antibody. J. Neurosci. 8, 580-592 (1988).
60. Schmidt, C. E., J. Dai, D. A. Lauffenburger, M. P. Sheetzand, A. F. Horwitz: Integrin-cytoskeletal interactions in neuronal growth cones. J. Neurosci. 15, 3400-3407 (1995).
61. Sparrow, J. R., C. McGuiness, M. Schwartz, G. Grafstein: Antibodies to gangliosides inhibit goldfish optic nerve regeneration in vitro. J. Neurosci. Res. 12, 233-243 (1984).
62. Spirman, N., B. A. Sela, E. Gilter, E. Calef, M. Schwartz: Regenerative capacity of the goldfish visual system is affected by antibodies specific to gangliosides injected intraocularly. J. Neuroimmunol. 6, 197-207 (1984).
63. Stallcup, W. B.: Involvement of gangliosides and glycoprotein fibronectin receptors in cellular adhesion to fibronectin. Exp. Cell Res. 177, 90-102 (1988).
64. Stallcup, W. B., R. Pytella, E. Ruoslahti: A neuroectoderm-associated ganglioside participates in fibronectin receptor-mediated adhesion of germinal cells to fibronectin. Dev. Biol. 132, 212-229 (1989).
65. Tanaka, E., J. Sabry: Making the connection: Cytoskeletal rearrangements during growth cone guidance. Cell 83, 171-176 (1995).
66. Thompson, K., P. M. Horowitz, K. L. Bentley, D. Thomas, J. F. Aldereh, R. J. Klebe: Localization of the ganglioside-binding site of fibronectin. J. Biol. Chem. 261, 5209-5214 (1986).
67. Vale, R., G. Banker, Z. W. Hall: The neuronal cytoskeleton. In: Z. Hall (ed.): An Introduction to Molecular Neurobiology. pp. 247-280. Sinauer Associates, Inc. Sunderland, MA/USA 1992.
68. Yates, A. J., C. L. Walters, C. L. Wood, D. Johnson: Ganglioside modulation of cyclic AMP-dependent protein kinase and cyclic nucleotide phosphodiesterase in vitro. J. Neurochem. 53, 162-167 (1989).
69. Yu. W, F. J. Ahmadand, P. W. Baas: Microtubule fragmentation and partitioning in the axon during collateral branch formation. J. Neurosci. 14, 5872-5884 (1994).