Juvenile and mature MAP2 isoforms induce distinct patterns of process outgrowth

Molecular Biology of the Cell

Volumn 7, Issue 3, 1996, Pages 443-455

  Leclerc, Nicole ^a   Baas, Peter W ^b   Garner, Craig C ^c   Kosik, Kenneth S ^d,e  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d Brigham and Women's Hospital Center for Neurologic Diseases   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSKELETON PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; PROTEIN SUBUNIT;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CYTOARCHITECTURE; GENE EXPRESSION; INSECT; MICROTUBULE ASSEMBLY; MOLECULAR WEIGHT; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

EID: 0029921189     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.3.443     Document Type: Article

References (44)

1. Baas, P.W., Deitch, J.S., Blade, M.M., and Banker, G.A. (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. USA 85, 8335-8339.
2. Baas, P.W., and Heidemann, S.R. (1986). Microtubule reassembly from nucleating fragments during the regrowth of amputated neuntes. J. Cell Biol. 21, 397-427.
3. Baas, P.W., Pienkowski, T.P., and Kosik, K.S. (1991). Processes induced by tau expression in Sf9 cells have an axon-like microtubule organization. J. Cell Biol. 115, 1333-1344.
4. Baas, P.W., Sinclair, G.I., and Heidemann, S.R. (1987). Role of microtubules in the cytoplasmic compartmentation of neurons. Brain Res. 420, 73-81.
5. Banker, G , and Goslin, K. (1990). Culturing Nerve Cells, ed. C.F. Stevens, Cambridge, MA: The MIT Press.
6. Bartlett, W.P., and Banker, G.A. (1984). An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. I Cells which develop without intercellular contacts J. Neurosci. 4, 1944-1953
7. Black, M.M (1987). Comparison of the effects of microrubule-associated protein 2 and tau on the packing density of in vitro-assembled microtubules. Proc. Natl. Acad. Sci. USA 84, 7783-7787.
8. Brandt, R., and Lee, G. (1993a). Functional organization of microtubule-associated protein tau. J. Biol. Chem. 268, 3414-3419.
9. Brandt, R., and Lee, G. (1993b). The balance between tau protein's microtubule growth and nucleation activities: implications for the formation of axonal microtubules. J. Neurochem. 61, 997-1005.
10. Burton, P.R., and Paige, J.L. (1981). Polarity of axoplasmic microtubules in the olfactory nerve of the frog. Proc. Natl. Acad. Sci. USA 78, 3269-3273.
11. Caceres, A., and Kosik, K.S. (1990). Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
12. Caceres, A., Mautino, J., and Kosik, K.S. (1992). Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9, 607-618.
13. Caceres, A , Potrebic, S., and Kosik, K. (1991). The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J. Neurosci. 11, 1515-1523.
14. Chen, J., Kanai, Y., Cowan, N.J., and Hirokawa, N. (1992). Projection domains of MAP2 and tau determine the spacings between microtubules in dendrites and axons. Nature 360, 674-677.
15. Cheley, S., Kosik, K.S., Paskevich, P., Bakalis, S., and Bayley, H. (1992). Phosphorylated baculovirus p10 is a heat-stable microtubule-associated protein associated with process formation in Sf9 cells. J. Cell Sci. 102, 739-752.
16. Cleveland, D., Monteiro, M.J., Wong, P.C., Gill, S.R., Geirhart, J.D., and Hoffman, P.N. (1991). Involvement of neurofilaments in the radial growth of axons. J. Cell Sci Suppl. 15, 85-95.
17. de Waegh, S.M., Lee, V.M.-Y., and Brady, S.T. (1992). Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 68, 451-463.
18. Drechsel, D.N., Hyman, A.A., Cobb, M.H., and Kirschner, M.W. (1992). Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol. Biol. Cell 3, 1141-1154.
19. Edson, K., Weisshaar, B., and Matus, A. (1993). Actin depolymerization induces process formation on MAP2-transfected non-neuronal cells. Development 117, 689-700.
20. Fung, M.-C., Chiu, K.Y.M., Weber, T., Chang, T.W., and Chang, N.T. (1988). Detection and purification of a recombinant human B lymphotropic virus (HHV-6) in the baculovirus expression system by limiting dilution and DNA dot-blot hybridization. J. Virol. Methods 19, 33-42.
21. Garner, C.C., and Matus, A. (1988). Different forms of microtubule-associated protein 2 are encoded by separate mRNA transcripts J. Cell Biol. 106, 779-783.
22. Hagestedt, T., Lichenberg, B., Wille, H., Mandelkow, E.M., and Mandelkow, E. (1989). Tau protein becomes long and stiff upon phosphorylation: correlation between paracrystalline structure and degree of phosphorylation. J. Cell Biol. 109, 1643-1651.
23. Heidemann, S.R., Landers, J.M., and Hamburg, M.A. (1981). Polarity orientation of axonal microtubules. J. Cell Biol 91, 661-665.
24. Hillman, D.E. (1988). Parameters of dendritic shape and substructure: intrinsic and extrinsic determinants? In: Intrinsic Determinants of Neuronal Form and Function. ed. R.J. Lasek and M.M. Black, New York: Alan R. Liss, 83-113.
25. Hoffman, P.N., Cleveland, D.W , Griffin, J.W., Landes, P.W., Cowan, N.J., and Price, D.L. (1987). Neurofilament gene expression: a major determinant of axonal caliber. Proc. Natl. Acad. Sci. USA 84, 3472-3476.
26. Kindler, S., Schulz, B., Goedert, M., and Garner, C.C. (1990). Molecular structure of microtubule-associated protein 2b and 2c from rat brain J. Biol. Chem. 265, 19679-19684.
27. Kitts, P.A., Ayres, MD., and Possee, R.D. (1990). Linearization of baculovirus DNA enhances the recovery of recombinant virus expression vectors. Nucleic Acids Res. 18, 5667-5672.
28. Knops, J., Kosik, K.S., Lee, G., Pardee, J.D., Cohen-Gould, L., and McConlogue, L. (1991). Overexpression of tau in a nonneuronal cell induces long cellular processes. J. Cell Biol. 114, 725-733.
29. Knowles, R., Leclerc, N., and Kosik, K.S. (1994). Organization of actin and microtubules during process formation in tau-expressing Sf9 cells Cell Motil. Cytoskeleton 28, 256-264.
30. Kosik, K.S., and Caceres, A. (1991). Tau protein and the establishment of an axonal morphology. J. Cell Sci. Suppl. 15, 69-74.
31. Kosik, K.S., and McConlogue, L. (1994). Microtubule-associated protein function: lessons from expression in Spodoptera frugiperda cells. Cell Motil. Cytoskeleton 28, 195-198.
32. Kosik, K.S., Orecchio, L D., Binder, L.I., Trojanowski, J., Lee, V., and Lee, G. (1988). Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1, 817-825.
33. Leclerc, N., Kosik, K.S., Cowan, N., Pienkowski, T.P., and Baas, P.W. (1993). Process formation in Sf9 cells induced by the expression of a microtubule-associated protein 2C-like construct. Proc. Natl. Acad. Sci. USA 90, 6223-6227.
34. Lewis, S.A., Wang, D., and Cowan, N.J. (1988). Microtubule-associated protein MAP2 shares a microtubule-binding motif with tau protein. Science 242, 936-939.
35. Ludin, B., and Matus, A. (1993). The neuronal cytoskeleton and its role in axonal and dendritic plasticity. Hippocampus 3, 61-72.
36. Mandel, J.W., Benson, D.L., and Banker, G.A. (1993). A spatial gradient of tau protein phosphorylation in nascent axons. Soc. Neurosci. 19, 1082 (Abstract 448.9).
37. Matus, A. (1994). Stiff microtubules and neuronal morphology. Trends Neurosci. 17, 19-22.
38. Papandrikopoulou, A., Doll, T., Tucker, R.P., Garner, C.C., and Matus, A. (1989). Embryonic MAP2 lacks the cross-linking sidearm sequences and dendritic targeting signal of adult MAP2. Nature 340, 650-652.
39. Sharma, N., Kress, Y., and Shafit-Zagardo, B. (1994). Antisense MAP2 oligonucleotides induce changes in microtubule assembly and neuritic elongation in pre-existing neurites of rat cortical neurons. Cell Motil. Cytoskeleton 27, 234-247.
40. Summers, M.D., and Smith, G.E. (1987). A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures, Bulletin No. 1555, College Station, TX: Texas Agricultural Experiment Station and Texas A&M University.
41. Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some application. Proc. Natl. Acad. Sci. USA 76, 4350-4353.
42. Tucker, R.P., Binder, L.I., Viereck, C., Hemmings, B.A., and Matus, A. (1988). The sequential appearance of low- and high-molecular weight forms of MAP2 in the developing cerebellum. J. Neurosci. 12, 4503-4512.
43. Umeyama, T., Okabe, S., Kanai, Y., and Hirokawa, N. (1993). Dynamics of microtubules bundled by microtubule-associated protein 2C (MAP2C). J. Cell Biol. 120, 451-465.
44. von Massow, A., Mandelkow, E.-M., and Mandelkow, E. (1989). Interaction between kinesin, microtubules, and microtubule-associated protein 2. Cell Motil Cytoskeleton 14, 562-571.