Overexpression of full- or partial-length MAP4 stabilizes microtubules and alters cell growth

Journal of Cell Science

Volumn 110, Issue 2, 1997, Pages 281-294

  Nguyen, Hoang Lan ^a   Chari, Sripriya ^a   Gruber, Dorota ^a   Lue, Chia Man ^a   Chapin, Steven J ^a,b   Bulinski, Jeannette Chloë ^a  

^a College of Physicians and Surgeons ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell cycle; Dexamethasone; Drug resistance; Inducible expression; Nocodazole; Stable microtubule

Indexed keywords

ALPHA TUBULIN; MICROTUBULE ASSOCIATED PROTEIN 4; NOCODAZOLE; PACLITAXEL;

ARTICLE; CELL GROWTH; CELL ORGANELLE; CONTROLLED STUDY; GROWTH INHIBITION; HUMAN; HUMAN CELL; MICROTUBULE; PRIORITY JOURNAL;

ANIMALS; CELL DIVISION; GENE EXPRESSION; HUMANS; L CELLS (CELL LINE); MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NOCODAZOLE; TRANSFECTION;

VERTEBRATA;

EID: 0031056220     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. r fragment which stimulates microtubule assembly. J. Biol. Chem. 262, 3782-3787.
2. r 190,000. J. Biol. Chem. 265, 13849-13855.
3. Aizawa, H., Emori, Y., Mori, A., Murofushi, H., Sakai, H. and Suzuki, K. (1991). Functional analysis of the domain structure of microtubule-associated protein 4 (MAPU). J. Biol. Chem. 266, 9841-9846.
4. Andersen, S. S., Bendia, B., Dominguez, J. E., Sawyer, A. and Karsenti, E. (1994). Effect on microtubule dynamics of XMAP230, a microtubule-associated protein present in Xenopus laevis eggs and dividing cells [published erratum appears in J. Cell Biol. 128 (1995) following p. 988]. J. Cell Biol. 127, 1289-1299.
5. Baas, P. W. and Black, M. M. (1990). Individual microtubules in the axon consist of domains that differ in both composition and stability. J. Cell Biol. 111, 495-509.
6. Barlow, S., Gonzalez-Garay, M. L., West, R. R., Olmsted, J. B. and Cabral, F. (1994). Stable expression of heterologous microtubule-associated proteins (MAPs) in Chinese hamster ovary cells: Evidence for differing roles of MAPs in MT organization. J. Cell Biol. 126, 1017-1030.
7. Belmont, L. D., Hyman, A. A., Sawin, K. E. and Mitchison, T. J. (1990). Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62, 579-589.
8. 396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099.
9. Bulinski, J. C. and Borisy, G. G. (1980a). Microtubule-associated proteins from cultured HeLa cells: Analysis of molecular properties and effects on microtubule polymerization. J. Biol. Chem. 255, 11570-11576.
10. Bulinski, J. C. and Borisy, G. G. (1980b). Widespread distribution of a 210,000 mol wt microtubule-associated protein in cells and tissues of primates. J. Cell Biol. 87, 802-808.
11. Bulinski, J. C. and Bossler, A. (1994). Purification and characterization of ensconsin, a novel microtubule stabilizing protein. J. Cell Sci. 107, 2839-2849.
12. Caceres, A. and Kosik, K. S. (1990). Inhibition of neurite polarity by antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
13. Chapin, S. and Bulinski, J. C. (1991). Non-neuronal 210 kDa microtubule-associated protein (MAP4) contains a domain homologous to the microtubule-binding domains of MAP2 and tau. J. Cell Sci. 98, 27-36.
14. Chapin, S. and Bulinski, J. C. (1992). Microtubule stabilization by assembly promoting microtubule-associated proteins: A repeat performance. Cell Motil. Cytoskel. 4, 236-243.
15. Chapin, S. and Bulinski, J. C. (1994). Cellular microtubules heterogeneous in their content of MAP4 (210 Kd MAP). Cell Motil. Cytoskel. 27, 133-149.
16. Chapin, S., Lue, C.-M., Yu, M. T. and Bulinski, J. C. (1995). Differential expression of alternatively spliced forms of MAP4: A repertoire of structurally different microtubule-binding domains. Biochemistry 34, 2289-2301.
17. Cleveland, D. W., Hwo, S.-Y. and Kirschner, M. W. (1977). Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J. Mol. Biol. 116, 227-247.
18. Crossin K. L. and Carney, D. H. (1981). Microtubule stabilization by Taxol inhibits initiation of DNA synthesis by thrombin and by epidermal growth factor. Cell 27, 341-350.
19. Dinsmore, J. H. and Solomon F. (1991). Inhibition of MAP2 expression affects both morphological and cell division phenotypes of neuronal differentiation. Cell 64, 817-826.
20. Dolbeare, F. and Selden, J. R. (1994). Immunochemical quantitation of bromodeoxyuridine: Application to cell-cycle kinetics. Meth. Cell. Biol. 41, 297-316.
21. Doll, T., Meichsner, M., Riederer, B. M., Honegger, P. and Matus, A. (1993). An isoform of microtubule-associated protein 2 (MAP2) containing four repeats of the tubulin-binding motif. J. Cell Sci. 106, 633-640.
22. Ferralli, J., Doll, T. and Matus, A. (1994). Sequence analysis of MAP2 function in living cells. J. Cell Sci. 107, 3115-3125.
23. Goedert, M. and Jakes, R. (1990). Expression of separate isoforms of tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J. 9, 4225-4230.
24. Graham, F. L. and van der Eb, A. J. (1973). A new technique for the assay of infectivity of human adenovirus DNA. Virology 52, 456-461.
25. Gundersen, G. G., Khawaja, S. and Bulinski, J. C. (1987). Postpolymerization detyrosination of alpha tubulin: a mechanism for subcellular differentiation of microtubules. J. Cell Biol. 105, 251-264.
26. Gundersen, G. G., Khawaja, S. and Bulinski, J. C. (1989). Generation of a stable, posttranslationally modified microtubule array is an early event in myogenic differentiation. J. Cell Biol. 109, 2275-2288.
27. Hall, C. V., Jacob, P. E., Ringold, G. M. and Lee, F. (1983). Expression and regulation of Escherichia coli LacZ gene fusions in mammalian cells. J. Mol. Appl. Gen. 2, 101-109.
28. Hwang, S. and Ding, A. (1995) Activation of NF-kappa B in murine macrophages by Taxol. Cancer Biochem. Biophys. 14, 465-472.
29. Itoh, T. J. and Hotani, H. (1994). Microtubule-stabilizing activity of microtubule-associated proteins (MAPs) is due to increase in frequency of rescue in dynamic instability: shortening length decreases with binding of MAPs onto microtubules. Cell Struct. Funct. 19, 279-290.
30. Jordan, M. A., Thrower, D. and Wilson, L. (1992). Effects of vinblastine, podophyllotoxin, and nocodazole on mitotic spindles: Implications for the role of microtubule dynamics in mitosis. J. Cell Sci. 102, 401-416.
31. Jordan, M. A., Toso, R. J., Thrower, D. and Wilson, L. (1993). Mechanism of mitotic block and inhibition of cell proliferation by Taxol at low concentrations. Proc. Nat. Acad. Sci. USA 90, 9552-9556.
32. Kanai, Y., Takemura, R., Oshima, T., Mori, H., Ihara, Y., Yanangisawa, M., Masaki, T. and Hirokawa, N. (1989). Expression of multiple isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J. Cell Biol. 109, 1173-1184.
33. Khawaja, S., Gundersen, G. G. and Bulinski, J. C. (1988). Enhanced stability of microtubules enriched in detyrosinated tubulin is not a direct function of detyrosination level. J. Cell Biol. 106, 141-149.
34. Liao, G., Nagasaki, T. and Gundersen, G. G. (1995). Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: Implications for the role of dynamic microtubules in cell locomotion. J. Cell Sci. 108, 3473-3483.
35. Lee, G. and Rook, S. L. (1992). Expression of tau protein in non-neuronal cells: microtubule binding and stabilization. J. Cell Sci. 102, 227-237.
36. Lewis, S. A., Ivanov, I. F., Lee, G. H. and Cowan, N. J. (1989). Organization of microtubules in dendrites and axons is determined by a short hydrophobic zipper in microtubule-associated proteins MAP2 and tau [correction appears in Nature (1990) 345, 674]. Nature 342, 498-505.
37. Mangan, M. E. and Olmsted, J. B. (1996). A muscle-specific variant of microtubule-associated protein 4 (MAP4) is required in myogenesis. Development 122, 771-781.
38. Masson, D. and Kreis, T. E. (1995). Binding of E-MAP-115 to microtubules is regulated by cell cycle-dependent phosphorylation. J. Cell Biol. 131, 1015-1024.
39. Meuth, M. and Greene, H. (1974). Induction of deoxydytidineless state in cultured mammalian cells by bromodeoxyuridine. Cell 2, 109-112.
40. Mitchison, T. J. and Kirschner, M. W. (1984). Dynamic instability in microtubule growth. Nature 312, 237-242.
41. Murofushi, H., Kotani, S., Aizawa, H., Hisanaga, S., Hirokawa, N. and Sakai, H. (1986). Purification and characterization of a 190-kD microtubule-associated protein from bovine adrenal cortex. J. Cell Biol. 103, 1911-1919.
42. Murphy, D. B. and Borisy, G. G. (1975). Association of high molecular weight proteins with microtubules and their role in microtubule assembly in vitro. Proc. Nat. Acad. Sci. USA 72, 2696-2700.
43. Nakata, T. and Hirokawa, N. (1995). Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J. Cell Biol. 131, 1039-1053.
44. Olsen, K. R., McIntosh, J. R. and Olmsted, J. B. (1995). Analysis of MAP4 function in living cells using green fluorescent protein (GFP) chimeras. J. Cell Biol. 130, 639-650.
45. cdc2 kinase to microtubules and is a potential regulator of M-phase microtubule dynamics. J. Cell Biol. 128, 849-862.
46. Otey, C. A., Kalnoski, M. H., Lessard, J. L. and Bulinski, J. C. (1986). Immunolocalization of the gamma isoform of nonmuscle actin in cultured cells. J. Cell Biol. 102, 1726-1737.
47. Parysek, L. M., Asnes, C. F. and Olmsted, J. B. (1984). MAP4: Occurrence in mouse tissues. J. Cell Biol. 99, 1309-1315.
48. Pereira, A., Doshen, E., Tanaka, E. and Goldstein, L. S. B. (1992). Genetic analysis of a Drosophila microtubule-associated protein. J. Cell Biol. 116, 377-383.
49. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. 2nd edn. New York: Cold Spring Harbor Laboratory Press.
50. Saxton, W. M., Stemple, D. L., Leslie, R. J., Salmon, E. D., Zavortink, M. and McIntosh, J. R. (1984). Tubulin dynamics in cultured mammalian cells. J. Cell Biol. 99, 2175-2186.
51. Shiina, N., Moriguichi, T., Ohta, K., Gotoh, Y. and Nishida E. (1992). Regulation of a major microtubule-associated protein by MPF and MAP kinase. EMBO J. 11, 3977-3984.
52. Studier, F. W., Rosenberg, A. W., Dunn, J. J. and Dubendorff, J. W. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Meth. Enzymol. 185, 60-89.
53. Tombes, R. M., Peloquin, J. G. and Borisy, G. G. (1991). Specific association of an M-phase kinase with isolated mitotic spindles and identification of two of its substrates as MAP4 and MAP1B. Cell Regul. 2, 861-874.
54. Vandré, D. D., Centonze, V. E., Peloquin, J., Tombes, R. M. and Borisy, G. G. (1991). Proteins of the mammalian mitotic spindle: phosphorylation/dephosphorylation of MAP4 during mitosis. J. Cell Sci. 98, 577-588.
55. Verde, F., Labbé, J. C., Dorée, M. and Karsenti, E. (1990). Regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs. Nature 343, 233-238.
56. Wang, Z.-W. and Rozengurt, E. (1983). Interplay of cyclic AMP and microtubules in modulating the initiation of DNA synthesis in 3T3 cells. J. Cell Biol. 96, 1743-1750.
57. Wang, X. M., Peloquin, J. G., Zhai, Y., Bulinski, J. C. and Borisy, G. G. (1996). Removal of MAP4 from microtubules in vivo produces no discernible phenotype at the cellular level. J. Cell Biol. 132, 349-358.
58. Wehland, J. and Weber, K. (1987). Turnover of the carboxy-terminal tyrosine of alpha-tubulin and means of reaching elevated levels of detyrosination in living cells. J. Cell Sci. 88, 185-203.
59. West, R. R., Tenbarge, K. M. and Olmsted, J. B. (1991). A model for microtubule-associated protein 4 structure. J. Biol. Chem. 266, 21886-21896.
60. 2 cells. Cell Motil. Cytoskel. 33, 252-262.
61. Zhai, Y. and Borisy G. G. (1994). Quantitative determination of the proportion of microtubule polymer present during the mitosis-interphase transition. J. Cell Sci. 107, 881-890.