Microtubule-associated protein 4 (MAP4) regulates assembly, protomer-polymer partitioning and synthesis of tubulin in cultured cells

Journal of Cell Science

Volumn 112, Issue 12, 1999, Pages 1813-1824

  Nguyen, H Lan ^a   Gruber, D ^a   Bulinski, J Chloë ^a  

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

Author keywords

Autoregulation; Cell morphology; Microtubule polymerization; MT nucleation; MTOC; Tubulin monomer

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 4; TUBULIN;

ARTICLE; AUTOREGULATION; CELL SHAPE; CELL SPREADING; CELL STRUCTURE; CENTROSOME; CONTROLLED STUDY; DEPOLYMERIZATION; HELA CELL; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

BIOPOLYMERS; HELA CELLS; HOMEOSTASIS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TUBULIN;

EID: 0032813799     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (53)

1. Aizawa, H., Murofushi, H., Kotani, S., Hisanaga, S.-I., Hirokawa, N. and Sakai, H. (1987). Limited chymotryptic digestion of bovine adrenal 190.000-Mr microtubule-associated protein and preparation of a 27,000-Mr fragment which stimulates microtubule assembly. J. Biol. Chem. 262, 3782-3787.
2. Aizawa, H., Emori, Y., Mori, A., Mirofushi, H., Sakai, H. and Suzuki, K. (1991). Functional analysis of the domain structure of MT-associated protein 4 (MAPU). J. Biol. Chem. 266, 9841-9846.
3. 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.
4. Belt, P. G. B. M., Groeneveld, H., Teubel, W. J., van de Putte, P. and Backendarf, C. (1989). Construction and properties of an Epstein-Barr-virus-derived cDNA expression vector for human cells. Gene 84, 407-417.
5. Ben-Ze'ev, A., Farmer, S. R. and Penman, S. (1979). Mechanisms of regulating tubulin synthesis in cultured mammalian cells. Cell 17, 319-325.
6. Bré, M.-H., Kreis, T. E. and Karsenti, E. (1987). Control of MT nucleation and stability in Madin-Darby canine kidney cells: the occurrence of noncentrosomal, stable MTs. J. Cell Biol. 105, 1283-1296.
7. Bulinski, J. C. (1994). MAP 4. In Microtubules (ed. J. Hyams and C. W. Lloyd), pp. 167-182. New York: Wiley & Sons.
8. Bulinski, J. C. and Borisy, G. G. (1979). Self-assembly of HeLa tubulin and the identification of HeLa microtubule-associated proteins. Proc. Natl. Acad. Sci. USA 76, 293-297.
9. Bulinski, J. C. and Borisy, G. G. (1980a). Microtubule-associated proteins from cultured HeLa cells: Analysis of molecular properties and effects on MT 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 Bossier, A. B. (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. Cachianes, G., Ho, C., Weber, R. F., Williams, S. R., Goeddel, D. V. and Leung, D. W. (1993). Epstein-Barr virus-derived vectors for transient and stable expression of recombinant proteins. BioTechniques 15, 255-258.
14. Caron, J. M., Jones, A. L., Ball, L. B. and Kirschner, M. W. (1985). Autoregulation of tubulin synthesis in enucleated cells. Nature 317, 648-651.
15. Chapin, S. and Bulinski, J. C. (1991a). Non-neuronal 210 kD MT-associated protein (MAP4) contains a domain homologous to the MT-binding domains of MAP2 and tau. J. Cell Sci. 98, 27-36.
16. Chapin, S. J. and Bulinski, J. C. (1991b). Preparation and functional assay of tyrosinated and detyrosinated tubulin. Meth. Enzymol. 196, 254-264.
17. 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 MT-binding domains. Biochemistry 34, 2289-2301.
18. Cleveland, D. W., Lopata, M. A., Sherline, P. and Kirschner, M. W. (1981). Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 25, 537-546.
19. Cleveland, D. W. and Theodorakis, N. G. (1994). Regulation of tubulin synthesis. In Microtubules (ed. J. Hyams and C. W. Lloyd), pp. 47-58. New York: Wiley & Sons.
20. 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.
21. Elinson, R. P. (1983). Cytoplasmic phases in the first cell cycle of the activated frog egg. Dev. Biol. 100, 440-450.
22. Elinson, R. P. (1985). Changes in the levels of polymeric tubulin associated with activation and dorsoventral polarization of the frog egg. Dev. Biol. 109, 224-233.
23. Esmaeli-Azad, B., McCarty, J. H. and Feinstein, S. C. (1994). Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107, 869-879.
24. Faruki, S. and Karsenti, E. (1994). Purification of microtubule proteins from Xenopus egg extracts: identification of a 230K MAP4-like protein. Cell Motil. Cytoskel. 28, 108-118.
25. Goedert, M., Baur, C. P., Ahringer, J., Jakes, R., Hasegawa, M., Spillantini, M. G., Smith, M. J. and Hill, F. (1996). PTL-1 a microtubule associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J. Cell Sci. 109, 2661-2672.
26. Gundersen, G. G., Khawaja, S. and Bulinski, J. C. (1987) Post-polymerization detyrosination of alpha tubulin: A mechanism for subcellular differentiation of microtubules. J. Cell Biol. 105, 251-264.
27. Harada, A., Oguchi, K., Okabe, S., Kuno, J., Terada, S., Ohshima, T., Sato-Yoshitake, R., Takei, Y., Noda, T. and Hirokawa, N. (1994). Altered MT organization in small-calibre axons of mice lacking tau protein. Nature 369, 488-491.
28. Huber, G. and Matus, A. (1990). MT-associated protein 3 (MAP3) expression in non-neuronal tissues. J. Cell Sci. 95, 237-246.
29. Itoh, T. J. and Hotani, H. (1994). MT-stabilizing activity of MT-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. Kroczek, R. A. and Siebert, E. (1990). Optimization of northern analysis by vacuum-blotting, RNA-transfer visualization and ultraviolet fixation. Anal. Biochem. 184, 90-5.
31. Mandelkow, E. and Mandelkow, E. M. (1995). Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7, 72-81.
32. 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.
33. Masson, D. and Kreis, T. E. (1993). Identification and molecular characterization of E-MAP-115, a novel microtubule-associated protein predominantly expressed in epithelial cells. J. Cell Biol. 123, 357-371.
34. McDermott, J. B., Aamodt, S. and Aamodt, E. (1996). ptl-1, a Caenorhabditis elegans gene whose products are homologous to the tau microtubule-associated proteins. Biochemistry 35, 9415-23.
35. Mitchison, T. J. and Kirschner, M. W. (1984). Dynamic instability in MT growth. Nature 312, 237-242.
36. Nguyen, H. L., Chari, S, Lue, C.-M., Gruber, D., Chapin, S. and Bulinski, J. C. (1997). Overexpression of full-or partial-length MAP4 stabilizes MTs and alters cell growth. J. Cell Sci. 110, 281-294.
37. 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.
38. Oosawa, F. and Asakura, S. (1975). Thermodynamics of the Polymerisation of Protein. London: Acadmemic Press.
39. Parysek, L. M., Asnes, C. F. and Olmsted, J. B. (1984). MAP4: occurrence in mouse tissues. J. Cell Biol. 99, 1309-1315.
40. Pittenger, M. F. and Cleveland, D. W. (1985). Retention of autoregulatory control of tubulin synthesis in cytoplasts: Demonstration of a cytoplasmic mechanism that regulates the level of tubulin expression. J. Cell Biol. 101, 1941-1952.
41. Quesada, P. Merola, M., Farina, B. and Leone, E. (1990). In vitro inhibition of HeLa cell nuclear ribonucleases by ADP ribosylation. Mol. Cell. Biochem. 94, 53-60.
42. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edition. New York: Cold Spring Harbor Laboratory Press.
43. Scharf, S. R. and Gerhart, J. C. (1983). Axis determination in eggs of Xenopus laevis: A critical period before first cleavage, identified by the common effects of cold, pressure and UV-irradiation. Dev. Biol. 99, 75-87.
44. Sato, H., Nagai, T., Kuppuswamy, D., Narishige, T., Koide, M. and Menick, D. R. (1997). Microtubule stabilization in pressure overload cardiac hypertrophy. J. Cell Biol. 139, 1-11.
45. Timasheff and Grisham, L. M. (1980). In vitro assembly of cytoplasmic microtubules. Ann. Rev. Biochem. 49, 565-591.
46. Tsutsui, H., Ishihara, K. and Cooper, G. (1993). Cytoskeletal role in the contractile dysfunction of hypertrophied myocardium. Science 260, 682-687.
47. Tsutsui, H., Tagawa, H., Kent, R. L., McCollam, P. L., Ishihara, K., Nagatsu, M. and Cooper, G. (1994). Role of microtubules in contractile dysfunction of hypertrophied cardiocytes. Circulation 90, 533-555.
48. Vorobjev, I. A., Svitkina, T. M. and Borisy, G. G. (1997). Cytoplasmic assembly of microtubules in cultured cells. J. Cell Sci. 110, 2635-45.
49. Walker, R. A., O'Brien, E. T., Pryer, N. K., Soboeiro, N. F., Voter, W. A., Erickson, H. P. and Salmon, E. D. (1988). Dynamic instability of individual microtubules: Rate constants and transition frequencies. J. Cell Biol. 107, 1437-1448.
50. Wang, X. M., Peloquin, J. J., Zhai, Y., Bulinski, J. C. and Borisy, G. G. (1996). Removal of MAP4 from MTs in vivo produces no discernible phenotype at the cellular level. J. Cell Biol. 132, 349-358.
51. West, R. R., Tenbarge, K. M. and Olmsted, J. B. (1991). A model for MT-associated protein 4 structure. J. Biol. Chem. 266, 21886-21896.
52. 2 cells. Cell Motil. Cytoskel. 33, 252-262.
53. Yvon, A. M. and Wadsworth, P. (1997). Non-centrosomal microtubule formation and measurement of minus end microtubule dynamics in A498 cells. J. Cell Sci. 110, 2391-2401.