E-MAP-115 (ensconsin) associates dynamically with microtubules in vivo and is not a physiological modulator of microtubule dynamics

Journal of Cell Science

Volumn 112, Issue 23, 1999, Pages 4243-4255

  Faire, Kathleen ^a   Waterman Storer, Clare M ^b,c   Gruber, Dorota ^a   Masson, Danièle ^d   Salmon, E D ^b   Bulinski, J Chloë ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Carcinoma cell; Fluorescent speckle microscopy; Non motor MAP; Taxol

Indexed keywords

ENSCONSIN; GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL LINE; CHIMERA; CONTROLLED STUDY; DYNAMICS; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; MICROTUBULE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION;

BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE; DNA PRIMERS; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC INDEX; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; RECOMBINANT FUSION PROTEINS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0033489921     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. 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 microtubule organisation. J. Cell Biol. 126, 1017-1029.
2. Bré, M. H., Pepperkok, R., Hill, A. M., Levilliers, N., Ansorge, W., Stelzer, E. H. and Karsenti, E. (1990). Regulation of microtubule dynamics and nucleation during polarization in MDCK II cells. J. Cell Biol. 111, 3013-3021.
3. Bulinski, J. C. and Borisy, G. G. (1979). Self-assembly of Hela tubulin and the identification of HeLa microtubule-associated proteins. Proc. Nat. Acad. Sci. USA 76, 293-297.
4. Bulinski, J. C. and Borisy, G. G. (1980). Microtubule-associated proteins from cultured HeLa cells: Analysis of molecular properties and effects on microtubule polymerization. J. Biol. Chem. 255, 11570-11576.
5. Bulinski, J. C. and Bossler, A. (1994). Purification and characterization of ensconsin, a novel microtubule stabilizing protein. J. Cell Sci. 107, 2839-2849.
6. Bulinski, J. C., McGraw, T., Gruber, D., Nguyen, H. L. and Sheetz, M. P. (1997). Overexpression of MAP4 inhibits organelle motility in vivo. J. Cell Sci. 110, 3055-3064.
7. Bulinski, J. C., Gruber, D., Faire, K., Prasad, P. and Chang, W. (1999). GFP chimeras of E-MAP-115 (ensconsin) domains mimic behavior of the endogenous protein in vitro and in vivo. Cell Struct. Funct. (in press).
8. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. and Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805.
9. Chapin, S. and Bulinski, J. C. (1991a). Non-neuronal 210kD microtubule-associated protein (MAP4) contains a domain homologous to the microtubule-binding domains of neuronal MAP2 and tau. J. Cell Sci. 98, 27-36.
10. Chapin, S. J. and Bulinski, J. C. (1991b). Preparation and functional assay of tyrosinated and detyrosinated tubulin. Meth. Enzymol. 196, 254-264.
11. Chapin, S. and Bulinski, J. C. (1994). Cellular microtubules heterogeneous in their content of MAP4 (210Kd MAP). Cell Motil. Cytoskel. 27, 133-149.
12. Cormack, B. P., Valdivia, R. H. and Falkow, S. (1996). FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33-38.
13. Dickson, R. M., Cubitt, A. B., Tsien, R. Y. and Moerner, W. E. (1997). On/off blinking and switching behaviour of single molecules of green fluorescent protein. Nature 388, 355-358.
14. Doyle, T. and Botstein, D. (1996). Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc. Nat. Acad. Sci. USA 93, 3886-3891.
15. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E.-M. and Mandelkow, E. (1997). MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89, 297-308.
16. Ehrig, T., O'Kane, D. J. and Prendergast, F. G. (1995). Green fluorescent protein mutants with altered excitation spectra. FEBS Lett. 367, 163-166.
17. Fabré-Jonca, N., Allaman, J.-M., Radlgruber, G., Meda, P., Kiss, J. Z., French, L. E. and Masson, D. (1998). The distribution of murine 115-kDa epithelial MT-associated protein (E-MAP-115) during embryogenesis and in adult organs suggests a role in epithelial polarization and differentiation. Differentiation 63, 169-180.
18. Fabré-Jonca, N., Viard, I., French, L. E. and Masson, D. (1999). Upregulation and redistribution of E-MAP-115 (epithelial microtubule-associated protein of 115-kDa) in terminally differentiating keratinocytes is coincident with the formation of intercellular contacts. J. Invest. Dermatol. 112, 216-225.
19. mark. J. Biol. Chem. 271, 1-10.
20. 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.
21. Kaech, S., Ludin, B. and Matus, A. (1996). Cytoskeletal plasticity in cells expressing neuronal microtubule-associated proteins. Neuron 17, 1189-1199.
22. Liao, G., Nagasaki, T. and Gundersen, G. G. (1995). Low concentrations of nocodazole and taxol 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.
23. Ludueña, R. F. (1998). Multiple forms of tubulin: Different gene products and covalent modifications. Int. Rev. Cytol. 178, 207-275.
24. Ludin, B. and Matus, A. (1998). FFP illuminates the cytoskeleton. Trends Cell Biol. 8, 72-77.
25. Mandelkow, E. and Mandelkow, E. M. (1995). Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7, 72-81.
26. Marschall, L., Jeng, R. L., Mulholland, J. and Stearns, T. (1996) Analysis of Tub4p, a yeast γ-tubulin-like protein: Implications for microtubule-organizing center function. J. Cell Biol. 134, 443-454.
27. 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.
28. 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.
29. Matus, A. (1988). Microtubule-associated proteins: Their potential role in determining neuronal morphology. Annu. Rev. Neurosci. 11, 29-44.
30. Nguyen, H.-L., Chari, S., Gruber, D. Gruber, Lue, C.-M., Chapin, S. J. and Bulinski, J. C. (1997). Overexpression of full- or partial-length MAP4 stabilizes microtubules and alters cell growth. J. Cell Sci. 110, 281-294.
31. Nguyen, H. L., Gruber, D. and Bulinski, J. C. (1999). Microtubule-associated protein 4 (MAP4) regulates assembly, protomer-polymer partitioning and synthesis of tubulin in cultured cells. J. Cell Sci. 112, 1813-1824.
32. 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.
33. Pepperkok, R., Bre, M. H., Davoust, J. and Kreis, T. E. (1990). Microtubules are stabilized in confluent epithelial cells but not in fibroblasts. J. Cell Biol. 111, 3003-3012.
34. Perez, F., Diamantopoulos, G. S., Stalder, R. and Kreis, T. E. (1999). CLIP-170 highlights growing microtuhule ends in vivo. Cell 96, 517-527.
35. Salmon, E. D., Shaw, S. L. Waters, J., Waterman-Storer, C. M., Maddox, P. S., Yeh, E. and Bloom, K. (1998). Meth. Cell Biol. 56, 185-214.
36. Tanaka, E., Ho, T. and Kirschner, M. W. (1995). The role of microtubule dynamics in growth cone motility and axonal growth. J. Cell Biol. 128, 139-155.
37. Toso, R. J., Jordan, M. A., Farrell, K. W., Matsumoto, B. and Wilson, L. (1993). Kinetic stabilization of microtubule dynamic instability in vitro by vinblastine. Biochemistry 32, 1285-1293.
38. Walker, R. A., O'Brien, E. T., Pryer, N. K., Soboeiro, M. F., Voter, W. A., Erickson, H. P. and Salmon, E. D. (1988). Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J. Cell Biol. 107, 1437-1448.
39. Wang, X. M., Peloquin, J. J., Zhai, Y., Bulinski, J. C. and Borisy, G. G. (1996). Removal of MAP4 from microtubules: Removal of MAP4 from MTs in vivo produces no discernible phenotype at the cellular level. J. Cell Biol. 132, 349-358.
40. Waterman-Storer, C. M. and Salmon, E. D. (1997). Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J. Cell Biol. 139, 417-434.
41. Waterman-Storer, C. M. and Salmon, E. D. (1998a). How microtubules get fluorescent speckles. Biophys. J. 15, 2059-2069.
42. Waterman-Storer, C. M. and Salmon, E. D. (1998b). Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr. Biol. 8, 798-806.
43. Waterman-Storer, Desai, A., Bulinski, J. C. and Salmon E. D. (1998). Fluorescent speckle imaging: Visualizing the movement, assembly and turnover of macromolecular assemblies in living cells. Curr. Biol. 8, 227-230
44. Weatherbee, J. A., Luftig, R. B. and Weihing, R. R. (1980). Purification and reconstitution of HeLa microtubules. Biochemistry 19, 4116-4123.
45. Westphal, M., Jungbluth, A., Heidecker, M., Muhlbauer, B., Heizer, C., Schwartz, J.-M., Marriot, G. and Gerisch, G. (1997). Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr. Biol. 7, 176-183.