Domains of neuronal microtubule-associated proteins and flexural rigidity of microtubules

Journal of Cell Biology

Volumn 138, Issue 5, 1997, Pages 1067-1075

  Felgner, Harald ^a   Frank, Rainer ^a   Biernat, Jacek ^b   Mandelkow, Eva Maria ^b   Mandelkow, Eckhard ^b   Ludin, Beat ^c   Matus, Andrew ^c   Schliwa, Manfred ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; MICROTUBULE ASSOCIATED PROTEIN 2; TAU PROTEIN;

ANIMAL TISSUE; ARTICLE; AXONEME; BINDING AFFINITY; DISSOCIATION CONSTANT; MICROTUBULE ASSEMBLY; MOLECULAR INTERACTION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SWINE;

ADSORPTION; ANIMALS; BRAIN; CHLAMYDOMONAS REINHARDTII; CLONING, MOLECULAR; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUTAGENESIS, SITE-DIRECTED; NEURONS; RECOMBINANT PROTEINS; REGRESSION ANALYSIS; SEQUENCE DELETION; SWINE; TAU PROTEINS;

ANIMALIA; SUS SCROFA;

EID: 0030955208     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.138.5.1067     Document Type: Article

References (71)

1. Bereiter-Hahn, J. 1978. A model for microtubular rigidity. Eur. J. Cell Biol. 17: 298-300.
2. Bernhardt, R., and A. Matus. 1984. Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: a difference between the dendritic and axonal cytoskeletons. J. Comp. Neurol. 226:203-221.
3. Biernat, J., E.-M. Mandelkow, C. Schröter, B. Lichtenberg-Kraag, B. Steiner, B. Berling, H.E. Meyer, M. Mercken, A. Vandermeeren, M. Goedert, et al. 1992. The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region. EMBO (Eur. Mol. Biol. Organ.) J. 11:1593-1597.
4. Biernat, J., N. Gustke, G. Drewes, E.-M. Mandelkow, and E. Mandelkow. 1993. Phosphorylation of serine 262 strongly reduces the binding of tau protein to microtubules: distinction between PHF-like immunoreactivity and microtubule binding. Neuron. 11:153-163.
5. Binder, L.I., A. Frankfurter, and L. Rebhun. 1985. The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101:1371-1378.
6. Black, M.M. 1987. Comparison of the effects of microtubule-associated protein 2 and tau on the packing density of in vitro assembled microtubules. Proc. Natl. Acad. Sci. USA. 84:7783-7787.
7. Brandt, R., and G. Lee. 1993. Functional organization of microtubule-associated protein tau: Identification of regions which affect microtubule growth, nucleation, and bundle formation in vitro. J. Biol. Chem. 268:3414-3419.
8. Bronstein, I.N. 1985. Taschenbuch der Mathematik. 22. Aufl. Harri Deutsch Verlag, Thun.
9. Brugg, B., and A. Matus. 1991. Phosphorylation determines the binding of microtubule-associated protein-2 (MAP2) to microtubules in living cells. J. Cell Biol. 114:735-743.
10. Butner, K.A., and M.W. Kirschner. 1991. Tau protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 115:717-730.
11. Caplow, M., R.L. Ruhlen, and J. Shanks. 1994. The free energy of hydrolysis of a microtubule-bound nucleotide triphosphate is near zero: all of the free energy for hydrolysis is stored in the microtubule lattice. J. Cell Biol. 127:779-788.
12. Cassimeris, L., N.K. Pryer, and E.D. Salmon. 1988. Real-time observation of microtubule dynamic instability in living cells. J. Cell Biol. 107:2223-2231.
13. r microtubule-associated protein (MAP4) contains a domain homologous to the microtubule-binding domains of neuronal MAP2 and tau. J. Cell Sci. 98:27-36.
14. Chen, J., Y. Kanai, N. Cowan, and N. Hirokawa. 1992. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature (Lond.). 360:674-677.
15. Coffey, R.L., and D.L. Purich. 1995. Non-cooperative binding of the MAP-2 microtubule-binding region to microtubules. J. Biol. Chem. 270:1035-1040.
16. Coffey, R.L., J.C. Joly, B.D. Cain, and D.L. Purich. 1994. Exploring the microtubule-binding region of bovine microtubule-associated protein-2 (MAP-2): cDNA sequencing, bacterial expression, and site-directed mutagenesis. Biochemistry. 33:13199-13207.
17. Doll, T., M. Meichsner, B.M. Riederer, P. Honegger, and A. Matus. 1993. An isoform of microtubule-associated protein-2 (MAP2) containing 4 repeats of the tubulin-binding motif. J. Cell. Sci. 106:633-640.
18. Drechsel, D.N., A.A. Hyman, M.H. Cobb, and M.W. Kirschner. 1992. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol. Biol. Cell. 3:1141-1154.
19. Drubin, D.G., and M.W. Kirschner. 1986. Tau protein function in living cells. J. Cell Biol. 103:2739-2746.
20. Drubin, D.G., S.C. Feinstein, E.M. Shooter, and M.W. Kirschner. 1985. Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J. Cell Biol. 101:1799-1807.
21. Dustin, P. 1984. Microtubules. Springer Verlag, Heidelberg, Germany. 482 pp.
22. Dye, R.B., S.P. Fink, and R.C. Williams. 1993. Taxol-induced flexibility of microtubules and its reversal by MAP2 and tau. J. Biol. Chem. 268:6847-6850.
23. Edson, K., B. Weisshaar, and A. Matus. 1993. Actin depolymerisation induces process formation in MAP2-transfected non-neuronal cells. Development (Camb.). 117:689-700.
24. Felgner, H., O. Müller, and M. Schliwa. 1995. Calibration of light forces in optical tweezers. Appl. Optics. 34:977-982.
25. Feigner, H., R. Frank, and M. Schliwa. 1996. Flexural rigidity of microtubules measured with the use of optical tweezers. J. Cell Sci. 109:509-516.
26. Ferhat, L., A. Bemard, L. Depouplana, Y. Benari, and M. Khrestchatisky. 1994. Structure, regional and developmental expression of rat MAP2d, a MAP2 splice variant encoding 4 microtubule-binding domains. Neurochem. Int. 25: 327-338.
27. Ferralli, J., T. Doll, and A. Matus. 1994. Sequence analysis of MAP2 function in living cells. J. Cell Sci. 107:3115-3125.
28. Garner, C.C., and A. Matus. 1988. Different forms of microtubule-associated protein 2 are encoded by separate mRNA transcripts. J. Cell Biol. 106:779-783.
29. Gittes, F., B. Mickey, J. Nettleton, and J. Howard. 1993. Flexural rigidity of microtubules and aclin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120:923-934.
30. Goedert, M., M. Spillantini, R. Jakes, D. Rutherford, and R.A. Crowther. 1989. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimers disease. Neuron. 3: 519-526.
31. Gustke, N., B. Trinczek, J. Biernat, E.-M. Mandelkow, and E. Mandelkow. 1994. Domains of tau protein and interactions with microtubules. Biochemistry. 33:9511-9522.
32. Himmler, A., D. Drechsel, M. Kirschner, and D. Martin. 1989. Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains. Mol. Cell. Biol. 9:1381-1388.
33. Hyams, J.S., and C.W. Lloyd. 1993. Microtubules. Wiley-Liss, New York. 1439 pp.
34. Illenberger, S., G. Drewes, B. Trinczek, J. Biernat, H.E. Meyer, J.B. Olmsted, E.M. Mandelkow, and E. Mandelkow. 1996. Phosphorylation of microtubule-associated proteins MAP2 and MAP4 by the protein kinase p110mark. Phosphorylation sites and regulation of microtubule dynamics. J. Biol. Chem. 271:10834-10843.
35. Kaech, S., B. Ludin, and A. Matus. 1996. Cytoskeletal plasticity in cells expressing neuronal microtubule-associated proteins. Neuron. 17:1189-1199.
36. Kanai, Y., R. Takemura, T. Oshima, H. Mori, Y. Ihara, M. Yanagisawa, T. Masaki, and N. Hirokawa. 1989. Expresion of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J. Cell Biol. 109:1173-1184.
37. King, S., T. Otter, and G.B. Witman. 1986. Purification and characterization of Chlamydomonas flagellar dyneins. Methods Enzymol. 123:291-306.
38. Kindler, S., B. Schulz, M. Goedert, and C.C. Garner. 1990. Molecular structure of microtubule-associated protein 2b and 2c from rat brain. J. Biol. Chem. 265:19679-19684.
39. Knops, J., K. Kosik, G. Lee, J. Pardee, L. Cohengould, and L. McConlogue. 1991. Overexpression of tau in a nonneuronal cell induces long cellular processes. J. Cell Biol. 114:725-733.
40. Kowalksi, R.J., and R.C. Williams. 1993. Microtubule-associated protein 2 alters dynamic properties of microtubule assembly and disassembly. J. Biol. Chem. 268:9847-9855.
41. Kurachi, M., M. Hoshi, and H. Tashiro. 1995. Buckling of a single microtubule by optical trapping forces: Direct measurement of microtubule rigidity. Cell Motil. Cytoskeleton. 30:221-228.
42. Kurz, J.C., and R.C. Williams. 1995. Microtubule-associated proteins and the flexibility of microtubules. Biochemistry. 34:13374-13380.
43. Lee, G., N. Cowan, and M. Kirschner. 1988. The primary structure and heterogeneity of tau protein from mouse brain. Science (Wash. DC). 239:285-288.
44. Lewis, S.A., D. Wang, and N.J. Cowan. 1988. Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science (Wash. DC). 242:936-939.
45. Lewis, S.A., I.E. Ivanov, G.H. Lee, and N.J. Cowan. 1989. Organization of microtubules in dendrites and axons is determined by a short hydrophobia zipper in microtubule-associated protein 2 and tau. Nature (Lond.). 342:498-505.
46. Ludin, B., U. Fünfschilling, K. Ashbridge, and A. Matus. 1996. Functional analysis of the MAP2 repeat domain. J. Cell Sci. 109:91-99.
47. Mandelkow, E., and E.-M. Mandelkow. 1995. Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7:72-81.
48. Mandelkow, E.-M., M. Herrmann, and U. Rühl. 1985. Tubulin domains probed by subunit-specific antibodies and limited proteolysis. J. Mol. Biol. 185:311-327.
49. Mandelkow, E.-M., G. Drewes, J. Biernat, N. Gustke, J. Van Lint, J.R. Vandenheede, and E. Mandelkow. 1992. Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett. 314:315-321.
50. Mandelkow, E.-M., E. Mandelkow, and R.A. Milligan. 1991. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopic study. J. Cell Biol. 114:977-991.
51. Matus, A. 1994. Stiff microtubules and neuronal morphology. Trends Neurosci. 17:19-22.
52. Mickey, B., and J. Howard. 1995. Rigidity of microtubules is increased by stabilizing agents. J. Cell Biol. 130:909-917.
53. Murphy, D.B., and G.G. Borisy. 1975. Association of high molecular weight proteins with microtubules and their role in microtubule assembly in vitro. Proc. Natl. Acad. Sci. USA. 72:2696-2700.
54. Olmsted, J.B. 1991. Non-motor microtubule-associated proteins. Curr. Opin. Cell. Biol. 3:52-58.
55. Olmsted, J.B., D. Stemple, W. Saxton, B. Neighbors, and J.R. McIntosh. 1989. Cell cycle-dependent changes in the dynamics of MAP2 and MAP4 in cultured cells. J. Cell Biol. 109:211-223.
56. Sammak, P.J., and G.G. Borisy. 1988. Direct observation of microtubule dynamics in living cells. Nature (Lond.). 332:724-726.
57. Schoenfeld, T.A., and R.A. Obar. 1994. Diverse distribution and function of fibrous microtubule-associated proteins in the nervous system. Int. Rev. Cytol. 151:67-137.
58. Schweers, O., E. Schönbrunn-Hanebeck, A. Marx, and E. Mandelkow. Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-slructure. J. Biol. Chem. 269:24290-24297.
59. Shelanski, M.L., F. Gaskin, and C.R. Cantor. 1973. Microtubule assembly in the absence of added nucleotides. Proc. Natl. Acad. Sci. USA. 70:765-768.
60. Sloboda, R.D., and J.L. Rosenbaum. 1979. Decoration and stabilization of intact, smooth-walled microtubules with microtubule-associated proteins. Biochemistry. 18:48-55.
61. Sontag, E., V. Nunbhakdicraig, G.S. Bloom, and M.C. Mumby. 1995. A novel pool of protein phosphatase 2a is associated with microtubules and is regulated during the cell cycle. J. Cell Biol. 128:1131-1144.
62. Stearns, M.E., and D.L. Brown. 1979. Purification of a microtubule-associated protein based on its preferential association with tubulin during microtubule initiation. FEBS Lett. 101:15-21.
63. Takemura, R., S. Okabe, T. Umeyama, Y. Kanai, N.J. Cowan, and N. Hirokawa. 1992. Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP 1 B, MAP2 or tau. J, Cell Sci. 103:953-964.
64. Trinczek, B., J. Biernat, K. Baumann, E.-M. Mandelkow, and E. Mandelkow. 1995. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol. Biol. Cell. 6:1887-1902.
65. Tucker, R.P., L.I. Binder, and A.I. Matus. 1988. Neuronal microtubule-associated proteins in the embryonic avian spinal cord. J. Comp. Neurol. 271:44-55.
66. Venier, P., A.C. Maggs, M.F. Carlier, and D. Pantaloni. 1994b. Analysis of microtubule rigidity using hydrodynamic flow and thermal fluctuations [published erratum appears in J. Biol. Chem. 270:17056]. J. Biol. Chem. 269: 13353-13360.
67. Verde, F., J.M. Berrez, C. Antony, and E. Karsenti. 1991. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112:1177-1187.
68. Wallis, K.T., S. Azhar, M.B. Rho, S.A. Lewis, N.J. Cowan, and D.B. Murphy. 1993. The mechanism of equilibrium binding of microtubule-associated protein 2 to microtubules. Binding is a multiphasic process and exhibits positive cooperativity. J. Biol. Chem. 268:15158-15167.
69. Weisshaar, B., T. Doll, and A. Matus. 1992. Reorganization of the microtubular cytoskeleton by embryonic microtubule-associated protein 2 (MAP2c). Development (Camb.). 116:1151-1161.
70. West, R.R., K.M. Tenbarge, and J.B. Olmsted. 1991. A model for microtubule-associated protein-4 structure; domains defined by comparisons of human, mouse, and bovine sequences. J. Biol. Chem. 266:21886-21896.
71. Witman, G.B. 1986. Isolation of Chlamydomonas flagella and flagellar axonemes. Methods Enzymol. 123:280-290.