Tau interaction with microtubules in vivo

Journal of Cell Science

Volumn 117, Issue 25, 2004, Pages 6129-6141

  Samsonov, Andrey ^a   Yu, Jiang Zhou ^a   Rasenick, Mark ^a   Popov, Sergey V ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Axon; Microtubule; Photobleaching; Rigidity; Tau; Tubulin

Indexed keywords

GREEN FLUORESCENT PROTEIN; PACLITAXEL; TAU PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL LABELING; CONTROLLED STUDY; EMBRYO; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN CELL; IMAGING; IN VIVO STUDY; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; XENOPUS;

ANIMALS; AXONS; CYTOSKELETON; DETERGENTS; DNA; EMBRYO, NONMAMMALIAN; FIBROBLASTS; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; LIGHT; MICROSCOPY, FLUORESCENCE; MICROTUBULES; NEURONS; PACLITAXEL; PROTEIN BINDING; TAU PROTEINS; TIME FACTORS; XENOPUS;

ANIMALIA;

EID: 12344301460     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01531     Document Type: Article

References (64)

1. Al-Bassam, J., Ozer, R. S., Safer, D., Halpain, S. and Milligan, R. A. (2002). MAP2 and tau bind longitudinally along the outer ridges of microtubule protofilaments. J. Cell Biol. 157 1187-1196.
2. 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.
3. Baas, P. W., Ahmad, F. J., Pienkowski, T. P., Brown, A. and Black, M. M. (1993). Sites of microtubule stabilization for the axon. J. Neurosci. 13, 2177-2185.
4. Biernat, J., Mandelkow, E. M., Schroter, C., Lichtenberg-Kraag, B., Steiner, B., Berling, B., Meyer, H., Mercken, M., Vandermeeren, A., Goedert, M. 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 J. 11, 1593-1597.
5. Black, M. M., Slaughter, T., Moshiach, S., Obrocka, M. and Fischer, I. (1996). Tau is enriched on dynamic microtubules in the distal region of growing axons. J. Neurosci. 16, 3601-3619.
6. Brandt, R., Leger, J. and Lee, G. (1995). Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J. Cell Biol. 131, 1327-1340.
7. Bulinski, J. C., Odde, D. J., Howell, B. J., Salmon, T. D. and Waterman-Storer, C. M. (2001). Rapid dynamics of the microtubule binding of ensconsin in vivo. J. Cell Sci. 114, 3885-3897.
8. Caceres, A. and Kosik, K. S. (1990). Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
9. Chang, S., Rodionov, V. I., Borisy, G. G. and Popov, S. V. (1998). Transport and turnover of microtubules in frog neurons depend on the pattern of axonal growth. J. Neurosci. 18, 821-829.
10. Chang, S., Svitkina, T. M., Borisy, G. G. and Popov, S. V. (1999). Speckle microscopic evaluation of microtubule transport in growing nerve processes. Nat. Cell Biol. 1, 399-403.
11. Chen, J., Kanai, Y., Cowan, N. J. and Hirokawa, N. (1992). Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360, 674-677.
12. Cunningham, C. C., Leclerc, N., Flanagan, L. A., Lu, M., Janmey, P. A. and Kosik, K. S. (1997). Microtubule-associated protein 2c reorganizes both microtubules and microfilaments into distinct cytological structures in an actin-binding protein-280-deficient melanoma cell line. J. Cell Biol. 136, 845-857.
13. D'Souza, I., Poorkaj, P., Hong, M., Nochlin, D., Lee, V. M., Bird, T. D. and Schellenberg, G. D. (1999). Missense and silent tau gene mutations cause frontotemporal dementia with parkinsonism-chromosome 17 type, by affecting multiple alternative RNA splicing regulatory elements. Proc. Natl. Acad. Sci. USA 96, 5598-5603.
14. Dehmelt, L., Smart, F. M., Ozer, R. S. and Halpain, S. (2003). The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J. Neurosci. 23, 9479-9490.
15. Desai, A. and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
16. 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.
17. Drewes, G., Ebneth, A. and Mandelkow, E. M. (1998). MAPs, MARKs and microtubule dynamics. Trends Biochem. Sci. 23 307-311.
18. Ebneth, A., Godemann, R., Stamer, K., Illenberger, S., Trinczek, B. and Mandelkow, E. (1998). Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 143, 777-794.
19. Faire, K., Waterman-Storer, C. M., Gruber, D., Masson, D., Salmon, E. D. and Bulinski, J. C. (1999). E-MAP-115 (ensconsin) associates dynamically with microtubules in vivo and is not a physiological modulator of microtubule dynamics. J. Cell Sci. 112, 4243-4255.
20. Felgner, H., Frank, R. and Schliwa, M. (1996). Flexural rigidity of microtubules measured with the use of optical tweezers. J. Cell Sci. 109, 509-516.
21. Garcia, M. L. and Cleveland, D. W. (2001). Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 13, 41-48.
22. Gittes, F., Mickey, B., Nettleton, J. and Howard, J. (1993). Flexural rigidity of micrombules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120, 923-934.
23. 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.
24. Gustke, N., Trinczek, B., Biernat, J., Mandelkow, E. M. and Mandelkow, E. (1994). Domains of tau protein and interactions with microtubules. Biochemistry 33, 9511-9522.
25. Harada, A., Oguchi, K., Okabe, S., Kuno, J., Terada, S., Ohshima, T., Sato-Yoshitake, R., Takei, Y., Noda, T. and Hirokawa, N. (1994). Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369, 488-491.
26. Hasegawa, M., Smith, M. J., Iijima, M., Tabira, T. and Goedert, M. (1999). FTDP-17 mutations N279K and S305N in tau produce increased splicing of exon 10. FEBS Lett. 443, 93-96.
27. Heidary, G. and Fortini, M. E. (2001). Identification and characterization of the Drosophila tau homolog. Mech. Dev. 108, 171-178.
28. Hutton, M., Lendon, C. L., Rizzu, P., Baker, M., Froelich, S., Houlden, H., Pickering-Brown, S., Chakraverty, S., Isaacs, A., Grover, A. et al. (1998). Association of missense and 5′ -splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393 702-705.
29. Kabir, N., Schaefer, A. W., Nakhost, A., Sossin, W. S. and Forscher, P. (2001). Protein kinase C activation promotes microtubule advance in neuronal growth cones by increasing average microtubule growth lifetimes. J. Cell Biol. 152, 1033-1044.
30. Kaech, S., Ludin, B. and Matus, A. (1996). Cytoskeletal plasticity in cells expressing neuronal microtubule-associated proteins. Neuron 17, 1189-1199.
31. Kanai, Y., Chen, J. and Hirokawa, N. (1992). Microtubule bundling by tau proteins in vivo: analysis of functional domains. EMBO J. 11, 3953-3961.
32. Kar, S., Fan, J., Smith, M. J., Goedert, M. and Amos, L. A. (2003). Repeat motifs of tau bind to the insides of microtubules in the absence of taxol. EMBO J. 22, 70-77.
33. Kis, A., Kasas, S., Babic, B., Kulik, A. J., Benoit, W., Briggs, G. A., Schonenberger, C., Catsicas, S. and Forro, L. (2002). Nanomechanics of microtubules. Phys. Rev. Lett. 89, 248101.
34. 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.
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. Lee, V. M., Goedert, M. and Trojanowski, J. Q. (2001). Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24, 1121-1159.
37. Littauer, U. Z., Giveon, D., Thierauf, M., Ginzburg, I. and Ponstingl, H. (1986). Common and distinct tubulin binding sites for microtubule-associated proteins. Proc. Natl. Acad. Sci. USA 83, 7162-7166.
38. Makrides, V., Massie, M. R., Feinstein, S. C. and Lew, J. (2004). Evidence for two distinct binding sites for tau on microtubules. Proc. Natl. Acad. Sci. USA 101, 6746-6751.
39. Mandelkow, E. and Mandelkow, E. M. (1995). Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7 72-81.
40. Melki, R., Kerjan, P., Waller, J. P., Carlier, M. F. and Pantaloni, D. (1991). Interaction of microtubule-associated proteins with microtubules: yeast lysyl- and valyl-tRNA synthetases and tau 218-235 synthetic peptide as model systems. Biochemistry 30, 11536-11545.
41. Mercken, M., Fischer, I., Kosik, K. and Nixon, R. (1995). Three distinct axonal transport rates for tau, tubulin, and other microtubule-associated proteins: evidence for dynamic interactions of tau with microtubules in vivo. J. Neurosci. 15, 8259-8267.
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. Natl. Acad. Sci. USA 72, 2696-2700.
43. Nogales, E., Whittaker, M., Milligan, R. A. and Downing, K. H. (1999). High-resolution model of the microtubule. Cell 96, 79-88.
44. Olmsted, J. B., Stemple, D. L., Saxton, W. M., Neighbors, B. W. and McIntosh, J. R. (1989). Cell cycle-dependent changes in the dynamics of MAP 2 and MAP 4 in cultured cells. J. Cell Biol. 109 211-223.
45. Ozer, R. S. and Halpain, S. (2000). Phosphorylation-dependent localization of microtubule-associated protein MAP2c to the actin cytoskeleton. Mol. Biol. Cell 11, 3573-3587.
46. Peltier, A. C. and Russell, J. W. (2002). Recent advances in drug-induced neuropathies. Curr. Opin. Neurol. 15 633-638.
47. Popov, S., Brown, A. and Poo, M. M. (1993). Forward plasma membrane flow in growing nerve processes. Science 259, 244-246.
48. Rodionov, V. I., Lim, S. S., Gelfand, V. I. and Borisy, G. G. (1994). Microtubule dynamics in fish melanophores. J. Cell Biol. 126, 1455-1464.
49. Santarella, R. A., Skiniotis, G., Goldie, K. N., Tittmann, P., Gross, H., Mandelkow, E. M., Mandelkow, E. and Hoenger, A. (2004 . Surface-decoration of microtubules by human tau. J. Mol. Biol. 339, 539-553.
50. Scherson, T., Kreis, T. E., Schlessinger, J., Littauer, U. Z., Borisy, G. G. and Geiger, B. (1984). Dynamic interactions of fluorescently labeled microtubule-associated proteins in living cells. J. Cell Biol. 99, 425-434.
51. Shahani, N. and Brandt, R. (2002). Functions and malfunctions of the tau proteins. Cell Mol. Life Sci. 59, 1668-1680.
52. Shtil, A. A., Mandlekar, S., Yu, R., Walter, R. J., Hagen, K., Tan, T. H., Roninson, I. B. and Kong, A. N. (1999). Differential regulation of mitogen-activated protein kinases by microtubule-binding agents in human breast cancer cells. Oncogene 18, 377-384.
53. Sloboda, R. D. and Rosenbaum, J. L. (1979). Decoration and stabilization of intact, smooth-walled microtubules with microtubule-associated proteins. Biochemistry 18, 48-55.
54. Spillantini, M. G., Murrell, J. R., Goedert, M., Farlow, M. R., Klug, A. and Ghetti, B. (1998). Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl. Acad. Sci. USA 95, 7737-7741.
55. Spitzer, N. C. and Lamborghini, J. E. (1976). The development of the action potential mechanism of amphibian neurons isolated in culture. Proc. Natl. Acad. Sci. USA 73, 1641-1645.
56. Stamer, K., Vogel, R., Thies, E., Mandelkow, E. and Mandelkow, E. M. (2002). Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J. Cell Biol. 156, 1051-1063.
57. Takei, Y., Teng, J., Harada, A. and Hirokawa, N. (2000). Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J. Cell Biol. 150, 989-1000.
58. Tanaka, E. M. and Kirschner, M. W. (1991). Microtubule behavior in the growth cones of living neurons during axon elongation. J. Cell Biol. 115, 345-363.
59. Trinczek, B., Ebneth, A., Mandelkow, E. M. and Mandelkow, E. (1999). Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J. Cell Sci. 112, 2355-2367.
60. 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.
61. Waterman-Storer, C. M., Desai, A., Bulinski, J. C. and Salmon, E. D. (1998). Fluorescent speckle microscopy, a method to visualize the dynamics of protein assemblies in living cells. Curr. Biol. 8, 1227-1230.
62. Yu, J. Z., Kuret, J. and Rasenick, M. M. (2002). Transient expression of fluorescent tau proteins promotes process formation in PC12 cells: contributions of the tau C-terminus to this process. J. Neurosci. Res. 67, 625-633.
63. Yujiri, T., Fanger, G. R., Garrington, T. P., Schlesinger, T. K., Gibson, S. and Johnson, G. L. (1999). MEK kinase 1 (MEKK1) transduces c-Jun NH2-terminal kinase activation in response to changes in the microtubule cytoskeleton. J. Biol. Chem. 274, 12605-12610.
64. Zakharenko, S. and Popov, S. (1998). Dynamics of axonal microtubules regulate the topology of new membrane insertion into the growing neurites. J. Cell Biol. 143, 1077-1086.