EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration (original) (raw)

References

  1. Gundersen, G.G. & Bulinski, J.C. Microtubule arrays in differentiated cells contain elevated levels of a post-translationally modified form of tubulin. Eur. J. Cell Biol. 42, 288–294 (1986).
    CAS PubMed Google Scholar
  2. Gundersen, G.G. & Bulinski, J.C. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc. Natl Acad. Sci. USA 85, 5946–5950 (1988).
    Article CAS Google Scholar
  3. Gundersen, G.G., Khawaja, S. & Bulinski, J.C. Generation of a stable, posttranslationally modified microtubule array is an early event in myogenic differentiation. J. Cell. Biol. 109, 2275–2288 (1989).
    Article CAS Google Scholar
  4. Cook, T.A., Nagasaki, T. & Gundersen, G.G. Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J. Cell Biol. 141, 175–185 (1998).
    Article CAS Google Scholar
  5. Palazzo, A.F., Cook, T.A., Alberts, A.S. & Gundersen, G.G. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nature Cell Biol. 3, 723–729 (2001).
    Article CAS Google Scholar
  6. Palazzo, A.F., Eng, C.H., Schlaepfer, D.D., Marcantonio, E.E. & Gundersen, G.G. Localized stabilization of miicrotubules by integrin and FAK facilitated Rho signaling. Science 303, 836–839 (2004).
    Article CAS Google Scholar
  7. Webster, D.R., Gundersen, G.G., Bulinski, J.C. & Borisy, G.G. Differential turnover of tyrosinated and detyrosinated microtubules. Proc. Natl Acad. Sci. USA 84, 9040–9044 (1987).
    Article CAS Google Scholar
  8. Infante, A.S., Stein, M.S., Zhai, Y., Borisy, G.G. & Gundersen, G.G. Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap. J. Cell Sci. 113, 3907–3919 (2000).
    CAS PubMed Google Scholar
  9. Westermann, S. & Weber, K. Post-translational modifications regulate microtubule function. Nature Rev. Mol. Cell Biol. 4, 938–947 (2003).
    Article CAS Google Scholar
  10. Gundersen, G.G., Kalnoski, M.H. & Bulinski, J.C. Distinct populations of microtubules: tyrosinated and nontyrosinated α-tubulin are distributed differently in vivo. Cell 38, 779–789 (1984).
    Article CAS Google Scholar
  11. Liao, G. & Gundersen, G.G. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273, 9797–9803 (1998).
    Article CAS Google Scholar
  12. Lin, S.X., Gundersen, G.G. & Maxfield, F.R. Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol. Biol. Cell 13, 96–109 (2002).
    Article CAS Google Scholar
  13. Gurland, G. & Gundersen, G.G. Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J. Cell Biol. 131, 1275–1290 (1995).
    Article CAS Google Scholar
  14. Kreitzer, G., Liao, G. & Gundersen, G.G. Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism. Mol. Biol. Cell 10, 1105–1118 (1999).
    Article CAS Google Scholar
  15. Schuyler, S.C. & Pellman, D. Microtubule “plus-end-tracking proteins”: The end is just the beginning. Cell 105, 421–424 (2001).
    Article CAS Google Scholar
  16. Kohno, H., Tanaka, K., Mino, A., Umikawa, M. & Takai, Y. Bni1 implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in S. cerevisiae. EMBO J. 15, 6060–6068 (1996).
    Article CAS Google Scholar
  17. Lee, L., Klee, S.K., Evangelista, M., Boone, C. & Pellman, D. Control of mitotic spindle position by the Saccharomyces cerevisiae Formin Bni1p. J. Cell Biol. 144, 947–961 (1999).
    Article CAS Google Scholar
  18. Adames, N.R. & Cooper, J.A. Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae. J. Cell Biol. 149, 863–874 (2000).
    Article CAS Google Scholar
  19. Bloom, K. It's a kar9ochore to capture microtubules. Nature Cell Biol. 2, E96–E98 (2000).
    Article CAS Google Scholar
  20. Schuyler, S.C. & Pellman, D. Search, capture and signal: games microtubules and centrosomes play. J. Cell Sci. 114, 247–255 (2001).
    CAS PubMed Google Scholar
  21. Kusch, J., Liakopoulos, D. & Barral, Y. Spindle asymmetry: a compass for the cell. Trends Cell Biol. 13, 562–569 (2003).
    Article CAS Google Scholar
  22. Yin, H., Pruyne, D., Huffaker, T.C. & Bretscher, A. Myosin V orientates the mitotic spindle in yeast. Nature 406, 1013–1015 (2000).
    Article CAS Google Scholar
  23. Beach, D.L., Thibodeaux, J., Maddox, P., Yeh, E. & Bloom, K. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast. Curr. Biol. 10, 1497–1506 (2000).
    Article CAS Google Scholar
  24. Su, L.K. et al. APC binds to the novel protein EB1. Cancer Res. 55, 2971–2977 (1995).
    Google Scholar
  25. Bienz, M. Spindles cotton on to junctions, APC and EB1. Nature Cell Biol. 3, E67–E68 (2001).
    Article CAS Google Scholar
  26. Munemitsu, S. et al. The APC gene product associates with microtubules in vivo and promotes their assembly in vitro. Cancer Res. 54, 3676–3681 (1994).
    CAS PubMed Google Scholar
  27. Berrueta, L. et al. The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules. Proc. Natl Acad. Sci. USA 95, 10596–10601 (1998).
    Article CAS Google Scholar
  28. Zumbrunn, J., Kinoshita, K., Hyman, A.A. & Nathke, I.S. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3β phosphorylation. Curr. Biol. 11, 44–49 (2001).
    Article CAS Google Scholar
  29. Askham, J.M., Vaughan, K.T., Goodson, H.V. & Morrison, E.E. Evidence that an interaction between EB1 and p150(Glued) is required for the formation and maintenance of a radial microtubule array anchored at the centrosome. Mol. Biol. Cell 13, 3627–3645 (2002).
    Article CAS Google Scholar
  30. Ligon, L.A., Shelly, S.S., Tokito, M. & Holzbaur, E.L. The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol. Biol. Cell 14, 1405–1417 (2003).
    Article CAS Google Scholar
  31. Gundersen, G.G. Evolutionary conservation of microtubule-capture mechanisms. Nature Rev. Mol. Cell Biol. 3, 296–304 (2002).
    Article CAS Google Scholar
  32. Berrueta, L., Tirnauer, J.S., Schuyler, S.C., Pellman, D. & Bierer, B.E. The APC-associated protein EB1 associates with components of the dynactin complex and cytoplasmic dynein intermediate chain. Curr. Biol. 9, 425–428 (1999).
    Article CAS Google Scholar
  33. Tirnauer, J.S., O'Toole, E., Berrueta, L., Bierer, B.E. & Pellman, D. Yeast Bim1p promotes the G1-specific dynamics of microtubules. J. Cell Biol. 145, 993–1007 (1999).
    Article CAS Google Scholar
  34. Rogers, S.L., Rogers, G.C., Sharp, D.J. & Vale, R.D. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 158, 873–884 (2002).
    Article CAS Google Scholar
  35. Mimori-Kiyosue, Y., Shiina, N. & Tsukita, S. The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr. Biol. 10, 865–868 (2000).
    Article CAS Google Scholar
  36. Alberts, A.S. Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J. Biol. Chem. 276, 2824–2830 (2001).
    Article CAS Google Scholar
  37. Palazzo, A.F. et al. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr. Biol. 11, 1536–1541 (2001).
    Article CAS Google Scholar
  38. Askham, J.M., Moncur, P., Markham, A.F. & Morrison, E.E. Regulation and function of the interaction between the APC tumour suppressor protein and EB1. Oncogene 19, 1950–1958 (2000).
    Article CAS Google Scholar
  39. Fukata, M. et al. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109, 873–885 (2002).
    Article CAS Google Scholar
  40. Watanabe, N., Kato, T., Fujita, A., Ishizaki, T. & Narumiya, S. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nature Cell Biol. 1, 136–143 (1999).
    Article CAS Google Scholar
  41. Wallar, B.J. & Alberts, A.S. The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 13, 435–446 (2003).
    Article CAS Google Scholar
  42. Yasuda, S. et al. Cdc42 and mDia3 regulate microtubule attachment to kinetochores. Nature 428, 767–771 (2004).
    Article CAS Google Scholar
  43. Nakamura, M., Zhou, X.Z., Kishi, S. & Lu, K.P. Involvement of the telomeric protein Pin2/TRF1 in the regulation of the mitotic spindle. FEBS Lett. 514, 193–198 (2002).
    Article CAS Google Scholar
  44. Subramanian, A. et al. Shortstop recruits EB1/APC1 and promotes microtubule assembly at the muscle-tendon junction. Curr. Biol. 13, 1086–1095 (2003).
    Article CAS Google Scholar
  45. Leung, C.L., Sun, D., Zheng, M., Knowles, D.R. & Liem, R.K. Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J. Cell Biol. 147, 1275–1286 (1999).
    Article CAS Google Scholar
  46. Karakesisoglou, I., Yang, Y. & Fuchs, E. An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J. Cell Biol. 149, 195–208 (2000).
    Article CAS Google Scholar
  47. Sun, D., Leung, C.L. & Liem, R.K. Characterization of the microtubule binding domain of microtubule actin crosslinking factor (MACF): identification of a novel group of microtubule associated proteins. J. Cell Sci. 114, 161–172 (2001).
    CAS PubMed Google Scholar
  48. Kodama, A., Karakesisoglou, I., Wong, E., Vaezi, A. & Fuchs, E. ACF7. An essential integrator of microtubule dynamics. Cell 115, 343–354 (2003).
    Article CAS Google Scholar
  49. Evangelista, M., Zigmond, S. & Boone, C. Formins: signaling effectors for assembly and polarization of actin filaments. J. Cell Sci. 116, 2903–2911 (2003).
    Article Google Scholar
  50. Elbashir, S.M., Harborth, J., Weber, K. & Tuschl, T. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26, 199–213 (2002).
    Article CAS Google Scholar

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