The formin mDia regulates GSK3β through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts

Molecular Biology of the Cell

Volumn 17, Issue 12, 2006, Pages 5004-5016

  Eng, Christina H ^a   Huckaba, Thomas M ^a   Gundersen, Gregg G ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; CELL PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOGEN SYNTHASE KINASE 3BETA INHIBITOR; INHIBITOR PROTEIN; ISOPROTEIN; LITHIUM CHLORIDE; LYSOPHOSPHATIDIC ACID; METHENAMINE; PROTEIN EB1; PROTEIN KINASE C; PROTEIN MDIA; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SERINE;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL MIGRATION; CELL STRAIN 3T3; CELL TRANSPORT; CONTROLLED STUDY; CYTOSKELETON; ENZYME REGULATION; FIBROBLAST; FUNCTIONAL PROTEOMICS; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MICROTUBULE; MICROTUBULE ASSEMBLY; MICROTUBULE STABILIZATION; MITOCHONDRIAL ORGANIZING CENTER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SERUM; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CARRIER PROTEINS; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; FIBROBLASTS; GLYCOGEN SYNTHASE KINASE 3; ISOENZYMES; LYSOPHOSPHOLIPIDS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULE-ORGANIZING CENTER; MICROTUBULES; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C; RHO GTP-BINDING PROTEINS; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 33845459805     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-10-0914     Document Type: Article

References (57)

1. Akhmanova, A., et al. (2001). CLASPS are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935.
2. Aktories, K., Braun, U., Rosener, S., Just, I., and Hall, A. (1989). The rho gene product expressed in E. coli is a substrate of botulinum ADP-ribosyltransferase C3. Biochem. Biophys. Res. Commun. 158, 209-213.
3. Alberts, A. S. (2001). Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J. Biol. Chem. 276, 2824-2830.
4. Arakawa, Y., Bito, H., Furuyashiki, T., Tsuji, T., Takemoto-Kimura, S., Kimura, K., Nozaki, K., Hashimoto, N., and Narumiya, S. (2003). Control of axon elongation via an SDF-1alpha/Rho/mDia pathway in cultured cerebellar granule neurons. J. Cell Biol. 161, 381-391.
5. Askham, J. M., Moncur, P., Markham, A. F., and Morrison, E. E. (2000). Regulation and function of the interaction between the APC tumour suppressor protein and EB1. Oncogene 19, 1950-1958.
6. Bulinski, J. C., and Gundersen, G. G. (1991). Stabilization of post-translational modification of microtubules during cellular morphogenesis. Bioessays 13, 285-293.
7. Coghlan, M. P., Chou, M. M., and Carpenter, C. L. (2000). Atypical protein kinases Clambda and -zeta associate with the GTP-binding protein Cdc42 and mediate stress fiber loss. Mol. Cell. Biol. 20, 2880-2889.
8. Cook, T. A., Nagasaki, T., and Gundersen, G. G. (1998). Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J. Cell Biol. 141, 175-185.
9. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M., and Hemmings, B. A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
10. Erck, C., et al. (2005). A vital role of tubulin-tyrosine-ligase for neuronal organization. Proc Natl. Acad. Sci. USA 102, 7853-7858.
11. Etienne-Manneville, S., and Hall, A. (2001). Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCζ. Cell 106, 489-498.
12. Etienne-Manneville, S., and Hall, A. (2003). Cdc42 regulates GSK-3β and adenomatous polyposis coli to control cell polarity. Nature 421, 753-756.
13. Fang, X., Yu, S., Tanyi, J. L., Lu, Y., Woodgett, J. R., and Mills, G. B. (2002). Convergence of multiple signaling cascades at glycogen synthase kinase 3, Edg receptor-mediated phosphorylation and inactivation by lysophosphatidic acid through a protein kinase C-dependent intracellular pathway. Mol. Cell. Biol. 22, 2099-2110.
14. Gomes, E. R., Jani, S., and Gundersen, G. G. (2005). Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451-463.
15. Goold, R. G., Owen, R., and Gordon-Weeks, P. R. (1999). Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112(Pt 19), 3373-3384.
16. Gotlieb, A. I., May, L. M., Subrahmanyan, L., and Kalnins, V. I. (1981). Distribution of microtubule organizing centers in migrating sheets of endothelial cells. J. Cell Biol. 91, 589-594.
17. Goulimari, P., Kitzing, T. M., Knieling, H., Brandt, D. T., Offermarms, S., and Grosse, R. (2005). Galpha12/13 is essential for directed cell migration and localized Rho-Dial function. J. Biol. Chem. 280, 42242-42251.
18. Gundersen, G. G., and Bulinski, J. C. (1986). Microtubule arrays in differentiated cells contain elevated levels of a post-translationally modified form of tubulin. Eur. J. Cell Biol. 42, 288-294.
19. Gundersen, G. G., and Bulinski, J. C. (1988). Selective stabilization of microtubules oriented toward the direction of cell migration. Proc. Natl. Acad. Sci. USA 85, 5946-5950.
20. Gundersen, G. G., Gomes, E. R., and Wen, Y. (2004). Cortical control of microtubule stability and polarization. Curr. Opin. Cell Biol. 16, 106-112.
21. Gundersen, G. G., Kalnoski, M. H., and Bulinski, J. C. (1984). Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell 38, 779-789.
22. Gundersen, G. G., Kim, I., and Chapin, C. J. (1994). Induction of stable microtubules in 3T3 fibroblasts by TGF-beta and serum. J. Cell Sci. 107(Pt 3), 645-659.
23. Gurland, G., and Gundersen, G. G. (1995). Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J. Cell Biol. 131, 1275-1290.
24. Hernandez, R. M., Wescott, G. G., Mayhew, M. W., McJilton, M. A., and Terrian, D. M. (2001). Biochemical and morphogenic effects of the interaction between protein kinase C-epsilon and actin in vitro and in cultured NIH3T3 cells. J. Cell. Biochem. 83, 532-546.
25. Infante, A. S., Stein, M. S., Zhai, Y., Borisy, G. G., and Gundersen, G. G. (2000). Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap. J. Cell Sci. 113, 3907-3919.
26. Jiang, H., Guo, W., Liang, X., and Rao, Y. (2005). Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120, 123-135.
27. Kato, T., Watanabe, N., Morishima, Y., Fujita, A., Ishizaki, T., and Narumiya, S. (2001). Localization of a mammalian homolog of diaphanous, mDia1, to the mitotic spindle in HeLa cells. J. Cell Sci. 114, 775-784.
28. Khawaja, S., Gundersen, G. G., and Bulinski, J. C. (1988). Enhanced stability of microtubules enriched in detyrosinated tubulin is not a direct function of detyrosination level. J. Cell Biol. 106, 141-149.
29. Kodama, A., Karakesisoglou, I., Wong, E., Vaezi, A., and Fuchs, E. (2003). ACF7, an essential integrator of microtubule dynamics. Cell 115, 343-354.
30. Kreitzer, G., Liao, G., and Gundersen, G. G. (1999). Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism. Mol. Biol. Cell 10, 1105-1118.
31. Krylova, O., Messenger, M. J., and Salinas, P. C. (2000). Dishevelled-1 regulates microtubule stability: a new function mediated by glycogen synthase kinase-3beta. J. Cell Biol. 151, 83-94.
32. Kupfer, A., Dennert, G., and Singer, S. J. (1983). Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc. Natl. Acad. Sci. USA 80, 7224-7228.
33. Kupfer, A., Louvard, D., and Singer, S. J. (1982). Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc. Natl. Acad. Sci. USA 79, 2603-2607.
34. Leung, T., Chen, X. Q., Manser, E., and Lim, L. (1996). The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16, 5313-5327.
35. Liao, G., and Gundersen, G. G. (1998). Kinesin is a candidate for crossbridging microtubules and intermediate filaments. J. Biol. Chem. 273, 9797-9803.
36. Lin, S. X., Gundersen, G. G., and Maxfield, F. R. (2002). Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol. Biol. Cell 13, 96-109.
37. Lovestone, S., Hartley, C. L., Pearce, J., and Anderton, B. H. (1996). Phosphorylation of tau by glycogen synthase kinase-3 beta in intact mammalian cells: the effects on the organization and stability of microtubules. Neuroscience 73, 1145-1157.
38. Naranatt, P. P., Krishnan, H. H., Smith, M. S., and Chandran, B. (2005). Kaposi's sarcoma-associated herpes virus modulates microtubule dynamics via RhoA-GTP-diaphanous 2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus. J. Virol 79, 1191-1206.
39. Palazzo, A. F., Cook, T. A., Alberts, A. S., and Gundersen, G. G. (2001a). mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat. Cell Biol. 3, 723-729.
40. Palazzo, A. F., Eng, C. H., Schlaepfer, D. D., Marcantonio, E. E., and Gundersen, G. G. (2004). Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303, 836-839.
41. Palazzo, A. F., Joseph, H. L., Chen, Y. J., Dujardin, D. L., Alberts, A. S., Pfister, K. K., Vallee, R. B., and Gundersen, G. G. (2001b). Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr. Biol. 11, 1536-1541.
42. Prekeris, R., Mayhew, M. W., Cooper, J. B., and Terrian, D. M. (1996). Identification and localization of an actin-binding motif that is unique to the epsilon isoform of protein kinase C and participates in the regulation of synaptic function. J. Cell Biol. 132, 77-90.
43. Ridley, A. J., and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
44. Shi, S. H., Cheng, T., Jan, L. Y., and Jan, Y. N. (2004). APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14, 2025-2032.
45. Soh, J. W., Lee, E. H., Prywes, R., and Weinstein, I. B. (1999). Novel roles of specific isoforms of protein kinase C in activation of the c-fos serum response element. Mol. Cell. Biol. 19, 1313-1324.
46. Tominaga, T., Sahai, E., Chardin, P., McCormick, F., Courtneidge, S. A., and Alberts, A. S. (2000). Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol. Cell 5, 13-25.
47. Tzima, E., Kiosses, W. B., del Pozo, M. A., and Schwartz, M. A. (2003). Localized cdc42 activation, detected using a novel assay, mediates microtubule organizing center positioning in endothelial cells in response to fluid shear stress. J. Biol. Chem. 278, 31020-31023.
48. Wagner, U., Utton, M., Gallo, J. M., and Miller, C. C. (1996). Cellular phosphorylation of tau by GSK-3 beta influences tau binding to microtubules and microtubule organisation. J. Cell Sci. 109(Pt 6), 1537-1543.
49. Wallar, B. J., and Alberts, A. S. (2003). The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 13, 435-446.
50. Watanabe, N., Madaule, P., Reid, T., Ishizaki, T., Watanabe, G., Kakizuka, A., Saito, Y., Nakao, K., Jockusch, B. M., and Narumiya, S. (1997). p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16, 3044-3056.
51. Webster, D. R., Gundersen, G. G., Bulinski, J. C., and Borisy, G. G. (1987). Differential turnover of tyrosinated and detyrosinated microtubules. Proc. Natl. Acad. Sci. USA 84, 9040-9044.
52. Wen, Y., Eng, C. H., Schmoranzer, J., Cabrera-Poch, N., Morris, E. J., Chen, M., Wallar, B. J., Alberts, A. S., and Gundersen, G. G. (2004). EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6, 820-830.
53. Wittmann, T., and Waterman-Storer, C. M. (2005). Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J. Cell Biol. 169, 929-939.
54. Yang, M., Zhong, W. W., Srivastava, N., Slavin, A., Yang, J., Hoey, T., and An, S. (2005). G protein-coupled lysophosphatidic acid receptors stimulate proliferation of colon cancer cells through the β-catenin pathway. Proc. Natl. Acad. Sci. USA 102, 6027-6032.
55. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., and Kaibuchi, K. (2005). GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-149.
56. Zigmond, S. H. (2004). Formin-induced nucleation of actin filaments. Curr. Opin. Cell Biol. 16, 99-105.
57. Zumbrunn, J., Kinoshita, K., Hyman, A. A., and Nathke, I. S. (2001). Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr. Biol. 11, 44-49.