Novel localization of formin mDia2: importin β-mediated delivery to and retention at the cytoplasmic side of the nuclear envelope

Biology Open

Volumn 4, Issue 11, 2015, Pages 1569-1575

  Shao, Xiaowei ^a   Kawauchi, Keiko ^a,b   Shivashankar, G V ^a,c,d   Bershadsky, Alexander D ^a,e  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b KONAN UNIVERSITY   (Japan)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^e WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Formin mDia2; Importin ; Nuclear rim

Indexed keywords

4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; CALCIMYCIN; CALCIUM ION; DIAPHANOUS RELATED FORMIN 1; DIAPHANOUS RELATED FORMIN 3; F ACTIN; GUANOSINE TRIPHOSPHATASE; INVERTED FORMIN 2; KARYOPHERIN BETA; LAMIN B1; METHENAMINE; NUP153 PROTEIN; PROTEIN; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ARTICLE; BIOACCUMULATION; CELL FUNCTION; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; PROTEIN INTERACTION; SEQUENCE ANALYSIS;

EID: 84982834027     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.013649     Document Type: Article

References (34)

1. Adam, S. A., Marr, R. S. and Gerace, L. (1990). Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111, 807-816.
2. Baarlink, C., Wang, H. and Grosse, R. (2013). Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 340, 864-867.
3. Bartolini, F., Moseley, J. B., Schmoranzer, J., Cassimeris, L., Goode, B. L. and Gundersen, G. G. (2008). The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J. Cell Biol. 181, 523-536.
4. Beli, P., Mascheroni, D., Xu, D. L. and Innocenti, M. (2008). WAVE and Arp2/3 jointly inhibit filopodium formation by entering into a complex with mDia2. Nat. Cell Biol. 10, 849-857.
5. Bhattacharya, D., Mazumder, A., Miriam, S. A. and Shivashankar, G. V. (2006). EGFP-tagged core and linker histones diffuse via distinct mechanisms within living cells. Biophys. J. 91, 2326-2336.
6. Bhattacharya, D., Talwar, S., Mazumder, A. and Shivashankar, G. V. (2009). Spatio-temporal plasticity in chromatin organization in mouse cell differentiation and during Drosophila embryogenesis. Biophys. J. 96, 3832-3839.
7. Campellone, K. G. and Welch, M. D. (2010). A nucleator arms race: cellular control of actin assembly. Nat. Rev. Microbiol. 11, 237-251.
8. Chesarone, M. A., DuPage, A. G. and Goode, B. L. (2010). Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat. Rev. Mol. Cell Biol. 11, 62-74.
9. Ciciarello, M., Mangiacasale, R., Thibier, C., Guarguaglini, G., Marchetti, E., Di Fiore, B. and Lavia, P. (2004). Importin beta is transported to spindle poles during mitosis and regulates Ran-dependent spindle assembly factors in mammalian cells. J. Cell Sci. 117, 6511-6522.
10. Crisp, M., Liu, Q., Roux, K., Rattner, J. B., Shanahan, C., Burke, B., Stahl, P. D. and Hodzic, D. (2006). Coupling of the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172, 41-53.
11. DeWard, A. D. and Alberts, A. S. (2009). Ubiquitin-mediated degradation of the formin mDia2 upon completion of cell division. J. Biol. Chem. 284, 20061-20069.
12. Foo, Y., Korzh, V. and Wohland, T. (2012). Fluorescence correlation and crosscorrelation spectroscopy using fluorescent proteins for measurements of biomolecular processes in living organisms. In Fluorescent Proteins II (ed. G. Jung), pp. 213-248. Berlin, Heidelberg: Springer.
13. Gaillard, J., Ramabhadran, V., Neumanne, E., Gurel, P., Blanchoin, L., Vantard, M. and Higgs, H. N. (2011). Differential interactions of the formins INF2, mDia1, and mDia2 with microtubules. Mol. Biol. Cell 22, 4575-4587.
14. Mechanisms of plasma membrane targeting of formin mDia2 through its amino terminal domains. Mol. Biol. Cell 22, 189-201.
15. Gustafsson, M. G. L., Shao, L., Carlton, P. M., Wang, C. J. R., Golubovskaya, I. N., Cande, W. Z., Agard, D. A. and Sedat, J. W. (2008). Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957-4970.
16. Harris, E. S., Gauvin, T. J., Heimsath, E. G. and Higgs, H. N. (2010). Assembly of filopodia by the formin FRL2 (FMNL3). Cytoskeleton 67, 755-772.
17. Ji, P., Jayapal, S. R. and Lodish, H. F. (2008). Enucleation of cultured mouse fetal erythroblasts requires Rac GTPases and mDia2. Nat. Cell Biol. 10, 314-321.
18. Kalab, P. and Heald, R. (2008). The RanGTP gradient - a GPS for the mitotic spindle. J. Cell Sci. 121, 1577-1586.
19. Kim, H.-C., Jo, Y.-J., Kim, N.-H. and Namgoong, S. (2015). Small Molecule Inhibitor of Formin Homology 2 Domains (SMIFH2) reveals the roles of the formin family of proteins in spindle assembly and asymmetric division in mouse oocytes. PLoS ONE 10, e0123438.
20. Kraynov, V. S., Chamberlain, C., Bokoch, G. M., Schwartz, M. A., Slabaugh, S. and Hahn, K. M. (2000). Localized Rac activation dynamics visualized in living cells. Science 290, 333-337.
21. Kutscheidt, S., Zhu, R., Antoku, S., Luxton, G. W. G., Stagljar, I., Fackler, O. T. and Gundersen, G. G. (2014). FHOD1 interaction with nesprin-2G mediates TAN line formation and nuclear movement. Nat. Cell Biol. 16, 708-715.
22. Lammers, M., Meyer, S., Kuhlmann, D. and Wittinghofer, A. (2008). Specificity of Interactions between mDia Isoforms and Rho Proteins. J. Biol. Chem. 283, 35236-35246.
23. Ma, Y., Cai, S., Lv, Q., Jiang, Q., Zhang, Q., Sodmergen, Q., Zhai, Z. and Zhang, C. (2007). Lamin B receptor plays a role in stimulating nuclear envelope production and targeting membrane vesicles to chromatin during nuclear envelope assembly through direct interaction with importin beta. J. Cell Sci. 120, 520-530.
24. Miki, T., Okawa, K., Sekimoto, T., Yoneda, Y., Watanabe, S., Ishizaki, T. and Narumiya, S. (2009). mDia2 shuttles between the nucleus and the cytoplasm through the importin-α/β- and CRM1-mediated nuclear transport mechanism. J. Biol. Chem. 284, 5753-5762.
25. Pellegrin, S. and Mellor, H. (2005). The Rho family GTPase Rif induces filopodia through mDia2. Curr. Biol. 15, 129-133.
26. Shao, X., Li, Q., Mogilner, A., Bershadsky, A. D. and Shivashankar, G. V. (2015). Mechanical stimulation induces formin-dependent assembly of a perinuclear actin rim. Proc. Natl. Acad. Sci. USA 112, E2595-E2601.
27. Wallar, B. J., DeWard, A. D., Resau, J. H. and Alberts, A. S. (2007). RhoB and the mammalian Diaphanous-related formin mDia2 in endosome trafficking. Exp. Cell Res. 313, 560-571.
28. Watanabe, N., Kato, T., Fujita, A., Ishizaki, T. and Narumiya, S. (1999). Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat. Cell Biol. 1, 136-143.
29. Watanabe, S., Ando, Y., Yasuda, S., Hosoya, H., Watanabe, N., Ishizaki, T. and Narumiya, S. (2008). mDia2 induces the actin scaffold for the contractile ring and stabilizes its position during cytokinesis in NIH 3T3 cells. Mol. Biol. Cell 19, 2328-2338.
30. Watanabe, S., Okawa, K., Miki, T., Sakamoto, S., Morinaga, T., Segawa, K., Arakawa, T., Kinoshita, M., Ishizaki, T. and Narumiya, S. (2010). Rho and anillin-dependent control of mDia2 localization and function in cytokinesis. Mol. Biol. Cell 21, 3193-3204.
31. Weiss, M., Elsner, M., Kartberg, F. and Nilsson, T. (2004). Anomalous subdiffusion is a measure for cytoplasmic crowding in living cells. Biophys. J. 87, 3518-3524.
32. Wu, J., Corbett, A. H. and Berland, K. M. (2009). The intracellular mobility of nuclear import receptors and NLS cargoes. Biophys. J. 96, 3840-3849.
33. Yang, W. and Musser, S. M. (2006). Nuclear import time and transport efficiency depend on importin beta concentration. J. Cell Biol. 174, 951-961.
34. Yang, C., Czech, L., Gerboth, S., Kojima, S.-I., Scita, G. and Svitkina, T. (2007). Novel roles of formin mDia2 in lamellipodia and filopodia formation in motile cells. PLoS Biol. 5, e317.