Local RhoA activation induces cytokinetic furrows independent of spindle position and cell cycle stage

Journal of Cell Biology

Volumn 213, Issue 6, 2016, Pages 641-649

  Wagner, Elizabeth ^a   Glotzer, Michael ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; MICROTUBULE ASSOCIATED PROTEIN;

3T3 CELL LINE; ANAPHASE; ARTICLE; CELL CYCLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINESIS; ENZYME ACTIVATION; ENZYME INDUCTION; HELA CELL LINE; INTERPHASE; LIGHT; MAMMAL CELL; METAPHASE; MITOSIS SPINDLE; PHOTOSTIMULATION; POLAR BODY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; REGULATORY MECHANISM; ANIMAL; CELL LINE; HUMAN; METABOLISM; MOUSE; NIH 3T3 CELL LINE; PHYSIOLOGY; SPINDLE APPARATUS; TUMOR CELL LINE;

ANAPHASE; ANIMALS; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CYTOKINESIS; HELA CELLS; HUMANS; INTERPHASE; METAPHASE; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NIH 3T3 CELLS; RHOA GTP-BINDING PROTEIN; SPINDLE APPARATUS;

EID: 84975502225     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201603025     Document Type: Article

References (32)

1. Adams, R.R., M. Carmena, and W.C. Earnshaw. 2001. Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol. 11:49-54. http://dx.doi.org/10.1016/S0962-8924(00)01880-8
2. Basant, A., S. Lekomtsev, Y.C. Tse, D. Zhang, K.M. Longhini, M. Petronczki, and M. Glotzer. 2015. Aurora B kinase promotes cytokinesis by inducing centralspindlin oligomers that associate with the plasma membrane. Dev. Cell. 33:204-215. http://dx.doi.org/10.1016/j.devcel.2015.03.015
3. Bement, W.M., M. Leda, A.M. Moe, A.M. Kita, M.E. Larson, A.E. Golding, C. Pfeuti, K.-C. Su, A.L. Miller, A.B. Goryachev, and G. von Dassow. 2015. Activator-inhibitor coupling between Rho signalling and actin assembly makes the cell cortex an excitable medium. Nat. Cell Biol. 17:1471-1483. http://dx.doi.org/10.1038/ncb3251
4. Burkard, M.E., J. Maciejowski, V. Rodriguez-Bravo, M. Repka, D.M. Lowery, K.R. Clauser, C. Zhang, K.M. Shokat, S.A. Carr, M.B. Yaffe, and P.V. Jallepalli. 2009. Plk1 self-organization and priming phosphorylation of HsCYK-4 at the spindle midzone regulate the onset of division in human cells. PLoS Biol. 7:e1000111. http://dx.doi.org/10.1371/journal.pbio.1000111
5. Drechsel, D.N., A.A. Hyman, A. Hall, and M. Glotzer. 1997. A requirement for Rho and Cdc42 during cytokinesis in Xenopus embryos. Curr. Biol. 7:12-23. http://dx.doi.org/10.1016/S0960-9822(06)00023-6
6. Fededa, J.P., and D.W. Gerlich. 2012. Molecular control of animal cell cytokinesis. Nat. Cell Biol. 14:440-447. http://dx.doi.org/10.1038/ncb2482
7. Golsteyn, R.M., K.E. Mundt, A.M. Fry, and E.A. Nigg. 1995. Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. J. Cell Biol. 129:1617-1628. http://dx.doi.org/10.1083/jcb.129.6.1617
8. Jaiswal, M., L. Gremer, R. Dvorsky, L.C. Haeusler, I.C. Cirstea, K. Uhlenbrock, and M.R. Ahmadian. 2011. Mechanistic insights into specificity, activity, and regulatory elements of the regulator of G-protein signaling (RGS)-containing Rho-specific guanine nucleotide exchange factors (GEFs) p115, PDZ-RhoGEF (PRG), and leukemia-associated RhoGEF (LARG). J. Biol. Chem. 286:18202-18212. http://dx.doi.org/10.1074/jbc.M111.226431
9. Kishi, K., T. Sasaki, S. Kuroda, T. Itoh, and Y. Takai. 1993. Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI). J. Cell Biol. 120:1187-1195. http://dx.doi.org/10.1083/jcb.120.5.1187
10. Kosako, H., T. Yoshida, F. Matsumura, T. Ishizaki, S. Narumiya, and M. Inagaki. 2000. Rho-kinase/ROCK is involved in cytokinesis through the phosphorylation of myosin light chain and not ezrin/radixin/moesin proteins at the cleavage furrow. Oncogene. 19:6059-6064. http://dx.doi.org/10.1038/sj.onc.1203987
11. Liu, X., T. Zhou, R. Kuriyama, and R.L. Erikson. 2004. Molecular interactions of Polo-like-kinase 1 with the mitotic kinesin-like protein CHO1/MKLP-1. J. Cell Sci. 117:3233-3246. http://dx.doi.org/10.1242/jcs.01173
12. Loria, A., K.M. Longhini, and M. Glotzer. 2012. The RhoGAP domain of CYK-4 has an essential role in RhoA activation. Curr. Biol. 22:213-219. http://dx.doi.org/10.1016/j.cub.2011.12.019
13. Lowery, D.M., K.R. Clauser, M. Hjerrild, D. Lim, J. Alexander, K. Kishi, S.-E. Ong, S. Gammeltoft, S.A. Carr, and M.B. Yaffe. 2007. Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate. EMBO J. 26:2262-2273. http://dx.doi.org/10.1038/sj.emboj.7601683
14. Meyer, E.J., A. Ikmi, and M.C. Gibson. 2011. Interkinetic nuclear migration is a broadly conserved feature of cell division in pseudostratified epithelia. Curr. Biol. 21:485-491. http://dx.doi.org/10.1016/j.cub.2011.02.002
15. Neef, R., C. Preisinger, J. Sutcliffe, R. Kopajtich, E.A. Nigg, T.U. Mayer, and F.A. Barr. 2003. Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. J. Cell Biol. 162:863-875. http://dx.doi.org/10.1083/jcb.200306009
16. Niiya, F., T. Tatsumoto, K.S. Lee, and T. Miki. 2006. Phosphorylation of the cytokinesis regulator ECT2 at G2/M phase stimulates association of the mitotic kinase Plk1 and accumulation of GTP-bound RhoA. Oncogene. 25:827-837. http://dx.doi.org/10.1038/sj.onc.1209124
17. Otomo, T., C. Otomo, D.R. Tomchick, M. Machius, and M.K. Rosen. 2005. Structural basis of Rho GTPase-mediated activation of the formin mDia1. Mol. Cell. 18:273-281. http://dx.doi.org/10.1016/j.molcel.2005.04.002
18. Petronczki, M., M. Glotzer, N. Kraut, and J.-M. Peters. 2007. Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. Dev. Cell. 12:713-725. http://dx.doi.org/10.1016/j.devcel.2007.03.013
19. Piekny, A.J., and M. Glotzer. 2008. Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr. Biol. 18:30-36. http://dx.doi.org/10.1016/j.cub.2007.11.068
20. Rappaport, R. 1985. Repeated furrow formation from a single mitotic apparatus in cylindrical sand dollar eggs. J. Exp. Zool. 234:167-171. http://dx.doi.org/10.1002/jez.1402340120
21. Skelton, N.J., M.F.T. Koehler, K. Zobel, W.L. Wong, S. Yeh, M.T. Pisabarro, J.P. Yin, L.A. Lasky, and S.S. Sidhu. 2003. Origins of PDZ domain ligand specificity. Structure determination and mutagenesis of the Erbin PDZ domain. J. Biol. Chem. 278:7645-7654. http://dx.doi.org/10.1074/jbc.M209751200
22. Stewart, M.P., J. Helenius, Y. Toyoda, S.P. Ramanathan, D.J. Muller, and A.A. Hyman. 2011. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature. 469:226-230. http://dx.doi.org/10.1038/nature09642
23. Strickland, D., Y. Lin, E. Wagner, C.M. Hope, J. Zayner, C. Antoniou, T.R. Sosnick, E.L. Weiss, and M. Glotzer. 2012. TUL IPs: Tunable, lightcontrolled interacting protein tags for cell biology. Nat. Methods. 9:379-384. http://dx.doi.org/10.1038/nmeth.1904
24. Tatsumoto, T., X. Xie, R. Blumenthal, I. Okamoto, and T. Miki. 1999. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J. Cell Biol. 147:921-928. http://dx.doi.org/10.1083/jcb.147.5.921
25. Toettcher, J.E., O.D. Weiner, and W.A. Lim. 2013. Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module. Cell. 155:1422-1434. http://dx.doi.org/10.1016/j.cell.2013.11.004
26. van Oostende Triplet, C., M. Jaramillo Garcia, H. Haji Bik, D. Beaudet, and A. Piekny. 2014. Anillin interacts with microtubules and is part of the astral pathway that defines cortical domains. J. Cell Sci. 127:3699-3710. http://dx.doi.org/10.1242/jcs.147504
27. Watanabe, S., Y. Ando, S. Yasuda, H. Hosoya, N. Watanabe, T. Ishizaki, and S. Narumiya. 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. http://dx.doi.org/10.1091/mbc.E07-10-1086
28. Werner, M., E. Munro, and M. Glotzer. 2007. Astral signals spatially bias cortical myosin recruitment to break symmetry and promote cytokinesis. Curr. Biol. 17:1286-1297. http://dx.doi.org/10.1016/j.cub.2007.06.070
29. Wolfe, B.A., T. Takaki, M. Petronczki, and M. Glotzer. 2009. Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol. 7:e1000110. http://dx.doi.org/10.1371/journal.pbio.1000110
30. Yüce, O., A. Piekny, and M. Glotzer. 2005. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J. Cell Biol. 170:571-582. http://dx.doi.org/10.1083/jcb.200501097
31. Zanin, E., A. Desai, I. Poser, Y. Toyoda, C. Andree, C. Moebius, M. Bickle, B. Conradt, A. Piekny, and K. Oegema. 2013. A conserved RhoGAP limits M phase contractility and coordinates with microtubule asters to confine RhoA during cytokinesis. Dev. Cell. 26:496-510. http://dx.doi.org/10.1016/j.devcel.2013.08.005
32. Zhang, D., and M. Glotzer. 2015. The RhoGAP activity of CYK-4/MgcRacGAP functions non-canonically by promoting RhoA activation during cytokinesis. eLife. 4:e08898. http://dx.doi.org/10.7554/eLife.08898