SLK-dependent activation of ERMs controls LGN-NuMA localization and spindle orientation

Journal of Cell Biology

Volumn 205, Issue 6, 2014, Pages 791-799

  Machicoane, Mickael ^a,b,c   de Frutos, Cristina A ^b,d   Fink, Jenny ^b,e   Rocancourt, Murielle ^a,b   Lombardi, Yannis ^a,b   Gare, Sonia ^a,b,d   Piel, Matthieu ^b,e   Echard, Arnaud ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d ECOLE NORMALE SUPÉRIEURE   (France)

^e INSTITUT CURIE   (France)

Author keywords

E, embryonic day; ERM, ezrin radixin moesin; LGN, leucine glycine asparagine repeat protein; NuMA, nuclear mitotic apparatus; SLK, ste20 like kinase

Indexed keywords

EZRIN; F ACTIN; GLYCINE ASPARAGINE REPEAT PROTEIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MOESIN; NUCLEAR MITOTIC APPARATUS PROTEIN; NUCLEAR PROTEIN; PROTEIN KINASE; PROTEIN SLK; RADIXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIVISION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MAMMAL CELL; MITOSIS SPINDLE; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANTIGENS, NUCLEAR; CELL DIVISION; CYTOSKELETAL PROTEINS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; NUCLEAR MATRIX-ASSOCIATED PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SPINDLE APPARATUS;

EID: 84903135719     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201401049     Document Type: Article

References (41)

1. Belkina, N.V., Y. Liu, J.J. Hao, H. Karasuyama, and S. Shaw. 2009. LOK is a major ERM kinase in resting lymphocytes and regulates cytoskeletal rearrangement through ERM phosphorylation. Proc. Natl. Acad. Sci. USA. 106:4707-4712. http://dx.doi.org/10.1073/pnas.0805963106
2. Carreno, S., I. Kouranti, E.S. Glusman, M.T. Fuller, A. Echard, and F. Payre. 2008. Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. J. Cell Biol. 180:739-746. http://dx.doi.org/10.1083/jcb.200709161
3. Castanon, I., L. Abrami, L. Holtzer, C.P. Heisenberg, F.G. van der Goot, and M. Gonzalez-Gaitan. 2013. Anthrax toxin receptor 2a controls mitotic spindle positioning. Nat. Cell Biol. 15:28-39. http://dx.doi.org/10.1038/ ncb2632
4. Chesneau, L., D. Dambournet, M. Machicoane, I. Kouranti, M. Fukuda, B. Goud, and A. Echard. 2012. An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr. Biol. 22:147-153. http:// dx.doi.org/10.1016/j.cub.2011.11.058
5. Dambournet, D., M. Machicoane, L. Chesneau, M. Sachse, M. Rocancourt, A. El Marjou, E. Formstecher, R. Salomon, B. Goud, and A. Echard. 2011. Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat. Cell Biol. 13:981-988. http://dx.doi.org/10 .1038/ncb2279
6. Deck, M., L. Lokmane, S. Chauvet, C. Mailhes, M. Keita, M. Niquille, M. Yoshida, Y. Yoshida, C. Lebrand, F. Mann, et al. 2013. Pathfinding of corticothalamic axons relies on a rendezvous with thalamic projections. Neuron. 77:472-484. http://dx.doi.org/10.1016/j.neuron.2012.11.031
7. Du, Q., and I.G. Macara. 2004. Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell. 119:503-516. http://dx .doi.org/10.1016/j.cell.2004.10.028
8. Fehon, R.G., A.I. McClatchey, and A. Bretscher. 2010. Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11:276-287. http://dx.doi.org/10.1038/nrm2866
9. Fietz, S.A., and W.B. Huttner. 2011. Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr. Opin. Neurobiol. 21:23-35. http://dx.doi.org/10.1016/j.conb.2010.10.002
10. Fievet, B.T., A. Gautreau, C. Roy, L. Del Maestro, P. Mangeat, D. Louvard, and M. Arpin. 2004. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164:653-659. http://dx.doi.org/10.1083/jcb.200307032
11. Fink, J., N. Carpi, T. Betz, A. Bétard, M. Chebah, A. Azioune, M. Bornens, C. Sykes, L. Fetler, D. Cuvelier, and M. Piel. 2011. External forces control mitotic spindle positioning. Nat. Cell Biol. 13:771-778. http://dx.doi .org/10.1038/ncb2269
12. Gimeno, L., A. Corradi, I. Cobos, G.G. Consalez, and S. Martinez. 2004. Ezrin gene, coding for a membrane-cytoskeleton linker protein, is regionally expressed in the developing mouse neuroepithelium. Gene Expr. Patterns. 4:749-754. http://dx.doi.org/10.1016/j.modgep.2004.03.007
13. Gonzalez, C. 2007. Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat. Rev. Genet. 8:462-472. http://dx.doi .org/10.1038/nrg2103
14. Hipfner, D.R., N. Keller, and S.M. Cohen. 2004. Slik Sterile-20 kinase regulates Moesin activity to promote epithelial integrity during tissue growth. Genes Dev. 18:2243-2248. http://dx.doi.org/10.1101/gad.303304
15. Kawano, Y., Y. Fukata, N. Oshiro, M. Amano, T. Nakamura, M. Ito, F. Matsumura, M. Inagaki, and K. Kaibuchi. 1999. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147:1023-1038. http://dx.doi.org/10.1083/jcb.147.5.1023
16. Kiyomitsu, T., and I.M. Cheeseman. 2012. Chromosome-and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat. Cell Biol. 14:311-317. http://dx.doi.org/10.1038/ncb2440
17. Kiyomitsu, T., and I.M. Cheeseman. 2013. Cortical dynein and asymmetric membrane elongation coordinately position the spindle in anaphase. Cell. 154:391-402. http://dx.doi.org/10.1016/j.cell.2013.06.010
18. Knoblich, J.A. 2008. Mechanisms of asymmetric stem cell division. Cell. 132:583-597. http://dx.doi.org/10.1016/j.cell.2008.02.007
19. Konno, D., G. Shioi, A. Shitamukai, A. Mori, H. Kiyonari, T. Miyata, and F. Matsuzaki. 2008. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10:93-101. http://dx.doi.org/10.1038/ncb1673
20. Kotak, S., C. Busso, and P. Gönczy. 2012. Cortical dynein is critical for proper spindle positioning in human cells. J. Cell Biol. 199:97-110. http://dx .doi.org/10.1083/jcb.201203166
21. Kunda, P., and B. Baum. 2009. The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol. 19:174-179. http://dx.doi.org/10.1016/j .tcb.2009.01.006
22. Kunda, P., A.E. Pelling, T. Liu, and B. Baum. 2008. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18:91-101. http://dx.doi.org/10.1016/j.cub.2007.12.051
23. Kunda, P., N.T. Rodrigues, E. Moeendarbary, T. Liu, A. Ivetic, G. Charras, and B. Baum. 2012. PP1-mediated moesin dephosphorylation couples polar relaxation to mitotic exit. Curr. Biol. 22:231-236. http://dx.doi.org/10 .1016/j.cub.2011.12.016
24. Luxenburg, C., H.A. Pasolli, S.E. Williams, and E. Fuchs. 2011. Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat. Cell Biol. 13:203-214. http://dx.doi.org/10.1038/ncb2163
25. Matsui, T., M. Maeda, Y. Doi, S. Yonemura, M. Amano, K. Kaibuchi, S. Tsukita, and S. Tsukita. 1998. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140:647-657. http://dx.doi.org/10 .1083/jcb.140.3.647
26. Minc, N., and M. Piel. 2012. Predicting division plane position and orientation. Trends Cell Biol. 22:193-200. http://dx.doi.org/10.1016/j.tcb .2012.01.003
27. Mire, E., C. Mezzera, E. Leyva-Díaz, A.V. Paternain, P. Squarzoni, L. Bluy, M. Castillo-Paterna, M.J. López, S. Peregrín, M. Tessier-Lavigne, et al. 2012. Spontaneous activity regulates Robo1 transcription to mediate a switch in thalamocortical axon growth. Nat. Neurosci. 15:1134-1143. http://dx.doi.org/10.1038/nn.3160
28. Miserey-Lenkei, S., G. Chalancon, S. Bardin, E. Formstecher, B. Goud, and A. Echard. 2010. Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat. Cell Biol. 12:645-654. http://dx.doi .org/10.1038/ncb2067
29. Morin, X., and Y. Bellaïche. 2011. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev. Cell. 21:102-119. http://dx.doi.org/10.1016/j.devcel.2011.06.012
30. Nakajima, Y., E.J. Meyer, A. Kroesen, S.A. McKinney, and M.C. Gibson. 2013. Epithelial junctions maintain tissue architecture by directing planar spindle orientation. Nature. 500:359-362. http://dx.doi.org/10 .1038/nature12335
31. O'Reilly, P.G., S. Wagner, D.J. Franks, K. Cailliau, E. Browaeys, C. Dissous, and L.A. Sabourin. 2005. The Ste20-like kinase SLK is required for cell cycle progression through G2. J. Biol. Chem. 280:42383-42390. http:// dx.doi.org/10.1074/jbc.M510763200
32. Roubinet, C., B. Decelle, G. Chicanne, J.F. Dorn, B. Payrastre, F. Payre, and S. Carreno. 2011. Molecular networks linked by Moesin drive remodeling of the cell cortex during mitosis. J. Cell Biol. 195:99-112. http://dx.doi .org/10.1083/jcb.201106048
33. Sandquist, J.C., A.M. Kita, and W.M. Bement. 2011. And the dead shall rise: actin and myosin return to the spindle. Dev. Cell. 21:410-419. http:// dx.doi.org/10.1016/j.devcel.2011.07.018
34. Siller, K.H., and C.Q. Doe. 2009. Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11:365-374. http://dx.doi.org/10.1038/ ncb0409-365
35. Solinet, S., K. Mahmud, S.F. Stewman, K. Ben El Kadhi, B. Decelle, L. Talje, A. Ma, B.H. Kwok, and S. Carreno. 2013. The actin-binding ERM protein Moesin binds to and stabilizes microtubules at the cell cortex. J. Cell Biol. 202:251-260. http://dx.doi.org/10.1083/jcb.201304052
36. Théry, M., V. Racine, A. Pépin, M. Piel, Y. Chen, J.B. Sibarita, and M. Bornens. 2005. The extracellular matrix guides the orientation of the cell division axis. Nat. Cell Biol. 7:947-953. http://dx.doi.org/10.1038/ncb1307
37. Théry, M., A. Jiménez-Dalmaroni, V. Racine, M. Bornens, and F. Jülicher. 2007. Experimental and theoretical study of mitotic spindle orientation. Nature. 447:493-496. http://dx.doi.org/10.1038/nature05786
38. Toyoshima, F., and E. Nishida. 2007. Integrin-mediated adhesion orients the spindle parallel to the substratum in an EB1-and myosin Xdependent manner. EMBO J. 26:1487-1498. http://dx.doi.org/10.1038/sj .emboj.7601599
39. Viswanatha, R., P.Y. Ohouo, M.B. Smolka, and A. Bretscher. 2012. Local phosphocycling mediated by LOK/SLK restricts ezrin function to the apical aspect of epithelial cells. J. Cell Biol. 199:969-984. http://dx.doi.org/ 10.1083/jcb.201207047
40. Woodard, G.E., N.N. Huang, H. Cho, T. Miki, G.G. Tall, and J.H. Kehrl. 2010. Ric-8A and Giα recruit LGN, NuMA, and dynein to the cell cortex to help orient the mitotic spindle. Mol. Cell. Biol. 30:3519-3530. http:// dx.doi.org/10.1128/MCB.00394-10
41. Zheng, Z., Q. Wan, J. Liu, H. Zhu, X. Chu, and Q. Du. 2013. Evidence for dynein and astral microtubule-mediated cortical release and transport of Gαi/ LGN/NuMA complex in mitotic cells. Mol. Biol. Cell. 24:901-913. http://dx.doi.org/10.1091/mbc.E12-06-0458