Moesin is a major regulator of centrosome behavior in epithelial cells with extra centrosomes

Current Biology

Volumn 25, Issue 7, 2015, Pages 879-889

  Sabino, Dora ^a,c   Gogendeau, Delphine ^a   Gambarotto, Davide ^a   Nano, Maddalena ^a   Pennetier, Carole ^a   Dingli, Florent ^b   Arras, Guillaume ^b   Loew, Damarys ^b   Basto, Renata ^a  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c UMR 8126   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; MOESIN;

ANEUPLOIDY; ANIMAL; CELL DEATH; CENTROSOME; CYTOLOGY; DROSOPHILA; EPITHELIUM CELL; METABOLISM; SPINDLE APPARATUS; UPREGULATION;

ANEUPLOIDY; ANIMALS; CELL DEATH; CENTROSOME; DROSOPHILA; EPITHELIAL CELLS; MICROFILAMENT PROTEINS; SPINDLE APPARATUS; UP-REGULATION;

EID: 84932622309     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2015.01.066     Document Type: Article

References (44)

1. Kellogg, D.R., Moritz, M., and Alberts, B.M. (1994). The centrosome and cellular organization. Annu. Rev. Biochem. 63, 639-674.
2. Bornens, M. (2002). Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25-34.
3. Nigg, E.A. (2006). Origins and consequences of centrosome aberrations in human cancers. Int. J. Cancer 119, 2717-2723.
4. Zyss, D., and Gergely, F. (2009). Centrosome function in cancer: guilty or innocent? Trends Cell Biol. 19, 334-346.
5. Kwon, M., Godinho, S.A., Chandhok, N.S., Ganem, N.J., Azioune, A., Thery, M., and Pellman, D. (2008). Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 22, 2189-2203.
6. Basto, R., Brunk, K., Vinadogrova, T., Peel, N., Franz, A., Khodjakov, A., and Raff, J.W. (2008). Centrosome amplification can initiate tumorigenesis in flies. Cell 133, 1032-1042.
7. Ganem, N.J., Godinho, S.A., and Pellman, D. (2009). A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282.
8. Leber, B., Maier, B., Fuchs, F., Chi, J., Riffel, P., Anderhub, S., Wagner, L., Ho, A.D., Salisbury, J.L., Boutros, M., and Krämer, A. (2010). Proteins required for centrosome clustering in cancer cells. Sci. Transl. Med. 2, 33ra38.
9. Marthiens, V., Rujano, M.A., Pennetier, C., Tessier, S., Paul-Gilloteaux, P., and Basto, R. (2013). Centrosome amplification causes microcephaly. Nat. Cell Biol. 15, 731-740.
10. Habedanck, R., Stierhof, Y.D., Wilkinson, C.J., and Nigg, E.A. (2005). The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7, 1140-1146.
11. Bettencourt-Dias, M., Rodrigues-Martins, A., Carpenter, L., Riparbelli, M., Lehmann, L., Gatt, M.K., Carmo, N., Balloux, F., Callaini, G., and Glover, D.M. (2005). SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15, 2199-2207.
12. Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Habedanck, R., Stierhof, Y.D., and Nigg, E.A. (2007). Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202.
13. Weinberg, R.A. (2006). The Biology of Cancer. (New York: Garland).
14. Lee, H.S., Simon, J.A., and Lis, J.T. (1988). Structure and expression of ubiquitin genes of Drosophila melanogaster. Mol. Cell. Biol. 8, 4727-4735.
15. Adler, P.N., and MacQueen, M. (1984). Cell proliferation and DNA replication in the imaginal wing disc of Drosophila melanogaster. Dev. Biol. 103, 28-37.
16. Martinez-Campos, M., Basto, R., Baker, J., Kernan, M., and Raff, J.W. (2004). The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J. Cell Biol. 165, 673-683.
17. Silkworth, W.T., Nardi, I.K., Scholl, L.M., and Cimini, D. (2009). Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS ONE 4, e6564.
18. Silkworth, W.T., and Cimini, D. (2012). Transient defects of mitotic spindle geometry and chromosome segregation errors. Cell Div. 7, 19.
19. Pandey, R., Heeger, S., and Lehner, C.F. (2007). Rapid effects of acute anoxia on spindle kinetochore interactions activate the mitotic spindle checkpoint. J. Cell Sci. 120, 2807-2818.
20. Schittenhelm, R.B., Heeger, S., Althoff, F., Walter, A., Heidmann, S., Mechtler, K., and Lehner, C.F. (2007). Spatial organization of a ubiquitous eukaryotic kinetochore protein network in Drosophila chromosomes. Chromosoma 116, 385-402.
21. Thompson, S.L., and Compton, D.A. (2010). Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J. Cell Biol. 188, 369-381.
22. Holland, A.J., and Cleveland, D.W. (2012). Losing balance: the origin and impact of aneuploidy in cancer. EMBO Rep. 13, 501-514.
23. Pfau, S.J., and Amon, A. (2012). Chromosomal instability and aneuploidy in cancer: from yeast to man. EMBO Rep. 13, 515-527.
24. Dekanty, A., Barrio, L., Muzzopappa, M., Auer, H., and Milán, M. (2012). Aneuploidy-induced delaminating cells drive tumorigenesis in Drosophila epithelia. Proc. Natl. Acad. Sci. USA 109, 20549-20554.
25. Guilgur, L.G., Prudêncio, P., Ferreira, T., Pimenta-Marques, A.R., and Martinho, R.G. (2012). Drosophila aPKC is required for mitotic spindle orientation during symmetric division of epithelial cells. Development 139, 503-513.
26. Nakajima, Y., Meyer, E.J., Kroesen, A., McKinney, S.A., and Gibson, M.C. (2013). Epithelial junctions maintain tissue architecture by directing planar spindle orientation. Nature 500, 359-362.
27. Poulton, J.S., Cuningham, J.C., and Peifer, M. (2014). Acentrosomal Drosophila epithelial cells exhibit abnormal cell division, leading to cell death and compensatory proliferation. Dev. Cell 30, 731-745.
28. D'Avino, P.P., Savoian, M.S., and Glover, D.M. (2005). Cleavage furrow formation and ingression during animal cytokinesis: a microtubule legacy. J. Cell Sci. 118, 1549-1558.
29. Gisselsson, D., Jin, Y., Lindgren, D., Persson, J., Gisselsson, L., Hanks, S., Sehic, D., Mengelbier, L.H., Øra, I., Rahman, N., et al. (2010). Generation of trisomies in cancer cells by multipolar mitosis and incomplete cytokinesis. Proc. Natl. Acad. Sci. USA 107, 20489-20493.
30. Caussinus, E., and Gonzalez, C. (2005). Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster. Nat. Genet. 37, 1125-1129.
31. Morais da Silva, S., Moutinho-Santos, T., and Sunkel, C.E. (2013). A tumor suppressor role of the Bub3 spindle checkpoint protein after apoptosis inhibition. J. Cell Biol. 201, 385-393.
32. Gonzalez, C. (2013). Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics. Nat. Rev. Cancer 13, 172-183.
33. Uhlirova, M., and Bohmann, D. (2006). JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J. 25, 5294-5304.
34. Polesello, C., and Payre, F. (2004). Small is beautiful: what flies tell us about ERM protein function in development. Trends Cell Biol. 14, 294-302.
35. Kunda, P., and Baum, B. (2009). The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol. 19, 174-179.
36. Kunda, P., Pelling, A.E., Liu, T., and Baum, B. (2008). Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18, 91-101.
37. Vilmos, P., Jankovics, F., Szathmári, M., Lukácsovich, T., Henn, L., and Erdélyi, M. (2009). Live imaging reveals that the Drosophila actin-binding ERM protein, moesin, co-localizes with the mitotic spindle. Eur. J. Cell Biol. 88, 609-619.
38. Lucas, E.P., and Raff, J.W. (2007). Maintaining the proper connection between the centrioles and the pericentriolar matrix requires Drosophila centrosomin. J. Cell Biol. 178, 725-732.
39. Conduit, P.T., Feng, Z., Richens, J.H., Baumbach, J., Wainman, A., Bakshi, S.D., Dobbelaere, J., Johnson, S., Lea, S.M., and Raff, J.W. (2014). The centrosome-specific phosphorylation of Cnn by Polo/Plk1 drives Cnn scaffold assembly and centrosome maturation. Dev. Cell 28, 659-669.
40. Solinet, S., Mahmud, K., Stewman, S.F., Ben El Kadhi, K., Decelle, B., Talje, L., Ma, A., Kwok, B.H., and Carreno, S. (2013). The actin-binding ERM protein Moesin binds to and stabilizes microtubules at the cell cortex. J. Cell Biol. 202, 251-260.
41. Hebert, A.M., DuBoff, B., Casaletto, J.B., Gladden, A.B., and McClatchey, A.I. (2012). Merlin/ERM proteins establish cortical asymmetry and centrosome position. Genes Dev. 26, 2709-2723.
42. Haynes, J., Srivastava, J., Madson, N., Wittmann, T., and Barber, D.L. (2011). Dynamic actin remodeling during epithelial-mesenchymal transition depends on increased moesin expression. Mol. Biol. Cell 22, 4750-4764.
43. Charafe-Jauffret, E., Monville, F., Bertucci, F., Esterni, B., Ginestier, C., Finetti, P., Cervera, N., Geneix, J., Hassanein, M., Rabayrol, L., et al. (2007). Moesin expression is a marker of basal breast carcinomas. Int. J. Cancer 121, 1779-1785.
44. Wang, C.C., Liau, J.Y., Lu, Y.S., Chen, J.W., Yao, Y.T., and Lien, H.C. (2012). Differential expression of moesin in breast cancers and its implication in epithelial-mesenchymal transition. Histopathology 61, 78-87.