GAS2L3, a target gene of the DREAM complex, is required for proper cytokinesis and genomic stability

Journal of Cell Science

Volumn 125, Issue 10, 2012, Pages 2393-2406

  Wolter, Patrick ^a   Schmitt, Kathrin ^a   Fackler, Marc ^a   Kremling, Heidi ^a   Probst, Leona ^a   Hauser, Stefanie ^a   Gruss, Oliver J ^b   Gaubatz, Stefan ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL CYCLE PROTEIN; DREAM COMPLEX; F ACTIN; MESSENGER RNA; PROTEIN GAS2L3; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ANEUPLOIDY; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CHROMATIN; CHROMOSOME LOSS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOKINESIS; GENE TARGETING; GENOMIC INSTABILITY; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERPHASE; MICROTUBULE; MITOSIS SPINDLE; MULTINUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; RNA INTERFERENCE;

CYTOKINESIS; GENOMIC INSTABILITY; HELA CELLS; HUMANS; KV CHANNEL-INTERACTING PROTEINS; MICROFILAMENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PROTEIN BINDING; PROTEIN TRANSPORT; REPRESSOR PROTEINS;

MAMMALIA;

EID: 84864796136     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.097253     Document Type: Article

References (50)

1. Andersson, A., Ritz, C., Lindgren, D., Edén, P., Lassen, C., Heldrup, J., Olofsson, T., Råde, J., Fontes, M., Porwit-Macdonald, A. et al. (2007). Microarray-based classification of a consecutive series of 121 childhood acute leukemias: prediction of leukemic and genetic subtype as well as of minimal residual disease status. Leukemia 21, 1198-1203.
2. Brancolini, C., Bottega, S. and Schneider, C. (1992). Gas2, a growth arrest-specific protein, is a component of the microfilament network system. J. Cell Biol. 117, 1251-1261.
3. Bredel, M., Bredel, C., Juric, D., Harsh, G. R., Vogel, H., Recht, L. D. and Sikic, B. I. (2005). Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYC-interacting genes in human gliomas. Cancer Res. 65, 8679-8689.
4. Burkhart, D. L. and Sage, J. (2008). Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat. Rev. Cancer 8, 671-682.
5. Cai, S., Weaver, L. N., Ems-McClung, S. C. and Walczak, C. E. (2010). Proper organization of microtubule minus ends is needed for midzone stability and cytokinesis. Curr. Biol. 20, 880-885.
6. Cobrinik, D. (2005). Pocket proteins and cell cycle control. Oncogene 24, 2796-2809.
7. Dimova, D. K. and Dyson, N. J. (2005). The E2F transcriptional network: old acquaintances with new faces. Oncogene 24, 2810-2826.
8. Eggert, U. S., Mitchison, T. J. and Field, C. M. (2006). Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75, 543-566.
9. Gagrica, S., Hauser, S., Kolfschoten, I., Osterloh, L., Agami, R. and Gaubatz, S. (2004). Inhibition of oncogenic transformation by mammalian Lin-9, a pRBassociated protein. EMBO J. 23, 4627-4638.
10. Goriounov, D., Leung, C. L. and Liem, R. K. H. (2003). Protein products of human Gas2-related genes on chromosomes 17 and 22 (hGAR17 and hGAR22) associate with both microfilaments and microtubules. J. Cell Sci. 116, 1045-1058.
11. Gromley, A., Yeaman, C., Rosa, J., Redick, S., Chen, C.-T., Mirabelle, S., Guha, M., Sillibourne, J. and Doxsey, S. J. (2005). Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123, 75-87.
12. Hickson, G. R. X. and O'Farrell, P. H. (2008). Anillin: a pivotal organizer of the cytokinetic machinery. Biochem. Soc. Trans. 36, 439-441.
13. Holland, A. J. and Cleveland, D. W. (2009). Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat. Rev. Mol. Cell Biol. 10, 478-487.
14. Kittler, R., Pelletier, L., Heninger, A.-K., Slabicki, M., Theis, M., Miroslaw, L., Poser, I., Lawo, S., Grabner, H., Kozak, K. et al. (2007). Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat. Cell Biol. 9, 1401-1412.
15. Knight, A. S., Notaridou, M. and Watson, R. J. (2009). A Lin-9 complex is recruited by B-Myb to activate transcription of G2/M genes in undifferentiated embryonal carcinoma cells. Oncogene 28, 1737-1747.
16. Lengauer, C., Kinzler, K. W. and Vogelstein, B. (1997). Genetic instability in colorectal cancers. Nature 386, 623-627.
17. Litovchick, L., Sadasivam, S., Florens, L., Zhu, X., Swanson, S. K., Velmurugan, S., Chen, R., Washburn, M. P., Liu, X. S. and DeCaprio, J. A. (2007). Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 26, 539-551.
18. Matuliene, J. and Kuriyama, R. (2002). Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells. Mol. Biol. Cell 13, 1832-1845.
19. Michel, L. S., Liberal, V., Chatterjee, A., Kirchwegger, R., Pasche, B., Gerald, W., Dobles, M., Sorger, P. K., Murty, V. V. and Benezra, R. (2001). MAD2 haploinsufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409, 355-359.
20. Miller, A. L., Wang, Y., Mooseker, M. S. and Koleske, A. J. (2004). The Abl-related gene (Arg) requires its F-actin-microtubule cross-linking activity to regulate lamellipodial dynamics during fibroblast adhesion. J. Cell Biol. 165, 407-419.
21. Mishima, M., Kaitna, S. and Glotzer, M. (2002). Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell 2, 41-54.
22. Mitchison, T. and Kirschner, M. (1984). Microtubule assembly nucleated by isolated centrosomes. Nature 312, 232-237.
23. Mollinari, C., Kleman, J.-P., Jiang, W., Schoehn, G., Hunter, T. and Margolis, R. L. (2002). PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157, 1175-1186.
24. Narumiya, S. and Yasuda, S. (2006). Rho GTPases in animal cell mitosis. Curr. Opin. Cell Biol. 18, 199-205.
25. Osterloh, L., von Eyss, B., Schmit, F., Rein, L., Hübner, D., Samans, B., Hauser, S. and Gaubatz, S. (2007). The human synMuv-like protein LIN-9 is required for transcription of G2/M genes and for entry into mitosis. EMBO J. 26, 144-157.
26. Piekny, A. J. and Glotzer, M. (2008). Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr. Biol. 18, 30-36.
27. Piekny, A. J. and Maddox, A. S. (2010). The myriad roles of Anillin during cytokinesis. Semin. Cell Dev. Biol. 21, 881-891.
28. Piekny, A., Werner, M. and Glotzer, M. (2005). Cytokinesis: welcome to the Rho zone. Trends Cell Biol. 15, 651-658.
29. Pilkinton, M., Sandoval, R. and Colamonici, O. R. (2007a). Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cyclephase-dependent context distinct from the Drosophila dREAM complex. Oncogene 26, 7535-7543.
30. Pilkinton, M., Sandoval, R., Song, J., Ness, S. A. and Colamonici, O. R. (2007b). Mip/LIN-9 regulates the expression of B-Myb and the induction of cyclin A, cyclin B, and CDK1. J. Biol. Chem. 282, 168-175.
31. Pohl, C. and Jentsch, S. (2008). Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 132, 832-845.
32. Rankin, K. E. and Wordeman, L. (2010). Long astral microtubules uncouple mitotic spindles from the cytokinetic furrow. J. Cell Biol. 190, 35-43.
33. Reichert, N., Wurster, S., Ulrich, T., Schmitt, K., Hauser, S., Probst, L., Götz, R., Ceteci, F., Moll, R., Rapp, U. et al. (2010). Lin9, a subunit of the mammalian DREAM complex, is essential for embryonic development, for survival of adult mice, and for tumor suppression. Mol. Cell. Biol. 30, 2896-2908.
34. Sagona, A. P. and Stenmark, H. (2010). Cytokinesis and cancer. FEBS Lett. 584, 2652-2661.
35. Schmit, F., Korenjak, M., Mannefeld, M., Schmitt, K., Franke, C., von Eyss, B., Gagrica, S., Hänel, F., Brehm, A. and Gaubatz, S. (2007). LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6, 1903-1913.
36. Schmit, F., Cremer, S. and Gaubatz, S. (2009). LIN54 is an essential core subunit of the DREAM/LINC complex that binds to the cdc2 promoter in a sequence-specific manner. FEBS J. 276, 5703-5716.
37. Schneider, C., King, R. M. and Philipson, L. (1988). Genes specifically expressed at growth arrest of mammalian cells. Cell 54, 787-793.
38. Smith, D. S., Niethammer, M., Ayala, R., Zhou, Y., Gambello, M. J., Wynshaw-Boris, A. and Tsai, L. H. (2000). Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nat. Cell Biol. 2, 767-775.
39. Steigemann, P., Wurzenberger, C., Schmitz, M. H. A., Held,M., Guizetti, J., Maar, S. and Gerlich, D. W. (2009). Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-484.
40. Straight, A. F., Field, C. M. and Mitchison, T. J. (2005). Anillin binds nonmuscle myosin II and regulates the contractile ring. Mol. Biol. Cell 16, 193-201.
41. Stroud, M. J., Kammerer, R. A. and Ballestrem, C. (2011). Characterization of G2L3 (GAS2-like 3), a new microtubule- and actin-binding protein related to spectraplakins. J. Biol. Chem. 286, 24987-24995.
42. Sun, L., Hui, A.-M., Su, Q., Vortmeyer, A., Kotliarov, Y., Pastorino, S., Passaniti, A., Menon, J., Walling, J., Bailey, R. et al. (2006). Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell 9, 287-300.
43. Tighe, A., Staples, O. and Taylor, S. (2008). Mps1 kinase activity restrains anaphase during an unperturbed mitosis and targets Mad2 to kinetochores. J. Cell Biol. 181, 893-901.
44. Toso, A., Winter, J. R., Garrod, A. J., Amaro, A. C., Meraldi, P. and McAinsh, A. D. (2009). Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly. J. Cell Biol. 184, 365-372.
45. Trimarchi, J. M. and Lees, J. A. (2002). Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3, 11-20.
46. van den Heuvel, S. and Dyson, N. J. (2008). Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9, 713-724.
47. 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.
48. Wyler, E., Zimmermann, M., Widmann, B., Gstaiger, M., Pfannstiel, J., Kutay, U. and Zemp, I. (2011). Tandem affinity purification combined with inducible shRNA expression as a tool to study the maturation of macromolecular assemblies. RNA 17, 189-200.
49. Zhao, W.-M. and Fang, G. (2005). Anillin is a substrate of anaphase-promoting complex/cyclosome (APC/C) that controls spatial contractility of myosin during late cytokinesis. J. Biol. Chem. 280, 33516-33524.
50. Zucman-Rossi, J., Legoix, P. and Thomas, G. (1996). Identification of new members of the Gas2 and Ras families in the 22q12 chromosome region. Genomics 38, 247-254.