A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A

Nature Cell Biology

Volumn 12, Issue 12, 2010, Pages 1186-1193

  Lagana, Anaïck ^a,b   Dorn, Jonas F ^a,b   De Rop, Valérie ^a   Ladouceur, Anne Marie ^a   Maddox, Amy S ^a,b   Maddox, Paul S ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FACTOR; CENTROMERE PROTEIN A; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN CDC42; PROTEIN ECT2; PROTEIN HSKNL2; PROTEIN MGCRACGAP; RAC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CENTROMERE; CONTROLLED STUDY; ENZYME ACTIVITY; EPIGENETICS; FUNCTIONAL PROTEOMICS; HELA CELL; HUMAN; HUMAN CELL; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

ANIMALS; AUTOANTIGENS; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA REPLICATION; EPIGENESIS, GENETIC; HUMANS; MONOMERIC GTP-BINDING PROTEINS;

EID: 78649835035     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb2129     Document Type: Article

References (52)

1. Goldberg, A. D., Allis, C. D. & Bernstein, E. Epigenetics: a landscape takes shape. Cell 128, 635-638 (2007).
2. Karpen, G. H. & Allshire, R. C. The case for epigenetic effects on centromere identity and function. Trends Genet. 13, 489-496 (1997).
3. Palmer, D. K., O'Day, K., Trong, H. L., Charbonneau, H. & Margolis, R. L. Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone. Proc. Natl Acad. Sci. USA 88, 3734-3738 (1991).
4. Choo, K. H. Centromerization. Trends Cell Biol. 10, 182-188 (2000).
5. Bernad, R., Sanchez, P. & Losada, A. Epigenetic specification of centromeres by CENP-A. Exp. Cell Res. 315, 3233-3241 (2009).
6. Sullivan, K. F., Hechenberger, M. & Masri, K. Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J. Cell Biol. 127, 581-592 (1994).
7. Cleveland, D. W., Mao, Y. & Sullivan, K. F. Centromeres and kinetochores: from epige-netics to mitotic checkpoint signaling. Cell 112, 407-421 (2003).
8. Schuh, M., Lehner, C. F. & Heidmann, S. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17, 237-243 (2007).
9. Jansen, L. E., Black, B. E., Foltz, D. R. & Cleveland, D. W. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176, 795-805 (2007).
10. Hayashi, T. et al. Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118, 715-729 (2004).
11. Fujita, Y. et al. Priming of centromere for CENP-A recruitment by human hMis18α, hMis18β, and M18BP1. Dev. Cell 12, 17-30 (2007).
12. Maddox, P. S., Hyndman, F., Monen, J., Oegema, K. & Desai, A. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J. Cell Biol. 176, 757-763 (2007).
13. Foltz, D. R. et al. Centromere-specific assembly of CENP-A nucleosomes is mediated by HJURP. Cell 137, 472-484 (2009).
14. Dunleavy, E. M. et al. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137, 485-497 (2009).
15. Silva, M. C. & Jansen, L. E. At the right place at the right time: novel CENP-A binding proteins shed light on centromere assembly. Chromosoma 118, 567-574 (2009).
16. Perpelescu, M., Nozaki, N., Obuse, C., Yang, H. & Yoda, K. Active establishment of cen-tromeric CENP-A chromatin by RSF complex. J. Cell Biol. 185, 397-407 (2009).
17. Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629-635 (2002).
18. Izuta, H. et al. Comprehensive analysis of the ICEN (interphase centromere complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11, 673-684 (2006).
19. Kawashima, T. et al. MgcRacGAP is involved in the control of growth and differentiation of hematopoietic cells. Blood 96, 2116-2124 (2000).
20. Minoshima, Y. et al. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev. Cell 4, 549-560 (2003).
21. Toure, A. et al. MgcRacGAP, a new human GTPase-activating protein for Rac and Cdc42 similar to Drosophila rotundRacGAP gene product, is expressed in male germ cells. J. Biol. Chem. 273, 6019-6023 (1998).
22. Yuce, O., Piekny, A. & Glotzer, M. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J. Cell Biol. 170, 571-582 (2005).
23. Canman, J. C. et al. Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science 322, 1543-1546 (2008).
24. Miller, A. L. & Bement, W. M. Regulation of cytokinesis by Rho GTPase flux. Nat. Cell Biol. 11, 71-77 (2009).
25. Hirose, K., Kawashima, T., Iwamoto, I., Nosaka, T. & Kitamura, T. MgcRacGAP is involved in cytokinesis through associating with mitotic spindle and midbody. J. Biol. Chem. 276, 5821-5828 (2001).
26. Jantsch-Plunger, V. et al. CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149, 1391-1404 (2000).
27. Pavicic-Kaltenbrunner, V., Mishima, M. & Glotzer, M. Cooperative assembly of CYK-4/ MgcRacGAP and ZEN-4/MKLP1 to form the centralspindlin complex. Mol. Biol. Cell 18, 4992-5003 (2007).
28. Maddox, A. S. & Oegema, K. Closing the GAP: a role for a RhoA GAP in cytokinesis. Mol. Cell 11, 846-848 (2003).
29. Black, B. E. et al. Centromere identity maintained by nucleosomes assembled with his-tone H3 containing the CENP-A targeting domain. Mol. Cell 25, 309-322 (2007).
30. Foltz, D. R. et al. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8, 458-469 (2006).
31. Von Dassow, G., Verbrugghe, K. J., Miller, A. L., Sider, J. R. & Bement, W. M. Action at a distance during cytokinesis. J. Cell Biol. 187, 831-845 (2009).
32. Yasuda, S. et al. Cdc42 and mDia3 regulate microtubule attachment to kinetochores. Nature 428, 767-771 (2004).
33. Oceguera-Yanez, F. et al. Ect2 and MgcRacGAP regulate the activation and function of Cdc42 in mitosis. J. Cell Biol. 168, 221-232 (2005).
34. Sanders, L. C., Matsumura, F., Bokoch, G. M. & de Lanerolle, P. Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085 (1999).
35. Rando, O. J., Zhao, K. & Crabtree, G. R. Searching for a function for nuclear actin. Trends Cell Biol. 10, 92-97 (2000).
36. Glotzer, M. The molecular requirements for cytokinesis. Science 307, 1735-1739 (2005).
37. Maddox, A. S. & Oegema, K. Deconstructing cytokinesis. Nat. Cell Biol. 5, 773-776 (2003).
38. Field, C., Li, R. & Oegema, K. Cytokinesis in eukaryotes: a mechanistic comparison. Curr. Opin. Cell Biol. 11, 68-80 (1999).
39. Chen, M. & Shen, X. Nuclear actin and actin-related proteins in chromatin dynamics. Curr. Opin. Cell Biol. 19, 326-330 (2007).
40. Tomonaga, T. et al. Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res. 63, 3511-3516 (2003).
41. Collins, K. A., Furuyama, S. & Biggins, S. Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr. Biol. 14, 1968-1972 (2004).
42. Ye, J., Zhao, J., Hoffmann-Rohrer, U. & Grummt, I. Nuclear myosin I acts in concert with polymeric actin to drive RNA polymerase I transcription. Genes Dev. 22, 322-330 (2008).
43. Theriot, J. A., Mitchison, T. J., Tilney, L. G. & Portnoy, D. A. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357, 257-260 (1992).
44. Stelzer, E. H., Wacker, I. & De Mey, J. R. Confocal fluorescence microscopy in modern cell biology. Semin. Cell Biol. 2, 145-152 (1991).
45. Otsu, N. A threshold selection method from gray-level histograms. IEEE Transactions Syst. Man Cybern. 9, 62-66 (1979).
46. Lindeberg, T. & Eklundh, J. O. Scale detection and region extraction from a scale-space primal sketch. Proc. 3rd International Conference on Computer Vision (Osaka, Japan) 416-426 (1990).
47. Dorn, J. F., Danuser, G. & Yang, G. Computational processing and analysis of dynamic fluorescence image data. Methods Cell Biol. 85, 497-538 (2008).
48. Jaqaman, K. et al. Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases. J. Cell Biol. 188, 665-679 (2010).
49. Dorn, J. F. et al. Yeast kinetochore microtubule dynamics analyzed by high-resolution three-dimensional microscopy. Biophys. J. 89, 2835-2854 (2005).
50. Carroll, C. W., Silva, M. C., Godek, K. M., Jansen, L. E. & Straight, A. F. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 11, 896-902 (2009).
51. Cheeseman, I. M. & Desai, A. A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci STKE 2005, pl1 (2005).
52. Cheeseman, I. M. et al. A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev. 18, 2255-2268 (2004).