Dyskerin, tRNA genes, and condensin tether pericentric chromatin to the spindle axis in mitosis

Journal of Cell Biology

Volumn 207, Issue 2, 2014, Pages 189-199

  Snider, Chloe E ^a   Stephens, Andrew D ^a   Kirkland, Jacob G ^b   Hamdani, Omar ^b   Kamakaka, Rohinton T ^b   Bloom, Kerry ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONDENSIN; DYSKERIN; TRANSFER RNA; ADENOSINE TRIPHOSPHATASE; CBF5 PROTEIN, S CEREVISIAE; CHROMATIN; DNA BINDING PROTEIN; HYDROLYASE; MICROTUBULE ASSOCIATED PROTEIN; MULTIPROTEIN COMPLEX; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; CENTROMERE; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; KINETOCHORE MICROTUBULE; LACTOSE OPERON; METAPHASE; MITOSIS SPINDLE; NONHUMAN; PERICENTRIC CHROMATIN; PERICENTROMERE; PROTEIN RNA BINDING; REGULATORY MECHANISM; RNA GENE; SCHIZOSACCHAROMYCES POMBE; TRANSFER RNA GENE; WILD TYPE; CENTROSOME; CYTOLOGY; GENETICS; METABOLISM; MITOSIS; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; SPINDLE APPARATUS; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATASES; CENTROSOME; CHROMATIN; DNA-BINDING PROTEINS; HYDRO-LYASES; KINETOCHORES; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MULTIPROTEIN COMPLEXES; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPINDLE APPARATUS;

EID: 84910616376     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201405028     Document Type: Article

References (40)

1. Alawi, F., and P. Lin. 2013. Dyskerin localizes to the mitotic apparatus and is required for orderly mitosis in human cells. PLoS ONE. 8:e80805. http:/ dx.doi.org/10.1371/journal.pone.008080
2. Blat, Y., and N. Kleckner. 1999. Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell. 98:249-259. http://dx.doi.org/10.1016/S0092-8674(00)81019
3. Bressan, D.A., J. Vazquez, and J.E. Haber. 2004. Mating type-dependent constraints on the mobility of the left arm of yeast chromosome III. J. Cell Biol. 164:361-371. http://dx.doi.org/10.1083/jcb.20031106
4. Brito, I.L., F. Monje-Casas, and A. Amon. 2010. The Lrs4-Csm1 monopolin complex associates with kinetochores during anaphase and is required for accurate chromosome segregation. Cell Cycle. 9:3611-3618. http://dx .doi.org/10.4161/cc.9.17.1288
5. Burrack, L.S., S.E. Applen Clancey, J.M. Chacón, M.K. Gardner, and J. Berman. 2013. Monopolin recruits condensin to organize centromere DNA and repetitive DNA sequences. Mol. Biol. Cell. 24:2807-2819. http://dx.doi .org/10.1091/mbc.E13-05-022
6. D'Ambrosio, C., C.K. Schmidt, Y. Katou, G. Kelly, T. Itoh, K. Shirahige, and F. Uhlmann. 2008. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev. 22:2215-2227. http://dx .doi.org/10.1101/gad.167570
7. Donze, D., C.R. Adams, J. Rine, and R.T. Kamakaka. 1999. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev. 13:698-708. http://dx.doi.org/10.1101/gad.13.6.69
8. Gardano, L., L. Holland, R. Oulton, T. Le Bihan, and L. Harrington. 2012. Native gel electrophoresis of human telomerase distinguishes active complexes with or without dyskerin. Nucleic Acids Res. 40:e36. http://dx.doi.org/ 10.1093/nar/gkr124
9. Goshima, G., and M. Yanagida. 2000. Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell. 100:619-633. http://dx.doi.org/ 10.1016/S0092-8674(00)80699
10. Gu, B., M. Bessler, and P.J. Mason. 2009. Dyskerin, telomerase and the DNA damage response. Cell Cycle. 8:6-10. http://dx.doi.org/10.4161/cc.8.1.726
11. Haeusler, R.A., M. Pratt-Hyatt, P.D. Good, T.A. Gipson, and D.R. Engelke. 2008. Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev. 22:2204-2214. http://dx.doi.org/10.1101/gad.167590
12. Hirano, T. 2006. At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol. 7:311-322. http://dx.doi.org/10.1038/nrm190
13. Hoang, C., and A.R. Ferré-D'Amaré. 2001. Cocrystal structure of a tRNA Psi5 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzyme. Cell. 107:929-939. http://dx.doi.org/10.1016/S0092-8674(01)00618
14. Iwasaki, O., and K. Noma. 2012. Global genome organization mediated by RNA polymerase III-transcribed genes in fission yeast. Gene. 493:195-200. http://dx.doi.org/10.1016/j.gene.2010.12.011
15. Janke, C., M.M. Magiera, N. Rathfelder, C. Taxis, S. Reber, H. Maekawa, A. Moreno-Borchart, G. Doenges, E. Schwob, E. Schiebel, and M. Knop. 2004. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast. 21:947-962. http://dx.doi.org/10.1002/yea.114
16. Jiang, W., K. Middleton, H.J. Yoon, C. Fouquet, and J. Carbon. 1993. An essential yeast protein, CBF5p, binds in vitro to centromeres and microtubules. Mol. Cell. Biol. 13:4884-4893.
17. Kendall, A., M.W. Hull, E. Bertrand, P.D. Good, R.H. Singer, and D.R. Engelke. 2000. A CBF5 mutation that disrupts nucleolar localization of early tRNA biosynthesis in yeast also suppresses tRNA gene-mediated transcriptional silencing. Proc. Natl. Acad. Sci. USA. 97:13108-13113. http://dx.doi .org/10.1073/pnas.24045499
18. Kirkland, J.G., and R.T. Kamakaka. 2013. Long-range heterochromatin association is mediated by silencing and double-strand DNA break repair proteins. J. Cell Biol. 201:809-826. http://dx.doi.org/10.1083/jcb.
19. Kuhn, R.M., L. Clarke, and J. Carbon. 1991. Clustered tRNA genes in Schizosaccharomyces pombe centromeric DNA sequence repeats. Proc. Natl. Acad. Sci. USA. 88:1306-1310. http://dx.doi.org/10.1073/pnas.88.4.130
20. Liao, C., C. Rovira, H. He, and J.E. Edström. 1998. Site-specific insertion of a SINE-like element, Cp1, into centromeric tandem repeats from Chironomus pallidivittatus. J. Mol. Biol. 280:811-820. http://dx.doi.org/10.1006/ jmbi.1998.189
21. Megee, P.C., C. Mistrot, V. Guacci, and D. Koshland. 1999. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences. Mol. Cell. 4:445-450. http://dx.doi.org/10.1016/S1097-2765(00)80347
22. Moqtaderi, Z., J. Wang, D. Raha, R.J. White, M. Snyder, Z. Weng, and K. Struhl. 2010. Genomic binding profiles of functionally distinct RNA polymerase III transcription complexes in human cells. Nat. Struct. Mol. Biol. 17:635-640. http://dx.doi.org/10.1038/nsmb.179
23. Mumberg, D., R. Müller, and M. Funk. 1994. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22:5767-5768. http://dx.doi.org/10.1093/nar/22.25.576
24. Pearson, C.G., P.S. Maddox, E.D. Salmon, and K. Bloom. 2001. Budding yeast chromosome structure and dynamics during mitosis. J. Cell Biol. 152:1255- 1266. http://dx.doi.org/10.1083/jcb.152.6.125
25. Raab, J.R., J. Chiu, J. Zhu, S. Katzman, S. Kurukuti, P.A. Wade, D. Haussler, and R.T. Kamakaka. 2012. Human tRNA genes function as chromatin insulators. EMBO J. 31:330-350. http://dx.doi.org/10.1038/emboj.2011.40
26. Renshaw, M.J., J.J. Ward, M. Kanemaki, K. Natsume, F.J. Nédélec, and T.U. Tanaka. 2010. Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev. Cell. 19:232-244. http://dx.doi.org/10.1016/j.devcel.2010.07.01
27. Ribeiro, S.A., J.C. Gatlin, Y. Dong, A. Joglekar, L. Cameron, D.F. Hudson, C.J. Farr, B.F. McEwen, E.D. Salmon, W.C. Earnshaw, and P. Vagnarelli. 2009. Condensin regulates the stiffness of vertebrate centromeres. Mol. Biol. Cell. 20:2371-2380. http://dx.doi.org/10.1091/mbc.E08-11-112
28. Robinett, C.C., A. Straight, G. Li, C. Willhelm, G. Sudlow, A. Murray, and A.S. Belmont. 1996. In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J. Cell Biol. 135:1685-1700. http://dx.doi.org/10.1083/jcb.135.6.168
29. Rohner, S., S.M. Gasser, and P. Meister. 2008. Modules for cloning-free chromatin tagging in Saccharomyces cerevisiae. Yeast. 25:235-239. http://dx.doi .org/10.1002/yea.158
30. Rovira, C., and J.E. Edström. 1996. Centromeric polymerase III transcription units in Chironomus pallidivittatus. Nucleic Acids Res. 24:1662-1668. http://dx.doi.org/10.1093/nar/24.9.166
31. Scott, K.C., C.V. White, and H.F. Willard. 2007. An RNA polymerase III-dependent heterochromatin barrier at fission yeast centromere 1. PLoS ONE. 2:e1099. http://dx.doi.org/10.1371/journal.pone.000109
32. Stephens, A.D., J. Haase, L. Vicci, R.M. Taylor II, and K. Bloom. 2011. Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring. J. Cell Biol. 193:1167-1180. http://dx.doi.org/ 10.1083/jcb.20110313
33. Stephens, A.D., R.A. Haggerty, P.A. Vasquez, L. Vicci, C.E. Snider, F. Shi, C. Quammen, C. Mullins, J. Haase, R.M. Taylor II, et al. 2013a. Pericentric chromatin loops function as a nonlinear spring in mitotic force balance. J. Cell Biol. 200:757-772. http://dx.doi.org/10.1083/jcb.20120816
34. Stephens, A.D., C.W. Quammen, B. Chang, J. Haase, R.M. Taylor II, and K. Bloom. 2013b. The spatial segregation of pericentric cohesin and condensin in the mitotic spindle. Mol. Biol. Cell. 24:3909-3919. http://dx.doi .org/10.1091/mbc.E13-06-032
35. Stephens, A.D., C.E. Snider, J. Haase, R.A. Haggerty, P.A. Vasquez, M.G. Forest, and K. Bloom. 2013c. Individual pericentromeres display coordinated motion and stretching in the yeast spindle. J. Cell Biol. 203:407-416. http://dx.doi.org/10.1083/jcb.201307104
36. Straight, A.F., A.S. Belmont, C.C. Robinett, and A.W. Murray. 1996. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion. Curr. Biol. 6:1599-1608. http://dx.doi.org/10.1016/S0960-9822(02)70783
37. Van Bortle, K., M.H. Nichols, L. Li, C.T. Ong, N. Takenaka, Z.S. Qin, and V.G. Corces. 2014. Insulator function and topological domain border strength scale with architectural protein occupancy. Genome Biol. 15:R82. http:/ dx.doi.org/10.1186/gb-2014-15-5-r8
38. Verdaasdonk, J.S., P.A. Vasquez, R.M. Barry, T. Barry, S. Goodwin, M.G. Forest, and K. Bloom. 2013. Centromere tethering confines chromosome domains. Mol. Cell. 52:819-831. http://dx.doi.org/10.1016/j.molcel.2013.10.02
39. Wach, A., A. Brachat, C. Alberti-Segui, C. Rebischung, and P. Philippsen. 1997. Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast. 13:1065-1075. http://dx.doi.org/10.1002/(SICI)1097-0061(19970915)13:11 <1065::AID-YEA159>3.0.CO;2-K
40. Yong-Gonzalez, V., B.D. Wang, P. Butylin, I. Ouspenski, and A. Strunnikov. 2007. Condensin function at centromere chromatin facilitates proper kinetochore tension and ensures correct mitotic segregation of sister chromatids. Genes Cells. 12:1075-1090. http://dx.doi.org/10.1111/j.1365-2443.2007.01109.x