23
Views
23
CrossRef citations to date
0
Altmetric
Article

The Condensin Complex Is Essential for Amitotic Segregation of Bulk Chromosomes, but Not Nucleoli, in the Ciliate Tetrahymena thermophila

, , &
Pages 4690-4700 | Received 04 Dec 2005, Accepted 13 Apr 2006, Published online: 27 Mar 2023

REFERENCES

  • Allis, C. D., C. V. Glover, J. K. Bowen, and M. A. Gorovsky. 1980. Histone variants specific to the transcriptionally active, amitotically dividing macronucleus of the unicellular eucaryote, Tetrahymena thermophila. Cell 20:609–617.
  • Aono, N., T. Sutani, T. Tomonaga, S. Mochida, and M. Yanagida. 2002. Cnd2 has dual roles in mitotic condensation and interphase. Nature 417:197–202.
  • Bhalla, N., S. Biggins, and A. W. Murray. 2002. Mutation of YCS4, a budding yeast condensin subunit, affects mitotic and nonmitotic chromosome behavior. Mol. Biol. Cell 13:632–645.
  • Bhat, M. A., A. V. Philp, D. M. Glover, and H. J. Bellen. 1996. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with topoisomerase II. Cell 87:1103–1114.
  • Bruns, P. J., and D. Cassidy-Hanley. 2000. Biolistic transformation of macro- and micronuclei. Methods Cell Biol. 62:501–512.
  • Bruns, P. J., A. L. Katzen, L. Martin, and E. H. Blackburn. 1985. A drug-resistant mutation in the ribosomal DNA of Tetrahymena. Proc. Natl. Acad. Sci. USA 82:2844–2846.
  • Cervantes, M. D., X. Xi, D. Vermaak, M. C. Yao, and H. S. Malik. 2006. The CNA1 histone of the ciliate Tetrahymena thermophila is essential for chromosome segregation in the germline micronucleus. Mol. Biol. Cell 17:485–497.
  • Chan, R. C., A. F. Severson, and B. J. Meyer. 2004. Condensin restructures chromosomes in preparation for meiotic divisions. J. Cell Biol. 167:613–625.
  • Chen, E. S., T. Sutani, and M. Yanagida. 2004. Cti1/C1D interacts with condensin SMC hinge and supports the DNA repair function of condensin. Proc. Natl. Acad. Sci. USA 101:8078–8083.
  • Cobbe, N., and M. M. Heck. 2004. The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21:332–347.
  • Coelho, P. A., J. Queiroz-Machado, and C. E. Sunkel. 2003. Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis. J. Cell Sci. 116:4763–4776.
  • Coyne, R. S., M. A. Nikiforov, J. F. Smothers, C. D. Allis, and M. C. Yao. 1999. Parental expression of the chromodomain protein Pdd1p is required for completion of programmed DNA elimination and nuclear differentiation. Mol. Cell 4:865–872.
  • D'Amours, D., F. Stegmeier, and A. Amon. 2004. Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA. Cell 117:455–469.
  • Doerder, F. P., J. C. Deak, and J. H. Lief. 1992. Rate of phenotypic assortment in Tetrahymena thermophila. Dev. Genet. 13:126–132.
  • Flickinger, C. J. 1965. The fine structure of the nuclei of Tetrahymena pyriformis throughout the cell cycle. J. Cell Biol. 27:519–529.
  • Freeman, L., L. Aragon-Alcaide, and A. Strunnikov. 2000. The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J. Cell Biol. 149:811–824.
  • Fujiu, K., and O. Numata. 2000. Reorganization of microtubules in the amitotically dividing macronucleus of tetrahymena. Cell Motil. Cytoskelet. 46:17–27.
  • Gaertig, J., L. Gu, B. Hai, and M. A. Gorovsky. 1994. High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res. 22:5391–5398.
  • Guacci, V., E. Hogan, and D. Koshland. 1994. Chromosome condensation and sister chromatid pairing in budding yeast. J. Cell Biol. 125:517–530.
  • Hagstrom, K. A., V. F. Holmes, N. R. Cozzarelli, and B. J. Meyer. 2002. C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 16:729–742.
  • Hirano, T., R. Kobayashi, and M. Hirano. 1997. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 89:511–521.
  • Hirano, T., and T. J. Mitchison. 1994. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79:449–458.
  • Huang, H., J. F. Smothers, E. A. Wiley, and C. D. Allis. 1999. A nonessential HP1-like protein affects starvation-induced assembly of condensed chromatin and gene expression in macronuclei of Tetrahymena thermophila. Mol. Cell. Biol. 19:3624–3634.
  • Huang, H., E. A. Wiley, C. R. Lending, and C. D. Allis. 1998. An HP1-like protein is missing from transcriptionally silent micronuclei of Tetrahymena. Proc. Natl. Acad. Sci. USA 95:13624–13629.
  • Hudson, D. F., P. Vagnarelli, R. Gassmann, and W. C. Earnshaw. 2003. Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev. Cell 5:323–336.
  • Jaeckel-Williams, R. 1978. Nuclear divisions with reduced numbers of microtubules in Tetrahymena. J. Cell Sci. 34:303–319.
  • Lavoie, B. D., E. Hogan, and D. Koshland. 2004. In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev. 18:76–87.
  • Lavoie, B. D., K. M. Tuffo, S. Oh, D. Koshland, and C. Holm. 2000. Mitotic chromosome condensation requires Brn1p, the yeast homologue of Barren. Mol. Biol. Cell 11:1293–1304.
  • Loidl, J., and H. Scherthan. 2004. Organization and pairing of meiotic chromosomes in the ciliate Tetrahymena thermophila. J. Cell Sci. 117:5791–5801.
  • Marsh, T. C., E. S. Cole, and D. P. Romero. 2001. The transition from conjugal development to the first vegetative cell division is dependent on RAD51 expression in the ciliate Tetrahymena thermophila. Genetics 157:1591–1598.
  • Marsh, T. C., E. S. Cole, K. R. Stuart, C. Campbell, and D. P. Romero. 2000. RAD51 is required for propagation of the germinal nucleus in Tetrahymena thermophila. Genetics 154:1587–1596.
  • McGrath, K. E., J. F. Smothers, C. A. Dadd, M. T. Madireddi, M. A. Gorovsky, and C. D. Allis. 1997. An abundant nucleolar phosphoprotein is associated with ribosomal DNA in Tetrahymena macronuclei. Mol. Biol. Cell 8:97–108.
  • Merriam, E. V., and P. J. Bruns. 1988. Phenotypic assortment in Tetrahymena thermophila: assortment kinetics of antibiotic-resistance markers, tsA, death, and the highly amplified rDNA locus. Genetics 120:389–395.
  • Numata, O., K. Fujiu, and K. Gonda. 1999. Macronuclear division and cytokinesis in Tetrahymena. Cell Biol. Int. 23:849–857.
  • Ono, T., A. Losada, M. Hirano, M. P. Myers, A. F. Neuwald, and T. Hirano. 2003. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115:109–121.
  • Pfitzer, P. 1980. Amitosis: a historical misinterpretation? Pathol. Res. Pract. 167:292–300.
  • Saka, Y., T. Sutani, Y. Yamashita, S. Saitoh, M. Takeuchi, Y. Nakaseko, and M. Yanagida. 1994. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J. 13:4938–4952.
  • Savvidou, E., N. Cobbe, S. Steffensen, S. Cotterill, and M. M. Heck. 2005. Drosophila CAP-D2 is required for condensin complex stability and resolution of sister chromatids. J. Cell Sci. 118:2529–2543.
  • Schmidt, H. A., K. Strimmer, M. Vingron, and A. von Haeseler. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504.
  • Shang, Y., B. Li, and M. A. Gorovsky. 2002. Tetrahymena thermophila contains a conventional gamma-tubulin that is differentially required for the maintenance of different microtubule-organizing centers. J. Cell Biol. 158:1195–1206.
  • Smith, J. J., J. S. Yakisich, G. M. Kapler, E. S. Cole, and D. P. Romero. 2004. A beta-tubulin mutation selectively uncouples nuclear division and cytokinesis in Tetrahymena thermophila. Eukaryot. Cell 3:1217–1226.
  • Steffensen, S., P. A. Coelho, N. Cobbe, S. Vass, M. Costa, B. Hassan, S. N. Prokopenko, H. Bellen, M. M. Heck, and C. E. Sunkel. 2001. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr. Biol. 11:295–307.
  • Strunnikov, A. V. 2005. A case of selfish nucleolar segregation. Cell Cycle 4:113–117.
  • Strunnikov, A. V., E. Hogan, and D. Koshland. 1995. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev. 9:587–599.
  • Stuart, K. R., and E. S. Cole. 2000. Nuclear and cytoskeletal fluorescence microscopy techniques. Methods Cell Biol. 62:291–311.
  • Tucker, J. B., J. Beisson, D. L. Roche, and J. Cohen. 1980. Microtubules and control of macronuclear ‘amitosis’ in Paramecium. J. Cell Sci. 44:135–151.
  • Wang, H., S. Oliferenko, and M. K. Balasubramanian. 2003. Cytokinesis: relative alignment of the cell division apparatus and the mitotic spindle. Curr. Opin. Cell Biol. 15:82–87.
  • Wei, Y., C. A. Mizzen, R. G. Cook, M. A. Gorovsky, and C. D. Allis. 1998. Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc. Natl. Acad. Sci. USA 95:7480–7484.
  • Wiley, E. A., T. Myers, K. Parker, T. Braun, and M. C. Yao. 2005. Class I histone deacetylase Thd1p affects nuclear integrity in Tetrahymena thermophila. Eukaryot. Cell 4:981–990.
  • Williams, N. E., and R. J. Williams. 1976. Macronuclear division with and without microtubules in Tetrahymena. J. Cell Sci. 20:61–77.
  • Wong, L., L. Klionsky, S. Wickert, V. Merriam, E. Orias, and E. P. Hamilton. 2000. Autonomously replicating macronuclear DNA pieces are the physical basis of genetic coassortment groups in Tetrahymena thermophila. Genetics 155:1119–1125.
  • Yao, M. C., and J. L. Chao. 2005. RNA-guided DNA deletion in Tetrahymena: an RNAi-based mechanism for programmed genome rearrangements. Annu. Rev. Genet. 39:537–559.
  • Yao, M. C., P. Fuller, and X. Xi. 2003. Programmed DNA deletion as an RNA-guided system of genome defense. Science 300:1581–1584.
  • Zhong, D., and S. P. Bajaj. 1993. A PCR-based method for site-specific domain replacement that does not require restriction recognition sequences. BioTechniques 15:874–878.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.