Literature DB >> 19119011

Three distinct condensin complexes control C. elegans chromosome dynamics.

Gyorgyi Csankovszki1, Karishma Collette, Karin Spahl, James Carey, Martha Snyder, Emily Petty, Uchita Patel, Tomoko Tabuchi, Hongbin Liu, Ian McLeod, James Thompson, Ali Sarkeshik, Ali Sarkesik, John Yates, Barbara J Meyer, Kirsten Hagstrom.   

Abstract

BACKGROUND: Condensin complexes organize chromosome structure and facilitate chromosome segregation. Higher eukaryotes have two complexes, condensin I and condensin II, each essential for chromosome segregation. The nematode Caenorhabditis elegans was considered an exception, because it has a mitotic condensin II complex but appeared to lack mitotic condensin I. Instead, its condensin I-like complex (here called condensin I(DC)) dampens gene expression along hermaphrodite X chromosomes during dosage compensation.
RESULTS: Here we report the discovery of a third condensin complex, condensin I, in C. elegans. We identify new condensin subunits and show that each complex has a conserved five-subunit composition. Condensin I differs from condensin I(DC) by only a single subunit. Yet condensin I binds to autosomes and X chromosomes in both sexes to promote chromosome segregation, whereas condensin I(DC) binds specifically to X chromosomes in hermaphrodites to regulate transcript levels. Both condensin I and II promote chromosome segregation, but associate with different chromosomal regions during mitosis and meiosis. Unexpectedly, condensin I also localizes to regions of cohesion between meiotic chromosomes before their segregation.
CONCLUSIONS: We demonstrate that condensin subunits in C. elegans form three complexes, one that functions in dosage compensation and two that function in mitosis and meiosis. These results highlight how the duplication and divergence of condensin subunits during evolution may facilitate their adaptation to specialized chromosomal roles and illustrate the versatility of condensins to function in both gene regulation and chromosome segregation.

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Year:  2009        PMID: 19119011      PMCID: PMC2682549          DOI: 10.1016/j.cub.2008.12.006

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  45 in total

1.  Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners.

Authors:  Alexander Schleiffer; Susanne Kaitna; Sebastian Maurer-Stroh; Michael Glotzer; Kim Nasmyth; Frank Eisenhaber
Journal:  Mol Cell       Date:  2003-03       Impact factor: 17.970

2.  Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells.

Authors:  Takao Ono; Ana Losada; Michiko Hirano; Michael P Myers; Andrew F Neuwald; Tatsuya Hirano
Journal:  Cell       Date:  2003-10-03       Impact factor: 41.582

3.  Distinct functions of condensin I and II in mitotic chromosome assembly.

Authors:  Toru Hirota; Daniel Gerlich; Birgit Koch; Jan Ellenberg; Jan-Michael Peters
Journal:  J Cell Sci       Date:  2004-11-30       Impact factor: 5.285

Review 4.  Condensins: organizing and segregating the genome.

Authors:  Tatsuya Hirano
Journal:  Curr Biol       Date:  2005-04-12       Impact factor: 10.834

Review 5.  X-Chromosome dosage compensation.

Authors:  Barbara J Meyer
Journal:  WormBook       Date:  2005-06-25

6.  C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis.

Authors:  Kirsten A Hagstrom; Victor F Holmes; Nicholas R Cozzarelli; Barbara J Meyer
Journal:  Genes Dev       Date:  2002-03-15       Impact factor: 11.361

7.  Chromosome morphogenesis: condensin-dependent cohesin removal during meiosis.

Authors:  Hong-Guo Yu; Douglas Koshland
Journal:  Cell       Date:  2005-11-04       Impact factor: 41.582

8.  Condensin regulates rDNA silencing by modulating nucleolar Sir2p.

Authors:  Felix Machín; Konstantinos Paschos; Adam Jarmuz; Jordi Torres-Rosell; Corinna Pade; Luis Aragón
Journal:  Curr Biol       Date:  2004-01-20       Impact factor: 10.834

9.  Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes.

Authors:  Rebecca A Haeusler; Matthew Pratt-Hyatt; Paul D Good; Theresa A Gipson; David R Engelke
Journal:  Genes Dev       Date:  2008-08-15       Impact factor: 11.361

10.  Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment.

Authors:  Jeffrey H Stear; Mark B Roth
Journal:  Genes Dev       Date:  2002-06-15       Impact factor: 11.361

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  89 in total

1.  A highly efficient multifunctional tandem affinity purification approach applicable to diverse organisms.

Authors:  Hanhui Ma; Janel R McLean; Lucy Fang-I Chao; Sebastian Mana-Capelli; Murugan Paramasivam; Kirsten A Hagstrom; Kathleen L Gould; Dannel McCollum
Journal:  Mol Cell Proteomics       Date:  2012-04-03       Impact factor: 5.911

Review 2.  Condensin and cohesin complexity: the expanding repertoire of functions.

Authors:  Andrew J Wood; Aaron F Severson; Barbara J Meyer
Journal:  Nat Rev Genet       Date:  2010-05-05       Impact factor: 53.242

3.  High nucleosome occupancy is encoded at X-linked gene promoters in C. elegans.

Authors:  Sevinç Ercan; Yaniv Lubling; Eran Segal; Jason D Lieb
Journal:  Genome Res       Date:  2010-12-22       Impact factor: 9.043

Review 4.  Nuclear organization and dosage compensation.

Authors:  Jennifer C Chow; Edith Heard
Journal:  Cold Spring Harb Perspect Biol       Date:  2010-10-13       Impact factor: 10.005

Review 5.  C. elegans dosage compensation: a window into mechanisms of domain-scale gene regulation.

Authors:  Sevinc Ercan; Jason D Lieb
Journal:  Chromosome Res       Date:  2009       Impact factor: 5.239

Review 6.  Condensin: Architect of mitotic chromosomes.

Authors:  Damien F Hudson; Kathryn M Marshall; William C Earnshaw
Journal:  Chromosome Res       Date:  2009       Impact factor: 5.239

7.  SUMOylation is essential for sex-specific assembly and function of the Caenorhabditis elegans dosage compensation complex on X chromosomes.

Authors:  Rebecca R Pferdehirt; Barbara J Meyer
Journal:  Proc Natl Acad Sci U S A       Date:  2013-09-16       Impact factor: 11.205

8.  Untangling the Contributions of Sex-Specific Gene Regulation and X-Chromosome Dosage to Sex-Biased Gene Expression in Caenorhabditis elegans.

Authors:  Maxwell Kramer; Prashant Rao; Sevinc Ercan
Journal:  Genetics       Date:  2016-06-29       Impact factor: 4.562

9.  Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution.

Authors:  Bayly S Wheeler; Erika Anderson; Christian Frøkjær-Jensen; Qian Bian; Erik Jorgensen; Barbara J Meyer
Journal:  Elife       Date:  2016-08-30       Impact factor: 8.140

10.  xol-1, the master sex-switch gene in C. elegans, is a transcriptional target of the terminal sex-determining factor TRA-1.

Authors:  Balázs Hargitai; Vera Kutnyánszky; Timothy A Blauwkamp; Attila Steták; Györgyi Csankovszki; Krisztina Takács-Vellai; Tibor Vellai
Journal:  Development       Date:  2009-12       Impact factor: 6.868

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