An SMC-like protein binds and regulates Caenorhabditis elegans condensins

Structural Maintenance of Chromosomes (SMC) family proteins participate in multisubunit complexes that govern chromosome structure and dynamics. SMC-containing condensin complexes create chromosome topologies essential for mitosis/meiosis, gene expression, recombination, and repair. Many eukaryotes have two condensin complexes (I and II); C. elegans has three (I, II, and the X-chromosome specialized condensin IDC) and their regulation is poorly understood. Here we identify a novel SMC-like protein, SMCL-1, that binds to C. elegans condensin SMC subunits, and modulates condensin functions. Consistent with a possible role as a negative regulator, loss of SMCL-1 partially rescued the lethal and sterile phenotypes of a hypomorphic condensin mutant, while over-expression of SMCL-1 caused lethality, chromosome mis-segregation, and disruption of condensin IDC localization on X chromosomes. Unlike canonical SMC proteins, SMCL-1 lacks hinge and coil domains, and its ATPase domain lacks conserved amino acids required for ATP hydrolysis, leading to the speculation that it may inhibit condensin ATPase activity. SMCL-1 homologs are apparent only in the subset of Caenorhabditis species in which the condensin I and II subunit SMC-4 duplicated to create the condensin IDC- specific subunit DPY-27, suggesting that SMCL-1 helps this lineage cope with the regulatory challenges imposed by evolution of a third condensin complex. Our findings uncover a new regulator of condensins and highlight how the duplication and divergence of SMC complex components in various lineages has created new proteins with diverse functions in chromosome dynamics.

• Publication year

  2017

• Venue

  PLoS Genetics

• Publication date

  2017-03-01

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1371/journal.pgen.1006614PMID 28301465PMCID 5373644
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Explorer Molecular and Genetic Analysis of Condensin Function in Vertebrate Cells

  2017cited by this paper
• Multistep assembly of DNA condensation clusters by SMC

  2016cited by this paper
• SMC complexes: from DNA to chromosomes

  2016cited by this paper
• Condensin-Based Chromosome Organization from Bacteria to Vertebrates.

  2016cited by this paper
• Condensin-Driven Remodeling of X-Chromosome Topology during Dosage Compensation

  2015cited by this paper
• WormBase 2016: expanding to enable helminth genomic research

  2015cited by this paper
• Balancing acts of two HEAT subunits of condensin I support dynamic assembly of chromosome axes.

  2015cited by this paper
• SMC condensin entraps chromosomal DNA by an ATP hydrolysis dependent loading mechanism in Bacillus subtilis

  2015cited by this paper
• Condensin-mediated chromosome organization and gene regulation

  2015cited by this paper
• Disruption of a Conserved CAP-D3 Threonine Alters Condensin Loading on Mitotic Chromosomes Leading to Chromosome Hypercondensation*

  2015cited by this paper
• Drosophila Casein Kinase I Alpha Regulates Homolog Pairing and Genome Organization by Modulating Condensin II Subunit Cap-H2 Levels

  2015cited by this paper
• Interaction between TBP and Condensin Drives the Organization and Faithful Segregation of Mitotic Chromosomes.

  2015cited by this paper
• Balancing up and downregulation of the C. elegans X chromosomes.

  2015cited by this paper
• Control of chromosome interactions by condensin complexes.

  2015cited by this paper
• Regulation of the X chromosomes in Caenorhabditis elegans.

  2014cited by this paper
• The maintenance of chromosome structure: positioning and functioning of SMC complexes

  2014cited by this paper
• Insulator function and topological domain border strength scale with architectural protein occupancy

  2014cited by this paper
• Association of condensin with chromosomes depends on DNA binding by its HEAT-repeat subunits

  2014cited by this paper
• Condensins and the evolution of torsion-mediated genome organization.

  2014cited by this paper
• Genome-wide analysis of condensin binding in Caenorhabditis elegans

  2013cited by this paper
• Ensembl 2014

  2013cited by this paper
• SUMOylation is essential for sex-specific assembly and function of the Caenorhabditis elegans dosage compensation complex on X chromosomes

  2013cited by this paper
• The CRAPome: a Contaminant Repository for Affinity Purification Mass Spectrometry Data

  2013cited by this paper
• Condensin and the spindle midzone prevent cytokinesis failure induced by chromatin bridges in C. elegans embryos.

  2013cited by this paper
• SCFSlimb ubiquitin ligase suppresses condensin II–mediated nuclear reorganization by degrading Cap-H2

  2013cited by this paper
• Condensin: crafting the chromosome landscape

  2013cited by this paper
• A Highly Efficient Multifunctional Tandem Affinity Purification Approach Applicable to Diverse Organisms*

  2012influential reference
• Methods in Cell Biology

  2012cited by this paper
• WormBase

  2012cited by this paper
• Epigenetic regulation of condensin-mediated genome organization during the cell cycle and upon DNA damage through histone H3 lysine 56 acetylation.

  2012cited by this paper
• Contrasting roles of condensin I and condensin II in mitotic chromosome formation

  2012cited by this paper
• Condensin association with histone H2A shapes mitotic chromosomes

  2011cited by this paper
• Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega

  2011influential reference
• Condensin structures chromosomal DNA through topological links

  2011cited by this paper
• Chromosome Segregation: Monopolin Attracts Condensin

  2011cited by this paper
• MCPH1 regulates chromosome condensation and shaping as a composite modulator of condensin II

  2011cited by this paper
• An SMC ATPase mutant disrupts chromosome segregation in Caulobacter

  2011influential reference
• The relative ratio of condensin I to II determines chromosome shapes.

  2011cited by this paper
• Different roles for Aurora B in condensin targeting during mitosis and meiosis

  2011cited by this paper
• Targeting X chromosomes for repression.

  2010cited by this paper
• Targeted gene deletions in C. elegans using transposon excision

  2010cited by this paper
• A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome.

  2009cited by this paper
• Restricting Dosage Compensation Complex Binding to the X Chromosomes by H2A.Z/HTZ-1

  2009cited by this paper
• The cis element and factors required for condensin recruitment to chromosomes.

  2009cited by this paper
• Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure.

  2009cited by this paper
• The NemaGENETAG initiative: large scale transposon insertion gene-tagging in Caenorhabditis elegans

  2009cited by this paper
• Three distinct condensin complexes control C. elegans chromosome dynamics.

  2009influential reference
• Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions.

  2009cited by this paper
• RBF1 promotes chromatin condensation through a conserved interaction with the Condensin II protein dCAP-D3.

  2008cited by this paper
• Single-copy insertion of transgenes in Caenorhabditis elegans

  2008cited by this paper
• SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation

  2008cited by this paper
• Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit.

  2008cited by this paper
• Identification of cis-acting sites for condensin loading onto budding yeast chromosomes.

  2008cited by this paper
• Reconstitution and subunit geometry of human condensin complexes

  2007cited by this paper
• Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae.

  2006cited by this paper
• Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells.

  2006cited by this paper
• Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interactions.

  2006cited by this paper
• Clustered DNA motifs mark X chromosomes for repression by a dosage compensation complex

  2006cited by this paper
• Misregulated Chromosome Condensation in MCPH1 Primary Microcephaly is Mediated by Condensin II

  2006cited by this paper
• Structural biochemistry of ATP-driven dimerization and DNA-stimulated activation of SMC ATPases.

  2004cited by this paper
• Recruitment and Spreading of the C. elegans Dosage Compensation Complex Along X Chromosomes

  2004cited by this paper
• Condensin restructures chromosomes in preparation for meiotic divisions

  2004cited by this paper
• Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously.

  2004cited by this paper
• Distinct functions of condensin I and II in mitotic chromosome assembly

  2004cited by this paper
• Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells.

  2004cited by this paper
• Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners.

  2003cited by this paper
• Identification of a subunit of a novel Kleisin-beta/SMC complex as a potential substrate of protein phosphatase 2A.

  2003cited by this paper
• Recruitment of C. elegans dosage compensation proteins for gene-specific versus chromosome-wide repression

  2003cited by this paper
• The Conserved Glutamate Residue Adjacent to the Walker-B Motif Is the Catalytic Base for ATP Hydrolysis in the ATP-binding Cassette Transporter BmrA*

  2003cited by this paper
• Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells.

  2003cited by this paper
• C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis.

  2002cited by this paper
• Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment.

  2002cited by this paper
• Bimodal activation of SMC ATPase by intra‐ and inter‐molecular interactions

  2001influential reference
• Basic local alignment search tool.

  1990cited by this paper
• Genes that implement the hermaphrodite mode of dosage compensation in Caenorhabditis elegans.

  1989cited by this paper

• Parallel Evolution of X Chromosome-Specific Structural Maintenance of Chromosomes Complexes in Two Nematode Lineages

  2025cites this paper
• Parallel evolution of X chromosome-specific SMC complexes in two nematode lineages

  2024cites this paper
• Mechanisms of sex determination and X-chromosome dosage compensation

  2022cites this paper
• Loss of NSE-4 Perturbs Genome Stability and DNA Repair in Caenorhabditis elegans

  2022cites this paper
• The zebrafish meiotic cohesion complex protein Smc1b is required for 1 key events in meiotic prophase I

  2021cites this paper
• The histone H4 lysine 20 demethylase DPY-21 regulates the dynamics of condensin DC binding

  2021cites this paper
• A noncatalytic activity of the H4K20 demethylase DPY-21 regulates condensin DC binding

  2021cites this paper
• The zebrafish meiotic cohesion complex protein Smc1b is required for key events in meiotic prophase I

  2021cites this paper
• The Zebrafish Meiotic Cohesin Complex Protein Smc1b Is Required for Key Events in Meiotic Prophase I

  2021cites this paper
• Cuminal Inhibits Trichothecium roseum Growth by Triggering Cell Starvation: Transcriptome and Proteome Analysis

  2020cites this paper
• Condensin action and compaction

  2018cites this paper