How Chromatin Motor Complexes Influence the Nuclear Architecture: A Review of Chromatin Organization, Cohesins, and Condensins with a Focus on C. elegans

Abstract

Chromatin is the complex of DNA and associated proteins found in the nuclei of living organisms. How it is organized is a major research field as it has implications for replication, repair, and gene expression. This review summarizes the current state of the chromatin organization field, with a special focus on chromatin motor complexes cohesin and condensin. Containing the highly conserved SMC proteins, these complexes are responsible for organizing chromatin during cell division. Additionally, research has demonstrated that condensin and cohesin also have important functions during interphase to shape the organization of chromatin and regulate expression of genes. Using the model organism C. elegans, the authors review the current knowledge of how these complexes perform such diverse roles and what open questions still exist in the field.

Keywords: C. elegans; SMC proteins; TADs; chromatin architecture; cohesin; condensin; dosage compensation.

Figure 1.

SMC protein folding. An SMC protein is shown at the top with globular N and C terminal domains that are separated by a pair of alpha-helices on either side of a “hinge” domain. Once the hinge folds on itself, the two alpha-helices make up a coiled-coil, which allows for the N and C terminal domains to interact as the ATPase “head”. The coiled-coil is sometimes referred to as an “arm” with an “elbow”, where flexible bends can occur.

Figure 2.

Chromatin motor complexes in Caenorhabditis elegans. SMC proteins that interact with the N-terminus of the kleisin are in pink or purple, while SMC proteins that interact with the C-terminus of the kleisin are in orange or yellow. Kleisins are in shades of blue. HAWKs are in shades of green, and Kites are in shades of red. (A) The 4 subunits of cohesin in the closed ring conformation, shown here with the C. elegans subunit names. (B) Condensin I, condensin II, and condensin I^DC are shown in the closed ring conformation, shown here with the C. elegans subunit names. (C) The SMC-5/6 complex is shown here with the characteristic “boomerang” shape and C. elegans subunit names.

Figure 3.

Chromatin motor complex localization during C. elegans cell division. (A) In mitosis, cohesin is already present on the chromosomes before S-phase. After replication, cohesin is responsible for cohesion between the sister chromatids. Condensin II localizes to the chromosomes during prophase, while condensin I localizes to the chromosomes after nuclear envelope breakdown in prometaphase. In anaphase, cohesin is removed and a portion of condensin I moves to the spindle midzone. (B) In meiosis, cohesin is present along the chromosomes. After homologous recombination, condensin II localizes to the chromosomes at the end of prophase I. Condensin I localizes after nuclear envelope breakdown, specifically between the bivalents in metaphase I. In anaphase I, cohesin is removed from the bivalent short arms to allow for homolog separation and condensin I remains in the spindle midzone. Condensin II and cohesin remain on the long arm of the bivalent to keep sister chromatids attached.

Figure 4.

The C. elegans Dosage Compensation Complex (DCC). Condensin I^DC is shown with the other members of the DCC. Functions of the other members are highlighted in corresponding colors. The SDC proteins SDC-1, SDC-2, and SDC-3 are colored similarly to highlight their shared function in sex determination.