SMC-mediated chromosome mechanics: a conserved scheme from bacteria to vertebrates?

The assembly of mitotic chromosomes is a fundamental cellular event that ensures the faithful segregation of genetic information during cell division. It involves two processes that are, in principle, mechanistically distinct. The first process, establishment of sister chromatid cohesion, occurs during or soon after chromosome duplication. The linkage between two sister chromatids is maintained throughout G2 phase and secures the bipolar attachment of each chromosome to the spindle apparatus from prometaphase through metaphase. The second process, chromosome condensation, can be visualized most dramatically at the onset of mitosis, converting the chromatids into physically strong, rod-shaped structures. The resulting metaphase chromosome consists of two condensed sister chromatids tightly paired at their centromeric regions as well as along their entire arms. At the onset of anaphase, the linkage between the sister chromatids is dissolved, allowing them to be pulled apart to opposite poles of the cell. This dynamic behavior of chromosomes had been described by cytologists long before the central role of DNA as the genetic material was recognized and long before the biochemical basis of cell cycle progression was elucidated. Nevertheless, the molecular mechanisms underlying these structural changes of chromosomes have remained poorly understood to date. A recent breakthrough in this field was the discovery of a novel family of chromosomal ATPases, the structural maintenance of chromosome (SMC) family. Genetic and biochemical studies have shown that in eukaryotes, two distinct classes of SMC protein complexes, condensins and cohesins, play central roles in chromosome condensation and sister-chromatid cohesion, respectively. Other SMC protein complexes are involved in chromosome-wide gene repression (dosage compensation) and recombinational repair. SMC proteins are also conserved among bacteria and archaea, and their functional characterization is just beginning to emerge. In this paper recent progress in the SMC field is discussed and an attempt is made to deduce a …