Hirano, T. (February 2002) The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion and repair. Genes & Development, 16 (4). pp. 399-414. ISSN 0890-9369
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Abstract
The first draft of the human genome sequence was reported a year ago. It may be a good time to remind ourselves that the genetic information encoded in the ∼3000-Mb sequence is stored not only in the public or private databases but also in the tiny space of the cell nucleus. The total length of human genomic DNA, which resides in 23 chromosomes, reaches approximately one meter. It is by no means a simple task to fold up the long DNA molecules and package them within a cell nucleus whose diameter is only ∼10 μm. Even more striking is that the DNA molecules are faithfully duplicated and segregated into two daughter cells in an extremely limited space. Although more than 100 years have passed since Walther Flemming first described the dynamic behavior of chromosomes (or mitosis) during cell division, it remains highly mysterious how this remarkable process of chromosome segregation is achieved at a mechanistic level. From a cytological point of view, two dramatic events occur on chromosomes during mitosis. The first one is the conversion of an amorphous mass of interphase chromatin into a discrete set of rod-shaped chromosomes (chromosome condensation), which occurs from prophase to metaphase (Koshland and Strunnikov 1996; Hirano 2000). The second is the splitting of chromosomes into two halves, which takes place highly synchronously at the onset of anaphase (Dej and Orr-Weaver 2000; Nasmyth et al. 2000). As a crucial prerequisite for these events, duplicated chromosomes (sister chromatids) must be held together immediately after DNA replication in S phase and throughout G2 phase. The importance of this process (sister chromatid cohesion) has been fully appreciated only recently because the pairing of sister chromatids cannot be visualized by classical cytology before chromosomes condense in early mitosis. Recent genetic and biochemical studies have begun to shed light on the molecular mechanisms underlying cohesion, condensation, and separation of chromosomes during the mitotic cell cycle. One of the unexpected findings is that chromosome condensation and sister chromatid cohesion are regulated by distinct, yet structurally similar, protein complexes termed condensin and cohesin, respectively. At the heart of the two protein complexes lie members of a family of chromosomal ATPases, the structural maintenance of chromosomes (SMC) family. Equally intriguing, SMC proteins are found in most, if not all, bacterial and archaeal species, implicating that their fundamental contribution to chromosome dynamics started even before the acquisition of histones during evolution. The goal of this review article is to discuss the current understanding of higher-order chromosome dynamics with an emphasis on the role of SMC proteins. I start with the basic description and classification of SMC proteins and then summarize emerging information on the diverse chromosomal functions supported by SMC proteins. Finally, I discuss the mechanistic aspects of bacterial and eukaryotic SMC proteins and try to make an integrated picture of their seemingly different actions.
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