The Symmetrical Structure of Structural Maintenance of Chromosomes (SMC) and MukB Proteins: Long, Antiparallel Coiled Coils, Folded at a Flexible Hinge

Abstract

Structural maintenance of chromosomes (SMC) proteins function in chromosome condensation and several other aspects of DNA processing. They are large proteins characterized by an NH2-terminal nucleotide triphosphate (NTP)-binding domain, two long segments of coiled coil separated by a hinge, and a COOH-terminal domain. Here, we have visualized by EM the SMC protein from Bacillus subtilis (BsSMC) and MukB from Escherichia coli, which we argue is a divergent SMC protein. Both BsSMC and MukB show two thin rods with globular domains at the ends emerging from the hinge. The hinge appears to be quite flexible: the arms can open up to 180°, separating the terminal domains by 100 nm, or close to near 0°, bringing the terminal globular domains together.A surprising observation is that the ∼300–amino acid–long coiled coils are in an antiparallel arrangement. Known coiled coils are almost all parallel, and the longest antiparallel coiled coils known previously are 35–45 amino acids long. This antiparallel arrangement produces a symmetrical molecule with both an NH2- and a COOH-terminal domain at each end. The SMC molecule therefore has two complete and identical functional domains at the ends of the long arms. The bifunctional symmetry and a possible scissoring action at the hinge should provide unique biomechanical properties to the SMC proteins.

The bacterial nucleoid: A highly organized and dynamic structure

“…These motifs fold back on each other, thus creating a long antiparallel coiled-coil and allowing the assembly of the two terminal segments into a functional ATP-binding domain [Melby et al, 1998;Hirano and Hirano, 2002]. The linker regions of two monomers then interact to form a V-shaped complex with a variable opening angle between 0 and 1808 [Melby et al, 1998;Hirano et al, 2001]. A similar arrangement was observed for MukB from E. coli, which might represent a highly divergent SMC homolog [Niki et al, 1991[Niki et al, , 1992Melby et al, 1998].…”

“…The central part consists of two coiled-coil motifs that are separated by a moderately conserved linker region. These motifs fold back on each other, thus creating a long antiparallel coiled-coil and allowing the assembly of the two terminal segments into a functional ATP-binding domain [Melby et al, 1998;Hirano and Hirano, 2002]. The linker regions of two monomers then interact to form a V-shaped complex with a variable opening angle between 0 and 1808 [Melby et al, 1998;Hirano et al, 2001].…”

“…The linker regions of two monomers then interact to form a V-shaped complex with a variable opening angle between 0 and 1808 [Melby et al, 1998;Hirano et al, 2001]. A similar arrangement was observed for MukB from E. coli, which might represent a highly divergent SMC homolog [Niki et al, 1991[Niki et al, , 1992Melby et al, 1998]. In the presence of DNA, ATP binding promotes end-to-end association of different SMC dimers, which initiates the formation of larger nucleoprotein complexes, but in turn also activates hydrolysis of the bound nucleotides [Hirano et al, 2001].…”

Bidirectional migration of SeqA‐bound hemimethylated DNA clusters and pairing of oriC copies in Escherichia coli

“…7A). None of these species have a homologue of Smc, which is a member of the Smc/MukB superfamily (Melby et al 1998) and exists widely in Achaea and Bacteria except the above E. colirelated bacteria. Other species of the Proteobacteria À Rickettsia prowazekii, Sinorhizobium meliloti, Caulobacter crescentus, Helicobacter pylori, Campylobacter jejuni, Neisseria gonorrhoeae, Neisseria meningitides, Bordetella bronchiseptica, Bordetella pertussis, Thiobacillus ferrooxidans, Legionella pneumophila and Pseudomonas aeruginosa À do not have Dam, SeqA, MutH and MukFEB, but all, except Rickettsia prowazekii and Helicobacter pylori, do have Smc (Fig.…”

Closing the ring: Links between SMC proteins and chromosome partitioning, condensation, and supercoiling

“…What links this fate of muk Ϫ bacteria to our story is that their chromosomes are decondensed (3) and that MukB is the structural and functional analogue of the ubiquitous SMC family of proteins (4). These huge molecules form coiled-coil dimers that, along with associated proteins, are thought to bind DNA segments separated by as much as 1,000 Å and then to contract the intervening DNA at the expense of ATP (5). Sawitzke and Austin show that the severity of the Muk phenotype can be controlled by changing the level of supercoiling in the cell.…”