Mitotic chromosome motions are driven by microtubules (MTs) and associated proteins that couple kinetochores to MT ends. A good coupler should ensure a high stability of attachment, even when the chromosome changes direction or experiences a large opposing force. The optimal coupler is also expected to be efficient in converting the energy of MT depolymerization into chromosome motility. As was shown years ago, a ''sleeve''-based, chromosomeassociated structure could, in principle, couple MT dynamics to chromosome motion. A recently identified kinetochore complex from yeast, the ''Dam1'' or ''DASH'' complex, may function as an encircling coupler in vivo. Some features of the Dam1 ring differ from those of the ''sleeve,'' but whether these differences are significant has not been examined. Here, we analyze theoretically the biomechanical properties of encircling couplers that have properties of the Dam1/DASH complex, such as its large diameter and inward-directed extensions. We demonstrate that, if the coupler is modeled as a wide ring with links that bind the MT wall, its optimal performance is achieved when the linkers are flexible and their binding to tubulin dimers is strong. The diffusive movement of such a coupler is limited, but MT depolymerization can drive its motion via a ''forced walk,'' whose features differ significantly from those of the mechanisms based on biased diffusion. Our analysis identifies key experimental parameters whose values should determine whether the Dam1/DASH ring moves via diffusion or a forced walk.biased diffusion ͉ kinetochore ͉ mathematical model ͉ power stroke ͉ energy-transducing coupler C hromosome segregation during cell division depends on the activities of microtubules (MTs), which are cylindrical arrangements of 13 linear polymers of ␣-tubulin dimers called protofilaments (PFs) (1). Tubulin complexed with GTP elongates PF ends, but this GTP is hydrolyzed soon after dimers have added (2). The preferred conformation of the GDP dimers is more bent, so the PFs tend to curve (3, 4). In a growing MT, this tendency is counteracted by a relatively straight ''GTP cap,'' but if the terminal layers are lost, the PFs are no longer restrained (1, 2). As they splay out, the dimers dissociate from their longitudinal neighbors, and the MT shortens (5, 6). Consequently, the ends of depolymerizing MTs in vitro and in vivo display curved PFs (3,[5][6][7][8][9]. Representative images of kinetochore MTs are shown in Fig. 1A; the length of PF flares in anaphase mammalian cells is 53 Ϯ 7 nm, n ϭ 368 PFs (J.R.M., E.L.G., A.E., K. Zhudenkov, M. Morphew, et al., unpublished work).It is well documented that MTs can move chromosomes or microbeads that associate with their shortening ends (9-15). Several hypotheses have explained these force-transducing attachments with the help of a coupler that encircles the MT (16-18). Movement in these models is driven ultimately by the energy released during hydrolysis of tubulin-associated GTP (Ϸ12 k B T; k B , Boltzmann constant). However, the design of a ...