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Cell Architecture: Putting the Building Blocks Together COCEBI-1090; NO. OF PAGES 3 Available online at www.sciencedirect.com Cell architecture: putting the building blocks together Editorial overview Anna Akhmanova and Tim Stearns Current Opinion in Cell Biology 2012, 25:xx–yy 0955-0674/$ – see front matter, # 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ceb.2012.12.003 Anna Akhmanova Cell Biology, Faculty of Science, Utrecht In considering cell architecture it is important to realize that for cells, as for University, Padualaan 8, 3584 CH Utrecht, buildings, the underpinning for the external shape is provided by a complex The Netherlands internal superstructure. And for cells, this cytoskeletal underpinning must e-mail: [email protected] be highly dynamic to effect the changes in morphology and organization associated with division, growth and differentiation. Cytoskeletal elements Anna Akhmanova is Professor of Cell Biology at Utrecht University, the Netherlands, and a were some of the first components of intracellular structure described by member of EMBO. Her lab uses cell early microscopists in the late 19th century, but it was not until a century biological approaches, in vitro reconstitutions later that the remarkable complexity of the cytoskeleton, in both compo- and high-resolution microscopy to study sition and behavior, has been revealed. Advances in genomics and proteo- molecular mechanisms of microtubule mics have provided us with near-comprehensive lists of the molecular dynamics and vesicle trafficking and their players associated with the various cytoskeletal systems. The challenge contribution to mammalian development and human disease. now is to understand how these components work together, and this is one of the central themes of this issue of Current Opinion in Cell Biology. Tim Stearns Because of the highly interconnected nature of the cytoskeletal networks, it Department of Biology, Stanford University, Stanford, CA 94062, USA is often most useful to study individual components or systems in simplified e-mail: [email protected] settings in vitro. Mullins and Hansen provide an overview of the recent in vitro studies of actin network architecture and assembly. New methods of Tim Stearns is Professor of Biology at sample preparation and imaging provided insight into key features of actin Stanford University and Professor of polymerization and made it possible to perform reconstitutions where Genetics at Stanford Medical School. His lab cooperation between multiple actin regulators was recapitulated. By localiz- studies the structure and function of the ing actin nucleators to different substrates impressive progress has been centrosome and cilium in animal cells and the relationship of defects in these signaling made in reconstitution of protrusive actin networks and even cell spreading. centers to human disease. Microtubules have benefited from recent in vitro approaches as well. Gardner, Zanic and Howard review recent insights into the mechanisms underlying the dynamic instability of microtubules. Studies in cells and in vitro show that previously underappreciated phenomena such as microtu- bule aging, the presence in the microtubule lattice of GTP-tubulin islands and mechanical tension at microtubule ends can regulate the transitions between microtubule growth and depolymerization. Dogterom and Surrey discuss the progress in understanding how complex microtubule patterns are generated and maintained. Although many types of microtubule arrange- ments exist, they can be roughly categorized into three types: asters, anti- parallel overlaps, and bundles. Complex reconstitution experiments with purified microtubule motors, microtubule binding and bundling proteins combined with modeling provide insights into how these patterns are formed and positioned within the confining geometry of cells. One of the means by which cytoskeletal systems are regulated is post-translational modification of the major subunit proteins. Terman and Kashina provide a comprehensive overview of all known covalent www.sciencedirect.com Current Opinion in Cell Biology 2012, 25:1–3 Please cite this article in press as: Akhmanova A, Stearns TCell architecture: putting the building blocks together, Curr Opin Cell Biol (2012), http://dx.doi.org/10.1016/j.ceb.2012.12.003 COCEBI-1090; NO. OF PAGES 3 2 Cell architecture modifications of actin. The variety of known actin the nine-fold symmetry. In many cells the centriole modifications is broad, ranging from conventional post- serves as a basal body for a cilium, which is involved in translational modifications such as phosphorylation and important motility and sensory functions. Benmerah acetylation to those much less studied, such as arginyla- focuses on a specialized membrane domain, the ciliary tion and site-specific oxidation. These modifications con- pocket, that is at the base of cilium in many cells and is tribute to the rich diversity of the regulatory mechanisms the site of membrane and protein trafficking to and from affecting actin dynamics and function. the cilium. This underappreciated structure might be responsible for some of the specialized signaling roles Actin is an essential player at the adherens junctions, that the cilium plays. and recent studies are gradually revealing how actin nucleating factors, motors and bundling proteins con- The cytoskeleton is closely associated with membrane tribute to actin filament assembly and dynamics at the trafficking and dynamics. Angus and Griffiths discuss the junctions. Brieher and Yap discuss the cross-talk be- complex set of events leading to the formation of tween cadherin-based cell–cell junctions and the cytos- immunological synapse and polarized secretion by keleton. Novel structural and signaling links between immune cells. Movement of the centrosome to the microtubules and cadherin junctions are also being plasma membrane plays a key role in this process, and discovered, indicating that microtubules are an recent studies have begun to reveal the cytoskeletal important albeit a more variable regulator of these components and signalling molecules involved in centro- structures. some relocalization and targeted delivery of cytolytic granules. Like the immunological synapse, the cytoki- Intermediate filaments were less well-studied during the netic furrow of animal cells is a site of polarized mem- renaissance of interest in the cytoskeleton in the 60’s and brane trafficking. Schiel and Prekeris review the events of 70’s. As described by Pan, Hobbs, and Coulombe, there is late cytokinesis, considering the role of endosomal mem- much recent progress in understanding the role of kera- branes and how membrane dynamics are coordinated tins, a prominent group of intermediate filaments. Ker- with the actin cytoskeleton, providing complementary atins provide cells with structural support for shaping activities resulting in final abscission. tissues and individual organelles, including the nucleus, but are also intimately involved in signaling, stress In another example of cytoskeletal involvement in polar- response, apoptosis and cell motility, and in regulating izing cell components, Pratt and Mowry provide an over- cell architecture in normal and pathological conditions. view of the recent advances in understanding mRNA localization. This process depends on cis-acting signals The relationship between the nucleus and cytoskeleton within localizing transcripts, and recent studies revealed is further discussed by Tapley and Starr who focus on how their structures contribute to their functional proper- the proteins that physically link the two. The LINC ties. High-resolution imaging experiments showed that complex spans the nuclear envelope, establishing con- the intermediates of mRNA transport can be diverse: nections between the nuclear lamina inside the nucleus while some transported mRNA are assembled into large and a variety of cytoskeletal elements outside. These granules, others travel alone. Surprisingly, mRNA local- connections are important in positioning the nucleus ization pathways can also intersect with endosomal sort- within the cell, and the organization of organelles such ing, as the components of endocytic machinery as the centrosome around the nucleus. Within the participate in mRNA anchoring. nucleus there is another protein complex, cohesin, that links sister chromatids. This chromatid cohesion is Understanding of cytoskeletal properties increasingly essential for proper chromosome segregation in mitosis depends on mathematical modeling. Allard and Mogilner and meiosis. Remeseiro and Losada review the mech- discuss a fascinating type of complex non-steady state anisms by which cohesion is established in interphase cytoskeletal dynamics — self-organized actin travelling and released in mitosis, and additional roles that cohe- waves. Waves of protrusion, retraction and actin density sin plays in DNA damage repair and interphase chro- can be observed in a broad variety of cells and might help matin structure. them to avoid obstacles or squeeze through the extra- cellular matrix. The diverse types of waves result from Many elements of the cytoskeleton are characterized by activation and inhibition feedbacks in actin dynamics, highly ordered arrangement of protein subunits. The and their mechanisms can only be understood through a centrioles at the core of the centrosome are an extreme tight combination of experiments and theory. example, with a highly-conserved nine-fold symmetric structure and defined length. The centrioles are dupli- One of the keys to understanding
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