Self‐regulative organization of the cytoskeleton

Despite its impressive complexity the cytoskeleton succeeds to persistently organize itself and thus the cells' interior. In contrast to classical man‐made machines, much of the cellular organization originates from inherent self‐assembly and self‐organization allowing a high degree of autonomy for various functional units. Recent experimental and theoretical studies revealed numerous examples of cytoskeleton components that arrange and organize in a self‐regulative way. In the present review we want to shortly summarize some of the principle mechanisms that are able to inherently trigger and regulate the cytoskeleton organization. Although taken individually most of these regulative principles are rather simple with intuitively predictable consequences, combinations of two or more of these mechanisms can quickly give rise to very complex, unexpected behavior and might even be able to explain the formation of different functional units out of a common pool of available building blocks.

[1]  M. Kirschner,et al.  Dynamic instability of microtubule growth , 1984, Nature.

[2]  Marie-France Carlier,et al.  Control of actin filament treadmilling in cell motility. , 2010, Annual review of biophysics.

[3]  S. Ishiwata,et al.  Characterization of single actomyosin rigor bonds: load dependence of lifetime and mechanical properties. , 2000, Biophysical journal.

[4]  Marileen Dogterom,et al.  Direct measurement of force generation by actin filament polymerization using an optical trap , 2007, Proceedings of the National Academy of Sciences.

[5]  Florian Huber,et al.  Robust Organizational Principles of Protrusive Biopolymer Networks in Migrating Living Cells , 2011, PloS one.

[6]  E. M. De La Cruz Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. , 2005, Journal of molecular biology.

[7]  Dimitrios Vavylonis,et al.  Actin polymerization kinetics, cap structure, and fluctuations. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[8]  J. Sellers,et al.  Load-dependent kinetics of myosin-V can explain its high processivity , 2005, Nature Cell Biology.

[9]  C S Peskin,et al.  Cellular motions and thermal fluctuations: the Brownian ratchet. , 1993, Biophysical journal.

[10]  Tabish Mufti,et al.  Myosin Motors Drive Long Range Alignment of Actin Filaments* , 2009, The Journal of Biological Chemistry.

[11]  Phillip L Geissler,et al.  Membrane-induced bundling of actin filaments. , 2008, Nature physics.

[12]  S. Leibler,et al.  Physical Properties Determining Self-Organization of Motors and Microtubules , 2001, Science.

[13]  Kerry Bloom,et al.  Dynamic Microtubules Lead the Way for Spindle Positioning , 2004, Nature Reviews Molecular Cell Biology.

[14]  Alex R. Hodges,et al.  Differential Regulation of Unconventional Fission Yeast Myosins via the Actin Track , 2010, Current Biology.

[15]  R. Ellis Macromolecular crowding : obvious but underappreciated , 2022 .

[16]  M. Carlier,et al.  Control of Actin Dynamics in Cell Motility , 2022 .

[17]  Denis Wirtz,et al.  Morphology of the lamellipodium and organization of actin filaments at the leading edge of crawling cells. , 2005, Biophysical journal.

[18]  Klemens Rottner,et al.  On the Rho'd: The regulation of membrane protrusions by Rho‐GTPases , 2008, FEBS letters.

[19]  David Sept,et al.  Effects of solution crowding on actin polymerization reveal the energetic basis for nucleotide-dependent filament stability. , 2008, Journal of molecular biology.

[20]  H. Kueh,et al.  Rapid actin monomer–insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1 , 2006, The Journal of cell biology.

[21]  Laurent Blanchoin,et al.  Coronin switches roles in actin disassembly depending on the nucleotide state of actin. , 2009, Molecular cell.

[22]  David J Odde,et al.  Traction Dynamics of Filopodia on Compliant Substrates , 2008, Science.

[23]  P. Davies,et al.  The Re-Emergence of Emergence: The Emergentist Hypothesis from Science to Religion , 2008 .

[24]  Erwin Frey,et al.  Polar patterns of driven filaments , 2010, Nature.

[25]  Judith Herzfeld,et al.  Crowding‐induced organization in cells: spontaneous alignment and sorting of filaments with physiological control points , 2004, Journal of molecular recognition : JMR.

[26]  J. Bamburg,et al.  Roles of ADF/cofilin in actin polymerization and beyond , 2010, F1000 biology reports.

[27]  Qi Wen,et al.  The hard life of soft cells. , 2009, Cell motility and the cytoskeleton.

[28]  T D Pollard,et al.  Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. , 2000, Annual review of biophysics and biomolecular structure.

[29]  J. Bamburg,et al.  ADF/cofilin: a functional node in cell biology. , 2010, Trends in cell biology.

[30]  E. Hardeman,et al.  Tropomyosin isoforms: divining rods for actin cytoskeleton function. , 2005, Trends in cell biology.

[31]  Dawen Cai,et al.  Tubulin modifications and their cellular functions. , 2008, Current opinion in cell biology.

[32]  Marie-France Carlier,et al.  Actin Depolymerizing Factor (ADF/Cofilin) Enhances the Rate of Filament Turnover: Implication in Actin-based Motility , 1997, The Journal of cell biology.

[33]  Jonathon Howard,et al.  Mechanical signaling in networks of motor and cytoskeletal proteins. , 2009, Annual review of biophysics.

[34]  Marie-France Carlier,et al.  The dynamics of actin-based motility depend on surface parameters , 2002, Nature.

[35]  Terrence W. Deacon,et al.  Emergence: The Hole at the Wheel’s Hub1 , 2008 .

[36]  Melanie J. I. Müller,et al.  Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors , 2008, Proceedings of the National Academy of Sciences.

[37]  Alexei Kurakin,et al.  Self-organization versus watchmaker: molecular motors and protein translocation. , 2006, Bio Systems.

[38]  P. Baas,et al.  Acetylation of Microtubules Influences Their Sensitivity to Severing by Katanin in Neurons and Fibroblasts , 2010, The Journal of Neuroscience.

[39]  Anne J. Ridley,et al.  Mammalian Rho GTPases: new insights into their functions from in vivo studies , 2008, Nature Reviews Molecular Cell Biology.

[40]  David Sept,et al.  The kinetics of cooperative cofilin binding reveals two states of the cofilin-actin filament. , 2010, Biophysical journal.

[41]  Dirar Homouz,et al.  Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding , 2010, Proceedings of the National Academy of Sciences.

[42]  A. Bausch,et al.  Cross-linker unbinding and self-similarity in bundled cytoskeletal networks. , 2007, Physical review letters.

[43]  A. Carlsson,et al.  Model of reduction of actin polymerization forces by ATP hydrolysis , 2008, Physical biology.

[44]  B. Peter,et al.  BAR Domains as Sensors of Membrane Curvature: The Amphiphysin BAR Structure , 2004, Science.

[45]  Anna Akhmanova,et al.  Tracking the ends: a dynamic protein network controls the fate of microtubule tips , 2008, Nature Reviews Molecular Cell Biology.

[46]  Gregory M Grason,et al.  Structural reorganization of parallel actin bundles by crosslinking proteins: incommensurate states of twist. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  D. Kovar,et al.  Fimbrin and Tropomyosin Competition Regulates Endocytosis and Cytokinesis Kinetics in Fission Yeast , 2010, Current Biology.

[48]  Y. Goldman,et al.  Motor Number Controls Cargo Switching at Actin-Microtubule Intersections In Vitro , 2010, Current Biology.

[49]  M. Carlier,et al.  Control of Actin Dynamics in Cell Motility , 1999, The Journal of Biological Chemistry.

[50]  Marileen Dogterom,et al.  Dynamic instability of microtubules is regulated by force , 2003, The Journal of cell biology.

[51]  Enrique M. De La Cruz,et al.  Cofilin binding to muscle and non-muscle actin filaments: isoform-dependent cooperative interactions. , 2005 .

[52]  Marie-France Carlier,et al.  Reconstitution of actin-based motility of Listeria and Shigella using pure proteins , 1999, Nature.

[53]  J. Käs,et al.  Growing actin networks form lamellipodium and lamellum by self-assembly. , 2008, Biophysical journal.

[54]  Wah Chiu,et al.  Cofilin Changes the Twist of F-Actin: Implications for Actin Filament Dynamics and Cellular Function , 1997, The Journal of cell biology.