JCB_201502062 1..9

The cytoskeleton underlies many aspects of cell physiology, including mitosis, cell division, volume control, cell stiffness, cell polarity, and extracellular matrix patterning. These events in turn impact development and tissue differentiation. The cytoskeleton receives, integrates, and transmits both intracellular and extracellular signaling cues. Most of these cues have to signal through a lipid bilayer before reaching the cytoskeleton. Thus, membrane–cytoskeleton interactions are central to deciphering how cytoskeletal remodeling is integrated throughout cells and tissues. Although signaling occurs across both the plasma and intracellular membranes, in this review we focus on the interplay between the cytoskeleton and the plasma membrane, which is predominantly composed of phospholipids (for a detailed review of plasma membrane lipid composition and localization, see Suetsugu et al., 2014). Common to eukaryotic cytoskeletal networks is the fact that they are formed from proteins with the inherent ability to self-assemble into long polymers. These polymers exist in a dynamic equilibrium with a monomeric pool, resulting in constant turnover in the cell. The ensemble of regulatory proteins, which regulates these dynamics, acts as the interface between cellular signaling and cytoskeletal remodeling. Not surprisingly then,

[1]  K. Gould,et al.  The Cdc15 and Imp2 SH3 domains cooperatively scaffold a network of proteins that redundantly ensure efficient cell division in fission yeast , 2015, Molecular biology of the cell.

[2]  J. Haugh,et al.  Profilin-1 serves as a gatekeeper for actin assembly by Arp2/3-dependent and -independent pathways. , 2015, Developmental cell.

[3]  Satoshi Okada,et al.  Architecture and dynamic remodeling of the septin cytoskeleton during the cell cycle , 2014, Nature Communications.

[4]  S. Kurisu,et al.  Dynamic shaping of cellular membranes by phospholipids and membrane-deforming proteins. , 2014, Physiological reviews.

[5]  Barry P. Young,et al.  Polarization of the Endoplasmic Reticulum by ER-Septin Tethering , 2014, Cell.

[6]  Guillaume Charras,et al.  Cellular Control of Cortical Actin Nucleation , 2014, Current Biology.

[7]  A. Echard,et al.  SLK-dependent activation of ERMs controls LGN–NuMA localization and spindle orientation , 2014, The Journal of cell biology.

[8]  J. Eskin,et al.  The F-BAR protein Hof1 tunes formin activity to sculpt actin cables during polarized growth , 2014, Molecular biology of the cell.

[9]  E. Snapp,et al.  A sphingolipid-dependent diffusion barrier confines ER stress to the yeast mother cell , 2014, eLife.

[10]  K. Keren,et al.  Symmetry breaking in reconstituted actin cortices , 2014, eLife.

[11]  M. Mavrakis,et al.  Septins promote F-actin ring formation by crosslinking actin filaments into curved bundles , 2014, Nature Cell Biology.

[12]  Q. Du,et al.  Cell cycle–regulated membrane binding of NuMA contributes to efficient anaphase chromosome separation , 2014, Molecular biology of the cell.

[13]  Shalin B. Mehta,et al.  Septin assemblies form by diffusion-driven annealing on membranes , 2014, Proceedings of the National Academy of Sciences.

[14]  N. Grishin,et al.  The WAVE Regulatory Complex Links Diverse Receptors to the Actin Cytoskeleton , 2014, Cell.

[15]  A. Piekny,et al.  Microtubules and actin crosstalk in cell migration and division , 2014, Cytoskeleton.

[16]  F. Cvrčková Formins and membranes: anchoring cortical actin to the cell wall and beyond , 2013, Front. Plant Sci..

[17]  N. Galjart,et al.  Protein 4.1R binds to CLASP2 and regulates dynamics, organization and attachment of microtubules to the cell cortex , 2013, Journal of Cell Science.

[18]  David A Weitz,et al.  The role of vimentin intermediate filaments in cortical and cytoplasmic mechanics. , 2013, Biophysical journal.

[19]  Shannon F. Stewman,et al.  The actin-binding ERM protein Moesin binds to and stabilizes microtubules at the cell cortex , 2013, The Journal of cell biology.

[20]  J. Förtsch,et al.  The yeast cell cortical protein Num1 integrates mitochondrial dynamics into cellular architecture , 2013, Journal of Cell Science.

[21]  P. Roy,et al.  Profilin-1 versus profilin-2: two faces of the same coin? , 2013, Breast Cancer Research.

[22]  Marcel Mettlen,et al.  An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry , 2013, Nature.

[23]  J. Grosshans,et al.  The F-BAR protein Cip4/Toca-1 antagonizes the formin Diaphanous in membrane stabilization and compartmentalization , 2013, Journal of Cell Science.

[24]  C. Ponting,et al.  MISP is a novel Plk1 substrate required for proper spindle orientation and mitotic progression , 2013, The Journal of cell biology.

[25]  K. Labib,et al.  Hof1 and Rvs167 Have Redundant Roles in Actomyosin Ring Function during Cytokinesis in Budding Yeast , 2013, PloS one.

[26]  J. Nunnari,et al.  Endoplasmic reticulum-associated mitochondria–cortex tether functions in the distribution and inheritance of mitochondria , 2013, Proceedings of the National Academy of Sciences.

[27]  C. Heisenberg,et al.  Anthrax toxin receptor 2a controls mitotic spindle positioning , 2012, Nature Cell Biology.

[28]  Daniel Feliciano,et al.  SLAC, a complex between Sla1 and Las17, regulates actin polymerization during clathrin-mediated endocytosis , 2012, Molecular biology of the cell.

[29]  Scott D. Hansen,et al.  Differential remodeling of actin cytoskeleton architecture by profilin isoforms leads to distinct effects on cell migration and invasion. , 2012, Cancer cell.

[30]  M. Bezanilla,et al.  Class II formin targeting to the cell cortex by binding PI(3,5)P2 is essential for polarized growth , 2012, The Journal of cell biology.

[31]  L. Blanchoin,et al.  Structure and activity of full‐length formin mDia1 , 2012, Cytoskeleton.

[32]  Wei-Lih Lee,et al.  A novel patch assembly domain in Num1 mediates dynein anchoring at the cortex during spindle positioning , 2012, The Journal of cell biology.

[33]  I. Cheeseman,et al.  Chromosome and spindle pole-derived signals generate an intrinsic code for spindle position and orientation , 2012, Nature Cell Biology.

[34]  J. Dorn,et al.  Molecular networks linked by Moesin drive remodeling of the cell cortex during mitosis , 2011, The Journal of cell biology.

[35]  M. Gullberg,et al.  Deciphering the rules governing assembly order of mammalian septin complexes , 2011, Molecular biology of the cell.

[36]  Michel Bornens,et al.  External forces control mitotic spindle positioning , 2011, Nature Cell Biology.

[37]  H. Pasolli,et al.  Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation , 2011, Nature Cell Biology.

[38]  Daniel J. Muller,et al.  Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding , 2011, Nature.

[39]  Patricia Grob,et al.  Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. , 2010, Journal of molecular biology.

[40]  H. Higgs,et al.  Bi-modal Regulation of a Formin by srGAP2* , 2010, The Journal of Biological Chemistry.

[41]  Kathleen L. Gould,et al.  Setting the F-BAR: Functions and regulation of the F-BAR protein family , 2010, Cell cycle.

[42]  Xiaowei Zhuang,et al.  Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system , 2010, Nature Cell Biology.

[43]  Matthew F Krummel,et al.  Control of cortical rigidity by the cytoskeleton: Emerging roles for septins , 2010, Cytoskeleton.

[44]  M. Scott,et al.  A Septin Diffusion Barrier at the Base of the Primary Cilium Maintains Ciliary Membrane Protein Distribution , 2010, Science.

[45]  S. Keeney,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 and S2 References Movie S1 Fcho Proteins Are Nucleators of Clathrin-mediated Endocytosis , 2022 .

[46]  S. Suetsugu,et al.  Subcellular membrane curvature mediated by the BAR domain superfamily proteins. , 2010, Seminars in cell & developmental biology.

[47]  Matthew D. Welch,et al.  A nucleator arms race: cellular control of actin assembly , 2010, Nature Reviews Molecular Cell Biology.

[48]  B. Wendland,et al.  The F-BAR Protein Syp1 Negatively Regulates WASp-Arp2/3 Complex Activity during Endocytic Patch Formation , 2009, Current Biology.

[49]  Thomas D. Pollard,et al.  Actin, a Central Player in Cell Shape and Movement , 2009, Science.

[50]  Roberto Dominguez,et al.  Actin filament nucleation and elongation factors – structure–function relationships , 2009, Critical reviews in biochemistry and molecular biology.

[51]  M. Kessels,et al.  F-BAR Proteins of the Syndapin Family Shape the Plasma Membrane and Are Crucial for Neuromorphogenesis , 2009, The Journal of Neuroscience.

[52]  Wei-Lih Lee,et al.  A CAAX motif can compensate for the PH domain of Num1 for cortical dynein attachment , 2009, Cell cycle.

[53]  L. Blanchoin,et al.  Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth , 2009, Proceedings of the National Academy of Sciences.

[54]  Rebecca A. Meseroll,et al.  Regulation of distinct septin rings in a single cell by Elm1p and Gin4p kinases. , 2009, Molecular biology of the cell.

[55]  B. Goode,et al.  Actin nucleation and elongation factors: mechanisms and interplay. , 2009, Current opinion in cell biology.

[56]  K. Takiguchi,et al.  Septin-Mediated Uniform Bracing of Phospholipid Membranes , 2009, Current Biology.

[57]  D. Kovar,et al.  Formin Differentially Utilizes Profilin Isoforms to Rapidly Assemble Actin Filaments* , 2009, Journal of Biological Chemistry.

[58]  Shiro Suetsugu,et al.  EFC/F‐BAR proteins and the N‐WASP–WIP complex induce membrane curvature‐dependent actin polymerization , 2008, The EMBO journal.

[59]  C. Doe,et al.  Lis1/dynactin regulates metaphase spindle orientation in Drosophila neuroblasts. , 2008, Developmental biology.

[60]  A. Echard,et al.  Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells , 2008, The Journal of cell biology.

[61]  Andrew E. Pelling,et al.  Moesin Controls Cortical Rigidity, Cell Rounding, and Spindle Morphogenesis during Mitosis , 2008, Current Biology.

[62]  R. Dominguez,et al.  Structural basis for the recruitment of profilin–actin complexes during filament elongation by Ena/VASP , 2007, The EMBO journal.

[63]  M. Kiebler,et al.  The GTP-Binding Protein Septin 7 Is Critical for Dendrite Branching and Dendritic-Spine Morphology , 2007, Current Biology.

[64]  J. Labbé,et al.  Heterotrimeric G protein signaling functions with dynein to promote spindle positioning in C. elegans , 2007, The Journal of cell biology.

[65]  P. Gönczy,et al.  Coupling of cortical dynein and Gα proteins mediates spindle positioning in Caenorhabditis elegans , 2007, Nature Cell Biology.

[66]  H. Higgs,et al.  The many faces of actin: matching assembly factors with cellular structures , 2007, Nature Cell Biology.

[67]  E. Nishida,et al.  Integrin‐mediated adhesion orients the spindle parallel to the substratum in an EB1‐ and myosin X‐dependent manner , 2007, The EMBO journal.

[68]  F. Chang,et al.  Shaping the actin cytoskeleton using microtubule tips. , 2007, Current opinion in cell biology.

[69]  M. Rosen,et al.  Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLα and mDia1 , 2006, The Journal of cell biology.

[70]  Adam C. Martin,et al.  Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. , 2006, Developmental cell.

[71]  C. Doe,et al.  The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts , 2006, Nature Cell Biology.

[72]  S. Bowman,et al.  The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. , 2006, Developmental cell.

[73]  Alan L. Munn,et al.  The BAR Domain Proteins: Molding Membranes in Fission, Fusion, and Phagy , 2006, Microbiology and Molecular Biology Reviews.

[74]  T. Pollard,et al.  Control of the Assembly of ATP- and ADP-Actin by Formins and Profilin , 2006, Cell.

[75]  Shiro Suetsugu,et al.  Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis , 2006, The Journal of cell biology.

[76]  Bianca Habermann,et al.  Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. , 2005, Developmental cell.

[77]  Manuel Théry,et al.  The extracellular matrix guides the orientation of the cell division axis , 2005, Nature Cell Biology.

[78]  A. Reilein,et al.  APC is a component of an organizing template for cortical microtubule networks , 2005, Nature Cell Biology.

[79]  A. Rodal,et al.  Actin and septin ultrastructures at the budding yeast cell cortex. , 2004, Molecular Biology of the Cell.

[80]  Marie-France Carlier,et al.  Formin Is a Processive Motor that Requires Profilin to Accelerate Actin Assembly and Associated ATP Hydrolysis , 2004, Cell.

[81]  M. Matsuda,et al.  A Novel Dynamin-associating Molecule, Formin-binding Protein 17, Induces Tubular Membrane Invaginations and Participates in Endocytosis* , 2004, Journal of Biological Chemistry.

[82]  Christian Roy,et al.  Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin , 2004, The Journal of cell biology.

[83]  K. Gould,et al.  The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe , 2003, The Journal of cell biology.

[84]  A. Rodal,et al.  Negative Regulation of Yeast WASp by Two SH3 Domain-Containing Proteins , 2003, Current Biology.

[85]  G. C. Rogers,et al.  Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle , 2002, The Journal of cell biology.

[86]  J. Vandekerckhove,et al.  Mutational analysis of human profilin I reveals a second PI(4,5)-P2 binding site neighbouring the poly(L-proline) binding site , 2002, BMC Biochemistry.

[87]  C. Hoogenraad,et al.  LIS1, CLIP-170's Key to the Dynein/Dynactin Pathway , 2002, Molecular and Cellular Biology.

[88]  J. Cooper,et al.  The Cortical Protein Num1p Is Essential for Dynein-Dependent Interactions of Microtubules with the Cortex , 2000, The Journal of cell biology.

[89]  J. Derisi,et al.  Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. , 2000, Science.

[90]  Y. Wang,et al.  Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion. , 2000, Molecular biology of the cell.

[91]  M. Snyder,et al.  Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. , 2000, Molecular cell.

[92]  J. Cooper,et al.  Dynein-dependent movements of the mitotic spindle in Saccharomyces cerevisiae Do not require filamentous actin. , 2000, Molecular biology of the cell.

[93]  S. Grinstein,et al.  Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP , 1999, Current Biology.

[94]  Fred Chang,et al.  cdc12p, a Protein Required for Cytokinesis in Fission Yeast, Is a Component of the Cell Division Ring and Interacts with Profilin , 1997, The Journal of cell biology.

[95]  Ching-shih Chen,et al.  Lipid products of phosphoinositide 3-kinase bind human profilin with high affinity. , 1996, Biochemistry.

[96]  J. Pringle,et al.  Localization and possible functions of Drosophila septins. , 1995, Molecular biology of the cell.

[97]  M. Farkašovský,et al.  Yeast Num1p associates with the mother cell cortex during S/G2 phase and affects microtubular functions , 1995, The Journal of cell biology.

[98]  T. Pollard,et al.  Regulation of phospholipase C-gamma 1 by profilin and tyrosine phosphorylation. , 1991, Science.

[99]  U. Lindberg,et al.  Specificity of the interaction between phosphatidylinositol 4,5‐bisphosphate and the profilin:actin complex , 1988, Journal of cellular biochemistry.

[100]  U. Lindberg,et al.  Specific interaction between phosphatidylinositol 4,5-bisphosphate and profilactin , 1985, Nature.

[101]  U. Lindberg,et al.  Actin polymerizability is influenced by profilin, a low molecular weight protein in non-muscle cells. , 1977, Journal of molecular biology.

[102]  B. Byers,et al.  A highly ordered ring of membrane-associated filaments in budding yeast , 1976, The Journal of cell biology.

[103]  Laurent Blanchoin,et al.  Actin dynamics, architecture, and mechanics in cell motility. , 2014, Physiological reviews.

[104]  P. Lappalainen,et al.  Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. , 2010, Physiological reviews.

[105]  P. Aspenström Roles of F-BAR/PCH proteins in the regulation of membrane dynamics and actin reorganization. , 2009, International review of cell and molecular biology.

[106]  M. Rothkegel,et al.  The profile of profilins. , 2007, Reviews of physiology, biochemistry and pharmacology.

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