Membrane curvature at a glance

ABSTRACT Membrane curvature is an important parameter in defining the morphology of cells, organelles and local membrane subdomains. Transport intermediates have simpler shapes, being either spheres or tubules. The generation and maintenance of curvature is of central importance for maintaining trafficking and cellular functions. It is possible that local shapes in complex membranes could help to define local subregions. In this Cell Science at a Glance article and accompanying poster, we summarize how generating, sensing and maintaining high local membrane curvature is an active process that is mediated and controlled by specialized proteins using general mechanisms: (i) changes in lipid composition and asymmetry, (ii) partitioning of shaped transmembrane domains of integral membrane proteins or protein or domain crowding, (iii) reversible insertion of hydrophobic protein motifs, (iv) nanoscopic scaffolding by oligomerized hydrophilic protein domains and, finally, (v) macroscopic scaffolding by the cytoskeleton with forces generated by polymerization and by molecular motors. We also summarize some of the discoveries about the functions of membrane curvature, where in addition to providing cell or organelle shape, local curvature can affect processes like membrane scission and fusion as well as protein concentration and enzyme activation on membranes.

[1]  S. Vanni,et al.  Polyunsaturated phospholipids facilitate membrane deformation and fission by endocytic proteins , 2014, Science.

[2]  John M. Walker,et al.  Potassium Channels , 2009, Methods in Molecular Biology.

[3]  D. Daleke Phospholipid Flippases* , 2007, Journal of Biological Chemistry.

[4]  R. Schekman,et al.  COPII and the regulation of protein sorting in mammals , 2011, Nature Cell Biology.

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

[6]  Harvey T. McMahon,et al.  Membrane Curvature in Synaptic Vesicle Fusion and Beyond , 2010, Cell.

[7]  Max A. Horlbeck,et al.  ER Cargo Properties Specify a Requirement for COPII Coat Rigidity Mediated by Sec13p , 2012, Science.

[8]  H. Fertuck,et al.  Localization of acetylcholine receptor by 125I-labeled alpha-bungarotoxin binding at mouse motor endplates. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Randy Schekman,et al.  Sar1p N-Terminal Helix Initiates Membrane Curvature and Completes the Fission of a COPII Vesicle , 2005, Cell.

[10]  G. Drin,et al.  Amphipathic helices and membrane curvature , 2010, FEBS letters.

[11]  J. Dittman,et al.  Membrane curvature sensing by the C-terminal domain of complexin , 2014, Nature Communications.

[12]  W. Marshall,et al.  Building the cell: design principles of cellular architecture , 2008, Nature Reviews Molecular Cell Biology.

[13]  Edwin R. Chapman,et al.  Synaptotagmin-Mediated Bending of the Target Membrane Is a Critical Step in Ca2+-Regulated Fusion , 2009, Cell.

[14]  J. Bewersdorf,et al.  Lipidation of the LC3/GABARAP family of autophagy proteins relies upon a membrane curvature-sensing domain in Atg3 , 2014, Nature Cell Biology.

[15]  S. Vanni,et al.  A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment , 2014, Nature Communications.

[16]  Christopher J. Ryan,et al.  Membrane bending by protein–protein crowding , 2012, Nature Cell Biology.

[17]  R. Hirata,et al.  High-curvature domains of the ER are important for the organization of ER exit sites in Saccharomyces cerevisiae , 2012, Journal of Cell Science.

[18]  Howard A. Stone,et al.  Geometric Cue for Protein Localization in a Bacterium , 2009, Science.

[19]  Vinzenz M Unger,et al.  Membrane curvature and its generation by BAR proteins. , 2012, Trends in biochemical sciences.

[20]  S. Korn,et al.  Potassium channels , 2005, IEEE Transactions on NanoBioscience.

[21]  Aurélien Roux,et al.  Mechanics of dynamin-mediated membrane fission. , 2013, Annual review of biophysics.

[22]  E. Neher,et al.  Protein scaffolds in the coupling of synaptic exocytosis and endocytosis , 2011, Nature Reviews Neuroscience.

[23]  Bruno Antonny,et al.  Asymmetric Tethering of Flat and Curved Lipid Membranes by a Golgin , 2008, Science.

[24]  J. Errington,et al.  Localisation of DivIVA by targeting to negatively curved membranes , 2009, The EMBO journal.

[25]  O. Daumke,et al.  Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling , 2007, Nature.

[26]  M. Kozlov,et al.  Protein-lipid interplay in fusion and fission of biological membranes. , 2003, Annual review of biochemistry.

[27]  R. Kuehn,et al.  Deletion of N-terminal rapsyn domains disrupts clustering and has dominant negative effects on clustering of full-length rapsyn , 2005, Neuroscience.

[28]  R. Huganir,et al.  Presynaptic Clustering of mGluR7a Requires the PICK1 PDZ Domain Binding Site , 2000, Neuron.

[29]  H. McMahon,et al.  Interactions , 2019, Mathematical Models in Science.

[30]  Elina Ikonen,et al.  Cellular cholesterol trafficking and compartmentalization , 2008, Nature Reviews Molecular Cell Biology.

[31]  M. Kozlov,et al.  Formation of cell protrusions by an electric field: a thermodynamic analysis , 1992, European Biophysics Journal.

[32]  M. Kozlov,et al.  Measured effects of diacylglycerol on structural and elastic properties of phospholipid membranes. , 1996, Biophysical journal.

[33]  M. Kozlov,et al.  How lipid flippases can modulate membrane structure. , 2008, Biochimica et biophysica acta.

[34]  T. Graham,et al.  Interplay of proteins and lipids in generating membrane curvature. , 2010, Current opinion in cell biology.

[35]  J. Rohn,et al.  Actin and cellular architecture at a glance , 2010, Journal of Cell Science.

[36]  T. Pomorski,et al.  Identification of a novel mouse P4-ATPase family member highly expressed during spermatogenesis , 2009, Journal of Cell Science.

[37]  Bruno Antonny,et al.  Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. , 2012, Developmental cell.

[38]  A. Callan-Jones,et al.  Membrane shape modulates transmembrane protein distribution. , 2014, Developmental cell.

[39]  J. Hurley,et al.  Membrane budding and scission by the ESCRT machinery: it's all in the neck , 2010, Nature Reviews Molecular Cell Biology.

[40]  Harvey T. McMahon,et al.  Membrane curvature and mechanisms of dynamic cell membrane remodelling , 2005, Nature.

[41]  F. Noé,et al.  Structural insights into dynamin-mediated membrane fission. , 2012, Structure.

[42]  D. Douguet,et al.  Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers , 2011, The Journal of cell biology.

[43]  Reinhard Jahn,et al.  SNAREs — engines for membrane fusion , 2006, Nature Reviews Molecular Cell Biology.

[44]  M. Kozlov,et al.  The hydrophobic insertion mechanism of membrane curvature generation by proteins. , 2008, Biophysical journal.

[45]  Kartik Chandran,et al.  Endocytosis by Random Initiation and Stabilization of Clathrin-Coated Pits , 2004, Cell.

[46]  V. Haucke,et al.  Membrane shaping by the Bin/amphiphysin/Rvs (BAR) domain protein superfamily , 2011, Cellular and Molecular Life Sciences.

[47]  Robert G. Parton,et al.  Caveolae as plasma membrane sensors, protectors and organizers , 2013, Nature Reviews Molecular Cell Biology.

[48]  Yoko Shibata,et al.  Mechanisms shaping the membranes of cellular organelles. , 2009, Annual review of cell and developmental biology.

[49]  Adi Pick,et al.  Membrane Fission Is Promoted by Insertion of Amphipathic Helices and Is Restricted by Crescent BAR Domains , 2012, Cell.

[50]  M. Deserno,et al.  Coupling between lipid shape and membrane curvature. , 2006, Biophysical journal.

[51]  Junjie Hu,et al.  Weaving the Web of ER Tubules , 2011, Cell.

[52]  S. Emr,et al.  Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation. , 2013, Developmental cell.

[53]  N. Unwin,et al.  Refined structure of the nicotinic acetylcholine receptor at 4A resolution. , 2005, Journal of molecular biology.

[54]  Katharina Gaus,et al.  Shiga toxin induces tubular membrane invaginations for its uptake into cells , 2007, Nature.

[55]  G. Drin,et al.  A general amphipathic α-helical motif for sensing membrane curvature , 2007, Nature Structural &Molecular Biology.

[56]  R. Schekman,et al.  COPII-mediated vesicle formation at a glance , 2011, Journal of Cell Science.

[57]  Pietro De Camilli,et al.  Phosphoinositides in cell regulation and membrane dynamics , 2006, Nature.

[58]  M. Kozlov,et al.  How Synaptotagmin Promotes Membrane Fusion , 2007, Science.

[59]  R. Lamb,et al.  Viral membrane scission. , 2013, Annual review of cell and developmental biology.

[60]  Petra Schwille,et al.  GM1 structure determines SV40-induced membrane invagination and infection , 2010, Nature Cell Biology.

[61]  Michael M. Kozlov,et al.  How proteins produce cellular membrane curvature , 2006, Nature Reviews Molecular Cell Biology.

[62]  M. Palmgren,et al.  Flippases: still more questions than answers , 2008, Cellular and Molecular Life Sciences.

[63]  Harvey T. McMahon,et al.  Molecular mechanism and physiological functions of clathrin-mediated endocytosis , 2011, Nature Reviews Molecular Cell Biology.

[64]  B. Peter,et al.  Arf family GTP loading is activated by, and generates, positive membrane curvature , 2008, The Biochemical journal.

[65]  Siewert J Marrink,et al.  Mechanisms shaping cell membranes. , 2014, Current opinion in cell biology.

[66]  M. Rudolph,et al.  A hinge in the distal end of the PACSIN 2 F-BAR domain may contribute to membrane-curvature sensing. , 2010, Journal of molecular biology.

[67]  L. Niels Cornelisse,et al.  Doc2b Is a High-affinity Ca 2+ Sensor for Spontaneous Neurotransmitter Release , 2022 .

[68]  T. Kirchhausen,et al.  Three ways to make a vesicle , 2000, Nature Reviews Molecular Cell Biology.

[69]  R. Chan,et al.  Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. , 2011, Developmental cell.

[70]  H. McMahon,et al.  Mechanisms of membrane fusion: disparate players and common principles , 2008, Nature Reviews Molecular Cell Biology.

[71]  Q. Zhong,et al.  Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L) , 2011, Proceedings of the National Academy of Sciences.

[72]  C. Sorzano,et al.  3D cryo-electron reconstruction of BmrA, a bacterial multidrug ABC transporter in an inward-facing conformation and in a lipidic environment. , 2014, Journal of molecular biology.

[73]  Michael P. Sheetz,et al.  Cell control by membrane–cytoskeleton adhesion , 2001, Nature Reviews Molecular Cell Biology.

[74]  H. Korswagen,et al.  Sorting nexins provide diversity for retromer-dependent trafficking events , 2011, Nature Cell Biology.

[75]  J. Bessereau,et al.  The C. elegans P4‐ATPase TAT‐1 Regulates Lysosome Biogenesis and Endocytosis , 2009, Traffic.

[76]  G. Drin,et al.  ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif , 2005, The EMBO journal.

[77]  Iosune Ibiricu,et al.  Cargo binding to Atg19 unmasks further Atg8 binding sites to mediate membrane-cargo apposition during selective autophagy , 2014, Nature Cell Biology.

[78]  Xianghong Jing,et al.  Influenza Virus M2 Protein Mediates ESCRT-Independent Membrane Scission , 2010, Cell.

[79]  Harvey T. McMahon,et al.  The dynamin superfamily: universal membrane tubulation and fission molecules? , 2004, Nature Reviews Molecular Cell Biology.

[80]  G. Marcus,et al.  The eloquent ape: genes, brains and the evolution of language , 2006, Nature Reviews Genetics.

[81]  Jacques Prost,et al.  Mechanism of membrane nanotube formation by molecular motors. , 2010, Biochimica et biophysica acta.

[82]  Ian G. Mills,et al.  Curvature of clathrin-coated pits driven by epsin , 2002, Nature.

[83]  P. De Camilli,et al.  Arf1-GTP-induced Tubule Formation Suggests a Function of Arf Family Proteins in Curvature Acquisition at Sites of Vesicle Budding* , 2008, Journal of Biological Chemistry.

[84]  Pietro De Camilli,et al.  Dynamin, a membrane-remodelling GTPase , 2012, Nature Reviews Molecular Cell Biology.

[85]  J. Nunnari,et al.  Mitochondrial form and function , 2014, Nature.