Mechanics of dynamin-mediated membrane fission.

In eukaryotic cells, membrane compartments are split into two by membrane fission. This ensures discontinuity of membrane containers and thus proper compartmentalization. The first proteic machinery implicated in catalyzing membrane fission was dynamin. Dynamin forms helical collars at the neck of endocytic buds. This structural feature suggested that the helix of dynamin could constrict in order to promote fission of the enclosed membrane. However, verifying this hypothesis revealed itself to be a challenge, which inspired many in vitro and in vivo studies. The primary goal of this review is to discuss recent structural and physical data from biophysical studies that have refined our understanding of the dynamin mechanism. In addition to the constriction hypothesis, other models have been proposed to explain how dynamin induces membrane fission. We present experimental data supporting these various models and assess which model is the most probable.

[1]  A. Roux,et al.  Mechanical requirements for membrane fission: Common facts from various examples , 2009, FEBS letters.

[2]  P. De Camilli,et al.  Generation of high curvature membranes mediated by direct endophilin bilayer interactions , 2001, The Journal of cell biology.

[3]  Frank Noé,et al.  Crystal structure of nucleotide-free dynamin , 2011, Nature.

[4]  Kazuhiko Kinosita,et al.  F1-ATPase Is a Highly Efficient Molecular Motor that Rotates with Discrete 120° Steps , 1998, Cell.

[5]  K. Sandvig,et al.  Clathrin-coated pits with long, dynamin-wrapped necks upon expression of a clathrin antisense RNA , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. Kochs,et al.  Structural basis of oligomerization in the stalk region of dynamin-like MxA , 2010, Nature.

[7]  D. Danino,et al.  Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. , 2004, Journal of structural biology.

[8]  R. Goody,et al.  Individual rate constants for the interaction of Ras proteins with GTPase-activating proteins determined by fluorescence spectroscopy. , 1997, Biochemistry.

[9]  Frank McCormick,et al.  The GTPase superfamily: a conserved switch for diverse cell functions , 1990, Nature.

[10]  T. Kirchhausen,et al.  Dynasore, a cell-permeable inhibitor of dynamin. , 2006, Developmental cell.

[11]  J. Heuser,et al.  Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation , 1989, The Journal of cell biology.

[12]  J. Hinshaw,et al.  Dynamin Assembles into Spirals under Physiological Salt Conditions upon the Addition of GDP and γ-Phosphate Analogues* , 1997, The Journal of Biological Chemistry.

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

[14]  S. Schmid,et al.  Mutations in human dynamin block an intermediate stage in coated vesicle formation , 1993, The Journal of cell biology.

[15]  R. Vallee,et al.  Dynamin is a GTPase stimulated to high levels of activity by microtubules , 1992, Nature.

[16]  S. Schmid,et al.  GTPase Cycle of Dynamin Is Coupled to Membrane Squeeze and Release, Leading to Spontaneous Fission , 2008, Cell.

[17]  Noah W. Gray,et al.  Dynamin 3 Is a Component of the Postsynapse, Where it Interacts with mGluR5 and Homer , 2003, Current Biology.

[18]  S. Schmid,et al.  Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding , 1995, Nature.

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

[20]  E. Furst,et al.  Motor-driven dynamics in actin-myosin networks. , 2001, Physical review letters.

[21]  S. Schmid,et al.  An intramolecular signaling element that modulates dynamin function in vitro and in vivo. , 2009, Molecular biology of the cell.

[22]  G. Chalancon,et al.  Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex , 2010, Nature Cell Biology.

[23]  G. Cappello,et al.  Membrane Shape at the Edge of the Dynamin Helix Sets Location and Duration of the Fission Reaction , 2012, Cell.

[24]  P. Camilli,et al.  Generation of Coated Intermediates of Clathrin-Mediated Endocytosis on Protein-Free Liposomes , 1998, Cell.

[25]  B. Antonny,et al.  The Long and Short of Membrane Fission , 2008, Cell.

[26]  Yonathan Kozlovsky,et al.  Membrane fission: model for intermediate structures. , 2003, Biophysical journal.

[27]  S. Schmid,et al.  Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals , 1995, Nature.

[28]  S. Schmid,et al.  Crystal structure of the GTPase domain of rat dynamin 1. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. McCaffery,et al.  Dnm1 forms spirals that are structurally tailored to fit mitochondria , 2005, The Journal of cell biology.

[30]  R. Vallee,et al.  Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins , 1990, Nature.

[31]  Thuy D. Vo,et al.  Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells , 2011, Nature Cell Biology.

[32]  Michelle D. Wang,et al.  Estimating the persistence length of a worm-like chain molecule from force-extension measurements. , 1999, Biophysical journal.

[33]  S. Schmid,et al.  Induction of mutant dynamin specifically blocks endocytic coated vesicle formation , 1994, The Journal of cell biology.

[34]  M. Kozlov.  Dynamin: possible mechanism of "Pinchase" action. , 1999, Biophysical journal.

[35]  J. Howard,et al.  Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape , 1993, The Journal of cell biology.

[36]  I. Mills,et al.  GTPase activity of dynamin and resulting conformation change are essential for endocytosis , 2001, Nature.

[37]  J. Mears,et al.  A corkscrew model for dynamin constriction. , 2007, Structure.

[38]  J. Nunnari,et al.  A continuous, regenerative coupled GTPase assay for dynamin-related proteins. , 2005, Methods in enzymology.

[39]  E. O'Toole,et al.  Overlapping Role of Dynamin Isoforms in Synaptic Vesicle Endocytosis , 2011, Neuron.

[40]  J. Rothman,et al.  Complexin activates and clamps SNAREpins by a common mechanism involving an intermediate energetic state , 2011, Nature Structural &Molecular Biology.

[41]  S. Schmid,et al.  Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis , 1999, Nature.

[42]  S. Schmid,et al.  Dynamin Self-assembly Stimulates Its GTPase Activity* , 1996, The Journal of Biological Chemistry.

[43]  K. Ikeda,et al.  Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Brian A. Camley,et al.  Beyond the creeping viscous flow limit for lipid bilayer membranes: theory of single-particle microrheology, domain flicker spectroscopy, and long-time tails. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[45]  J. Löwe,et al.  Dynamin architecture--from monomer to polymer. , 2010, Current opinion in structural biology.

[46]  S. Schmid,et al.  Domain structure and intramolecular regulation of dynamin GTPase , 1997, The EMBO journal.

[47]  E. Querfurth,et al.  Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. , 1996, The EMBO journal.

[48]  Anne Houdusse,et al.  Structural and functional insights into the Myosin motor mechanism. , 2010, Annual review of biophysics.

[49]  R. Vallee,et al.  Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules , 1989, Cell.

[50]  C. Collins,et al.  Activation of dynamin GTPase is a result of positive cooperativity. , 1994, The Journal of biological chemistry.

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

[52]  S. Schmid,et al.  An assembly-incompetent mutant establishes a requirement for dynamin self-assembly in clathrin-mediated endocytosis in vivo. , 2004, Molecular biology of the cell.

[53]  P. Bassereau,et al.  Membrane curvature controls dynamin polymerization , 2010, Proceedings of the National Academy of Sciences.

[54]  S. Schmid,et al.  Real-Time Visualization of Dynamin-Catalyzed Membrane Fission and Vesicle Release , 2008, Cell.

[55]  Rachel M. Devay,et al.  Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion , 2009, The Journal of cell biology.

[56]  Takayuki Fujiwara,et al.  Isolated Chloroplast Division Machinery Can Actively Constrict After Stretching , 2006, Science.

[57]  J. Joanny,et al.  Deformation of dynamin helices damped by membrane friction. , 2010, Biophysical journal.

[58]  Richard B. Vallee,et al.  Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis , 1991, Nature.

[59]  J. Joanny,et al.  Mechanochemical action of the dynamin protein. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  D. Perrais,et al.  A High Precision Survey of the Molecular Dynamics of Mammalian Clathrin-Mediated Endocytosis , 2011, Microscopy and Microanalysis.

[61]  Cori Bargmann,et al.  A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[62]  A. M. van der Bliek,et al.  A Model for Dynamin Self-assembly Based on Binding Between Three Different Protein Domains* , 1999, The Journal of Biological Chemistry.

[63]  Pietro De Camilli,et al.  Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis , 1999, Nature Cell Biology.

[64]  J. Rothman,et al.  Energetics and dynamics of SNAREpin folding across lipid bilayers , 2007, Nature Structural &Molecular Biology.

[65]  S. Schmid,et al.  A Pseudoatomic Model of the Dynamin Polymer Identifies a Hydrolysis-Dependent Powerstroke , 2011, Cell.

[66]  Adam Frost,et al.  Structural Basis of Membrane Invagination by F-BAR Domains , 2008, Cell.

[67]  S. Schmid,et al.  G domain dimerization controls dynamin's assembly-stimulated GTPase activity , 2010, Nature.

[68]  M. Kozlov,et al.  Mechanics of membrane fusion , 2008, Nature Structural &Molecular Biology.

[69]  P. De Camilli,et al.  A Selective Activity-Dependent Requirement for Dynamin 1 in Synaptic Vesicle Endocytosis , 2007, Science.

[70]  M. Kozlov,et al.  The Protein Coat in Membrane Fusion: Lessons from Fission , 2002, Traffic.

[71]  M. Ehlers,et al.  Postsynaptic Positioning of Endocytic Zones and AMPA Receptor Cycling by Physical Coupling of Dynamin-3 to Homer , 2007, Neuron.

[72]  S. Jenni,et al.  The crystal structure of dynamin , 2011, Nature.

[73]  Peijun Zhang,et al.  The stalk region of dynamin drives the constriction of dynamin tubes , 2004, Nature Structural &Molecular Biology.

[74]  P. Camilli,et al.  Accessory factors in clathrin-dependent synaptic vesicle endocytosis , 2000, Nature Reviews Neuroscience.

[75]  Peijun Zhang,et al.  Three-dimensional reconstruction of dynamin in the constricted state , 2001, Nature Cell Biology.

[76]  J. Heymann,et al.  OPA1 disease alleles causing dominant optic atrophy have defects in cardiolipin-stimulated GTP hydrolysis and membrane tubulation , 2010, Human molecular genetics.

[77]  P. Camilli,et al.  GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission , 2006, Nature.

[78]  B. Finlay,et al.  The role of dynamin 3 in the testis , 2007, Journal of cellular physiology.

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

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

[81]  S. Schmid,et al.  Ubiquitously expressed dynamin-II has a higher intrinsic GTPase activity and a greater propensity for self-assembly than neuronal dynamin-I. , 1997, Molecular biology of the cell.

[82]  J. Hinshaw,et al.  Dynamin Undergoes a GTP-Dependent Conformational Change Causing Vesiculation , 1998, Cell.

[83]  P. De Camilli,et al.  The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[84]  M. Stowell,et al.  Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring , 1999, Nature Cell Biology.

[85]  Andrew Callan-Jones,et al.  Nature of curvature coupling of amphiphysin with membranes depends on its bound density , 2011, Proceedings of the National Academy of Sciences.

[86]  V. Murthy,et al.  Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis , 2006, Proceedings of the National Academy of Sciences.