Actin: From cell biology to atomic detail

Over the past 2 decades our knowledge about actin filaments has evolved from a rigid "pearls on a string" model to that of a complex, highly dynamic protein polymer which can now be analyzed at atomic detail. To achieve this, exploring actin's oligomerization, polymerization, polymorphism, and dynamic behavior has been crucial to understanding in detail how this abundant and ubiquitous protein can fulfill its various functions within living cells. In this review, a correlative view of a number of distinct aspects of actin is presented, and the functional implications of recent structural, biochemical, and mechanical data are critically evaluated. Rational analysis of these various experimental data is achieved using an integrated structural approach which combines intermediate-resolution electron microscopy-based 3-D reconstructions of entire actin filaments with atomic resolution X-ray data of monomeric and polymeric actin.

[1]  T. Pollard,et al.  The rate constant for ATP hydrolysis by polymerized actin , 1984, FEBS letters.

[2]  J. Sagara,et al.  Deficient polymerization in vitro of a point-mutated beta-actin expressed in a transformed human fibroblast cell line. , 1988, Journal of Biochemistry (Tokyo).

[3]  K. Holmes,et al.  An atomic model of the unregulated thin filament obtained by X-ray fiber diffraction on oriented actin-tropomyosin gels. , 1995, Journal of molecular biology.

[4]  A. Engel,et al.  Application of scanning transmission electron microscopy to the study of biological structure. , 1993, Current Opinion in Biotechnology.

[5]  E. Egelman,et al.  Structural dynamics of F-actin: I. Changes in the C terminus. , 1995, Journal of molecular biology.

[6]  P. Janmey,et al.  Distribution of actin filament lengths measured by fluorescence microscopy. , 1992, The American journal of physiology.

[7]  N. Davidson,et al.  Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner , 1983, Cell.

[8]  D. Drubin,et al.  Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site. , 1993, Molecular biology of the cell.

[9]  J. Small,et al.  Actin and cell movement. , 1993, Symposia of the Society for Experimental Biology.

[10]  E. Egelman,et al.  A conformational change in the actin subunit can change the flexibility of the actin filament. , 1993, Journal of molecular biology.

[11]  J. Vandekerckhove,et al.  Vegetative Dictyostelium cells containing 17 actin genes express a single major actin , 1980, Nature.

[12]  Kenneth A. Taylor,et al.  Three-dimensional reconstruction of rigor insect flight muscle from tilted thin sections , 1984, Nature.

[13]  T. Pollard,et al.  An actin-binding protein from Acanthamoeba regulates actin filament polymerization and interactions , 1980, Nature.

[14]  E. Uberbacher,et al.  Formation of actin dimers as studied by small angle neutron scattering. , 1986, The Journal of biological chemistry.

[15]  J. Leavitt,et al.  Expression of a variant form of actin and additional polypeptide changes following chemical-induced in vitro neoplastic transformation of human fibroblasts. , 1980, The Journal of biological chemistry.

[16]  T D Pollard,et al.  Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. , 1986, Annual review of biochemistry.

[17]  F. Oosawa.  Physical chemistry of actin: past, present and future. , 1993, Biophysical chemistry.

[18]  K. Trybus,et al.  Skeletal muscle myosin light chains are essential for physiological speeds of shortening , 1993, Nature.

[19]  D. Purich,et al.  Dynamic remodeling of the actin cytoskeleton: Lessons learned from Listeria locomotion , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[20]  T. Pollard.  Assembly and dynamics of the actin filament system in nonmuscle cells , 1986, Journal of cellular biochemistry.

[21]  A 13-A map of the actin-scruin filament from the limulus acrosomal process [published erratum appears in J Cell Biol 1993 Dec;123(6 Pt 1):1621] , 1993, The Journal of cell biology.

[22]  T. Pollard,et al.  Structure of the actin molecule determined from electron micrographs of crystalline actin sheets with a tentative alignment of the molecule in the actin filament. , 1983, Journal of molecular biology.

[23]  M. Carlier,et al.  Actin: protein structure and filament dynamics. , 1991, The Journal of biological chemistry.

[24]  U. Aebi,et al.  The Three‐Dimensional Structure of the Actin Filament Revisited a , 1986, Annals of the New York Academy of Sciences.

[25]  U. Aebi,et al.  The structure of the F-actin filament and the actin molecule. , 1992, Current opinion in cell biology.

[26]  D. Drummond,et al.  Molecular genetics of actin function. , 1993, The Biochemical journal.

[27]  H. Mannherz,et al.  The actin monomers in the ternary gelsolin: 2 actin complex are in an antiparallel orientation. , 1993, European journal of biochemistry.

[28]  H. Mannherz,et al.  Crystallization of the complex of actin with gelsolin segment 1. , 1992, Journal of molecular biology.

[29]  U. Aebi,et al.  Probing actin polymerization by intermolecular cross-linking , 1988, The Journal of cell biology.

[30]  E. Egelman,et al.  Allostery, cooperativity, and different structural states in F-actin. , 1995, Journal of structural biology.

[31]  D. DeRosier,et al.  Three-dimensional reconstruction of F-actin, thin filaments and decorated thin filaments. , 1970, Journal of molecular biology.

[32]  J. Donady,et al.  Actin Heterogeneity in primary embryonic culture cells from Drosophila melanogaster. , 1979, Developmental biology.

[33]  C. Schutt,et al.  The structure of crystalline profilin–β-actin , 1993, Nature.

[34]  R. Karlsson,et al.  Characterization of yeast-expressed beta-actins, site-specifically mutated at the tumor-related residue Gly245. , 1992, European journal of biochemistry.

[35]  J. E. Estes,et al.  Presence of oligomers at subcritical actin concentrations , 1985 .

[36]  D. DeRosier,et al.  The variable twist of actin and its modulation by actin-binding proteins , 1987, The Journal of cell biology.

[37]  P. Janmey,et al.  Effect of ATP on actin filament stiffness , 1990, Nature.

[38]  D. DeRosier,et al.  F-actin is a helix with a random variable twist , 1982, Nature.

[39]  W. Kabsch,et al.  Atomic model of the actin filament , 1990, Nature.

[40]  J. Clayton,et al.  Drosophila actin mutants and the study of myofibrillar assembly and function. , 1992, Symposia of the Society for Experimental Biology.

[41]  Heat shock gene activation by mutant actin is independent of myofibril degeneration in Drosophila muscle. , 1991, Journal of biochemistry.

[42]  H. Hamada,et al.  Variations in expression of mutant β actin accompanying incremental increases in human fibroblast tumorigenicity , 1982, Cell.

[43]  E. Egelman,et al.  Structural dynamics of F-actin: II. Cooperativity in structural transitions. , 1995, Journal of molecular biology.

[44]  D. DeRosier,et al.  Determination of the alpha-actinin-binding site on actin filaments by cryoelectron microscopy and image analysis , 1994, The Journal of cell biology.

[45]  E. Egelman,et al.  Structural basis for the destabilization of F-actin by phosphate release following ATP hydrolysis. , 1992, Journal of molecular biology.

[46]  T. Pollard,et al.  Structure of crystalline actin sheets , 1980, Nature.

[47]  A. Bershadsky,et al.  Swinholide A Is a Microfilament Disrupting Marine Toxin That Stabilizes Actin Dimers and Severs Actin Filaments (*) , 1995, The Journal of Biological Chemistry.

[48]  M. Peckham,et al.  Alteration in crossbridge kinetics caused by mutations in actin , 1990, Nature.

[49]  K C Holmes,et al.  Refinement of the F-actin model against X-ray fiber diffraction data by the use of a directed mutation algorithm. , 1993, Journal of molecular biology.

[50]  Computer-generated Fourier transforms of helical particles , 1974 .

[51]  M. Whittaker,et al.  Molecular structure of F-actin and location of surface binding sites , 1990, Nature.

[52]  T. Pollard,et al.  Characterization of actin filament severing by actophorin from Acanthamoeba castellanii , 1991, The Journal of cell biology.

[53]  E. Egelman,et al.  New insights into actin filament dynamics. , 1995, Current opinion in structural biology.

[54]  Ueli Aebi,et al.  A Correlative Analysis of Actin Filament Assembly, Structure, and Dynamics , 1997, The Journal of cell biology.

[55]  P. Janmey,et al.  Cooperativity in F-actin: binding of gelsolin at the barbed end affects structure and dynamics of the whole filament. , 1996, Journal of molecular biology.

[56]  H. Mannherz,et al.  Structure of gelsolin segment 1-actin complex and the mechanism of filament severing , 1993, Nature.

[57]  A. KLUG,et al.  Optical Filtering of Electron Micrographs: Reconstruction of One-Sided Images , 1966, Nature.

[58]  T. Stossel.  On the crawling of animal cells. , 1993, Science.

[59]  R A Milligan,et al.  Structure of the actin-myosin complex and its implications for muscle contraction. , 1993, Science.

[60]  T. Pollard.  Polymerization of ADP-actin , 1984, The Journal of cell biology.

[61]  M. Steinmetz,et al.  Cortexillins, Major Determinants of Cell Shape and Size, Are Actin-Bundling Proteins with a Parallel Coiled-Coil Tail , 1996, Cell.

[62]  P. Knight,et al.  p-NN'-phenylenebismaleimide, a specific cross-linking agent for F-actin. , 1978, The Biochemical journal.

[63]  J. Spudich,et al.  Subtilisin cleavage of actin inhibits in vitro sliding movement of actin filaments over myosin , 1990, The Journal of cell biology.

[64]  C. Schutt,et al.  Structural aspects of actin-binding proteins. , 1994, Current opinion in cell biology.

[65]  W. Kabsch,et al.  Muscle proteins: actin , 1991 .

[66]  X. Chen,et al.  Yeast actin with a mutation in the "hydrophobic plug" between subdomains 3 and 4 (L266D) displays a cold-sensitive polymerization defect , 1993, The Journal of cell biology.

[67]  M. Elzinga,et al.  F-actin is intermolecularly crosslinked by N,N'-p-phenylenedimaleimide through lysine-191 and cysteine-374. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[68]  U Aebi,et al.  Towards atomic interpretation of F-actin filament three-dimensional reconstructions. , 1994, Journal of molecular biology.

[69]  J. Vandekerckhove,et al.  The phalloidin binding site of F‐actin. , 1985, The EMBO journal.

[70]  M. Way,et al.  Molecular model of an actin filament capped by a severing protein. , 1995, Journal of structural biology.

[71]  J. Lepault,et al.  Small angle X-ray scattering and electron cryomicroscopy study of actin filaments: role of the bound nucleotide in the structure of F-actin. , 1994, Journal of Structural Biology.

[72]  Paul T Matsudalra.  Modular organization of actin crosslinking proteins. , 1991 .

[73]  J. Small,et al.  Actin filament organization in the fish keratocyte lamellipodium , 1995, The Journal of cell biology.

[74]  A. Hitt,et al.  Membrane interactions with the actin cytoskeleton. , 1994, Current opinion in cell biology.

[75]  M. Carlier,et al.  Binding of phosphate to F-ADP-actin and role of F-ADP-Pi-actin in ATP-actin polymerization. , 1988, The Journal of biological chemistry.

[76]  J Jakana,et al.  Three-dimensional structure of a single filament in the Limulus acrosomal bundle: scruin binds to homologous helix-loop-beta motifs in actin , 1994, The Journal of cell biology.

[77]  Theories of muscle contraction. , 1995, Journal of structural biology.

[78]  M. Bubb,et al.  Actobindin binds with high affinity to a covalently cross-linked actin dimer. , 1994, The Journal of biological chemistry.

[79]  H. Isambert,et al.  Flexibility of actin filaments derived from thermal fluctuations. Effect of bound nucleotide, phalloidin, and muscle regulatory proteins , 1995, The Journal of Biological Chemistry.

[80]  W. Villiger,et al.  Ultramicrotomy of biological objects: from the beginning to the present. , 1990, Journal of structural biology.

[81]  E. Reisler,et al.  Dynamic properties of actin. Structural changes induced by beryllium fluoride. , 1994, The Journal of biological chemistry.

[82]  Thomas Kreis,et al.  Guidebook to cytoskeletal and motor proteins , 1999 .

[83]  W. Kabsch,et al.  Crystals of skeletal muscle actin: Pancreatic DNAase I complex , 1977, FEBS letters.

[84]  J. Spudich,et al.  Assays for actin sliding movement over myosin-coated surfaces. , 1991, Methods in enzymology.

[85]  H. Erickson,et al.  Co-operativity in protein-protein association. The structure and stability of the actin filament. , 1989, Journal of molecular biology.

[86]  K. Holmes.  Solving the structure of macromolecular complexes with the help of X-ray fiber diffraction diagrams. , 1995, Journal of structural biology.

[87]  A. Wegner,et al.  Head to tail polymerization of actin. , 1976, Journal of molecular biology.

[88]  U. Aebi,et al.  Bundling of actin filaments by alpha-actinin depends on its molecular length , 1990, The Journal of cell biology.

[89]  W. Kabsch,et al.  Atomic structure of the actin: DNase I complex , 1990, Nature.

[90]  J. Spudich,et al.  Single myosin molecule mechanics: piconewton forces and nanometre steps , 1994, Nature.

[91]  A. Hoenger,et al.  3-D Reconstructions from Ice-Embedded and Negatively Stained Biomacromolecular Assemblies: A Critical Comparison , 1996 .

[92]  T. Pollard,et al.  The structural basis for the intrinsic disorder of the actin filament: the "lateral slipping" model , 1991, The Journal of cell biology.

[93]  K. Trybus,et al.  Function of skeletal muscle myosin heavy and light chain isoforms by an in vitro motility assay. , 1993, The Journal of biological chemistry.

[94]  E. Korn,et al.  Actin polymerization and ATP hydrolysis. , 1987, Science.

[95]  T. Pollard,et al.  Crystalline actin sheets: their structure and polymorphism , 1981, The Journal of cell biology.

[96]  T. Yanagida,et al.  Inhibition of sliding movement of F-actin by crosslinking emphasizes the role of actin structure in the mechanism of motility. , 1990, Journal of molecular biology.

[97]  J. Condeelis,et al.  Life at the leading edge: the formation of cell protrusions. , 1993, Annual review of cell biology.

[98]  J. Small,et al.  Leading edge movement and ultrastructure in mouse macrophages. , 1991, Journal of structural biology.

[99]  T. Pollard.  Measurement of rate constants for actin filament elongation in solution. , 1983, Analytical biochemistry.