Cytoskeleton and cell communication
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1 Cytoskeleton and cell communication Actin monomer has subdomains 1-4. A simplified cartoon is at right. ATP binds, along with Mg ++, within a deep cleft between subdomains 2 & 4. G-actin (globular actin), with bound ATP, can polymerize to form F-actin (filamentous). Actin can hydrolyze its bound ATP ADP + P i, releasing P i. The actin monomer can exchange bound ADP for ATP. The conformation of actin is different, depending on whether ATP or ADP is in the nucleotide-binding site. F-actin may hydrolyze bound ATP ADP + P i & release P i. ADP release from the filament does not occur because the cleft opening is blocked. ADP/ATP exchange: G-actin can release ADP & bind ATP, which is usually present at higher concentration than ADP in the cytosol. Actin filaments have polarity. The actin monomers all orient with their cleft toward the same end of the filament, called the minus end. The diagram above is oversimplified. Actin monomers spiral around the axis of the filament, with a structure resembling a double helix. The polarity of actin filaments may be visualized by decoration with globular heads (S1) cleaved off of myosin by proteases. Bound myosin heads cause an appearance of arrowheads in electron micrographs. 1
2 Actin filaments may undergo treadmilling, in which filament length remains approximately constant, while actin monomers add at the (+) end and dissociate from the (-) end. This has been monitored using brief exposure to labeled actin monomers (pulse labeling). Capping proteins bind at the ends of actin filaments. Different capping proteins may either stabilize an actin filament or promote disassembly. They may have a role in determining filament length. Examples: Tropomodulins cap the minus end, preventing dissociation of actin monomers. CapZ capping protein binds to the plus end, inhibiting polymerization. If actin monomers continue to dissociate from the minus end, the actin filament will shrink. Cross-linking proteins organize actin filaments into bundles or networks. Actin-binding domains of several cross-linking proteins (e.g., filamin, α-actinin, spectrin, dystrophin & fimbrin) are homologous. Most cross-linking proteins are dimeric or have 2 actin-binding domains. Some actin-binding proteins such as α-actinin, villin & fimbrin bind actin filaments into parallel bundles. Depending on the length of a cross-linking protein, or the distance between actin-binding domains, actin filaments in parallel bundles may be held close, or may be far enough apart to allow interaction with other proteins, e.g., myosin. Filamins dimerize, through antiparallel association of their C-terminal domains, to form V-shaped cross-linking proteins that have a flexible shape due to hinge regions. Filamins organize actin filaments into loose networks that give some areas of the cytosol a gel-like consistency. Filamins may also have scaffolding roles relating to their ability to bind constituents of signal pathways such as plasma membrane receptors. Cell structures that involve actin: Filopodia (microspikes) are long, thin and transient processes that extend out from the cell surface. Bundles of parallel actin filaments, with plus ends oriented toward the filopodial tip, are cross-linked by a small actin-binding protein such as fascin. The closely spaced actin filaments provide stiffness. Cell structures that involve actin: Microvilli are shorter & more numerous protrusions of the cell surface found in some cells. Tightly bundled actin filaments within these structures also have their plus ends oriented toward the tip. Small cross-linking proteins such as fimbrin and villin bind actin filaments together within microvilli. 2
3 Lamellipodia are thin but broad projections at the edge of a mobile cell. Lamellipodia are dynamic structures, constantly changing shape. Lamellipodia, at least in some motile cells, have been shown to contain extensively branched arrays of actin filaments, oriented with their plus (barbed) ends toward the plasma membrane. Forward extension of a lamellipodium occurs by growth of actin filaments adjacent to the plasma membrane. The cell was transfected with GFP-VASP, which is recruited to adhesion foci, as well as to the very tip of advancing lamellipodia. Stress fibers form when a cell makes stable connections to a substrate. Bundles of actin filaments extend from the cell surface through the cytosol. The actin filaments, whose plus ends are oriented toward the cell surface on opposite sides of the cell, may overlap in more interior regions of a cell in anti-parallel arrays. Myosin mediates sliding of anti-parallel actin filaments during contraction of stress fibers. α-actinin may cross-link actin filaments within stress fibers. Some cells have a cytoskeletal network just inside the plasma membrane that includes actin along with various other proteins such as spectrin. This cytoskeleton has a role in maintaining cell shape. An example is found in erythrocytes. Actin filaments have an essential role in the contractile ring responsible for cytokinesis at the end of mitosis in animal cells. Actin is found in the cell nucleus as well as in the cytoplasm. Recent data indicate involvement of actin in regulation of gene transcription. Nucleation of actin polymerization: Arp2/3 nucleates actin polymerization in lamellipodia. Arp2/3 complex includes 2 actin-related proteins, Arp2 & Arp3, plus 5 smaller proteins. When activated by a nucleation promoting factor (NPF), Arp2/3 complex binds to the side of an existing actin filament and nucleates assembly of a new filament branch. The resulting branch structure is Y-shaped. In this oversimplified diagram, Arp2 & Arp3 are shown forming the start of a new branch of double-helical F-actin. At the leading edge of a lamellipodium, plus end capping proteins may keep actin filaments short, while Arp2/3 keeps initiating new branches to propel the edge of the cell forward. It has been argued that the network of short, branching actin filaments seen in lamellipodia of some cell types could be more effective in pushing the leading edge forward than unbranched filaments, given the flexibility of actin filaments. 3
4 Further back from the leading edge, actin-destabilizing proteins, e.g., cofilin & gelsolin (to be discussed), would promote loss of actin monomers from the minus end. The continuous plus-end filament growth at the leading edge, and minus-end disassembly behind, show up as treadmilling of labeled actin monomers. A schematic illustration of the actin cytoskeleton of a fibroblast, indicating the Rho-family members involved in signaling different subcompartment assemblies of actin filaments: Rac, lamellipodia and focal complexes; Cdc42, filopodia and focal complexes; Rho, stress fibre bundles and focal adhesions (modified from Kaverina et al., 2002). Abbreviations: FX, focal complexes; FA, focal adhesions, Lam, lamellipodium; Fil, Filopodium; SF, stress fibre bundle; CB, Concave bundle (essentially stress fibre bundle at non-motile cell edges); Arc, arc shaped bundles sometimes observed under the dorsal cell surface; LM, loose meshwork of actin filaments; Rf, ruffle (corresponding to upfolding lamellipodium). Click on picture to enlarge Formins nucleate formation of unbranched actin filaments, such as those in stress fibers. Formins are found at the plus ends of actin filaments. Formin is said to be processive, because it remains bound to the plus end of an actin filament as actin monomers are added at the plus end. The continued presence of formin prevents binding of plus-end capping proteins that would inhibit filament growth. Each formin includes an actin-binding FH2 domain that dimerizes to form a ring-like structure with flexible links. Models have been proposed involving "stair stepping" by the dimeric formin to explain its ability to remain at the plus end as actin monomers are added. Other formin domains: Another actin-binding domain (FH1) binds monomeric actin complexed with profilin (to be discusssed). This may increase the effective concentration of monomeric actin adjacent to the polymerization site. Regulatory domains of formins allow for autoinhibition that is turned off during activation of actin polymerization by the GTP-binding signal protein Rho (to be discussed). Integrins: heterodimeric cell surface receptors. Each of the 2 integrin subunits, designated α & β, is a single-pass transmembrane protein. Integrins mediate adhesion of cells to the extracellular matrix as well as to other cells. Cytosolic domains of integrins bind to adaptor proteins (e.g., α-actinin, talin, filamin) that link integrins to elements of the cytoskeleton such as actin filaments. 4
5 Extracellular ligands bind at the α/β subunit interface. Extracellular domains of both α & β integrin subunits contribute residues to the ligand binding site. There are multiple isoforms of α & β subunits. Different combinations of α & β subunits yield a variety of integrins with different binding specificity. E.g.: Extracellular domain of α 1 β 1 integrin binds collagen. Extracellular domain of α 5 β 1 integrin binds fibronectin. Integrins mediate dynamic connections between the actin cytoskeleton inside a cell and constituents of the extracellular matrix. Moving cells make & break contacts with the matrix, whereas stationary cells may form more stable complexes with extracellular constituents. Integrins have signaling as well as adhesive roles. Outside-in signaling: Binding of ligands by extracellular domains may generate conformational changes that affect interaction of integrins with intracellular cytoskeletal and signal proteins. Inside-out signaling: The affinity of integrins for extracellular ligands is subject to regulation by cell signals. The inactive integrin has a bent over conformation, while in the fully activated state globular ligand binding domains extend out maximally from the cell surface. In focal adhesions stress fibers attach via adapter proteins to plasma membrane integrins. The adapter proteins that link actin filaments to cytosolic domains of integrins include α-actinin & talin. With extracellular domains of the integrins linked to matrix proteins, a cell is firmly attached to the external matrix. Gelsolin functions in gel sol transitions in the cytosol. When activated by Ca ++, gelsolin, severs an actin filament and caps the (+) end, blocking filament regrowth. Gelsolin may also function to promote forward extension of a lamellipodium. By severing actin filaments, gelsolin contributes to the development of the branched actin filament networks that grow to propel forward the plasma membrane at the leading edge. Gelsolin in the absence of Ca ++ does not bind actin. 5
6 A Cofilin az ADF család tagja (actin depolymerizing factor) A Cofilin ADP-aktint köt annak oldalán, megszüntetve az F-aktin spirális szerkezetét. Aktin filamentum severing tulajdonságú. Twinfilin is a protein structurally related to cofilin that binds G-actin-ADP, and may have a role in sequestering actin monomers. Thymosin β4 is a small protein (5 kda) that also forms a 1:1 complex with G-actin. Thymosin is proposed to buffer the concentration of free actin, by maintaining a pool of monomeric actin. An increase in the concentration of thymosin β4 may promote depolymerization of F-actin, by lowering the concentration of free G-actin. Profilin has a role in regulating actin polymerization. Profilin forms a 1:1 complex with G-actin. Profilin binding at the plus end, opposite the nucleotide-binding cleft, alters the conformation of G-actin, making its nucleotide-binding site more open to the cytosol. Regulation of assembly and disassembly of the actin cytoskeleton is very complex. Derivatives of the membrane lipid phosphatidylinositol are involved in signal cascades. Signal-activated kinases convert phosphatidylinositol to PIP 2 (phosphatidylinositol-4,5-bisphosphate). PIP 2 binds profilin at the cytosolic surface of the plasma membrane. This prevents profilin-actin interaction. Signal-activated PIP 2 hydrolysis releases profilin, which may bind G-actin and promote ADP/ATP exchange. The increase in G-actin-ATP promotes actin polymerization adjacent to the plasma membrane. Nucleation promoting factors that activate the Arp2/3 complex include proteins called WASP & Scar (WAVE). The genetic disease Wiskott -Aldrich Syndrome gave WASP its name. WASP/Scar proteins have domains that bind & activate Arp2/3, plus domains that recognize & bind to signaling factors that may be locally generated in a cell. Thus WASP/Scar proteins may determine where in a cell actin polymerization will occur. Some WASP proteins are activated by binding to proteins of the Rho family (see below) and/or to PIP 2. 6
7 Rho is a family of small GTP-binding proteins that regulate the actin cytoskeleton. Some members of the Rho family: Rac activates formation of lamellipodia, in part through activation of WASP. Cdc42 activates formation of filopodia, in part through activation of the WASP family protein Scar (WAVE). Cell protrusions Filopodia Lamellipodia Dorsal ruffles Pseudopods are temporary projections of eukaryotic cells. Rho activates formation of focal adhesions & stress fibers, in part through activation of formins. In each case the active form of the Rho family protein has bound GTP. What stabilize the filopodia? Inverse-BAR domains: MIM, ABBA and IRSp53 Bar-domains GFP-I-BAR MIM (Missing in Metastasis) and ABBA (actin-bundling protein with BAIAP2 homology. MIM and ABBA have an IMD and WH2 domains as well as serine and proline rich sequences. The IMD is a sensor of negatively charged membranes, e.g PS, PIP2 or PIP3. IRSp53 I-BAR domains Rac IMD Cdc42 CRIB SH3 WAVE2 Eps8 mdia1 Mena WW PDZ Overexpression leads to formation of filopodia - like protrusions Insulin Receptor Substrate protein of 53 kda 8 different isoforms, including ABBA, MIM, other IRSp53 variants. All vary at the C terminus. All contain the IMD 7
8 GFP-IMD Makes straight lipid tubules on the plasma membrane Andrew Waller Image captured every 0.5s over 5 minutes 100 fps playback. IMD and lipids Incubating liposomes with IMD led to invaginations in PIP2-containing vesicles. 100 nm Matilla et al, J. Cell Biol MIM induced ruffles are different to tubules What does MIM do? F-actin/ Myc F-actin/myc-MIM A375 cells Cos7 cells Images taken every 0.5s over 3 minutes. 50 fps playback. TIRF movies of GFP-MIM 8
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