Intermediate filaments: from cell architecture to nanomechanics

Intermediate filaments (IFs) constitute a major structural element of animal cells. They build two distinct systems, one in the nucleus and one in the cytoplasm. In both cases, their major function is assumed to be that of a mechanical stress absorber and an integrating device for the entire cytoskeleton. In line with this, recent disease mutations in human IF proteins indicate that the nanomechanical properties of cell-type-specific IFs are central to the pathogenesis of diseases as diverse as muscular dystrophy and premature ageing. However, the analysis of these various diseases suggests that IFs also have an important role in cell-type-specific physiological functions.

[1]  M. Kellermayer,et al.  Nanomechanical properties of desmin intermediate filaments. , 2006, Journal of structural biology.

[2]  Walter Birchmeier,et al.  Mutations in the desmosomal protein plakophilin-2 are common in arrhythmogenic right ventricular cardiomyopathy , 2004, Nature Genetics.

[3]  Donald E. Ingber,et al.  Jcb: Article Introduction , 2002 .

[4]  B. Helfand,et al.  The dynamic and motile properties of intermediate filaments. , 2003, Annual review of cell and developmental biology.

[5]  R L Lieber,et al.  Muscle cytoskeletal disruption occurs within the first 15 min of cyclic eccentric contraction. , 1996, Journal of applied physiology.

[6]  S. Suresh,et al.  Cell and molecular mechanics of biological materials , 2003, Nature materials.

[7]  J. Goldman,et al.  GFAP mutations in Alexander disease , 2002, International Journal of Developmental Neuroscience.

[8]  K. Davies,et al.  Molecular mechanisms of muscular dystrophies: old and new players , 2006, Nature Reviews Molecular Cell Biology.

[9]  F. Terzi,et al.  Recovery of Na-glucose cotransport activity after renal ischemia is impaired in mice lacking vimentin. , 2004, American journal of physiology. Renal physiology.

[10]  Katherine L. Wilson,et al.  The nuclear lamina comes of age , 2005, Nature Reviews Molecular Cell Biology.

[11]  T. Sejersen,et al.  Forced expression of desmin and desmin mutants in cultured cells: impact of myopathic missense mutations in the central coiled-coil domain on network formation. , 2006, Experimental cell research.

[12]  U Aebi,et al.  Exploring the mechanical behavior of single intermediate filaments. , 2005, Journal of molecular biology.

[13]  J. Holton,et al.  Conspicuous involvement of desmin tail mutations in diverse cardiac and skeletal myopathies , 2007, Human mutation.

[14]  J. Schweizer,et al.  Characterization of a novel human type II epithelial keratin K1b, specifically expressed in eccrine sweat glands. , 2005, The Journal of investigative dermatology.

[15]  C. Babinet,et al.  Cardiovascular lesions and skeletal myopathy in mice lacking desmin. , 1996, Developmental biology.

[16]  R. Windoffer,et al.  Focal adhesions are hotspots for keratin filament precursor formation , 2006, The Journal of cell biology.

[17]  J. Sadoshima,et al.  Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism. , 1993, The EMBO journal.

[18]  D. Parry Hendecad repeat in segment 2A and linker L2 of intermediate filament chains implies the possibility of a right-handed coiled-coil structure. , 2006, Journal of structural biology.

[19]  M. Omary,et al.  "Heads and tails" of intermediate filament phosphorylation: multiple sites and functional insights. , 2006, Trends in biochemical sciences.

[20]  M. Mavroidis,et al.  Desmin Cytoskeleton Linked to Muscle Mitochondrial Distribution and Respiratory Function , 2000, The Journal of cell biology.

[21]  Ueli Aebi,et al.  Monitoring intermediate filament assembly by small-angle x-ray scattering reveals the molecular architecture of assembly intermediates , 2006, Proceedings of the National Academy of Sciences.

[22]  M. Vorgerd,et al.  Pathogenic effects of a novel heterozygous R350P desmin mutation on the assembly of desmin intermediate filaments in vivo and in vitro. , 2005, Human molecular genetics.

[23]  G. Taffet,et al.  Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[24]  P M Steinert,et al.  Molecular and cellular biology of intermediate filaments. , 1988, Annual review of biochemistry.

[25]  P. Coulombe,et al.  Keratin function in skin epithelia: a broadening palette with surprising shades. , 2007, Current opinion in cell biology.

[26]  Ueli Aebi,et al.  Functional complexity of intermediate filament cytoskeletons: from structure to assembly to gene ablation. , 2003, International review of cytology.

[27]  U Aebi,et al.  Characterization of distinct early assembly units of different intermediate filament proteins. , 1999, Journal of molecular biology.

[28]  Jinbao Liu,et al.  Impairment of the Ubiquitin-proteasome System in Desminopathy Mouse Hearts Clonal Hek Cell Lines Stably Expressing a Surrogate Ups Substrate (gfpu) , 2022 .

[29]  R. Moll,et al.  Attachment of vimentin filaments to desmosomal plaques in human meningiomal cells and arachnoidal tissue , 1984, The Journal of cell biology.

[30]  Y. Capetanaki Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. , 2002, Trends in cardiovascular medicine.

[31]  C. Schönenberger,et al.  Nanomechanics of microtubules. , 2002, Physical review letters.

[32]  S. Jalkanen,et al.  Vimentin function in lymphocyte adhesion and transcellular migration , 2006, Nature Cell Biology.

[33]  C. Babinet,et al.  Mice lacking vimentin develop and reproduce without an obvious phenotype , 1994, Cell.

[34]  Katherine L. Wilson,et al.  SUN-domain proteins: 'Velcro' that links the nucleoskeleton to the cytoskeleton , 2006, Nature Reviews Molecular Cell Biology.

[35]  Eran Perlson,et al.  Vimentin-Dependent Spatial Translocation of an Activated MAP Kinase in Injured Nerve , 2005, Neuron.

[36]  A. Prescott,et al.  The Alexander disease-causing glial fibrillary acidic protein mutant, R416W, accumulates into Rosenthal fibers by a pathway that involves filament aggregation and the association of alpha B-crystallin and HSP27. , 2006, American journal of human genetics.

[37]  L. Thornell,et al.  Null mutation in the desmin gene gives rise to a cardiomyopathy. , 1997, Journal of molecular and cellular cardiology.

[38]  E. Lazarides Intermediate filaments as mechanical integrators of cellular space , 1980, Nature.

[39]  P. Janmey,et al.  Nonlinear elasticity in biological gels , 2004, Nature.

[40]  T. Yanagida,et al.  Torsional rigidity of single actin filaments and actin-actin bond breaking force under torsion measured directly by in vitro micromanipulation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[41]  D. Allen,et al.  Loss of desmin leads to impaired voluntary wheel running and treadmill exercise performance. , 2003, Journal of applied physiology.

[42]  B. Lévy,et al.  Reduction of renal mass is lethal in mice lacking vimentin. Role of endothelin-nitric oxide imbalance. , 1997, The Journal of clinical investigation.

[43]  U. Aebi,et al.  Severe muscle disease-causing desmin mutations interfere with in vitro filament assembly at distinct stages. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  U. Aebi,et al.  Assembly defects of desmin disease mutants carrying deletions in the alpha-helical rod domain are rescued by wild type protein. , 2007, Journal of structural biology.

[45]  Francis S. Collins,et al.  Human laminopathies: nuclei gone genetically awry , 2006, Nature Reviews Genetics.

[46]  A. C. Park,et al.  Rheology of stratum corneum--I: A molecular interpretation of the stress-strain curve , 1972 .

[47]  P. Steinert,et al.  The function of intermediate filaments in cell shape and cytoskeletal integrity , 1996, The Journal of cell biology.

[48]  Joe Tien,et al.  Mechanotransduction at cell-matrix and cell-cell contacts. , 2004, Annual review of biomedical engineering.

[49]  M. Inagaki,et al.  Regulatory mechanisms and functions of intermediate filaments: A study using site‐ and phosphorylation state‐specific antibodies , 2006, Cancer science.

[50]  D. Parry,et al.  Keratin intermediate filament structure. Crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly. , 1993, Journal of molecular biology.

[51]  Jinbao Liu,et al.  Intrasarcoplasmic Amyloidosis Impairs Proteolytic Function of Proteasomes in Cardiomyocytes by Compromising Substrate Uptake , 2005, Circulation research.

[52]  A. Samarel,et al.  Costameres, focal adhesions, and cardiomyocyte mechanotransduction. , 2005, American journal of physiology. Heart and circulatory physiology.

[53]  W. Franke,et al.  The area composita of adhering junctions connecting heart muscle cells of vertebrates. VI. Different precursor structures in non-mammalian species. , 2008, European journal of cell biology.

[54]  F. Ren,et al.  Thermal stability of W ohmic contacts to n‐type GaN , 1996 .

[55]  Y. Capetanaki,et al.  Disruption of muscle architecture and myocardial degeneration in mice lacking desmin , 1996, The Journal of cell biology.

[56]  M. Beckerle,et al.  Striated muscle cytoarchitecture: an intricate web of form and function. , 2002, Annual review of cell and developmental biology.

[57]  D. Ingber,et al.  Cellular mechanotransduction: putting all the pieces together again , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[58]  R. Liem,et al.  Plakins: Goliaths that link cell junctions and the cytoskeleton , 2004, Nature Reviews Molecular Cell Biology.

[59]  R. Foisner,et al.  A-type lamin complexes and regenerative potential: a step towards understanding laminopathic diseases? , 2005, Histochemistry and Cell Biology.

[60]  R. Kayed,et al.  Reversal of amyloid-induced heart disease in desmin-related cardiomyopathy. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[61]  U. Aebi,et al.  Exploring the mechanical properties of single vimentin intermediate filaments by atomic force microscopy. , 2006, Journal of molecular biology.

[62]  H. van Essen,et al.  Altered flow-induced arterial remodeling in vimentin-deficient mice. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[63]  C. Stewart,et al.  Aging and nuclear organization: lamins and progeria. , 2004, Current opinion in cell biology.

[64]  Ueli Aebi,et al.  A Quantitative Kinetic Model for the in Vitro Assembly of Intermediate Filaments from Tetrameric Vimentin* , 2007, Journal of Biological Chemistry.

[65]  Hans Janssen,et al.  Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin , 2005, The Journal of cell biology.

[66]  K Weber,et al.  Intermediate filaments: structure, dynamics, function, and disease. , 1994, Annual review of biochemistry.

[67]  M. Omary,et al.  Intermediate filament proteins and their associated diseases. , 2004, The New England journal of medicine.

[68]  J. Hess,et al.  Characterization of the linker 2 region in human vimentin using site-directed spin labeling and electron paramagnetic resonance. , 2006, Biochemistry.

[69]  J. Gosline,et al.  Molecular design of the α–keratin composite: insights from a matrix–free model, hagfish slime threads , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  U. Aebi,et al.  Conserved segments 1A and 2B of the intermediate filament dimer: their atomic structures and role in filament assembly , 2002, The EMBO journal.

[71]  C. Grund,et al.  The area composita of adhering junctions connecting heart muscle cells of vertebrates. I. Molecular definition in intercalated disks of cardiomyocytes by immunoelectron microscopy of desmosomal proteins. , 2006, European journal of cell biology.

[72]  Peter F. Davies,et al.  Shear Stress Biology of the Endothelium , 2005, Annals of Biomedical Engineering.

[73]  R. Goldman,et al.  Disruption of Nuclear Lamin Organization Blocks the Elongation Phase of DNA Replication , 2000, The Journal of cell biology.

[74]  L. Kreplak,et al.  Investigation of the morphology of intermediate filaments adsorbed to different solid supports. , 2005, Journal of structural biology.

[75]  Richard J. Goss,et al.  10 – Heads and Tails , 1969 .

[76]  P. Coulombe,et al.  Intermediate filaments and tissue repair. , 2004, Experimental cell research.

[77]  R. Robson,et al.  Assembly of vimentin in vitro and its implications concerning the structure of intermediate filaments. , 1985, Journal of molecular biology.

[78]  D. Ingber,et al.  Mechanotransduction across the cell surface and through the cytoskeleton , 1993 .

[79]  ElizabethMurphy,et al.  Mitochondrial Dysfunction and Apoptosis Underlie the Pathogenic Process in α-B-Crystallin Desmin-Related Cardiomyopathy , 2005 .

[80]  F. Muntoni,et al.  Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy , 1999, Nature Genetics.

[81]  U. Aebi,et al.  The nuclear lamina is a meshwork of intermediate-type filaments , 1986, Nature.

[82]  Ueli Aebi,et al.  Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. , 2003, Annual review of biochemistry.

[83]  Elaine Fuchs,et al.  Intercellular adhesion, signalling and the cytoskeleton , 2002, Nature Cell Biology.

[84]  E. Lane,et al.  Keratins and skin disorders , 2004, The Journal of pathology.

[85]  C. S. Chen,et al.  Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[86]  R. Merkel,et al.  Desmin filaments studied by quasi-elastic light scattering. , 1999, Biophysical journal.

[87]  P. Janmey,et al.  Viscoelastic properties of vimentin compared with other filamentous biopolymer networks , 1991, The Journal of cell biology.

[88]  W. Birchmeier,et al.  Requirement of plakophilin 2 for heart morphogenesis and cardiac junction formation , 2004, The Journal of cell biology.

[89]  N. Balaban,et al.  Adhesion-dependent cell mechanosensitivity. , 2003, Annual review of cell and developmental biology.

[90]  H. Worman,et al.  Nuclear envelope, nuclear lamina, and inherited disease. , 2005, International review of cytology.

[91]  G Büldt,et al.  Imaging purple membranes in aqueous solutions at sub-nanometer resolution by atomic force microscopy. , 1995, Biophysical journal.

[92]  Yiider Tseng,et al.  A Direct Interaction between Actin and Vimentin Filaments Mediated by the Tail Domain of Vimentin* , 2006, Journal of Biological Chemistry.

[93]  K. Campbell,et al.  Interactions of intermediate filament protein synemin with dystrophin and utrophin. , 2006, Biochemical and biophysical research communications.

[94]  Laurent Kreplak,et al.  Biomechanical properties of intermediate filaments: from tissues to single filaments and back , 2007, BioEssays : news and reviews in molecular, cellular and developmental biology.

[95]  U Aebi,et al.  Structure and assembly properties of the intermediate filament protein vimentin: the role of its head, rod and tail domains. , 1996, Journal of molecular biology.

[96]  R. Goldman,et al.  Pathway of incorporation of microinjected lamin A into the nuclear envelope , 1992, The Journal of cell biology.

[97]  S. Müller,et al.  Impact of disease mutations on the desmin filament assembly process. , 2006, Journal of molecular biology.

[98]  R. Lal,et al.  Disulfide bonds in the outer layer of keratin fibers confer higher mechanical rigidity: correlative nano-indentation and elasticity measurement with an AFM. , 1999, Biochemistry.

[99]  C. Babinet,et al.  Cerebellar defect and impaired motor coordination in mice lacking vimentin , 1999, Glia.

[100]  Andrew D McCulloch,et al.  Structural and functional roles of desmin in mouse skeletal muscle during passive deformation. , 2004, Biophysical journal.

[101]  David A Weitz,et al.  The cell as a material. , 2007, Current opinion in cell biology.

[102]  D. Wirtz,et al.  Nuclear Envelope Breakdown Requires Overcoming the Mechanical Integrity of the Nuclear Lamina* , 2004, Journal of Biological Chemistry.

[103]  J Langowski,et al.  Assessing the flexibility of intermediate filaments by atomic force microscopy. , 2004, Journal of molecular biology.

[104]  J. Schloss,et al.  Cytoplasmic fibers in mammalian cells: cytoskeletal and contractile elements. , 1979, Annual review of physiology.

[105]  D. Adams,et al.  Human and rat hepatic stellate cells express synemin, a protein bridging intermediate filaments to focal adhesions , 2005 .