Intermediate filaments: From cell architecture to nanomechanics

Nature Reviews Molecular Cell Biology

Volumn 8, Issue 7, 2007, Pages 562-573

  Herrmann, Harald ^a   Bär, Harald ^a,b   Kreplak, Laurent ^c   Strelkov, Sergei V ^d   Aebi, Ueli ^c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; LAMIN; NUCLEAR PROTEIN; SMAD PROTEIN; VIMENTIN;

ALEXANDER DISEASE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL JUNCTION; CELL MEMBRANE; CELL NUCLEUS; CELL STRUCTURE; CELL TYPE; CYTOARCHITECTURE; CYTOPLASM; CYTOSKELETON; DYNAMICS; HUMAN; INTERMEDIATE FILAMENT; MECHANICAL STRESS; MECHANOTRANSDUCTION; MOLECULAR MECHANICS; MUSCULAR DYSTROPHY; MUTATION; MYOPATHY; NONHUMAN; PATHOGENESIS; PHYSIOLOGY; PREMATURE AGING; PRIORITY JOURNAL; PROGERIA; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; TISSUE SPECIFICITY; WERNER SYNDROME;

AMINO ACID SEQUENCE; ANIMALS; BIOMECHANICS; CELL NUCLEUS; CYTOPLASM; CYTOSKELETON; DIMERIZATION; HUMANS; INTERMEDIATE FILAMENTS; LAMINS; MODELS, BIOLOGICAL; MUTATION; NANOTECHNOLOGY; PROTEIN STRUCTURE, TERTIARY;

ANIMALIA;

EID: 34250880140     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2197     Document Type: Review

References (106)

1. Goldman, R. D., Milsted, A., Schloss, J. A., Starger, J. & Yerna, M. J. Cytoplasmic fibers in mammalian cells: cytoskeletal and contractile elements. Annu. Rev. Physiol. 41, 703-722 (1979).
2. Lazarides, E. Intermediate filaments as mechanical integrators of cellular space. Nature 283, 249-256 (1980).
3. Fuchs, E. & Weber, K. Intermediate filaments: structure, dynamics, function, and disease. Annu. Rev. Biochem. 63, 345-382 (1994).
4. Herrmann, H., Hesse, M., Reichenzeller, M., Aebi, U. & Magin, T. M. Functional complexity of intermediate filament cytoskeletons: from structure to assembly to gene ablation. Int. Rev. Cytol. 223, 83-175 (2003).
5. Omary, M. B., Coulombe, P. A. & McLean, W. H. Intermediate filament proteins and their associated diseases. N. Engl. J. Med. 351, 2087-2100 (2004).
6. Capell, B. C. & Collins, F. S. Human laminopathies: nuclei gone genetically awry. Nature Rev. Genet. 7, 940-952 (2006).
7. Green, K. J., Bohringer, M., Gocken, T. & Jones, J. C. Intermediate filament associated proteins. Adv. Protein Chem. 70, 143-202 (2005).
8. Bershadsky, A. D., Balaban, N. Q. & Geiger, B. Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19, 677-695 (2003).
9. Herrmann, H. & Aebi, U. Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds. Annu. Rev. Biochem. 73, 749-789 (2004).
10. Goldman, R. D., Khuon, S., Chou, Y. H., Opal, P. & Steinert, P. M. The function of intermediate filaments in cell shape and cytoskeletal integrity. J. Cell Biol. 134, 971-983 (1996). The injection of peptides that represent coil 1A of vimentin into fibroblasts leads to the disassembly of IFs, followed by a massive reorganization of the whole cytoskeleton and alterations of cellular shape.
11. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. & Wilson, K. L. The nuclear lamina comes of age. Nature Rev. Mol. Cell Biol. 6, 21-31 (2005).
12. Tzur, Y. B., Wilson, K. L. & Gruenbaum, Y. SUN-domain proteins: 'Velcro' that links the nucleoskeleton to the cytoskeleton. Nature Rev. Mol. Cell Biol. 7, 782-788 (2006).
13. Roper, K., Gregory, S. L. & Brown, N. H. The 'spectraplakins': cytoskeletal giants with characteristics of both spectrin and plakin families. J. Cell Sci. 115, 4215-4225 (2002).
14. Wilhelmsen, K. et al. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 171, 799-810 (2005). The outer nuclear membrane protein nesprin-3 is shown to bind to and recruit plectin to the nuclear periphery, suggesting that a continuous connection between the nucleus and the extracellular matrix is mediated with the help of the IF cytoskeleton and the integrin system.
15. Jefferson, J. J., Leung, C. L. & Liem, R. K. Plakins: goliaths that link cell junctions and the cytoskeleton. Nature Rev. Mol. Cell Biol. 5, 542-553 (2004).
16. Maniotis, A. J., Chen, C. S. & Ingber, D. E. Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl Acad. Sci. USA 94, 849-854 (1997).
17. Chen, C. S., Tan, J. & Tien, J. Mechanotransduction at cell-matrix and cell-cell contacts. Annu. Rev. Biomed. Eng. 6, 275-302 (2004).
18. Langbein, L. et al. Characterization of a novel human type II epithelial keratin K1b, specifically expressed in eccrine sweat glands. J. Invest. Dermatol. 125, 428-444 (2005).
19. Kartenbeck, J., Schwechheimer, K., Moll, R. & Franke, W. W. Attachment of vimentin filaments to desmosomal plaques in human meningiomal cells and arachnoidal tissue. J. Cell Biol. 98, 1072-1081 (1984).
20. Franke, W. W., Borrmann, C. M., Grund, C. & Pieperhoff, S. 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. Eur. J. Cell Biol. 85, 69-82 (2006).
21. Gerull, B. et al. Mutations in the desmosomal protein plakophilin-2 are common in arrhythmogenic right ventricular cardiomyopathy. Nature Genet. 36, 1162-1164 (2004).
22. Grossmann, K. S. et al. Requirement of plakophilin 2 for heart morphogenesis and cardiac junction formation. J. Cell Biol. 167, 149-160 (2004).
23. DePianto, D. & Coulombe, P. A. Intermediate filaments and tissue repair. Exp. Cell Res. 301, 68-76 (2004).
24. Aebi, U., Cohn, J., Buhle, L. & Gerace, L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323, 560-564 (1986).
25. Foeger, N. et al. Solubility properties and specific assembly pathways of the B-type lamin from Caenorhabditis elegans. J. Struct. Biol. 155, 340-350 (2006). Characterizes the solution state of several forms of recombinant lamins and shows that lamin assembly can progress extremely fast in vitro compared with the assembly of cytoplasmic IF protein vimentin.
26. Steinert, P. M., Marekov, L. N., Fraser, R. D. & Parry, D. A. Keratin intermediate filament structure. Crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly. J. Mol. Biol. 230, 436-452 (1993).
27. Izawa, I. & Inagaki, M. Regulatory mechanisms and functions of intermediate filaments: a study using site-and phosphorylation state-specific antibodies. Cancer Sci. 97, 167-174 (2006).
28. Ip, W., Hartzer, M. K., Pang, Y. Y. & Robson, R. M. Assembly of vimentin in vitro and its implications concerning the structure of intermediate filaments. J. Mol. Biol. 183, 365-375 (1985).
29. Herrmann, H. et al. Structure and assembly properties of the intermediate filament protein vimentin: The role of its head, rod and tail domains. J. Mol. Biol. 264, 933-953 (1996).
30. Helfand, B. T., Chang, L. & Goldman, R. D. The dynamic and motile properties of intermediate filaments. Annu. Rev. Cell Dev. Biol. 19, 445-467 (2003).
31. Samarel, A. M. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am. J. Physiol. Heart Circ. Physiol. 289, H2291-H2301 (2005).
32. Bhosle, R. C., Michele, D. E., Campbell, K. P., Li, Z. & Robson, R. M. Interactions of intermediate filament protein synemin with dystrophin and utrophin. Biochem. Biophys. Res. Commun. 346, 768-777 (2006).
33. Uyama, N. et al. Hepatic stellate cells express synemin, a protein bridging intermediate filaments to focal adhesions. Gut 55, 1276-1289 (2006).
34. Kasza, K. E. et al. The cell as a material. Curr. Opin. Cell Biol. 19, 101-107 (2007).
35. Sokolova, A. V. et al. Monitoring intermediate filament assembly by small-angle x-ray scattering reveals the molecular architecture of assembly intermediates. Proc. Natl Acad. Sci. USA 103, 16206-16211 (2006). The first study of vimentin assembly in solution using small-angle X-ray scattering, which led to 3D molecular models of tetramers, octamers and the ULFs.
36. Herrmann, H., Haner, M., Brettel, M., Ku, N. O. & Aebi, U. Characterization of distinct early assembly units of different intermediate filament proteins. J. Mol. Biol. 286, 1403-1420 (1999).
37. Kirmse, R. et al. A quantitative kinetic model for the in vitro assembly of intermediate filaments from tetrameric vimentin. J. Biol. Chem. 2 Apr 2007 (doi:10.1074/jbc.M701063200).
38. Panorchan, P., Schafer, B. W., Wirtz, D. & Tseng, Y. Nuclear envelope breakdown requires overcoming the mechanical integrity of the nuclear lamina. J. Biol. Chem. 279, 43462-43467 (2004).
39. Windoffer, R., Kolsch, A., Woll, S. & Leube, R. E. Focal adhesions are hotspots for keratin filament precursor formation. J. Cell Biol. 173, 341-348 (2006). The regulatory potential of focal adhesions for keratin IF assembly is demonstrated, and this property provides a basis for the coordinated shaping of the cytoskeleton during structural reorganization events of the cell.
40. Goldman, A. E., Moir, R. D., Montag-Lowy, M., Stewart, M. & Goldman, R. D. Pathway of incorporation of microinjected lamin A into the nuclear envelope. J. Cell Biol. 119, 725-735 (1992).
41. Moir, R. D., Spann, T. P., Herrmann, H. & Goldman, R. D. Disruption of nuclear lamin organization blocks the elongation phase of DNA replication. J. Cell Biol. 149, 1179-1192 (2000).
42. Mücke, N., Kirmse, R., Wedig, T., Leterrier, J. F. & Kreplak, L. Investigation of the morphology of intermediate filaments adsorbed to different solid supports. J. Struct. Biol. 150, 268-276 (2005).
43. Mücke, N. et al. Assessing the flexibility of intermediate filaments by atomic force microscopy. J. Mol. Biol. 335, 1241-1250 (2004).
44. Storm, C., Pastore, J. J., MacKintosh, F. C., Lubensky, T. C. & Janmey, P. A. Nonlinear elasticity in biological gels. Nature 435, 191-194 (2005).
45. Park, A. C. & Baddiel, C. B. Rheology of the stratum corneum: a molecular interpretation of the stress-strain curve. J. Soc. Cosmet. Chem. 23, 3-12 (1972).
46. Fudge, D. S. & Gosline, J. M. Molecular design of the ?-keratin composite: insights from a matrix-free model, hagfish slime threads. Proc. Biol. Sci. 271, 291-299 (2004).
47. Parbhu, A. N., Bryson, W. G. & Lal, R. Disulfide bonds in the outer layer of keratin fibers confer higher mechanical rigidity: correlative nano-indentation and elasticity measurement with an AFM. Biochemistry 38, 11755-11761 (1999).
48. Kreplak, L., Bär, H., Leterrier, J. F., Herrmann, H. & Aebi, U. Exploring the mechanical behavior of single intermediate filaments. J. Mol. Biol. 354, 569-577 (2005).
49. Janmey, P. A., Euteneuer, U., Traub, P. & Schliwa, M. Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J. Cell Biol. 113, 155-160 (1991).
50. Kreplak, L. & Fudge, D. Biomechanical properties of intermediate filaments: from tissues to single filaments and back. Bioessays 29, 26-35 (2007).
51. Tsuda, Y., Yasutake, H., Ishijima, A. & Yanagida, T. Torsional rigidity of single actin filaments and actin-actin bond breaking force under torsion measured directly by in vitro micromanipulation. Proc. Natl Acad. Sci. USA 93, 12937-12942 (1996).
52. Brangwynne, C. P. et al. Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J. Cell Biol. 173, 733-741 (2006).
53. Esue, O., Carson, A. A., Tseng, Y. & Wirtz, D. A direct interaction between actin and vimentin filaments mediated by the tail domain of vimentin. J. Biol. Chem. 281, 30393-30399 (2006).
54. Hohenadl, M., Storz, T., Kirpal, H., Kroy, K. & Merkel, R. Desmin filaments studied by quasi-elastic light scattering. Biophys. J. 77, 2199-2209 (1999).
55. Bao, G. & Suresh, S. Cell and molecular mechanics of biological materials. Nature Mater. 2, 715-725 (2003).
56. Wang, N., Butler, J. P. & Ingber, D. E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127 (1993).
57. Sadoshima, J. & Izumo, S. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism. EMBO J. 12, 1681-1692 (1993).
58. Omary, M. B., Ku, N. O., Tao, G. Z., Toivola, D. M. & Liao, J. "Heads and tails" of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem. Sci. 31, 383-394 (2006).
59. Gu, L. H. & Coulombe, P. A. Keratin function in skin epithelia: a broadening palette with surprising shades. Curr. Opin. Cell Biol. 19, 13-23 (2007).
60. Ingber, D. E. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20, 811-827 (2006).
61. Colucci-Guyon, E. et al. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79, 679-694 (1994).
62. Terzi, F. et al. Reduction of renal mass is lethal in mice lacking vimentin. Role of endothelin-nitric oxide imbalance. J. Clin. Invest. 100, 1520-1528 (1997).
63. Schiffers, P. M. et al. Altered flow-induced arterial remodeling in vimentin-deficient mice. Arterioscler. Thromb. Vasc. Biol. 20, 611-616 (2000).
64. Davies, P. F., Spaan, J. A. & Krams, R. Shear stress biology of the endothelium. Ann. Biomed. Eng. 33, 1714-1718 (2005).
65. Runembert, I. et al. Recovery of Na-glucose cotransport activity after renal ischemia is impaired in mice lacking vimentin. Am. J. Physiol. Renal Physiol. 287, F960-F968 (2004).
66. Colucci-Guyon, E., Gimenez, Y. R. M., Maurice, T., Babinet, C. & Privat, A. Cerebellar defect and impaired motor coordination in mice lacking vimentin. Glia 25, 33-43 (1999).
67. Perlson, E. et al. Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45, 715-726 (2005).
68. Nieminen, M. et al. Vimentin function in lymphocyte adhesion and transcellular migration. Nature Cell Biol. 8, 156-162 (2006).
69. Lane, E. B. & McLean, W. H. Keratins and skin disorders. J. Pathol. 204, 355-366 (2004).
70. Goldfarb, L. G., Vicart, P., Goebel, H. H. & Dalakas, M. C. Desmin myopathy. Brain 127, 723-734 (2004).
71. Bonne, G. et al. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nature Genet. 21, 285-288 (1999).
72. Worman, H. J. & Courvalin, J. C. Nuclear envelope, nuclear lamina, and inherited disease. Int. Rev. Cytol. 246, 231-279 (2005).
73. Mounkes, L. C. & Stewart, C. L. Aging and nuclear organization: lamins and progeria. Curr. Opin. Cell Biol. 16, 322-327 (2004).
74. Gotzmann, J. & Foisner, R. A-type lamin complexes and regenerative potential: a step towards understanding laminopathic diseases? Histochem. Cell Biol. 125, 33-41 (2006).
75. Li, R., Messing, A., Goldman, J. E. & Brenner, M. GFAP mutations in Alexander disease. Int. J. Dev. Neurosci. 20, 259-268 (2002).
76. Der Perng, M. 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 αB-crystallin and HSP27. Am. J. Hum. Genet. 79, 197-213 (2006). Describes the consequences of an Arg to Trp mutation in GFAP. Specifically, impaired assembly leading to protein aggregation and chaperone sequestration are shown to represent early events in Alexander disease.
77. Jamora, C. & Fuchs, E. Intercellular adhesion, signalling and the cytoskeleton. Nature Cell Biol. 4, E101-E108 (2002).
78. Clark, K. A., McElhinny, A. S., Beckerle, M. C. & Gregorio, C. C. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18, 637-706 (2002).
79. Bär, H. et al. Severe muscle disease-causing desmin mutations interfere with in vitro filament assembly at distinct stages. Proc. Natl Acad. Sci. USA 102, 15099-15104 (2005).
80. Bär, H. et al. Impact of disease mutations on the desmin filament assembly process. J. Mol. Biol. 360, 1031-1042 (2006). The structural implications for the polymorphism of IFs generated by mutant desmin are revealed using several biophysical methods, including analytical ultracentrifugation, viscometry and scanning transmission electron microscopy.
81. Bär, H., Mücke, N., Katus, H. A., Aebi, U. & Herrmann, H. Assembly defects of desmin disease mutants carrying deletions in the α-helical rod domain are rescued by wild type protein. J. Struct. Biol. 158, 107-115 (2007).
82. Bär, H. et al. Conspicuous involvement of desmin tail mutations in diverse cardiac and skeletal myopathies. Hum. Mutat. 28, 374-386 (2007).
83. Bär, H. 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. Exp. Cell Res. 312, 1554-1565 (2006).
84. Chen, Q. et al. Intrasarcoplasmic amyloidosis impairs proteolytic function of proteasomes in cardiomyocytes by compromising substrate uptake. Circ. Res. 97, 1018-1026 (2005).
85. Liu, J. et al. Impairment of the ubiquitin-proteasome system in desminopathy mouse hearts. FASEB J. 20, 362-364 (2006).
86. Sanbe, A. et al. Reversal of amyloid-induced heart disease in desmin-related cardiomyopathy. Proc. Natl Acad. Sci. USA 102, 13592-13597 (2005).
87. Milner, D. J., Mavroidis, M., Weisleder, N. & Capetanaki, Y. Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J. Cell Biol. 150, 1283-1298 (2000). Physiological studies with muscle derived from desmin-null mice demonstrate that desmin IFs are important for proper mitochondrial positioning and respiratory function in cardiac and skeletal muscle.
88. Maloyan, A. et al. Mitochondrial dysfunction and apoptosis underlie the pathogenic process in α-B-crystallin desmin-related cardiomyopathy. Circulation 112, 3451-3461 (2005).
89. Davies, K. E. & Nowak, K. J. Molecular mechanisms of muscular dystrophies: old and new players. Nature Rev. Mol. Cell Biol. 7, 762-773 (2006).
90. Lieber, R. L., Thornell, L. E. & Friden, J. Muscle cytoskeletal disruption occurs within the first 15 min of cyclic eccentric contraction. J. Appl. Physiol. 80, 278-284 (1996).
91. Shah, S. B. et al. Structural and functional roles of desmin in mouse skeletal muscle during passive deformation. Biophys. J. 86, 2993-3008 (2004).
92. Li, Z. et al. Cardiovascular lesions and skeletal myopathy in mice lacking desmin. Dev. Biol. 175, 362-366 (1996).
93. Milner, D. J., Weitzer, G., Tran, D., Bradley, A. & Capetanaki, Y. Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J. Cell Biol. 134, 1255-1270 (1996).
94. Thornell, L., Carlsson, L., Li, Z., Mericskay, M. & Paulin, D. Null mutation in the desmin gene gives rise to a cardiomyopathy. J. Mol. Cell. Cardiol. 29, 2107-2124 (1997).
95. Weisleder, N., Taffet, G. E. & Capetanaki, Y. Bcl-2 overexpression corrects mitochondrial defects and ameliorates inherited desmin null cardiomyopathy. Proc. Natl Acad. Sci. USA 101, 769-774 (2004).
96. Capetanaki, Y. Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc. Med. 12, 339-348 (2002).
97. Haubold, K. W., Allen, D. L., Capetanaki, Y. & Leinwand, L. A. Loss of desmin leads to impaired voluntary wheel running and treadmill exercise performance. J. Appl. Physiol. 95, 1617-1622 (2003).
98. Steinert, P. M. & Roop, D. R. Molecular and cellular biology of intermediate filaments. Annu. Rev. Biochem. 57, 593-625 (1988).
99. Strelkov, S. V. et al. Conserved segments 1A and 2B of the intermediate filament dimer: their atomic structures and role in filament assembly. EMBO J. 21, 1255-1266 (2002).
100. Parry, D. A. Hendecad repeat in segment 2A and linker L2 of intermediate filament chains implies the possibility of a right-handed coiled-coil structure. J. Struct. Biol. 155, 370-374 (2006).
101. Hess, J. F., Budamagunta, M. S., Shipman, R. L., FitzGerald, P. G. & Voss, J. C. Characterization of the linker 2 region in human vimentin using site-directed spin labeling and electron paramagnetic resonance. Biochemistry 45, 11737-11743 (2006).
102. Müller, D. J., Schabert, F. A., Buldt, G. & Engel, A. Imaging purple membranes in aqueous solutions at sub-nanometer resolution by atomic force microscopy. Biophys. J. 68, 1681-1686 (1995).
103. Kiss, B., Karsai, A. & Kellermayer, M. S. Nanomechanical properties of desmin intermediate filaments. J. Struct. Biol. 155, 327-339 (2006).
104. Kis, A. et al. Nanomechanics of microtubules. Phys. Rev. Lett. 89, 248101 (2002).
105. Guzman, C. et al. Exploring the mechanical properties of single vimentin intermediate filaments by atomic force microscopy. J. Mol. Biol. 360, 623-630 (2006). Using AFM, the bending modulus of non-stabilized single vimentin IFs, hanging over a porous membrane, was determined by elastic deformation with the tip of the microscope cantilever.
106. Bär, H. et al. Pathogenic effects of a novel heterozygous R350P desmin mutation on the assembly of desmin intermediate filaments in vivo and in vitro. Hum. Mol. Genet. 14, 1251-1260 (2005).