Impaired mechanical stability, migration and contractile capacity in vimentin deficient fibroblasts

Journal of Cell Science

Volumn 111, Issue 13, 1998, Pages 1897-1907

  Eckes, Beate ^a   Dogic, Dagmar ^b   Colucci Guyon, Emma ^c   Wang, Ning ^d   Maniotis, Andrew ^e   Ingber, Donald ^e   Merckling, Alexandra ^a   Langa, Francina ^c   Aumailley, Monique ^b   Delouvée, Annie ^f   Koteliansky, Victor ^f   Babinet, Charles ^c   Krieg, Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^c INSTITUT PASTEUR   (France)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f INSTITUT CURIE   (France)

Author keywords

Collagen lattice; Cytoskeleton; In vitro wound healing; Mechanotransduction; Tensegrity

Indexed keywords

ACTIN; COLLAGEN FIBRIL; VIMENTIN;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL MOTILITY; EMBRYO; FIBROBLAST; MICROFILAMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL;

NASA DISCIPLINE CELL BIOLOGY; NON-NASA CENTER;

ACTINS; ANIMALS; CELL ADHESION; CELL MOVEMENT; CELL SIZE; CELLS, CULTURED; CHEMOTAXIS; COLLAGEN; FIBROBLASTS; INTERCELLULAR JUNCTIONS; MICE; MICE, KNOCKOUT; STRESS, MECHANICAL; VIMENTIN;

ANIMALIA;

EID: 0031850378     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Albini, A. and Adelmann-Grill, B. C. (1985). Collagenolytic cleavage products of collagen lype I as chemoattractants for human dermal fibroblasts. Eur. J. Cell Biol. 36, 104-107.
2. Bell, E., Ivarsson, B. and Merill, C. (1979). Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Nat. Acad. USA 76, 1274-1278.
3. Bershadsky, A. D., Tint, I. S. and Svitkina, T. M. (1987). Association of intermediate filaments with vinculin-containing adhesion plaques of fibroblasts. Cell Motil. Cytoskel. 8, 274-283.
4. Capetanaki, Y., Starnes, S. and Smith, S. (1989). Expression of the chicken vimentin gene in transgenic mice: Efficient assembly of the avian protein into the cytoskeleton. Proc. Nat. Acad. Sci. USA 86, 4882-4886.
5. Capetanaki, Y., Smith, S. and Heath, J. P. (1989a). Overexprcssion of the vimentin gene in transgenic mice exhibits normal lens cell differentiation. J. Cell Biol. 109, 1653-1664.
6. Cochard, P. and Paulin, D. (1984). Initial expression of neurofilaments and vimentin in the central and peripheral nervous system of the mouse embryo in vivo. J. Neurosci. 4, 2080-2094.
7. Colucci-Guyon, E., Portier, M. M., Dunia, I., Paulin, D., Pournin, S. and Babinet, C. (1994). Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79, 679-694.
8. Dunia, I., Pieper, F., Manenti, S., van de Kemp, A., Devilliers, G., Benedetti, E. L. and Bloemendal, H. (1990). Plasma membranecytoskeleton damage in eye lenses of transgenic mice expressing desmin. Eur. J. Cell Biol. 53, 59-74.
9. Franke, W. W., Grand, C., Kuhn, C., Jackson, B. W. and Illmensee, K. (1982). Formation of cytoskeletal elements during mouse embryogenesis. III. Primary mesenchymal cells and the first appearance of vimentin filaments. Differentiation 23, 43-59.
10. Franke, W. W., Hergt, M. and Grund, C. (1987). Rearrangement of vimentin cytoskeleton during adipose conversion: formation of an intermediate filament cage around lipid globules. Cell 49, 131-141.
11. Fuchs, E., Coulombe, P., Cheng, J., Chan, Y., Hutton, E., Snyder, A., Degenstein, L., Letai, Y. Q.-C. A. and Vassar, R. (1994). Gentic basis of epidermolysis bullosa simplex and epidermolytic hyperkeratosis. J. Invest. Dermatol. 103, 25s-30s.
12. Fürst, D, O., Osborn, M. and Weber, K. (1989). Myogenesis in the mouse embryo: Differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J. Cell Biol. 109, 517-527.
13. Gailit, J. and Clark, R. A. F. (1994). Wound repair in the context of extracellular matrix. Curr. Opin. Cell Biol. 6, 717-725.
14. Galou, M., Colucci-Guyon, E., Ensergueix, D., Ridet, J.-L., Gimenez y Ribotta, M., Privat, A., Babinet, C. and Dupouey, P. (1996). Disrupted glial fibrillary acidic protein network in astrocytes from vimentin knockout mice. J. Cell Biol. 133, 853-863.
15. Gawlitta, W., Osborn, M. and Weber, K. (1981). Coiling of intermediate filaments by microinjection of a vimentin specific antibody does not interfere with locomotion and mitosis. Eur. J. Cell Biol. 26, 83-90.
16. Goldman, R. D., Khuon, S., Chou, Y. H., Opal, P. and Steínert, P. M. (1996). The function of intermediate filaments in cell shape and cytoskeletal integrity. J. Cell Biol. 134, 971-983.
17. Gotwals, P. J., Chi-Rosso, G., Lindner, V., Yang, J., Ling, L., Fawell, S. E. and Koteliansky, V. E. (1996). The α1β1 integrin is expressed during neointima formation in rat arteries and mediates collagen matrix reorganization. J. Clin. Invest. 97, 2469-2477.
18. Green, K. J. and Goldman, R. D. (1986). Evidence for an interaction between the cell surface and intermediate filaments in cultured fibroblasts. Cell Motil. Cytoskel. 6, 389-405.
19. Grinnell, F. (1994). Fibroblasts, myofibroblasts, and wound contraction. J. Cell Biol. 124, 401-404.
20. Gurland, G. and Gunderson, G. G. (1995). Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J. Cell Biol. 131, 1275-1290.
21. Hedberg, K. K. and Chen, L. B. (1986). Absence of intermediate filaments in a human adrenal cortex carcinoma-derived cell line. Exp. Cell Res. 163, 509-517.
22. Holwell, T. A., Schweitzer, S. C. and Evans, R. M. (1997) Tetracycline regulated expression of vimentin in fibroblasls derived from vimemin null mice. J. Cell Sci. 110, 1947-1956
23. Ingber, D. E. (1990). Fibronectin controls capillary endothelial cell growth by modulating cell shape. Proc. Nat. Acad. Sci. USA 87, 3579-3583.
24. Ingber, D. E., Dike, L., Hansen, L., Karp, S., Liley, H., Maniotis, A., McNamee, H., Mooney, D., Plopper, G., Sims, J. and Wang, N. (1994) Cellular tensegrity: exploring how mechanical changes in the cytoskeleton regulate cell growth, migration and tissue pattern during morphogenesis. Int. Rev. Cytol. 150, 173-224.
25. Janmey, P. A. (1991). Mechanical properties of cytoskeletal polymers. Curr. Opin. Cell Biol. 2, 4-11.
26. Janmey, P. A., Euteneuer, U., Traub, P. and Schliwa, M. (1991). Viscoelastic properties of vimentin compared with other filamentous biopolymer networks. J. Cell Biol. 113, 155-160.
27. Klein, C. K., Dressel, D., Steinmayer, T., Mauch, C., Eckes, B., Krieg, T., Bankert, R. B. and Weber, L. (1991). Integrin α2β1 is upregulated in fibroblasts and highly aggressive melanoma cells in three-dimensional collagen lattices and mediates the reorganization of collagen I fibrils. J. Cell Biol. 115, 1427-1436.
28. Klymkowsky, M. W. (1981). Intermediate filaments in 3T3 cells collapse after intracellular injection of a monoclonal anti-intermediate filament antibody. Nature 291, 249-251.
29. Klymkowsky, M. W., Bachant, J. B. and Domingo, A. (1989). Functions of intermediate filaments. Cell Motil. Cytoskel. 14, 309-331.
30. Koller, B. H. and Smithies, O. (1992). Altering genes in animals by gene targeting. Anna. Rev. Immunol. 10, 705-730.
31. Lambert, C. A., Soudant E. P., Nusgens, B. V. and Lapière, Ch. M. (1992). Pretranslational regulation of extracellular matrix macromolecules and collagenase expression in fibroblasts by mechanical forces. Lab. Invest. 66, 444-451.
32. Lane, E. B., Hogan, L. M., Kurkinen, M. and Garrels, J. I. (1983). Coexpression of vimenlin and cytokeratin in parietal endoderm cells of early mouse embryo. Nature 303, 701-704.
33. Langholz, O., Röckel, D., Mauch C., Kozlowska, E., Bank, I., Krieg, T. and Eckes, B. (1995). Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by α1β1 and α2β1 integrins. J. Cell Biol. 131, 1903-1915.
34. Lee, J., Ishihara, A. and Jacobson, K. (1993) How do cells move along surfaces? Trends Cell Biol. 3, 366-370.
35. Lehtonen, E., Lento, V. P., Paasivuo, R. and Virtanen, 1, (1983). Parietal and visceral endoderm differ in their expression of intermediate filaments. EMRO J. 2, 1023-1028.
36. Li, Z. E., Colucci-Guyon, E., Pincon-Raymond, M., Mericskay, M., Pournin, S., Paulin, D. and Babinet, C. (1996). Cardiac lesions and skeletal myopathy in mice lacking desmin. Dev. Biol. 175, 362-366.
37. Lin, J. J.-C. and Feramisco, J. R. (1981). Disruption of the in vivo distribution of the intermediate filaments in fibroblasts through the microinjection of a specific monoclonal antibody. Cell 24, 185-193.
38. Lotz, M. M., Burdsal, C. A., Ericksen, H. P. and McClay, D. R. (1989). Cell adhesion to fibronectin and tenascin: quantitative measurements of initial binding and subsequent strengthening response. J. Cell Biol. 109, 1795-1805.
39. Maniotis, A. J., Chen, C. S. and Ingber, D. E. (1997) Control of cell and nuclear shape by mechanical stresses transmitted from integrins to the nucleus over direct cytoskeletal interconnections. Proc. Nat. Acad. Sci. USA 94, 849-854.
40. Milner, D. J., Weitzer, G., Tran, U., Bradley, A. and Capetanaki, Y. (1996). Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J. Cell Biol. 134, 1255-1270.
41. Monteiro, M. J., Hoffmann, P. N., Gearhart, J. D. and Cleveland, D. W. (1990). Expression of NF-L in both neuronal and nonneuronal cells of transgenic mice: Increased neurofilament density in axons without affecting caliber. J. Cell Biol. 111, 1543-1557.
42. Parry, D. A. D. and Steinert, P. M. (1995). Intermediate Filament Structure. Molecular Biology Intelligence Unit. R. G. Landis Co., Austin, Texas.
43. Schliwa, M. and Höner, B. (1993). Microtubules, centrosomes and intermediate filaments in directed cell movement. Trends Cell Biol. 3, 377-380.
44. Steinert, P. M., North, A. C. T. and Parry, D. A. D. (1994). Structural features of keratine intermediate filaments. J. Invest. Dermarol. 103, 19s-24s.
45. Stopak, D. and Harris, A. K. (1982). Connective tissue morphogenesis by libroblast traction. Dev. Biol. 90, 383-398.
46. Svitkina., T. M., Verkhovsky, A. B. and Borisy, G. G. (1996) Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton. J. Cell Biol. 135, 991-1007.
47. Thomas, K. R. and Capecchi, M. R. (1987). Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503-512.
48. Torpey, N., Wylie, C. C. and Heasman, J. (1992). Function of maternal eytokeratin in Xenopus development. Nature 357, 413-415.
49. Venetianer, A., Schiller, D. L., Magin, T. and Franke, W. W. (1983). Cessation of cytokeratin expression in a rat hepatoma cell line lacking differentiated functions. Nature 305, 730-733.
50. Wang, N., Butler, J. P. and Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127.
51. Wang, N. and Ingber, D. E. (1994). Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66, 2181-2189.
52. Yang, Y., Dowling, J., Yu, Q.-C., Kouklis, P., Cleveland, D. W. and Fuchs, E. (1996). An essential cytoskeletal linker protein connecting actin microtilaments to intermediate filaments. Cell 86, 655-665.