Effects of keratin phosphorylation on the mechanical properties of keratin filaments in living cells

FASEB Journal

Volumn 27, Issue 4, 2013, Pages 1322-1329

  Fois, Giorgio ^a   Weimer, Michael ^a   Busch, Tobias ^b   Felder, Erika T ^a   Oswald, Franz ^b   Wichert, Götz Von ^b   Seufferlein, Thomas ^b   Dietl, Paul ^a   Felder, Edward ^a  

^a UNIVERSITY OF ULM   (Germany)

^b Department of Internal Medicine I   (Germany)

Author keywords

Cytoarchitecture; Cytoskeleton; Mechanical stress; Tension

Indexed keywords

CYTOKERATIN 18; CYTOKERATIN 8; PHOSPHOPROTEIN; SERINE;

ACTIN MYOSIN INTERACTION; ANTIBODY LABELING; ARTICLE; CANCER CELL; CELLULAR PARAMETERS; CONTROLLED STUDY; DEPHOSPHORYLATION; HUMAN; HUMAN CELL; MECHANICS; MUTANT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SQUAMOUS CELL CARCINOMA; WILD TYPE;

ACTINS; CELL SURVIVAL; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; INTERMEDIATE FILAMENTS; KERATINS; PHOSPHORYLATION; SERINE;

EID: 84875726086     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-215632     Document Type: Article

References (36)

1. Crick, F. H. (1952) Is alpha-keratin a coiled coil? Nature 170, 882-883.
2. Fudge, D. S., Gardner, K. H., Forsyth, V. T., Riekel, C., and Gosline, J. M. (2003) The mechanical properties of hydrated intermediate filaments: insights from hagfish slime threads. Biophys. J. 85, 2015-2027.
3. Kreplak, L., and Fudge, D. (2007) Biomechanical properties of intermediate filaments: from tissues to single filaments and back. Bioessays 29, 26-35.
4. Felder, E., Siebenbrunner, M., Busch, T., Fois, G., Miklavc, P., Walther, P., and Dietl, P. (2008) Mechanical strain of alveolar type II cells in culture: changes in the transcellular cytokeratin network and adaptations. Am. J. Physiol. Lung Cell Mol. Physiol. 295, L849-L857.
5. Fudge, D., Russell, D., Beriault, D., Moore, W., Lane, E. B., and Vogl, A. W. (2008) The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient. PLoS ONE 3, e2327.
6. Russell, D., Andrews, P. D., James, J., and Lane, E. B. (2004) Mechanical stress induces profound remodelling of keratin filaments and cell junctions in epidermolysis bullosa simplex keratinocytes. J. Cell Sci. 117, 5233-5243.
7. Green, K. J., Bohringer, M., Gocken, T., and Jones, J. C. (2005) Intermediate filament associated proteins. Adv. Protein Chem. 70, 143-202.
8. Omary, M. B., Ku, N. O., Tao, G. Z., Toivola, D. M., and Liao, J. (2006) "Heads and tails" of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem. Sci. 31, 383-394.
9. Beil, M., Micoulet, A., von, W. G., Paschke, S., Walther, P., Omary, M. B., Van Veldhoven, P. P., Gern, U., Wolff-Hieber, E., Eggermann, J., Waltenberger, J., Adler, G., Spatz, J., and Seufferlein, T. (2003) Sphingosylphosphorylcholine regulates keratin network architecture and visco-elastic properties of human cancer cells. Nat. Cell Biol. 5, 803-811.
10. Ku, N. O., Liao, J., and Omary, M. B. (1998) Phosphorylation of human keratin 18 serine 33 regulates binding to 14-3-3 proteins. EMBO J. 17, 1892-1906.
11. Omary, M. B., Ku, N. O., Liao, J., and Price, D. (1998) Keratin modifications and solubility properties in epithelial cells and in vitro. Subcell. Biochem. 31, 105-140.
12. Ridge, K. M., Linz, L., Flitney, F. W., Kuczmarski, E. R., Chou, Y. H., Omary, M. B., Sznajder, J. I., and Goldman, R. D. (2005) Keratin 8 phosphorylation by protein kinase C delta regulates shear stress-mediated disassembly of keratin intermediate filaments in alveolar epithelial cells. J. Biol. Chem. 280, 30400-30405.
13. Liao, J., and Omary, M. B. (1996) 14-3-3 proteins associate with phosphorylated simple epithelial keratins during cell cycle progression and act as a solubility cofactor. J. Cell Biol. 133, 345-357.
14. Strnad, P., Windoffer, R., and Leube, R. E. (2001) In vivo detection of cytokeratin filament network breakdown in cells treated with the phosphatase inhibitor okadaic acid. Cell Tissue Res. 306, 277-293.
15. Strnad, P., Windoffer, R., and Leube, R. E. (2002) Induction of rapid and reversible cytokeratin filament network remodeling by inhibition of tyrosine phosphatases. J. Cell Sci. 115, 4133-4148.
16. Gerstmair, A., Fois, G., Innerbichler, S., Dietl, P., and Felder, E. (2009) A device for simultaneous live cell imaging during uni-axial mechanical strain or compression. J. Appl. Physiol. 107, 613-620.
17. Busch, T., Armacki, M., Eiseler, T., Joodi, G., Temme, C., Jansen, J., von Wichert, G. von Wichert, Omary, M. B., Spatz, J., and Seufferlein, T. (2012) Keratin 8 phosphorylation regulates keratin reorganization and migration of epithelial tumor cells. J. Cell Sci. 125, 2148-2159.
18. Wiedenmann, J., Ivanchenko, S., Oswald, F., Schmitt, F., Rocker, C., Salih, A., Spindler, K. D., and Nienhaus, G. U. (2004) EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc. Natl. Acad. Sci. U. S. A. 101, 15905-15910.
19. Fuchs, J., Bohme, S., Oswald, F., Hedde, P. N., Krause, M., Wiedenmann, J., and Nienhaus, G. U. (2010) A photoactivatable marker protein for pulse-chase imaging with superresolution. Nat. Methods 7, 627-630.
20. Kredel, S., Oswald, F., Nienhaus, K., Deuschle, K., Rocker, C., Wolff, M., Heilker, R., Nienhaus, G. U., and Wiedenmann, J. (2009) mRuby, a bright monomeric red fluorescent protein for labeling of subcellular structures. PLoS ONE 4, e4391.
21. Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z., Sixt, M., and Wedlich-Soldner, R. (2008) Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607.
22. Miklavc, P., Hecht, E., Hobi, N., Wittekindt, O. H., Dietl, P., Kranz, C., and Frick, M. (2012) Actin coating and compression of fused secretory vesicles are essential for surfactant secretion; a role for Rho, formins and myosin II. J. Cell Sci. 125, 2765-2774.
23. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. (2004) Image processing with ImageJ. Biophotonics. Int. 11, 36-42.
24. Sauk, J. J., Krumweide, M., Cocking-Johnson, D., and White, J. G. (1984) Reconstitution of cytokeratin filaments in vitro: further evidence for the role of nonhelical peptides in filament assembly. J. Cell Biol. 99, 1590-1597.
25. Kreplak, L., Bar, H., Leterrier, J. F., Herrmann, H., and Aebi, U. (2005) Exploring the mechanical behavior of single intermediate filaments. J. Mol. Biol. 354, 569-577.
26. Guzman, C., Jeney, S., Kreplak, L., Kasas, S., Kulik, A. J., Aebi, U., and Forro, L. (2006) Exploring the mechanical properties of single vimentin intermediate filaments by atomic force microscopy. J. Mol. Biol. 360, 623-630.
27. Magin, T. M., Vijayaraj, P., and Leube, R. E. (2007) Structural and regulatory functions of keratins. Exp. Cell Res. 313, 2021- 2032.
28. Sivaramakrishnan, S., DeGiulio, J. V., Lorand, L., Goldman, R. D., and Ridge, K. M. (2008) Micromechanical properties of keratin intermediate filament networks. Proc. Natl. Acad. Sci. U. S. A. 105, 889-894.
29. Qin, Z., Buehler, M. J., and Kreplak, L. (2010) A multi-scale approach to understand the mechanobiology of intermediate filaments. J. Biomech. 43, 15-22.
30. Kolsch, A., Windoffer, R., Wurflinger, T., Aach, T., and Leube, R. E. (2010) The keratin-filament cycle of assembly and disassembly. J. Cell Sci. 123, 2266-2272.
31. Woll, S., Windoffer, R., and Leube, R. E. (2005) Dissection of keratin dynamics: different contributions of the actin and microtubule systems. Eur. J. Cell Biol. 84, 311-328.
32. Harada, H., Mitsuyasu, T., Seta, Y., Maruoka, Y., Toyoshima, K., and Yasumoto, S. (1998) Overexpression of bcl-2 protein inhibits terminal differentiation of oral keratinocytes in vitro. J. Oral Pathol. Med. 27, 11-17.
33. Moll, R., Divo, M., and Langbein, L. (2008) The human keratins: biology and pathology. Histochem. Cell Biol. 129, 705- 733.
34. Fuchs, E., and Cleveland, D. W. (1998) A structural scaffolding of intermediate filaments in health and disease. Science 279, 514-519.
35. Kim, S., and Coulombe, P. A. (2007) Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 21, 1581-1597.
36. Sen-Chowdhry, S., Syrris, P., and McKenna, W. J. (2005) Genetics of right ventricular cardiomyopathy. J. Cardiovasc. Electrophysiol. 16, 927-935.