Self-organization of keratin intermediate filaments into cross-linked networks

Journal of Cell Biology

Volumn 186, Issue 3, 2009, Pages 409-421

  Lee, Chang Hun ^a   Coulombe, Pierre A ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 14; CYTOKERATIN 5; HETERODIMER; INTERMEDIATE FILAMENT PROTEIN; KERATIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL STRAIN BHK; CONTROLLED STUDY; INTERMEDIATE FILAMENT; MECHANICAL STRESS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; FIBROBLASTS; HUMANS; INTERMEDIATE FILAMENTS; KERATIN-14; KERATIN-5; KERATINOCYTES; MICE; SEQUENCE HOMOLOGY;

EID: 68549090936     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200810196     Document Type: Article

References (61)

1. Aebi, U., W.E. Fowler, P. Rew, and T.T. Sun. 1983. The fibrillar substructure of keratin filaments unraveled. J. Cell Biol. 97:1131-1143.
2. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter. 2002. Molecular Biology of the Cell, 4th edition. Garland Science, New York. 1,616 pp.
3. Andra, K., H. Lassmann, R. Bittner, S. Shorny, R. Fassler, F. Propst, and G. Wiche. 1997. Targeted inactivation of plectin reveals essential function in maintaining the integrity of skin, muscle, and heart cytoarchitecture. Genes Dev. 11:3143-3156.
4. Behne, M.J., J.W. Meyer, K.M. Hanson, N.P. Barry, S. Murata, D. Crumrine, R.W. Clegg, E. Gratton, W.M. Holleran, P.M. Elias, and T.M. Mauro. 2002. NHE1 regulates the stratum corneum permeability barrier homeostasis. Microenvironment acidification assessed with fluorescence lifetime imaging. J. Biol. Chem. 277:47399-47406.
5. Beil, M., A. Micoulet, G. von Wichert, S. Paschke, P. Walther, M.B. Omary, P.P. Van Veldhoven, U. Gern, E. Wolff-Hieber, J. Eggermann, et al. 2003. Sphingosylphosphorylcholine regulates keratin network architecture and visco-elastic properties of human cancer cells. Nat. Cell Biol. 5:803-811.
6. Bernot, K.M., C.H. Lee, and P.A. Coulombe. 2005. A small surface hydrophobic stripe in the coiled-coil domain of type I keratins mediates tetramer stability. J. Cell Biol. 168:965-974.
7. Bolte, S., and F.P. Cordelieres. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224:213-232.
8. Bousquet, O., L. Ma, S. Yamada, C. Gu, T. Idei, K. Takahashi, D. Wirtz, and P.A. Coulombe. 2001. The nonhelical tail domain of keratin 14 promotes filament bundling and enhances the mechanical properties of keratin intermediate filaments in vitro. J. Cell Biol. 155:747-754.
9. Coulombe, P.A. 2002. A new fold on an old story: attachment of intermediate filaments to desmosomes. Nat. Struct. Biol. 9:560-562.
10. Coulombe, P.A., and E. Fuchs. 1990. Elucidating the early stages of keratin filament assembly. J. Cell Biol. 111:153-169.
11. Coulombe, P.A., O. Bousquet, L. Ma, S. Yamada, and D. Wirtz. 2000. The 'ins' and 'outs' of intermediate filament organization. Trends Cell Biol. 10:420-428.
12. Crimmins, D.L., D.W. McCourt, R.S. Thoma, M.G. Scott, K. Macke, and B.D. Schwartz. 1990. In situ chemical cleavage of proteins immobilized to glass-fiber and polyvinylidenedifluoride membranes: cleavage at tryptophan residues with 2-(2'-nitrophenylsulfenyl)-3-methyl-3′-bromoindolenine to obtain internal amino acid sequence. Anal. Biochem. 187:27-38.
13. Edmondson, D.G., and S.Y. Roth. 2001. Identification of protein interactions by far Western analysis. Curr. Protoc. Mol. Biol. Chapter 20:Unit 20.6.
14. Eichner, R., T.T. Sun, and U. Aebi. 1986. The role of keratin subfamilies and keratin pairs in the formation of human epidermal intermediate filaments. J. Cell Biol. 102:1767-1777.
15. Flitney, E.W., E.R. Kuczmarski, S.A. Adam, and R.D. Goldman. 2009. Insights into the mechanical properties of epithelial cells: the effects of shear stress on the assembly and remodeling of keratin intermediate filaments. FASEB J. 23:2110-2119.
16. Franke, W.W. 1987. Homology of a conserved sequence in the tail domain of intermediate filament proteins with the loop region of calcium binding proteins. Cell Biol. Int. Rep. 11:831.
17. Fuchs, E., and D.W. Cleveland. 1998. A structural scaffolding of intermediate filaments in health and disease. Science. 279:514-519.
18. Fudge, D., D. Russell, D. Beriault, W. Moore, E.B. Lane, and A.W. Vogl. 2008. The intermediate filament network in cultured human keratinocytes is remarkably extensible and resilient. PLoS ONE. 3:e2327.
19. Gardner, A.M., R.R. Vaillancourt, C.A. Lange-Carter, and G.L. Johnson. 1994. MEK-1 phosphorylation by MEK kinase, Raf, and mitogen-activated protein kinase: analysis of phosphopeptides and regulation of activity. Mol. Biol. Cell. 5:193-201.
20. Geisbrecht, B.V., S. Bouyain, and M. Pop. 2006. An optimized system for expression and purification of secreted bacterial proteins. Protein Expr. Purif. 46:23-32.
21. Green, K.J., M. Bohringer, T. Gocken, and J.C. Jones. 2005. Intermediate filament associated proteins. Adv. Protein Chem. 70:143-202.
22. Gross, S.R., and T.G. Kinzy. 2005. Translation elongation factor 1 A is essential for regulation of the actin cytoskeleton and cell morphology. Nat. Struct. Mol. Biol. 12:772-778.
23. Gu, L.H., and P.A. Coulombe. 2007. Keratin function in skin epithelia: a broadening palette with surprising shades. Curr. Opin. Cell Biol. 19:13-23.
24. Heckman, K.L., and L.R. Pease. 2007. Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protocols. 2:924-932.
25. Hofmann, I., H. Herrmann, and W.W. Franke. 1991. Assembly and structure of calcium-induced thick vimentin filaments. Eur. J. Cell Biol. 56:328-341.
26. Hutton, E., R.D. Paladini, Q.C. Yu, M.-Y. Yen, P.A. Coulombe, and E. Fuchs. 1998. Functional differences between keratins of stratified and simple epithelia. J. Cell Biol. 143:487-499.
27. Izawa, I., and M. Inagaki. 2006. Regulatory mechanisms and functions of intermediate filaments: a study using site- and phosphorylation state-specific antibodies. Cancer Sci. 97:167-174.
28. Janmey, P.A. 1991. Mechanical properties of cytoskeletal polymers. Curr. Opin. Cell Biol. 3:4-11.
29. Karakozova, M., M. Kozak, C.C. Wong, A.O. Bailey, J.R. Yates III, A. Mogilner, H. Zebroski, and A. Kashina. 2006. Arginylation of beta-actin regulates actin cytoskeleton and cell motility. Science. 313:192-196.
30. Kerns, M.L., D. DePianto, A.T. Dinkova-Kostova, P. Talalay, and P.A. Coulombe. 2007. Reprogramming of keratin biosynthesis by sulforaphane restores skin integrity in epidermolysis bullosa simplex. Proc. Natl. Acad. Sci. USA. 104:14460-14465.
31. Kim, S., and P.A. Coulombe. 2007. Intermediate filament scaffolds fulfill mechanical, organizational, and signaling functions in the cytoplasm. Genes Dev. 21:1581-1597.
32. Kotadiya, P., B.K. McMichael, and B.S. Lee. 2008. High molecular weight tropomyosins regulate osteoclast cytoskeletal morphology. Bone. 43:951-960.
33. Kreplak, L., and D. Fudge. 2007. Biomechanical properties of intermediate filaments: from tissues to single filaments and back. Bioessays. 29:26-35.
34. Larouche, D., X. Tong, J. Fradette, P.A. Coulombe, and L. Germain. 2008. Vibrissa hair bulge houses two populations of skin epithelial stem cells distinct by their keratin profile. FASEB J. 22:1404-1415.
35. Ma, L., S. Yamada, D. Wirtz, and P.A. Coulombe. 2001. A 'hot-spot' mutation alters the mechanical properties of keratin filament networks. Nat. Cell Biol. 3:503-506.
36. MacLean-Fletcher, S.D., and T.D. Pollard. 1980. Viscometric analysis of the gelation of Acanthamoeba extracts and purification of two gelation factors. J. Cell Biol. 85:414-428.
37. Omary, M.B., P.A. Coulombe, and W.H.I. McLean. 2004. Intermediate filament proteins and their associated diseases. N. Engl. J. Med. 351:2087-2100.
38. Omary, M.B., N.O. Ku, G.Z. Tao, D.M. Toivola, and J. Liao. 2006. "Heads and tails" of intermediate filament phosphorylation: Multiple sites and functional insights. Trends Biochem. Sci. 31:383-394.
39. Osmanagic-Myers, S., M. Gregor, G. Walko, G. Burgstaller, S. Reipert, and G. Wiche. 2006. Plectin-controlled keratin cytoarchitecture affects MAP kinases involved in cellular stress response and migration. J. Cell Biol. 174:557-568.
40. Paladini, R.D., and P.A. Coulombe. 1999. The functional diversity of epidermal keratins revealed by the partial rescue of the keratin 14 null phenotype by keratin 16. J. Cell Biol. 146:1185-1201.
41. Paladini, R.D., K. Takahashi, T.M. Gant, and P.A. Coulombe. 1995. cDNA cloning and bacterial expression of the human type I keratin 16. Biochem. Biophys. Res. Commun. 215:517-523.
42. Paladini, R.D., K. Takahashi, N.S. Bravo, and P.A. Coulombe. 1996. Onset of re-epithelialization after skin injury correlates with a reorganization of keratin filaments in wound edge keratinocytes: defining a potential role for keratin 16. J. Cell Biol. 132:381-397.
43. Perng, M.D., L. Cairns, P. van den Jssel, A. Prescott, A.M. Hutcheson, and R.A. Quinlan. 1999. Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J. Cell Sci. 112:2099-2112.
44. Peters, B., J. Kirfel, H. Bussow, M. Vidal, and T.M. Magin. 2001. Complete cytolysis and neonatal lethality in keratin 5 knockout mice reveal its fundamental role in skin integrity and in epidermolysis bullosa simplex. Mol. Biol. Cell. 12:1775-1789.
45. Pollard, T.D., and J.A. Cooper. 1982. Methods to characterize actin filament networks. Methods Enzymol. 85 Pt B:211-233.
46. Sonnenberg, A., and R.K. Liem. 2007. Plakins in development and disease. Exp. Cell Res. 313:2189-2203.
47. Spazierer, D., J. Raberger, K. Gross, P. Fuchs, and G. Wiche. 2008. Stress-induced recruitment of epiplakin to keratin networks increases their resistance to hyperphosphorylation-induced disruption. J. Cell Sci. 121:825-833.
48. Steinbock, F.A., B. Nikolic, P.A. Coulombe, E. Fuchs, P. Traub, and G. Wiche. 2000. Dose-dependent linkage, assembly inhibition and disassembly of vimentin and cytokeratin 5/14 filaments through plectin's intermediate filament-binding domain. J. Cell Sci. 113:483-491.
49. Strelkov, S.V., H. Herrmann, N. Geisler, T. Wedig, R. Zimbelmann, U. Aebi, and P. Burkhard. 2002. Conserved segments 1A and 2B of the intermediate filament dimer: their atomic structures and role in filament assembly. EMBO J. 21:1255-1266.
50. Strickland, J.E., D.A. Greenhalgh, A. Koceva-Chyla, H. Hennings, C. Restrepo, M. Balaschak, and S.H. Yuspa. 1988. Development of murine epidermal cell lines which contain an activated rasHa oncogene and form papillomas in skin grafts on athymic nude mouse hosts. Cancer Res. 48:165-169.
51. Studier, F.W., A.H. Rosenberg, J.J. Dunn, and J.W. Dubendorff. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60-89.
52. Szeverenyi, I., A.J. Cassidy, C.W. Chung, B.T. Lee, J.E. Common, S.C. Ogg, H. Chen, S.Y. Sim, W.L. Goh, K.W. Ng, et al. 2008. The Human Intermediate Filament Database: comprehensive information on a gene family involved in many human diseases. Hum. Mutat. 29:351-360.
53. Toivola, D.M., Q. Zhou, L.S. English, and M.B. Omary. 2002. Type II keratins are phosphorylated on a unique motif during stress and mitosis in tissues and cultured cells. Mol. Biol. Cell. 13:1857-1870.
54. Wang, W., H. Sumiyoshi, H. Yoshioka, and S. Fujiwara. 2006. Interactions between epiplakin and intermediate filaments. J. Dermatol. 33:518-527.
55. Warrens, A.N., M.D. Jones, and R.I. Lechler. 1997. Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest. Gene. 186:29-35.
56. Wawersik, M., R.D. Paladini, E. Noensie, and P.A. Coulombe. 1997. A proline residue in the alpha-helical rod domain of type I keratin 16 destabilizes keratin heterotetramers and influences incorporation into filaments. J. Biol. Chem. 272:32557-32565.
57. Wilhelmsen, K., S.H. Litjens, I. Kuikman, N. Tshimbalanga, H. Janssen, I. van den Bout, K. Raymond, and A. Sonnenberg. 2005. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J. Cell Biol. 171:799-810.
58. Wilson, A.K., P.A. Coulombe, and E. Fuchs. 1992. The roles of K5 and K14 head, tail, and R/K L L E G E domains in keratin filament assembly in vitro. J. Cell Biol. 119:401-414.
59. Wong, P., E. Colucci-Guyon, K. Takahashi, C. Gu, C. Babinet, and P.A. Coulombe. 2000. Introducing a null mutation in the mouse K6α and K6β genes reveals their essential structural role in the oral mucosa. J. Cell Biol. 150:921-928.
60. Yamada, S., D. Wirtz, and S.C. Kuo. 2000. Mechanics of living cells measured by laser tracking microrheology. Biophys. J. 78:1736-1747.
61. Yamada, S., D. Wirtz, and P.A. Coulombe. 2002. Pairwise assembly determines the intrinsic potential for self- organization and mechanical properties of keratin filaments. Mol. Biol. Cell. 13:382-391.