Unique amino acid signatures that are evolutionarily conserved distinguish simple-type, epidermal and hair keratins

Journal of Cell Science

Volumn 124, Issue 24, 2011, Pages 4221-4232

  Strnad, Pavel ^a   Usachov, Valentyn ^a   Debes, Cedric ^b   Grä, Frauke ^b   Parry, David A D ^c   Omary Bishr, M ^d  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b HEIDELBERG INSTITUTE FOR THEORETICAL STUDIES   (Germany)

^c MASSEY UNIVERSITY   (New Zealand)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Amino acids; Glandular epithelium; Keratins; Skin

Indexed keywords

ALANINE; AMINO ACID; CYSTEINE; CYTOKERATIN 1; CYTOKERATIN 10; CYTOKERATIN 14; CYTOKERATIN 18; CYTOKERATIN 19; CYTOKERATIN 2; CYTOKERATIN 20; CYTOKERATIN 31; CYTOKERATIN 35; CYTOKERATIN 5; CYTOKERATIN 7; CYTOKERATIN 8; CYTOKERATIN 81; CYTOKERATIN 85; CYTOKERATIN 86; GLYCINE; HISTIDINE; KERATIN; PHENYLALANINE; PROLINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; EPIDERMIS; HAIR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SOLUBILITY;

AMINO ACIDS; ANIMALS; CATTLE; EPIDERMIS; EVOLUTION, MOLECULAR; HUMANS; KERATINS; KERATINS, HAIR-SPECIFIC; MICE; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, PROTEIN;

EID: 84856826693     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.089516     Document Type: Article

References (70)

1. Albers, K. M., Davis, F. E., Perrone, T. N., Lee, E. Y., Liu, Y. and Vore, M.(1995). Expression of an epidermal keratin protein in liver of transgenic mice causes structural and functional abnormalities. J. Cell Biol. 128, 157-169.
2. Alberts, A. J., Lewis, J., Raff, M., Roberts, K. and Walter, P.(2008). The cytoskeleton. In Molecular Biology of the Cell (ed. M. Anderson and S. Granum), pp. 965-1052. New York: Garland Science.
3. Berg, J. M., Tymoczko, J. L. and Stryer, L.(2007). Protein composition and function. In Biochemistry (ed. P. Zimmerman), pp. 25-64, New York: W. H. Freeman.
4. Blessing, M., Nanney, L. B., King, L. E., Jones, C. M. and Hogan, B. L.(1993). Transgenic mice as a model to study the role of TGF-beta-related molecules in hair follicles. Genes Dev. 7, 204-215.
5. Chen, J., Cheng, X., Merched-Sauvage, M., Caulin, C., Roop, D. R. and Koch, P. J.(2006). An unexpected role for keratin 10 end domains in susceptibility to skin cancer. J. Cell Sci. 119, 5067-5076.
6. Chipev, C. C., Yang, J. M., DiGiovanna, J. J., Steinert, P. M., Marekov, L., Compton, J. G. and Bale, S. J.(1994). Preferential sites in keratin 10 that are mutated in epidermolytic hyperkeratosis. Am. J. Hum. Genet. 54, 179-190.
7. Conway, J. F. and Parry, D. A. D.(1990). Structural features in the heptad substructures and longer range repeats of two-stranded alpha-fibrous proteins. Int. J. Biol. Macromol. 12, 328-334.
8. Coulombe, P. A. and Omary, M. B.(2002). 'Hard' and 'soft' principles defining the structure, function and regulation of keratin intermediate filaments. Curr. Opin. Cell Biol. 14, 110-122.
9. Coulombe, P. A., Kerns, M. L. and Fuchs, E.(2009). Epidermolysis bullosa simplex: a paradigm for disorders of tissue fragility. J. Clin. Invest. 119, 1784-1793.
10. Crewther, W. G., Dowling, L. M., Parry, D. A. D. and Steinert, P. M.(1983). The structure of Intermediate Filaments. Int. J. Biol. Macromol. 5, 267-274.
11. Eriksson, J. E., Thomas, T., Grin, B., Helfand, B., Mendez, M., Pallari, H.-M. and Goldman, R. D.(2009). Introducing intermediate filaments: from discovery to disease. J. Clin. Invest. 119, 1763-1771.
12. Fraser, R. D. B. and Parry, D. A. D.(2007). Structural changes in the trichocyte intermediate filaments accompanying the transition from the reduced to the oxidized form. J. Struct. Biol. 159, 36-45.
13. Fraser, R. D. B., MacRae, T. P., Sparrow, L. G. and Parry, D. A. D.(1988). Disulphide bonding in alpha keratin. Int. J. Biol. Macromol. 10, 106-112.
14. Geisler, N., Kaufmann, E. and Weber, K.(1982). Proteinchemical characterization of three structurally distinct domains along the protofilament unit of desmin 10 nm filaments. Cell 30, 277-286.
15. Gu, L. H. and Coulombe, P. A.(2007). Keratin function in skin epithelia: a broadening palette with surprising shades. Curr. Opin. Cell. Biol. 19, 13-23.
16. Hatzfeld, M. and Franke, W. W.(1985). Pair formation and promiscuity of cytokeratins: formation in vitro of heterotypic complexes and intermediate-sized filaments by homologous and heterologous recombinations of purified polypeptides. J. Cell Biol. 101, 1826-1841.
17. Hatzfeld, M. and Weber, K.(1990). The coiled-coil of in vitro assembled keratin filaments is a heterodimer of type I and II keratins: Use of site-specific mutagenesis and recombinant protein expression. J. Cell Biol. 110, 1199-1210.
18. Herrling, J. and Sparrow, L. G.(1991). Interaction of intermediate filament proteins from wool. Int. J. Biol. Macromol. 13, 115-119.
19. Herrmann, H., Wedig, T., Porter, R. M., Lane, E. B. and Aebi, U.(2002). Characterization of early assembly intermediates of recombinant human keratins. J. Struct. Biol. 137, 82-96.
20. Herrmann, H., Strelkov, S. V., Burkhard, P. and Aebi, U.(2009). Intermediate filaments: primary determinants of cell architecture and plasticity. J. Clin. Invest. 119, 1772-1783.
21. Hesse, M., Franz, T., Tamai, Y., Taketo, M. M., Magin, T. M.(2000). Targeted deletion of keratins 18 and 19 leads to trophoblast fragility and early embryonic lethality. EMBO J. 19, 5060-5070.
22. Hesse, M., Watson, E. D., Schwaluk, T. and Magin, T. M.(2005). Rescue of keratin 18/19 doubly deficient mice using aggregation with tetraploid embryos. Eur. J. Cell Biol. 84, 355-361.
23. Hesse, M., Grund, C., Herrmann, H., Bröhl, D., Franz, T., Omary, M. B. and Magin, T. M.(2007). A mutation of keratin 18 within the coil 1A consensus motif causes widespread keratin aggregation but cell type-restricted lethality in mice. Exp. Cell Res. 313, 3127-3140.
24. Hutton, E., Paladini, R. D., Yu, Q. C., Yen, M.-Y., Coulombe, P. A. and Fuchs, E.(1998). Functional differences between keratins of stratified and simple epithelia. J. Cell Biol. 143, 1-13.
25. Hyder, C. L., Pallari, H. M., Kochin, V. and Eriksson, J. E.(2008). Providing cellular signposts-post-translational modifications of intermediate filaments. FEBS Lett. 582, 2140-2148.
26. Klinge, E. M., Sylvestre, Y. R., Freedberg, I. M. and Blumenberg, M.(1987). Evolution of keratin genes: different protein domains evolve by different pathways. J. Mol. Evol. 24, 319-329.
27. Knapp, A. C. and Franke, W. W.(1989). Spontaneous losses of control of cytokeratin gene expression in transformed, non-epithelial human cells occurring at different levels of regulation. Cell 59, 67-79.
28. Ku, N. O. and Omary, M. B.(2006). A disease- and phosphorylation-related nonmechanical function for keratin 8. J. Cell Biol. 174, 115-125.
29. Ku, N. O., Zhou, X., Toivola, D. M. and Omary, M. B.(1999). The cytoskeleton of digestive epithelia in health and disease. Am. J. Physiol. Gastrointest. Liver Physiol. 277, G1108-G1137.
30. Ku, N. O., Gish, R., Wright, T. L. and Omary, M. B.(2001). Keratin 8 mutations in patients with cryptogenic liver disease. N. Engl. J. Med. 344, 1580-1587.
31. Ku, N. O., Lim, J. K., Krams, S. M., Esquivel, C. O., Keeffe, E. B., Wright, T. L., Parry, D. A. D. and Omary, M. B.(2005). Keratins as susceptibility genes for endstage liver disease. Gastroenterology 129, 885-893.
32. Ku, N. O., Strnad, P., Zhong, B. H., Tao, G. Z. and Omary, M. B.(2007). Keratins let liver live: mutations predispose to liver disease and crosslinking generates Mallory-Denk bodies. Hepatology 46, 1639-1649.
33. Langbein, L., Yoshida, H., Praetzel-Wunder, S., Parry, D. A. and Schweizer, J.(2010). The keratins of the human beard hair medulla: the riddle in the middle. J. Invest. Dermatol. 130, 55-73.
34. Lee, C. H. and Coulombe, P. A.(2009). Self-organization of keratin intermediate filaments into cross-linked networks. J. Cell Biol. 186, 409-421.
35. Ma, L., Yamada, S., Wirtz, D. and Coulombe, P. A.(2001). A 'hot-spot' mutation alters the mechanical properties of keratin filament networks. Nat. Cell Biol. 3, 503-506.
36. Mack, J. W., Torchia, D. A. and Steinert, P. M.(1988). Solid-state NMR studies of the dynamics and structure of mouse keratin intermediate filaments. Biochemistry 27, 5418-5426.
37. Mohrenweiser, H.(1994). International Commission for Protection Against Environmental Mutagens and Carcinogens. Working paper no. 5. Impact of the molecular spectrum of mutational lesions on estimates of germinal gene-mutation rates. Mutat. Res. 304, 119-137.
38. Moll, R., Franke, W. W., Schiller, D. L., Geiger, B. and Krepler, R.(1982). The catalog of human cytokeratins - patterns of expression in normal epithelia, tumors and cultured cells. Cell 31, 11-24.
39. Moll, R., Divo, M. and Langbein, L.(2008). The human keratins: biology and pathology. Histochem. Cell Biol. 129, 705-733.
40. Navsaria, H. A., Swensson, O., Ratnavel, R. C., Shamsher, M., McLean, W. H., Lane, E. B., Griffiths, D., Eady, R. A. and Leigh, I. M.(1995). Ultrastructural changes resulting from keratin-9 gene mutations in two families with epidermolytic palmoplantar keratoderma. J. Invest. Dermatol. 104, 425-429.
41. 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.
42. Omary, M. B., Ku, N. O., Tao, G. Z., Toivola, D. M. and Liao, J.(2006). Heads-andtails of intermediate filament phosphorylation: multiple sites and functional insights. Trends Biochem. Sci. 31, 383-394.
43. Omary, M. B., Ku, N. O., Strnad, P. and Hanada, S.(2009). Toward unraveling the complexity of simple epithelial keratins in health and disease. J. Clin. Invest. 119, 1794-1805.
44. Owens, D. W. and Lane, E. B.(2004). Keratin mutations and intestinal pathology. J. Pathol. 204, 377-385.
45. Paladini, R. D. and Coulombe, P. A.(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.
46. Pang, Y. Y., Schermer, A., Yu, J. and Sun, T. T.(1993). Suprabasal change and subsequent formation of disulfide-stabilized homo- and hetero-dimers of keratins during esophageal epithelial differentiation. J. Cell Sci. 104, 727-740.
47. Parry, D. A. D.(2005). Microdissection of the sequence and structure of intermediate filament chains. Adv. Protein Chem. 70, 113-142.
48. Parry, D. A. D. and Fraser, R. D. B.(1985). Intermediate filament structure. 1. Analysis of IF protein sequence data. Int. J. Biol. Macromol. 7, 203-213.
49. Parry, D. A. D. and Steinert, P. M.(1995). Intermediate Filament Structure, pp. 1-183. Heidelberg: Springer-Verlag.
50. Parry, D. A. D. and North, A. C. T.(1998). Hard a-keratin intermediate filament chains: substructure of the N- and C-terminal domains and the predicted structure and function of the C-Terminal domains of Type I and Type II chains. J. Struct. Biol. 122, 67-75.
51. Parry, D. A. D., Steven, A. C. and Steinert, P. M.(1985). The coiled-coil molecules of intermediate filaments consist of two parallel chains in exact axial register. Biochem. Biophys. Res. Commun. 127, 1012-1018.
52. Parry, D. A. D., Strelkov, S. V., Burkhard, P., Aebi, U. and Herrmann, H.(2007). Towards a molecular description of intermediate filament structure and assembly. Exp. Cell Res. 313, 2204-2216.
53. Parry, D. A. D., Fraser, R. D. B. and Squire, J. M.(2008). Fifty years of coiled-coils and α-helical bundles: a close relationship between sequence and structure. J. Struct. Biol. 163, 258-269.
54. Pfeifer, G. P.(2006). Mutagenesis at methylated CpG sequences. Curr. Top. Microbiol. Immunol. 301, 259-281.
55. Quinlan, R. A., Cohlberg, J. A., Schiller, D. L., Hatzfeld, M. and Franke, W. W.(1984). Heterotypic tetramer (A2D2) complexes of non-epidermal keratins isolated from cytoskeletons of rat hepatocytes and hepatoma cells. J. Mol. Biol. 178, 365-388.
56. Quinlan, R. A., Hatzfeld, M., Franke, W. W., Lustig, A., Schulthess, T. and Engel, J.(1986). Characterization of dimer subunits of intermediate filament proteins. J. Mol. Biol. 192, 337-349.
57. Schweizer, J., Langbein, L., Rogers, M. A. and Winter, H.(2007). Hair folliclespecific keratins and their diseases. Exp. Cell Res. 313, 2010-2020.
58. Smith, T. A. and Parry, D. A. D.(2007). Sequence analyses of Type I and Type II chains in human hair and epithelial keratin intermediate filaments: promiscuous obligate heterodimers. Type II template for molecule formation and a rationale for heterodimer formation. J. Struct. Biol. 158, 344-357.
59. Snider, N. T., Weerasinghe, S. V. W., Iniguez-Lluhi, J. A., Herrmann, H. and Omary, M. B.(2011). Keratin hypersumoylation alters filament dynamics and is a marker for human liver disease and keratin mutation. J. Biol. Chem. 286, 2273-2284.
60. Sommer, S. S.(1992). Assessing the underlying pattern of human germline mutations: lessons from the factor IX gene. FASEB J. 6, 2767-2774.
61. Steinert, P. M.(1990). The two-chain coiled-coil molecule of native epidermal keratin intermediate filaments is a Type I-Type II heterodimer. J. Biol. Chem. 265, 8766-8774.
62. Steinert, P. M., Parry, D. A. D., Idler, W.W., Johnson, L. D., Steven, A. C. and Roop, D. R.(1985). Amino acid sequences of mouse and human epidermal type II keratins of Mr 67.000 provide a systematic basis for the structural and functional diversity of the end domains of keratin intermediate filament subunits. J. Biol. Chem. 260, 7142-7149.
63. Steinert, P. M., Mack, J. W., Korge, B. P., Gan, S.-Q., Haynes, S. R. and Steven, A. C.(1991). Glycine loops in proteins: Their occurrence in certain intermediate filament chains, loricrins and single-stranded RNA binding proteins. Int. J. Biol. Macromol. 13, 130-139.
64. Strnad, P., Zhou, Q., Hanada, S., Lazzeroni, L. C., Zhong, B. H., So, P., Davern, T. J., Lee, W. M., Acute Liver Failure Study Group and Omary, M. B.(2010). Keratin variants predispose to acute liver failure and adverse outcome: race and ethnic associations. Gastroenterology 139, 828-835.
65. Sun, T.-T., Eichner, R., Cooper, D., Schermer, A., Nelson, W. G. and Weiss, R. A.(1984). In The Cancer Cell, Vol. 1 (ed. A. Levine, W. Topp, G. Van de Woude and J. Watson), pp. 169-176. New York: Cold Spring Harbor Laboratory Press.
66. Takahashi, K., Folmer, J. and Coulombe, P. A.(1994). Increased expression of keratin 16 causes anomalies in cytoarchitecture and keratinization in transgenic mouse skin. J. Cell Biol. 127, 505-520.
67. Tao, G. Z., Nakamichi, I., Ku, N.-O., Wang, J., Frolkis, M., Gong, X., Zhu, W., Pytela, R. and Omary, M. B.(2006). Bispecific and human disease-related antikeratin rabbit monoclonal antibodies. Exp. Cell Res. 312, 411-422.
68. Tao, G. Z., Strnad, P., Zhou, Q., Kamal, A., Zhang, L., Madani, N. D., Kugathasan, S., Brant, S. R., Cho, J. H., Omary, M. B. and Duerr, R. H.(2007). Analysis of keratin polypeptides 8 and 19 variants in inflammatory bowel disease. Clin. Gastroenterol. Hepatol. 5, 857-864.
69. Wawersik, M., Paladini, R. D., Noensie, E. and Coulombe, P. A.(1997). A proline residue in the alphα-helical rod domain of type I keratin 16 destabilizes keratin heterotetramers. J. Biol. Chem. 272, 32557-32565.
70. Zhang, Y.-Q. and Sarge, K. D.(2008). Sumoylation regulates lamin A function and is lost in lamin A mutants associated with familial cardiomyopathies. J. Cell Biol. 182, 35-39.