A small surface hydrophobic stripe in the coiled-coil domain of type I keratins mediates tetramer stability

Journal of Cell Biology

Volumn 168, Issue 6, 2005, Pages 965-974

  Bernot, Kelsie M ^a   Lee, Chang Hun ^a   Coulombe, Pierre A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 1; KERATIN; TETRAMER;

ARTICLE; CELL NUCLEUS; CYTOPLASM; EUKARYOTE; HUMAN; HYDROPHOBICITY; INTERMEDIATE FILAMENT; MOLECULAR MODEL; MOLECULAR STABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELLS, CULTURED; CHROMATOGRAPHY, ION EXCHANGE; CONSENSUS SEQUENCE; CROSS-LINKING REAGENTS; DIMERIZATION; ELECTROPHORESIS, AGAR GEL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; HUMANS; HYDROPHOBICITY; KERATINOCYTES; KERATINS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PRECIPITIN TESTS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EUKARYOTA;

EID: 15444365572     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200408116     Document Type: Article

References (58)

1. Aebi, U., M. Haner, J. Troncoso, R. Eichner, and A. Engel. 1988. Unifying principles in intermediate filament assembly. Protoplasma. 145:73-81.
2. Bernot, K.M., P.A. Coulombe, and K.M. McGowan. 2002. Keratin 16 expression defines a subset of epithelial cells during skin morphogenesis and the hair cycle. J. Invest. Dermatol. 119:1137-1149.
3. Briki, F., J. Doucet, and C. Etchebest. 2002. A procedure for refining a coiled coil protein structure using x-ray fiber diffraction and modeling. Biophys. J. 83:1774-1783.
4. Burkhard, P., R.A. Kammerer, M.O. Steinmetz, G.P. Bourenkov, and U. Aebi. 2000. The coiled-coil trigger site of the rod domain of cortexillin I unveils a distinct network of interhelical and intrahelical salt bridges. Struct. Fold. Des. 8:223-230.
5. Chou, C.F., C.L. Riopel, L.S. Rott, and M.B. Omary. 1993. A significant soluble keratin fraction in "simple" epithelial cells. Lack of an apparent phosphorylation and glycosylation role in keratin solubility. J. Cell Sci. 105:433-445.
6. Cohen, C., and D.A. Parry. 1990. Alpha-helical coiled coils and bundles: how to design an alpha-helical protein. Proteins. 7:1-15.
7. Coulombe, P.A., and E. Fuchs. 1990. Elucidating the early stages of keratin filament assembly. J. Cell Biol. 111:153-169.
8. Coulombe, P.A., and M.B. Omary. 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., and P. Wong. 2004. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat. Cell Biol. 6:699-706.
10. Crick, F.H. 1952. Is alpha-keratin a coiled coil? Nature. 170:882-883.
11. Er Rafik, M., J. Doucet, and F. Briki. 2004. The intermediate filament architecture as determined by X-ray diffraction modeling of hard alpha-keratin. Biophys. J. 86:3893-3904.
12. Fenn, T.D., D. Ringe, and G.A. Petsko. 2003. POVScript+: a program for model and data visualization using persistence of vision ray-tracing. J. Appl. Crystallogr. 36:944-947.
13. Fradette, J., L. Germain, P. Sessaiah, and P.A. Coulombe. 1998. The type I keratin 19 possesses distinct and context-dependent assembly properties. J. Biol. Chem. 273:35176-35184.
14. Fuchs E., and D.W. Cleveland. 1998. A structural scaffolding of intermediate filaments in health and disease. Science. 279:514-519.
15. Geisler, N., J. Schunemann, and K. Weber. 1992. Chemical cross-linking indicates a staggered and antiparallel protofilament of desmin intermediate filaments and characterizes one higher-level complex between protofilaments. Eur. J. Biochem. 206:841-852.
16. Guex, N., and M.C. Peitsch. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18: 2714-2723.
17. Hatzfeld, M., and M. Burba. 1994. Function of type I and type II keratin head domains: their role in dimer, tetramer and filament formation. J. Cell Sci. 107:1959-1972.
18. Hermann, H., and U. Aebi. 1998. Intermediate filament assembly: fibrillogenesis is driven by decisive dimer-dimer interactions. Curr. Opin. Struct. Biol. 8:177-185.
19. Herrmann, H., M. Haner, M. Brettel, N.O. Ku, and U. Aebi. 1999. Characterization of distinct early assembly units of different intermediate filament proteins. J. Mol. Biol. 286:1403-1420.
20. Hess, J.F., M.S. Budamagunta, J.C. Voss, and P.G. FitzGerald. 2004. Structural characterization of human vimentin rod 1 and the sequencing of assembly steps in intermediate filament formation in vitro using SDSL and EPR. J. Biol. Chem. 279:44841-44846.
21. Hess, J.F., J.C. Voss, and P.G. FitzGerald. 2002. Real-time observation of coiled-coil domains and subunit assembly in intermediate filaments. J. Biol. Chem. 277:35516-35522.
22. Hesse, M., T.M. Magin, and K. Weber. 2001. Genes for intermediate filament proteins and the draft sequence of the human genome: novel keratin genes and a surprisingly high number of pseudogenes related to keratin genes 8 and 18. J. Cell Sci. 114:2569-2575.
23. Janmey, P.A. 1991. Mechanical properties of cytoskeletal polymers. Curr. Opin. Cell Biol. 3:4-11.
24. Koradi, R., M. Billeter, and K. Wuthrich. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55, 29-32.
25. Kreplak, L., A. Franbourg, F. Briki, F. Leroy, D. Dalle, and J. Doucet. 2002. A new deformation model of hard alpha-keratin fibers at the nanometer scale: implications for hard alpha-keratin intermediate filament mechanical properties. Biophys. J. 82:2265-2274.
26. Kulesh, D.A., G. Cecena, Y.M. Darmon, M. Vasseur, and R.G. Oshima. 1989. Posttranslational regulation of keratins: degradation of mouse and human keratins 18 and 8. Mol. Cell Biol. 9:1553-1565.
27. Lersch, R., V. Stellmach, C. Stocks, G. Giudice, and E. Fuchs. 1989. Isolation, sequence, and expression of a human keratin K5 gene: transcriptional regulation of keratins and insights into pairwise control. Mol. Cell. Biol. 9:3685-3697.
28. Li, Y., J.H. Brown, L. Reshetnikova, A. Blazsek, L. Farkas, L. Nyitray, and C. Cohen. 2003. Visualization of an unstable coiled coil from the scallop myosin rod. Nature. 424:341-345.
29. McGowan, K.M., and P.A. Coulombe. 1998. Onset of keratin 17 expression coincides with the definition of major epithelial lineages during skin development. J. Cell Biol. 143:469-486.
30. McGowan, K.M., X. Tong, E. Colucci-Guyon, F. Langa, C. Babinet, and P.A. Coulombe. 2002. Keratin 17 null mice exhibit age- and strain-dependent alopecia. Genes Dev. 16:1412-1422.
31. McLachlan, A.D., and M. Stewart. 1982. Periodic charge distribution in the intermediate filament proteins desmin and vimentin. J. Mol. Biol. 162: 693-698.
32. Mehrani, T., K.C. Wu, M.I. Morasso, J.T. Bryan, L.N. Marekov, D.A. Parry, and P.M. Steinert. 2001. Residues in the 1A rod domain segment and the linker L2 are required for stabilizing the A11 molecular alignment mode in keratin intermediate filaments. J. Biol. Chem. 276:2088-2097.
33. Meng, J.J., S. Khan, and W. Ip. 1994. Charge interactions in the rod domain drive formation of tetramers during intermediate filament assembly. J. Biol. Chem. 269:18679-18685.
34. Merritt, E.A., and D.J. Bacon. 1997. Raster3D: photorealistic molecular graphics in enzymology. Methods Enzymol. 277:505-524.
35. Mucke, N., T. Wedig, A. Burer, L.N. Marekov, P.M. Steinert, J. Langowski, U. Aebi, and H. Herrmann. 2004. Molecular and biophysical characterization of assembly-starter units of human vimentin. J. Mol. Biol. 340:97-114.
36. Omary, M.B., P.A. Coulombe, and I.M. McLean. 2004. Intermediate filament proteins and their associated diseases. N. Engl. J. Med. 351:2087-2100.
37. 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.
38. 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.
39. Parry, D.A., W.G. Crewther, R.D. Fraser, and T.P. MacRae. 1977. Structure of alpha-keratin: structural implication of the amino acid sequences of the type I and type II chain segments. J. Mol. Biol. 113:449-454.
40. Parry, D.A., and P.M. Steinert. 1999. Intermediate filaments: molecular architecture, assembly, dynamics and polymorphism. Q. Rev. Biophys. 32:99-187.
41. Porter, R.M., A.M. Hutcheson, E.L. Rugg, R.A. Quinlan, and E.B. Lane. 1998. cDNA cloning, expression, and assembly characteristics of mouse keratin 16. J. Biol. Chem. 273:32265-32272.
42. Quinlan, R.A., J.A. Cohlberg, D.L. Schiller, M. Hatzfeld, and W.W. Franke. 1984. Heterotypic tetramer (A2D2) complexes of non-epidermal keratins isolated from cytoskeletons of rat hepatocytes and hepatoma cells. J. Mol. Biol. 178:365-388.
43. Sali, A., and T.L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
44. Schagger, H. 2001. Blue-native gels to isolate protein complexes from mitochondria. Methods Cell Biol. 65:231-244.
45. Semisotnov, G.V., N.A. Rodionova, O.I. Razgulyaev, V.N. Uversky, A.F. Gripas, and R.I. Gilmanshin. 1991. Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers. 31:119-128.
46. Soellner, P., R.A. Quinlan, and W.W. Franke. 1985. Identification of a distinct soluble subunit of an intermediate filament protein: tetrameric vimentin from living cells. Proc. Natl. Acad. Sci. USA. 82:7929-7933.
47. Steinert, P.M. 1991. Analysis of the mechanism of assembly of mouse keratin 1/keratin 10 intermediate filaments in vitro suggests that intermediate filaments are built from multiple oligomeric units rather than a unique tetrameric building block. J. Struct. Biol. 107:175-188.
48. Steinert, P.M., L.N. Marekov, R.D. Fraser, and D.A. Parry. 1993a. Keratin intermediate filament structure. Crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly. J. Mol. Biol. 230:436-452.
49. Steinert, P.M., L.N. Marekov, and D.A. Parry. 1993b. Conservation of the structure of keratin intermediate filaments: molecular mechanism by which different keratin molecules integrate into preexisting keratin intermediate filaments during differentiation. Biochemistry. 32:10046-10056.
50. Steinert, P.M., L.N. Marekov, and D.A. Parry. 1993c. Diversity of intermediate filament structure. Evidence that the alignment of coiled-coil molecules in vimentin is different from that in keratin intermediate filaments. J. Biol. Chem. 268:24916-24925.
51. Strelkov, S.V., H. Herrmann, and U. Aebi. 2003. Molecular architecture of intermediate filaments. Bioessays. 25:243-251.
52. Strelkov, S.V., H. Herrmann, N. Geisler, A. Lustig, S. Ivaninskii, R. Zimbelmann, P. Burkhard, and U. Aebi. 2001. Divide-and-conquer crystallographic approach towards an atomic structure of intermediate filaments. J. Mol. Biol. 306:773-781.
53. 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.
54. Thompson, J.D., T.J. Gibson, F. Plewniak, F. Jeanmougin, and D.G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
55. Wawersik, M., R.D. Paladini, E. Noensie, and P.A. Coulombe. 1997. A proline residue in the a-helical rod domain of type I keratin 16 destabilizes keratin heterotetramers and influences incorporation into filaments. J. Biol. Chem. 272:32557-32565.
56. Wong, P., E. Colucci-Guyon, K. Takahashi, C. Gu, C. Babinet, and P.A. Coulombe. 2000. Introducing a null mutation in the mouse K6alpha and K6beta genes reveals their essential structural role in the oral mucosa. J. Cell Biol. 150:921-928.
57. Wong, P., and P.A. Coulombe. 2003. Loss of keratin 6 (K6) proteins reveals a function for intermediate filaments during wound repair. J. Cell Biol. 163:327-337.
58. 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.