Three-dimensional modelling of interchain sequence similarities and differences in the coiled-coil segments of keratin intermediate filament heterodimers highlight features important in assembly

Journal of Structural Biology

Volumn 162, Issue 1, 2008, Pages 139-151

  Smith, Thomasin A ^a   Parry, David A D ^a  

^a MASSEY UNIVERSITY   (New Zealand)

Author keywords

Coiled coil; Heterodimers; Keratin

Indexed keywords

ACID PROTEIN; BASIC PROTEIN; HETERODIMER; KERATIN;

ARTICLE; COILED COIL SEGMENT; CRYSTAL STRUCTURE; MOLECULE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RESIDUE ANALYSIS; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING;

COMPUTER SIMULATION; DIMERIZATION; INTERMEDIATE FILAMENTS; KERATINS; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 41649085802     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.11.005     Document Type: Article

References (43)

1. Ahmadi B., and Speakman P.T. Suberimidate crosslinking shows that a rod-shaped, low-cystine, high-helix protein prepared by limited proteolysis of reduced wool has four protein chains. FEBS Lett. 94 (1978) 365-367
2. Brown J.H., Cohen C., and Parry D.A.D. Heptad breaks in α-helical coiled coils: stutters and stammers. Proteins: Struct. Funct. Genet. 26 (1996) 134-145
3. Ching G.Y., and Liem R.K. Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments. J. Cell Biol. 122 (1993) 1323-1335
4. Conway J.F., and Parry D.A.D. Structural features in the heptad substructure and longer range repeats of two-stranded α-fibrous proteins. Int. J. Biol. Macromol. 10 (1990) 328-334
5. Crewther W.G., and Dowling L.M. The preparation and properties of large peptides from the helical regions of the low-sulphur proteins of wool. Appl. Polym. Symp. 18 (1971) 1-20
6. Crewther W.G., Inglis A.S., and McKern N.M. Amino acid sequences of α-helical segments from S-carboxymethylkerateine-A. II. Complete sequence of a type II segment. Biochem. J. 173 (1978) 365-371
7. Fraser R.D.B., and MacRae T.P. Intermediate filament structure. Biosci. Rep. 5 (1985) 573-579
8. Fraser R.D.B., and MacRae T.P. Surface lattice in α-keratin filaments. Int. J. Biol. Macromol. 10 (1988) 178-184
9. Fraser R.D.B., and Parry D.A.D. Structural changes in the trichocyte intermediate filaments accompanying the transition from the reduced to the oxidized form. J. Struct. Biol. 159 (2007) 36-45
10. Harbury P.B., Zhang T., Kim P.S., and Alber T. A switch between two-, three- and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262 (1993) 1401-1407
11. Harbury P.B., Kim P.S., and Alber T. Crystal structure of an isoleucine-zipper trimer. Nature (London) 371 (1994) 80-83
12. Hatzfeld M., and Weber K. 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 (1990) 1199-1210
13. Herrling J., and Sparrow L.G. Interactions of intermediate filament proteins from wool. Int. J. Biol. Macromol. 13 (1991) 115-119
14. Herrmann H., and Aebi U. Intermediate filaments and their associates: multitalented structural elements specifying cyto-architecture and cyto-dynamics. Curr. Opin. Cell Biol. 12 (2000) 79-90
15. Herrmann H., Häner M., Brettel M., Ku N.O., and Aebi U. Characterization of distinct early assembly units of different intermediate filament proteins. J. Mol. Biol. 286 (1999) 1403-1420
16. Herrmann H., Strelkov S.V., Feja B., Rogers K.R., Brettel M., Lustig A., Häner M., Parry D.A.D., Steinert P.M., Burkhard P., and Aebi U. The intermediate filament protein consensus motif of segment 2B:its atomic structure and contribution to assembly. J. Mol. Biol. 298 (2000) 817-832
17. Jones L.N., Simon M., Watts N.R., Booy F.P., Steven A.C., and Parry D.A.D. Intermediate filament structure: hard α-keratin. Biophys. Chem. 68 (1997) 83-93
18. Lee M.K., Xu Z., Wong P.C., and Cleveland D.W. Neurofilaments are obligate heteropolymers in vivo. J. Cell Biol. 122 (1993) 1337-1350
19. Lupas A.N., and Gruber M. The structure of α-helical coiled coils. Adv. Pro. Chem. 70 (2005) 37-78
20. McLachlan A.D., and Stewart M. Tropomyosin coiled-coil interactions: evidence for an unstaggered structure. J. Mol. Biol. 98 (1975) 293-304
21. Monteiro M.J., and Cleveland D.W. Expression of NF-L and NF-M in fibroblasts reveals coassembly of neurofilament and vimentin subunits. J. Cell Biol. 108 (1989) 579-593
22. O'Shea E.K., Klemm J.D., Kim P.S., and Alber T. X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 254 (1991) 539-544
23. Papapostolou D., Smith A.M., Atkins E.D.T., Oliver S.J., Ryadnov M.G., Serpell L.C., and Woolfson D.N. Engineering nanoscale order into a designed protein fiber. Proc. Natl. Acad. Sci. USA 104 (2007) 10853-10858
24. Parry D.A.D. Microdissection of the sequence and structure of intermediate filament chains. Adv. Pro. Chem. 70 (2005) 113-142
25. Parry D.A.D., and Steinert P.M. Intermediate filaments: molecular architecture, assembly, dynamics and polymorphism. Quart. Rev. Biophys. 32 (1999) 99-187
26. Parry D.A.D., Crewther W.G., Fraser R.D.B., and MacRae T.P. Structure of α-keratin: structural implication of the amino acid sequences of the type I and type II chain segments. J. Mol. Biol. 113 (1977) 449-454
27. Parry D.A.D., Steven A.C., and Steinert P.M. The coiled-coil molecules of intermediate filaments consist of two parallel chains in exact axial register. Biochem. Biophys. Res. Commun. 127 (1985) 1012-1018
28. Parry D.A.D., Strelkov S.V., Burkhard P., Aebi U., and Herrmann H. Towards a molecular description of intermediate filament structure and assembly. Expt. Cell Res. 313 (2007) 2204-2216
29. Schweizer J., Bowden P.E., Coulombe P.A., Langbein L., Lane E.B., Magin T.M., Maltheis L., Omary M.B., Parry D.A.D., Rogers M.A., and Wright M. New consensus nomenclature for mammalian keratins. J. Cell Biol. 174 (2006) 169-174
30. Smith T.A., and Parry D.A.D. 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 (2007) 344-357
31. Smith T.A., Strelkov S.V., Burkhard P., Aebi U., and Parry D.A.D. Sequence comparisons of intermediate filament chains: evidence of a unique functional/structural role for the coiled-coil segment 1A and linker L1. J. Struct. Biol. 137 (2002) 128-145
32. Steinert P.M. The two-chain coiled-coil molecule of native epidermal keratin intermediate filaments is a type I-type II heterodimer. J. Biol. Chem. 265 (1990) 8766-8774
33. Steinert P.M., Idler W.W., Cabral F., Gottesman M.M., and Goldman R.D. In vitro assembly of homopolymer and copolymer filaments from intermediate filament subunits of muscle and fibroblastic cells. Proc. Natl. Acad. Sci. USA 78 (1981) 3692-3696
34. Steinert P.M., Marekov L.N., and Parry D.A.D. Molecular parameters of type IV α-internexin and type IV-type III α-internexin-vimentin copolymer intermediate filaments. J. Biol. Chem. 274 (1999) 1657-1666
35. Steinert P.M., Chou Y.H., Prahlad V., Parry D.A.D., Marekov L.N., Wu K.C., Jang S.I., and Goldman R.D. A high molecular weight intermediate filament-associated protein in BHK-21 cells is nestin, a type IV intermediate filament protein: limited co-assembly in vitro to form heteropolymers with type III vimentin and type IV α-internexin. J. Biol. Chem. 274 (1999) 9881-9890
36. Strelkov S.V., and Burkhard P. Analysis of α-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J. Struct. Biol. 137 (2002) 54-64
37. Strelkov S.V., Herrmann H., Geisler N., Wedig T., Zimbelmann R., Aebi U., and Burkhard P. Conserved segments 1A and 2B of the intermediate filament dimer: their atomic structures and role in filament assembly. EMBO J. 21 (2002) 1255-1266
38. Strelkov S.V., Schumacher J., Burkhard P., Aebi U., and Herrmann H. Crystal structure of the human lamin A coil 2B dimer: implications for the head-to-tail association of nuclear lamins. J. Mol. Biol. 343 (2004) 1067-1080
39. Wang H., Parry D.A.D., Jones L.N., Idler W.W., Marekov L.N., and Steinert P.M. In vitro assembly and structure of trichocyte keratin intermediate filaments: a novel role for stabilization by disulfide bonding. J. Cell Biol. 151 (2000) 1459-1468
40. Watts N.R., Jones L.N., Cheng N., Wall J.S., Parry D.A.D., and Steven A.C. Cryo-electron microscopy of trichocyte (hard α-keratin) intermediate filaments reveals a low-density core. J. Struct. Biol. 137 (2002) 109-118
41. Woods E.F. The number of polypeptide chains in the rod domain of bovine epidermal keratin. Biochem. Int. 7 (1983) 769-774
42. Woods E.F., and Inglis A.S. Organization of the coiled-coils in the wool microfibril. Int. J. Biol. Macromol. 6 (1984) 277-283
43. Woolfson D.N. The design of coiled-coil structures and assemblies. Adv. Pro. Chem. 70 (2005) 79-112