Advertisement

The Three-Dimensional Structure of IF

  • R. D. B. Fraser
  • T. P. MacRae
  • David A. D. Parry

Abstract

Although it is only comparatively recently that intermediate filaments (IF) have been recognized as a class of cytoskeletal structures, it is now more than 50 years since information was first collected on the three-dimensional structure of individual members of the class. For example, in discussing Speakman’s observations on the sorption of water by wool and his own x-ray studies of wool, Astbury (1933) stated that “A wool fibre... becomes as much as about 18% greater in diameter but only about 1% longer. This transformation is easily explained from the results of x-ray analysis, which shows that the regain water is for the most part spread over the surfaces of the tiny crystalline aggregates which are much longer than they are thick. Because the crystals are so very tiny, perhaps not more than some twenty times thicker than the water molecules themselves....”

Keywords

Intermediate Filament Scanning Transmission Electron Microscopy Terminal Domain Coiled Coil Contact Plane 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aebi, U., Fowler, W. E., Rew, P., and Sun, T.-T., 1983, The fibrillar substructure of keratin filaments unraveled, J. Cell Biol. 97: 1131–1143.PubMedCrossRefGoogle Scholar
  2. Ahmadi, B., and Speakman, P. T., 1978, 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: 365–367.PubMedCrossRefGoogle Scholar
  3. Astbury, W. T., 1933, Fundamentals of Fibre Structure, Oxford University Press, London, p. 95.Google Scholar
  4. Astbury, W. T., and Street, A., 1931, X-ray studies of the structure of hair, wool and related fibres. I. General, Philos. Trans. R. Soc. London Ser. A 230: 75–101.Google Scholar
  5. Astbury, W. T., and Woods, H. J., 1933, X-ray studies of the structure of hair, wool and related fibres. II. The molecular structure and elastic properties of hair keratin, Philos. Trans. R. Soc. London Ser. A 232: 333–394.Google Scholar
  6. Bear, R. S., 1944, X-ray diffraction studies on protein fibers. II. Feather rachis, porcupine quill tip and clam muscle, J. Am. Chem. Soc. 66: 2043–2050.CrossRefGoogle Scholar
  7. Bear, R. S., and Selby, C. C., 1956, The structure of paramyosin fibrils according to X-ray diffraction, J. Biophys. Biochem. Cytol. 2: 55–70.PubMedCrossRefGoogle Scholar
  8. Bragg, W. L., Kendrew, J. C., and Perutz, M. F., 1950, Polypeptide chain configurations in crystalline proteins, Proc. R. Soc. London Ser. A 203: 321–357.CrossRefGoogle Scholar
  9. Brodsky, B., Eikenberry, E. F., and Cassidy, K., 1980, An unusual collagen periodicity in skin, Biochim. Biophys. Acta 621: 162–166.PubMedCrossRefGoogle Scholar
  10. Conway, J. F., and Parry, D. A. D., 1988, Intermediate filament structure 3: Analysis of sequence homologies, Int. J. Biol. Macromol. 10: 79–98.CrossRefGoogle Scholar
  11. Corey, R. B., and Wyckoff, R. W. G., 1936, Long spacings in macromolecular solids, J. Biol. Chem. 114: 407–414.Google Scholar
  12. Crewther, W. G., and Dowling, L. M., 1971, The preparation and properties of large peptides from the helical regions of the low-sulphur proteins of wool, Appl. Polym. Symp. No. 18, 1-20.Google Scholar
  13. Crewther, W. G., Inglis, A. S., and McKern, N. M., 1978, Amino acid sequences of α-helical segments from S-carboxymethylkerateine-A. II. Complete sequence of a type II segment, Biochem. J. 173: 365–371.PubMedGoogle Scholar
  14. Crewther, W. G., Dowling, L. M., Steinert, P. M., and Parry, D. A. D., 1983, Structure of intermediate filaments, Int. J. Biol. Macromol. 5: 267–274.CrossRefGoogle Scholar
  15. Crick, F. H. C., 1952, Is a-keratin a coiled-coil? Nature 170: 882–883.PubMedCrossRefGoogle Scholar
  16. Crick, F. H. C., 1953a, The Fourier transform of a coiled-coil, Acta Crystallogr. 6: 685–689.CrossRefGoogle Scholar
  17. Crick, F. H. C., 1953b, The packing of α-helices: Simple coiled-coils, Acta Crystallogr. 6: 689–697.CrossRefGoogle Scholar
  18. Doyle, B. B., Hukins, D. W. L., Hulmes, D. J. S., Miller, A., and Woodhead-Galloway, J., 1975, Collagen polymorphism: Its origins in the amino acid sequence, J. Mol. Biol. 91: 79–99.PubMedCrossRefGoogle Scholar
  19. Eichner, R., Rew, P., Engel, A., and Aebi, U., 1985, Human epidermal keratin filaments: Studies on their structure and assembly, in: Intermediate Filaments (E. Wang, D. Fischman, R. K. H. Liem, and T. T. Sun, eds.), New York Academy of Sciences, New York, pp. 381–402.Google Scholar
  20. Engel, A., Eichner, R., and Aebi, U., 1985, Polymorphism of reconstituted human epidermal keratin filaments: Determination of their mass-per-length and width by scanning transmission electron microscopy (STEM), J. Ultrastruct. Res. 90: 323–335.PubMedCrossRefGoogle Scholar
  21. Eriksson, A., and Thornell, L. E., 1979, Intermediate (skeletin) filaments in heart Purkinje fibers: A correlative morphological and biochemical identification with evidence of a cytoskeletal function, J. Cell Biol. 80: 231–247.PubMedCrossRefGoogle Scholar
  22. Filshie, B. K., and Rogers, G. E., 1961, The fine structure of a-keratin, J. Cell Biol. 3: 784–786.Google Scholar
  23. Franke, W. W., Schiller, D. L., and Grund, C., 1982, Protofilamentous and annular structures as intermediates during reconstitution of cytokeratin filaments in vitro, Biol. Cell 46: 257–268.Google Scholar
  24. Fraser, R. D. B., and MacRae, T. P., 1958, Structural implications of the equatorial X-ray diffraction pattern of a-keratin, Biochim. Biophys. Acta 29: 229–240.PubMedCrossRefGoogle Scholar
  25. Fraser, R. D. B., and MacRae, T. P., 1961, α-Configuration of fibrous proteins, Nature 189: 572–573.CrossRefGoogle Scholar
  26. Fraser, R. D. B., and MacRae, T. P., 1971, Structure of a-keratin, Nature 233: 138–140.PubMedCrossRefGoogle Scholar
  27. Fraser, R. D. B., and MacRae, T. P., 1973a, Conformation in Fibrous Proteins and Related Synthetic Polypeptides, Academic Press, New York.Google Scholar
  28. Fraser, R. D. B., and MacRae, T. P., 1973b, The structure of α-keratin, Polymer 14: 61–67.CrossRefGoogle Scholar
  29. Fraser, R. D. B., and MacRae, T. P., 1982, The fine structure of keratin fibers, in: Milton Harris: Chemist, Innovator and Entrepreneur (M. M. Breuer, ed.), American Chemical Society, Washington, D.C., pp. 109–137.Google Scholar
  30. Fraser, R. D. B., and MacRae, T. P., 1983, The structure of the α-keratin microfibril, Biosci. Rep. 3: 517–525.PubMedCrossRefGoogle Scholar
  31. Fraser, R. D. B., and MacRae, T. P., 1985, Intermediate filament structure, Biosci. Rep. 5: 573–579.PubMedCrossRefGoogle Scholar
  32. Fraser, R. D. B., and MacRae, T. P., 1988, Surface lattice in α-keratin filaments, Int. J. Biol. Macromol. 10: 178–184.CrossRefGoogle Scholar
  33. Fraser, R. D. B., MacRae, T. P., and Rogers, G. E., 1960, Recent observations on the structure of α-keratin, J. Text. Inst. Trans. 51: T497–T505.CrossRefGoogle Scholar
  34. Fraser, R. D. B., MacRae, T. P., and Miller, A., 1964a, The coiled-coil model of α-keratin structure, J. Mol. Biol. 10: 147–156.PubMedCrossRefGoogle Scholar
  35. Fraser, R. D. B., MacRae, T. P., and Miller, A., 1964b, Molecular structure of α-keratin, Nature 203: 1231–1233.CrossRefGoogle Scholar
  36. Fraser, R. D. B., MacRae, T. P., and Miller, A., 1965, X-ray diffraction patterns of α-fibrous proteins, J. Mol. Biol. 14: 432–442.PubMedCrossRefGoogle Scholar
  37. Fraser, R. D. B., MacRae, T. P., Millward, G. R., Parry, D. A. D., Suzuki, E., and Tulloch, P. A., 1971, The molecular structure of keratins, Appl. Polym. Symp. No. 18, 65-83.Google Scholar
  38. Fraser, R. D. B., MacRae, T. P., and Rogers, G. E., 1972, Keratins: Their Composition, Structure and Biosynthesis, Thomas, Springfield, 111.Google Scholar
  39. Fraser, R. D. B., Gillespie, J. M., and MacRae, T. P., 1973, Tyrosine-rich proteins in keratins, Comp. Biochem. Physiol. 44B: 943–947.Google Scholar
  40. Fraser, R. D. B., MacRae, T. P., and Suzuki, E., 1976, Structure of the α-keratin microfibril, J. Mol Biol. 108: 435–452.PubMedCrossRefGoogle Scholar
  41. Fraser, R. D. B., MacRae, T. P., Suzuki, E., and Tulloch, P. A., 1981, Ordered assemblies in fibrous proteins, in: Structural Aspects of Recognition and Assembly in Biological Macromolecules (M. Balaban, J. L. Sussman, W. Traub, and A. Yonath, eds.), Balaban ISS, Rehovot, Israel, pp. 327–340.Google Scholar
  42. Fraser, R. D. B., MacRae, T. P., Suzuki, E., and Parry, D. A. D., 1985, Intermediate filament structure: 2. Molecular interactions in the filament, Int. J. Biol. Macromol. 7: 258–274.CrossRefGoogle Scholar
  43. Fraser, R. D. B., MacRae, T. P., Parry, D. A. D., and Suzuki, E., 1986, Intermediate filaments in α-keratins, Proc. Natl. Acad. Sci. USA 83:1179–1183.PubMedCrossRefGoogle Scholar
  44. Fraser, R. D. B., MacRae, T. P., Sparrow, L. G., and Parry, D. A. D., 1988, Disulphide bonding in α-keratin, Int. J. Biol. Macromol. 10: 106–112.CrossRefGoogle Scholar
  45. Fraser, R. D. B., Conway, J. F., and Parry, D. A. D., Int. J. Biol. Macromol., in preparation.Google Scholar
  46. Geisler, N., and Weber, K., 1982, The amino acid sequence of chicken muscle desmin provides a common structural model for intermediate filament proteins, EMBO J. 1: 1649–1656.PubMedGoogle Scholar
  47. Geisler, N., Kaufmann, E., and Weber, K., 1985, Antiparallel orientation of the two double-stranded coiled-coils in the tetrameric protofilament unit of intermediate filaments, J. Mol. Biol. 182: 173–177.PubMedCrossRefGoogle Scholar
  48. Gough, K. H., Inglis, A. S., and Crewther, W. G., 1978, Amino acid sequences of α-helical segments from S-carboxymethylkerateine-A. Complete sequence of a type I segment, Biochem. J. 173: 373–385.PubMedGoogle Scholar
  49. Gruen, L. C., and Woods, E. F., 1983, Structural studies on the microfibrillar proteins of wool, Biochem. J. 209: 587–595.PubMedGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. Hofmann, H., Fietzek, P. P., and Kuhn, K., 1978, The role of polar and hydrophobic interactions for the molecular packing of type I collagen: A three-dimensional evaluation of the amino acid sequence, J. Mol. Biol. 125: 137–165.PubMedCrossRefGoogle Scholar
  52. Hulmes, D. J. S., Miller, A., Parry, D. A. D., Piez, K. A., and Woodhead-Galloway, J., 1973, Analysis of the primary structure of collagen for the origins of molecular packing, J. Mol. Biol. 79: 137–148.PubMedCrossRefGoogle Scholar
  53. Ip, W., Hartzer, M. K., Pang, Y.-Y. S., and Robson, R. M., 1985, Assembly of vimentin in vitro and its implications concerning the structure of intermediate filaments, J. Mol. Biol. 183: 365–375.PubMedCrossRefGoogle Scholar
  54. Kallman, F., and Wessels, N. K., 1967, Periodic repeat units of epithelial cell tonofilaments, J. Cell Biol. 32: 227–231.PubMedCrossRefGoogle Scholar
  55. Kaufmann, E., Weber, K., and Geisler, N., 1985, Intermediate filament forming ability of desmin derivatives lacking either the amino-terminal 67 or the carboxy-terminal 27 residues, J. Mol. Biol. 185: 733–742.PubMedCrossRefGoogle Scholar
  56. Klug, A., Crick, F. H. C., and Wyckoff, H. W., 1958, Diffraction by helical structures, Acta Crystallogr. 11: 199–213.CrossRefGoogle Scholar
  57. Krishnan, N., Kaiserman-Abramof, I. R., and Raymond, J. L., 1979, Helical structure of neurofilaments isolated from Myxicola and giant squid axons, J. Cell Biol. 82: 323–335.PubMedCrossRefGoogle Scholar
  58. Lang, A. R., 1956, An X-ray study of a-keratin. II. Diffractometer measurements of the complete diffraction pattern of Canadian porcupine quill, Acta Crystallogr. 9: 446–451.CrossRefGoogle Scholar
  59. MacArthur, I., 1943, Structure of a-keratin, Nature 152: 38–41.CrossRefGoogle Scholar
  60. McLachlan, A. D., and Stewart, M., 1982, Periodic charge distribution in the intermediate filament proteins desmin and vimentin, J. Mol. Biol. 162: 693–698.PubMedCrossRefGoogle Scholar
  61. Milam, L., and Erickson, H. P., 1982, Visualization of a 21 nm axial periodicity in shadowed keratin filaments and neurofilaments, J. Cell Biol. 94: 592–596.PubMedCrossRefGoogle Scholar
  62. Millward, G. R., 1970, The substructure of α-keratin microfibrils, J. Ultrastruct. Res. 31: 349–355.PubMedCrossRefGoogle Scholar
  63. Parry, D. A. D., 1975, Double helix of tropomyosin, Nature 256: 346–347.PubMedCrossRefGoogle Scholar
  64. Parry, D. A. D., and Elliott, A., 1967, The structure of a paracrystalline phase of poly-γ-benzyl-L-glutamate in dimethylformamide, J. Mol. Biol. 25: 1–13.PubMedCrossRefGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. Parry, D. A. D., Crewther, W. G., Fraser, R. D. B., and MacRae, T. P., 1977, Structure of α-keratin: Structural implication of the amino acid sequences of the type I and type II chain segments, J. Mol. Biol. 113: 449–454.PubMedCrossRefGoogle Scholar
  67. 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.PubMedCrossRefGoogle Scholar
  68. Pauling, L., and Corey, R. B., 1951, Atomic coordinates and structure factors for two helical configurations of polypeptide chains, Proc. Natl. Acad. Sci. USA 37: 235–240.PubMedCrossRefGoogle Scholar
  69. Pauling, L., and Corey, R. B., 1953, Compound helical configurations of polypeptide chains: Structure of proteins of the α-keratin type, Nature 171: 59–61.PubMedCrossRefGoogle Scholar
  70. Renner, W., Franke, W. W., Schmid, E., Geisler, N., Weber, K., and Mandelkow, E., 1981, Reconstitution of intermediate-sized filaments from denatured monomeric vimentin, J. Mol. Biol. 149: 285–306.PubMedCrossRefGoogle Scholar
  71. Rudall, K. M., 1952, The proteins of the mammalian epidermis, Adv. Protein Chem. 7: 253–290.PubMedCrossRefGoogle Scholar
  72. 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.PubMedCrossRefGoogle Scholar
  73. Selby, C. C., and Bear, R. S., 1956, The structure of actin-rich filaments of muscles according to X-ray diffraction, J. Biophys. Biochem. Cytol. 2: 71–84.PubMedCrossRefGoogle Scholar
  74. Sheridan, R. P., Levy, R. M., and Salemme, F. R., 1982, α-Helix dipole moment and electrostatic stabilization of 4-α-helical proteins, Proc. Natl. Acad. Sci. USA 79: 4545–4549.PubMedCrossRefGoogle Scholar
  75. Shoemaker, K. R., Kim, P. S., York, E. J., Stewart, J. M., and Baldwin, R. L., 1987, Tests of the helix dipole model for stabilization for α-helices, Nature 326: 563–567.PubMedCrossRefGoogle Scholar
  76. Skerrow, D., Matoltsy, A. G., and Matoltsy, M. N., 1973, Isolation and characterization of the α-helical regions of epidermal prekeratin, J. Biol. Chem. 248: 4820–4826.PubMedGoogle Scholar
  77. Squire, J. M., 1985, Muscle myosin filaments: Internal structure and crossbridge organization, Comments Mol. Cell. Biophys. 3: 155–177.Google Scholar
  78. Squire, J. M., and Elliott, A., 1969, Liquid crystalline phases of poly-γ-benzyl-glutamate in solution, Mol. Cryst. Liquid Cryst. 7: 457–468.CrossRefGoogle Scholar
  79. Steinert, P. M., 1977, The mechanism of assembly of bovine epidermal keratin filaments in vitro, in: Biochemistry of Cutaneous Epidermal Differentiation (M. Seiji and I. A. Bernstein, eds.), University of Tokyo Press, Tokyo, pp. 444–464.Google Scholar
  80. Steinert, P. M., 1978, Structure of the three-chain unit of the bovine epidermal keratin filament, J. Mol. Biol. 123: 49–70.PubMedCrossRefGoogle Scholar
  81. Steinert, P. M., 1981, Intermediate filaments (IF), in: Electron Microscopy of Proteins (J. R. Harris, ed.), Academic Press, New York, Volume 1, pp. 125–166.Google Scholar
  82. Steinert, P. M., and Parry, D. A. D., 1985, Intermediate filaments: Conformity and diversity of expression and structure, Annu. Rev. Cell Biol. 1: 41–65.PubMedCrossRefGoogle Scholar
  83. Steinert, P. M., Idler, W. W., and Goldman, R. D., 1980, Intermediate filaments of baby hamster kidney (BHK-21) cells and bovine epidermal keratinocytes have similar ultrastructures and subunit domain structures, Proc. Natl. Acad. Sci. USA 77: 4534–4538.PubMedCrossRefGoogle Scholar
  84. Steinert, P. M., Idler, W. W., Cabrai, F., Gottesman, M. M., and Goldman, R. D., 1981, In vitro assembly of homopolymer and copolymer filaments from intermediate filament subunits of muscle and fibroblastic cells, Proc. Natl. Acad. Sci. USA 78: 3692–3696.PubMedCrossRefGoogle Scholar
  85. Steven, A. C., Wall, J., Hainfeld, J., and Steinert, P. M., 1982, Structure of fibroblastic intermediate filaments: Analysis by scanning transmission electron microscopy, Proc. Natl. Acad. Sci. USA 79: 3101–3105.PubMedCrossRefGoogle Scholar
  86. Steven, A. C., Hainfeld, J. F., Trus, B. L., Wall, J. S., and Steinert, P. M., 1983a, Epidermal keratin filaments assembled in vitro have masses-per-unit-length that scale according to average subunit mass: Structural basis for homologous packing of subunits in intermediate filaments, J. Cell Biol. 97: 1939–1944.PubMedCrossRefGoogle Scholar
  87. Steven, A. C., Hainfeld, J. F., Trus, B. L., Wall, J. S., and Steinert, P. M., 1983b, The distribution of mass in heteropolymer intermediate filaments assembled in vitro, J. Biol. Chem. 258: 8323–8329.PubMedGoogle Scholar
  88. Suzuki, E., Crewther, W. G., Fraser, R. D. B., MacRae, T. P., and McKern, N. M., 1973, X-ray diffraction and infrared studies of an α-helical fragment from α-keratin, J. Mol. Biol. 73: 275–278.PubMedCrossRefGoogle Scholar
  89. Traub, P., and Vorgias, C. E., 1983, Involvement of the N-terminal polypeptide of vimentin in the formation of intermediate filaments, J. Cell Sci. 63: 43–67.PubMedGoogle Scholar
  90. Trus, B. L., and Piez, K. A., 1976, Molecular packing of collagen: Three-dimensional analysis of electrostatic interactions, J. Mol. Biol. 108: 705–732.PubMedCrossRefGoogle Scholar
  91. Wais-Steider, C., Eagles, P. A. M., Gilbert, D. S., and Hopkins, J. M., 1983, Structural similarities and differences amongst neurofilaments, J. Mol. Biol. 165: 393–400.PubMedCrossRefGoogle Scholar
  92. Woods, E. F., 1983, The number of polypeptide chains in the rod domain of bovine epidermal keratin, Biochem. Int. 7: 769–774.PubMedGoogle Scholar
  93. Woods, E. F., and Inglis, A. S., 1984, Organization of the coiled-coils in the wool microfibril, Int. J. Biol. Macromol. 6: 277–283.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • R. D. B. Fraser
    • 1
  • T. P. MacRae
    • 1
  • David A. D. Parry
    • 2
  1. 1.Division of Wool TechnologyCSIROParkvilleAustralia
  2. 2.Department of Physics and BiophysicsMassey UniversityPalmerston NorthNew Zealand

Personalised recommendations