Advertisement

The Structure and Evolution of Intermediate Filament Genes

  • Dennis R. Roop
  • Peter M. Steinert

Abstract

Intermediate filaments (IF) are major cytoskeletal components of most eukaryotic cells (Lazarides, 1980; Steinert et al., 1984a). They have been classified into at least five distinct subclasses, each of which contains from 1 to 30 subunits encoded by separate genes (Lazarides, 1980; Fuchs and Hanakoglu, 1983). These genes are differentially expressed in different tissues and during different stages of differentiation (Lazarides, 1980; Steinert et al., 1984a; Fuchs and Hanukoglu, 1983; Moll et al., 1982; Eichner et al., 1984; Roop et al., 1984b). We have isolated and characterized cDNA clones corresponding to the major keratins synthesized in mouse epidermis (Roop et al., 1983, 1985b). Several lines of evidence are presented which suggest that the expression of subsets of keratin genes is coordinately regulated and dependent on the state of differentiation. Analysis of amino acid sequence data deduced for these keratin subunits (Steinert et al., 1983, 1984b, 1985a) has revealed fundamental differences in the primary sequences of keratin subunits that are expressed at different states of differentiation that may alter the properties and function of filaments containing these subunits (Steinert et al., 1985a). In addition, a comparison of these amino acid sequences with those of other IF subunits (Hanakoglu and Fuchs, 1982, 1983; Quax et al., 1983; Geisler and Weber, 1982; Lewis et al., 1984) has shown that all IF subunits possess a common secondary structure, consisting of a conserved central α-helical rod domain and non-α-helical end domains of variable size and sequence.

Keywords

Heptad Repeat Intermediate Filament Keratin Gene Epidermal Keratin Primordial Gene 
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. Alexander, F., Young, P. R., and Tilghman, S. M., 1984, Evolution of the albumin:a-fetoprotein ancestral gene from the amplification of a 27 nucleotide sequence, J. Mol. Biol. 173: 159–176.PubMedCrossRefGoogle Scholar
  2. Craik, C. S., Rutter, W. J., and Fletterick, R., 1983, Splice junctions: Association with variation in protein structure, Science 220: 1125–1129.PubMedCrossRefGoogle Scholar
  3. Crewther, W. G., Dowling, L. M., Steinert, P. M., and Parry, D. A. D., 1983, The structure of intermediate filaments, Int. J. Biol. Macromol. 5: 267–274.CrossRefGoogle Scholar
  4. Eichner, R., Bonitz, P., and Sun, T.-T., 1984, Classification of epidermal keratins according to their immunoreactivity, isoelectric point, and mode of expression, J. Cell Biol. 98: 1388 — 1396.PubMedCrossRefGoogle Scholar
  5. Fuchs, E., and Hanakoglu, I., 1983, Unraveling the structure of the intermediate filaments, Cell 34: 332–334.PubMedCrossRefGoogle Scholar
  6. 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
  7. Gilbert, W., 1978, Why genes in pieces? Nature 271: 501.PubMedCrossRefGoogle Scholar
  8. Gillespie, J. M., 1983, The structural proteins of hair: Isolation, characterization and regulation of biosynthesis, in: Biochemistry and Physiology of the Skin ( L. A. Goldsmith, ed.), pp. 475–510, Oxford University Press, New York.Google Scholar
  9. Hanukoglu, I., and Fuchs, E., 1982, The cDNA sequence of a human epidermal keratin: diver¬gence of sequence but conservation of structure among intermediate filament proteins, Cell 31: 243–252.PubMedCrossRefGoogle Scholar
  10. Hanukoglu, I., and Fuchs, E., 1983, The cDNA sequence of a type II cytoskeletal keratin reveals constant and variable structural domains among keratins, Cell 33: 915–924.PubMedCrossRefGoogle Scholar
  11. Johnson, L. D., Idler, W. W., Zhou, X-M., Roop, D. R., and Steinert, P. M., 1985, The structure of the gene for the human epidermal keratin of 67,000 molecular weight, Proc. Natl. Acad. Sci. USA 82: 1896–1900.PubMedCrossRefGoogle Scholar
  12. Krieg, T. M., Schafer, M. P., Cheng, C. K., Filpula, D., Flaherty, P., Steinert, P. M., and Roop, D. R., 1985, Organization of a type I keratin gene: Evidence for evolution of intermediate filaments from a common ancestral gene, J. Biol. Chem. 260: 5867–5870.PubMedGoogle Scholar
  13. Lau, S. Y. M., Taneja, A. K., and Hodges, R. S., 1984, Synthesis of a model protein of defined secondary and quaternary structure. Effect of chain length on the stabilization and forma¬tion of two-stranded a-helical coiled-coils, J. Biol. Chem. 259: 13253–13261.PubMedGoogle Scholar
  14. Lazarides, E., 1980, Intermediate filaments as mechanical integrators of cellular space, Nature 282: 249–256.CrossRefGoogle Scholar
  15. Lehnert, M. E., Jorcano, J. L., Hanswalter, Z., Blessing, M., Franz, J. K., and Franke, W. W., 1984, Characterization of bovine epidermal keratin genes: Similarities of exon patterns in genes coding for different keratins, EMBO J. 3: 3279–3287.PubMedGoogle Scholar
  16. Lewis, S. A., Balcarek, J. M., Krek, V., Shelanski, M. L., and Cowan, N. J., 1984, Sequence of a cDNA clone encoding mouse glial fibrillary acidic protein: Structural conservation of inter¬mediate filaments, Proc. Natl. Acad. Sci. U.S.A. 81: 2743–2746.PubMedCrossRefGoogle Scholar
  17. Lomedico, P., Rosenthal, N., Efstratiadis, Gilbert, W., Kolodner, R., and Tizard, R., 1979, The structure and evolution of the two nonallelic rat preproinsulin genes, Cell 18: 545–558.Google Scholar
  18. Lonberg, N., and Gilbert, W., 1985, Intron/exon structure of the chicken pyruvate kinase gene, Cell 40: 81–90.PubMedCrossRefGoogle Scholar
  19. Marchuk, D., McCrohon, S., and Fuchs, E., 1984, Remarkable conservation of structure among intermediate filament genes, Cell 39: 491–498.PubMedCrossRefGoogle Scholar
  20. Moll, R., Franke, W. W., Schiller, D. L., Geiger, B., and Krepler, R., 1982, The catalog of human cy to keratins: Patterns of expression in normal epithelia, tumors and cultured cells, Cell 31: 11–21.PubMedCrossRefGoogle Scholar
  21. Mount, S. M., 1982, A catalogue of splice junction sequence, Nucl. Acid Res. 10: 459–472.CrossRefGoogle Scholar
  22. Ohno, S., Matsunaga, T., and Wallace, R. B., 1982, Identification of the 48-base-long primordial building block sequence of mouse immunoglobulin variable region genes, Proc. Natl. Acad. Sci. U.S.A. 77: 1999–2002.CrossRefGoogle Scholar
  23. Parry, D. A. D., Crewther, W. G., Fraser, R. D. B., and MacRae, T. P., 1977, Structure of alpha- keratin: structural implications of the amino acid sequences of the type I and type II chain segments, J. Mol. Biol. 113: 448–454.CrossRefGoogle Scholar
  24. Quax, W., Egberts, W. V., Hendricks, W., Quax-Jeuken, Y., and Bloemendal, H., 1983, The structure of the vimentin gene, Cell, 35: 215–223.PubMedCrossRefGoogle Scholar
  25. Roop, D. R., Hawley-Nelson, P., Cheng, C. K., and Yuspa, S. H., 1983, Keratin gene expression in mouse epidermis and cultured epidermal cells, Proc. Natl. Acad. Sci. U.S.A. 80: 716–720.PubMedCrossRefGoogle Scholar
  26. Roop, D. R., Cheng, C. K., Titterington, L., Meyers, C. A., Stanley, J. R., Steinert, P. M., and Yuspa, S. H., 1984a, Synthetic peptides corresponding to keratin subunits elicit highly specific antibodies, J. Biol. Chem. 259: 8037–8040.PubMedGoogle Scholar
  27. Roop, D. R., Toftgard, R., Yuspa, S. H., Kronenberg, M. S., and Clark, J. H., 1984b, Changes in mouse keratin gene expression during differentiation, in: The Molecular Biology of the Cytoskeleton (G. G. Borisy, D. W. Cleveland, and D. B. Murphy, eds.), pp. 409–414, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.Google Scholar
  28. Roop, D. R., Cheng, C. K., Toftgard, R., Stanley, J. R., Steinert, P. M., and Yuspa, S. H., 1985a, The use of cDNA-cones and monospecific antibodies as probes to monitor keratin gene expression, Ann. NY Acad. Sci. 455: 426–435.PubMedCrossRefGoogle Scholar
  29. Roop, D. R., Cheng, C. K., Toftgard, R., and Yuspa, S. H., 1985b, The isolation of cDNA clones corresponding to keratin expressed in basal epidermal cells, (submitted for publication).Google Scholar
  30. Seidman, J. G., Leder, A., Nau, M., Norman, B., and Leder, P., 1978, Antibody diversity: The structure of cloned immunoglobulin genes suggests a mechanism for generating new sequences, Science 202: 11–16.PubMedCrossRefGoogle Scholar
  31. Steinert, P. M., Rice, R. H., Roop, D. R., Trus, B. L., and Steven, A. C., 1983, Complete amino acid sequence of a mouse epidermal keratin subunit: Implications for the structure of intermediate filaments, Nature 302: 79–800.CrossRefGoogle Scholar
  32. Steinert, P. M., Jones, J. C. R., and Goldman, R. D., 1984a, Intermediate filaments, J. Cell Biol. 99: 22s–27s.PubMedCrossRefGoogle Scholar
  33. Steinert, P. M., Parry, D. A. D., Racoosin, E. L., Idler, W. W., Steven, A. C., Trus, B. L., and Roop, D. R., 1984b, The complete cDNA and deduced amino acid sequence of a Type II mouse epidermal keratin of 60,000 molecular weight: Analysis of sequence differences between Type I and Type II keratins, Proc. Natl. Acad. Sci. U.S.A. 81: 5709–5713.PubMedCrossRefGoogle Scholar
  34. Steinert, P. M., Parry, D. A. D., Idler, W. W., Johnson, L. J., Stevens, A. C., and Roop, D. R., 1985a, 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.Google Scholar
  35. Steinert, P. M., Steven, A. C., and Roop, D. R., 1985b, The molecular biology of intermediate filaments, Cell 42: 411–419.PubMedCrossRefGoogle Scholar
  36. Sun, T.-T., Eichner, R., Schermer, A., Cooper, D., Nelson, W. G., and Weiss, R. A., 1984, Classification, expression and possible mechanisms of evolution of mammalian epithelial keratins: a unifying model, in: Cancer Cells 1, The Transformed Phenotype, pp. 169–176, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.Google Scholar
  37. Yamada, K., Avvedimento, V. E., Mudryji, M., Ohkubo, H., Vogeli, G., Irani, M., Pastan, I., and de Crombrugghe, B., 1980, The collagen gene: Evidence for its evolutionary assembly by amplification of a DNA segment containing an exon of 54 bp, Cell 22: 887–892.PubMedCrossRefGoogle Scholar
  38. Yuspa, S. H., Hawley-Nelson, P., Stanley, J. R., and Hennings, H., 1980, Epidermal cell culture, Transpl. Proc. 12 (suppl 1): 114–122.Google Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • Dennis R. Roop
    • 1
  • Peter M. Steinert
    • 2
  1. 1.Laboratory of Cellular Carcinogenesis and Tumor PromotionNational Cancer Institute, National Institutes of HealthBethesdaUSA
  2. 2.Dermatology BranchNational Cancer Institute, National Institutes of HealthBethesdaUSA

Personalised recommendations