Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1986 Aug;5(8):1865–1875. doi: 10.1002/j.1460-2075.1986.tb04438.x

Amino acid sequence and gene organization of cytokeratin no. 19, an exceptional tail-less intermediate filament protein.

B L Bader, T M Magin, M Hatzfeld, W W Franke
PMCID: PMC1167052  PMID: 2428612

Abstract

We have isolated a cDNA clone from a bovine bladder urothelium library which encodes the smallest intermediate filament (IF) protein known, i.e. the simple epithelial cytokeratin (equivalent to human cytokeratin 19) previously thought to have mol. wt 40,000. This clone was then used to isolate the corresponding gene from which we have determined the complete nucleotide sequence and deduced the amino acid sequence of the encoded protein. This cytokeratin of 399 amino acids (mol. wt 43,893) is identified as a typical acidic (type I) cytokeratin but differs from all other IF proteins in that it does not show the carboxyterminal, non-alpha-helical tail domain. Instead it contains a 13 amino acids extension of the alpha-helical rod. The gene encoding cytokeratin 19 is also exceptional. It contains only five introns which occur in positions corresponding to intron positions in other IF protein genes. However, an intron which in all other IF proteins demarcates the region corresponding to the transition from the alpha-helical rod into the non-alpha-helical tail is missing in the cytokeratin 19 gene. Using in vitro reconstitution of purified cytokeratin 19 we show that it reacts like other type I cytokeratins in that it does not form, in the absence of a type II cytokeratin partner, typical IF. Instead it forms 40-90 nm rods of 10-11 nm diameter which appear to represent lateral associations of a number of cytokeratin molecules. Our results demonstrate that the non-alpha-helical tail domain is not an indispensable feature of IF proteins. The gene structure of this protein provides a remarkable case of a correlation of a change in protein conformation with an exon boundary.

Full text

PDF
1865

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Balcarek J. M., Cowan N. J. Structure of the mouse glial fibrillary acidic protein gene: implications for the evolution of the intermediate filament multigene family. Nucleic Acids Res. 1985 Aug 12;13(15):5527–5543. doi: 10.1093/nar/13.15.5527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Banks-Schlegel S. P., Quintero J. Growth and differentiation of human esophageal carcinoma cell lines. Cancer Res. 1986 Jan;46(1):250–258. [PubMed] [Google Scholar]
  3. Bartek J., Durban E. M., Hallowes R. C., Taylor-Papadimitriou J. A subclass of luminal epithelial cells in the human mammary gland, defined by antibodies to cytokeratins. J Cell Sci. 1985 Apr;75:17–33. doi: 10.1242/jcs.75.1.17. [DOI] [PubMed] [Google Scholar]
  4. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  5. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  6. Chou P. Y., Fasman G. D. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. doi: 10.1146/annurev.bi.47.070178.001343. [DOI] [PubMed] [Google Scholar]
  7. Cooper A. D., Crain W. R., Jr Complete nucleotide sequence of a sea urchin actin gene. Nucleic Acids Res. 1982 Jul 10;10(13):4081–4092. doi: 10.1093/nar/10.13.4081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Craik C. S., Rutter W. J., Fletterick R. Splice junctions: association with variation in protein structure. Science. 1983 Jun 10;220(4602):1125–1129. doi: 10.1126/science.6344214. [DOI] [PubMed] [Google Scholar]
  9. Dynan W. S., Tjian R. Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. 1985 Aug 29-Sep 4Nature. 316(6031):774–778. doi: 10.1038/316774a0. [DOI] [PubMed] [Google Scholar]
  10. Eckert R. L., Green H. Cloning of cDNAs specifying vitamin A-responsive human keratins. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4321–4325. doi: 10.1073/pnas.81.14.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fornwald J. A., Kuncio G., Peng I., Ordahl C. P. The complete nucleotide sequence of the chick a-actin gene and its evolutionary relationship to the actin gene family. Nucleic Acids Res. 1982 Jul 10;10(13):3861–3876. doi: 10.1093/nar/10.13.3861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Franke W. W., Schiller D. L., Hatzfeld M., Winter S. Protein complexes of intermediate-sized filaments: melting of cytokeratin complexes in urea reveals different polypeptide separation characteristics. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7113–7117. doi: 10.1073/pnas.80.23.7113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Franke W. W., Schmid E., Osborn M., Weber K. Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5034–5038. doi: 10.1073/pnas.75.10.5034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Franke W. W., Schmid E., Schiller D. L., Winter S., Jarasch E. D., Moll R., Denk H., Jackson B. W., Illmensee K. Differentiation-related patterns of expression of proteins of intermediate-size filaments in tissues and cultured cells. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):431–453. doi: 10.1101/sqb.1982.046.01.041. [DOI] [PubMed] [Google Scholar]
  15. Franke W. W., Winter S., Grund C., Schmid E., Schiller D. L., Jarasch E. D. Isolation and characterization of desmosome-associated tonofilaments from rat intestinal brush border. J Cell Biol. 1981 Jul;90(1):116–127. doi: 10.1083/jcb.90.1.116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Franz J. K., Gall L., Williams M. A., Picheral B., Franke W. W. Intermediate-size filaments in a germ cell: Expression of cytokeratins in oocytes and eggs of the frog Xenopus. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6254–6258. doi: 10.1073/pnas.80.20.6254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fuchs E. V., Coppock S. M., Green H., Cleveland D. W. Two distinct classes of keratin genes and their evolutionary significance. Cell. 1981 Nov;27(1 Pt 2):75–84. doi: 10.1016/0092-8674(81)90362-7. [DOI] [PubMed] [Google Scholar]
  18. Fuchs E., Green H. Regulation of terminal differentiation of cultured human keratinocytes by vitamin A. Cell. 1981 Sep;25(3):617–625. doi: 10.1016/0092-8674(81)90169-0. [DOI] [PubMed] [Google Scholar]
  19. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  20. Geisler N., Kaufmann E., Weber K. Proteinchemical characterization of three structurally distinct domains along the protofilament unit of desmin 10 nm filaments. Cell. 1982 Aug;30(1):277–286. doi: 10.1016/0092-8674(82)90033-2. [DOI] [PubMed] [Google Scholar]
  21. Geisler N., Weber K. The amino acid sequence of chicken muscle desmin provides a common structural model for intermediate filament proteins. EMBO J. 1982;1(12):1649–1656. doi: 10.1002/j.1460-2075.1982.tb01368.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gilbert W. Genes-in-pieces revisited. Science. 1985 May 17;228(4701):823–824. doi: 10.1126/science.4001923. [DOI] [PubMed] [Google Scholar]
  23. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  24. Hanukoglu I., Fuchs E. The cDNA sequence of a Type II cytoskeletal keratin reveals constant and variable structural domains among keratins. Cell. 1983 Jul;33(3):915–924. doi: 10.1016/0092-8674(83)90034-x. [DOI] [PubMed] [Google Scholar]
  25. Hanukoglu I., Fuchs E. The cDNA sequence of a human epidermal keratin: divergence of sequence but conservation of structure among intermediate filament proteins. Cell. 1982 Nov;31(1):243–252. doi: 10.1016/0092-8674(82)90424-x. [DOI] [PubMed] [Google Scholar]
  26. Hatzfeld M., Franke W. W. 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. 1985 Nov;101(5 Pt 1):1826–1841. doi: 10.1083/jcb.101.5.1826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hoffmann W., Franz J. K. Amino acid sequence of the carboxy-terminal part of an acidic type I cytokeratin of molecular weight 51 000 from Xenopus laevis epidermis as predicted from the cDNA sequence. EMBO J. 1984 Jun;3(6):1301–1306. doi: 10.1002/j.1460-2075.1984.tb01966.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hunkapiller M. W., Hewick R. M., Dreyer W. J., Hood L. E. High-sensitivity sequencing with a gas-phase sequenator. Methods Enzymol. 1983;91:399–413. doi: 10.1016/s0076-6879(83)91038-8. [DOI] [PubMed] [Google Scholar]
  29. Johnson L. D., Idler W. W., Zhou X. M., Roop D. R., Steinert P. M. Structure of a gene for the human epidermal 67-kDa keratin. Proc Natl Acad Sci U S A. 1985 Apr;82(7):1896–1900. doi: 10.1073/pnas.82.7.1896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jonas E., Sargent T. D., Dawid I. B. Epidermal keratin gene expressed in embryos of Xenopus laevis. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5413–5417. doi: 10.1073/pnas.82.16.5413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Jorcano J. L., Franz J. K., Franke W. W. Amino acid sequence diversity between bovine epidermal cytokeratin polypeptides of the basic (type II) subfamily as determined from cDNA clones. Differentiation. 1984;28(2):155–163. doi: 10.1111/j.1432-0436.1984.tb00278.x. [DOI] [PubMed] [Google Scholar]
  32. Jorcano J. L., Magin T. M., Franke W. W. Cell type-specific expression of bovine keratin genes as demonstrated by the use of complementary DNA clones. J Mol Biol. 1984 Jun 15;176(1):21–37. doi: 10.1016/0022-2836(84)90380-2. [DOI] [PubMed] [Google Scholar]
  33. Jorcano J. L., Rieger M., Franz J. K., Schiller D. L., Moll R., Franke W. W. Identification of two types of keratin polypeptides within the acidic cytokeratin subfamily I. J Mol Biol. 1984 Oct 25;179(2):257–281. doi: 10.1016/0022-2836(84)90468-6. [DOI] [PubMed] [Google Scholar]
  34. Kaufmann E., Weber K., Geisler N. Intermediate filament forming ability of desmin derivatives lacking either the amino-terminal 67 or the carboxy-terminal 27 residues. J Mol Biol. 1985 Oct 20;185(4):733–742. doi: 10.1016/0022-2836(85)90058-0. [DOI] [PubMed] [Google Scholar]
  35. Kim K. H., Rheinwald J. G., Fuchs E. V. Tissue specificity of epithelial keratins: differential expression of mRNAs from two multigene families. Mol Cell Biol. 1983 Apr;3(4):495–502. doi: 10.1128/mcb.3.4.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kim K. H., Schwartz F., Fuchs E. Differences in keratin synthesis between normal epithelial cells and squamous cell carcinomas are mediated by vitamin A. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4280–4284. doi: 10.1073/pnas.81.14.4280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Krieg T. M., Schafer M. P., Cheng C. K., Filpula D., Flaherty P., Steinert P. M., Roop D. R. Organization of a type I keratin gene. Evidence for evolution of intermediate filaments from a common ancestral gene. J Biol Chem. 1985 May 25;260(10):5867–5870. [PubMed] [Google Scholar]
  38. Lazarides E. Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins. Annu Rev Biochem. 1982;51:219–250. doi: 10.1146/annurev.bi.51.070182.001251. [DOI] [PubMed] [Google Scholar]
  39. Lee M. G., Lewis S. A., Wilde C. D., Cowan N. J. Evolutionary history of a multigene family: an expressed human beta-tubulin gene and three processed pseudogenes. Cell. 1983 Jun;33(2):477–487. doi: 10.1016/0092-8674(83)90429-4. [DOI] [PubMed] [Google Scholar]
  40. Lehnert M. E., Jorcano J. L., Zentgraf H., Blessing M., Franz J. K., Franke W. W. Characterization of bovine keratin genes: similarities of exon patterns in genes coding for different keratins. EMBO J. 1984 Dec 20;3(13):3279–3287. doi: 10.1002/j.1460-2075.1984.tb02290.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lonberg N., Gilbert W. Intron/exon structure of the chicken pyruvate kinase gene. Cell. 1985 Jan;40(1):81–90. doi: 10.1016/0092-8674(85)90311-3. [DOI] [PubMed] [Google Scholar]
  42. Lusky M., Berg L., Weiher H., Botchan M. Bovine papilloma virus contains an activator of gene expression at the distal end of the early transcription unit. Mol Cell Biol. 1983 Jun;3(6):1108–1122. doi: 10.1128/mcb.3.6.1108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Magin T. M., Jorcano J. L., Franke W. W. Cytokeratin expression in simple epithelia. II. cDNA cloning and sequence characteristics of bovine cytokeratin A (no. 8). Differentiation. 1986;30(3):254–264. doi: 10.1111/j.1432-0436.1986.tb00788.x. [DOI] [PubMed] [Google Scholar]
  44. Magin T. M., Jorcano J. L., Franke W. W. Translational products of mRNAs coding for non-epidermal cytokeratins. EMBO J. 1983;2(8):1387–1392. doi: 10.1002/j.1460-2075.1983.tb01596.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Marchuk D., McCrohon S., Fuchs E. Complete sequence of a gene encoding a human type I keratin: sequences homologous to enhancer elements in the regulatory region of the gene. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1609–1613. doi: 10.1073/pnas.82.6.1609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Marchuk D., McCrohon S., Fuchs E. Remarkable conservation of structure among intermediate filament genes. Cell. 1984 Dec;39(3 Pt 2):491–498. doi: 10.1016/0092-8674(84)90456-2. [DOI] [PubMed] [Google Scholar]
  47. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  48. McKeon F. D., Kirschner M. W., Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986 Feb 6;319(6053):463–468. doi: 10.1038/319463a0. [DOI] [PubMed] [Google Scholar]
  49. McLachlan A. D., Karn J. Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature. 1982 Sep 16;299(5880):226–231. doi: 10.1038/299226a0. [DOI] [PubMed] [Google Scholar]
  50. McLachlan A. D., Stewart M. Tropomyosin coiled-coil interactions: evidence for an unstaggered structure. J Mol Biol. 1975 Oct 25;98(2):293–304. doi: 10.1016/s0022-2836(75)80119-7. [DOI] [PubMed] [Google Scholar]
  51. Moll R., Franke W. W., Schiller D. L., Geiger B., Krepler R. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell. 1982 Nov;31(1):11–24. doi: 10.1016/0092-8674(82)90400-7. [DOI] [PubMed] [Google Scholar]
  52. Moll R., Krepler R., Franke W. W. Complex cytokeratin polypeptide patterns observed in certain human carcinomas. Differentiation. 1983;23(3):256–269. doi: 10.1111/j.1432-0436.1982.tb01291.x. [DOI] [PubMed] [Google Scholar]
  53. Morris A., Steinberg M. L., Defendi V. Keratin gene expression in simian virus 40-transformed human keratinocytes. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8498–8502. doi: 10.1073/pnas.82.24.8498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Naora H., Deacon N. J. Relationship between the total size of exons and introns in protein-coding genes of higher eukaryotes. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6196–6200. doi: 10.1073/pnas.79.20.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  57. Parry D. A., Steven A. C., Steinert P. M. The coiled-coil molecules of intermediate filaments consist of two parallel chains in exact axial register. Biochem Biophys Res Commun. 1985 Mar 29;127(3):1012–1018. doi: 10.1016/s0006-291x(85)80045-0. [DOI] [PubMed] [Google Scholar]
  58. Perler F., Efstratiadis A., Lomedico P., Gilbert W., Kolodner R., Dodgson J. The evolution of genes: the chicken preproinsulin gene. Cell. 1980 Jun;20(2):555–566. doi: 10.1016/0092-8674(80)90641-8. [DOI] [PubMed] [Google Scholar]
  59. Quax W., Egberts W. V., Hendriks W., Quax-Jeuken Y., Bloemendal H. The structure of the vimentin gene. Cell. 1983 Nov;35(1):215–223. doi: 10.1016/0092-8674(83)90224-6. [DOI] [PubMed] [Google Scholar]
  60. Quax W., van den Broek L., Egberts W. V., Ramaekers F., Bloemendal H. Characterization of the hamster desmin gene: expression and formation of desmin filaments in nonmuscle cells after gene transfer. Cell. 1985 Nov;43(1):327–338. doi: 10.1016/0092-8674(85)90038-8. [DOI] [PubMed] [Google Scholar]
  61. Quinlan R. A., Cohlberg J. A., Schiller D. L., Hatzfeld M., Franke W. W. Heterotypic tetramer (A2D2) complexes of non-epidermal keratins isolated from cytoskeletons of rat hepatocytes and hepatoma cells. J Mol Biol. 1984 Sep 15;178(2):365–388. doi: 10.1016/0022-2836(84)90149-9. [DOI] [PubMed] [Google Scholar]
  62. Quinlan R. A., Schiller D. L., Hatzfeld M., Achtstätter T., Moll R., Jorcano J. L., Magin T. M., Franke W. W. Patterns of expression and organization of cytokeratin intermediate filaments. Ann N Y Acad Sci. 1985;455:282–306. doi: 10.1111/j.1749-6632.1985.tb50418.x. [DOI] [PubMed] [Google Scholar]
  63. Rheinwald J. G., O'Connell T. M. Intermediate filament proteins as distinguishing markers of cell type and differentiated state in cultured human urinary tract epithelia. Ann N Y Acad Sci. 1985;455:259–267. doi: 10.1111/j.1749-6632.1985.tb50416.x. [DOI] [PubMed] [Google Scholar]
  64. Rieger M., Jorcano J. L., Franke W. W. Complete sequence of a bovine type I cytokeratin gene: conserved and variable intron positions in genes of polypeptides of the same cytokeratin subfamily. EMBO J. 1985 Sep;4(9):2261–2267. doi: 10.1002/j.1460-2075.1985.tb03924.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  66. Romano V., Hatzfeld M., Magin T. M., Zimbelmann R., Franke W. W., Maier G., Ponstingl H. Cytokeratin expression in simple epithelia. I. Identification of mRNA coding for human cytokeratin no. 18 by a cDNA clone. Differentiation. 1986;30(3):244–253. doi: 10.1111/j.1432-0436.1986.tb00787.x. [DOI] [PubMed] [Google Scholar]
  67. Ruppert S., Scherer G., Schütz G. Recent gene conversion involving bovine vasopressin and oxytocin precursor genes suggested by nucleotide sequence. Nature. 1984 Apr 5;308(5959):554–557. doi: 10.1038/308554a0. [DOI] [PubMed] [Google Scholar]
  68. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Schiller D. L., Franke W. W., Geiger B. A subfamily of relatively large and basic cytokeratin polypeptides as defined by peptide mapping is represented by one or several polypeptides in epithelial cells. EMBO J. 1982;1(6):761–769. doi: 10.1002/j.1460-2075.1982.tb01243.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Schmidt W. N., Pardue R. L., Tutt M. C., Briggs R. C., Brinkley B. R., Hnilica L. S. Identification of cytokeratin antigens in Novikoff ascites hepatoma. Proc Natl Acad Sci U S A. 1982 May;79(10):3138–3142. doi: 10.1073/pnas.79.10.3138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Singer P. A., Trevor K., Oshima R. G. Molecular cloning and characterization of the Endo B cytokeratin expressed in preimplantation mouse embryos. J Biol Chem. 1986 Jan 15;261(2):538–547. [PubMed] [Google Scholar]
  72. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  73. Steinert P. M., Idler W. W., Goldman R. D. Intermediate filaments of baby hamster kidney (BHK-21) cells and bovine epidermal keratinocytes have similar ultrastructures and subunit domain structures. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4534–4538. doi: 10.1073/pnas.77.8.4534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Steinert P. M., Parry D. A., Idler W. W., Johnson L. D., Steven A. C., Roop D. R. 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. 1985 Jun 10;260(11):7142–7149. [PubMed] [Google Scholar]
  75. Steinert P. M., Rice R. H., Roop D. R., Trus B. L., Steven A. C. Complete amino acid sequence of a mouse epidermal keratin subunit and implications for the structure of intermediate filaments. Nature. 1983 Apr 28;302(5911):794–800. doi: 10.1038/302794a0. [DOI] [PubMed] [Google Scholar]
  76. Steinert P. M., Steven A. C., Roop D. R. The molecular biology of intermediate filaments. Cell. 1985 Sep;42(2):411–420. doi: 10.1016/0092-8674(85)90098-4. [DOI] [PubMed] [Google Scholar]
  77. Stone E. M., Rothblum K. N., Schwartz R. J. Intron-dependent evolution of chicken glyceraldehyde phosphate dehydrogenase gene. Nature. 1985 Feb 7;313(6002):498–500. doi: 10.1038/313498a0. [DOI] [PubMed] [Google Scholar]
  78. Strehler E. E., Mahdavi V., Periasamy M., Nadal-Ginard B. Intron positions are conserved in the 5' end region of myosin heavy-chain genes. J Biol Chem. 1985 Jan 10;260(1):468–471. [PubMed] [Google Scholar]
  79. Sun T. T., Green H. Immunofluorescent staining of keratin fibers in cultured cells. Cell. 1978 Jul;14(3):469–476. doi: 10.1016/0092-8674(78)90233-7. [DOI] [PubMed] [Google Scholar]
  80. Sun T. T., Tseng S. C., Huang A. J., Cooper D., Schermer A., Lynch M. H., Weiss R., Eichner R. Monoclonal antibody studies of mammalian epithelial keratins: a review. Ann N Y Acad Sci. 1985;455:307–329. doi: 10.1111/j.1749-6632.1985.tb50419.x. [DOI] [PubMed] [Google Scholar]
  81. Südhof T. C., Goldstein J. L., Brown M. S., Russell D. W. The LDL receptor gene: a mosaic of exons shared with different proteins. Science. 1985 May 17;228(4701):815–822. doi: 10.1126/science.2988123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Tseng S. C., Jarvinen M. J., Nelson W. G., Huang J. W., Woodcock-Mitchell J., Sun T. T. Correlation of specific keratins with different types of epithelial differentiation: monoclonal antibody studies. Cell. 1982 Sep;30(2):361–372. doi: 10.1016/0092-8674(82)90234-3. [DOI] [PubMed] [Google Scholar]
  83. Tyner A. L., Eichman M. J., Fuchs E. The sequence of a type II keratin gene expressed in human skin: conservation of structure among all intermediate filament genes. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4683–4687. doi: 10.1073/pnas.82.14.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Ueyama H., Hamada H., Battula N., Kakunaga T. Structure of a human smooth muscle actin gene (aortic type) with a unique intron site. Mol Cell Biol. 1984 Jun;4(6):1073–1078. doi: 10.1128/mcb.4.6.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Vasseur M., Duprey P., Brûlet P., Jacob F. One gene and one pseudogene for the cytokeratin endo A. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1155–1159. doi: 10.1073/pnas.82.4.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Weber K., Geisler N. Intermediate filaments: structural conservation and divergence. Ann N Y Acad Sci. 1985;455:126–143. doi: 10.1111/j.1749-6632.1985.tb50408.x. [DOI] [PubMed] [Google Scholar]
  88. Woods E. F. The number of polypeptide chains in the rod domain of bovine epidermal keratin. Biochem Int. 1983 Dec;7(6):769–774. [PubMed] [Google Scholar]
  89. Wu Y. J., Parker L. M., Binder N. E., Beckett M. A., Sinard J. H., Griffiths C. T., Rheinwald J. G. The mesothelial keratins: a new family of cytoskeletal proteins identified in cultured mesothelial cells and nonkeratinizing epithelia. Cell. 1982 Dec;31(3 Pt 2):693–703. doi: 10.1016/0092-8674(82)90324-5. [DOI] [PubMed] [Google Scholar]
  90. Wu Y. J., Rheinwald J. G. A new small (40 kd) keratin filament protein made by some cultured human squamous cell carcinomas. Cell. 1981 Sep;25(3):627–635. doi: 10.1016/0092-8674(81)90170-7. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES