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. 1986 Sep;83(17):6475–6479. doi: 10.1073/pnas.83.17.6475

Cloning of cDNA and amino acid sequence of a cytokeratin expressed in oocytes of Xenopus laevis.

J K Franz, W W Franke
PMCID: PMC386526  PMID: 2428034

Abstract

Using a cDNA clone from the ovary of the frog, Xenopus laevis, we have identified the mRNA and determined the complete amino acid sequence of a major cytoskeletal protein expressed in the oocyte. A comparison with other cytoskeletal proteins of Xenopus and mammals identifies this polypeptide Mr 55,700 as a nonepidermal kind of cytokeratin of the basic (type II) subfamily, which represents the amphibian equivalent to cytokeratin no. 8 of simple epithelia of higher mammals. The sequence data demonstrate the high evolutionary stability of this protein. This cytokeratin and its mRNA are present in oocytes, eggs, embryos, liver, and intestinal mucosa of adult frogs, as well as cultured kidney epithelial cells. We suggest that epithelial cell differentiation in early stages of Xenopus embryogenesis differs from other known pathways of cell differentiation in that major cell-type-specific proteins--i.e., cytokeratins of the simple epithelial type--and their mRNAs are maternally provided and distributed to early epithelial cells by special sorting mechanisms.

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Selected References

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

  1. Brûlet P., Babinet C., Kemler R., Jacob F. Monoclonal antibodies against trophectoderm-specific markers during mouse blastocyst formation. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4113–4117. doi: 10.1073/pnas.77.7.4113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Dawid I. B., Haynes S. R., Jamrich M., Jonas E., Miyatani S., Sargent T. D., Winkles J. A. Gene expression in Xenopus embryogenesis. J Embryol Exp Morphol. 1985 Nov;89 (Suppl):113–124. [PubMed] [Google Scholar]
  3. Duprey P., Morello D., Vasseur M., Babinet C., Condamine H., Brûlet P., Jacob F. Expression of the cytokeratin endo A gene during early mouse embryogenesis. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8535–8539. doi: 10.1073/pnas.82.24.8535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ellison T. R., Mathisen P. M., Miller L. Developmental changes in keratin patterns during epidermal maturation. Dev Biol. 1985 Dec;112(2):329–337. doi: 10.1016/0012-1606(85)90403-8. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. Freudenstein C., Franke W. W., Osborn M., Weber K. Reaction of tonofilament-like intermediate-sized filaments with antibodies raised against isolated defined polypeptides of bovine hoof prekeratin. Cell Biol Int Rep. 1978 Nov;2(6):591–600. doi: 10.1016/0309-1651(78)90068-1. [DOI] [PubMed] [Google Scholar]
  8. Fuchs E., Marchuk D. Type I and type II keratins have evolved from lower eukaryotes to form the epidermal intermediate filaments in mammalian skin. Proc Natl Acad Sci U S A. 1983 Oct;80(19):5857–5861. doi: 10.1073/pnas.80.19.5857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Glass C., Kim K. H., Fuchs E. Sequence and expression of a human type II mesothelial keratin. J Cell Biol. 1985 Dec;101(6):2366–2373. doi: 10.1083/jcb.101.6.2366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Godsave S. F., Anderton B. H., Heasman J., Wylie C. C. Oocytes and early embryos of Xenopus laevis contain intermediate filaments which react with anti-mammalian vimentin antibodies. J Embryol Exp Morphol. 1984 Oct;83:169–187. [PubMed] [Google Scholar]
  12. Godsave S. F., Wylie C. C., Lane E. B., Anderton B. H. Intermediate filaments in the Xenopus oocyte: the appearance and distribution of cytokeratin-containing filaments. J Embryol Exp Morphol. 1984 Oct;83:157–167. [PubMed] [Google Scholar]
  13. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  14. Gurdon J. B., Brennan S., Fairman S., Mohun T. J. Transcription of muscle-specific actin genes in early Xenopus development: nuclear transplantation and cell dissociation. Cell. 1984 Oct;38(3):691–700. doi: 10.1016/0092-8674(84)90264-2. [DOI] [PubMed] [Google Scholar]
  15. Gurdon J. B., Mohun T. J., Brennan S., Cascio S. Actin genes in Xenopus and their developmental control. J Embryol Exp Morphol. 1985 Nov;89 (Suppl):125–136. [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Hoffmann W., Franz J. K., Franke W. W. Amino acid sequence microheterogeneities of basic (type II) cytokeratins of Xenopus laevis epidermis and evolutionary conservativity of helical and non-helical domains. J Mol Biol. 1985 Aug 20;184(4):713–724. doi: 10.1016/0022-2836(85)90315-8. [DOI] [PubMed] [Google Scholar]
  19. Jackson B. W., Grund C., Schmid E., Bürki K., Franke W. W., Illmensee K. Formation of cytoskeletal elements during mouse embryogenesis. Intermediate filaments of the cytokeratin type and desmosomes in preimplantation embryos. Differentiation. 1980;17(3):161–179. doi: 10.1111/j.1432-0436.1980.tb01093.x. [DOI] [PubMed] [Google Scholar]
  20. Jackson B. W., Grund C., Winter S., Franke W. W., Illmensee K. Formation of cytoskeletal elements during mouse embryogenesis. II. Epithelial differentiation and intermediate-sized filaments in early postimplantation embryos. Differentiation. 1981;20(3):203–216. doi: 10.1111/j.1432-0436.1981.tb01177.x. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. 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]
  25. 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]
  26. 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]
  27. 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]
  28. Mohun T. J., Brennan S., Dathan N., Fairman S., Gurdon J. B. Cell type-specific activation of actin genes in the early amphibian embryo. Nature. 1984 Oct 25;311(5988):716–721. doi: 10.1038/311716a0. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Nelson W. J., Traub P. Intermediate (10 nm) filament proteins and the Ca2+-activated proteinase specific for vimentin and desmin in the cells from fish to man: an example of evolutionary conservation. J Cell Sci. 1982 Oct;57:25–49. doi: 10.1242/jcs.57.1.25. [DOI] [PubMed] [Google Scholar]
  31. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell. 1982 Oct;30(3):675–686. doi: 10.1016/0092-8674(82)90272-0. [DOI] [PubMed] [Google Scholar]
  32. Newport J., Kirschner M. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell. 1982 Oct;30(3):687–696. doi: 10.1016/0092-8674(82)90273-2. [DOI] [PubMed] [Google Scholar]
  33. Oshima R. G. Developmental expression of murine extra-embryonic endodermal cytoskeletal proteins. J Biol Chem. 1982 Apr 10;257(7):3414–3421. [PubMed] [Google Scholar]
  34. Perry M. M. Microfilaments in the external surface layer of the early amphibian embryo. J Embryol Exp Morphol. 1975 Feb;33(1):127–146. [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Sargent T. D., Dawid I. B. Differential gene expression in the gastrula of Xenopus laevis. Science. 1983 Oct 14;222(4620):135–139. doi: 10.1126/science.6688681. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. 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]

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