Home LiteratureArticle Details
PMID: 1720124 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Intermediate filaments formed de novo from tail-less cytokeratins in the cytoplasm and in the nucleus.

The Journal of cell biology ·Vol. 115 ·No. 5 ·1991-12-00 ·Pages 1293-307

Bader BL, Magin TM, Freudenmann M, Stumpp S, Franke WW

Abstract

The roles of the different molecular domains of intermediate filament (IF) proteins in the assembly and higher order organization of IF structures have recently been studied by various groups but with partially controversial results. To examine the requirement of the aminoterminal (head) and the carboxyterminal (tail) domain of cytokeratins (CKs) for de novo IF formation in the living cell, we have constructed cDNAs coding for intact as well as head- and/or tail-less human CKs 8 and 18 and the naturally tail-less human CK 19, all under the control of the human beta-actin promoter. After transient and stable transfections of mouse 3T3-L1 cells, which are devoid of any CKs, we have studied, with such constructs, the resulting gene products by gel electrophoresis and immunolocalization techniques. By light and electron microscopy we show that extended cytoplasmic IF meshworks are formed from pairs of the type II CK 8 with the type I CKs 18 or 19 as well as from pairs of tail-less CK 8 with tail-less CKs 18 or 19 in the transfected cells, proving that the absence of the tail domain in both types of CKs does not prevent the de novo formation of regular IFs. Most surprisingly, however, we have observed spectacular alterations in the nucleocytoplasmic distribution of the IFs formed from tail-less CKs. In many of the transfected cells, a large part, or all, of the detectable CKs was found to occur in extensive IF bundles in the nucleoplasm. Intranuclear accumulations of CK deposits, however mostly nonfibrillar, were also observed when the cells had been transfected with cDNAs encoding tail-less CKs also lacking their head domains, whereas CKs deleted only in the head domain were found exclusively in the cytoplasm. The specific domain requirements for the assembly of cytoplasmic IF bundles are discussed and possible mechanisms of intranuclear accumulation of IFs are proposed.

MeSH Terms
3T3 Cells Amino Acid Sequence Animals Base Sequence Cell Nucleus/metabolism,ultrastructure Cloning, Molecular Cytoplasm/metabolism,ultrastructure DNA Fluorescent Antibody Technique Humans Intermediate Filaments/metabolism Keratins/metabolism Mice Microscopy, Electron Molecular Sequence Data Transfection
Chemicals
Keratins DNA
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Bader B L
Institute of Cell and Tumor Biology, German Cancer Research Center, Heidelberg.
Magin T M
Freudenmann M
Stumpp S
Franke W W
References (70)
70 references, click to expand
  1. Cloning of the human keratin 18 gene and its expression in nonepithelial mouse cells.
    Mol Cell Biol. 1988 Apr;8(4):1540-50 PMID: 2454392
  2. Cytokeratin domains involved in heterotypic complex formation determined by in-vitro binding assays.
    J Mol Biol. 1987 Sep 20;197(2):237-55 PMID: 2445997
  3. The expression of mutant epidermal keratin cDNAs transfected in simple epithelial and squamous cell carcinoma lines.
    J Cell Biol. 1987 Aug;105(2):791-806 PMID: 2442174
  4. Identification of the conserved, conformation-dependent cytokeratin epitope recognized by monoclonal antibody (lu-5).
    Virchows Arch A Pathol Anat Histopathol. 1987;411(2):137-47 PMID: 2440176
  5. The human keratin genes and their differential expression.
    Curr Top Dev Biol. 1987;22:5-34 PMID: 2443316
  6. A human beta-actin expression vector system directs high-level accumulation of antisense transcripts.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4831-5 PMID: 2440031
  7. Molecular interactions in paracrystals of a fragment corresponding to the alpha-helical coiled-coil rod portion of glial fibrillary acidic protein: evidence for an antiparallel packing of molecules and polymorphism related to intermediate filament structure.
    J Cell Biol. 1989 Jul;109(1):225-34 PMID: 2745549
  8. Intermediate filament formation after transfection with modified hamster vimentin and desmin genes.
    J Cell Sci. 1987 Nov;88 ( Pt 4):475-82 PMID: 3332670
  9. Plakoglobin: a protein common to different kinds of intercellular adhering junctions.
    Cell. 1986 Sep 26;46(7):1063-73 PMID: 3530498
  10. 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):733-42 PMID: 3903168
  11. Conformity and diversity in the structures of intermediate filaments.
    Ann N Y Acad Sci. 1985;455:371-80 PMID: 3866509
  12. Identification of a distinct soluble subunit of an intermediate filament protein: tetrameric vimentin from living cells.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):7929-33 PMID: 3865206
  13. Intermediate filament assembly and stability in vitro: effect and implications of the removal of head and tail domains of vimentin by the human immunodeficiency virus type 1 protease.
    Cell Biol Int Rep. 1990 Jul;14(7):583-94 PMID: 2203542
  14. Retrovirus-mediated transgenic keratin expression in cultured fibroblasts: specific domain functions in keratin stabilization and filament formation.
    Cell. 1990 Aug 24;62(4):681-96 PMID: 1696851
  15. Identification of protein IT of the intestinal cytoskeleton as a novel type I cytokeratin with unusual properties and expression patterns.
    J Cell Biol. 1990 Aug;111(2):567-80 PMID: 1696264
  16. Organization and sequence of the human gene encoding cytokeratin 8.
    Gene. 1990 Feb 14;86(2):241-9 PMID: 1691124
  17. Increase in a 55-kDa keratin-like protein in the nuclear matrix of rat liver cells during proliferative activation.
    Exp Cell Res. 1990 Feb;186(2):346-53 PMID: 1688805
  18. Localization of newly synthesized vimentin subunits reveals a novel mechanism of intermediate filament assembly.
    Cell. 1990 Feb 9;60(3):415-27 PMID: 2406021
  19. Molecular architecture of the neurofilament. II. Reassembly process of neurofilament L protein in vitro.
    J Mol Biol. 1990 Feb 20;211(4):871-82 PMID: 2313699
  20. Disruption of the keratin filament network during epithelial cell division.
    EMBO J. 1982;1(11):1365-72 PMID: 6202508
  21. 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 PMID: 6296171
  22. Involvement of the N-terminal polypeptide of vimentin in the formation of intermediate filaments.
    J Cell Sci. 1983 Sep;63:43-67 PMID: 6313713
  23. Association of cytokeratin p39 with DNA in intact Novikoff hepatoma cells.
    Proc Natl Acad Sci U S A. 1984 Jan;81(2):419-23 PMID: 6198648
  24. Monoclonal cytokeratin antibody recognizing a heterotypic complex: immunological probing of conformational states of cytoskeletal proteins in filaments and in solution.
    Exp Cell Res. 1987 Nov;173(1):17-37 PMID: 2445593
  25. Analysis of cytokeratin domains by cloning and expression of intact and deleted polypeptides in Escherichia coli.
    EMBO J. 1987 Sep;6(9):2607-15 PMID: 2445561
  26. Cytokeratin expression in simple epithelia. III. Detection of mRNAs encoding human cytokeratins nos. 8 and 18 in normal and tumor cells by hybridization with cDNA sequences in vitro and in situ.
    Differentiation. 1986;33(1):69-85 PMID: 2434381
  27. Comparison of mouse and human keratin 18: a component of intermediate filaments expressed prior to implantation.
    Differentiation. 1986;33(1):61-8 PMID: 2434380
  28. The transfection of epidermal keratin genes into fibroblasts and simple epithelial cells: evidence for inducing a type I keratin by a type II gene.
    Cell. 1987 Feb 13;48(3):453-63 PMID: 2433047
  29. Amino acid sequence and gene organization of cytokeratin no. 19, an exceptional tail-less intermediate filament protein.
    EMBO J. 1986 Aug;5(8):1865-75 PMID: 2428612
  30. Nuclear lamin proteins: domains required for nuclear targeting, assembly, and cell-cycle-regulated dynamics.
    Curr Opin Cell Biol. 1991 Feb;3(1):82-6 PMID: 1854488
  31. How proteins enter the nucleus.
    Cell. 1991 Feb 8;64(3):489-97 PMID: 1991319
  32. Assembly of amino-terminally deleted desmin in vimentin-free cells.
    J Cell Biol. 1990 Nov;111(5 Pt 1):1971-85 PMID: 1699950
  33. Assembly properties of dominant and recessive mutations in the small mouse neurofilament (NF-L) subunit.
    J Cell Biol. 1990 Nov;111(5 Pt 1):2005-19 PMID: 2121744
  34. Characterization of dominant and recessive assembly-defective mutations in mouse neurofilament NF-M.
    J Cell Biol. 1990 Nov;111(5 Pt 1):1987-2003 PMID: 2121743
  35. Disruption of keratin filaments in embryonic epithelial cell types.
    New Biol. 1990 Nov;2(11):1004-14 PMID: 1714295
  36. De novo formation of cytokeratin filaments in calf lens cells and cytoplasts after transfection with cDNAs or microinjection with mRNAs encoding human cytokeratins.
    Eur J Cell Biol. 1990 Dec;53(2):333-48 PMID: 1706999
  37. Deletions in epidermal keratins leading to alterations in filament organization in vivo and in intermediate filament assembly in vitro.
    J Cell Biol. 1990 Dec;111(6 Pt 2):3049-64 PMID: 1702787
  38. Tailless keratins assemble into regular intermediate filaments in vitro.
    J Cell Sci. 1990 Oct;97 ( Pt 2):317-24 PMID: 1703550
  39. Properties of the desmin tail domain: studies using synthetic peptides and antipeptide antibodies.
    J Cell Biol. 1990 Nov;111(5 Pt 1):2063-75 PMID: 2229186
  40. Location of nuclear antigen(s) recognized by DSB389 MAb, a monoclonal antibody against desmin, observed by confocal laser scanning fluorescence microscopy.
    Cell Biol Int Rep. 1990 Aug;14(8):727-36 PMID: 2225085
  41. Structure of the peripheral domains of neurofilaments revealed by low angle rotary shadowing.
    J Mol Biol. 1988 Jul 20;202(2):297-305 PMID: 3172218
  42. Molecular and cellular biology of intermediate filaments.
    Annu Rev Biochem. 1988;57:593-625 PMID: 3052284
  43. Cytokeratins and cytokeratin filaments in subpopulations of cultured human and rodent cells of nonepithelial origin: modes and patterns of formation.
    Differentiation. 1989 Dec;42(2):81-102 PMID: 2483839
  44. Spontaneous losses of control of cytokeratin gene expression in transformed, non-epithelial human cells occurring at different levels of regulation.
    Cell. 1989 Oct 6;59(1):67-79 PMID: 2477157
  45. Isolation, sequence, and expression of a human keratin K5 gene: transcriptional regulation of keratins and insights into pairwise control.
    Mol Cell Biol. 1989 Sep;9(9):3685-97 PMID: 2476664
  46. Low level expression of cytokeratins 8, 18 and 19 in vascular smooth muscle cells of human umbilical cord and in cultured cells derived therefrom, with an analysis of the chromosomal locus containing the cytokeratin 19 gene.
    Eur J Cell Biol. 1988 Dec;47(2):300-19 PMID: 2468493
  47. 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):1826-41 PMID: 2414304
  48. Expression in Escherichia coli of fragments of glial fibrillary acidic protein: characterization, assembly properties and paracrystal formation.
    J Cell Sci. 1989 May;93 ( Pt 1):71-83 PMID: 2693466
  49. Assembly properties of two CNBr fragments of avian desmin that correspond to the headpiece domain and helix 1B.
    Biochem Biophys Res Commun. 1989 Dec 29;165(3):1059-66 PMID: 2610680
  50. Integration of different keratins into the same filament system after microinjection of mRNA for epidermal keratins into kidney epithelial cells.
    Cell. 1984 Apr;36(4):813-25 PMID: 6200235
  51. Assembly of keratin onto PtK1 cytoskeletons: evidence for an intermediate filament organizing center.
    J Cell Biol. 1982 Feb;92(2):575-8 PMID: 6174532
  52. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells.
    Cell. 1982 Nov;31(1):11-24 PMID: 6186379
  53. De novo synthesis and specific assembly of keratin filaments in nonepithelial cells after microinjection of mRNA for epidermal keratin.
    Cell. 1983 Apr;32(4):1125-37 PMID: 6188536
  54. Dimethylsulfoxide and the ionophore A23187 affect the arrangement of actin and induce nuclear actin paracrystals in PtK2 cells.
    Exp Cell Res. 1980 Sep;129(1):103-14 PMID: 6775963
  55. Intermediate filament proteins in nonfilamentous structures: transient disintegration and inclusion of subunit proteins in granular aggregates.
    Cell. 1982 Aug;30(1):103-13 PMID: 6751555
  56. 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 1:431-53 PMID: 7049531
  57. Reversible translocation of cytoplasmic actin into the nucleus caused by dimethyl sulfoxide.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5268-72 PMID: 7001475
  58. Proteinchemical characterization of three structurally distinct domains along the protofilament unit of desmin 10 nm filaments.
    Cell. 1982 Aug;30(1):277-86 PMID: 6889923
  59. Antibody to prekeratin. Decoration of tonofilament like arrays in various cells of epithelial character.
    Exp Cell Res. 1978 Oct 15;116(2):429-45 PMID: 361424
  60. Nuclear actin bundles in Amoeba, Dictyostelium and human HeLa cells induced by dimethyl sulfoxide.
    Exp Cell Res. 1979 May;120(2):451-5 PMID: 571346
  61. An established pre-adipose cell line and its differentiation in culture.
    Cell. 1974 Oct;3(2):127-33 PMID: 4426090
  62. Posttranslational regulation of keratins: degradation of mouse and human keratins 18 and 8.
    Mol Cell Biol. 1989 Apr;9(4):1553-65 PMID: 2471065
  63. Expression of mutant keratin cDNAs in epithelial cells reveals possible mechanisms for initiation and assembly of intermediate filaments.
    J Cell Biol. 1989 Apr;108(4):1477-93 PMID: 2466849
  64. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998-9002 PMID: 2461560
  65. Patterns of expression of trichocytic and epithelial cytokeratins in mammalian tissues. I. Human and bovine hair follicles.
    Differentiation. 1988;37(2):137-57 PMID: 2456239
  66. Synthesis and fate of keratins 8 and 18 in nonepithelial cells transfected with cDNA.
    Exp Cell Res. 1988 Dec;179(2):352-61 PMID: 2461310
  67. Sequence of cDNA coding for human keratin 19.
    Nucleic Acids Res. 1987 Dec 10;15(23):10058 PMID: 2447559
  68. Molecular characterization and expression of the stratification-related cytokeratins 4 and 15.
    J Cell Biol. 1988 Apr;106(4):1249-61 PMID: 2452170
  69. Soluble cytokeratins in Xenopus laevis oocytes and eggs.
    Biol Cell. 1987;61(1-2):33-8 PMID: 2451957
  70. Sequence of the human 40-kDa keratin reveals an unusual structure with very high sequence identity to the corresponding bovine keratin.
    Proc Natl Acad Sci U S A. 1988 Feb;85(4):1114-8 PMID: 2448790
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1991-12-00
Pages
1293-307
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2289233
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]