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PMID: 8138568 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

IFAP 300 is common to desmosomes and hemidesmosomes and is a possible linker of intermediate filaments to these junctions.

The Journal of cell biology ·Vol. 125 ·No. 1 ·1994-04-00 ·Pages 159-70

Skalli O, Jones JC, Gagescu R, Goldman RD

Abstract

The distribution of IFAP 300, a protein previously characterized as cross-linking vimentin intermediate filaments (IF), has been investigated in epithelial cells. In frozen sections of bovine tongue epithelium the staining obtained with IFAP 300 antibodies is concentrated in the peripheral cytoplasm of keratinocytes, including the entire peripheral region of basal cells. Further immunofluorescence studies reveal that in primary cultures of mouse keratinocytes the distribution of IFAP 300 is similar to that of the desmosomal protein desmoplakin. In rat bladder carcinoma 804G cells the staining pattern of IFAP 300 antibodies coincides with that obtained with antibodies against the hemidesmosomal protein BP 230. By immunogold electron microscopy IFAP 300 is mainly located at sites where IF appear to attach to desmosomes and hemidesmosomes. Morphometric analyses of the distribution of the gold particles show that IFAP 300 overlaps with desmoplakin and BP 230, but also that it extends deeper into the cytoplasm than these latter two proteins. The staining reaction seen in epithelial cells by immunofluorescence and immunogold is specific for IFAP 300 as shown by immunoblotting. Immunoblotting also reveals that IFAP 300 is present in both cell-free preparations of desmosomes and hemidesmosomes. These morphological and biochemical results are intriguing since, in recent years, the proteins appearing in these two types of junctions have been found to be different. One possible exception is plectin, a protein that has been suggested to be very similar to IFAP 300. However, we show here that IFAP 300 differs from plectin in several respects, including differences at the primary sequence level. We also show that purified IFAP 300 pellets with in vitro polymerized IF prepared from desmosome-associated keratins under conditions in which IFAP 300 alone is not sedimentable. This indicates that IFAP 300 can associate with keratin IF. These data, taken together with the immunogold results, suggest that IFAP 300 functions in epithelial cells as a linker protein connecting IF to desmosomes as well as to hemidesmosomes, possibly through structurally related proteins such as desmoplakin and BP 230, respectively.

MeSH Terms
Amino Acid Sequence Animals Cattle Cricetinae Desmosomes/ultrastructure Fluorescent Antibody Technique Immunohistochemistry Intermediate Filament Proteins/metabolism,physiology Intermediate Filaments/ultrastructure Mice Mice, Inbred BALB C Molecular Sequence Data Plectin Rats Sequence Alignment Sequence Homology, Amino Acid
Chemicals
Intermediate Filament Proteins Plec protein, mouse Plec protein, rat Plectin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Skalli O
Department of Cell, Molecular, and Structural Biology, Northwestern University Medical School, Chicago, Illinois 60611.
Jones J C
Gagescu R
Goldman R D
References (62)
62 references, click to expand
  1. Cell cycle-dependent changes in the organization of an intermediate filament-associated protein: correlation with phosphorylation by p34cdc2.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11959-63 PMID: 1281546
  2. Identification of a new hemidesmosomal protein, HD1: a major, high molecular mass component of isolated hemidesmosomes.
    J Cell Biol. 1992 Mar;116(6):1497-506 PMID: 1541639
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Cytoplasmic network arrays demonstrated by immunolocalization using antibodies to a high molecular weight protein present in cytoskeletal preparations from cultured cells.
    Exp Cell Res. 1982 Mar;138(1):15-29 PMID: 7040089
  5. A 300,000-mol-wt intermediate filament-associated protein in baby hamster kidney (BHK-21) cells.
    J Cell Biol. 1985 Feb;100(2):620-31 PMID: 3881459
  6. A mutation in the conserved helix termination peptide of keratin 5 in hereditary skin blistering.
    Nature. 1992 Mar 19;356(6366):244-6 PMID: 1372711
  7. Efficient isolation of genes by using antibody probes.
    Proc Natl Acad Sci U S A. 1983 Mar;80(5):1194-8 PMID: 6219389
  8. Purification of the 300K intermediate filament-associated protein and its in vitro recombination with intermediate filaments.
    J Cell Biol. 1985 Sep;101(3):802-13 PMID: 3897249
  9. A function for keratins and a common thread among different types of epidermolysis bullosa simplex diseases.
    J Cell Biol. 1991 Dec;115(6):1661-74 PMID: 1721910
  10. Production of rabbit antibodies against carboxy-terminal epitopes encoded by bullous pemphigoid cDNA.
    J Invest Dermatol. 1990 May;94(5):617-23 PMID: 1691240
  11. Plectin and IFAP-300K are homologous proteins binding to microtubule-associated proteins 1 and 2 and to the 240-kilodalton subunit of spectrin.
    J Biol Chem. 1987 Jan 25;262(3):1320-5 PMID: 3027087
  12. Formation of hemidesmosomes in vitro by a transformed rat bladder cell line.
    J Cell Biol. 1991 Jan;112(1):159-68 PMID: 1986003
  13. Structure and function of intercellular junctions.
    Int Rev Cytol. 1974;39:191-283 PMID: 4611943
  14. Cloning and sequencing of rat plectin indicates a 466-kD polypeptide chain with a three-domain structure based on a central alpha-helical coiled coil.
    J Cell Biol. 1991 Jul;114(1):83-99 PMID: 2050743
  15. Demonstration of intra- and extracellular localization of bullous pemphigoid antigen using cryofixation and freeze substitution for postembedding immunoelectron microscopy.
    Arch Dermatol Res. 1989;281(7):443-8 PMID: 2610516
  16. A function for the integrin alpha 6 beta 4 in the hemidesmosome.
    Cell Regul. 1991 Jun;2(6):427-38 PMID: 1883873
  17. Is the hemidesmosome a half desmosome? An immunological comparison of mammalian desmosomes and hemidesmosomes.
    Cell Motil Cytoskeleton. 1986;6(6):560-9 PMID: 3542242
  18. Localisation of the protein and glycoprotein components of bovine nasal epithelial desmosomes by immunoelectron microscopy.
    EMBO J. 1987 Apr;6(4):885-9 PMID: 3595561
  19. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  20. Intermediate filament-associated proteins.
    Curr Opin Cell Biol. 1991 Feb;3(1):75-81 PMID: 1854487
  21. High molecular weight polypeptides (270,000-340,000) from cultured cells are related to hog brain microtubule-associated proteins but copurify with intermediate filaments.
    Proc Natl Acad Sci U S A. 1980 Aug;77(8):4808-12 PMID: 6933530
  22. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  23. Desmocalmin: a calmodulin-binding high molecular weight protein isolated from desmosomes.
    J Cell Biol. 1985 Dec;101(6):2070-80 PMID: 2415534
  24. Epidermolysis bullosa simplex: evidence in two families for keratin gene abnormalities.
    Science. 1991 Nov 22;254(5035):1202-5 PMID: 1720261
  25. Comparative structural analysis of desmoplakin, bullous pemphigoid antigen and plectin: members of a new gene family involved in organization of intermediate filaments.
    Int J Biol Macromol. 1992 Jun;14(3):145-53 PMID: 1390446
  26. Desmoplakin I and desmoplakin II. Purification and characterization.
    J Biol Chem. 1989 May 15;264(14):8310-8 PMID: 2470743
  27. Point mutations in human keratin 14 genes of epidermolysis bullosa simplex patients: genetic and functional analyses.
    Cell. 1991 Sep 20;66(6):1301-11 PMID: 1717157
  28. Cytoskeletal components of lymphoid organs. I. Synthesis of cytokeratins 8 and 18 and desmin in subpopulations of extrafollicular reticulum cells of human lymph nodes, tonsils, and spleen.
    Differentiation. 1987;36(2):145-63 PMID: 2452110
  29. Isolation of epidermal desmosomes.
    J Cell Biol. 1974 Nov;63(2 Pt 1):515-23 PMID: 4138144
  30. Isolation and symmetrical splitting of desmosomal structures in 9 M urea.
    Eur J Cell Biol. 1983 Nov;32(1):117-30 PMID: 6686818
  31. Structure of the human desmoplakins. Implications for function in the desmosomal plaque.
    J Biol Chem. 1990 Feb 15;265(5):2603-12 PMID: 1689290
  32. Antigenic interrelationship between the 40-kilodalton cytokeratin polypeptide and desmoplakins.
    Cell Motil Cytoskeleton. 1986;6(6):628-39 PMID: 2433058
  33. The hemidesmosomal plaque. I. Characterization of a major constituent protein as a differentiation marker for certain forms of epithelia.
    Differentiation. 1990 Dec;45(3):207-20 PMID: 2090522
  34. Identification of plectin in different human cell types and immunolocalization at epithelial basal cell surface membranes.
    Exp Cell Res. 1984 Nov;155(1):43-9 PMID: 6386498
  35. Evidence for heterogeneity in the 160/165 x 10(3) Mr glycoprotein components of desmosomes.
    J Cell Sci. 1987 Nov;88 ( Pt 4):513-20 PMID: 3332672
  36. The internal affairs of an integrin.
    Trends Cell Biol. 1991 Jul;1(1):2-4 PMID: 14731802
  37. Isolation of complementary DNA for bullous pemphigoid antigen by use of patients' autoantibodies.
    J Clin Invest. 1988 Dec;82(6):1864-70 PMID: 2461961
  38. Desmoplakins of epithelial and myocardial desmosomes are immunologically and biochemically related.
    Differentiation. 1982;23(2):115-27 PMID: 6762309
  39. Alpha 6 beta 4 integrin heterodimer is a component of hemidesmosomes.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8970-4 PMID: 2247472
  40. Intermediate filament-plasma membrane interactions.
    Curr Opin Cell Biol. 1991 Feb;3(1):127-32 PMID: 1854477
  41. Desmosomes and hemidesmosomes.
    Curr Opin Cell Biol. 1993 Feb;5(1):30-40 PMID: 8448028
  42. On the molecular organization, diversity and functions of desmosomal proteins.
    Ciba Found Symp. 1987;125:3-25 PMID: 2435471
  43. Mutant keratin expression in transgenic mice causes marked abnormalities resembling a human genetic skin disease.
    Cell. 1991 Jan 25;64(2):365-80 PMID: 1703046
  44. Calcium regulation of growth and differentiation of mouse epidermal cells in culture.
    Cell. 1980 Jan;19(1):245-54 PMID: 6153576
  45. Desmosomes and hemidesmosomes: constitutive molecular components.
    Annu Rev Cell Biol. 1990;6:461-91 PMID: 2275820
  46. Dynamic aspects of the supramolecular organization of intermediate filament networks in cultured epidermal cells.
    Cell Motil. 1982;2(3):197-213 PMID: 6756644
  47. Occurrence and immunolocalization of plectin in tissues.
    J Cell Biol. 1983 Sep;97(3):887-901 PMID: 6350322
  48. A protein antigenically related to nuclear lamin B mediates the association of intermediate filaments with desmosomes.
    J Cell Biol. 1990 Aug;111(2):581-8 PMID: 2199461
  49. Further analyses of epitopes for human monoclonal anti-basement membrane zone antibodies produced by stable human hybridoma cell lines constructed with Epstein-Barr virus transformants.
    J Invest Dermatol. 1993 Mar;100(3):310-5 PMID: 7680057
  50. Monoclonal antibody mapping of structural and functional plectin epitopes.
    J Cell Biol. 1991 Feb;112(3):397-405 PMID: 1704007
  51. Biochemical and immunological characterization of desmoplakins I and II, the major polypeptides of the desmosomal plaque.
    J Mol Biol. 1983 Feb 5;163(4):647-71 PMID: 6341602
  52. Biochemical and immunological analysis of rapidly purified 10-nm filaments from baby hamster kidney (BHK-21) cells.
    J Cell Biol. 1978 Jul;78(1):93-109 PMID: 566763
  53. Identification of a basic protein of Mr 75,000 as an accessory desmosomal plaque protein in stratified and complex epithelia.
    J Cell Biol. 1988 May;106(5):1679-91 PMID: 3131348
  54. Immunochemical characterization of three components of the hemidesmosome and their expression in cultured epithelial cells.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3377-90 PMID: 2689457
  55. Intermediate filaments and the initiation of desmosome assembly.
    J Cell Biol. 1985 Aug;101(2):506-17 PMID: 3894376
  56. Altered differentiation of mouse epidermal cells treated with retinyl acetate in vitro.
    Exp Cell Res. 1974 May;86(1):95-105 PMID: 4857507
  57. Peptide mapping.
    Methods Enzymol. 1990;182:613-26 PMID: 2179669
  58. The desmoplakin carboxyl terminus coaligns with and specifically disrupts intermediate filament networks when expressed in cultured cells.
    J Cell Biol. 1992 Mar;116(5):1197-209 PMID: 1740472
  59. Comparison of molecularly cloned bullous pemphigoid antigen to desmoplakin I confirms that they define a new family of cell adhesion junction plaque proteins.
    J Biol Chem. 1991 Jul 5;266(19):12555-9 PMID: 1712022
  60. Intermediate filament networks: organization and possible functions of a diverse group of cytoskeletal elements.
    J Cell Sci Suppl. 1986;5:69-97 PMID: 3308919
  61. Cytokeratin filaments and desmosomes in the epithelioid cells of the perineurial and arachnoidal sheaths of some vertebrate species.
    Differentiation. 1989 May;40(2):129-49 PMID: 2474473
  62. Fractionation of desmosomes and comparison of the polypeptide composition of desmosomes prepared from two bovine epithelial tissues.
    J Cell Biochem. 1988 Mar;36(3):223-36 PMID: 2454237
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-04-00
Pages
159-70
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120004
Subset
IM
Grants
NIGMS NIH HHS · GM 36806 · United States
NIGMS NIH HHS · GM 38470 · United States
Databases
GENBANK
X77631
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