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PMID: 8207063 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Liver-intestine cadherin: molecular cloning and characterization of a novel Ca(2+)-dependent cell adhesion molecule expressed in liver and intestine.

The Journal of cell biology ·Vol. 125 ·No. 6 ·1994-06-00 ·Pages 1353-69

Berndorff D, Gessner R, Kreft B, Schnoy N, Lajous-Petter AM, Loch N, Reutter W, Hortsch M, Tauber R

Abstract

A novel member of the cadherin family of cell adhesion molecules has been characterized by cloning from rat liver, sequencing of the corresponding cDNA, and functional analysis after heterologous expression in nonadhesive S2 cells. cDNA clones were isolated using a polyclonal antibody inhibiting Ca(2+)-dependent intercellular adhesion of hepatoma cells. As inferred from the deduced amino acid sequence, the novel molecule has homologies with E-, P-, and N-cadherins, but differs from these classical cadherins in four characteristics. Its extracellular domain is composed of five homologous repeated domains instead of four characteristic for the classical cadherins. Four of the five domains are characterized by the sequence motifs DXNDN and DXD or modifications thereof representing putative Ca(2+)-binding sites of classical cadherins. In its NH2-terminal region, this cadherin lacks both the precursor segment and the endogenous protease cleavage site RXKR found in classical cadherins. In the extracellular EC1 domain, the novel cadherin contains an AAL sequence in place of the HAV sequence motif representing the common cell adhesion recognition sequence of E-, P-, and N-cadherin. In contrast to the conserved cytoplasmic domain of classical cadherins with a length of 150-160 amino acid residues, that of the novel cadherin has only 18 amino acids. Examination of transfected S2 cells showed that despite these structural differences, this cadherin mediates intercellular adhesion in a Ca(2+)-dependent manner. The novel cadherin is solely expressed in liver and intestine and was, hence, assigned the name LI-cadherin. In these tissues, LI-cadherin is localized to the basolateral domain of hepatocytes and enterocytes. These results suggest that LI-cadherin represents a new cadherin subtype and may have a role in the morphological organization of liver and intestine.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Cadherins/genetics,isolation & purification Calcium/pharmacology Cell Adhesion/drug effects Cloning, Molecular DNA, Complementary/genetics Drosophila/genetics Intestine, Small/chemistry Liver/chemistry Membrane Proteins/genetics,isolation & purification Microscopy, Immunoelectron Molecular Sequence Data Rats Sequence Analysis, DNA Sequence Homology, Amino Acid Tissue Distribution Transfection
Chemicals
Cadherins DNA, Complementary Membrane Proteins Calcium
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Berndorff D
Institut für Klinische Chemie und Biochemie, Universitätsklinikum Rudolf Virchow, Freie Universität Berlin, Federal Republic of Germany.
Gessner R
Kreft B
Schnoy N
Lajous-Petter A M
Loch N
Reutter W
Hortsch M
Tauber R
References (89)
89 references, click to expand
  1. Analysis of the gene encoding the largest subunit of RNA polymerase II in Drosophila.
    Mol Gen Genet. 1989 Jan;215(2):266-75 PMID: 2496296
  2. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species.
    EMBO J. 1989 Jun;8(6):1711-7 PMID: 2788574
  3. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  4. Protein degradation in the plasma membrane of regenerating liver and Morris hepatomas.
    Eur J Biochem. 1978 Feb 1;83(1):37-45 PMID: 203463
  5. 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
  6. A cell surface molecule involved in aggregation of embryonic liver cells.
    Proc Natl Acad Sci U S A. 1980 Aug;77(8):4831-5 PMID: 6933535
  7. A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos.
    Cell. 1980 Oct;21(3):927-34 PMID: 6159985
  8. Steps in the biosynthesis of mosquito cell membrane glycoproteins and the effects of tunicamycin.
    Biochim Biophys Acta. 1981 Feb 6;640(3):672-86 PMID: 7213699
  9. Localization of gold in biological tissue. A photochemical method for light and electronmicroscopy.
    Histochemistry. 1981;71(1):81-8 PMID: 6785260
  10. Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4515-9 PMID: 6270680
  11. Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium.
    Cell. 1981 Nov;26(3 Pt 1):447-54 PMID: 6976838
  12. Intercellular adhesion of rat hepatocytes. Identification of a cell surface glycoprotein involved in the initial adhesion process.
    J Biol Chem. 1982 Jun 25;257(12):6788-95 PMID: 7085603
  13. A simple method for displaying the hydropathic character of a protein.
    J Mol Biol. 1982 May 5;157(1):105-32 PMID: 7108955
  14. Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells.
    Proc Natl Acad Sci U S A. 1983 Feb;80(4):1038-42 PMID: 6573655
  15. Changes in methylation pattern of albumin and alpha-fetoprotein genes in developing rat liver and neoplasia.
    Nucleic Acids Res. 1983 Jul 11;11(13):4335-54 PMID: 6191280
  16. Intramolecular heterogeneity of degradation in plasma membrane glycoproteins: evidence for a general characteristic.
    Proc Natl Acad Sci U S A. 1983 Jul;80(13):4026-9 PMID: 6575394
  17. Calcium-dependent cell-cell adhesion molecules common to hepatocytes and teratocarcinoma stem cells.
    J Cell Biol. 1983 Sep;97(3):944-8 PMID: 6885928
  18. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  19. Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells.
    J Biol Chem. 1984 Feb 25;259(4):2375-82 PMID: 6698972
  20. Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells.
    J Cell Biol. 1985 Jan;100(1):327-32 PMID: 3880756
  21. Some structural and functional aspects of the cell adhesion molecule uvomorulin.
    Cell Differ. 1984 Dec;15(2-4):269-73 PMID: 6336035
  22. Biochemical characterization of domain-specific glycoproteins of the rat hepatocyte plasma membrane.
    J Biol Chem. 1985 Oct 15;260(23):12792-802 PMID: 2864346
  23. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide.
    J Cell Biol. 1986 Feb;102(2):457-68 PMID: 3511070
  24. Different oligosaccharide processing of the membrane-integrated and the secretory form of gp 80 in rat liver.
    EMBO J. 1986 Sep;5(9):2109-14 PMID: 3536485
  25. Topographic localization of the heparin-binding domain of the neural cell adhesion molecule N-CAM.
    J Cell Biol. 1986 Nov;103(5):1739-44 PMID: 2430978
  26. Families of neural adhesion molecules.
    Ciba Found Symp. 1989;145:156-69, discussion 169-72 PMID: 2477202
  27. Fasciclin III: a novel homophilic adhesion molecule in Drosophila.
    Cell. 1989 Oct 20;59(2):313-23 PMID: 2509076
  28. Distribution and dynamics of cell surface-associated cellCAM 105 in cultured rat hepatocytes.
    Exp Cell Res. 1989 Nov;185(1):132-42 PMID: 2680537
  29. Detection of an altered form of cell-CAM 105 on rat transplantable and primary hepatocellular carcinomas.
    Cancer Res. 1989 Dec 1;49(23):6788-94 PMID: 2684401
  30. Rapid intramolecular turnover of N-linked glycans in plasma membrane glycoproteins. Extension of intramolecular turnover to the core sugars in plasma membrane glycoproteins of hepatoma.
    Eur J Biochem. 1989 Dec 8;186(1-2):55-62 PMID: 2598940
  31. The oligosaccharides of influenza virus hemagglutinin expressed in insect cells by a baculovirus vector.
    Virology. 1990 Feb;174(2):418-29 PMID: 2407026
  32. Calcium-dependent cell adhesion molecules.
    Curr Opin Cell Biol. 1989 Oct;1(5):892-7 PMID: 2697291
  33. Localization of specificity determining sites in cadherin cell adhesion molecules.
    Cell. 1990 Apr 6;61(1):147-55 PMID: 2317870
  34. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth.
    J Cell Biol. 1990 Apr;110(4):1253-60 PMID: 2324197
  35. Identification of a cadherin cell adhesion recognition sequence.
    Dev Biol. 1990 May;139(1):227-9 PMID: 2328837
  36. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila.
    Cell. 1990 May 4;61(3):523-34 PMID: 2185893
  37. Identification of a Ca2(+)-dependent cell-cell adhesion molecule in endothelial cells.
    J Cell Biol. 1990 May;110(5):1745-56 PMID: 2335569
  38. Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting.
    J Cell Biol. 1990 May;110(5):1825-32 PMID: 2335571
  39. Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule.
    Proc Natl Acad Sci U S A. 1990 Jun;87(11):4246-50 PMID: 2349235
  40. Leukocyte adhesion to endothelium in inflammation.
    Cell. 1990 Jul 13;62(1):3-6 PMID: 2194672
  41. Cadherins: a molecular family important in selective cell-cell adhesion.
    Annu Rev Biochem. 1990;59:237-52 PMID: 2197976
  42. Correct proteolytic cleavage is required for the cell adhesive function of uvomorulin.
    J Cell Biol. 1990 Oct;111(4):1645-50 PMID: 2211831
  43. Desmoglein shows extensive homology to the cadherin family of cell adhesion molecules.
    Biochem Biophys Res Commun. 1990 Dec 31;173(3):1224-30 PMID: 1702628
  44. Two-dimensional maps in the most extended (pH 2.5-11) immobilized pH gradient interval.
    J Biochem Biophys Methods. 1990 Jul-Aug;21(2):173-9 PMID: 2273202
  45. Identification of desmoglein, a constitutive desmosomal glycoprotein, as a member of the cadherin family of cell adhesion molecules.
    Eur J Cell Biol. 1990 Oct;53(1):1-12 PMID: 1706270
  46. Cadherin cell adhesion receptors as a morphogenetic regulator.
    Science. 1991 Mar 22;251(5000):1451-5 PMID: 2006419
  47. Antibodies to the retina N-acetylgalactosaminylphosphotransferase modulate N-cadherin-mediated adhesion and uncouple the N-cadherin transferase complex from the actin-containing cytoskeleton.
    J Cell Biol. 1991 Apr;113(2):429-36 PMID: 1849140
  48. Molecular cloning and characterization of B-cadherin, a novel chick cadherin.
    J Cell Biol. 1991 May;113(4):893-905 PMID: 2026653
  49. Diversity of the cadherin family: evidence for eight new cadherins in nervous tissue.
    Cell Regul. 1991 Apr;2(4):261-70 PMID: 2059658
  50. C-CAM (cell-CAM 105)--a member of the growing immunoglobulin superfamily of cell adhesion proteins.
    Bioessays. 1991 May;13(5):227-34 PMID: 1892475
  51. A quantitative assay for intercellular adhesion.
    Proc Natl Acad Sci U S A. 1973 May;70(5):1569-73 PMID: 4351182
  52. Surface antigen in early differentiation.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4449-52 PMID: 270688
  53. Cell surface polarity in epithelia.
    Annu Rev Cell Biol. 1985;1:243-88 PMID: 3939606
  54. Cell-matrix interactions and cell adhesion during development.
    Annu Rev Cell Biol. 1986;2:27-47 PMID: 3548769
  55. The role of uvomorulin in the formation of epithelial occluding junctions.
    Ciba Found Symp. 1987;125:168-86 PMID: 3549195
  56. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing.
    Science. 1987 May 15;236(4803):799-806 PMID: 3576199
  57. The structure of cell adhesion molecule uvomorulin. Insights into the molecular mechanism of Ca2+-dependent cell adhesion.
    EMBO J. 1987 Dec 1;6(12):3647-53 PMID: 3501370
  58. Isolation of placental cadherin cDNA: identification of a novel gene family of cell-cell adhesion molecules.
    EMBO J. 1987 Dec 1;6(12):3655-61 PMID: 3428270
  59. Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells.
    Nucleic Acids Res. 1988 Feb 11;16(3):1043-61 PMID: 3125519
  60. Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family.
    J Cell Biol. 1988 Mar;106(3):873-81 PMID: 2831236
  61. Expression of M-cadherin, a member of the cadherin multigene family, correlates with differentiation of skeletal muscle cells.
    Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8024-8 PMID: 1840697
  62. T-cadherin, a novel cadherin cell adhesion molecule in the nervous system lacks the conserved cytoplasmic region.
    Neuron. 1991 Sep;7(3):391-402 PMID: 1654948
  63. Complete amino acid sequence of the epidermal desmoglein precursor polypeptide and identification of a second type of desmoglein gene.
    Eur J Cell Biol. 1991 Aug;55(2):200-8 PMID: 1935985
  64. Sticky molecules in not-so-sticky cells.
    Trends Biochem Sci. 1991 Aug;16(8):283-7 PMID: 1957349
  65. Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin.
    Cell Regul. 1989 Nov;1(1):37-44 PMID: 2519616
  66. Complexity and expression patterns of the desmosomal cadherins.
    Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):353-7 PMID: 1729705
  67. Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons.
    Cell. 1992 Jan 24;68(2):303-22 PMID: 1733501
  68. Temporal changes in the expression and distribution of adhesion molecules during liver development and regeneration.
    J Cell Biol. 1992 Mar;116(6):1507-15 PMID: 1531833
  69. Integrins: versatility, modulation, and signaling in cell adhesion.
    Cell. 1992 Apr 3;69(1):11-25 PMID: 1555235
  70. Structure of the N-linked oligosaccharides of the human transferrin receptor.
    Eur J Biochem. 1992 Apr 1;205(1):257-67 PMID: 1555586
  71. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain.
    Cell. 1992 Apr 17;69(2):225-36 PMID: 1568244
  72. Ganglioside modulation of neural cell adhesion molecule and N-cadherin-dependent neurite outgrowth.
    J Cell Biol. 1992 Jun;117(5):1093-9 PMID: 1577868
  73. The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties.
    J Cell Biol. 1992 Aug;118(3):681-91 PMID: 1639851
  74. Extrajunctional distribution of N-cadherin in cultured human endothelial cells.
    J Cell Sci. 1992 May;102 ( Pt 1):7-17 PMID: 1500442
  75. Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila.
    Cell. 1992 Aug 21;70(4):553-67 PMID: 1505024
  76. Biosynthesis and metabolism of dipeptidylpeptidase IV in primary cultured rat hepatocytes and Morris hepatoma 7777 cells.
    Eur J Biochem. 1992 Nov 15;210(1):161-8 PMID: 1359965
  77. Cadherins.
    Annu Rev Cell Biol. 1992;8:307-32 PMID: 1476802
  78. Expression of dopamine beta-hydroxylase in Drosophila Schneider 2 cells. Evidence for a mechanism of membrane binding other than uncleaved signal peptide.
    J Biol Chem. 1993 May 5;268(13):9490-5 PMID: 8486639
  79. Identification of a Drosophila homologue of alpha-catenin and its association with the armadillo protein.
    J Cell Biol. 1993 Jun;121(5):1133-40 PMID: 8501118
  80. Protocadherins: a large family of cadherin-related molecules in central nervous system.
    EMBO J. 1993 Jun;12(6):2249-56 PMID: 8508762
  81. Characterisation of the ATP-dependent taurocholate-carrier protein (gp110) of the hepatocyte canalicular membrane.
    Eur J Biochem. 1993 Jun 1;214(2):539-48 PMID: 8513803
  82. Phylogenetic analysis of the cadherin superfamily.
    Bioessays. 1992 Nov;14(11):743-8 PMID: 1365887
  83. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.
    J Cell Biol. 1963 Apr;17:208-12 PMID: 13986422
  84. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  85. Cell lines derived from late embryonic stages of Drosophila melanogaster.
    J Embryol Exp Morphol. 1972 Apr;27(2):353-65 PMID: 4625067
  86. The immunoglobulin superfamily--domains for cell surface recognition.
    Annu Rev Immunol. 1988;6:381-405 PMID: 3289571
  87. Morphoregulatory molecules.
    Biochemistry. 1988 May 17;27(10):3533-43 PMID: 3044445
  88. Characterization of the human transferrin receptor produced in a baculovirus expression system.
    J Biol Chem. 1988 Sep 15;263(26):13386-92 PMID: 3047122
  89. The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex.
    J Cell Biol. 1988 Oct;107(4):1575-87 PMID: 3049625
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-06-00
Pages
1353-69
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2290917
Subset
IM
Databases
GENBANK
X78997
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