Home LiteratureArticle Details
PMID: 7536748 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Plasticity in epithelial cell phenotype: modulation by expression of different cadherin cell adhesion molecules.

The Journal of cell biology ·Vol. 129 ·No. 2 ·1995-04-00 ·Pages 507-19

Marrs JA, Andersson-Fisone C, Jeong MC, Cohen-Gould L, Zurzolo C, Nabi IR, Rodriguez-Boulan E, Nelson WJ

Abstract

A primary function of cadherins is to regulate cell adhesion. Here, we demonstrate a broader function of cadherins in the differentiation of specialized epithelial cell phenotypes. In situ, the rat retinal pigment epithelium (RPE) forms cell-cell contacts within its monolayer, and at the apical membrane with the neural retina; Na+, K(+)-ATPase and the membrane cytoskeleton are restricted to the apical membrane. In vitro, RPE cells (RPE-J cell line) express an endogenous cadherin, form adherens junctions and a tight monolayer, but Na+,K(+)-ATPase is localized to both apical and basal-lateral membranes. Expression of E-cadherin in RPE-J cells results in restriction and accumulation of both Na+,K(+)-ATPase and the membrane cytoskeleton at the lateral membrane; these changes correlate with the synthesis of a different ankyrin isoform. In contrast to both RPE in situ and RPE-J cells that do not form desmosomes, E-cadherin expression in RPE-J cells induces accumulation of desmoglein mRNA, and assembly of desmosome-keratin complexes at cell-cell contacts. These results demonstrate that cadherins directly affect epithelial cell phenotype by remodeling the distributions of constitutively expressed proteins and by induced accumulation of specific proteins, which together lead to the generation of structurally and functionally distinct epithelial cell types.

MeSH Terms
Amino Acid Sequence Animals Ankyrins/biosynthesis,chemistry Cadherins/analysis,biosynthesis,genetics,physiology Cell Communication Cell Differentiation Cell Line Cytoskeletal Proteins/analysis,genetics Desmogleins Desmoplakins Desmosomes/chemistry,metabolism,ultrastructure Intermediate Filaments/ultrastructure Keratins/analysis Molecular Sequence Data Molecular Weight Phenotype Pigment Epithelium of Eye/cytology RNA, Messenger/analysis Rats Retina/cytology Sequence Homology, Amino Acid Sodium-Potassium-Exchanging ATPase/analysis
Chemicals
Ankyrins Cadherins Cytoskeletal Proteins Desmogleins Desmoplakins RNA, Messenger Keratins Sodium-Potassium-Exchanging ATPase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Marrs J A
Department of Molecular and Cellular Physiology, Stanford University School of Medicine, California 94305-5426, USA.
Andersson-Fisone C
Jeong M C
Cohen-Gould L
Zurzolo C
Nabi I R
Rodriguez-Boulan E
Nelson W J
References (54)
54 references, click to expand
  1. Expressed recombinant cadherins mediate cell sorting in model systems.
    Cell. 1988 Sep 23;54(7):993-1001 PMID: 3416359
  2. Colocalization and coprecipitation of ankyrin and Na+,K+-ATPase in kidney epithelial cells.
    Eur J Cell Biol. 1988 Feb;45(2):230-7 PMID: 2835237
  3. Cell adhesion molecules: implications for a molecular histology.
    Annu Rev Biochem. 1991;60:155-90 PMID: 1883195
  4. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  5. Cell adhesion and the molecular processes of morphogenesis.
    Annu Rev Biochem. 1985;54:135-69 PMID: 3896119
  6. Selective adhesion of embryonal carcinoma cells and differentiated cells by Ca2+-dependent sites.
    Dev Biol. 1981 Oct 30;87(2):340-50 PMID: 6793433
  7. Ankyrin binding to (Na+ + K+)ATPase and implications for the organization of membrane domains in polarized cells.
    Nature. 1987 Aug 6-12;328(6130):533-6 PMID: 3039371
  8. Alterations in epithelial polarity and the pathogenesis of disease states.
    N Engl J Med. 1994 Jun 2;330(22):1580-8 PMID: 8177249
  9. Regulation of cell surface polarity from bacteria to mammals.
    Science. 1992 Nov 6;258(5084):948-55 PMID: 1439806
  10. A membrane-cytoskeletal complex containing Na+,K+-ATPase, ankyrin, and fodrin in Madin-Darby canine kidney (MDCK) cells: implications for the biogenesis of epithelial cell polarity.
    J Cell Biol. 1989 Mar;108(3):893-902 PMID: 2537837
  11. Spatial and temporal dissection of immediate and early events following cadherin-mediated epithelial cell adhesion.
    J Cell Biol. 1993 Mar;120(5):1217-26 PMID: 8436592
  12. The distribution of Na+,K(+)-ATPase in the retinal pigmented epithelium from chicken embryo is polarized in vivo but not in primary cell culture.
    Exp Eye Res. 1990 Oct;51(4):435-46 PMID: 2170160
  13. Immortalization of polarized rat retinal pigment epithelium.
    J Cell Sci. 1993 Jan;104 ( Pt 1):37-49 PMID: 8383696
  14. Dynamics of membrane-skeleton (fodrin) organization during development of polarity in Madin-Darby canine kidney epithelial cells.
    J Cell Biol. 1986 Nov;103(5):1751-65 PMID: 3023391
  15. Distribution of transport proteins over animal cell membranes.
    J Membr Biol. 1984;77(3):169-86 PMID: 6321741
  16. Diversity of the cadherin family: evidence for eight new cadherins in nervous tissue.
    Cell Regul. 1991 Apr;2(4):261-70 PMID: 2059658
  17. Protocadherins: a large family of cadherin-related molecules in central nervous system.
    EMBO J. 1993 Jun;12(6):2249-56 PMID: 8508762
  18. Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7043-7 PMID: 2780560
  19. Integral and peripheral protein composition of the apical and basolateral membrane domains in MDCK cells.
    J Membr Biol. 1989 Mar;107(3):277-86 PMID: 2716048
  20. Apical polarity of Na,K-ATPase in retinal pigment epithelium is linked to a reversal of the ankyrin-fodrin submembrane cytoskeleton.
    J Cell Biol. 1991 Mar;112(5):863-72 PMID: 1847929
  21. Classical cadherins.
    Semin Cell Biol. 1992 Jun;3(3):149-55 PMID: 1623204
  22. Second messengers underlying cell-contact-dependent axonal growth stimulated by transfected N-CAM, N-cadherin, or L1.
    Cold Spring Harb Symp Quant Biol. 1992;57:431-40 PMID: 1339679
  23. Regulation of C-cadherin function during activin induced morphogenesis of Xenopus animal caps.
    J Cell Biol. 1994 Jul;126(2):519-27 PMID: 8034750
  24. Mechanism for regulating cell surface distribution of Na+,K(+)-ATPase in polarized epithelial cells.
    Science. 1991 Nov 8;254(5033):847-50 PMID: 1658934
  25. Cadherin subclasses: differential expression and their roles in neural morphogenesis.
    Cold Spring Harb Symp Quant Biol. 1990;55:319-25 PMID: 2132824
  26. Involvement of the membrane-cytoskeleton in development of epithelial cell polarity.
    Semin Cell Biol. 1990 Oct;1(5):359-71 PMID: 1966328
  27. Localization of sodium pumps in the choroid plexus epithelium.
    J Cell Biol. 1973 Sep;58(3):724-30 PMID: 4747925
  28. Basement membrane stimulates the polarized distribution of integrins but not the Na,K-ATPase in the retinal pigment epithelium.
    Cell Regul. 1991 Nov;2(11):939-49 PMID: 1667092
  29. Molecular cloning and characterization of B-cadherin, a novel chick cadherin.
    J Cell Biol. 1991 May;113(4):893-905 PMID: 2026653
  30. Response.
    Science. 1993 Apr 23;260(5107):554-6 PMID: 17830435
  31. Polarity of epithelial and neuronal cells.
    Annu Rev Cell Biol. 1992;8:395-427 PMID: 1476804
  32. Making a connection: direct binding between keratin intermediate filaments and desmosomal proteins.
    J Cell Biol. 1994 Nov;127(4):1049-60 PMID: 7525601
  33. The expression of B-cadherin during embryonic chick development.
    Dev Biol. 1994 Jan;161(1):107-25 PMID: 8293867
  34. Signaling between the extracellular matrix and the cytoskeleton: tyrosine phosphorylation and focal adhesion assembly.
    Cold Spring Harb Symp Quant Biol. 1992;57:193-202 PMID: 1285049
  35. Cytoskeletons of retinal pigment epithelial cells: interspecies differences of expression patterns indicate independence of cell function from the specific complement of cytoskeletal proteins.
    Cell Tissue Res. 1988 Nov;254(2):301-15 PMID: 3058315
  36. Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9313-7 PMID: 2687880
  37. Morphogenesis of the polarized epithelial cell phenotype.
    Science. 1989 Aug 18;245(4919):718-25 PMID: 2672330
  38. Identification of the ubiquitous human desmoglein, Dsg2, and the expression catalogue of the desmoglein subfamily of desmosomal cadherins.
    Exp Cell Res. 1994 Apr;211(2):391-9 PMID: 8143788
  39. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis.
    Development. 1988 Apr;102(4):639-55 PMID: 3048970
  40. Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and -deficient cell lines.
    J Cell Biol. 1990 Nov;111(5 Pt 1):2077-88 PMID: 2172261
  41. Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity.
    Cell. 1990 Jul 27;62(2):309-16 PMID: 2164888
  42. The anion exchanger and Na+K(+)-ATPase interact with distinct sites on ankyrin in in vitro assays.
    J Biol Chem. 1990 Oct 5;265(28):17252-6 PMID: 2170369
  43. Abnormal sodium pump distribution during renal tubulogenesis in congenital murine polycystic kidney disease.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7447-51 PMID: 1323837
  44. Cell adhesion molecules in the regulation of animal form and tissue pattern.
    Annu Rev Cell Biol. 1986;2:81-116 PMID: 3548776
  45. Cadherin cell adhesion receptors as a morphogenetic regulator.
    Science. 1991 Mar 22;251(5000):1451-5 PMID: 2006419
  46. Morphoregulatory activities of NCAM and N-cadherin can be accounted for by G protein-dependent activation of L- and N-type neuronal Ca2+ channels.
    Cell. 1991 Oct 4;67(1):21-33 PMID: 1680564
  47. Spectrin-based membrane skeleton: a multipotential adaptor between plasma membrane and cytoplasm.
    Physiol Rev. 1990 Oct;70(4):1029-65 PMID: 2271059
  48. Distinguishing roles of the membrane-cytoskeleton and cadherin mediated cell-cell adhesion in generating different Na+,K(+)-ATPase distributions in polarized epithelia.
    J Cell Biol. 1993 Oct;123(1):149-64 PMID: 8408194
  49. Desmosomes and hemidesmosomes: constitutive molecular components.
    Annu Rev Cell Biol. 1990;6:461-91 PMID: 2275820
  50. Ankyrin links fodrin to the alpha subunit of Na,K-ATPase in Madin-Darby canine kidney cells and in intact renal tubule cells.
    J Cell Biol. 1989 Feb;108(2):455-65 PMID: 2537316
  51. Apical polarization of N-CAM in retinal pigment epithelium is dependent on contact with the neural retina.
    J Cell Biol. 1993 Apr;121(2):335-43 PMID: 8468350
  52. Epithelial morphogenesis.
    Cell. 1992 May 1;69(3):385-7 PMID: 1581959
  53. Delivery of Na+,K(+)-ATPase in polarized epithelial cells.
    Science. 1993 Apr 23;260(5107):552-4; author reply 554-6 PMID: 8386395
  54. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression.
    Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):206-9 PMID: 8278366
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1995-04-00
Pages
507-19
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2199912
Subset
IM
Grants
NEI NIH HHS · EY08538-04 · United States
NIGMS NIH HHS · GM 35527 · United States
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: product@genelibs.com