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PMID: 3198691 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Selective anchoring in the specific plasma membrane domain: a role in epithelial cell polarity.

The Journal of cell biology ·Vol. 107 ·No. 6 Pt 1 ·1988-12-00 ·Pages 2363-76

Salas PJ, Vega-Salas DE, Hochman J, Rodriguez-Boulan E, Edidin M

Abstract

We have studied the role of restrictions to lateral mobility in the segregation of proteins to apical and basolateral domains of MDCK epithelial cells. Radioimmunoassay and semiquantitative video analysis of immunofluorescence on frozen sections showed that one apical and three basolateral glycoproteins, defined by monoclonal antibodies and binding of beta-2-microglobulin, were incompletely extracted with 0.5% Triton X-100 in a buffer that preserves the cortical cytoskeleton (Fey, E. G., K. M. Wan, and S. Penman. 1984. J. Cell Biol. 98:1973-1984; Nelson, W. T. and P. J. Veshnock. 1986. J. Cell Biol. 103:1751-1766). The marker proteins were preferentially extracted from the "incorrect" domain (i.e., the apical domain for a basolateral marker), indicating that the cytoskeletal anchoring was most effective on the "correct" domain. The two basolateral markers were unpolarized and almost completely extractable in cells prevented from establishing cell-cell contacts by incubation in low Ca++ medium, while an apical marker was only extracted from the basal surface under the same conditions. Procedures were developed to apply fluorescent probes to either the apical or the basolateral surface of live cells grown on native collagen gels. Fluorescence recovery after photobleaching of predominantly basolateral antigens showed a large percent of cells (28-52%) with no recoverable fluorescence on the basal domain but normal fluorescence recovery on the apical surface of most cells (92-100%). Diffusion coefficients in cells with normal fluorescence recovery were in the order of 1.1 x 10(-9) cm2/s in the apical domain and 0.6-0.9 x 10(-9) cm2/s in the basal surface, but the difference was not significant. The data from both techniques indicate (a) the existence of mobile and immobile protein fractions in both plasma membrane domains, and (b) that linkage to a domain specific submembrane cytoskeleton plays an important role in the maintenance of epithelial cell surface polarity.

MeSH Terms
Antibodies, Monoclonal/immunology Cell Compartmentation Cell Line Cell Membrane/physiology,ultrastructure Cytoskeleton/physiology Epithelium/ultrastructure Membrane Proteins/physiology Microscopy, Fluorescence Polyethylene Glycols Solubility
Chemicals
Antibodies, Monoclonal Membrane Proteins Polyethylene Glycols
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Salas P J
Department of Cell Biology and Anatomy, Cornell University Medical College, New York 10021.
Vega-Salas D E
Hochman J
Rodriguez-Boulan E
Edidin M
References (81)
81 references, click to expand
  1. A cytoskeleton-associated plasma membrane heparan sulfate proteoglycan in Schwann cells.
    J Biol Chem. 1986 Jun 5;261(16):7518-25 PMID: 2940243
  2. Lateral diffusion of H-2 antigens on mouse fibroblasts.
    J Cell Biol. 1982 Nov;95(2 Pt 1):458-62 PMID: 6815209
  3. International workshop on the application of fluorescence photobleaching techniques to problems in cell biology.
    Fed Proc. 1983 Jan;42(1):72-9 PMID: 6848381
  4. Lateral distribution of sodium and potassium channels in frog skeletal muscle: measurements with a patch-clamp technique.
    J Physiol. 1983 Mar;336:261-84 PMID: 6308223
  5. Transepithelial transport of a viral membrane glycoprotein implanted into the apical plasma membrane of Madin-Darby canine kidney cells. I. Morphological evidence.
    J Cell Biol. 1983 Sep;97(3):627-37 PMID: 6885914
  6. Transepithelial transport of a viral membrane glycoprotein implanted into the apical plasma membrane of Madin-Darby canine kidney cells. II. Immunological quantitation.
    J Cell Biol. 1983 Sep;97(3):638-43 PMID: 6411736
  7. Characterization of the 110-kdalton actin-calmodulin-, and membrane-binding protein from microvilli of intestinal epithelial cells.
    J Cell Biol. 1983 Oct;97(4):974-85 PMID: 6311843
  8. Effects of cell density and extracellular matrix on the lateral diffusion of major histocompatibility antigens in cultured fibroblasts.
    J Cell Biol. 1986 Jul;103(1):215-22 PMID: 3722263
  9. Large deletions in the cytoplasmic kinase domain of the epidermal growth factor receptor do not affect its laternal mobility.
    J Cell Biol. 1986 Aug;103(2):327-31 PMID: 3015981
  10. Agorins: major structural proteins of the plasma membrane skeleton of P815 tumor cells.
    J Cell Biol. 1986 Aug;103(2):351-60 PMID: 3090052
  11. The function of tight junctions in maintaining differences in lipid composition between the apical and the basolateral cell surface domains of MDCK cells.
    EMBO J. 1986 Jul;5(7):1455-64 PMID: 3743548
  12. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia.
    J Cell Biol. 1986 Sep;103(3):755-66 PMID: 3528172
  13. Sorting of an apical plasma membrane glycoprotein occurs before it reaches the cell surface in cultured epithelial cells.
    J Cell Biol. 1984 Dec;99(6):2131-9 PMID: 6501415
  14. Lateral diffusion of wild-type and mutant Ld antigens in L cells.
    J Cell Biol. 1984 Dec;99(6):2333-5 PMID: 6501428
  15. Distribution of platelet glycoproteins and phosphoproteins in hydrophobic and hydrophilic phases in Triton X-114 phase partition.
    Biochim Biophys Acta. 1984 Dec 19;778(3):463-9 PMID: 6509048
  16. Biogenesis of epithelial cell polarity: intracellular sorting and vectorial exocytosis of an apical plasma membrane glycoprotein.
    Cell. 1984 Dec;39(3 Pt 2):537-46 PMID: 6509551
  17. Polarized delivery of viral glycoproteins to the apical and basolateral plasma membranes of Madin-Darby canine kidney cells infected with temperature-sensitive viruses.
    J Cell Biol. 1985 Jan;100(1):136-51 PMID: 2981229
  18. Localization of a liver transglutaminase and a large molecular weight transglutaminase substrate to a distinct plasma membrane domain.
    J Biol Chem. 1986 Nov 5;261(31):14833-6 PMID: 2876987
  19. 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
  20. Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule.
    Nature. 1986 Dec 4-10;324(6096):462-5 PMID: 3537809
  21. Restriction of the lateral motion of band 3 in the erythrocyte membrane by the cytoskeletal network: dependence on spectrin association state.
    Biochemistry. 1986 Oct 7;25(20):6133-9 PMID: 3790510
  22. A novel cadherin cell adhesion molecule: its expression patterns associated with implantation and organogenesis of mouse embryos.
    J Cell Biol. 1986 Dec;103(6 Pt 2):2649-58 PMID: 3539943
  23. A C-terminal signal prevents secretion of luminal ER proteins.
    Cell. 1987 Mar 13;48(5):899-907 PMID: 3545499
  24. Cytoskeletal proteins of the rat kidney proximal tubule brush border.
    Eur J Cell Biol. 1986 Dec;42(2):319-27 PMID: 3545840
  25. Visualization of the hexagonal lattice in the erythrocyte membrane skeleton.
    J Cell Biol. 1987 Mar;104(3):527-36 PMID: 2434513
  26. Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border.
    Annu Rev Cell Biol. 1985;1:209-41 PMID: 3916317
  27. Cell surface polarity in epithelia.
    Annu Rev Cell Biol. 1985;1:243-88 PMID: 3939606
  28. Cell adhesion molecules in the regulation of animal form and tissue pattern.
    Annu Rev Cell Biol. 1986;2:81-116 PMID: 3548776
  29. The fluid mosaic model of the structure of cell membranes.
    Science. 1972 Feb 18;175(4023):720-31 PMID: 4333397
  30. Collagen substrata for studies on cell behavior.
    J Cell Biol. 1972 Sep;54(3):626-37 PMID: 4339818
  31. Continuous cultures of fused cells secreting antibody of predefined specificity.
    Nature. 1975 Aug 7;256(5517):495-7 PMID: 1172191
  32. Surface modulation in cell recognition and cell growth.
    Science. 1976 Apr 16;192(4236):218-26 PMID: 769162
  33. Redistribution of surface macromolecules in dissociated epithelial cells.
    J Cell Biol. 1976 Dec;71(3):907-20 PMID: 62756
  34. Role of the intrinsic transglutaminase in the Ca2+-mediated crosslinking of erythrocyte proteins.
    Proc Natl Acad Sci U S A. 1976 Dec;73(12):4479-81 PMID: 12508
  35. Twenty-first Bowditch lecture. The epithelial junction: bridge, gate, and fence.
    Physiologist. 1977 Feb;20(1):10-8 PMID: 16304
  36. Enzymatic basis for the Ca2+-induced cross-linking of membrane proteins in intact human erythrocytes.
    Biochemistry. 1978 Jun 27;17(13):2598-604 PMID: 28146
  37. Polarized monolayers formed by epithelial cells on a permeable and translucent support.
    J Cell Biol. 1978 Jun;77(3):853-80 PMID: 567227
  38. The outer boundary of the cytoskeleton: a lamina derived from plasma membrane proteins.
    Cell. 1979 Aug;17(4):859-65 PMID: 573666
  39. Rotational and lateral diffusion of membrane proteins.
    Biochim Biophys Acta. 1979 Dec 20;559(4):289-327 PMID: 391281
  40. Identification and organization of the components in the isolated microvillus cytoskeleton.
    J Cell Biol. 1979 Dec;83(3):667-73 PMID: 574874
  41. Integral membrane protein interaction with Triton cytoskeletons of erythrocytes.
    Biochim Biophys Acta. 1979 Oct 19;557(1):122-34 PMID: 549630
  42. Lateral mobility of integral membrane proteins is increased in spherocytic erythrocytes.
    Nature. 1980 Jun 12;285(5765):510-1 PMID: 7402296
  43. Redistribution of membrane proteins in isolated mouse intestinal epithelial cells.
    J Cell Biol. 1980 Sep;86(3):849-57 PMID: 7410482
  44. Anchorage of a band 3 population at the erythrocyte cytoplasmic membrane surface: protein rotational diffusion measurements.
    Proc Natl Acad Sci U S A. 1980 Aug;77(8):4702-6 PMID: 6933517
  45. Phase separation of integral membrane proteins in Triton X-114 solution.
    J Biol Chem. 1981 Feb 25;256(4):1604-7 PMID: 6257680
  46. Occluding junctions and cytoskeletal components in a cultured transporting epithelium.
    J Cell Biol. 1980 Dec;87(3 Pt 1):746-54 PMID: 7193213
  47. Interaction of cytoskeletal proteins on the human erythrocyte membrane.
    Cell. 1981 Apr;24(1):24-32 PMID: 6453651
  48. Fluorescent membrane probes and the mechanism of maintenance of cellular asymmetry in epithelia.
    Fed Proc. 1982 Jan;41(1):48-53 PMID: 7056398
  49. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum.
    J Cell Biol. 1982 Apr;93(1):97-102 PMID: 7068762
  50. The molecular basis for membrane - cytoskeleton association in human erythrocytes.
    J Cell Biochem. 1982;18(1):49-65 PMID: 6461664
  51. Modulation of lateral mobility of band 3 in the red cell membrane by oxidative cross-linking of spectrin.
    Nature. 1982 Jun 3;297(5865):424-5 PMID: 7078652
  52. Effect of microvilli on lateral diffusion measurements made by the fluorescence photobleaching recovery technique.
    Biophys J. 1982 Jun;38(3):295-7 PMID: 7104441
  53. Distribution of transport proteins over animal cell membranes.
    J Membr Biol. 1984;77(3):169-86 PMID: 6321741
  54. Intracellular transport of influenza virus hemagglutinin to the apical surface of Madin-Darby canine kidney cells.
    J Cell Biol. 1984 Jan;98(1):308-19 PMID: 6707094
  55. Studies on the development and maintenance of epithelial cell surface polarity with monoclonal antibodies.
    J Cell Biol. 1984 May;98(5):1777-87 PMID: 6725399
  56. Epithelial cytoskeletal framework and nuclear matrix-intermediate filament scaffold: three-dimensional organization and protein composition.
    J Cell Biol. 1984 Jun;98(6):1973-84 PMID: 6202700
  57. A cell surface integral membrane glycoprotein of 85,000 mol wt (gp85) associated with triton X-100-insoluble cell skeleton.
    J Cell Biol. 1984 Aug;99(2):512-9 PMID: 6378925
  58. Intracellular sorting and basolateral appearance of the G protein of vesicular stomatitis virus in Madin-Darby canine kidney cells.
    J Cell Biol. 1985 Aug;101(2):470-6 PMID: 2991300
  59. A T-lymphoma transmembrane glycoprotein (gp180) is linked to the cytoskeletal protein, fodrin.
    J Cell Biol. 1985 Aug;101(2):477-87 PMID: 3874872
  60. Tight junction formation in cultured epithelial cells (MDCK).
    J Membr Biol. 1985;86(2):113-25 PMID: 4032460
  61. Colocalization of band 3 with ankyrin and spectrin at the basal membrane of intercalated cells in the rat kidney.
    Science. 1985 Dec 13;230(4731):1287-9 PMID: 2933809
  62. 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
  63. Subcellular location and identification of a large molecular weight substrate for the liver plasma membrane transglutaminase.
    J Biol Chem. 1986 Mar 5;261(7):3451-6 PMID: 2869032
  64. On the molecular organization, diversity and functions of desmosomal proteins.
    Ciba Found Symp. 1987;125:3-25 PMID: 2435471
  65. Formation of the apical pole of epithelial (Madin-Darby canine kidney) cells: polarity of an apical protein is independent of tight junctions while segregation of a basolateral marker requires cell-cell interactions.
    J Cell Biol. 1987 Apr;104(4):905-16 PMID: 3558485
  66. Lateral diffusion of proteins in membranes.
    Annu Rev Physiol. 1987;49:163-75 PMID: 3551795
  67. Modulation of the expression of an apical plasma membrane protein of Madin-Darby canine kidney epithelial cells: cell-cell interactions control the appearance of a novel intracellular storage compartment.
    J Cell Biol. 1987 May;104(5):1249-59 PMID: 3553208
  68. Modulation of fodrin (membrane skeleton) stability by cell-cell contact in Madin-Darby canine kidney epithelial cells.
    J Cell Biol. 1987 Jun;104(6):1527-37 PMID: 3584240
  69. A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum.
    Cell. 1987 Jul 17;50(2):311-7 PMID: 2954653
  70. Protein sorting by selective retention in the endoplasmic reticulum and Golgi stack.
    Cell. 1987 Aug 14;50(4):521-2 PMID: 3607878
  71. Effects of mutations in three domains of the vesicular stomatitis viral glycoprotein on its lateral diffusion in the plasma membrane.
    J Cell Biol. 1987 Jul;105(1):69-75 PMID: 3038931
  72. 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
  73. A specific transmembrane domain of a coronavirus E1 glycoprotein is required for its retention in the Golgi region.
    J Cell Biol. 1987 Sep;105(3):1205-14 PMID: 2821010
  74. Collagen receptors mediate early events in the attachment of epithelial (MDCK) cells.
    J Membr Biol. 1987;98(3):223-36 PMID: 3681953
  75. Specific associations of fluorescent beta-2-microglobulin with cell surfaces. The affinity of different H-2 and HLA antigens for beta-2-microglobulin.
    J Immunol. 1988 Apr 1;140(7):2322-9 PMID: 2450918
  76. Exocytosis of vacuolar apical compartment (VAC): a cell-cell contact controlled mechanism for the establishment of the apical plasma membrane domain in epithelial cells.
    J Cell Biol. 1988 Nov;107(5):1717-28 PMID: 3053735
  77. Mutants of the membrane-binding region of Semliki Forest virus E2 protein. II. Topology and membrane binding.
    J Cell Biol. 1986 Mar;102(3):902-10 PMID: 3949882
  78. The effect of mild diamide oxidation on the structure and function of human erythrocyte spectrin.
    J Biol Chem. 1986 Apr 5;261(10):4620-8 PMID: 3957910
  79. The lateral mobility of the (Na+,K+)-dependent ATPase in Madin-Darby canine kidney cells.
    J Cell Biol. 1986 Apr;102(4):1256-63 PMID: 3007531
  80. Identification of actin-, alpha-actinin-, and vinculin-containing plaques at the lateral membrane of epithelial cells.
    J Cell Biol. 1986 May;102(5):1843-52 PMID: 3084501
  81. Microtubules and actin filaments are not critically involved in the biogenesis of epithelial cell surface polarity.
    J Cell Biol. 1986 May;102(5):1853-67 PMID: 2871031
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.107.6.2363
Published
1988-12-00
Pages
2363-76
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2115698
Subset
IM
Grants
NIAID NIH HHS · AI-14584 · United States
NIGMS NIH HHS · GM-34107 · United States
External Links
PubMed source DOI: 10.1083/jcb.107.6.2363 PMC Full Text View journal details
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