Membrane polarity in epithelial cells: Protein sorting and establishment of polarized domains

American Journal of Physiology - Renal Physiology

Volumn 272, Issue 4 41-4, 1997, Pages

  Caplan, Michael J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytoskeleton; Ion pumps; Membrane domains; Sorting signals; Targeting

Indexed keywords

ANIMAL CELL; BASOLATERAL MEMBRANE; CELL MEMBRANE DEPOLARIZATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CYTOSKELETON; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GENETIC TRANSCRIPTION; ION TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; TUMOR SUPPRESSOR GENE;

EID: 33751339795     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.1997.272.4.f425     Document Type: Review

References (60)

1. Ahn, K. Y., and B. C. Kone. Expression and cellular localization of mRNA encoding the "gastric" isoform of H-K-ATPase α-subunit in rat kidney. Am. J. Physiol. 268 (Renal Fluid Electrolyte Physiol. 37): F99-F109, 1994.
2. Behrens, J., W. Birchmeier, S. C. Goodman, and B. A. Imhof. Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-Arc-1: mechanistic aspects and identification of the antigen as a component related to uvomorulin. J. Cell Biol. 101: 1307-1315, 1985.
3. Beltzer, J. P., and M. Spiess. In vitro binding of the asialoglyco-protein receptor to the β adaptin of plasma membrane coated vesicles. EMBO J. 10: 3735-3742, 1991.
4. Bennett, V., and P. J. Stenbuck. Association between ankyrin and the cytoplasmic domain of band 3 isolated from the human erythrocyte membrane. J. Biol. Chem. 255: 2540-2548, 1980.
5. Brown, D. A., B. Crise, and J. K. Rose. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 245: 1499-1501, 1989.
6. Brown, D., and J. K. Rose. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68: 533-544, 1992.
7. Caplan, M. J. Biogenesis and sorting of plasma membrane proteins. Curr. Top. Membr. 39: 37-86, 1991.
8. Caplan, M. J., and K. S. Matlin. Sorting of membrane and secretory proteins in polarized epithelial cells. In: Functional Epithelial Cells in Culture, edited K. S. Matlin and J. D. Valentich. New York: Liss, 1989, p. 71-127.
9. Cassanova, J. E., G. Apodaca, and K. E. Mostov. An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell 66: 65-75, 1991.
10. Danielsen, E. M. Involvement of detergent-insoluble complexes in the intracellular transport of intestinal brush border enzymes Biochemistry 34: 1596-1605, 1995.
11. Dragsten, P. R., R. Blumenthal, and J. S. Handler. Membrane asymmetry in epithelia: is the tight junction a barrier to diffusion in the plasma membrane? Nature 294: 718-722, 1981.
12. Fagotto, F., N. Funayama, U. Gluck, and B. M. Gumbiner. Binding to cadherins antagonizes the signaling activity of β-catenin during axis formation in Xenopus. J. Cell Biol. 132: 1105-1114, 1996.
13. Fiedler, K., R. G. Parton, R. Kellner, T. Etzold, and K. Simons. VIP 36, a novel component of glycolipid rafts and exocytic carrier vesicles in epithelial cells. EMBO J. 13: 1729-1740, 1994.
14. Forte, T. M., T. E. Machen, and J. G. Forte. Ultrastructural change in oxyntic cell associated with secretory function: a membrane-recycling hypothesis. Gastroenterology 73: 941-955, 1977.
15. Garcia, M., C. Mirre, A. Quaroni, H. Reggio, and A. Le Bivic. GPI-anchored proteins associate to form microdomains during their intracellular transport in Caco-2 cells. J. Cell Sci. 104: 1281-1290, 1994.
16. Gottardi, C. J., and M. J. Caplan. Molecular requirements for the cell surface expression of multisubunit ion transporting ATPases: identification of protein domains that participate in Na,K-ATPase and H,K-ATPase subunit assembly. J. Biol. Chem. 268: 14342-14347, 1993.
17. Gottardi, C. J., and M. J. Caplan. An ion transporting ATPase encodes multiple apical localization signals. J. Cell Biol. 121: 283-293, 1993.
18. Gumbiner, B. M. Signal transduction by β-catenin. Curr. Opin. Cell Biol. 7: 634-640, 1995.
19. Gumbiner, B. M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84: 345-357, 1996.
20. Gumbiner, B., and K. Simons. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of an uvomorulin-like polypeptide. J. Cell Biol. 102: 457-468, 1986.
21. Hammerton, R. W., K. A. Krzeminski, R. W. Mays, T. A. Ryan, D. A. Wollner, and W. J. Nelson. Mechanism for regulating cell surface distribution of Na,K-ATPase in polarized epithelial cells. Science 254: 847-850, 1991.
22. Heasman, J., A. Crawford, K. Goldstone, P. Garner-Hamrick, B. Gumbiner, P. McCrea, C. Kintner, C. Y. Noro, and C. Wylie. Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79: 791-803, 1994.
23. Hunziker, W., C. Harter, K. Matter, and I. Mellman. Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell 66: 907-920, 1991.
24. Hynes, R. O. Integrins: versatility, modulation, and signalling in cell adhesion. Cell 69: 11-25, 1992.
25. Imhof, B. A., H. P. Vollmers, S. C. Goodman, and W. Birchmeier. Cell-cell interaction and polarity of epithelial cells: specific perturbation using a monoclonal antibody. Cell 35: 667-675, 1983.
26. Jaisser, F., B. Escoubet, N. Coutry, E. Eugene, J. P. Bonvalet, and N. Farman. Differential regulation of putative K-ATPase by low-K diet and corticosteroids in rat distal colon and kidney. Am. J. Physiol. 270 (Cell Physiol. 39): C679-C689, 1996.
27. Kundu, A., R. T. Avalos, C. M. Sanderson, and D. P. Nayak. Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells. J. Virol. 70: 6508-6515, 1996.
28. Lisanti, M. P., I. W. Caras, M.A. Davitz, and E. J. Rodriguez-Boulan. A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J. Cell Biol. 109: 2145-2156, 1989.
29. Lisanti, M. P., A. Le Bivic, A. R. Saltiel, and E. J. Rodriguez-Boulan. Preferred apical distribution of glycosyl-phosphatidlinositol (GPI) anchored proteins: a highly conserved feature of the polarized epithelial phenotype. J. Membr. Biol. 113: 155-167, 1990.
30. Lisanti, M. P., M. Sargiacomo, L. Graeve, A. R. Saltiel, and E. J. Rodriguez-Boulan. Polarized apical distribution of glycosyl-phosphatidyl-anchored proteins in a renal epithelial cell line. Proc. Natl. Acad. Sci. USA 85: 9557-9561, 1988.
31. Matter, K., E. M. Yamamoto, and I. Mellman. Structural requirements and sequence motifs for polarized sorting and endocytosis of LDL and Fc receptors in MDCK cells. J. Cell Biol. 126: 991-1004, 1994.
32. Mays, R. W., K. A. Siemers, B. A. Fritz, A. L. Lowe, G. van Meer, and W. J. Nelson. Hierarchy of mechanisms involved in generating Na,K-ATPase polarity in MDCK epithelial cells. J. Cell Biol. 130: 1105-1115, 1995.
33. Morrow, J. S., C. D. Cianci, T. Ardito, A. S. Mann, and M. Kashgarian. Ankyrin links fodrin to the α-subunit of Na,K-ATPase in MDCK cells and in intact renal tubules. J. Cell Biol. 108: 455-465, 1989.
34. Nelson, W. J., and R. W. Hammerton. A membrane-cytoskeletal complex containing Na,K-ATPase, ankyrin and fodrin in MDCK cells: implications for the biogenesis of epithelial cell polarity. J. Cell Biol. 108: 893-902, 1989.
35. Nelson, W. J., E. M. Shore, A. Z. Wang, and R. W. Hammerton. Identification of a membrane-cytoskeleton complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin and fodrin in MDCK epithelial cells. J. Cell Biol. 110: 349-357, 1990.
36. Nelson, W. J., and P. J. Veshnock. Dynamics of membrane skeleton (fodrin) organization during development of polarity in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 103: 1751-1765, 1986.
37. Nelson, W. J., and P. J. Veshnock. Modulation of fodrin (membrane skeleton) stability by cell-cell contact in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 104: 1527-1537, 1987.
38. Nelson, W. J., and P. J. Veshnock. Ankyrin binding to Na,K-ATPase and implications for the organization of membrane domains in polarized cells. Nature 328: 533-536, 1987.
39. Ohno, H., J. Stewart, M. C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J. S. Bonifacino. Interaction of tyrosine based sorting signals with clathrin associated proteins. Science 269: 1872-1875, 1995.
40. Okamoto, C. T., S. P. Shia, C. Bird, K. E. Mostov, and M. G. Roth. The cytoplasmic domain of the polymeric immunoglobulin receptor contains two internalization signals that are distinct from its basolateral sorting signal. J. Biol. Chem. 267: 9925-9932, 1992.
41. Pearse, B. M. F. Assembly of the mannose-6-phosphate receptor onto reconstituted clathrin coats. EMBO J. 4: 2457-2460, 1985.
42. Pearse, B. M. F. Receptors compete for adaptors found in plasma membrane coated pits. EMBO J. 7: 3331-3336, 1988.
43. Pearse, B. M. F., and M. S. Robinson. Clathrin, adaptors and sorting. Annu. Rev. Cell Biol. 6: 151-171, 1990.
44. Rabon, E. C., and M. A. Reuben. The mechanism and structure of the gastric H,K-ATPase. Annu. Rev. Physiol. 52: 321-344, 1990.
45. Rimm, D. L., E. R. Koslov, P. Kebriaei, C. D. Cianci, and J. S. Morrow. α1 (E)-Catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Natl. Acad. Sci. USA 92: 8813-8817, 1995.
46. Rubinfeld, B., B. Souza, I. Albert, O. Muller, S. H. Chamberlain, F. R. Masiarz, S. Munemitsu, and P. Polakis. Association of the APC gene product with β-catenin. Science 262: 1731-1734, 1993.
47. Scheiffele, P., J. Peranen, and K. Simons. N-glycans as apical sorting signals in epithelial cells. Nature 378: 96-98, 1995.
48. Segal, A. S., E. L. Boulpaep, and A. B. Maunsbach. A novel preparation of dissociated renal proximal tubule cells that maintain epithelial polarity in suspension. Am. J. Physiol. 270 (Cell Physiol. 39): C1843-C1863, 1996.
49. Simons, K., and G. van Meer. Lipid sorting in epithelial cells. Biochemistry 27: 6197-6202, 1988.
50. Simons, K., and A. Wandinger-Ness. Polarized sorting in epithelia. Cell 62: 207-210, 1990.
51. Skibbens, J. E., M. G. Roth, and K. S. Matlin. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and non-polarized fibroblasts. J. Cell Biol. 108: 821-832, 1989.
52. Smolka, A., H. F. Helander, and G. Sachs. Monoclonal antibodies against gastric H-K-ATPase. Am. J. Physiol. 245 (Gastrointest. Liver Physiol. 8): G589-G596, 1983.
53. Su, L. K., B. Vogelstein, and K. W. Kinzler. Association of the APC tumor suppressor protein with catenins. Science 262: 1734-1737, 1993.
54. Takeichi, M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251: 1451-1455, 1991.
55. Thomas, D. C., and M. G. Roth. The basolateral targeting signal in the cytoplasmic domain of glycoprotein G from vesicular stomatitis virus resembles a variety of intracellular targeting motifs related by primary sequence but having diverse targeting activities. J. Biol. Chem. 269: 15732-15739, 1994.
56. Urushidani, T., and J. G. Forte. Stimulation-associated redistribution of H-K-ATPase activity in isolated gastric glands. Am. J. Physiol. 252 (Gastrointest. Liver Physiol. 15): G458-G465, 1987.
57. Vega-Salas, D. E., P. J. I. Salas, D. Gunderson, and E. J. Rodriguez-Boulan. 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. 104: 905-916, 1987.
58. Vega-Salas, D. E., P. J. I. Salas, and E. J. Rodriguez-Boulan. Modulation of the expression of an apical plasma membrane protein of Madin-Darby canine kidney cells: cell-cell interactions control the appearance of a novel intracellular storage compartment. J. Cell Biol. 104: 1249-1259, 1987.
59. Younes-Ibrahim, M., C. Barlet-Bas, B. Buffin-Meyer, L. Cheval, R. Rajerison, and A. Doucet. Ouabain-sensitive and -insensitive K-ATPases in rat nephron: effect of K depletion. Am. J. Physiol. 268 (Renal Fluid Electrolyte Physiol. 37): F1141-F1147, 1995.
60. Wingo, C. S., and F. E. Armitage. Rubidium absorption and proton secretion by rabbit outer medullary collecting duct via K-ATPase. Am. J. Physiol. 263 (Renal Fluid Electrolyte Physiol. 32): F849-F857, 1992.