N-Glycans, not the GPI anchor, mediate the apical targeting of a naturally glycosylated, GPI-anchored protein in polarised epithelial cells

Journal of Cell Science

Volumn 117, Issue 21, 2004, Pages 5079-5086

  Pang, Susan ^a   Urquhart, Paula ^a   Hooper, Nigel M ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Glycosyl phosphatidylinositol; Lipid rafts; MDCK cells; Membrane dipeptidase; N glycans

Indexed keywords

CELL SURFACE PROTEIN; DETERGENT; DIPEPTIDASE; GLYCAN DERIVATIVE; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL ADHESION; CELL POLARITY; CELL STRAIN; CELL SURFACE; CELL TYPE; CONTROLLED STUDY; EPITHELIUM CELL; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; LIPID SOLUBILITY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CACO-2 CELLS; CELL LINE; CELL MEMBRANE; DNA, COMPLEMENTARY; DOGS; EPITHELIAL CELLS; GLYCOSYLATION; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; MEMBRANE MICRODOMAINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; POINT MUTATION; POLYSACCHARIDES; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 8744246234     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01386     Document Type: Article

References (42)

1. Ali, N. and Evans, W. H. (1990). Priority targeting of glycosyl-phosphatidylinositol-anchored proteins to the bile-canalicular (apical) plasma membrane of hepatocytes. Involvement of 'late' endosomes. Biochem. J. 271, 193-199.
2. Benting, J. H., Rietveld, A. G. and Simons, K. (1999). N-Glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells. J. Cell Biol. 146 313-320.
3. Brewis, I. A., Turner, A. J. and Hooper, N. M. (1994). Activation of the glycosyl-phosphatidylinositol-anchored membrane dipeptidase upon release from porcine kidney membranes by phospholipase C. Biochem. J. 303, 633-638.
4. Brewis, I. A., Ferguson, M. A. J., Mehlert, A., Turner, A. J. and Hooper, N. M. (1995). Structures of the glycosyl-phosphatidylinositol anchors of porcine and human membrane dipeptidase. Interspecies comparison of the glycan core structures and further structural studies on the porcine anchor. J. Biol. Chem. 270, 22946-22956.
5. Brown, D. A., Crise, B. and Rose, J. K. (1989). Mechanism of membrane anchoring affects polarised expression of two proteins in MDCK cells. Science 245, 1499-1501.
6. Gut, A., Kappeler, F., Hyka, N., Balda, M. S., Hauri, H.-P. and Matter, K. (1998). Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins. EMBO J. 17, 1919-1929.
7. Hara-Kuge, S., Ohkura, T., Ideo, H., Shimada, O., Atsumi, S. and Yamashita, K. (2002). Involvement of VIP36 in intracellular transport and secretion of glycoproteins in polarized Madin-Darby canine kidney (MDCK) cells. J. Biol. Chem. 277, 16332-16339.
8. Hooper, N. M. and Turner, A. J. (1987). Isolation of two differentially glycosylated forms of peptidyl-dipeptidase A (angiotensin converting enzyme) from pig brain: a re-evaluation of their role in neuropeptide metabolism. Biochem. J. 241, 625-633.
9. Hooper, N. M. and Turner, A. J. (1988). Ectoenzymes of the kidney microvillar membrane. Differential solubilization by detergents can predict a glycosyl-phosphatidylinositol membrane anchor. Biochem. J. 250, 865-869.
10. Hooper, N. M., Low, M. G. and Turner, A. J. (1987). Renal dipeptidase is one of the membrane proteins released by phosphatidylinositol-specific phospholipase C. Biochem. J. 244 465-469.
11. Huang, X. F., Compans, R. W., Chen, S., Lamb, R. A. and Arvan, P. (1997). Polarized apical targeting directed by the signal/anchor region of simian virus 5 hemagglutinin-neuraminidase. J. Biol. Chem. 272, 27598-27604.
12. Ikonen, E. (2001). Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13, 470-477.
13. Keller, P. and Simons, K. (1997). Post-Golgi biosynthetic trafficking. J. Cell Sci. 110, 3001-3009.
14. Kuhn, U., Cohn, D. V. and Gorr, S. U. (2000). Polarized secretion of the regulated secretory protein chromogranin A. Biochem. Biophys. Res. Commun. 270, 631-636.
15. Kundu, A., Avalos, R. T., Sanderson, C. M. and Nayak, D. P. (1996). Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells. J. Virol. 70, 6508-6515.
16. Larsen, J. E., Avvakumov, G. V., Hammond, G. L. and Vogel, L. K. (1999). N-glycans are not the signal for apical sorting of corticosteroid binding globulin in MDCK cells. FEBS Lett. 451 19-22.
17. Lin, S., Naim, H. Y., Rodriguez, A. C. and Roth, M. G. (1998). Mutations in the middle of the transmembrane domain reverse the polarity of transport of the influenza virus hemagglutinin in MDCK epithelial cells. J. Cell Biol. 142, 51-57.
18. Lisanti, M. P., Sargiacomo, M., Graeve, L., Saltiel, A. R. and Rodriguez-Boulan, E. (1988). Polarised apical distribution of glycosyl-phosphatidylinositol-anchored proteins in a renal epithelial cell line. Proc. Natl. Acad. Sci. USA 85, 9557-9561.
19. Lisanti, M. P., Darnell, J. C., Chan, B. L., Rodriguez-Boulan, E. and Saltiel, A. R. (1989). The distribution of glycosyl-phosphatidylinositol anchored proteins is differentially regulated by serum and insulin. Biochem. Biophys. Res. Commun. 164, 824-832.
20. Lisanti, M. P., Caras, I. W., Gilbert, T., Hanzel, D. and Rodriguez-Boulan, E. (1990a). Vectorial apical delivery and slow endocytosis of a glycolipid anchored fusion protein in transfected MDCK cells. Proc. Natl. Acad. Sci. USA 87, 7419-7423.
21. Lisanti, M. P., le Bivic, A., Saltiel, A. R. and Rodriguez-Boulan, E. (1990b). Preferred apical distribution of glycosyl-phosphatidylinositol (GPI) anchored proteins: a highly conserved feature of the polarised epithelial cell phenotype. J. Membr. Biol. 113, 155-167.
22. Lisanti, M. P., Tang, Z. and Sargiacomo, M. (1993). Caveolin forms a hetero-oligomeric protein complex that interacts with an apical GPI-linked protein: implications for the biogenesis of caveolae. J. Cell Biol. 123, 595-604.
23. Littlewood, G. M., Hooper, N. M. and Turner, A. J. (1989). Ectoenzymes of the kidney microvillar membrane. Affinity purification, characterization and localization of the phospholipase C-solubilized form of renal dipeptidase. Biochem. J. 257, 361-367.
24. Marzolo, M. P., Bull, P. and Gonzalez, A. (1997). Apical sorting of hepatitis B surface antigen (HBsAg) is independent of N-glycosylation and glycosylphosphatidylinositol-anchored protein segregation. Proc. Natl. Acad. Sci. USA 94, 1834-1839.
25. Matter, K. (2000). Epithelial polarity: sorting out the sorters. Curr. Biol. 10, R39-R42.
26. Meerson, N. R., Bello, V., Delaunay, J. L., Slimane, T. A., Delautier, D., Lenoir, C., Trugnan, G. and Maurice, M. (2000). Intracellular traffic of the ecto-nucleotide pyrophosphatase/phosphodiesterase NPP3 to the apical plasma membrane of MDCK and caco-2 cells: apical targeting occurs in the absence of N-glycosylation. J. Cell Sci. 113, 4193-4202.
27. Morin, P. J., Sparks, A. B., Korinek, V., Barker, N., Clevers, H., Vogelstein, B. and Kinzler, K. W. (1997). Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275, 1787-1790.
28. Naim, H. Y., Dodds, D. T., Brewer, C. B. and Roth, M. G. (1995). Apical and basolateral coated pits of MDCK cells differ in their rates of maturation into coated vesicles, but not in the ability to distinguish between mutant hemagglutinin proteins with different internalization signals. J. Cell Biol. 129, 1241-1250.
29. Neame, S. J., Uff, C. R., Sheikh, H., Wheatley, S. C. and Isacke, C. M. (1995). CD44 exhibits a cell type dependent interaction with Triton X-100 insoluble, lipid rich, plasma membrane domains. J. Cell Sci. 108, 3127-3135.
30. Nosjean, O., Briolay, A. and Roux, B. (1997). Mammalian GPI proteins: sorting, membrane residence and functions. Biochim. Biophys. Acta 1331, 153-186.
31. Powell, S. K., Lisanti, M. P. and Rodriguez-Boulan, E. J. (1991). Thy-1 expresses two signals for apical localization in epithelial cells. Am. J. Physiol. 260, C715-C720.
32. Rached, E., Hooper, N. M., James, P., Semenza, G., Turner, A. J. and Mantei, N. (1990). cDNA cloning and expression in Xenopus laevis oocytes of pig renal dipeptidase, a glycosyl-phosphatidylinositol-anchored ectoenzyme. Biochem. J. 271, 755-760.
33. Rodriguez-Boulan, E. and Gonzalez, A. (1999). Glycans in post-Golgi apical targeting: sorting signals or structural props? Trends Cell Biol. 9, 291-294.
34. Scheiffele, P., Peranen, J. and Simons, K. (1995). N-glycans as apical sorting signals in epithelial cells. Nature 378, 96-98.
35. Scheiffele, P., Verkade, P., Fra, A. M., Virta, H., Simons, K. and Ikonen, E. (1998). Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J. Cell Biol. 140, 795-806.
36. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
37. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, B. J., Olson, B. J. and Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
38. Soole, K. L., Jepson, M. A., Hazlewood, G. P., Gilbert, H. J. and Hirst, B. H. (1995). Epithelial sorting of a glycosylphosphatidylinositol-anchored bacterial protein expressed in polarized renal MDCK and intestinal Caco-2 cells. J. Cell Sci. 108, 369-377.
39. Su, T., Cariappa, R. and Stanley, K. (1999). N-glycans are not a universal signal for apical sorting of secretory proteins. FEBS Lett. 453, 391-394.
40. van't Hoff, W., Rodriguez-Boulan, E. and Menon, A. K. (1995). Nonpolarized distribution of glycosylphosphatidylinositols in the plasma membrane of polarized Madin-Darby canine kidney cells. J. Biol. Chem. 270, 24150-24155.
41. Wessels, H. P., Geffen, I. and Spiess, M. (1989). A hepatocyte-specific basolateral membrane protein is targeted to the same domain when expressed in Madin-Darby canine kidney cells. J. Biol. Chem. 264, 17-20.
42. Yeaman, C., le Gall, A. H., Baldwin, A. N., Monlauzeur, L., le Bivic, A. and Rodriguez-Boulan, E. (1997). The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J. Cell Biol. 139, 929-940.