N-glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells

Journal of Cell Biology

Volumn 146, Issue 2, 1999, Pages 313-320

  Benting, Jürgen H ^b   Rietveld, Anton G ^b   Simons, Kai ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b NONE

Author keywords

GPI anchored proteins; Lipid rafts; Madin Darby canine kidney cells; N glycans; Sorting

Indexed keywords

CELL SURFACE PROTEIN; CHIMERIC PROTEIN; GLYCAN DERIVATIVE; GLYCOSYLPHOSPHATIDYLINOSITOL; GROWTH HORMONE; SECRETORY PROTEIN;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL MEMBRANE TRANSPORT; CELL POLARITY; CELL SURFACE; CONTROLLED STUDY; DOG; IMMUNOFLUORESCENCE MICROSCOPY; KIDNEY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING;

ANIMALIA; CANIS FAMILIARIS;

EID: 0033606823     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.146.2.313     Document Type: Article

References (53)

1. Ahmed, S.N., D.A. Brown, and E. London. 1997. On the origin of sphingolipid-cholesterol rich detergent-insoluble domains in cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry. 36:10944-10953.
2. Alonso, M.A., L. Fan, and B. Alarcon. 1997. Multiple sorting signals determine apical localization of a non-glycosylated integral membrane protein. J. Biol. Chem. 272:30748-30752.
3. Arreaza, G., and D.A. Brown. 1995. Sorting and intracellular trafficking of a glycosylphosphatidylinositol-anchored protein and two hybrid transmembrane proteins with the same ectodomain in Madin-Darby canine kidney epithelial cells. J. Biol. Chem. 270:23641-23647.
4. Brown, D.A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
5. Brown, D.A., and J.K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
6. Brown, D. A., B. Crise, and J.K. Rose. 1989. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science. 245: 1499-1501.
7. Cheong, K.H., D. Zacchetti, E.E. Schneeberger, and K. Simons. 1999. VIP17/ MAL, a lipid raft-associated protein is involved in apical transport in MDCK cells. Proc. Natl. Acad. Sci. USA. 96:6241-6248.
8. Fiedler, K., and K. Simons. 1996. Characterization of VIP36, an animal lectin homologous to leguminous lectins. J. Cell Sci. 109:271-276.
9. Fiedler, K., R.G. Parton, R. Kellner, T. Etzold, and K. Simons. 1994. VIP36, a novel component of glycolipid rafts and exocytic carrier vesicles in epithelial cells. EMBO (Eur. Mol. Biol. Organ.) J. 13:1729-1740.
10. Fiedler, K., F. Lafont, R.G. Parton, and K. Simons. 1995. Annexin XIIIb: a novel epithelial specific annexin is implicated in vesicular traffic to the apical plasma membrane. J. Cell Biol. 128:1043-1053.
11. Friedrichson, T., and T.V. Kurzchalia. 1998. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature. 394:802-805.
12. Füllekrug, J., P. Scheiffele, and K. Simons. 1999. VIP36 localisation to the early secretory pathway. J. Cell Sci. In press.
13. Gottlieb, T.A., G. Beaudry, L. Rizzolo, A. Colman, M. Rindler, M. Adesnik, and D.D. Sabatini. 1986. Secretion of endogenous and exogenous proteins from polarized MDCK cell monolayers. Proc. Natl. Acad. Sci. USA. 83: 2100-2104.
14. Guan, J.-L., and J.K. Rose. 1984. Conversion of a secretory protein into a transmembrane protein results in its transport to the Golgi complex but not to the cell surface. Cell. 37:779-787.
15. Guan. J.L., C.E. Machamer, and J.K. Rose. 1985. Glycosylation allows cell-surface transport of an anchored secretory protein. Cell. 42:489-496.
16. Gut, A., F. Kappeler, N. Hyka, M.S. Balda, H.-P. Hauri, and K. Matter. 1998. Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins. EMBO (Eur. Mol. Biol. Organ.) J. 17:1919-1929.
17. Hannan, L.A., and M. Edidin. 1996. Traffic, polarity, and detergent solubility of a glycosylphosphatidylinositol-anchored protein after LDL deprivation of MDCK cells. J. Cell Biol. 133:1265-1276.
18. Hannan, L.A., M.P. Lisanti, E. Rodriguez-Boulan, and M. Edidin. 1993. Correctly sorted molecules of a GPI-anchored protein are clustered and immobile when they arrive at the apical surface of MDCK cells. J. Cell Biol. 120: 353-358.
19. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929-942.
20. He, T.-C., S. Zhou, L.T. da Costa, K.W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA. 95:2509-2514.
21. Keller, P., and K. Simons. 1998. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140:1357-1367.
22. Kenworthy, A.K., and M. Edidin. 1998. Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 A using imaging fluorescence resonance energy transfer (published erratum appeared in J. Cell Biol. 1998. 142:883). J. Cell Biol. 142: 69-84.
23. Kondor-Koch, C., R. Bravo, S.D. Fuller, D. Cutler, and H. Garoff. 1985. Exocytic pathways exists to both the apical and the basolateral cell surface of the polarized epithelial cell MDCK. Cell. 43:297-306.
24. Lafont, F., S. Lecat, P. Verkade, and K. Simons. 1998. Annexin XIIIb associates with lipid microdomains to function in apical delivery. J. Cell Biol. 142:1413-1427.
25. Lisanti, M.P., M. Sargiacomo, L. Graeve, A.R. Saltiel, and E. Rodriguez-Boulan. 1988. Polarized apical distribution of glycosyl-phosphatidylinositol-anchored proteins in a renal epithelial cell line. Proc. Natl. Acad. Sci. USA. 85:9557-9561.
26. Lisanti, M.P., I.W. Caras, M.A. Davitz, and E. Rodriguez-Boulan. 1989. A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J. Cell Biol. 109:2145-2156.
27. Lisanti, M.P., A. Le Bivic, A.R. Saltiel, and E. Rodriguez-Boulan. 1990. Preferred apical distribution of glycosyl-phosphatidylinositol (GPI) anchored proteins: a highly conserved feature of the polarized epithelial cell phenotype. J. Membr. Biol. 113:155-167.
28. Marzolo, M.P., P. Bull, and A. Gonzalez. 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.
29. Matter, K., and I. Mellman. 1994. Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr. Opin. Cell Biol. 6:545-554.
30. Matter, K., W. Hunzicker, and I. Mellman. 1992. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell. 71:741-753.
31. Mays, R.W., K.A. Siemers, B.A. Fritz, A.W. Lowe, G. van Meer, and W.J. Nelson. 1995. Hierarchy of mechanisms involved in generating Na/K-ATPase polarity in MDCK epithelial cells. J. Cell Biol. 130:1105-1115.
32. Mertens, G., B. van der Schueren, H. van den Berghe, and G. David. 1996. Heparan sulfate expression in polarized epithelial cells: the apical sorting of glypican (GPI-anchored proteoglycan) is inversely related to its heparan sulfate content. J. Cell Biol. 132:487-497.
33. Naim, H.Y., D.T. Dodds, C.B. Brewer, and M.G. Roth. 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.
34. Neame, S.J., and C.M. Isacke. 1993. The cytoplasmic tail of CD44 is required for basolateral localization in epithelial MDCK cells but does not mediate association with the detergent-insoluble cytoskeleton of fibroblasts. J. Cell Biol. 121:1299-1310.
35. Neame, S.J., C.R. Uff, H. Sheikh, S.C. Wheatly, and C.M. Isacke. 1995. CD44 exhibits a cell type dependent interaction with Triton X-100 insoluble, lipid-rich, plasma membrane domains. J. Cell Sci. 108:3127-3135.
36. Pimplikar, S.W., E. Ikonen, and K. Simons. 1994. Basolateral protein transport in streptolysin O-permeabilized MDCK cells. J. Cell Biol. 125:1025-1035.
37. Powell, S.K., M.P. Lisanti, and E. Rodriguez-Boulan. 1991. Thy-1 expresses two signals for apical localization in epithelial cells. Am. J. Physiol. 260:C715-C720.
38. Rietveld, A., and K. Simons. 1998. The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim. Biophys. Acta. 1376:467-479.
39. Rodriguez-Boulan, E., and A. Gonzalez. 1999. Apical sorting signals in epithelia. Trends Cell Biol. In press.
40. Rodriguez-Boulan, E., and S.K. Powell. 1992. Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol. 8:395-427.
41. Scheiffele, P., J. Peranen, and K. Simons. 1995. N-glycans as apical sorting signals in epithelial cells. Nature. 378:96-98.
42. Scheiffele, P., M.G. Roth, and K. Simons. 1997. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO (Eur. Mol. Biol. Organ.) J. 16:5501-5508.
43. Scheiffele, P., P. Verkade, A.M. Fra, H. Virta, K. Simons, and E. Ikonen. 1998. Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J. Cell Biol. 140: 795-806.
44. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
45. Simons, K., and G. van Meer. 1988. Lipid sorting in epithelial cells. Biochemistry. 27:6197-6202.
46. Soole, K.L., M.A. Jepson, G.P. Hazlewood, H.J. Gilbert, and B.H. Hirst. 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.
47. Urban, J., K. Parczyk, A. Leutz, M. Kayne, and C. Kondor-Koch. 1987. Constitutive apical secretion of an 80-kD sulfated glycoprotein in the polarized epithelial Madin-Darby canine kidney cell line. J. Cell Biol. 105:2735-2743.
48. van Meer, G. 1989. Lipid traffic in animal cells. Annu. Rev. Cell Biol. 5:247-275.
49. van't Hof, W., B.E. Rodriguez, and A.K. Menon. 1995. Nonpolarized distribution of glycosylphosphatidylinositols in the plasma membrane of polarized Madin-Darby canine kidney cells. J. Biol. Chem. 270:24150-24155.
50. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394:798-801.
51. Yeaman, C., A.H. Le Gall, A.N. Baldwin, L. Monlauzeur, A. Le Bivic, and E. Rodriguez-Boulan. 1997. The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J. Cell Biol. 139:929-940.
52. Zheng, X., D. Lu, and J.E. Sadler. 1999. Apical sorting of bovine enteropeptidase does not involve detergent-resistant association with sphingolipid-cholesterol rafts. J. Biol. Chem. 274:1596-1605.
53. Zurzolo, C., M.P. Lisanti, I.W. Caras, L. Nitsch, and E. Rodriguez-Boulan. 1993. Glycosyl-phosphatidylinositol-anchored proteins are preferentially targeted to the basolateral surface in Fischer rat thyroid epithelial cells. J. Cell Biol. 121:1031-1039.