Traffic, polarity, and detergent solubility of a glycosylphosphatidylinositol-anchored protein after LDL-deprivation of MDCK cells

Journal of Cell Biology

Volumn 133, Issue 6, 1996, Pages 1265-1276

  Hannan, Lisa A ^a,b   Edidin, Michael ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; DOG; EPITHELIUM CELL; INTRACELLULAR TRANSPORT; LIPID MEMBRANE; MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; TRANSPORT KINETICS;

ANIMALS; BIOLOGICAL TRANSPORT; CELL FRACTIONATION; CELL LINE; CELL MEMBRANE; CELL POLARITY; CHOLESTEROL; CHOLESTEROL, LDL; DETERGENTS; DOGS; ENDOCYTOSIS; GLYCOSYLATION; GLYCOSYLPHOSPHATIDYLINOSITOLS; HEXOSAMINIDASES; KIDNEY; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; OCTOXYNOL; PHOSPHATIDYLINOSITOL DIACYLGLYCEROL-LYASE; PHOSPHORIC DIESTER HYDROLASES; SOLUBILITY;

ANIMALIA; CANIS FAMILIARIS;

EID: 0029894832     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.133.6.1265     Document Type: Article

References (74)

1. Apodaca, G., L.A. Katz, and K.E. Mostov. 1994. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125:67-86.
2. yes. J. Biol. Chem. 269:19123-19127.
3. Bastiaanse, E.M., D.E. Atsma, M.M. Kuijpcrs, and A. Van der Laarse. 1994. The effect of sarcolemmal cholesterol content on intracellular calcium ion concentration in cultured cardiomyocytes. Arch. Biochem. Biophys. 313:58-63.
4. Bonnekoh, B., S. Daefler, G.R. Kruger, and G. Mahrle. 1990. Keratinocyte lipid fluidity under the influence of cholesterols, hydrocortisones, active lipid, tocopherol and retinoic acid-a fluorescence polarization study with regard to physiological and pathophysiological epidermopoiesis and its therapeutics. In Vivo (Attiki). 5:227-232.
5. Bordier, C. 1981. Phase separation of integral memhrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604-1607.
6. Brasitus, T.A., R. Dahiya, P.K. Dudeja, and B.M. Bissonelle. 1988. Cholesterol modulates alkaline phosphatase activity of rat intestinal microvillus membranes. J. Biol. Chem. 263:8592-8597.
7. Brown, D.A., and J.K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched memhrane subdomains during transport to the apical cell surface. Cell. 67:533-544.
8. Brown, D.A., B. Crise and J.K. Rose. 1989. Mechanism of anchoring affects polarized expression of two proteins in MDCK cells. Science. 245:1499-1501.
9. Cerneus, D.P., E. Ueffing, G. Posthuma, G.J. Strous, and A. van der Ende. 1993. Detergent insolubility of alkaline phosphatase during biosynthelic transport and endocytosis. J. Biol. Chem. 268:3150-3155.
10. Chang, W.J., K.G. Rothberg, B.A. Kamen, and R.G.W. Anderson. 1992. Lowering the cholesterol content of MA104 cells inhibits receptor-mediated transport of folate. J. Cell Biol. 118:64-69.
11. Cheetham, J.J., S. Nir, E. Johnson, T.D. Flanagan, and R.M. Epand. 1994. The effects of membrane physical properties on the fusion of Sendai virus with human erythrocyte ghosts and liposomes. Analysis of kinetics and extent of fusion. J. Biol. Chem. 269:5467-5472.
12. Cinek, T., and V. Horejsi. 1992. The nature of large non-covalent complexes containing glycosyl-phosphatidy-inositol-anchored membrane glycoproteins and protein tyrosine kinases. J. Immunol. 149:2262-2270.
13. Danielsen, E.M. 1995. Involvement of detergent-insoluble complexes in the intracellular transport of brush border enzymes. Biochemistry. 34:1596-1605.
14. Esfahani, M., R.D. Bigler, J.L. Alfieri, S. Lund-Katz, J.D. Baum, and L. Scerbo. 1993a. Cholesterol regulates the cell surface expression of glycophopspholipid-anchored CD14 antigen on human monocytes. Biochem. Biophys. Acta. 1149:217-223.
15. Esfahani, M., R.D. Bigler, and D. Gressen. 1993b. Effect of lovastatin on cell surface expression of Fc receptor or CD14 antigen in human monocytes. Biochem. Pharmacol. 46:2333-2336.
16. Fiedler, K., T. Kobayashi, T. V. Kurzchalia, and K. Simons. 1993. Glycosphingolipid-enriched, detergent-insoluble complexes in protein sorting in epithelial cells. Biochemistry. 32:6365-6373.
17. Gamble, W., M. Vaughan, H.S. Kruth, and J. Avignon. 1978. Procedure for determination of free and total cholesterol in micro- or nanogram amounts suitable for studies with cultured cells. J. Lipid Res. 19:1068-1070.
18. Garcia, M., C. Mirre, A. Quaroni, H. Reggio, and A. Le Bivic. 1993. GPI anchored proteins associate to form microdomains during their intracellular transport in Caco-2 cells. J. Cell Sci. 104:1281-1290.
19. Gennis, R.B. 1989. Biomembranes. Molecular Structure and Function. Springer-Verlag, New York.
20. Giocondi, M.-C., G. Friedlander, and C. Le Grimellec. 1990. ADH modulates plasma membrane lipid order of living MDCK cells via a cAMP-dependent process. Am. J. Physiol. 259:F95-F103.
21. Goldstein, J.L., and M.S. Brown. 1990. Regulation of the mevalonate pathway. Nature (Lond.). 343:425-430.
22. Hamilton K.S., K. Briere, H.C. Jarrell, and C.W. Grant. 1994. Acyl chain length effects related to glycosphingolipid crypticity in phospholipid membranes: probed by 2H-NMR. Biochim. Biophys. Acta. 1190:367-75.
23. Hanada, K., K. Ikezawa, M. Nishijima, and Y. Akamalsu. 1993. Sphingolipid deficiency induces hypersensitivity of CD14, a glycosyl phosphatidylinositolanchored protein, to phosphatidylinositol-specific phospholipase C. J. Biol. Chem. 268:13820-13823.
24. Hanada, K., M. Nishijima, Y. Akamatsu, and R.E. Pagano. 1995. Both sphingolipids and cholesterol participate in the detergent-insolubility of alkaline phosphatase, a glycosyl-phosphatidyinositol anchored protein in mammalian cells. J. Biol. Chem. 270:6254-6260.
25. Hannan, L.A., M. 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.
26. Khury, J.G., P. Fonteneau, G. Duportail, C. Maechling, and G. Laustrial. 1983. TMA-DPH: a suitable fluorescence polarization probe for specific plasma membrane fluidity studies in intact living cells. Cell Biophys. 5:129-140.
27. Koke, J.A., M. Yang, D.J. Henner, J.J. Volwerk, and O.H. Griffiths. 1991. High level expression in Escherichia coli and rapid purification of phosphatidyl-inositol-specific phospholipase C from Bucillus cereus and Bacillus thurin-giensis. Protein Expr. Purif. 2:51-58.
28. Leikin, A.I., and R.R. Brenner. 1988. In vivo cholesterol removal from liver microsomes induces changes in fatty acid desaturase activities. Biochim. Biophys. Acta. 963:311-319.
29. Lentz, B.R. 1989. Membrane "fluidity" as detected by diphenylhexatriene probes. Chem. Phys. Lipids. 50:171-190.
30. Li, C., S. Stifani, W.J. Schneider, and M.J. Poznansky. 1991. Low density lipoprutein receptors on epithelial cell (Madin-Darby canine kidney) monolayers. J. Biol. Chem. 266:9263-9270.
31. Lipsky, N.G., and R.E. Pagano. 1985. A vital stain for the Golgi apparatus. Science (Wash. DC). 228:745-747.
32. Lisanti, M.P., and E. Rodriguez-Boulan. 1990. Glycophospholipid membrane anchoring provides clues to the mechanism of protein sorting in polarized epithelial cells. Trends Bioclmn. Sci. 15:113-118.
33. 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.
34. 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.
35. Lisanti, M.P., Z-L. Tang and M. Sargiacomo. 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.
36. Lutton, C. 1991. Dietary cholesterol, membrane cholesterol and cholesterol synthesis. Biochimie (Paris). 73:1327-1334.
37. Mangold, H.K. 1969. Aliphatic lipids. In Thin Layer Chromatography. E. Stahl, editor. Springer-Verlag, New York, pp 363-121.
38. Martin, O.C., M.E. Comley, J. Blanchette-Mackie, P.O. Pentchev and R.E. Pagano. 1993. Cholesterol deprivation affects the fluorescence properties of a ceramide analog at the golgi apparatus of living cells. Proc. Natl. Acad. Sci. (USA). 90:2661-2665.
39. Matter, K., and I. Mellman. 1994. Mechanism of cell polarity: sorting and transport in epithelial cells. Curr. Opin. Cell Biol. 6:545-554.
40. Mayor, S., K.G. Rothberg, and F.R. Maxfield. 1994. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science (Wash. DC). 264:1948-1951.
41. Mayor, S., and F.R. Maxfield. 1995a. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol. Biol. Cell. 6:929-944.
42. Mayor, S., and F.R. Maxfield. 19956. Cholesterol-dependent sorting of GPI-anchored proteins in endosomes. Mol. Biol. Cell. 6:231a.
43. Muriana, F.J.G., C.M. Vasquez, and V. Ruiz-Guiterrez. 1992. Fatty acid composition and properties of rats fed diets enriched with cholesterol. J. Biochem. 112:562-567.
44. Nieva, J.L., R. Bron, J. Corver, and J. Wilschut. 1994. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO (Eur. Mol. Biol. Organ.) J. 13:2797-2804.
45. Novak, D.A., J.D. Carver, M. Ananthanarayanan, and W. Ray. 1994. Diet affects hepatocyte membrane composition, fluidity, and taurocholate transport in suckling rats. Am. J. Physiol. 1994. 267:G301-307.
46. Rodriguez-Lafrasse, C., R. Rousson, J. Bonnet, P.G. Penchev, P. Louisot, and M.T. Varier. 1990. Abnormal cholesterol metabolism in imipramine-treated fibroblast cultures. Similarities with Niemann Pick type C disease. Biochim. Biophys. Acta. 1043:123-128.
47. Roff, C.F., E. Golhin, M.E. Comly, A. Cooney, A. Brown, M.T. Vanier, S.P.F. Miller, R.O. Brady, and P.G. Penchev. 1993. Type C Niemann Pick disease: use of hydrophobic Amines to study defective cholesterol transport. Dev. Neurosci. 13:315-319.
48. Rosenwald, A.G., C.E. Machamer, and R.E. Pagano. 1992. Effects of sphingolipid synthesis inhibitor on membrane transport through the secretory pathway. Biochemistry. 31:3581-3590.
49. Rothnerg, K.G., Y.S. Ying, B.A. Kamen, and R.G.W. Anderson. 1990a. Cholesterol controls the clustering of glycophospholipid-anchored membrane receptor for the 5-inethyltetrahydrofolate. J. Cell Biol. 111:2931-2938.
50. Rothberg, K.G., Y.S. Ying, J.F. Kolhouse, B.A. Kamen, and R.G.W. Anderson. 1990b. The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J. Cell Biol. 110:637-649.
51. Sargiacomo, M., M. Sudol, Z. Tang, and M.P. Lisanti. 1993. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122:789-807.
52. Schroeder, R., E. London, and D. Brown. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc. Natl. Acad. Sci. USA 91:12130-12134.
53. Schnitzer, J.E., D.P. McIntosh, A.M. Dvorak, J. Liu, and P. Oh. 1995. Separation of caveolae from associated microdomains of GPI-anchored proteins. Science (Wash. DC). 269:1435-1439.
54. Schnitzer, J.E., P. Oh, E. Pinney, and J. Allard. 1994. Filipin-sensitive caveolae mediated transport in endothelium: reduced transcytosis, scavenger endocytosis. and capillary permeability of select macromolecules. J. Cell Biol. 127:1217-1232.
55. Shakarjian, M.P., E. Eiseman, R.C. Penhallow, and J.B. Bolen. 1993.3-Hydroxyl-3-melhylgluatryl-coenyzymeA reductase inhibition in a rat mast cell line. J. Biol. Chem. 268:15252-15259.
56. Shenoy-Scaria, A.M., D.J. Dietzen, J. Kwong, and D.C. Link. 1994. Cysleine of Src family protein tyrosine kinases determines palmitoylation and localization in caveolae. J. Cell. Biol. 126:353-363.
57. Shinitzky, M. 1984. Membrane fluidity and cellular functions. In Physiology of Membrane Fluidity. Vol. 1. (M. Shinilzky, editor). CRC Press, Boca Raton. FL. 1-51.
58. Shinitzky, M., and Y. Barenholz. 1978. Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim. Biophys. Acta. 525:367-394.
59. Showalter, S.D., M. Zweig, and B. Hampar. 1981. Monoclonal antibodies to Herpes simplex virus type I proteins, including the immediate-early protein ICP-4. Infect. Immun. 34:684-692.
60. Simons, K., and A. Wandinger-Ness. 1990. Polarized sorting in epithelia. Cell. 62:207-210.
61. Sinensky, M. 1980. Adaptive alterations in phospholipid composition of plasma membranes from a somatic cell mutant defective in the regulation of cholesterol biosynthesis. J. Cell Biol 85:166-169.
62. Skibbens, J.E., M.G. Roth, and K.S. Matlin. 1989. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts. J. Cell Biol. 108:821-832.
63. Sleight, R.G., and R.E. Pagano. 1984. Transhilayer movement of a fluorescent phosphatidylethanolamine analog across the plasma membranes of culture mammalian cells. J. Cell Biol. 99:742-751.
64. Smart, E.J., Y-S. Ying, P.A. Conrad, and R.G.W. Anderson. 1994. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127:1185-1197.
65. Stefanova, I., and V. Horejsi. 1991. Association of CD59 and CD55 cell surface glycoproteins with other membrane molecules. J. Immunol. 147:1587-1592.
66. Stefanova, I., V. Horejsi, I.J. Ansotegui, W. Knapp, and H. Stockinger. 1991. GPI-anchored cell surface molecules compiexed to protein tyrosine kinases. Science (Wash. DC). 254:1016-1019.
67. Taraboulos, A., M. Scott, A. Semenov, D. Avraham, L. Laszlo, and S.B. Prusiner. 1995. Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J. Cell Biol. 129:121-132.
68. Tarshis, M., M. Salman, and S. Rottem. 1993. Cholesterol is required for the fusion of single unilamellar vesicles with Mycoplasma capricolum. Biophys. J. 64:707-715.
69. Terasaki, M., L.B. Chen, and K. Fujiwara. 1986. Microtubules and ER are highly interdependent structures. J. Cell Biol. 103:1557.
70. Toptygin, D., and L. Brand. 1995. Determination of DPH order parameters in unoriented vesicles. J. Fluorescence. 5:39-49.
71. Urbani, L., and R.D. Simoni. 1990. Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulm to the plasma membrane. J. Biol. Chem. 265:1919-1923.
72. Wassler, M., I. Jonasson, R. Perssun, and E. Fries. 1987. Differential permeabilization of membranes by saponin treatment of isolated rat hepatocytes. Biochem. J. 247:407-415.
73. Weisz, O.A., C.E. Machamer, and A.L. Hubbard. 1992. Rat liver dipeptidylpeptidase IV contains competing apical and basolateral targeting information. J. Biol. Chem. 267:22282-22288.
74. Zurzolo, C., W. van't Hof, G. van Meer, and E. Rodriguez-Boulan. 1994. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO (Eur. Mol. Biol. Organ.) J. 13:42-53.