Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro

Molecular Biology of the Cell

Volumn 7, Issue 3, 1996, Pages 355-367

  Spiro, David J ^a   Boll, Werner ^a   Kirchhausen, Tomas ^a   Wessling Resnick, Marianne ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; TRANSFERRIN RECEPTOR; WORTMANNIN;

ARTICLE; CELL SURFACE; DOSE RESPONSE; ENDOCYTOSIS; ENZYME MECHANISM; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; RECEPTOR BINDING; RECEPTOR DENSITY; RECEPTOR DOWN REGULATION;

EID: 0029933270     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.3.355     Document Type: Article

References (50)

1. Acaro, A., and Wymann, M.P. (1993). Wortmannin is a potent phosphatidyl 3-kinase inhibitor: the role of phosphatidyl 3,4,5-triphosphate in neutrophil responses. Biochem. J. 296, 297-301.
2. Ahle, S., Mann, A., Eichelsbacher, U., and Ungewickell, E. (1988). Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J. 7, 919-929.
3. Braell, W.A. (1987). Fusion between endocytic vesicles in a cell-free system. Proc. Natl. Acad. Sci. USA 54, 1137-1141.
4. Brown, W.J., DeWald, D.B., Emr, S.D., Plutner, H., and Balch, W.B. (1995). Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell. Biol. 130, 781-796.
5. Carpenter, C.L., Duckworth, B.C., Auger, K.R., Cohen, B., Schaffhausen, B., and Cantley, L.C. (1990). Purification and characterization of phosphoinositide 3-kinase from rat liver. J. Biol. Chem. 265, 19704-19711.
6. Clague, M.J., Thorpe, C., and Jones, A.T. (1995). Phosphatidylinositol 3-kinase regulation of fluid phase endocytosis. FEBS Lett. 367, 272-274.
7. Clark, J.F., Young, P.W., Yonezawa, K., Kasuga, M., and Holman, G.D. (1994). Inhibition of the translocation of GLUT1 and GLUT4 in 3T3-L1 cells by the phosphatidylinositol 3-kinase inhibitor, wortmannin. Biochem. J. 300, 631-635.
8. Cross, M.J., Stewart, A., Hodgkin, M.N., Kerr, D.J., and Wakelam, M.J.O. (1995). Wortmannin and its structural analogue demethoxyviridin inhibit stimulated phospholipase A2 activity in Swiss 3T3 cells. J. Biol. Chem. 270, 25352-25355.
9. Dautry-Varsat, A., Ciechanover, A., and Lodish, H.F. (1983). pH and the recycling of transferrin during receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA 80, 2258-2262.
10. Davidson, H.W. (1995). Wortmannin causes mistargeting of procathepsin D: evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell. Biol. 130, 797-805.
11. Del Vecchio, R.L., and Pilch, P.F. (1991). Phosphatidyl 4-kinase is a component of glucose transporter (GLUT 4)-containing vesicles. J. Biol. Chem. 266, 13278-13283.
12. Geuze, H.J., Slot, J.W., Strous, G.J.A.M., Peppard, J., Von Figura, K., Hasilik, A., and Schwartz, A.L. (1984). Intracellular receptor sorting during endocytosis: comparative immunoelectron microscopy of multiple receptors in rat liver. Cell 37, 195-204.
13. Griffiths, G., and Gruenberg, J. (1991). The arguments for pre-existing early and late endosomes. Trends Cell Biol 1, 5-9.
14. Gruenberg, J., Griffiths, G., and Howell, K.E. (1989). Characterization of the early endosome and putative carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell. Biol. 108, 1301-1316.
15. Hansen, S.H., Olsson, A., and Casanova, J.E. (1995). Wortmannin, an inhibitor of phosphoinositide 3-kinase, inhibits transcytosis in polarized epithelial cells. J. Biol. Chem. 270, 28425-28432.
16. 2+-activated secretion. Nature 374, 173-177
17. Herman, P.K., and Emr, S.D. (1990). Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevise. Mol. Cell. Biol. 10, 6742-6754.
18. Hues, I.D., et al. (1992). Phosphatidylinositol 3-kinase: structure and expression of the 110 kD catalytic subunit. Cell 70, 419-429.
19. Joly, M, Kazlauskas, A., and Corvera, S. (1995). Phosphatidyl 3-kinase activity is required at a postendocytic step in platelet-derived growth factor receptor trafficking. J. Biol. Chem. 270, 13225-13230.
20. JoIy, M., Kazlauskas, A., Fay, F.S., and Corvera, S (1994). Disruption of PDGF receptor trafficking by mutation of its Pl 3-kinase binding sites. Science 263, 684-687.
21. Jones, A.T., and Clague, M.J. (1995). Phosphatidylinositol 3-kinase activity is required for early endosome fusion. Biochem. J. 311, 31-34.
22. Klausner, R.D., Ashwell, G., Van Renswoude, J., Ashwell, G., Kempf, C., Schechter, A.N., Dean, A., and Bridges, K.R. (1983b). Receptor-mediated endocytosis of transferrin in K562 cells. J Biol. Chem. 258, 4715-4724.
23. Klausner, R.D., Ashwell, G., Van Renswoude, J., Harford, J.B , and Bridges, K.R. (1983a). Binding of apotransferrin to K562 cells: explanation for the transferrin cycle. Proc. Natl. Acad. Sci. USA 80, 2263-2266.
24. Li, G., D'Souza-Schorey, C., Barbieri, M.A., Roberts, R.L., Williams, L.T., and Stahl, P.D. (1995). Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via rab 5. Proc. Natl. Acad. Sci. USA 92, 10207-10211.
25. 2 (PLA2) inhibitors points to a role for PLA2 in endocytosis. Proc. Natl. Acad. Sci. USA 90, 10255-10259.
26. +-ATPase-defective yeast: identification of six new END genes. J. Cell. Biol. 127, 373-386.
27. Murphy, R.F. (1991). Maturation models for endosome and lysosome biogenesis. Trends Cell. Biol. 1, 77-82.
28. Nakanishi, S., Catt, K.J., and Balla, T. (1995). A wortmannin-sensitive phosphatidyl 4-kinase that regulates hormone-sensitive pools of inositolphospholipids. Proc. Natl. Acad. Sci. USA 92, 5317-5321.
29. Ohashi, M., Jan de Vries, K., Frank, R., Snoek, G., Bankaitis, V., Wirtz, K., and Huttner, W.B. (1995). A role for phosphatidylinositol transfer protein in secretory vesicle formation. Nature 377, 544-547.
30. Okada, T., Kawano, Y., Sakakibara, T., Hazeki, O., and Ui, M. (1994). Essential role of phosphatidyl 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. J. Biol. Chem. 269, 3568-3573.
31. Powis, G., et al. (1994). Wortmannin, a selective and potent inhibitor of phosphatidyl 3-kinase. Cancer Res 54, 2419-2423.
32. Robinson, M.S., and Kreis, T.E. (1992). Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell 69, 129-138.
33. Salzman, N.H., and Maxfield, F.R. (1988). Fusion accessibility of endocytic compartments along the recycling and lysosomal endocytic pathways in intact cells. J. Cell. Biol. 109, 2097-2104.
34. Scatchard, G. (1949). The attraction of proteins for small molecules and ions. Ann. NY Acad. Sci. 51, 660-672.
35. Schonhorn, J.E., and Wessling-Resnick, M. (1994). Brefeldin A down-regulates the transferrin receptor in K562 Cells. Mol. Cell Biochem. 135, 159-169.
36. Schu, P.V., Takegawa, K., Fry, M.J., Stack, J.H., Waterfield, M D., and Emr, S.D. (1993). Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260, 88-91.
37. Shepherd, P.R., Soos, M.A., and Siddle, K. (1995). Inhibitors of phosphoinositide 3-kinase block exocytosis but not endocytosis of transferrin receptors in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 211, 533-539.
38. Snider, M.D., and Rogers, O.C. (1985). Intracellular movement of cell surface receptors after endocytosis: resialylation of asialo-transferrin receptor in human erythroleukemia cells. J. Cell Biol 100, 826-834.
39. Stack, J.H., DeWald, D.B., Takegawa, K., and Emr, S D. (1995). Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol. 129, 321-334.
40. Stack, J.H., and Emr, S.D. (1994). VPS34p required for yeast vacuolar protein sorting is a multiple specificity kinase that exhibits both protein kinase and phosphatidylinositol-specific PI 3-kinase activities. J. Biol. Chem. 269, 31552-31562.
41. Stack, J.H., Herman, P.K., Schu, P.V., and Emr, S.D. (1993). A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J. 22, 2195-2204.
42. Stein, B.S., and Sussman, H.H. (1986). Demonstration of two distinct transferrin receptor recycling pathways and transferrin-independent receptor internalization in K562 cells. J. Biol. Chem. 261, 10319-10331.
43. Stephens, L., Smrcka, A., Cooke, F.T., Jackson, T.R., Sternweis, P.C., and Hawkins, P.T. (1994). A novel phosphoinositide 3-kinase activity in myeloid-derived cells is activated by G proteins βγ subunits. Cell 77, 83-93.
44. Stoyanov, B., et al. (1995). Cloning and characterization of a G protein-activated human phosphoinositide 3-kinase. Science 269, 690-693.
45. Volinia, S., Dhand, R., Vanhaesebroeck, B., MacDougall, L.K., Stein, R., Zvelebil, M.J., Domin, J., Panaretou, C., and Waterfield, M.D. (1995). A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system. EMBO J. 14, 3339-3348.
46. Wessling-Resnick, M., and Braell, W.A. (1990). The sorting and segregation mechanism of the endocytic pathway is functional in a cell-free system. J. Biol. Chem. 265, 690-699.
47. Wiley, H.S, and Cunningham, D.D. (1982). The endocytic rate constant J. Biol. Chem. 257, 4222-4229.
48. Yamamoto, A , DeWald, D.B., Borenkov, I.V., Anderson, R.A., Emr, S.D., and Koshland, D. (1995). Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole function and morphology in yeast. Mol. Biol. Cell 6, 525-539.
49. Yamashiro, D.J., and Maxfield, F.R. (1987). Acidification of morphologically distinct endosomes in mutant and wild-type Chinese hamster ovary cells. J. Cell. Biol. 105, 2723-2733.
50. Yamashiro, D.J., Tycko, B., Fluss, S.R., and Maxfield, F.R. (1984) Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37, 789-800.