PIKfyve Controls Fluid Phase Endocytosis but Not Recycling/Degradation of Endocytosed Receptors or Sorting of Procathepsin D by Regulating Multivesicular Body Morphogenesis

Molecular Biology of the Cell

Volumn 14, Issue 11, 2003, Pages 4581-4591

  Ikonomov, Ognian C ^a   Sbrissa, Diego ^a   Foti, Michelangelo ^b   Carpentier, Jean Louis ^b   Shisheva, Assia ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; HORSERADISH PEROXIDASE; PHOSPHATIDYLINOSITOL KINASE; PROCATHEPSIN D; TRANSFERRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELL STRAIN COS1; CELL STRUCTURE; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; ENDOCYTOSIS; GENETIC TRANSFECTION; GOLGI COMPLEX; HUMAN; HUMAN CELL; KIDNEY CELL; LYSOSOME; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RECYCLING; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CATHEPSIN D; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOCYTOSIS; ENZYME PRECURSORS; EXTRACELLULAR FLUID; GOLGI APPARATUS; HORSERADISH PEROXIDASE; HUMANS; LYSOSOMES; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFERRIN; VACUOLES;

ANIMALIA; ARMORACIA RUSTICANA; MAMMALIA;

EID: 0345687290     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-04-0222     Document Type: Article

References (49)

1. Bright, N.A., Lindsay, M.R., Stewart, A., and Luzio, J.P. (2001). The relationship between lumenal and limiting membranes in swollen late endocytic compartments formed after wortmannin treatment or sucrose accumulation. Traffic 2, 631-642.
2. Brown, W.J., DeWald, D.B., Emr, S.D., Plutner, H., and Balch, W.E. (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.
3. Carpentier, J.L., Gorden, P., Amherdt, M., Van Obberghen, E., Kahn, C.R., and Orci, L. (1978). 125I-insulin binding to cultured human lymphocytes. Initiallocalization and fate of hormone determined by quantitative electron microscopic autoradiography. J. Clin. Investig. 61, 1056-1070.
4. Corvera, S. (2001). Phosphatidylinositol 3-kinase and the control of endosome dynamics: new players defined by structural motifs. Traffic 2, 859-866.
5. Davidson, H.W. (1995). Wortmannin causes mistargeting of procathespin D. Evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell Biol. 130, 797-805.
6. Fernandez-Borja, M., Wubbolts, R., Calafat, J., Janssen, H., Divecha, N., Dusseljee, S., and Neefjes, J. (1999). Multivesicular body morphogenesis requires phosphatidylinositol 3-kinase activity. Curr. Biol. 9, 55-58.
7. Fruman, D.A., Meyers, R.E., and Cantley, L.C. (1998). Phosphoinositide kinases. Annu. Rev. Biochem. 67, 481-507.
8. Futter, C.E., Collinson, L.M., Backer, J.M., and Hopkins, C.R. (2001). Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155, 1251-1263.
9. Gary, J.D., Wurmser, A.E., Bonangelino, C.J., Weisman, L.S., and Emr, S.D. (1998). Fab1p is essential for PtdIns(3)P5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J. Cell Biol. 143, 65-79.
10. Ghosh, P., Dahms, N.M., and Kornfeld, S. (2003). Mannose 6-phosphate receptors: new twists in the tail. Nat. Rev. Mol. Cell. Biol. 4, 202-213.
11. Gillooly, D.J., Morrow, I.C., Lindsay, M., Gould, R., Bryant, N.J., Gaullier, J.-M., Parton, R.G., and Stenmark, H. (2000). Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588.
12. Griffiths, G., Matteoni, R., Back, R., and Hoflack, B. (1990). Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J. Cell Sci. 95, 441-461.
13. Gruenberg, J. (2001). The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell. Biol. 2, 721-730.
14. Hewlett, L.J., Prescott, A.R., and Watts, C. (1994). The coated pit and macropinocytic pathways serve distinct endosome populations. J. Cell Biol. 124, 689-703.
15. Hopkins, C.R., Gibson, A., Shipman, M., Strickland, D.K., and Trowbridge, I.S. (1994). In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 125, 1265-1274.
16. Hunziker, W., and Geuze, H.J. (1996). Intracellular trafficking of lysosomal membrane proteins. Bioessays 18, 379-389.
17. 2 production for endomembrane integrity. J. Biol. Chem. 277, 9206-9211.
18. Ikonomov, O.C., Sbrissa, D., and Shisheva, A. (2001). Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve. J. Biol. Chem. 276, 26141-26147.
19. Ikonomov, O.C., Sbrissa, D., Yoshimori, T., Cover, T.L., and Shisheva, A. (2002b). PIKfyve kinase and SKD1 AAA ATPase define distinct endocytic compartments. J. Biol. Chem. 277, 46785-46790.
20. Katzmann, D.J., Odorizzi, G., and Emr, S.D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell. Biol. 3, 893-905.
21. Kundra, R., and Kornfeld, S. (1998). Wortmannin retards the movement of the mannose 6-phosphate/insulin-like growth factor II receptor and its ligand out of endosomes. J. Biol. Chem. 273, 3845-3853.
22. 2 regulation of surface membrane traffic. Curr. Opin. Cell. Biol. 13, 493-499.
23. Martys, J.L., Wjasow, C., Gangi, D.M., Kielian, M.C., McGraw, T.E., and Backer, J.M. (1996). Wortmannin-sensitive trafficking pathways in Chinese hamster ovary cells. J. Biol. Chem. 271, 10953-10962.
24. Mayor, S., Presley, J.F., and Maxfield, R.R. (1993). Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J. Cell Biol. 121, 1257-1269.
25. Miaczynska, M., and Zerial, M. (2002). Mosaic organization of the endocytic pathway. Exp. Cell Res. 272, 8-14.
26. Mills, I.G., Jones, A.T., and Clague, M.J. (1999). Regulation of endosome fusion. Mol. Memb. Biol. 16, 73-79.
27. Mukherjee, S., and Maxfield, F.R. (2000). Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic 1, 203-211.
28. Nordeng, T.W., Gregers, T.F., Kongsvik, T.L., Méresse, S., Gorvel, J.-P., Jourdan, F., Motta, A., and Bakke, O. (2002). The cytoplasmic tail of invariant chain regulates endosome fusion and morphology. Mol. Biol. Cell 13, 1846-1856.
29. Odorizzi, G., Babst, M., and Emr, S.D. (1998). Fablp PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847-858.
30. Odorizzi, G., Babst, M., and Emr, S.D. (2000). Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem. Sci. 25, 229-235.
31. Pfeffer, S. (2003). Membrane domains in the secretory and endocytic pathways. Cell 112, 507-517.
32. Piper, R.C., and Luzio, J.P. (2001). Late endosomes: sorting and partitioning in multivesicular bodies. Traffic 2, 612-621.
33. Rijnboutt, S., Stoorvogel, W., Geuze, H.J., and Strous, G.J. (1992). Identification of subcellular compartments involved in the biosynthetic processing of cathepsin D. J. Biol. Chem. 267, 15665-15672.
34. Row, P.E., Reaves, B.J., Domin, J., Luzio, J.P., and Davidson, H.W. (2001). Overexpression of a rat kinase-deficient phosphoinositide 3-kinase, Vps34p, inhibits cathepsin D maturation. Biochem. J. 353, 655-661.
35. A phosphoinositide 3-kinase in PIKfyve immune complexes from 3T3-L1 adipocytes. Mol. Cell. Endocrinol. 181, 35-46.
36. Sbrissa, D., Ikonomov, O.C., and Shisheva, A. (1999). PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. J. Biol. Chem. 274, 21589-21597.
37. Sbrissa, D., Ikonomov, O.C., and Shisheva, A. (2002a). PtdIns-3-P interacting domains in PIKfyve: binding specificity and role in PIKfyve endomembrane localizations. J. Biol. Chem. 277, 6073-6079.
38. Sbrissa, D., Ikonomov, O.C., Deeb, R., and Shisheva, A. (2002b). Phosphatidylinositol 5-phosphate biosynthesis is linked to PIKfyve and is involved in osmotic response pathway in mammalian cells. J. Biol. Chem. 277, 47276-47284.
39. 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.
40. 2. Cell Biol. Int. 25, 1201-1206.
41. Shisheva, A., Rusin, B., Ikonomov, O.C., DeMarco, C., and Sbrissa, D. (2001). Localization and insulin-regulated relocation of phosphoinositide 5-kinase PIKfyve in 3T3-L1 adipocytes. J. Biol. Chem. 276, 11859-11869.
42. 2+-binding FYVE finger-containing phosphoinositide kinase in insulin-sensitive cells. Mol. Cell. Biol. 19, 623-634.
43. Shpetner, H., Joly, M., Hartley, D., and Corvera, S. (1996). Potential sites of PI-3 kinase function in the endocytic pathway revealed by the PI-3 kinase inhibitor, wortmannin. J. Cell Biol. 132, 595-605.
44. Shurety, W., Stewart, N.L., and Stow, J.L. (1998). Fluid phase markers in the basolateral endocytic pathway accumulate in response to the actin assembly-promoting drug jasplakinolide. Mol. Biol. Cell 9, 957-975.
45. Siddhanta, U.M., McIlroy, J., Shah, A., Zhang, Y., and Backer, J.M. (1998). Distinct roles for the p110α and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J. Cell Biol. 143, 1647-1659.
46. Simonsen, A., Wurmser, A.E., Emr, S.D., and Stenmark, H. (2001). The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13, 485-492.
47. Spiro, D.J., Boll, W., Kirchhausen, T., and Wessling-Resnick, M. (1996). Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol. Biol. Cell 7, 355-367.
48. Wiley, H.S., and Cunningham, D.D. (1982). The endocytic rate constant. J. Biol. Chem. 257, 4222-4229.
49. Yamamoto, A., DeWald, D.B., Boronenkov, 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.