Phosphoinositide 3-kinase regulates maturation of lysosomes in rat hepatocytes

Biochemical Journal

Volumn 372, Issue 3, 2003, Pages 861-869

  Mousavi, Seyed Ali ^a   Brech, Andreas ^b   Berg, Trond ^a   Kjeken, Rune ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Asialo orosomucoid (ASOR); Endocytosis; Hybrid organelle; Multivesicular body; Phosphoinositide 3 kinase (PI3K); Wortmannin

Indexed keywords

AMINO ACIDS; BIOLOGICAL MEMBRANES; CELLS; MIXTURES;

AUTOPHAGY;

ENZYME INHIBITION;

2 MORPHOLINO 8 PHENYLCHROMONE; ASIALOOROSOMUCOID; CELLOBIOSE; ENZYME INHIBITOR; IODINE 125; LACTATE DEHYDROGENASE; PHOSPHATIDYLINOSITOL 3 KINASE; RECEPTOR PROTEIN; TYRAMINE; WORTMANNIN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL HYBRIDIZATION; CELL LABELING; CELL MATURATION; CELL ORGANELLE; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; INTERNALIZATION; INTRACELLULAR TRANSPORT; LIVER CELL; LIVER LYSOSOME; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; ASIALOGLYCOPROTEINS; BIOLOGICAL TRANSPORT; CHROMONES; ENDOSOMES; ENZYME INHIBITORS; HEPATOCYTES; IODINE RADIOISOTOPES; L-LACTATE DEHYDROGENASE; LYSOSOMES; MALE; MICROSCOPY, ELECTRON; MORPHOLINES; OROSOMUCOID; PHAGOCYTOSIS; RATS; RATS, WISTAR; TYRAMINE;

ANIMALIA;

EID: 0038605721     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021136     Document Type: Article

References (51)

1. Fruman, D. A., Meyers, R. E. and Cantley, L. C. (1998) Phosphoinositide kinases. Annu. Rev. Biochem. 67, 481-507
2. Martin, T. F. (1998) Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu. Rev. Cell. Dev. Biol. 14, 231-264
3. Whiteford, C. C., Best, C., Kazlauskas, A. and Ulug, E. T. (1996) D-3 phosphoinositide metabolism in cells treated with platelet-derived growth factor. Biochem. J. 319, 851-860
4. 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
5. Ui, M., Okada, T., Hazeki, K. and Hazeki, O. (1995) Wortmannin as a unique probe for an intracellular signalling protein, phosphoinositide 3-kinase. Trends Biochem. Sci. 20, 303-307
6. Vlahos, C. J., Matter, W. F., Hui, K.Y. and Brown, R. F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248
7. 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
8. 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
9. Corvera, S., D'Arrigo, A. and Stenmark, H. (1999) Phosphoinositides in membrane traffic. Curr. Opin. Cell Biol. 11, 460-465
10. Corvera, S. and Czech, M. P. (1998) Direct targets of phosphoinositide 3-kinase products in membrane traffic and signal transduction. Trends Cell Biol. 8, 442-446
11. 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, 535-539
12. Shepherd, P. R., Withers, D. J. and Siddle, K. (1998) Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem. J. 333, 471-490
13. Simonsen, A., Lippé, R., Christoforidis, S., Gaullier, J. M., Brech, A., Callaghan, J., Toh, B. H., Murphy, C., Zerial, M. and Stenmark, H. (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature (London) 394, 494-498
14. 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
15. Blommaart, E. F., Krause, U., Schellens, J. P., Vreeling-Sindelarova, H. and Meijer, A. J. (1997) The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243, 240-246
16. Odorizzi, G., Babst, M. and Emr, S. D. (1998) Fab1p Ptdlns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847-858
17. Fernandez-Borja, M., Wubbolts, R., Calafat, J., Janssen, H., Divecha, N., Dusseljee, S. and Neefjes, J. (1999) Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity. Curr. Biol. 9, 55-58
18. Gillooly, D. J., Simonsen, A. and Stenmark, H. (2001) Cellular functions of phosphatidylinositol 3-phosphate and FYVE domain proteins. Biochem. J. 355, 249-258
19. Kjeken, R., Mousavi, S. A., Brech, A., Griffiths, G. and Berg, T. (2001) Wortmannin-sensitive trafficking steps in the endocytic pathway in rat liver endothelial cells. Biochem. J. 357, 497-503
20. Berg, T., Kindberg, G. M., Ford, T. and Blomhoff, R. (1985) Intracellular transport of asialoglycoproteins in rat hepatocytes. Evidence for two subpopulations of endosomes. Exp. Cell Res. 161, 285-296
21. Kovàcs, A. L., Grinde, B. and Seglen, P. O. (1981) Inhibition of autophagic vacuole formation and protein degradation by amino acids in isolated hepatocytes. Exp. Cell Res. 133, 431-436
22. Seglen, P. O. (1976) Preparation of isolated rat liver cells. Methods Cell Biol. 13, 29-83
23. Barrett, A. J. (1972) Lysosomal enzymes. In Lysosomes: A Laboratory Handbook (Dingle, J. T., ed.), pp. 46-135, North-Holland, Amsterdam
24. Kopitz, J., Kisen, G. O., Gordon, P. B., Bohley, P. and Seglen, P. O. (1990) Nonselective autophagy of cytosolic enzymes by isolated rat hepatocytes. J. Cell Biol. 111, 941-953
25. Gaidarov, I., Smith, M. E., Domin, J. and Keen, J. H. (2001) The class II phosphoinositide 3-kinase C2α is activated by clathrin and regulates clathrin-mediated membrane trafficking. Mol. Cell 7, 443-449
26. Seglen, P. O. and Gordon, P. B. (1984) Amino acid control of autophagic sequestration and protein degradation in isolated rat hepatocytes. J. Cell Biol. 99, 435-444
27. Seglen, P. O., Gordon, P. B. and Poli, A. (1980) Amino acid inhibition of the autophagic/lysosomal pathway of protein degradation in isolated rat hepatocytes. Biochim. Biophys. Acta 630, 103-118
28. Mousavi, S. A., Kjeken, R., Berg, T. O., Seglen, P. O., Berg, T. and Brech, A. (2001) Effects of inhibitors of the vacuolar proton pump on hepatic heterophagy and autophagy. Biochim. Biophys. Acta 1510, 243-257
29. Drose, S. and Altendorf, K. (1997) Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol. 200, 1-8
30. Drose, S., Bindseil, K. U., Bowman, E. J., Siebers, A., Zeeck, A. and Altendorf, K. (1993) Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry 32, 3902-3906
31. Weigel, P. H. (1980) Characterization of the asialoglycoprotein receptor on isolated rat hepatocytes. J. Biol. Chem. 255, 6111-6120
32. Holen, I., Stromhaug, P. E., Gordon, P. B., Fengsrud, M., Berg, T. O. and Seglen, P. O. (1995) Inhibition of autophagy and multiple steps in asialoglycoprotein endocytosis by inhibitors of tyrosine protein kinases (tyrphostins). J. Biol. Chem. 270, 12823-12831
33. Kindberg, G. M., Refsnes, M., Christoffersen, T., Norum, K. R. and Berg, T. (1987) The relationship between autophagy and the intracellular degradation of asialoglycoproteins in cultured rat hepatocytes. J. Biol. Chem. 262, 7066-7071
34. Berg, T., Ford, T., Kindberg, G., Blomhoff, R. and Drevon, C. (1985) Intracellular degradation of asialoglycoproteins in hepatocytes starts in a subgroup of lysosomes. Exp. Cell Res. 156, 570-574
35. Nielsen, E., Christoforidis, S., Uttenweiler-Joseph, S., Miaczynska, M., Dewitte, F., Wilm, M., Hoflack, B. and Zerial, M. (2000) Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J. Cell Biol. 151, 601-12
36. Rubino, M., Miaczynska, M., Lippe, R. and Zerial, M. (2000) Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J. Biol. Chem. 275, 3745-3748
37. De Renzis, S., Sonnichsen, B. and Zerial, M. (2002) Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat. Cell Biol. 4, 124-133
38. Chen, X. and Wang, Z. (2001) Regulation of intracellular trafficking of the EGF receptor by Rab5 in the absence of phosphatidylinositol 3-kinase activity. EMBO Rep. 2, 68-74
39. Chen, X. and Wang, Z. (2001) Regulation of epidermal growth factor receptor endocytosis by wortmannin through activation of Rab5 rather than inhibition of phosphatidylinositol 3-kinase. EMBO Rep. 2, 842-849
40. 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, 1251-1264
41. Gary, J. D., Wurmser, A. E., Bonangelino, C. J., Weisman, L. S. and Emr, S. D. (1998) Fab1p is essential for Ptdlns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J. Cell Biol. 143, 65-79
42. Whiteford, C. C., Brearley, C. A. and Ulug, E. T. (1997) Phosphatidylinositol 3,5-bisphosphate defines a novel PI 3-kinase pathway in resting mouse fibroblasts. Biochem. J. 323, 597-601
43. Tolias, K. F., Rameh, L. E., Ishihara, H., Shibasaki, Y., Chen, J., Prestwich, G. D., Cantley, L. C. and Carpenter, C. L. (1998) Type I phosphatidylinositol-4-phosphate 5-kinases synthesize the novel lipids phosphatidylinositol 3,5-bisphosphate and phosphatidylinositol 5-phosphate. J. Biol. Chem. 273, 18040-18046
44. Sbrissa, D., Ikonomov, O. C. and Shisheva, A. (1999) PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin. J. Biol. Chem. 274, 21589-21597
45. 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
46. Mullock, B. M., Bright, N. A., Fearon, G. W., Gray, S. R. and Luzio, J. P. (1998) Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J. Cell Biol. 140, 591-601
47. Luzio, J. P., Rous, B. A., Bright, N. A., Pryor, P. R., Mullock, B. M. and Piper, R. C. (2000) Lysosome-endosome fusion and lysosome biogenesis. J. Cell Sci. 113, 1515-1524
48. Griffiths, G. (1996) On vesicles and membrane compartments. Protoplasma 195, 37-58
49. Bright, N. A., Reaves, B. J., Mullock, B. M. and Luzio, J. P. (1997) Dense core lysosomes can fuse with late endosomes and are re-formed from the resultant hybrid organelles. J. Cell Sci. 110, 2027-2040
50. Desjardins, M. (1995) Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol. 5, 183-186
51. + specifically inhibit clathrin-independent endocytic internalization of bulk fluid. J. Biochem. (Tokyo) 119, 887-897