Inhibitors of phosphoinositide 3-kinase cause defects in the postendocytic sorting of β2-adrenergic receptors

Experimental Cell Research

Volumn 313, Issue 12, 2007, Pages 2586-2596

  Awwad, Hibah O ^a   Iyer, Varsha ^a   Rosenfeld, Jennifer L ^a   Millman, Ellen E ^b   Foster, Estrella ^a   Moore, Robert H ^b   Knoll, Brian J ^a  

^a UNIVERSITY OF HOUSTON   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Endosomes; Lysosomes; PI 3 kinase; rab7; 2 adrenergic receptors

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BETA 2 ADRENERGIC RECEPTOR; ISOPRENALINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; RAB7 PROTEIN; WORTMANNIN;

ARTICLE; CELL STRAIN HEK293; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION;

EID: 34347211051     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.04.034     Document Type: Article

References (44)

1. 2-adrenergic receptor using phosphoserine-specific antibodies. Mol. Pharmacol. 65 (2004) 196-206
2. Benovic J.L., Strasser R.H., Caron M.G., and Lefkowitz R.J. β-Adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 2797-2801
3. Yuan N., Friedman J., Whaley B.S., and Clark R.B. cAMP-dependent protein kinase and protein kinase C consensus site mutations of the β-adrenergic receptor. Effect on desensitization and stimulation of adenylyl cyclase. J. Biol. Chem. 269 (1994) 23032-23038
4. Lohse M.J., Benovic J.L., Codina J., Caron M.G., and Lefkowitz R.J. β-Arrestin: a protein that regulates β-adrenergic function. Science 248 (1990) 1547-1550
5. 2-adrenergic receptor. Nature 383 (1996) 447-450
6. 2-adrenergic receptor/β-arrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3712-3717
7. 2-adrenergic receptors between the plasma membrane and endosomes containing transferrin receptors. J. Biol. Chem. 267 (1992) 3530-3538
8. 2-adrenergic receptor internalization via the constitutive endocytic pathway into rab5-containing endosomes. J. Cell Sci. 108 (1995) 2983-2991
9. 2-adrenergic receptor. J. Biol. Chem. 273 (1998) 6976-6981
10. 2-adrenergic receptors to lysosomes during downregulation. J. Cell Sci. 112 (1999) 329-338
11. Schu P.V., Takegawa K., Fry M.J., Stack J.H., Waterfield M.D., and Emr S.D. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260 (1993) 88-91
12. Jess T.J., Belham C.M., Thomson F.J., Scott P.H., Plevin R.J., and Gould G.W. Phosphatidylinositol 3′-kinase, but not p70 ribosomal S6 kinase, is involved in membrane protein recycling: wortmannin inhibits glucose transport and downregulates cell-surface transferrin receptor numbers independently of any effect on fluid-phase endocytosis in fibroblasts. Cell. Signal. 8 (1996) 297-304
13. Shpetner H., Joly M., Hartley D., and Corvera S. Potential sites of PI-3 kinase function in the endocytic pathway revealed by the PI-3 kinase inhibitor, wortmannin. J. Cell Biol. 132 (1996) 595-605
14. Spiro D.J., Boll W., Kirchhausen T., and Wessling-Resnick M. Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol. Biol. Cell 7 (1996) 355-367
15. Martys J.L., Wjasow C., Gangi D.M., Kielian M.C., McGraw T.E., and Backer J.M. Wortmannin-sensitive trafficking pathways in Chinese hamster ovary cells. Differential effects on endocytosis and lysosomal sorting. J. Biol. Chem. 271 (1996) 10953-10962
16. Joly M., Kazlauskas A., and Corvera S. Phosphatidylinositol 3-kinase activity is required at a postendocytic step in platelet-derived growth factor receptor trafficking. J. Biol. Chem. 270 (1995) 13225-13230
17. Reaves B.J., Bright N.A., Mullock B.M., and Luzio J.P. The effect of wortmannin on the localisation of lysosomal type I integral membrane glycoproteins suggests a role for phosphoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway. J. Cell Sci. 109 (1996) 749-762
18. Hunyady L., Baukal A.J., Gaborik Z., Olivares-Reyes J.A., Bor M., Szaszak M., Lodge R., Catt K.J., and Balla T. Differential PI 3-kinase dependence of early and late phases of recycling of the internalized AT1 angiotensin receptor. J. Cell Biol. 157 (2002) 1211-1222
19. 2-adrenergic receptor during agonist-induced steady-state redistribution. Mol. Pharmacol. 50 (1996) 692-699
20. Hiraoka Y., Sedat J.W., and Agard D.A. The use of a charge-coupled device for quantitative optical microscopy of biological structures. Science 238 (1987) 36-41
21. Vlahos C.J., Matter W.F., Hui K.Y., and Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269 (1994) 5241-5248
22. van Dam E.M., Ten Broeke T., Jansen K., Spijkers P., and Stoorvogel W. Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J. Biol. Chem. 277 (2002) 48876-48883
23. Shepherd P.R., Soos M.A., and Siddle K. Inhibitors of phosphoinositide 3-kinase block exocytosis but not endocytosis of transferrin receptors in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 211 (1995) 535-539
24. Oakley R.H., Laporte S.A., Holt J.A., Barak L.S., and Caron M.G. Association of β-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J. Biol. Chem. 274 (1999) 32248-32257
25. Futter C.E., Collinson L.M., Backer J.M., and Hopkins C.R. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155 (2001) 1251-1264
26. Petiot A., Faure J., Stenmark H., and Gruenberg J. PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J. Cell Biol. 162 (2003) 971-979
27. Vanhaesebroeck B., Leevers S.J., Ahmadi K., Timms J., Katso R., Driscoll P.C., Woscholski R., Parker P.J., and Waterfield M.D. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70 (2001) 535-602
28. Siddhanta U., McIlroy J., Shah A., Zhang Y., and Backer J.M. Distinct roles for the p110a and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J. Cell Biol. 143 (1998) 1647-1659
29. Stein M.P., Feng Y., Cooper K.L., Welford A.M., and Wandinger-Ness A. Human VPS34 and p150 are rab7 interacting partners. Traffic 4 (2003) 754-771
30. Gillooly D.J., Morrow I.C., Lindsay M., Gould R., Bryant N.J., Gaullier J.M., Parton R.G., and Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19 (2000) 4577-4588
31. Gillooly D.J., Raiborg C., and Stenmark H. Phosphatidylinositol 3-phosphate is found in microdomains of early endosomes. Histochem. Cell Biol. 120 (2003) 445-453
32. Gaullier J.M., Simonsen A., D'Arrigo A., Bremnes B., Stenmark H., and Aasland R. FYVE fingers bind PtdIns(3)P. Nature 394 (1998) 432-433
33. Ellson C.D., Andrews S., Stephens L.R., and Hawkins P.T. The PX domain: a new phosphoinositide-binding module. J. Cell Sci. 115 (2002) 1099-1105
34. 2-adrenergic receptor and β-arrestin. Science 294 (2001) 1307-1313
35. Chavrier P., Parton R.G., Hauri H.P., Simons K., and Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62 (1990) 317-329
36. Feng Y., Press B., and Wandinger-Ness A. Rab7: an important regulator of late endocytic membrane traffic. J. Cell Biol. 131 (1995) 1435-1452
37. Mukhopadhyay A., Funato K., and Stahl P.D. Rab7 regulates transport from early to late endocytic compartments in Xenopus oocytes. J. Biol. Chem. 272 (1997) 13055-13059
38. Vitelli R., Santillo M., Lattero D., Chiariello M., Bifulco M., Bruni C.B., and Bucci C. Role of the small GTPase RAB7 in the late endocytic pathway. J. Biol. Chem. 272 (1997) 4391-4397
39. Press B., Feng Y., Hoflack B., and Wandinger-Ness A. Mutant rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J. Cell Biol. 140 (1998) 1075-1089
40. Dale L.B., Seachrist J.L., Babwah A.V., and Ferguson S.S. Regulation of angiotensin II type 1A receptor intracellular retention, degradation, and recycling by Rab5, Rab7, and Rab11 GTPases. J. Biol. Chem. 279 (2004) 13110-13118
41. Ceresa B.P., and Bahr S.J. rab7 activity affects epidermal growth factor: epidermal growth factor receptor degradation by regulating endocytic trafficking from the late endosome. J. Biol. Chem. 281 (2006) 1099-1106
42. 2-adrenergic and muscarinic cholinergic receptor endocytosis after depletion of phosphatidylinositol bisphosphate. J. Pharmacol. Exp. Ther. 290 (1999) 603-610
43. Naga Prasad S.V., Barak L.S., Rapacciuolo A., Caron M.G., and Rockman H.A. Agonist-dependent recruitment of phosphoinositide 3-kinase to the membrane by β-adrenergic receptor kinase 1. A role in receptor sequestration. J. Biol. Chem. 276 (2001) 18953-18959
44. 2-Adrenergic receptor endocytic pathway is controlled by a saturable mechanism distinct from that of transferrin receptor. Recept. Channels 6 (1999) 255-269