Published online 11 August 2003. doi:10.1083/jcb.200302051
© The Rockefeller University Press,
0021-9525/2003/8/693 $5.00
The Journal of Cell Biology, Volume 162, Number 4, 693-701
Phosphatidylinositol phosphate 5-kinase Iß recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis
David Padrón1,
Ying Jie Wang2,
Masaya Yamamoto2,
Helen Yin2 and
Michael G. Roth1
1 Department of Biochemistry, The University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390
2 Department of Physiology, The University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390
Address correspondence to Michael G. Roth, The University of Texas Southwestern, 5323 Harry Hines Blvd., Dallas, TX 75930-9038. Tel.: (214) 648-3276. Fax: (214) 648-8856. email: michael.roth{at}utsouthwestern.edu
Overexpression of phosphatidylinositol phosphate 5-kinase (PIP5KI) isoforms
, ß, or
in CV-1 cells increased phosphatidylinositol 4,5-bisphosphate (PIP2) levels by 35, 180, and 0%, respectively. Endocytosis of transferrin receptors, association of AP-2 proteins with membranes, and the number of clathrin-coated pits at the plasma membrane increased when PIP2 increased. When expression of PIP5KIß was inhibited with small interference RNA in HeLa cells, expression of PIP5KI
was also reduced slightly, but PIP5KI
expression was increased. PIP2 levels and internalization of transferrin receptors dropped 50% in these cells; thus, PIP5KI
could not compensate for loss of PIP5KIß. When expression of PIP5KI
was reduced, expression of both PIP5KIß and PIP5KI
increased and PIP2 levels did not change. A similar increase of PIP5KI
and PIP5KIß occurred when PIP5KI
was inhibited. These results indicate that constitutive endocytosis in CV-1 and HeLa cells requires (and may be regulated by) PIP2 produced primarily by PIP5KIß.
Key Words: phosphatidylinositol kinase; endocytosis; clathrin; transferrin receptor; phosphatidylinositol 4,5-bisphosphate
Abbreviations used in this paper: HA, hemagglutinin; PIP2, phosphatidylinositol 4,5-bisphosphate; PIP5KI, phosphatidylinositol phosphate 5-kinase; siRNA, small interference RNA.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Cui, S., Guerriero, C. J., Szalinski, C. M., Kinlough, C. L., Hughey, R. P., Weisz, O. A.
(2010). OCRL1 function in renal epithelial membrane traffic. Am. J. Physiol. Renal Physiol.
298: F335-F345
[Abstract]
[Full Text]
-
van den Bout, I., Divecha, N.
(2009). PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions. J. Cell Sci.
122: 3837-3850
[Abstract]
[Full Text]
-
Chen, M. Z., Zhu, X., Sun, H.-Q., Mao, Y. S., Wei, Y., Yamamoto, M., Yin, H. L.
(2009). Oxidative Stress Decreases Phosphatidylinositol 4,5-Bisphosphate Levels by Deactivating Phosphatidylinositol- 4-phosphate 5-Kinase {beta} in a Syk-dependent Manner. J. Biol. Chem.
284: 23743-23753
[Abstract]
[Full Text]
-
Thieman, J. R., Mishra, S. K., Ling, K., Doray, B., Anderson, R. A., Traub, L. M.
(2009). Clathrin Regulates the Association of PIPKI{gamma}661 with the AP-2 Adaptor {beta}2 Appendage. J. Biol. Chem.
284: 13924-13939
[Abstract]
[Full Text]
-
Woodcock, E. A., Kistler, P. M., Ju, Y.-K.
(2009). Phosphoinositide signalling and cardiac arrhythmias. Cardiovasc Res
82: 286-295
[Abstract]
[Full Text]
-
Mao, Y. S., Yamaga, M., Zhu, X., Wei, Y., Sun, H.-Q., Wang, J., Yun, M., Wang, Y., Di Paolo, G., Bennett, M., Mellman, I., Abrams, C. S., De Camilli, P., Lu, C. Y., Yin, H. L.
(2009). Essential and unique roles of PIP5K-{gamma} and -{alpha} in Fc{gamma} receptor-mediated phagocytosis. JCB
184: 281-296
[Abstract]
[Full Text]
-
Barrero-Villar, M., Barroso-Gonzalez, J., Cabrero, J. R., Gordon-Alonso, M., Alvarez-Losada, S., Munoz-Fernandez, M. A., Sanchez-Madrid, F., Valenzuela-Fernandez, A.
(2008). PI4P5-Kinase I{alpha} Is Required for Efficient HIV-1 Entry and Infection of T Cells. J. Immunol.
181: 6882-6888
[Abstract]
[Full Text]
-
Wang, Y., Chen, X., Lian, L., Tang, T., Stalker, T. J., Sasaki, T., Brass, L. F., Choi, J. K., Hartwig, J. H., Abrams, C. S.
(2008). Loss of PIP5KI{beta} demonstrates that PIP5KI isoform-specific PIP2 synthesis is required for IP3 formation. Proc. Natl. Acad. Sci. USA
105: 14064-14069
[Abstract]
[Full Text]
-
Nelson, C. D., Kovacs, J. J., Nobles, K. N., Whalen, E. J., Lefkowitz, R. J.
(2008). {beta}-Arrestin Scaffolding of Phosphatidylinositol 4-Phosphate 5-Kinase I{alpha} Promotes Agonist-stimulated Sequestration of the {beta}2-Adrenergic Receptor. J. Biol. Chem.
283: 21093-21101
[Abstract]
[Full Text]
-
Abe, N., Inoue, T., Galvez, T., Klein, L., Meyer, T.
(2008). Dissecting the role of PtdIns(4,5)P2 in endocytosis and recycling of the transferrin receptor. J. Cell Sci.
121: 1488-1494
[Abstract]
[Full Text]
-
Micucci, F., Capuano, C., Marchetti, E., Piccoli, M., Frati, L., Santoni, A., Galandrini, R.
(2008). PI5KI-dependent signals are critical regulators of the cytolytic secretory pathway. Blood
111: 4165-4172
[Abstract]
[Full Text]
-
Weixel, K. M., Edinger, R. S., Kester, L., Guerriero, C. J., Wang, H., Fang, L., Kleyman, T. R., Welling, P. A., Weisz, O. A., Johnson, J. P.
(2007). Phosphatidylinositol 4-Phosphate 5-Kinase Reduces Cell Surface Expression of the Epithelial Sodium Channel (ENaC) in Cultured Collecting Duct Cells. J. Biol. Chem.
282: 36534-36542
[Abstract]
[Full Text]
-
Samaniego, R., Sanchez-Martin, L., Estecha, A., Sanchez-Mateos, P.
(2007). Rho/ROCK and myosin II control the polarized distribution of endocytic clathrin structures at the uropod of moving T lymphocytes. J. Cell Sci.
120: 3534-3543
[Abstract]
[Full Text]
-
Hilgemann, D. W.
(2007). On the physiological roles of PIP2 at cardiac Na+ Ca2+ exchangers and KATP channels: a long journey from membrane biophysics into cell biology. J. Physiol.
582: 903-909
[Abstract]
[Full Text]
-
Yaradanakul, A., Feng, S., Shen, C., Lariccia, V., Lin, M.-J., Yang, J., Kang T. M., , Dong, P., Yin, H. L., Albanesi, J. P., Hilgemann, D. W.
(2007). Dual control of cardiac Na+ Ca2+ exchange by PIP2: electrophysiological analysis of direct and indirect mechanisms. J. Physiol.
582: 991-1010
[Abstract]
[Full Text]
-
Wang, Y., Lian, L., Golden, J. A., Morrisey, E. E., Abrams, C. S.
(2007). PIP5KI{gamma} is required for cardiovascular and neuronal development. Proc. Natl. Acad. Sci. USA
104: 11748-11753
[Abstract]
[Full Text]
-
Sun, Y., Carroll, S., Kaksonen, M., Toshima, J. Y., Drubin, D. G.
(2007). PtdIns(4,5)P2 turnover is required for multiple stages during clathrin- and actin-dependent endocytic internalization. JCB
177: 355-367
[Abstract]
[Full Text]
-
Zoncu, R., Perera, R. M., Sebastian, R., Nakatsu, F., Chen, H., Balla, T., Ayala, G., Toomre, D., De Camilli, P. V.
(2007). Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc. Natl. Acad. Sci. USA
104: 3793-3798
[Abstract]
[Full Text]
-
Kim, S., Kim, H., Chang, B., Ahn, N., Hwang, S., Di Paolo, G., Chang, S.
(2006). Regulation of transferrin recycling kinetics by PtdIns[4,5]P2 availability. FASEB J.
20: 2399-2401
[Abstract]
[Full Text]
-
Yamamoto, M., Chen, M. Z., Wang, Y.-J., Sun, H.-Q., Wei, Y., Martinez, M., Yin, H. L.
(2006). Hypertonic Stress Increases Phosphatidylinositol 4,5-Bisphosphate Levels by Activating PIP5KIbeta. J. Biol. Chem.
281: 32630-32638
[Abstract]
[Full Text]
-
Krauss, M., Kukhtina, V., Pechstein, A., Haucke, V.
(2006). Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2{micro}-cargo complexes. Proc. Natl. Acad. Sci. USA
103: 11934-11939
[Abstract]
[Full Text]
-
Bairstow, S. F., Ling, K., Su, X., Firestone, A. J., Carbonara, C., Anderson, R. A.
(2006). Type I{gamma}661 Phosphatidylinositol Phosphate Kinase Directly Interacts with AP2 and Regulates Endocytosis. J. Biol. Chem.
281: 20632-20642
[Abstract]
[Full Text]
-
Hinrichsen, L., Meyerholz, A., Groos, S., Ungewickell, E. J.
(2006). Bending a membrane: How clathrin affects budding. Proc. Natl. Acad. Sci. USA
103: 8715-8720
[Abstract]
[Full Text]
-
Balla, T
(2006). Phosphoinositide-derived messengers in endocrine signaling. J Endocrinol
188: 135-153
[Abstract]
[Full Text]
-
Padron, D., Tall, R. D., Roth, M. G.
(2006). Phospholipase D2 Is Required for Efficient Endocytic Recycling of Transferrin Receptors. Mol. Biol. Cell
17: 598-606
[Abstract]
[Full Text]
-
Kegel, K. B., Sapp, E., Yoder, J., Cuiffo, B., Sobin, L., Kim, Y. J., Qin, Z.-H., Hayden, M. R., Aronin, N., Scott, D. L., Isenberg, G., Goldmann, W. H., DiFiglia, M.
(2005). Huntingtin Associates with Acidic Phospholipids at the Plasma Membrane. J. Biol. Chem.
280: 36464-36473
[Abstract]
[Full Text]
-
Lin, C.-W., Yan, F., Shimamura, S., Barg, S., Shyng, S.-L.
(2005). Membrane Phosphoinositides Control Insulin Secretion Through Their Effects on ATP-Sensitive K+ Channel Activity. Diabetes
54: 2852-2858
[Abstract]
[Full Text]
-
Choudhury, R., Diao, A., Zhang, F., Eisenberg, E., Saint-Pol, A., Williams, C., Konstantakopoulos, A., Lucocq, J., Johannes, L., Rabouille, C., Greene, L. E., Lowe, M.
(2005). Lowe Syndrome Protein OCRL1 Interacts with Clathrin and Regulates Protein Trafficking between Endosomes and the Trans-Golgi Network. Mol. Biol. Cell
16: 3467-3479
[Abstract]
[Full Text]
-
Galandrini, R., Micucci, F., Tassi, I., Cifone, M. G., Cinque, B., Piccoli, M., Frati, L., Santoni, A.
(2005). Arf6: a new player in Fc{gamma}RIIIA lymphocyte-mediated cytotoxicity. Blood
106: 577-583
[Abstract]
[Full Text]
-
Paleotti, O., Macia, E., Luton, F., Klein, S., Partisani, M., Chardin, P., Kirchhausen, T., Franco, M.
(2005). The Small G-protein Arf6GTP Recruits the AP-2 Adaptor Complex to Membranes. J. Biol. Chem.
280: 21661-21666
[Abstract]
[Full Text]
-
Balana, M. E., Niedergang, F., Subtil, A., Alcover, A., Chavrier, P., Dautry-Varsat, A.
(2005). ARF6 GTPase controls bacterial invasion by actin remodelling. J. Cell Sci.
118: 2201-2210
[Abstract]
[Full Text]
-
Sasaki, J., Sasaki, T., Yamazaki, M., Matsuoka, K., Taya, C., Shitara, H., Takasuga, S., Nishio, M., Mizuno, K., Wada, T., Miyazaki, H., Watanabe, H., Iizuka, R., Kubo, S., Murata, S., Chiba, T., Maehama, T., Hamada, K., Kishimoto, H., Frohman, M. A., Tanaka, K., Penninger, J. M., Yonekawa, H., Suzuki, A., Kanaho, Y.
(2005). Regulation of anaphylactic responses by phosphatidylinositol phosphate kinase type I {alpha}. JEM
201: 859-870
[Abstract]
[Full Text]
-
Redfern, D. A., Gericke, A.
(2005). pH-dependent domain formation in phosphatidylinositol polyphosphate/phosphatidylcholine mixed vesicles. J. Lipid Res.
46: 504-515
[Abstract]
[Full Text]
-
Wang, Y. J., Li, W. H., Wang, J., Xu, K., Dong, P., Luo, X., Yin, H. L.
(2004). Critical role of PIP5KI{gamma}87 in InsP3-mediated Ca2+ signaling. JCB
167: 1005-1010
[Abstract]
[Full Text]
-
Yang, S.-A., Carpenter, C. L., Abrams, C. S.
(2004). Rho and Rho-kinase Mediate Thrombin-induced Phosphatidylinositol 4-Phosphate 5-Kinase Trafficking in Platelets. J. Biol. Chem.
279: 42331-42336
[Abstract]
[Full Text]
-
Kanzaki, M., Furukawa, M., Raab, W., Pessin, J. E.
(2004). Phosphatidylinositol 4,5-Bisphosphate Regulates Adipocyte Actin Dynamics and GLUT4 Vesicle Recycling. J. Biol. Chem.
279: 30622-30633
[Abstract]
[Full Text]
-
Roth, M. G.
(2004). Phosphoinositides in Constitutive Membrane Traffic. Physiol. Rev.
84: 699-730
[Abstract]
[Full Text]
-
Weernink, P. A. O., Meletiadis, K., Hommeltenberg, S., Hinz, M., Ishihara, H., Schmidt, M., Jakobs, K. H.
(2004). Activation of Type I Phosphatidylinositol 4-Phosphate 5-Kinase Isoforms by the Rho GTPases, RhoA, Rac1, and Cdc42. J. Biol. Chem.
279: 7840-7849
[Abstract]
[Full Text]
-
Jha, A., Agostinelli, N. R., Mishra, S. K., Keyel, P. A., Hawryluk, M. J., Traub, L. M.
(2004). A Novel AP-2 Adaptor Interaction Motif Initially Identified in the Long-splice Isoform of Synaptojanin 1, SJ170. J. Biol. Chem.
279: 2281-2290
[Abstract]
[Full Text]