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Science 9 February 2001:
Vol. 291. no. 5506, pp. 1047 - 1051
DOI: 10.1126/science.291.5506.1047
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Reports

Role of the ENTH Domain in Phosphatidylinositol-4,5-Bisphosphate Binding and Endocytosis

Toshiki Itoh,1 Seizo Koshiba,2 Takanori Kigawa,23 Akira Kikuchi,4 Shigeyuki Yokoyama,235 Tadaomi Takenawa1*

Endocytic proteins such as epsin, AP180, and Hip1R (Sla2p) share a conserved modular region termed the epsin NH2-terminal homology (ENTH) domain, which plays a crucial role in clathrin-mediated endocytosis through an unknown target. Here, we demonstrate a strong affinity of the ENTH domain for phosphatidylinositol-4,5-bisphosphate [PtdIns(4,5)P2]. With nuclear magnetic resonance analysis of the epsin ENTH domain, we determined that a cleft formed with positively charged residues contributed to phosphoinositide binding. Overexpression of a mutant, epsin Lys76 rightarrow  Ala76, with an ENTH domain defective in phosphoinositide binding, blocked epidermal growth factor internalization in COS-7 cells. Thus, interaction between the ENTH domain and PtdIns(4,5)P2 is essential for endocytosis mediated by clathrin-coated pits.

1 Department of Biochemistry, Institute of Medical Science, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan.
2 RIKEN Genomic Sciences Center, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama-shi, Kanagawa 230-0045, Japan.
3 Cellular Signaling Laboratory, RIKEN Harima Institute at SPring-8, 1-1-1 Kouto, Mikazuki-cho, Sayo, Hyogo 679-5148, Japan.
4 Department of Biochemistry, Hiroshima University School of Medicine, 1-2-3 Kasumi, Minami-ku, Hiroshima 734-8551, Japan.
5 Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
*   To whom correspondence should be addressed. E-mail: takenawa{at}ims.u-tokyo.ac.jp

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J. Cell Sci. 115, 1099-1105
   Abstract »    Full Text »    PDF »
Unusual Structural Organization of the Endocytic Proteins AP180 and Epsin 1.
C. Kalthoff, J. Alves, C. Urbanke, R. Knorr, and E. J. Ungewickell (2002)
J. Biol. Chem. 277, 8209-8216
   Abstract »    Full Text »    PDF »
Phosphatidylinositol-4-phosphate 5-Kinase-1beta Is Essential for Epidermal Growth Factor Receptor-mediated Endocytosis.
M. A. Barbieri, C. M. Heath, E. M. Peters, A. Wells, J. N. Davis, and P. D. Stahl (2001)
J. Biol. Chem. 276, 47212-47216
   Abstract »    Full Text »    PDF »
Clathrin- and AP-2-binding Sites in HIP1 Uncover a General Assembly Role for Endocytic Accessory Proteins.
S. K. Mishra, N. R. Agostinelli, T. J. Brett, I. Mizukami, T. S. Ross, and L. M. Traub (2001)
J. Biol. Chem. 276, 46230-46236
   Abstract »    Full Text »    PDF »
Huntingtin Interacting Protein 1 Is a Clathrin Coat Binding Protein Required for Differentiation of late Spermatogenic Progenitors.
D. S. Rao, J. C. Chang, P. D. Kumar, I. Mizukami, G. M. Smithson, S. V. Bradley, A. F. Parlow, and T. S. Ross (2001)
Mol. Cell. Biol. 21, 7796-7806
   Abstract »    Full Text »    PDF »
In Vivo Role for Actin-regulating Kinases in Endocytosis and Yeast Epsin Phosphorylation.
H. A. Watson, M. J. T. V. Cope, A. C. Groen, D. G. Drubin, and B. Wendland (2001)
Mol. Biol. Cell 12, 3668-3679
   Abstract »    Full Text »    PDF »
HIP1 Functions in Clathrin-mediated Endocytosis through Binding to Clathrin and Adaptor Protein 2.
M. Metzler, V. Legendre-Guillemin, L. Gan, V. Chopra, A. Kwok, P. S. McPherson, and M. R. Hayden (2001)
J. Biol. Chem. 276, 39271-39276
   Abstract »    Full Text »    PDF »
A Novel Mechanism for Localizing Membrane Proteins to Yeast Trans-Golgi Network Requires Function of Synaptojanin-like Protein.
S.-A. Ha, J. T. Bunch, H. Hama, D. B. DeWald, and S. F. Nothwehr (2001)
Mol. Biol. Cell 12, 3175-3190
   Abstract »    Full Text »    PDF »
The actin-binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro.
A. E.Y. Engqvist-Goldstein, R. A. Warren, M. M. Kessels, J. H. Keen, J. Heuser, and D. G. Drubin (2001)
J. Cell Biol. 154, 1209-1224
   Abstract »    Full Text »    PDF »
Modulation of HIV-like particle assembly in vitro by inositol phosphates.
S. Campbell, R. J. Fisher, E. M. Towler, S. Fox, H. J. Issaq, T. Wolfe, L. R. Phillips, and A. Rein (2001)
PNAS
   Abstract »    Full Text »    PDF »
The huntingtin interacting protein HIP1 is a clathrin and {alpha}-adaptin-binding protein involved in receptor-mediated endocytosis.
S. Waelter, E. Scherzinger, R. Hasenbank, E. Nordhoff, R. Lurz, H. Goehler, C. Gauss, K. Sathasivam, G. P. Bates, H. Lehrach, et al. (2001)
Hum. Mol. Genet. 10, 1807-1817
   Abstract »    Full Text »    PDF »
Signaling with Phosphoinositides: Better than Binary.
M. Overduin, M. L. Cheever, and T. G. Kutateladze (2001)
Mol. Interv. 1, 150-159
   Abstract »    Full Text »    PDF »
Regulation of presynaptic phosphatidylinositol 4,5-biphosphate by neuronal activity.
K. D. Micheva, R. W. Holz, and S. J. Smith (2001)
J. Cell Biol. 154, 355-368
   Abstract »    Full Text »    PDF »
Phosphoinositides in membrane traffic at the synapse.
O Cremona and P De Camilli (2001)
J. Cell Sci. 114, 1041-1052
   Abstract »    PDF »
Golgi-localizing, gamma -Adaptin Ear Homology Domain, ADP-ribosylation Factor-binding (GGA) Proteins Interact with Acidic Dileucine Sequences within the Cytoplasmic Domains of Sorting Receptors through Their Vps27p/Hrs/STAM (VHS) Domains.
H. Takatsu, Y. Katoh, Y. Shiba, and K. Nakayama (2001)
J. Biol. Chem. 276, 28541-28545
   Abstract »    Full Text »    PDF »
Interaction of Two Structurally Distinct Sequence Types with the Clathrin Terminal Domain beta -Propeller.
M. T. Drake and L. M. Traub (2001)
J. Biol. Chem. 276, 28700-28709
   Abstract »    Full Text »    PDF »


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