Structural basis for the recognition of two consecutive mutually interacting DPF motifs by the SGIP1 μ homology domain

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Shimada, Atsushi ^a,b   Yamaguchi, Atsuko ^a   Kohda, Daisuke ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ADAPTIN; AMINO ACID; CARRIER PROTEIN; EPS15 PROTEIN, HUMAN; LIGAND; PROTEIN BINDING; SGIP1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AMINO ACID SEQUENCE; BINDING SITE; CALORIMETRY; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN MOTIF; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACIDS; BINDING SITES; CALORIMETRY; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; HUMANS; LIGANDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN DOMAINS; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84956637489     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19565     Document Type: Article

References (46)

1. McMahon, H. T., Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533 (2011).
2. Olesen, L. E. et al. Solitary and repetitive binding motifs for the AP2 complex ?-appendage in amphiphysin and other accessory proteins. J. Biol. Chem. 283, 5099-5109 (2008).
3. Praefcke, G. J. K. et al. Evolving nature of the AP2 ?-appendage hub during clathrin-coated vesicle endocytosis. EMBO J. 23, 4371-4383 (2004).
4. Salcini, A. E., Chen, H., Iannolo, G., De Camilli, P., Di Fiore, P. P. Epidermal growth factor pathway substrate 15, Eps15. Int. J. Biochem. Cell Biol. 31, 805-809 (1999).
5. van Bergen en Henegouwen, P. M. Eps15: a multifunctional adaptor protein regulating intracellular trafficking. Cell Commun. Signal. 7, 24 (2009).
6. Benmerah, A., Bue, B., Dautry-Varsat, A., Cerf-Bensussan, N. The ear of-adaptin interacts with the COOH-terminal domain of the Eps15 protein. J. Biol. Chem. 271, 12111-12116 (1996).
7. Owen, D. J. et al. A structural explanation for the binding of multiple ligands by the-adaptin appendage domain. Cell 97, 805-815 (1999).
8. Reider, A. et al. Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation. EMBO J. 28, 3103-3116 (2009).
9. Henne, W. M. et al. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281-1284 (2010).
10. Uezu, A. et al. Characterization of the EFC/F-BAR domain protein, FCHO2. Genes Cells 16, 868-878 (2011).
11. Mulkearns, E. E., Cooper, J. A. FCH domain only-2 organizes clathrin-coated structures and interacts with Disabled-2 for lowdensity lipoprotein receptor endocytosis. Mol. Biol. Cell 23, 1330-1342 (2012).
12. Itoh, T. et al. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804 (2005).
13. Tsujita, K. et al. Coordination between actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 172, 269-279 (2006).
14. Shimada, A. et al. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761-772 (2007).
15. Henne, W. M. et al. Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15, 839-852 (2007).
16. Frost, A. et al. Structural basis of membrane invagination by F-BAR domains. Cell 132, 807-817 (2008).
17. Cocucci, E., Aguet, F., Boulant, S., Kirchhausen, T. The first five seconds in the life of a clathrin-coated pit. Cell 150, 495-507 (2012).
18. Trevaskis, J. et al. Src homology 3-domain growth factor receptor-bound 2-like (endophilin) interacting protein 1, a novel neuronal protein that regulates energy balance. Endocrinology 146, 3757-3764 (2005).
19. Uezu, A. et al. SGIP1 is an endocytic protein that directly interacts with phospholipids and Eps15. J. Biol. Chem. 282, 26481-26489 (2007).
20. Hollopeter, G. et al. The membrane-associated proteins FCHo and SGIP are allosteric activators of the AP2 clathrin adaptor complex. eLife 3, e03648 (2014).
21. Umasankar, P. K. et al. A clathrin coat assembly role for the muniscin protein central linker revealed by TALEN-mediated gene editing. eLife 3, e04137 (2014).
22. Umasankar, P. K. et al. Distinct and separable activities of the endocytic clathrin-coat components Fcho1/2 and AP-2 in developmental patterning. Nat. Cell Biol. 14, 488-501 (2012).
23. Owen, D. J., Evans, P. R. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282, 1327-1332 (1998).
24. Mardones, G. A. et al. Structural basis for the recognition of tyrosine-based sorting signals by the 3A subunit of the AP-3 adaptor complex. J. Biol. Chem. 288, 9563-9571 (2013).
25. Burgos, P. V. et al. Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev. Cell 18, 425-436 (2010).
26. Lahav, A., Rozenherg, H., Parnis, A., Cassel, D., Adir, N. Structure of the bovine COPI subunit homology domain at 2.15 Å resolution. Acta Cryst. D71, 1328-1334 (2015).
27. Suckling, R. J. et al. Structural basis for the binding of tryptophan-based motifs by-COP. Proc. Natl. Acad. Sci. USA 112, 14242-14247 (2015).
28. Benmerah, A. et al. The tyrosine kinase substrate eps15 is constitutively associated with the plasma membrane adaptor AP-2. J. Cell Biol. 131, 1831-1838 (1995).
29. Cupers, P., Jadhav, A. P., Kirchhausen, T. Assembly of clathrin coats disrupts the association between Eps15 and AP-2 adaptors. J. Biol. Chem. 273, 1847-1850 (1998).
30. Owen, D. J., Vallis, Y., Pearse, B. M. F., McMahon, H. T., Evans, P. R. The structure and function of the 2-adaptin appendage domain. EMBO J. 19, 4216-4227 (2000).
31. Edeling, M. et al. Molecular switches involving the AP-2 2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev. Cell 10, 329-342 (2006).
32. Schmid, E. M. et al. Role of the AP2-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol. 4, e262 (2006).
33. Schmid, E. M., McMahon, H. T. Integrating molecular and network biology to decode endocytosis. Nature 448, 883-888 (2007).
34. Coda, L. et al. Eps15R is a tyrosine kinase substrate with characteristics of docking protein possibly involved in coated pits-mediated internalization. J. Biol. Chem. 273, 3003-3012 (1998).
35. Cummings, N. et al. Genetic variation in SH3-domain GRB2-like (endophilin)-interacting protein 1 has a major impact on fat mass. Int. J. Obes. (Lond) 36, 201-206 (2012).
36. Mishra, S. K. et al. Dual engagement regulation of protein interactions with the AP-2 adaptor appendage. J. Biol. Chem. 279, 46191-46203 (2004).
37. Rumpf, J. et al. Structure of the Eps15-stonin2 complex provides a molecular explanation for EH-domain ligand specificity. EMBO J. 27, 558-569 (2008).
38. de Beer, T. et al. Molecular mechanism of NPF recognition by EH domains. Nat. Struct. Biol. 7, 1018-1022 (2000).
39. Brett, T. J., Traub, L. M., Fremont, D. H. Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure 10, 797-809 (2002).
40. Rath, A., Davidson, A. R., Deber, C. M. The structure of "unstructured" regions in peptides and proteins: Role of the polyproline II helix in protein folding and recognition. Biopolymers 80, 179-185 (2005).
41. Adzhubei, A. A., Sternberg, M. J. E., Makarov, A. A. Polyproline-II helix in proteins: structure and function. J. Mol. Biol. 425, 2100-2132 (2013).
42. Keller, S. et al. High-precision isothermal titration calorimetry with automated peak-shape analysis. Anal. Chem. 84, 5066-5073 (2012).
43. Houtman, J. C. D. et al. Studying multi-site binary and ternary protein interactions by global analysis of isothermal titration calorimetry data in SEDPHAT: Application to adaptor protein complexes in cell signaling. Protein Sci. 16, 30-42 (2007).
44. Otwinowski, Z., Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276, 307-326 (1997).
45. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Cryst D66, 213-221 (2010).
46. Pupko, T., Bell, R. E., Mayrose, I., Glaser, F., Ben-Tal, N. Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues. Bioinformatics 18 (Suppl 1), S71-S77 (2002).