Charge effects in the selection of NPF motifs by the EH domain of EHD1

Biochemistry

Volumn 49, Issue 16, 2010, Pages 3381-3392

  Henry, Gillian D ^a   Corrigan, Daniel J ^a   Dineen, Joseph V ^a   Baleja, James D ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC RESIDUES; AMINO GROUP; BINDING PARTNERS; BINDING POCKETS; CELLULAR ACTIVITIES; CHARGE EFFECT; COMPLEX FORMATIONS; ELECTROSTATIC COMPONENTS; EXTENDED INTERACTION; HETERONUCLEAR SINGLE-QUANTUM COHERENCES; LYSINE SIDE CHAINS; NMR SPECTROSCOPY; ORDERS OF MAGNITUDE; STRUCTURAL CHANGE; TARGET PROTEINS; THERMODYNAMIC PROFILES; VESICLE TRAFFICKING;

AMINO ACIDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; QUANTUM THEORY;

COMPLEXATION;

AMINO ACID; ASPARAGYLPROLYLPHENYLALANINE; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15; GUANINE NUCLEOTIDE BINDING PROTEIN; LYSINE; PROTEIN FIP2; RAB PROTEIN; RAB11 PROTEIN; RABENOSYN 5; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; ENTHALPY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; THERMODYNAMICS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM-BINDING PROTEINS; CALORIMETRY; CIRCULAR DICHROISM; ENDOCYTOSIS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MAMMALS; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PEPTIDES; PHENYLALANINE; PHOSPHOPROTEINS; PROTEIN CONFORMATION; TYROSINE; VESICULAR TRANSPORT PROTEINS;

EID: 77951219926     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100065r     Document Type: Article

References (62)

1. Polo, S., Confalonieri, S., Salcini, A. E., and Di Fiore, P. P. (2003) EH and UIM: endocytosis and more Sci. STKE 2003, re17
2. Fazioli, F., Minichiello, L., Matoskova, B., Wong, W. T., and Di Fiore, P. P. (1993) Eps15, a novel tyrosine kinase substrate, exhibits transforming activity Mol. Cell. Biol. 13, 5814-5828 (Pubitemid 23260682)
3. Wong, W. T., Schumacher, C., Salcini, A. E., Romano, A., Castagnino, P., Pelicci, P. G., and Di Fiore, P. P. (1995) A protein-binding domain, EH, identified in the receptor tyrosine kinase substrate Eps15 and conserved in evolution Proc. Natl. Acad. Sci. U. S. A. 92, 9530-9534
4. Salcini, A. E., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minenkova, O., Cesareni, G., Pelicci, P. G., and Di Fiore, P. P. (1997) Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module Genes Dev. 11, 2239-2249 (Pubitemid 27387974)
5. Benmerah, A., Bayrou, M., Cerf-Bensussan, N., and Dautry-Varsat, A. (1999) Inhibition of clathrin-coated pit assembly by an Eps15 mutant J. Cell Sci. 112 (Pt 9) 1303-1311 (Pubitemid 29243453)
6. Yamaguchi, A., Urano, T., Goi, T., and Feig, L. A. (1997) An Eps homology (EH) domain protein that binds to the Ral-GTPase target, RalBP1 J. Biol. Chem. 272, 31230-31234 (Pubitemid 28013252)
7. Cullis, D. N., Philip, B., Baleja, J. D., and Feig, L. A. (2002) Rab11-FIP2, an adaptor protein connecting cellular components involved in internalization and recycling of epidermal growth factor receptors J. Biol. Chem. 277, 49158-49166
8. Grant, B., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H., and Hirsh, D. (2001) Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling Nat. Cell Biol. 3, 573-579
9. Lin, S. X., Grant, B., Hirsh, D., and Maxfield, F. R. (2001) Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells Nat. Cell Biol. 3, 567-572
10. Paoluzi, S., Castagnoli, L., Lauro, I., Salcini, A. E., Coda, L., Fre, S., Confalonieri, S., Pelicci, P. G., Di Fiore, P. P., and Cesareni, G. (1998) Recognition specificity of individual EH domains of mammals and yeast EMBO J. 17, 6541-6550
11. Enmon, J. L., de Beer, T., and Overduin, M. (2000) Solution structure of Eps15′s third EH domain reveals coincident Phe-Trp and Asn-Pro-Phe binding sites Biochemistry 39, 4309-4319
12. Chen, H., Fre, S., Slepnev, V. I., Capua, M. R., Takei, K., Butler, M. H., Di Fiore, P. P., and De Camilli, P. (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis Nature 394, 793-797
13. Martina, J. A., Bonangelino, C. J., Aguilar, R. C., and Bonifacino, J. S. (2001) Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery J. Cell Biol. 153, 1111-1120
14. Smith, C. A., Dho, S. E., Donaldson, J., Tepass, U., and McGlade, C. J. (2004) The cell fate determinant Numb interacts with EHD/Rme-1 family proteins and has a role in endocytic recycling Mol. Biol. Cell 15, 3698-3708
15. Xu, Y., Shi, H., Wei, S., Wong, S. H., and Hong, W. (2004) Mutually exclusive interactions of EHD1 with GS32 and syndapin II Mol. Membr. Biol. 21, 269-277
16. Mishra, S. K., Keyel, P. A., Hawryluk, M. J., Agostinelli, N. R., Watkins, S. C., and Traub, L. M. (2002) Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor EMBO J. 21, 4915-4926
17. Braun, A., Pinyol, R., Dahlhaus, R., Koch, D., Fonarev, P., Grant, B. D., Kessels, M. M., and Qualmann, B. (2005) EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling Mol. Biol. Cell 16, 3642-3658
18. Morgan, J. R., Prasad, K., Jin, S., Augustine, G. J., and Lafer, E. M. (2003) Eps15 homology domain-NPF motif interactions regulate clathrin coat assembly during synaptic vesicle recycling J. Biol. Chem. 278, 33583-33592
19. Haffner, C., Takei, K., Chen, H., Ringstad, N., Hudson, A., Butler, M. H., Salcini, A. E., Di Fiore, P. P., and De Camilli, P. (1997) Synaptojanin 1: localization on coated endocytic intermediates in nerve terminals and interaction of its 170 kDa isoform with Eps15 FEBS Lett. 419, 175-180
20. Doria, M., Salcini, A. E., Colombo, E., Parslow, T. G., Pelicci, P. G., and Di Fiore, P. P. (1999) The Eps15 homology (EH) domain-based interaction between Eps15 and Hrb connects the molecular machinery of endocytosis to that of nucleocytosolic transport J. Cell Biol. 147, 1379-1384
21. Fernandez-Chacon, R., Achiriloaie, M., Janz, R., Albanesi, J. P., and Sudhof, T. C. (2000) SCAMP1 function in endocytosis J. Biol. Chem. 275, 12752-12756
22. Guilherme, A., Soriano, N. A., Furcinitti, P. S., and Czech, M. P. (2004) Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes J. Biol. Chem. 279, 40062-40075
23. Doherty, K. R., Demonbreun, A. R., Wallace, G. Q., Cave, A., Posey, A. D., Heretis, K., Pytel, P., and McNally, E. M. (2008) The endocytic recycling protein EHD2 interacts with myoferlin to regulate myoblast fusion J. Biol. Chem. 283, 20252-20260
24. Naslavsky, N., Rahajeng, J., Sharma, M., Jovic, M., and Caplan, S. (2006) Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport Mol. Biol. Cell 17, 163-177
25. Naslavsky, N., Boehm, M., Backlund, P. S., Jr., and Caplan, S. (2004) Rabenosyn-5 and EHD1 interact and sequentially regulate protein recycling to the plasma membrane Mol. Biol. Cell 15, 2410-2422
26. de Beer, T., Carter, R. E., Lobel-Rice, K. E., Sorkin, A., and Overduin, M. (1998) Structure and Asn-Pro-Phe binding pocket of the Eps15 homology domain Science 281, 1357-1360
27. Koshiba, S., Kigawa, T., Iwahara, J., Kikuchi, A., and Yokoyama, S. (1999) Solution structure of the Eps15 homology domain of a human POB1 (partner of RalBP1) FEBS Lett. 442, 138-142
28. Kim, S., Cullis, D. N., Feig, L. A., and Baleja, J. D. (2001) Solution structure of the Reps1 EH domain and characterization of its binding to NPF target sequences Biochemistry 40, 6776-6785
29. Kieken, F., Jovic, M., Naslavsky, N., Caplan, S., and Sorgen, P. L. (2007) EH domain of EHD1 J. Biomol. NMR 39, 323-329
30. de Beer, T., Hoofnagle, A. N., Enmon, J. L., Bowers, R. C., Yamabhai, M., Kay, B. K., and Overduin, M. (2000) Molecular mechanism of NPF recognition by EH domains Nat. Struct. Biol. 7, 1018-1022
31. Kieken, F., Jovic, M., Tonelli, M., Naslavsky, N., Caplan, S., and Sorgen, P. L. (2009) Structural insight into the interaction of proteins containing NPF, DPF, and GPF motifs with the C-terminal EH-domain of EHD1 Protein Sci. 18, 2471-2479
32. Yamabhai, M., Hoffman, N. G., Hardison, N. L., McPherson, P. S., Castagnoli, L., Cesareni, G., and Kay, B. K. (1998) Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains J. Biol. Chem. 273, 31401-31407
33. Rumpf, J., Simon, B., Jung, N., Maritzen, T., Haucke, V., Sattler, M., and Groemping, Y. (2008) Structure of the Eps15-stonin2 complex provides a molecular explanation for EH-domain ligand specificity EMBO J. 27, 558-569
34. Lee, D. W., Zhao, X., Scarselletta, S., Schweinsberg, P. J., Eisenberg, E., Grant, B. D., and Greene, L. E. (2005) ATP binding regulates oligomerization and endosome association of RME-1 family proteins J. Biol. Chem. 280, 17213-17220
35. Blume, J. J., Halbach, A., Behrendt, D., Paulsson, M., and Plomann, M. (2007) EHD proteins are associated with tubular and vesicular compartments and interact with specific phospholipids Exp. Cell Res. 313, 219-231
36. Daumke, O., Lundmark, R., Vallis, Y., Martens, S., Butler, P. J., and McMahon, H. T. (2007) Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling Nature 449, 923-927
37. Caplan, S., Naslavsky, N., Hartnell, L. M., Lodge, R., Polishchuk, R. S., Donaldson, J. G., and Bonifacino, J. S. (2002) A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane EMBO J. 21, 2557-2567
38. George, M., Ying, G., Rainey, M. A., Solomon, A., Parikh, P. T., Gao, Q., Band, V., and Band, H. (2007) Shared as well as distinct roles of EHD proteins revealed by biochemical and functional comparisons in mammalian cells and C. elegans BMC Cell Biol. 8, 3
39. Grant, B. D. and Caplan, S. (2008) Mechanisms of EHD/RME-1 protein function in endocytic transport Traffic 9, 2043-2052
40. Pant, S., Sharma, M., Patel, K., Caplan, S., Carr, C. M., and Grant, B. D. (2009) AMPH-1/Amphiphysin/Bin1 functions with RME-1/EHD1 in endocytic recycling Nat. Cell Biol. 11, 1399-1410
41. 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, 601-612
42. Eathiraj, S., Pan, X., Ritacco, C., and Lambright, D. G. (2005) Structural basis of family-wide Rab GTPase recognition by Rabenosyn-5 Nature 436, 415-419
43. Lindsay, A. J. and McCaffrey, M. W. (2002) Rab11-FIP2 functions in transferrin recycling and associates with endosomal membranes via its COOH-terminal domain J. Biol. Chem. 277, 27193-27199
44. Jagoe, W. N., Lindsay, A. J., Read, R. J., McCoy, A. J., McCaffrey, M. W., and Khan, A. R. (2006) Crystal structure of Rab11 in complex with Rab11 family interacting protein 2 Structure 14, 1273-1283
45. Wei, J., Liu, Y., Bose, K., Henry, G. D., and Baleja, J. D. (2009) Disorder and structure in the Rab11 binding domain of Rab11 family interacting protein 2 Biochemistry 48, 549-557
46. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein Protein Sci. 4, 2411-2423
47. Turnbull, W. B. and Daranas, A. H. (2003) On the value of c: can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859-14866
48. Dunitz, J. D. (1995) Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions Chem. Biol. 2, 709-712
49. Cooper, A., Johnson, C. M., Lakey, J. H., and Nollmann, M. (2001) Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions Biophys. Chem. 93, 215-230
50. Crane-Robinson, C., Dragan, A. I., and Privalov, P. L. (2006) The extended arms of DNA-binding domains: a tale of tails Trends Biochem. Sci. 31, 547-552
51. Record, M. T., Jr., Lohman, M. L., and De Haseth, P. (1976) Ion effects on ligand-nucleic acid interactions J. Mol. Biol. 107, 145-158
52. Saecker, R. M. and Record, M. T., Jr. (2002) Protein surface salt bridges and paths for DNA wrapping Curr. Opin. Struct. Biol. 12, 311-319
53. Sharma, M., Panapakkam Giridharan, S. S., Rahajeng, J., Naslavsky, N., and Caplan, S. (2009) MICAL-L1 Links EHD1 to tubular recycling endosomes and regulates receptor recycling Mol. Biol. Cell 20, 5181-5194
54. Evans, P. R. and Owen, D. J. (2002) Endocytosis and vesicle trafficking Curr. Opin. Struct. Biol. 12, 814-821
55. Pawson, T. and Nash, P. (2003) Assembly of cell regulatory systems through protein interaction domains Science 300, 445-452
56. McNemar, C., Snow, M. E., Windsor, W. T., Prongay, A., Mui, P., Zhang, R., Durkin, J., Le, H. V., and Weber, P. C. (1997) Thermodynamic and structural analysis of phosphotyrosine polypeptide binding to Grb2-SH2 Biochemistry 36, 10006-10014
57. Mascotti, D. P. and Lohman, T. M. (1990) Thermodynamic extent of counterion release upon binding oligolysines to single-stranded nucleic acids Proc. Natl. Acad. Sci. U. S. A. 87, 3142-3146
58. Dragan, A. I., Read, C. M., Makeyeva, E. N., Milgotina, E. I., Churchill, M. E., Crane-Robinson, C., and Privalov, P. L. (2004) DNA binding and bending by HMG boxes: energetic determinants of specificity J. Mol. Biol. 343, 371-393
59. Takeda, Y., Ross, P. D., and Mudd, C. P. (1992) Thermodynamics of Cro protein-DNA interactions Proc. Natl. Acad. Sci. U. S. A. 89, 8180-8184
60. Bodemann, B. O. and White, M. A. (2008) Ral GTPases and cancer: linchpin support of the tumorigenic platform Nat. Rev. Cancer 8, 133-140
61. Jin, R., Junutula, J. R., Matern, H. T., Ervin, K. E., Scheller, R. H., and Brunger, A. T. (2005) Exo84 and Sec5 are competitive regulatory Sec6/8 effectors to the RalA GTPase EMBO J. 24, 2064-2074
62. Rocchia, W., Sridharan, S., Nicholls, A., Alexov, E., Chiabrera, A., and Honig, B. (2002) Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects J. Comput. Chem. 23, 128-137