Conformational differences between arrestin2 and pre-activated mutants as revealed by hydrogen exchange mass spectrometry

Journal of Molecular Biology

Volumn 351, Issue 4, 2005, Pages 865-878

  Carter, Jennifer M ^a   Gurevich, Vsevolod V ^b   Prossnitz, Eric R ^c   Engen, John R ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Conformational activation; G protein coupled receptors; Protein dynamics; Signal transduction

Indexed keywords

ARRESTIN 2; CLATHRIN; DEUTERIUM; G PROTEIN COUPLED RECEPTOR; HYDROGEN; MUTANT PROTEIN; RETINA S ANTIGEN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; RECEPTOR BINDING; WILD TYPE;

EID: 23444449590     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.06.048     Document Type: Article

References (55)

1. M. Gurrath Peptide-binding G protein-coupled receptors: new opportunities for drug design Curr. Med. Chem. 8 2001 1605 1648
2. R.J. Lefkowitz, and S.K. Shenoy Transduction of receptor signals by beta-arrestins Science 308 2005 512 517
3. V.V. Gurevich, and E.V. Gurevich The molecular acrobatics of arrestin activation Trends Pharmacol. Sci. 25 2004 105 111
4. R.J. Lefkowitz, and E.J. Whalen beta-arrestins: traffic cops of cell signaling Curr. Opin. Cell Biol. 16 2004 162 168
5. J.G. Krupnick, V.V. Gurevich, and J.L. Benovic Mechanism of quenching of phototransduction. Binding competition between arrestin and transducin for phosphorhodopsin J. Biol. Chem. 272 1997 18125 18131
6. K.L. Pierce, and R.J. Lefkowitz Classical and new roles of beta-arrestins in the regulation of G-protein-coupled receptors Nature Rev. Neurosci. 2 2001 727 733
7. J.A. Hirsch, C. Schubert, V.V. Gurevich, and P.B. Sigler The 2.8 Å crystal structure of visual arrestin: a model for arrestin's regulation Cell 97 1999 257 269
8. M. Han, V.V. Gurevich, S.A. Vishnivetskiy, P.B. Sigler, and C. Schubert Crystal structure of beta-arrestin at 1.9 Å: possible mechanism of receptor binding and membrane translocation Structure (Camb) 9 2001 869 880
9. V.V. Gurevich, S.B. Dion, J.J. Onorato, J. Ptasienski, C.M. Kim, and R. Sterne-Marr Arrestin interactions with G protein-coupled receptors. Direct binding studies of wild type and mutant arrestins with rhodopsin, beta 2- adrenergic, and m2 muscarinic cholinergic receptors J. Biol. Chem. 270 1995 720 731
10. V.V. Gurevich, and J.L. Benovic Visual arrestin interaction with rhodopsin. Sequential multisite binding ensures strict selectivity toward light-activated phosphorylated rhodopsin J. Biol. Chem. 268 1993 11628 11638
11. V.V. Gurevich The selectivity of visual arrestin for light-activated phosphorhodopsin is controlled by multiple nonredundant mechanisms J. Biol. Chem. 273 1998 15501 15506
12. V.V. Gurevich, and J.L. Benovic Mechanism of phosphorylation-recognition by visual arrestin and the transition of arrestin into a high affinity binding state Mol. Pharmacol. 51 1997 161 169
13. A. Kovoor, J. Celver, R.I. Abdryashitov, C. Chavkin, and V.V. Gurevich Targeted construction of phosphorylation-independent beta-arrestin mutants with constitutive activity in cells J. Biol. Chem. 274 1999 6831 6834
14. S.A. Vishnivetskiy, C. Schubert, G.C. Climaco, Y.V. Gurevich, M.G. Velez, and V.V. Gurevich An additional phosphate-binding element in arrestin molecule. Implications for the mechanism of arrestin activation J. Biol. Chem. 275 2000 41049 41057
15. R.M. Potter, T.A. Key, V.V. Gurevich, L.A. Sklar, and E.R. Prossnitz Arrestin variants display differential binding characteristics for the phosphorylated N-formyl peptide receptor carboxyl terminus J. Biol. Chem. 277 2002 8970 8978
16. C. Woodward, I. Simon, and E. Tüchsen Hydrogen exchange and the dynamic structure of proteins Mol. Cell. Biochem. 48 1982 135 160
17. S.W. Englander, and N.R. Kallenbach Hydrogen exchange and structural dynamics of proteins and nucleic acids Quart. Rev. Biophys. 16 1984 521 655
18. D.L. Smith, Y. Deng, and Z. Zhang Probing the non-covalent structure of proteins by amide hydrogen exchange and mass spectrometry J. Mass. Spectrom. 32 1997 135 146
19. M.M. Krishna, L. Hoang, Y. Lin, and S.W. Englander Hydrogen exchange methods to study protein folding Methods 34 2004 51 64
20. H.J. Dyson, and P.E. Wright Unfolded proteins and protein folding studied by NMR Chem. Rev. 104 2004 3607 3622
21. A.N. Hoofnagle, K.A. Resing, and N.G. Ahn Protein analysis by hydrogen exchange mass spectrometry Annu. Rev. Biophys. Biomol. Struct. 32 2003 1 25
22. S.J. Eyles, and I.A. Kaltashov Methods to study protein dynamics and folding by mass spectrometry Methods 34 2004 88 99
23. I.A. Kaltashov, and S.J. Eyles Studies of biomolecular conformations and conformational dynamics by mass spectrometry Mass Spectrom. Rev. 21 2002 37 71
24. I.A. Kaltashov, and S.J. Eyles Crossing the phase boundary to study protein dynamics and function: combination of amide hydrogen exchange in solution and ion fragmentation in the gas phase J. Mass Spectrom. 37 2002 557 565
25. R.A. Garcia, D. Pantazatos, and F.J. Villarreal Hydrogen/deuterium exchange mass spectrometry for investigating protein-ligand interactions Assay Drug Dev. Technol. 2 2004 81 91
26. J.R. Engen, and D.L. Smith Investigating protein structure and dynamics by hydrogen exchange MS Anal. Chem. 73 2001 256A 265A
27. K. Dharmasiri, and D.L. Smith Mass spectrometric determination of isotopic exchange rates of amide hydrogens located on the surfaces of proteins Anal. Chem. 68 1996 2340 2344
28. S.K. Milano, H.C. Pace, Y.M. Kim, C. Brenner, and J.L. Benovic Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis Biochemistry 41 2002 3321 3328
29. G. Vriend WHAT IF: a molecular modeling and drug design program J. Mol. Graph. 8 1990 52 56
30. Y. Bai, J.S. Milne, L. Mayne, and S.W. Englander Primary structure effects on peptide group hydrogen exchange Proteins: Struct. Funct. Genet. 17 1993 75 86
31. Z. Zhang, and D.L. Smith Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation Protein Sci. 2 1993 522 531
32. J.R. Engen, and D.L. Smith Investigating the higher order structure of proteins: hydrogen exchange, proteolytic fragmentation and mass spectrometry Methods Mol. Biol. 146 2000 95 112
33. A.N. Hoofnagle, K.A. Resing, and N.G. Ahn Practical methods for deuterium exchange/mass spectrometry Methods Mol. Biol. 250 2004 283 298
34. H. Ohguro, K. Palczewski, K.A. Walsh, and R.S. Johnson Topographic study of arrestin using differential chemical modifications and hydrogen/deuterium exchange Protein Sci. 3 1994 2428 2434
35. X. Yan, H. Zhang, J. Watson, M.I. Schimerlik, and M.L. Deinzer Hydrogen/deuterium exchange and mass spectrometric analysis of a protein containing multiple disulfide bonds: Solution structure of recombinant macrophage colony stimulating factor-beta (rhM-CSFbeta) Protein Sci. 11 2002 2113 2124
36. X. Yan, J. Watson, P.S. Ho, and M.L. Deinzer Mass spectrometric approaches using electrospray ionization charge states and hydrogen-deuterium exchange for determining protein structures and their conformational changes Mol. Cell. Proteomics 3 2004 10 23
37. O.B. Goodman Jr, J.G. Krupnick, V.V. Gurevich, J.L. Benovic, and J.H. Keen Arrestin/clathrin interaction. Localization of the arrestin binding locus to the clathrin terminal domain J. Biol. Chem. 272 1997 15017 15022
38. J.G. Krupnick, O.B. Goodman Jr, J.H. Keen, and J.L. Benovic Arrestin/clathrin interaction. Localization of the clathrin binding domain of nonvisual arrestins to the carboxy terminus J. Biol. Chem. 272 1997 15011 15016
39. O.B. Goodman Jr, J.G. Krupnick, F. Santini, V.V. Gurevich, R.B. Penn, and A.W. Gagnon Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor Nature 383 1996 447 450
40. A. Pulvermuller, K. Schroder, T. Fischer, and K.P. Hofmann Interactions of metarhodopsin II. Arrestin peptides compete with arrestin and transducin J. Biol. Chem. 275 2000 37679 37685
41. S.A. Laporte, R.H. Oakley, J. Zhang, J.A. Holt, S.S. Ferguson, M.G. Caron, and L.S. Barak The beta2-adrenergic receptor/betaarrestin complex recruits the clathrin adaptor AP-2 during endocytosis Proc. Natl Acad. Sci. USA 96 1999 3712 3717
42. S.A. Vishnivetskiy, M.M. Hosey, J.L. Benovic, and V.V. Gurevich Mapping the arrestin-receptor interface. Structural elements responsible for receptor specificity of arrestin proteins J. Biol. Chem. 279 2004 1262 1268
43. H. Ohguro, S. Chiba, Y. Igarashi, H. Matsumoto, T. Akino, and K. Palczewski Beta-arrestin and arrestin are recognized by autoantibodies in sera from multiple sclerosis patients Proc. Natl Acad. Sci. USA 90 1993 3241 3245
44. D.S. Gregerson, S.P. Fling, W.F. Obritsch, C.F. Merryman, and L.A. Donoso Identification of T cell recognition sites in S-antigen: dissociation of proliferative and pathogenic sites Cell. Immunol. 123 1989 427 440
45. A. Schleicher, H. Kuhn, and K.P. Hofmann Kinetics, binding constant, and activation energy of the 48-kDa protein-rhodopsin complex by extra-metarhodopsin II Biochemistry 28 1989 1770 1775
46. S.A. Vishnivetskiy, J.A. Hirsch, M.G. Velez, Y.V. Gurevich, and V.V. Gurevich Transition of arrestin into the active receptor-binding state requires an extended interdomain hinge J. Biol. Chem. 277 2002 43961 43967
47. V.V. Gurevich, C.Y. Chen, C.M. Kim, and J.L. Benovic Visual arrestin binding to rhodopsin. Intramolecular interaction between the basic N terminus and acidic C terminus of arrestin may regulate binding selectivity J. Biol. Chem. 269 1994 8721 8727
48. K. Xiao, S.K. Shenoy, K. Nobles, and R.J. Lefkowitz Activation-dependent conformational changes in {beta}-arrestin 2 J. Biol. Chem. 279 2004 55744 55753
49. S.A. Laporte, W.E. Miller, K.M. Kim, and M.G. Caron beta-Arrestin/AP-2 interaction in G protein-coupled receptor internalization: identification of a beta-arrestin binging site in beta 2-adaptin J. Biol. Chem. 277 2002 9247 9254
50. V.V. Gurevich, and J.L. Benovic Arrestin: mutagenesis, expression, purification, and functional characterization Methods Enzymol. 315 2000 422 437
51. J.R. Engen Analysis of protein complexes with hydrogen exchange and mass spectrometry Analyst 128 2003 623 628
52. J.R. Engen, T.E. Smithgall, W.H. Gmeiner, and D.L. Smith Comparison of SH3 and SH2 domain dynamics when expressed alone or in an SH(3+2) construct: the role of protein dynamics in functional regulation J. Mol. Biol. 287 1999 645 656
53. P. Glasoe, and F. Long Use of glass electrodes to measure acidities in deuterium oxide J. Phys. Chem. 64 1960 188 193
54. L. Wang, H. Pan, and D.L. Smith Hydrogen exchange-mass spectrometry: optimization of digestion conditions Mol. Cell. Proteomics 1 2002 132 138
55. Z. Zhang, C.B. Post, and D.L. Smith Amide hydrogen exchange determined by mass spectrometry: application to rabbit muscle aldolase Biochemistry 35 1996 779 791