Carboxyl-group footprinting maps the dimerization interface and phosphorylation-induced conformational changes of a membrane-associated tyrosine kinase

Molecular and Cellular Proteomics

Volumn 10, Issue 6, 2011, Pages

  Zhang, Hao ^a   Shen, Wei ^b   Rempel, Don ^a   Monsey, John ^b   Vidavsky, Ilan ^a   Gross, Michael L ^a   Bose, Ron ^b  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (3 DIMETHYLAMINOPROPYL) 3 ETHYLCARBODIIMIDE; ADENOSINE TRIPHOSPHATE; ASPARTIC ACID; CARBOXYL GROUP; CYANAMIDE; DIMER; EPIDERMAL GROWTH FACTOR RECEPTOR 4; GLUTAMIC ACID; GLYCINE ETHYL ESTER; MONOMER; TYROSINE; CARBOXYLIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; RECOMBINANT PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DIMERIZATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOOTPRINTING; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; CHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; HUMAN; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; TANDEM MASS SPECTROMETRY; TITRIMETRY;

CARBOXYLIC ACIDS; HUMANS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY; TITRIMETRY;

EID: 79957982249     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.005678     Document Type: Article

References (77)

1. Birchmeier, C. (2009) ErbB receptors and the development of the nervous system. Exp. Cell Res. 315, 611-618
2. Pentassuglia, L., and Sawyer, D. B. (2009) The role of Neuregulin-1beta/ErbB signaling in the heart. Exp. Cell Res. 315, 627-637
3. Gassmann, M., Casagranda, F., Orioli, D., Simon, H., Lai, C., Klein, R., and Lemke, G. (1995) Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378, 390-394
4. Ding, L., Getz, G., Wheeler, D. A., Mardis, E. R., McLellan, M. D., Cibulskis, K., Sougnez, C., Greulich, H., Muzny, D. M., Morgan, M. B., Fulton, L., Fulton, R. S., Zhang, Q., Wendl, M. C., Lawrence, M. S., Larson, D. E., Chen, K., Dooling, D. J., Sabo, A., Hawes, A. C., Shen, H., Jhangiani, S. N., Lewis, L. R., Hall, O., Zhu, Y., Mathew, T., Ren, Y., Yao, J., Scherer, S. E., Clerc, K., Metcalf, G. A., Ng, B., Milosavljevic, A., Gonzalez-Garay, M. L., Osborne, J. R., Meyer, R., Shi, X., Tang, Y., Koboldt, D. C., Lin, L., Abbott, R., Miner, T. L., Pohl, C., Fewell, G., Haipek, C., Schmidt, H., Dunford-Shore, B. H., Kraja, A., Crosby, S. D., Sawyer, C. S., Vickery, T., Sander, S., Robinson, J., Winckler, W., Baldwin, J., Chirieac, L. R., Dutt, A., Fennell, T., Hanna, M., Johnson, B. E., Onofrio, R. C., Thomas, R. K., Tonon, G., Weir, B. A., Zhao, X., Ziaugra, L., Zody, M. C., Giordano, T., Orringer, M. B., Roth, J. A., Spitz, M. R., Wistuba, II, Ozenberger, B., Good, P. J., Chang, A. C., Beer, D. G., Watson, M. A., Ladanyi, M., Broderick, S., Yoshizawa, A., Travis, W. D., Pao, W., Province, M. A., Weinstock, G. M., Varmus, H. E., Gabriel, S. B., Lander, E. S., Gibbs, R. A., Meyerson, M., and Wilson, R. K. (2008) Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455, 1069-1075
5. Prickett, T. D., Agrawal, N. S., Wei, X., Yates, K. E., Lin, J. C., Wunderlich, J. R., Cronin, J. C., Cruz, P., Rosenberg, S. A., and Samuels, Y. (2009) Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4. Nat. Genet. 41, 1127-1132
6. Carpenter, G. (2003) ErbB-4: mechanism of action and biology. Exp. Cell Res. 284, 66-77
7. Lemmon, M. A., and Schlessinger, J. (2010) Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134
8. Kaushansky, A., Gordus, A., Budnik, B. A., Lane, W. S., Rush, J., and MacBeath, G. (2008) System-wide investigation of ErbB4 reveals 19 sites of Tyr phosphorylation that are unusually selective in their recruitment properties. Chem. Biol. 15, 808-817
9. Zhang, X., Gureasko, J., Shen, K., Cole, P. A., and Kuriyan, J. (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149 (Pubitemid 43866200)
10. Ferguson, K. M., Darling, P. J., Mohan, M. J., Macatee, T. L., and Lemmon, M. A. (2000) Extracellular domains drive homo- but not hetero-dimerization of erbB receptors. EMBO J. 19, 4632-4643
11. Qiu, C., Tarrant, M. K., Choi, S. H., Sathyamurthy, A., Bose, R., Banjade, S., Pal, A., Bornmann, W. G., Lemmon, M. A., Cole, P. A., and Leahy, D. J. (2008) Mechanism of activation and inhibition of the HER4/ErbB4 kinase. Structure 16, 460-467 (Pubitemid 351324111)
12. Red Brewer, M., Choi, S. H., Alvarado, D., Moravcevic, K., Pozzi, A., Lemmon, M. A., and Carpenter, G. (2009) The juxtamembrane region of the EGF receptor functions as an activation domain. Mol. Cell 34, 641-651
13. Alvarado, D., Klein, D. E., and Lemmon, M. A. (2010) Structural basis for negative cooperativity in growth factor binding to an EGF receptor. Cell 142, 568-579
14. Jura, N., Endres, N. F., Engel, K., Deindl, S., Das, R., Lamers, M. H., Wemmer, D. E., Zhang, X., and Kuriyan, J. (2009) Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 137, 1293-1307
15. Monsey, J., Shen, W., Schlesinger, P., and Bose, R. (2010) Her4 and Her2/neu tyrosine kinase domains dimerize and activate in a reconstituted in vitro system. J. Biol. Chem. 285, 7035-7044
16. Macdonald, J. L., and Pike, L. J. (2008) Heterogeneity in EGF-binding affinities arises from negative cooperativity in an aggregating system. Proc. Natl. Acad. Sci. U.S.A. 105, 112-117
17. Mendoza, V. L., and Vachet, R. W. (2009) Probing protein structure by amino acid-specific covalent labeling and mass spectrometry. Mass Spectrom Rev 28, 785-815
18. Sperry, J. B., Shi, X., Rempel, D. L., Nishimura, Y., Akashi, S., and Gross, M. L. (2008) A mass spectrometric approach to the study of DNA-binding proteins: interaction of human TRF2 with telomeric DNA. Biochemistry 47, 1797-1807
19. Wales, T. E., and Engen, J. R. (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom. Rev. 25, 158-170
20. Xu, G., and Chance, M. R. (2007) Hydroxyl radical-mediated modification of proteins as probes for structural proteomics. Chem. Rev. 107, 3514-3543
21. Konermann, L., Tong, X., and Pan, Y. (2008) Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches. J. Mass Spectrom. 43, 1021-1036
22. Roulhac, P. L., Powell, K. D., Dhungana, S., Weaver, K. D., Mietzner, T. A., Crumbliss, A. L., and Fitzgerald, M. C. (2004) SUPREX (Stability of Unpurified Proteins from Rates of H/D Exchange) analysis of the thermodynamics of synergistic anion binding by ferric-binding protein (FbpA), a bacterial transferrin. Biochemistry 43, 15767-15774
23. Zhang, J., Adrián, F. J., Jahnke, W., Cowan-Jacob, S. W., Li, A. G., Iacob, R. E., Sim, T., Powers, J., Dierks, C., Sun, F., Guo, G. R., Ding, Q., Okram, B., Choi, Y., Wojciechowski, A., Deng, X., Liu, G., Fendrich, G., Strauss, A., Vajpai, N., Grzesiek, S., Tuntland, T., Liu, Y., Bursulaya, B., Azam, M., Manley, P. W., Engen, J. R., Daley, G. Q., Warmuth, M., and Gray, N. S. (2010) Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature 463, 501-506
24. Chitta, R. K., Rempel, D. L., Grayson, M. A., Remsen, E. E., and Gross, M. L. (2006) Application of SIMSTEX to oligomerization of insulin analogs and mutants. J. Am. Soc. Mass Spectrom. 17, 1526-1534
25. Perdivara, I., Deterding, L. J., Przybylski, M., and Tomer, K. B. (2010) Mass Spectrometric Identification of Oxidative Modifications of Tryptophan Residues in Proteins: Chemical Artifact or Post-Translational Modification? J. Am. Soc. Mass Spectrom. 21, 1114-1117
26. Hebling, C. M., Morgan, C. R., Stafford, D. W., Jorgenson, J. W., Rand, K. D., and Engen, J. R. (2010) Conformational analysis of membrane proteins in phospholipid bilayer nanodiscs by hydrogen exchange mass spectrometry. Anal. Chem. 82, 5415-5419
27. Pan, Y., Stocks, B. B., Brown, L., and Konermann, L. (2009) Structural characterization of an integral membrane protein in its natural lipid environment by oxidative methionine labeling and mass spectrometry. Anal. Chem. 81, 28-35
28. Zhu, Y., Guo, T., Park, J. E., Li, X., Meng, W., Datta, A., Bern, M., Lim, S. K., and Sze, S. K. (2009) Elucidating in vivo structural dynamics in integral membrane protein by hydroxyl radical footprinting. Mol. Cell Proteomics 8, 1999-2010
29. Hoare, D. G., Olson, A., and Koshland, D. E., Jr. (1968) The reaction of hydroxamic acids with water-soluble carbodiimides. A Lossen rearrangement. J. Am. Chem. Soc. 90, 1638-1643
30. Hoare, D. G., and Koshland, D. E., Jr. (1967) A method for the quantitative modification and estimation of carboxylic acid groups in proteins. J. Biol. Chem. 242, 2447-2453
31. Wen, J., Zhang, H., Gross, M. L., and Blankenship, R. E. (2009) Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting. Proc. Natl. Acad. Sci. U.S.A. 106, 6134-6139
32. Shrout, A. L., Montefusco, D. J., and Weis, R. M. (2003) Template-directed assembly of receptor signaling complexes. Biochemistry 42, 13379-13385
33. Montefusco, D. J., Asinas, A. E., and Weis, R. M. (2007) Liposome-mediated assembly of receptor signaling complexes. Methods Enzymol. 423, 267-298
34. Guo, A., Villén, J., Kornhauser, J., Lee, K. A., Stokes, M. P., Rikova, K., Possemato, A., Nardone, J., Innocenti, G., Wetzel, R., Wang, Y., Mac- Neill, J., Mitchell, J., Gygi, S. P., Rush, J., Polakiewicz, R. D., and Comb, M. J. (2008) Signaling networks assembled by oncogenic EGFR and c-Met. Proc. Natl. Acad. Sci. U.S.A. 105, 692-697 (Pubitemid 351171770)
35. Bose, R., Molina, H., Patterson, A. S., Bitok, J. K., Periaswamy, B., Bader, J. S., Pandey, A., and Cole, P. A. (2006) Phosphoproteomic analysis of Her2/neu signaling and inhibition. Proc. Natl. Acad. Sci. U.S.A. 103, 9773-9778
36. Mukherji, M., Brill, L. M., Ficarro, S. B., Hampton, G. M., and Schultz, P. G. (2006) A phosphoproteomic analysis of the ErbB2 receptor tyrosine kinase signaling pathways. Biochemistry 45, 15529-15540
37. Wolf-Yadlin, A., Kumar, N., Zhang, Y., Hautaniemi, S., Zaman, M., Kim, H. D., Grantcharova, V., Lauffenburger, D. A., and White, F. M. (2006) Effects of HER2 overexpression on cell signaling networks governing proliferation and migration. Mol. Syst. Biol. 2, 54
38. Huang, P. H., Mukasa, A., Bonavia, R., Flynn, R. A., Brewer, Z. E., Cavenee, W. K., Furnari, F. B., and White, F. M. (2007) Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc. Natl. Acad. Sci. U.S.A. 104, 12867-12872
39. Qiu, C., Tarrant, M. K., Boronina, T., Longo, P. A., Kavran, J. M., Cole, R. N., Cole, P. A., and Leahy, D. J. (2009) In vitro enzymatic characterization of near full length EGFR in activated and inhibited states. Biochemistry 48, 6624-6632
40. Szoka, F., Olson, F., Heath, T., Vail, W., Mayhew, E., and Papahadjopoulos, D. (1980) Preparation of unilamellar liposomes of intermediate size (0.1- 0.2 mumol) by a combination of reverse phase evaporation and extrusion through polycarbonate membranes. Biochim. Biophys. Acta 601, 559-571
41. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1, 2856-2860
42. Lente, G. (2010) The connection between the second law of thermodynamics and the principle of microscopic reversibility. J. Math. Chem. 47, 1106-1111
43. Tolman, R. C. (1925) The Principle of Microscopic Reversibility. Proc. Natl. Acad. Sci. U.S.A. 11, 436-439
44. Zhu, M. M., Rempel, D. L., and Gross, M. L. (2004) Modeling data from titration, amide H/D exchange, and mass spectrometry to obtain protein-ligand binding constants. J. Am. Soc. Mass Spectrom. 15, 388-397
45. Zhu, M. M., Rempel, D. L., Du, Z., and Gross, M. L. (2003) Quantification of protein-ligand interactions by mass spectrometry, titration, and H/D exchange: PLIMSTEX. J. Am. Chem. Soc. 125, 5252-5253
46. Williamson, R. E., Crowell, R. H., and Trotter, H. F. (1968) Calculus of Vector Functions, 2nd Ed., Prentice-Hall, Inc., Englewood Cliffs, New Jersey
47. Krantz, S. G., and Parks, H. R. (2003) The Implicit Function Theorem: History, Theory, and Applications, Birkhauser, Boston
48. Nagle, J. F., and Tristram-Nagle, S. (2000) Lipid bilayer structure. Curr. Opin. Struct. Biol. 10, 474-480 (Pubitemid 30496804)
49. Cullis, P. R., and Hope, M. J. (1991) Physical properties and functional roles of lipids in membranes. In: Vance, D. E., and Vance, J., eds. Biochemistry of Lipids, Lipoproteins, and Membranes, pp. 1-41, Elsevier, Amsterdam.
50. Zhang, H., Wen, J., Blankenship, R. E., and Gross, M. L. (2009) MS-based Carboxyl Group Protein Footprinting for Probing the Orientation of FMOProtein in Photosynthetic Bacterial Membranes. 57th ASMS Conference on Mass Spectrometry and Allied Topics, Philadelphia, PA
51. Huse, M., and Kuriyan, J. (2002) The conformational plasticity of protein kinases. Cell 109, 275-282 (Pubitemid 34606870)
52. Erdmann, D., Zimmermann, C., Fontana, P., Hau, J. C., De, Pover, A., and Chène, P. (2010) Simultaneous protein expression and modification: an efficient approach for production of unphosphorylated and biotinylated receptor tyrosine kinases by triple infection in the baculovirus expression system. J Biomol Tech 21, 9-17
53. Gupta, S., Bavro, V. N., D'Mello, R., Tucker, S. J., Vénien-Bryan, C., and Chance, M. R. (2010) Conformational changes during the gating of a potassium channel revealed by structural mass spectrometry. Structure 18, 839-846
54. Zheng, X., Wintrode, P. L., and Chance, M. R. (2008) Complementary structural mass spectrometry techniques reveal local dynamics in functionally important regions of a metastable serpin. Structure 16, 38-51
55. Hoofnagle, A. N., Resing, K. A., Goldsmith, E. J., and Ahn, N. G. (2001) Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange. Proc. Natl. Acad. Sci. U.S.A. 98, 956-961
56. Zhang, J., Chalmers, M. J., Stayrook, K. R., Burris, L. L., Garcia-Ordonez, R. D., Pascal, B. D., Burris, T. P., Dodge, J. A., and Griffin, P. R. (2010) Hydrogen/deuterium exchange reveals distinct agonist/partial agonist receptor dynamics within vitamin D receptor/retinoid X receptor heterodimer. Structure 18, 1332-1341
57. Zhang, X., Pickin, K. A., Bose, R., Jura, N., Cole, P. A., and Kuriyan, J. (2007) Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 450, 741-744 (Pubitemid 350207680)
58. Mi, L. Z., Grey, M. J., Nishida, N., Walz, T., Lu, C., and Springer, T. A. (2008) Functional and structural stability of the epidermal growth factor receptor in detergent micelles and phospholipid nanodiscs. Biochemistry 47, 10314-10323
59. Martin-Fernandez, M., Clarke, D. T., Tobin, M. J., Jones, S. V., and Jones, G. R. (2002) Preformed oligomeric epidermal growth factor receptors undergo an ectodomain structure change during signaling. Biophys. J. 82, 2415-2427
60. Moriki, T., Maruyama, H., and Maruyama, I. N. (2001) Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain. J. Mol. Biol. 311, 1011-1026
61. Cheng, Q. C., Tikhomirov, O., Zhou, W., and Carpenter, G. (2003) Ectodomain cleavage of ErbB-4: characterization of the cleavage site and m80 fragment. J. Biol. Chem. 278, 38421-38427 (Pubitemid 37221735)
62. Linggi, B., Cheng, Q. C., Rao, A. R., and Carpenter, G. (2006) The ErbB-4 s80 intracellular domain is a constitutively active tyrosine kinase. Oncogene 25, 160-163 (Pubitemid 43050015)
63. Ni, C. Y., Murphy, M. P., Golde, T. E., and Carpenter, G. (2001) gamma -Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294, 2179-2181 (Pubitemid 33150677)
64. Steichen, J. M., Iyer, G. H., Li, S., Saldanha, S. A., Deal, M. S., Woods, V. L., Jr., and Taylor, S. S. (2010) Global consequences of activation loop phosphorylation on protein kinase A. J. Biol. Chem. 285, 3825-3832
65. Sours, K. M., Kwok, S. C., Rachidi, T., Lee, T., Ring, A., Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2008) Hydrogen-exchange mass spectrometry reveals activation-induced changes in the conformational mobility of p38alpha MAP kinase. J. Mol. Biol. 379, 1075-1093
66. Stamos, J., Sliwkowski, M. X., and Eigenbrot, C. (2002) Structure of the epidermal growth factor receptor kinase domain alone and in complex with a 4-anilinoquinazoline inhibitor. J. Biol. Chem. 277, 46265-46272 (Pubitemid 35417619)
67. Gotoh, N., Tojo, A., Hino, M., Yazaki, Y., and Shibuya, M. (1992) A highly conserved tyrosine residue at codon 845 within the kinase domain is not required for the transforming activity of human epidermal growth factor receptor. Biochem. Biophys. Res. Commun. 186, 768-774
68. Hubbard, S. R. (1997) Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J. 16, 5572-5581
69. Canagarajah, B. J., Khokhlatchev, A., Cobb, M. H., and Goldsmith, E. J. (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90, 859-869 (Pubitemid 27381625)
70. Telesco, S. E., and Radhakrishnan, R. (2009) Atomistic insights into regulatory mechanisms of the HER2 tyrosine kinase domain: a molecular dynamics study. Biophys. J. 96, 2321-2334
71. Fraczkiewicz, R., and Braun, W. (1998) Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comp. Chem 19, 319-333 (Pubitemid 128592649)
72. Oliver, A. W., Knapp, S., and Pearl, L. H. (2007) Activation segment exchange: a common mechanism of kinase autophosphorylation? Trends Biochem. Sci 32, 351-356
73. Oliver, A. W., Paul, A., Boxall, K. J., Barrie, S. E., Aherne, G. W., Garrett, M. D., Mittnacht, S., and Pearl, L. H. (2006) Trans-activation of the DNA-damage signalling protein kinase Chk2 by T-loop exchange. EMBO J. 25, 3179-3190
74. Ogiso, H., Ishitani, R., Nureki, O., Fukai, S., Yamanaka, M., Kim, J. H., Saito, K., Sakamoto, A., Inoue, M., Shirouzu, M., and Yokoyama, S. (2002) Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 110, 775-787 (Pubitemid 35291060)
75. Tzahar, E., Waterman, H., Chen, X., Levkowitz, G., Karunagaran, D., Lavi, S., Ratzkin, B. J., and Yarden, Y. (1996) A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16, 5276-5287 (Pubitemid 26315047)
76. Jura, N., Shan, Y., Cao, X., Shaw, D. E., and Kuriyan, J. (2009) Structural analysis of the catalytically inactive kinase domain of the human EGF receptor 3. Proc. Natl. Acad. Sci. U.S.A. 106, 21608-21613
77. Shi, F., Telesco, S. E., Liu, Y., Radhakrishnan, R., and Lemmon, M. A. (2010) ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc. Natl. Acad. Sci. U.S.A. 107, 7692-7697