Conformational selection and substrate binding regulate the monomer/dimer equilibrium of the c-terminal domain of Escherichia coli enzyme I

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26989-26998

  Venditti, Vincenzo ^a   Clore, G Marius ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; CATALYTIC CYCLES; CONFORMATIONAL DYNAMICS; CONFORMATIONAL SELECTION; CONSERVED PROTEINS; CRYSTALLOGRAPHIC DATA; DIMER INTERFACE; EXCHANGE RATES; LIGAND BINDING; NMR ANALYSIS; NMR RELAXATION DISPERSION; PHOSPHATE GROUP; PHOSPHOENOLPYRUVATES; PHOSPHORYL TRANSFER; PHOSPHOTRANSFERASE SYSTEM; QUATERNARY STRUCTURE; RAPID TRANSITIONS; RESIDUAL DIPOLAR COUPLINGS; ROBUST PROTOCOL; SALT BRIDGES; SIDE-CHAINS; SIGNAL TRANSDUCTION PATHWAYS; SUBSTRATE BINDING; SUGAR TRANSPORT; TIME-SCALES;

CELL MEMBRANES; CYTOLOGY; ENZYMES; ESCHERICHIA COLI; RATE CONSTANTS; SIGNAL TRANSDUCTION; SUGARS;

DIMERS;

ARGININE; CARBOXY TERMINAL TELOPEPTIDE; DIMER; ESCHERICHIA COLI ENZYME I; ESCHERICHIA COLI PROTEIN; LYSINE; MONOMER; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM ISOLATION; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME REGULATION; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

DIMERIZATION; ESCHERICHIA COLI; HYDROLYSIS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOTRANSFERASES; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84864551231     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.382291     Document Type: Article

References (53)

1. Meadow, N. D., Fox, D. K., and Roseman, S. (1990) The bacterial phosphoenolpyruvate: Glycose phosphotransferase system. Annu. Rev. Biochem. 59, 497-542
2. Deutscher, J., Francke, C., and Postma, P. W. (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70, 939-1031 (Pubitemid 44958262)
3. Weigel, N., Waygood, E. B., Kukuruzinska, M. A., Nakazawa, A., and Roseman, S. (1982) Sugar transport by the bacterial phosphotransferase system. Isolation and characterization of enzyme I from Salmonella typhimurium. J. Biol. Chem. 257, 14461-14469
4. Weigel, N., Kukuruzinska, M. A., Nakazawa, A., Waygood, E. B., and Roseman, S. (1982) Sugar transport by the bacterial phosphotransferase system. Phosphoryl transfer reactions catalyzed by enzyme I of Salmonella typhimurium. J. Biol. Chem. 257, 14477-14491
5. Doucette, C. D., Schwab, D. J., Wingreen, N. S., and Rabinowitz, J. D. (2011) α-Ketoglutarate coordinates carbon and nitrogen utilization via enzyme I inhibition. Nature Chem. Biol. 7, 894-901
6. Mukhija, S., and Erni, B. (1997) Phage display selection of peptides against enzyme I of the phosphoenolpyruvate-sugar phosphotransferase system (PTS). Mol. Microbiol. 25, 1159-1166 (Pubitemid 27410194)
7. Chauvin, F., Brand, L., and Roseman, S. (1994) Sugar transport by the bacterial phosphotransferase system. Characterization of the Escherichia coli enzyme I monomer/dimer transition kinetics by fluorescence anisotropy. J. Biol. Chem. 269, 20270-20274
8. Chauvin, F., Fomenkov, A., Johnson, C. R., and Roseman, S. (1996) The N-terminal domain of Escherichia coli enzyme I of the phosphoenolpyruvate/ glycose phosphotransferase system: Molecular cloning and characterization. Proc. Natl. Acad. Sci. U.S.A. 93, 7028-7031 (Pubitemid 26243495)
9. Chauvin, F., Brand, L., and Roseman, S. (1996) Enzyme I: The first protein and potential regulator of the bacterial phosphoenolpyruvate:glycose phosphotransferase system. Res. Microbiol. 147, 471-479 (Pubitemid 26338125)
10. Liao, D. I., Silverton, E., Seok, Y. J., Lee, B. R., Peterkofsky, A., and Davies, D. R. (1996) The first step in sugar transport: Crystal structure of the amino terminal domain of enzyme I of the Escherichia coli PEP:sugar phosphotransferase system and a model of the phosphotransfer complex with HPr. Structure 4, 861-872 (Pubitemid 26312369)
11. Garrett, D. S., Seok, Y. J., Liao, D. I., Peterkofsky, A., Gronenborn, A. M., and Clore, G. M. (1997) Solution structure of the 30-kDa N-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system by multidimensional NMR. Biochemistry 36, 2517-2530 (Pubitemid 27106644)
12. Seok, Y. J., Lee, B. R., Zhu, P. P., and Peterkofsky, A. (1996) Importance of the carboxyl-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system for phosphoryl donor specificity. Proc. Natl. Acad. Sci. U.S.A. 93, 347-351 (Pubitemid 26038156)
13. Seok, Y. J., Zhu, P. P., Koo, B. M., and Peterkofsky, A. (1998) Autophosphorylation of enzyme I of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system requires dimerization. Biochem. Biophys. Res. Commun. 250, 381-384
14. Patel, H. V., Vyas, K. A., Mattoo, R. L., Southworth, M., Perler, F. B., Comb, D., and Roseman, S. (2006) Properties of the C-terminal domain of enzyme I of the Escherichia coli phosphotransferase system. J. Biol. Chem. 281, 17579-17587 (Pubitemid 44035557)
15. Teplyakov, A., Lim, K., Zhu, P. P., Kapadia, G., Chen, C. C., Schwartz, J., Howard, A., Reddy, P. T., Peterkofsky, A., and Herzberg, O. (2006) Structure of phosphorylated enzyme I, the phosphoenolpyruvate:sugar phosphotransferase system sugar translocation signal protein. Proc. Natl. Acad. Sci. U.S.A. 103, 16218-16223 (Pubitemid 44715177)
16. Oberholzer, A. E., Schneider, P., Siebold, C., Baumann, U., and Erni, B. (2009) Crystal structure of enzyme I of the phosphoenolpyruvate sugar phosphotransferase system in the dephosphorylated state. J. Biol. Chem. 284, 33169-33176
17. Schwieters, C. D., Suh, J. Y., Grishaev, A., Ghirlando, R., Takayama, Y., and Clore, G. M. (2010) Solution structure of the 128 kDa enzyme I dimer from Escherichia coli and its 146-kDa complex with HPr using residual dipolar couplings and small- and wide-angle X-ray scattering. J. Am. Chem. Soc. 132, 13026-13045
18. Takayama, Y., Schwieters, C. D., Grishaev, A., Ghirlando, R., and Clore, G. M. (2011) Combined use of residual dipolar couplings and solution x-ray scattering to rapidly probe rigid-body conformational transitions in a non-phosphorylatable active-site mutant of the 128-kDa enzyme I dimer. J. Am. Chem. Soc. 133, 424-427
19. Waygood, E. B., Meadow, N. D., and Roseman, S. (1979) Modified assay procedures for the phosphotransferase system in enteric bacteria. Anal. Biochem. 95, 293-304 (Pubitemid 9194294)
20. Saier, M. H., Jr., Schmidt, M. R., and Lin, P. (1980) Phosphoryl exchange reaction catalyzed by enzyme I of the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Kinetic characterization. J. Biol. Chem. 255, 8579-8584
21. Meadow, N. D., Mattoo, R. L., Savtchenko, R. S., and Roseman, S. (2005) Transient state kinetics of enzyme I of the phosphoenolpyruvate:glycose phosphotransferase system of Escherichia coli: equilibrium and second-order rate constants for the phosphotransfer reactions with phosphoenolpyruvate and HPr. Biochemistry 44, 12790-12796 (Pubitemid 41377318)
22. Patel, H. V., Vyas, K. A., Savtchenko, R., and Roseman, S. (2006) The monomer/dimer transition of enzyme I of the Escherichia coli phosphotransferase system. J. Biol. Chem. 281, 17570-17578 (Pubitemid 44035556)
23. Rohwer, J. M., Meadow, N. D., Roseman, S., Westerhoff, H. V., and Postma, P. W. (2000) Understanding glucose transport by the bacterial phosphoenolpyruvate:glycose phosphotransferase system on the basis of kinetic measurements in vitro. J. Biol. Chem. 275, 34909-34921
24. Suh, J. Y., Cai, M., and Clore, G. M. (2008) Impact of phosphorylation on structure and thermodynamics of the interaction between the N-terminal domain of enzyme I and the histidine phosphocarrier protein of the bacterial phosphotransferase system. J. Biol. Chem. 283, 18980-18989
25. r phosphoryl transfer complex between the N-terminal domain of enzyme I and HPr. Nature Struct. Biol. 6, 166-173
26. Márquez, J., Reinelt, S., Koch, B., Engelmann, R., Hengstenberg, W., and Scheffzek, K. (2006) Structure of the full-length enzyme I of the phosphoenolpyruvate-dependent sugar phosphotransferase system. J. Biol. Chem. 281, 32508-32515 (Pubitemid 46036805)
27. Oberholzer, A. E., Bumann, M., Schneider, P., Bächler, C., Siebold, C., Baumann, U., and Erni, B. (2005) Crystal structure of the phosphoenolpyruvate-binding enzyme I domain from the Thermoanaerobacter tengcongensis PEP:sugar phosphotransferase system (PTS). J. Mol. Biol. 346, 521-532
28. Navdaeva, V., Zurbriggen, A., Waltersperger, S., Schneider, P., Oberholzer, A. E., Bähler, P., Bächler, C., Grieder, A., Baumann, U., and Erni, B. (2011) Phosphoenolpyruvate:sugar phosphotransferase system from the hyperthermophilic Thermoanaerobacter tengcongensis. Biochemistry 50, 1184-1193
29. LiCalsi, C., Crocenzi, T. S., Freire, E., and Roseman, S. (1991) Sugar transport by the bacterial phosphotransferase system. Structural and thermodynamic domains of enzyme I of Salmonella typhimurium. J. Biol. Chem. 266, 19519-19527
30. Palmer, A. G., 3rd. (2004) NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104, 3623-3640
31. Mittermaier, A., and Kay, L. E. (2006) New tools provide new insights in NMR studies of protein dynamics. Science 312, 224-228
32. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
33. 2relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. U.S.A. 94, 12366-12371
34. Tugarinov, V., Muhandiram, R., Ayed, A., and Kay, L. E. (2002) Four-dimensional NMR spectroscopy of a 723-residue protein: Chemical shift assignments and secondary structure of malate synthase g. J. Am. Chem. Soc. 124, 10025-10035 (Pubitemid 34919738)
35. Clore, G. M., and Gronenborn, A. M. (1998) Determining the structures of large proteins and protein complexes by NMR. Trends Biotechnol. 16, 22-34 (Pubitemid 28064815)
36. Ulrich, E. L., Akutsu, H., Doreleijers, J. F., Harano, Y., Ioannidis, Y. E., Lin, J., Livny, M., Mading, S., Maziuk, D., Miller, Z., Nakatani, E., Schulte, C. F., Tolmie, D. E., Kent Wenger, R., Yao, H., and Markley, J. (2008) BioMagResBank. Nucleic Acids Res. 36, D402-D408 (Pubitemid 351149757)
37. Mulder, F. A., Schipper, D., Bott, R., and Boelens, R. (1999) Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins. J. Mol. Biol. 292, 111-123 (Pubitemid 29425657)
38. Bax, A., Kontaxis, G., and Tjandra, N. (2001) Dipolar couplings in macro-molecular structure determination. Methods Enzymol. 339, 127-174 (Pubitemid 32666560)
39. Clore, G. M., Starich, M. R., and Gronenborn, A. M. (1998) Measurement of residual dipolar couplings of macromolecules aligned in the nematic phase of a colloidal suspension of rod-shaped viruses. J. Am. Chem. Soc. 120, 10571-10572 (Pubitemid 28500376)
40. Hansen, M. R., Mueller, L., and Pardi, A. (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nature Struct. Biol. 5, 1065-1074 (Pubitemid 28546270)
41. 15N residual dipolar couplings in larger perdeuterated proteins. J. Biomol. NMR 48, 65-70
42. Schwieters, C. D., Kuszewski, J., and Clore, G. M. (2006) Using Xplor-NIH for NMR molecular structure determination. Progr. NMR Spectroscopy 48, 47-62
43. Loria, J. P., Rance, M., and Palmer, A. G., 3rd. (1999) A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J. Biomol. NMR 15, 151-155
44. 15N relaxation experiment. J. Magn. Reson. 171, 25-36
45. 15N relaxation dispersion NMR spectroscopy: Application to Asn and Gln residues in a cavity mutant of T4 lysozyme. J. Am. Chem. Soc. 123, 967-975
46. 2 (CPMG) methods. J. Magn. Reson. Ser. B 104, 266-275
47. Millet, O., Loria, J. P., Kroenke, C. D., Pons, M., and Palmer, A. G., III (2000) The static magnetic field dependence of chemical exchange line broadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122, 2867-2877 (Pubitemid 30191047)
48. Venditti, V., Fawzi, N. L., and Clore, G. M. (2012) An efficient protocol for incorporation of an unnatural amino acid in perdeuterated recombinant proteins using glucose-based media. J. Biomol. NMR 52, 191-195
49. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
50. Prestegard, J. H., al-Hashimi, H. M., and Tolman, J. R. (2000) NMR structures of biomolecules using field oriented media and residual dipolar couplings. Q. Rev. Biophys. 33, 371-424 (Pubitemid 32151707)
51. Clore, G. M. (2000) Accurate and rapid docking of protein-protein complexes on the basis of intermolecular nuclear overhauser enhancement data and dipolar couplings by rigid body minimization. Proc. Natl. Acad. Sci. U.S.A. 97, 9021-9025
52. Clore, G. M., and Garrett, D. S. (1999) R-factor, free R, and complete cross-validation for dipolar coupling refinement of NMR structures. J. Am. Chem. Soc. 121, 9008-9012
53. Ma, B., and Nussinov, R. (2010) Enzyme dynamics point to stepwise conformational selection in catalysis. Curr. Opin. Chem. Biol. 14, 652-659