Solution structure of the IIAChitobiose-HPr complex of the N,N′-diacetylchitobiose branch of the Escherichia coli phosphotransferase system

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 23819-23829

  Jung, Young Sang ^a,b   Cai, Mengli ^a   Clore, G Marius ^a  

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

^b Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ACTIVE SITE RESIDUES; BINDING SURFACE; CHARGED RESIDUES; CHITOBIOSE; CLOSE PROXIMITY; CONFORMATIONAL CHANGE; CONFORMATIONAL PLASTICITY; HYDROPHOBIC RESIDUES; INTERMOLECULAR INTERACTIONS; PHOSPHORYL TRANSFER; PHOSPHOTRANSFERASE SYSTEM; POLAR RESIDUES; SIDE-CHAINS; SOLUTION STRUCTURES; STRUCTURAL ELEMENTS; STRUCTURE ELUCIDATION; TRANSITION STATE;

ESCHERICHIA COLI; OLIGOMERS; PHOSPHORYLATION;

AMINO ACIDS;

CHITOBIOSE; GLUTAMINE; HISTIDINE; PHOSPHOTRANSFERASE; BACTERIAL PROTEIN; DISACCHARIDE; ESCHERICHIA COLI PROTEIN; N,N DIACETYLCHITOBIOSE; N,N-DIACETYLCHITOBIOSE; PHOSPHOCARRIER PROTEIN HPR; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CYTOPLASM; ESCHERICHIA COLI; HYDROPHOBICITY; INTERSPERSED REPEAT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SUGAR TRANSPORT; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ENZYME ACTIVE SITE; GENETICS; METABOLISM; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SOLUTION AND SOLUBILITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL PROTEINS; BINDING SITES; CATALYTIC DOMAIN; DISACCHARIDES; ESCHERICHIA COLI PROTEINS; HISTIDINE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTATION; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS;

EID: 84863618406     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.371492     Document Type: Article

References (71)

1. Kundig, W., Ghosh, S., and Roseman, S. (1964) Phosphate bound to histidine in a protein as an intermediate in a novel phosphotransferase system. Proc. Natl. Acad. Sci. U.S.A. 52, 1067-1074
2. Meadow, N. D., Fox, D. K., and Roseman, S. (1990) The bacterial phosphoenolpyruvate. Glycose phosphotransferase system. Annu. Rev. Biochem. 59, 497-542
3. Postma, P. W., Lengeler, J. W., and Jacobson, G. R. (1993) Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57, 543-594 (Pubitemid 23262509)
4. Robillard, G. T., and Broos, J. (1999) Structure/function studies on the bacterial carbohydrate transporters, enzymes II, of the phosphoenolpyruvate- dependent phosphotransferase system. Biochim. Biophys. Acta 1422, 73-104 (Pubitemid 29313326)
5. Siebold, C., Flükiger, K., Beutler, R., and Erni, B. (2001) Carbohydrate transporters of the bacterial phosphoenolpyruvate:sugar phosphotransferase system (PTS). FEBS Lett. 504, 104-111 (Pubitemid 32787057)
6. 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)
7. mannitol of the Escherichia coli phosphotransferase system. J. Biol. Chem. 279, 39115-39121
8. Mannitol of the Escherichia coli phosphotransferase system by NMR spectroscopy and residual dipolar couplings. J. Mol. Biol. 353, 1129-1136
9. cellobiose, reveals similarity to eukaryotic protein-tyrosine phosphatases. Structure 5, 217-225
10. cellobiose of the phosphoenolpyruvate-dependent phosphotransferase system of Escherichia coli. Protein Sci. 6, 304-314
11. Ab, E., Schuurman-Wolters, G. K., Nijlant, D., Dijkstra, K., Saier, M. H., Robillard, G. T., and Scheek, R. M. (2001) NMR structure of cysteinylphosphorylated enzyme IIB of the N,N′-diacetylchitobiose-specific phosphoenolpyruvate-dependent phosphotransferase system of Escherichia coli. J. Mol. Biol. 308, 993-1009 (Pubitemid 32574374)
12. Kalbitzer, H. R., and Hengstenberg, W. (1993) The solution structure of the histidine-containing protein (HPr) from Staphylococcus aureus as determined by two-dimensional 1H-NMR spectroscopy. Eur. J. Biochem. 216, 205-214 (Pubitemid 23255189)
13. Wittekind, M., Rajagopal, P., Branchini, B. R., Reizer, J., Saier, M. H., Jr., and Klevit, R. E. (1992) Solution structure of the phosphocarrier protein HPr from Bacillus subtilis by two-dimensional NMR spectroscopy. Protein Sci. 1, 1363-1376 (Pubitemid 23009230)
14. Eberstadt, M., Grdadolnik, S. G., Gemmecker, G., Kessler, H., Buhr, A., and Erni, B. (1996) Solution structure of the IIB domain of the glucose transporter of Escherichia coli. Biochemistry 35, 11286-11292 (Pubitemid 26299301)
15. Hu, J., Hu, K., Williams, D. C., Jr., Komlosh, M. E., Cai, M., and Clore, G. M. (2008) Solution NMR structures of productive and nonproductive complexes between the A and B domains of the cytoplasmic subunit of the mannose transporter of the Escherichia coli phosphotransferase system. J. Biol. Chem. 283, 11024-11037
16. Glucose of the Escherichia coli glucose phosphotransferase system. J. Biol. Chem. 278, 25191-25206
17. 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)
18. 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
19. Takayama, Y., Schwieters, C. D., Grishaev, A., Ghirlando, R., and Clore, G. M. (2010) Combined use of residual dipolar couplings and solution x-ray scattering to rapidly probe rigid-body conformational transitions in a nonphosphorylatable active-site mutant of the 128-kDa enzyme I dimer. J. Am. Chem. Soc.
20. Chitobiose from the N,N′-diacetylchitobiose branch of the Escherichia coli phosphotransferase system. J. Biol. Chem. 280, 11770-11780
21. mannitol reveals a novel fold with two conformations of the active site. Structure 6, 377-388
22. 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)
23. 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
24. 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
25. Sor domain of the sorbose permease from Klebsiella pneumoniae solved to 1.75-Å resolution. J. Mol. Biol. 327, 1111-1119
26. Liao, D. I., Kapadia, G., Reddy, P., Saier, M. H., Jr., Reizer, J., and Herzberg, O. (1991) Structure of the IIA domain of the glucose permease of Bacillus subtilis at 2.2-Å resolution. Biochemistry 30, 9583-9594
27. 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 E. coli PEP:sugar phosphotransferase system and a model of the phosphotransfer complex with HPr. Structure 4, 861-872 (Pubitemid 26312369)
28. Máarquez, 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)
29. Herzberg, O., Reddy, P., Sutrina, S., Saier, M. H., Jr., Reizer, J., and Kapadia, G. (1992) Structure of the histidine-containing phosphocarrier protein HPr from Bacillus subtilis at 2.0-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 89, 2499-2503
30. Jia, Z., Quail, J. W., Waygood, E. B., and Delbaere, L. T. (1993) The 2.0-Åresolution structure of Escherichia coli histidine-containing phosphocarrier protein HPr. A redetermination. J. Biol. Chem. 268, 22490-22501 (Pubitemid 23318300)
31. Worthylake, D., Meadow, N. D., Roseman, S., Liao, D. I., Herzberg, O., and Remington, S. J. (1991) Three-dimensional structure of the Escherichia coli phosphocarrier protein IIIGlc. Proc. Natl. Acad. Sci. U.S.A. 88, 10382-10386 (Pubitemid 21915839)
32. lactose from Lactococcus lactis reveals a new fold and points to possible interactions of a multicomponent system. Structure 5, 775-788
33. Nunn, R. S., Marković-Housley, Z., Génovésio- Taverne, J. C., Flükiger, K., Rizkallah, P. J., Jansonius, J. N., Schirmer, T., and Erni, B. (1996) Structure of the IIA domain of the mannose transporter from Escherichia coli at 1.7-Å resolution. J. Mol. Biol. 259, 502-511
34. Schauder, S., Nunn, R. S., Lanz, R., Erni, B., and Schirmer, T. (1998) Crystal structure of the IIB subunit of a fructose permease (IIBLev) from Bacillus subtilis. J. Mol. Biol. 276, 591-602 (Pubitemid 28116132)
35. Navdaeva, V., Zurbriggen, A., Waltersperger, S., Schneider, P., Oberholzer, A. E., Bahler, P., Bachler, C., Grieder, A., Baumann, U., and Erni, B. (2011) Phosphoenolpyruvate:sugar phosphotransferase system from the hyperthermophilic Thermoanaerobacter tengcongensis. Biochemistry 50, 1184-1193
36. r phosphoryl transfer complex between the N-terminal domain of enzyme I and HPr. Nature Struct. Biol. 6, 166-173
37. glucose of the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system. EMBO J. 19, 5635-5649
38. Mannitoland HPr of the Escherichia coli phosphotransferase system. J. Biol. Chem. 277, 42289-42298
39. Mannose-HPr complex of the Escherichia coli mannose phosphotransferase system. J. Biol. Chem. 280, 20775-20784
40. Suh, J. Y., Cai, M., Williams, D. C., Jr., and Clore, G. M. (2006) Solution structure of a post-transition state analog of the phosphotransfer reaction between the A and B cytoplasmic domains of the mannitol transporter IIMannitol of the Escherichia coli phosphotransferase system. J. Biol. Chem. 281, 8939-8949 (Pubitemid 43848001)
41. Suh, J. Y., Iwahara, J., and Clore, G. M. (2007) Intramolecular domaindomain association/dissociation and phosphoryl transfer in the mannitol transporter of Escherichia coli are not coupled. Proc. Natl. Acad. Sci. U.S.A. 104, 3153-3158 (Pubitemid 46364129)
42. 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
43. Chitobiose complex of the N,N′-diacetylchitobiose branch of the Escherichia coli phosphotransferase system. J. Biol. Chem. 285, 4173-4184
44. Tang, C., Iwahara, J., and Clore, G. M. (2006) Visualization of transient encounter complexes in protein-protein association. Nature 444, 383-386 (Pubitemid 44764115)
45. Suh, J. Y., Tang, C., and Clore, G. M. (2007) Role of electrostatic interactions in transient encounter complexes in protein-protein association investigated by paramagnetic relaxation enhancement. J. Am. Chem. Soc. 129, 12954-12955 (Pubitemid 350058334)
46. Fawzi, N. L., Doucleff, M., Suh, J. Y., and Clore, G. M. (2010) Mechanistic details of a protein-protein association pathway revealed by paramagnetic relaxation enhancement titration measurements. Proc. Natl. Acad. Sci. U.S.A. 107, 1379-1384
47. Garrett, D. S., Seok, Y. J., Peterkofsky, A., Clore, G. M., and Gronenborn, A. M. (1997) Identification by NMR of the binding surface for the histidine-containing phosphocarrier protein HPr on the N-terminal domain of enzyme I of the Escherichia coli phosphotransferase system. Biochemistry 36, 4393-4398 (Pubitemid 27180285)
48. 2H-labeled proteins. J. Biomol.NMR 13, 369-374
49. 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
50. Garrett, D. S., Powers, R., Gronenborn, A. M., and Clore, G. M. (1991) A common sense approach to picking two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams. J. Magn. Reson. 95, 214-220
51. Clore, G. M., and Gronenborn, A. M. (1991) Structures of larger proteins in solution. Three- and four-dimensional heteronuclear NMR spectroscopy. Science 252, 1390-1399 (Pubitemid 21917051)
52. N-detected triple resonance TROSY-based experiments. J. Biomol. NMR 13, 3-10
53. 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)
54. Cai, M., Huang, Y., Zheng, R., Wei, S. Q., Ghirlando, R., Lee, M. S., Craigie, R., Gronenborn, A. M., and Clore, G. M. (1998) Solution structure of the cellular factor BAF responsible for protecting retroviral DNA from autointegration. Nature Struct. Biol. 5, 903-909 (Pubitemid 28467414)
55. Clore, G. M., and Gronenborn, A. M. (1998) New methods of structure refinement for macromolecular structure determination by NMR. Proc. Natl. Acad. Sci. U.S.A. 95, 5891-5898 (Pubitemid 28248936)
56. Clore, G. M., Gronenborn, A. M., Nilges, M., and Ryan, C. A. (1987) Three-dimensional structure of potato carboxypeptidase inhibitor in solution. A study using nuclear magnetic resonance, distance geometry, and restrained molecular dynamics. Biochemistry 26, 8012-8023
57. 1H NMR. Proteins 17, 297-309
58. 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
59. 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
60. Schwieters, C. D., and Clore, G. M. (2001) Internal coordinates for molecular dynamics and minimization in structure determination and refinement. J. Magn. Reson. 152, 288-302
61. Schwieters, C. D., Kuszewski, J., and Clore, G. M. (2006) Using Xplor-NIH for NMR molecular structure determination. Progr. NMR Spectros. 48, 47-62
62. 1 rotamer populations and angles of mobile surface side chains are accurately predicted by a torsion angle database potential of mean force. J. Am. Chem. Soc. 124, 2866-2867
63. Schwieters, C. D., and Clore, G. M. (2008) A pseudopotential for improving the packing of ellipsoidal protein structures determined from NMR data. J. Phys. Chem. B 112, 6070-6073
64. Schwieters, C. D., and Clore, G. M. (2001) The VMD-XPLOR visualization package forNMRstructure refinement. J. Magn. Reson. 149, 239-244
65. Nicholls, A., Sharp, K. A., and Honig, B. (1991) Protein folding and association. Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296
66. Schwieters, C. D., and Clore, G. M. (2002) Reweighted atomic densities to represent ensembles of NMR structures. J. Biomol. NMR 23, 221-225 (Pubitemid 34982254)
67. Begley, G. S., Hansen, D. E., Jacobson, G. R., and Knowles, J. R. (1982) Stereochemical course of the reactions catalyzed by the bacterial phosphoenolpyruvate: glucose phosphotransferase system. Biochemistry 21, 5552-5556
68. Herzberg, O. (1992) An atomic model for protein-protein phosphoryl group transfer. J. Biol. Chem. 267, 24819-24823
69. Grzesiek, S., Stahl, S. J., Wingfield, P. T., and Bax, A. (1996) The CD4 determinant for down-regulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 35, 10256-10261 (Pubitemid 26277283)
70. Clore, G. M., and Garrett, D. S. (1999) R-factor, free R, and complete coss-validation for dipolar coupling refinement ofNMRstructures. J. Am. Chem. Soc. 121, 9008-9012
71. Laskowski, R. A., McArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK. A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291