Home LiteratureArticle Details
PMID: 11060015 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

Solution structure of the phosphoryl transfer complex between the signal transducing proteins HPr and IIA(glucose) of the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system.

The EMBO journal ·Vol. 19 ·No. 21 ·2000-11-01 ·Pages 5635-49

Wang G, Louis JM, Sondej M, Seok YJ, Peterkofsky A, Clore GM

Abstract

The solution structure of the second protein-protein complex of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system, that between histidine-containing phosphocarrier protein (HPr) and glucose-specific enzyme IIA(Glucose) (IIA(Glc)), has been determined by NMR spectroscopy, including the use of dipolar couplings to provide long-range orientational information and newly developed rigid body minimization and constrained/restrained simulated annealing methods. A protruding convex surface on HPr interacts with a complementary concave depression on IIA(Glc). Both binding surfaces comprise a central hydrophobic core region surrounded by a ring of polar and charged residues, positive for HPr and negative for IIA(Glc). Formation of the unphosphorylated complex, as well as the phosphorylated transition state, involves little or no change in the protein backbones, but there are conformational rearrangements of the interfacial side chains. Both HPr and IIA(Glc) recognize a variety of structurally diverse proteins. Comparisons with the structures of the enzyme I-HPr and IIA(Glc)-glycerol kinase complexes reveal how similar binding surfaces can be formed with underlying backbone scaffolds that are structurally dissimilar and highlight the role of redundancy and side chain conformational plasticity.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/chemistry,genetics Binding Sites Escherichia coli/enzymology,genetics Escherichia coli Proteins Glycerol Kinase/chemistry,genetics Macromolecular Substances Magnetic Resonance Spectroscopy Models, Molecular Phosphoenolpyruvate Sugar Phosphotransferase System/chemistry,genetics Protein Conformation Signal Transduction Solutions
Chemicals
Bacterial Proteins Escherichia coli Proteins Macromolecular Substances Solutions crr protein, E coli Phosphoenolpyruvate Sugar Phosphotransferase System phosphocarrier protein HPr Glycerol Kinase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wang G
Laboratory of Chemical Physics, Building 5, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892-0510, USA.
Louis J M
Sondej M
Seok Y J
Peterkofsky A
Clore G M
References (71)
71 references, click to expand
  1. Functional interactions between proteins of the phosphoenolpyruvate:sugar phosphotransferase systems of Bacillus subtilis and Escherichia coli.
    J Biol Chem. 1992 May 5;267(13):9158-69 PMID: 1577753
  2. Structural comparison of phosphorylated and unphosphorylated forms of IIIGlc, a signal-transducing protein from Escherichia coli, using three-dimensional NMR techniques.
    Biochemistry. 1992 Jun 9;31(22):5215-24 PMID: 1606145
  3. Overproduction and rapid purification of the phosphoenolpyruvate:sugar phosphotransferase system proteins enzyme I, HPr, and Protein IIIGlc of Escherichia coli.
    Protein Expr Purif. 1991 Apr-Jun;2(2-3):179-87 PMID: 1821787
  4. An atomic model for protein-protein phosphoryl group transfer.
    J Biol Chem. 1992 Dec 5;267(34):24819-23 PMID: 1447219
  5. Mapping of the binding interfaces of the proteins of the bacterial phosphotransferase system, HPr and IIAglc.
    Biochemistry. 1993 Jan 12;32(1):32-7 PMID: 8418852
  6. Structure of the regulatory complex of Escherichia coli IIIGlc with glycerol kinase.
    Science. 1993 Jan 29;259(5095):673-7 PMID: 8430315
  7. Bacterial adenylyl cyclases.
    Prog Nucleic Acid Res Mol Biol. 1993;44:31-65 PMID: 8434125
  8. NMRPipe: a multidimensional spectral processing system based on UNIX pipes.
    J Biomol NMR. 1995 Nov;6(3):277-93 PMID: 8520220
  9. Principles of protein-protein interactions.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):13-20 PMID: 8552589
  10. Structure of the IIA domain of the mannose transporter from Escherichia coli at 1.7 angstroms resolution.
    J Mol Biol. 1996 Jun 14;259(3):502-11 PMID: 8676384
  11. 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. 1996 Jul 9;93(14):7028-31 PMID: 8692938
  12. MOLMOL: a program for display and analysis of macromolecular structures.
    J Mol Graph. 1996 Feb;14(1):51-5, 29-32 PMID: 8744573
  13. Mutation of serine-46 to aspartate in the histidine-containing protein of Escherichia coli mimics the inactivation by phosphorylation of serine-46 in HPrs from gram-positive bacteria.
    Biochemistry. 1996 Sep 3;35(35):11260-7 PMID: 8784179
  14. Solution structure of the IIB domain of the glucose transporter of Escherichia coli.
    Biochemistry. 1996 Sep 3;35(35):11286-92 PMID: 8784182
  15. A common interface on histidine-containing phosphocarrier protein for interaction with its partner proteins.
    J Biol Chem. 2000 Jun 2;275(22):16401-3 PMID: 10764730
  16. Rational design of faster associating and tighter binding protein complexes.
    Nat Struct Biol. 2000 Jul;7(7):537-41 PMID: 10876236
  17. 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. 2000 Aug 1;97(16):9021-5 PMID: 10922057
  18. Sources of and solutions to problems in the refinement of protein NMR structures against torsion angle potentials of mean force.
    J Magn Reson. 2000 Oct;146(2):249-54 PMID: 11001840
  19. Sugar transport by the bacterial phosphotransferase system. Isolation and characterization of a phosphocarrier protein HPr from wild type and mutants of Salmonella typhimurium.
    J Biol Chem. 1982 Dec 10;257(23):14492-8 PMID: 6754731
  20. Sugar transport by the bacterial phosphotransferase system. Primary structure and active site of a general phosphocarrier protein (HPr) from Salmonella typhimurium.
    J Biol Chem. 1982 Dec 10;257(23):14499-509 PMID: 6754732
  21. Sugar transport by the bacterial phosphotransferase system. Isolation and characterization of a glucose-specific phosphocarrier protein (IIIGlc) from Salmonella typhimurium.
    J Biol Chem. 1982 Dec 10;257(23):14526-37 PMID: 6754734
  22. 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. 1996 Jul 15;4(7):861-72 PMID: 8805571
  23. Solution structure of the phosphocarrier protein HPr from Bacillus subtilis by two-dimensional NMR spectroscopy.
    Protein Sci. 1992 Oct;1(10):1363-76 PMID: 1303754
  24. The involvement of the arginine 17 residue in the active site of the histidine-containing protein, HPr, of the phosphoenolpyruvate:sugar phosphotransferase system of Escherichia coli.
    J Biol Chem. 1993 Jun 15;268(17):12325-33 PMID: 8509371
  25. Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques.
    Protein Sci. 1993 Apr;2(4):543-58 PMID: 8518729
  26. Involvement of various amino- and carboxyl-terminal residues in the active site of the histidine-containing protein HPr of the phosphoenolpyruvate-dependent phosphotransferase system of Staphylococcus carnosus: site-directed mutagenesis with the ptsH gene, biochemical characterization and NMR studies of the mutant proteins.
    Protein Eng. 1993 Jun;6(4):417-23 PMID: 8332599
  27. The solution structure of the histidine-containing protein (HPr) from Staphylococcus aureus as determined by two-dimensional 1H-NMR spectroscopy.
    Eur J Biochem. 1993 Aug 15;216(1):205-14 PMID: 8365407
  28. The 2.0-A resolution structure of Escherichia coli histidine-containing phosphocarrier protein HPr. A redetermination.
    J Biol Chem. 1993 Oct 25;268(30):22490-501 PMID: 8226757
  29. A calculation strategy for the structure determination of symmetric dimers by 1H NMR.
    Proteins. 1993 Nov;17(3):297-309 PMID: 8272427
  30. The high-resolution structure of the histidine-containing phosphocarrier protein HPr from Escherichia coli determined by restrained molecular dynamics from nuclear magnetic resonance nuclear Overhauser effect data.
    J Mol Biol. 1994 Apr 15;237(5):544-59 PMID: 8158637
  31. Measurement of homo- and heteronuclear J couplings from quantitative J correlation.
    Methods Enzymol. 1994;239:79-105 PMID: 7830604
  32. High-resolution structure of the phosphorylated form of the histidine-containing phosphocarrier protein HPr from Escherichia coli determined by restrained molecular dynamics from NMR-NOE data.
    J Mol Biol. 1995 Feb 10;246(1):180-93 PMID: 7853396
  33. Unique dicistronic operon (ptsI-crr) in Mycoplasma capricolum encoding enzyme I and the glucose-specific enzyme IIA of the phosphoenolpyruvate:sugar phosphotransferase system: cloning, sequencing, promoter analysis, and protein characterization.
    Protein Sci. 1994 Nov;3(11):2115-28 PMID: 7703858
  34. Unraveling a bacterial hexose transport pathway.
    Curr Opin Struct Biol. 1994 Dec;4(6):814-22 PMID: 7712285
  35. The nature of the transition state for enzyme-catalyzed phosphoryl transfer. Hydrolysis of O-aryl phosphorothioates by alkaline phosphatase.
    Biochemistry. 1995 Sep 26;34(38):12255-64 PMID: 7547968
  36. Rate and equilibrium constants for phosphoryltransfer between active site histidines of Escherichia coli HPr and the signal transducing protein IIIGlc.
    J Biol Chem. 1996 Dec 27;271(52):33440-5 PMID: 8969207
  37. Structures of active site histidine mutants of IIIGlc, a major signal-transducing protein in Escherichia coli. Effects on the mechanisms of regulation and phosphoryl transfer.
    J Biol Chem. 1996 Dec 27;271(52):33446-56 PMID: 8969208
  38. The structure of an energy-coupling protein from bacteria, IIBcellobiose, reveals similarity to eukaryotic protein tyrosine phosphatases.
    Structure. 1997 Feb 15;5(2):217-25 PMID: 9032081
  39. The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode.
    Nat Struct Biol. 1997 Feb;4(2):122-32 PMID: 9033593
  40. The NMR side-chain assignments and solution structure of enzyme IIBcellobiose of the phosphoenolpyruvate-dependent phosphotransferase system of Escherichia coli.
    Protein Sci. 1997 Feb;6(2):304-14 PMID: 9041631
  41. Solution structure of the 30 kDa N-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system by multidimensional NMR.
    Biochemistry. 1997 Mar 4;36(9):2517-30 PMID: 9054557
  42. 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. 1997 Apr 15;36(15):4393-8 PMID: 9109646
  43. Glucose transporter of Escherichia coli: NMR characterization of the phosphocysteine form of the IIB(Glc) domain and its binding interface with the IIA(Glc) subunit.
    Biochemistry. 1997 Jun 17;36(24):7408-17 PMID: 9200688
  44. The structure of enzyme IIAlactose from Lactococcus lactis reveals a new fold and points to possible interactions of a multicomponent system.
    Structure. 1997 Jun 15;5(6):775-88 PMID: 9261069
  45. High affinity binding and allosteric regulation of Escherichia coli glycogen phosphorylase by the histidine phosphocarrier protein, HPr.
    J Biol Chem. 1997 Oct 17;272(42):26511-21 PMID: 9334229
  46. Phosphorylation on histidine is accompanied by localized structural changes in the phosphocarrier protein, HPr from Bacillus subtilis.
    Protein Sci. 1997 Oct;6(10):2107-19 PMID: 9336834
  47. Structural studies of the Escherichia coli signal transducing protein IIAGlc: implications for target recognition.
    Biochemistry. 1997 Dec 23;36(51):16087-96 PMID: 9405042
  48. Determining the structures of large proteins and protein complexes by NMR.
    Trends Biotechnol. 1998 Jan;16(1):22-34 PMID: 9470228
  49. Direct structure refinement against residual dipolar couplings in the presence of rhombicity of unknown magnitude.
    J Magn Reson. 1998 Mar;131(1):159-62 PMID: 9533920
  50. Crystal structure of the IIB subunit of a fructose permease (IIBLev) from Bacillus subtilis.
    J Mol Biol. 1998 Feb 27;276(3):591-602 PMID: 9551099
  51. The structure of the Escherichia coli phosphotransferase IIAmannitol reveals a novel fold with two conformations of the active site.
    Structure. 1998 Mar 15;6(3):377-88 PMID: 9551558
  52. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra.
    J Magn Reson. 1998 Apr;131(2):373-8 PMID: 9571116
  53. New methods of structure refinement for macromolecular structure determination by NMR.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):5891-8 PMID: 9600889
  54. A robust method for determining the magnitude of the fully asymmetric alignment tensor of oriented macromolecules in the absence of structural information.
    J Magn Reson. 1998 Jul;133(1):216-21 PMID: 9654491
  55. A promiscuous binding surface: crystal structure of the IIA domain of the glucose-specific permease from Mycoplasma capricolum.
    Structure. 1998 Jun 15;6(6):697-710 PMID: 9705652
  56. Solution structure of the 40,000 Mr phosphoryl transfer complex between the N-terminal domain of enzyme I and HPr.
    Nat Struct Biol. 1999 Feb;6(2):166-73 PMID: 10048929
  57. Bicelle-based liquid crystals for NMR-measurement of dipolar couplings at acidic and basic pH values.
    J Biomol NMR. 1999 Feb;13(2):187-91 PMID: 10070759
  58. PHOSPHATE BOUND TO HISTIDINE IN A PROTEIN AS AN INTERMEDIATE IN A NOVEL PHOSPHO-TRANSFERASE SYSTEM.
    Proc Natl Acad Sci U S A. 1964 Oct;52:1067-74 PMID: 14224387
  59. A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams. 1991.
    J Magn Reson. 2011 Dec;213(2):357-63 PMID: 22152355
  60. Stereochemical course of the reactions catalyzed by the bacterial phosphoenolpyruvate:glucose phosphotransferase system.
    Biochemistry. 1982 Oct 26;21(22):5552-6 PMID: 6756472
  61. Sugar transport by the bacterial phosphotransferase system. Preparation of a fluorescein derivative of the glucose-specific phosphocarrier protein IIIGlc and its binding to the phosphocarrier protein HPr.
    J Biol Chem. 1983 Aug 25;258(16):9690-9 PMID: 6411705
  62. Allosteric regulation of glycerol kinase by enzyme IIIglc of the phosphotransferase system in Escherichia coli and Salmonella typhimurium.
    J Bacteriol. 1985 May;162(2):810-6 PMID: 2985549
  63. Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2.
    Protein Eng. 1988 Apr;2(1):27-38 PMID: 2855369
  64. Effect of phosphorylation on hydrogen-bonding interactions of the active site histidine of the phosphocarrier protein HPr of the phosphoenolpyruvate-dependent phosphotransferase system determined by 15N NMR spectroscopy.
    Biochemistry. 1990 Sep 4;29(35):8164-71 PMID: 2261470
  65. Secondary structure of the phosphocarrier protein IIIGlc, a signal-transducing protein from Escherichia coli, determined by heteronuclear three-dimensional NMR spectroscopy.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3479-83 PMID: 2014267
  66. Structures of larger proteins in solution: three- and four-dimensional heteronuclear NMR spectroscopy.
    Science. 1991 Jun 7;252(5011):1390-9 PMID: 2047852
  67. Epitope mapping by mutagenesis distinguishes between the two tertiary structures of the histidine-containing protein HPr.
    Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4877-81 PMID: 1711212
  68. Structure of the IIA domain of the glucose permease of Bacillus subtilis at 2.2-A resolution.
    Biochemistry. 1991 Oct 8;30(40):9583-94 PMID: 1911744
  69. Three-dimensional structure of the Escherichia coli phosphocarrier protein IIIglc.
    Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10382-6 PMID: 1961703
  70. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons.
    Proteins. 1991;11(4):281-96 PMID: 1758883
  71. Structure of the histidine-containing phosphocarrier protein HPr from Bacillus subtilis at 2.0-A resolution.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2499-503 PMID: 1549615
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/19.21.5635
Published
2000-11-01
Pages
5635-49
Language
English
Region
England
NLM ID
8208664
PMCID
PMC305802
Subset
IM
Databases
PDB
1GGR
External Links
PubMed source DOI: 10.1093/emboj/19.21.5635 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2