HPr kinase/phosphorylase, the sensor enzyme of catabolite repression in gram-positive bacteria: Structural aspects of the enzyme and the complex with its protein substrate

Journal of Bacteriology

Volumn 185, Issue 14, 2003, Pages 4003-4010

  Nessler, Sylvie ^a   Fieulaine, Sonia ^a   Poncet, Sandrine ^a   Galinier, Anne ^a   Deutscher, Josef ^a   Janin, Joël ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; HPR KINASE PHOSPHORYLASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CATABOLITE REPRESSION; COMPLEX FORMATION; DEPHOSPHORYLATION; ENZYME ACTIVE SITE; ENZYME STRUCTURE; GRAM POSITIVE BACTERIUM; LACTOBACILLUS CASEI; MYCOPLASMA PNEUMONIAE; NONHUMAN; PHOSPHATE TRANSPORT; PREDICTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; SHORT SURVEY; STAPHYLOCOCCUS XYLOSUS; STRUCTURE ANALYSIS; X RAY ANALYSIS;

BACTERIAL PROTEINS; BINDING SITES; CATALYTIC DOMAIN; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; GRAM-POSITIVE BACTERIA; MODELS, MOLECULAR; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PHOSPHORYLASES; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES;

BACTERIA (MICROORGANISMS); LACTOBACILLUS; LACTOBACILLUS CASEI; MYCOPLASMA; MYCOPLASMA PNEUMONIAE; POSIBACTERIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS XYLOSUS;

EID: 0037478850     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.14.4003-4010.2003     Document Type: Short Survey

References (56)

1. Allen, G. S., K. Steinhauer, W. Hillen, J. Stulke, and R. G. Brennan. 2003. Crystal structure of HPr kinase/phosphatase from Mycoplasma pneumoniae. J. Mol. Biol. 326:1203-1217.
2. Audette, G. F., R. Engelmann, W. Hengstenberg, J. Deutscher, K. Hayakawa, J. W. Quail, and L. T. Delbaere. 2000. The 1.9 Å resolution structure of phospho-serine 46 HPr from Enterococcus faecalis. J. Mol. Biol. 303:545-553.
3. Ben-Zeev, E., A. Berchanski, A. Heifetz, B. Shapira, and M. Eisenstein. 2003. Prediction of the unknown: Inspiring experience with the CAPRI experiment. Proteins 52:41-46.
4. Boël, G., I. Mijakovic, A. Mazé, S. Poncet, M.-K. Taha, M. Larribe, E. Darbon, A. Khemiri, A. Galinier, and J. Deutscher. 2003. Transcriptional regulators potentially controlled by HPr kinase/phosphorylase in gram-negative bacteria. J. Mol. Microbiol. Biotechnol. 5:206-215.
5. Chen, R., W. Tong, J. Mintseris, L. Li, and Z. Weng. 2003. ZDOCK predictions for the CAPRI challenge. Proteins 52:68-73.
6. Deutscher, J., A. Galinier, and I. Martin-Verstraete. 2001. Carbohydrate transporters and regulation of carbohydrate uptake and metabolism, p. 129-150. In A. L. Sonenschein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. American Society for Microbiology, Washington, D.C.
7. Deutscher, J., U. Kessler, and W. Hengstenberg. 1985. Streptococcal phosphoenolpyruvate: sugar phosphotransferase system: purification and characterization of a phosphoprotein phosphatase which hydrolyzes the phosphoryl bond in seryl-phosphorylated histidine-containing protein. J. Bacteriol. 163:1203-1209.
8. Deutscher, J., E. Küster, U. Bergstedt, V. Charrier, and W. Hillen. 1995. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol. Microbiol. 15:1049-1053.
9. Deutscher, J., B. Pevec, K. Beyreuther, H. H. Kiltz, and W. Hengstenberg. 1986. Streptococcal phosphoenolpyruvate-sugar phosphotransferase system: amino acid sequence and site of ATP-dependent phosphorylation of HPr. Biochemistry 25:6543-6551.
10. Deutscher, J., and M. H. Saier, Jr. 1983. ATP-dependent protein kinase-catalyzed phosphorylation of a seryl residue in HPr, a phosphate carrier protein of the phosphotransferase system in Streptococcus pyogenes. Proc. Natl. Acad. Sci. USA 80:6790-6794.
11. Dossonnet, V., V. Monedero, M. Zagorec, A. Galinier, G. Perez-Martinez, and J. Deutscher. 2000. Phosphorylation of HPr by the bifunctional HPr Kinase/P-ser-HPr phosphatase from Lactobacillus casei controls catabolite repression and inducer exclusion but not inducer expulsion. J. Bacteriol. 182:2582-2590.
12. Duclos, B., E. Vaganay, M. Dadssi, and A. J. Cozzone. 1996. Pyrophosphate is a source of phosphoryl groups for Escherichia coli protein phosphorylation. FEMS Microbiol. Lett. 145:49-54.
13. Fernández-Recio, J., M. Totrov, and R. Abagyan. 2003. ICM-DISCO docking by global energy optimization with fully flexible side-chains. Proteins 52:113-117.
14. Fieulaine, S., S. Morera, S. Poncet, I. Mijakovic, A. Galinier, J. Janin, J. Deutscher, and S. Nessier. 2002. X-ray structure of a bifunctional protein kinase in complex with its protein substrate HPr. Proc. Natl. Acad. Sci. USA 99:13437-13441.
15. Fieulaine, S., S. Morera, S. Poncet, V. Monedero, V. Gueguen-Chaignon, A. Galinier, J. Janin, J. Deutscher, and S. Nessler. 2001. X-ray structure of HPr kinase: a bacterial protein kinase with a P-loop nucleotide-binding domain. EMBO J. 20:3917-3927.
16. Fujita, Y., Y. Miwa, A. Galinier, and J. Deutscher. 1995. Specific recognition of the Bacillus subtilis gnt cis-acting catabolite-responsive element by a protein complex formed between CcpA and seryl-phosphorylated HPr. Mol. Microbiol. 17:953-960.
17. Galinier, A., M. Kravanja, R. Engelmann, W. Hengstenberg, M. C. Kilhoffer, J. Deutscher, and J. Haiech. 1998. New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc. Natl. Acad. Sci. USA 95:1823-1828.
18. Galinier, A., J. P. Lavergne, C. Geourjon, S. Fieulaine, S. Nessier, and J. M. Jault. 2002. A new family of phosphotransferases with a P-loop motif. J. Biol. Chem. 277:11362-11367.
19. Gordon, E., B. Flouret, L. Chantalat, J. van Heijenoort, D. Mengin-Lecreulx, and O. Dideberg. 2001. Crystal structure of UDP-N- acetylmuramoyl-L-alanyl-D-glutamate: meso-diaminopimelate ligase from Escherichia coli. J. Biol. Chem. 276:10999-11006.
20. Halperin, I., B. Ma, H. Wolfson, and R. Nussinov. 2002. Principles of docking: an overview of search algorithms and a guide to scoring functions. Proteins 47:409-443.
21. Hanson, K. G., K. Steinhauer, J. Reizer, W. Hillen, and J. Stulke. 2002. HPr kinase/phosphatase of Bacillus subtilis: expression of the gene and effects of mutations on enzyme activity, growth and carbon catabolite repression. Microbiology 148:1805-1811.
22. Henkin, T. M., F. J. Grundy, W. L. Nicholson, and G. H. Chambliss. 1991. Catabolite repression of α-amylase gene expression in Bacillus subtilis involves a trans-acting gene product homologous to the Escherichia coli lacI and galR repressors. Mol. Microbiol. 5:575-584.
23. Hu, K. Y., and M. H. J. Saier. 2002. Phylogeny of phosphoryl transfer proteins of the phosphoenolpyruvate-dependent sugar-transporting phosphotransferase system. Res. Microbiol. 153:405-415.
24. Janin, J. 2002. Welcome to CAPRI: a critical assessment of predicted interactions. Proteins 47:257.
25. Janin, J., K. Henrick, J. Moult, L. Ten Eyck, M. Sternberg, S. Vajda, I. Vakser, and S. J. Wodak. 2003. CAPRI: a critical assessment of predicted interactions. Proteins 52:2-9.
26. Jault, J. M., S. Fieulaine, S. Nessler, P. Gonzalo, A. Di Pietro, J. Deutscher, and A. Galinier. 2000. The HPr kinase from Bacillus subtilis is a homooligomeric enzyme which exhibits strong positive cooperativity for nucleotide and fructose-1,6-bisphosphate binding. J. Biol. Chem. 275:1773-1780.
27. Jones, B. E., V. Dossonet, E. Küster, W. Hillen, J. Deutscher, and R. E. Klevit. 1997. Binding of the catabolite repressor protein CcpA to its DNA target is regulated by phosphorylation of its corepressor HPr. J. Biol. Chem. 272:26530-26535.
28. Kravanja, M., R. Engelmann, V. Dossonnet, M. Blüggel, H. E. Meyer, R. Frank, A. Galinier, J. Deutscher, N. Schnell, and G. Hengstenberg. 1999. The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: the HPr kinase/phosphatase. Mol. Microbiol. 31:59-66.
29. Lander, E. S., L. M. Linton, B. Birren, C. Nusbaum, M. C. Zody, J. Baldwin, K. Devon, K. Dewar, M. Doyle, W. FitzHugh, R. Funke, D. Gage, K. Harris, A. Heaford, J. Howland, L. Kann, J. Lehoczky, R. LeVine, P. McEwan, K. McKernan, J. Meldrim, J. P. Mesirov, C. Miranda, W. Morris, J. Naylor, C. Raymond, M. Rosetti, R. Santos, A. Sheridan, C. Sougnez, N. Stange-Thomann, N. Stojanovic, A. Subramanian, D. Wyman, J. Rogers, J. Suiston, R. Ainscough, S. Beck, D. Bentley, J. Burton, C. Clee, N. Carter, A. Coulson, R. Deadman, P. Deloukas, A. Dunham, I. Dunham, R. Durbin, L. French, D. Grafham, S. Gregory, T. Hubbard, S. Humphray, A. Hunt, M. Jones, C. Lloyd, A. McMurray, L. Matthews, S. Mercer, S. Milne, J. C. Mullikin, A. Mungall, R. Plumb, M. Ross, R. Shownkeen, S. Sims, R. H. Waterston, R. K. Wilson, L. W. Hillier, J. D. McPherson, M. A. Marra, E. R. Mardis, L. A. Fulton, A. T. Chinwalla, K. H. Pepin, W. R. Gish, S. L. Chissoe, M. C. Wendl, K. D. Delehaunty, T. L. Miner, A. Delehaunty, J. B. Kramer, L. L. Cook, R. S. Fulton, D. L. Johnson, P. J. Minx, S. W. Clifton, T. Hawkins, E. Branscomb, P. Predki, P. Richardson, S. Wenning, T. Slezak, N. Doggett, J. F. Cheng, A. Olsen, S. Lucas, C. Elkin, E. Uberbacher, M. Frazier, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
30. Lavergne, J. P., J. M. Jault, and A. Galinier. 2002. Insights into the functioning of Bacillus subtilis HPr kinase/phosphatase: affinity for its protein substrates and role of cations and phosphate. Biochemistry 41:6218-6225.
31. Liao, D. I., and O. Herzberg. 1994. Refined structures of the active Ser83→Cys and impaired Ser46→Asp histidine-containing phosphocarrier proteins. Structure 2:1203-1216.
32. Marquez, J. A., S. Hasenbein, B. Koch, S. Fieulaine, S. Nessler, R. B. Russell, W. Hengstenberg, and K. Scheffzek. 2002. Structure of the full-length HPr kinase/phosphatase from Staphylococcus xylosus at 1.95 A resolution: Mimicking the product/substrate of the phospho transfer reactions. Proc. Natl. Acad. Sci. USA 99:3458-3463.
33. Matte, A., H. Goldie, R. M. Sweet, and L. T. Delbaere. 1996. Crystal structure of Escherichia coli phosphoenolpyruvate carboxy-kinase: a new structural family with the P-loop nucleoside triphosphate hydrolase fold. J. Mol. Biol. 256:126-143.
34. Mendez, R., R. Leplae, L. de Maria, and S. J. Wodak. 2003. Assessment of blind predictions of protein-protein interactions: current status of docking methods. Proteins 52:51-67.
35. Mijakovic, I., S. Poncet, A. Galinier, V. Monedero, S. Fieulaine, J. Janin, S. Nessler, J. A. Marquez, K. Scheffzek, S. Hasenbein, W. Hengstenberg, and J. Deutscher. 2002. Pyrophosphate-producing protein dephosphorylation by HPr kinase/phosphorylase: a relic of early life? Proc. Natl. Acad. Sci. USA 99:13442-13447.
36. Miwa, Y., A. Nakata, A. Ogiwara, M. Yamamoto, and Y. Fujita. 2000. Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. Nucleic Acids Res. 28:1206-1210.
37. Monedero, V., O. P. Kuipers, E. Jamet, and J. Deutscher. 2001. Regulatory functions of serine-46-phosphorylated HPr in Lactococcus lactis. J. Bacteriol. 183:3391-3398.
38. Monedero, V., S. Poncet, I. Mijakovic, S. Fieulaine, V. Dossonnet, I. Martin-Verstraete, S. Nessler, and J. Deutscher. 2001. Mutations lowering the phosphatase activity of HPr kinase/phosphatase switch off carbon metabolism. EMBO J. 20:3928-3937.
39. Moreno, M. S., B. L. Schneider, R. R. Maile, W. Weyler, and M. H. Saier. 2001. Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol. Microbiol. 39:1366-1381.
40. Murzin, A. G., S. E. Brenner, T. Hubbard, and C. Chothia. 1995. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247:536-540.
41. Postma, P. W., J. W. Lengeler, and G. R. Jacobson. 1993. Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57:543-594.
42. Ramström, H., S. Sanglier, E. Leize-Wagner, C. Philippe, A. Van Dorsselaer, and J. Haiech. 2003. Properties and regulation of the bifunctional enzyme HPr kinase/phosphatase in Bacillus subtilis. J. Biol. Chem. 278:1174-1185.
43. Reizer, J., C. Hoischen, F. Titgemeyer, C. Rivolta, R. Rabus, J. Stulke, D. Karamata, M. H. Saier, and W. Hillen. 1998. A novel protein kinase that controls carbon catabolite repression in bacteria. Mol. Microbiol. 27:1157-1169.
44. Russell, R. B., J. A. Marquez, W. Hengstenberg, and K. Scheffzek. 2002. Evolutionary relationship between the bacterial HPr kinase and the ubiquitous PEP-carboxykinase: expanding the P-loop nucleotidyl transferase superfamily. FEBS Lett. 517:1-6.
45. Saraste, M., P. R. Sibbald, and A. Wittinghofer. 1990. The P-loop-a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci. 15:430-434.
46. Schneidman-Duhovny, D., Y. Inbar, V. Polak, M. Shatsky, I. Halperin, H. Benyamini, A. Barzilai, O. Dror, N. Haspel, R. Nussinov, and H. J. Wolfson. 2003. Taking geometry to its edge: fast unbound rigid (and hinge-bent) docking. Proteins 52:107-112.
47. Steinhauer, K., T. Jepp, W. Hillen, and J. Stulke. 2002. A novel mode of control of Mycoplasma pneumoniae HPr kinase/phosphatase activity reflects its parasitic lifestyle. Microbiology 148:3277-3284.
48. Sudom, A. M., L. Prasad, H. Goldie, and L. T. Delbaere. 2001. The phosphoryl-transfer mechanism of Escherichia coli phosphoenolpyruvate carboxykinase from the use of AIF(3). J. Mol. Biol. 314:83-92.
49. 2+ clusters in enzyme-catalyzed phosphoryl-transfer reactions. Nat Struct. Biol. 4:990-994.
50. 2+-oxalate ternary complex of Escherichia coli PEP carboxykinase. Nat. Struct. Biol. 3:355-363.
51. Valencia, A., and F. Pazos. 2002. Computational methods for the prediction of protein interactions. Curr. Opin. Struct. Biol. 12:368-373.
52. Vonrhein, C., H. Bönisch, G. Schäfer, and G. E. Schulz. 1998. The structure of a trimeric archaeal adenylate kinase. J. Mol. Biol. 282:167-179.
53. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982. Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
54. Wittekind, M., J. Reizer, J. Deutscher, M. H. Saier, and R. E. Klevit. 1989. Common structural changes accompany the functional inactivation of HPr by seryl phosphorylation or by serine to aspartate substitution. Biochemistry 28:9908-9912.
55. Wodak, S. J., and J. Janin, 2002. Structural basis of macromolecular recognition. Adv. Protein Chem. 61:9-73.
56. Zhu, P. P., O. Herzberg, and A. Peterkofsky. 1998. Topography of the interaction of HPr(Ser) kinase with HPr. Biochemistry 37:11762-11770.