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

Journal of Bacteriology

Volumn 182, Issue 9, 2000, Pages 2582-2590

  Dossonnet, Valérie ^a   Monedero, Vicente ^a   Zagorec, Monique ^b   Galinier, Anne ^c   Pérez Martînez, Caspar ^d   Deutscher, Josef ^a,e  

^a Lab de Genet des Microorganismes   (France)

^b Lab de Recherche Sur la Viande   (France)

^c INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^d INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATASE; PHOSPHOENOLYPYRUVATE; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CATABOLITE REPRESSION; ENZYME BINDING; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME PURIFICATION; LACTOBACILLUS CASEI; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATOR GENE; STRAIN DIFFERENCE;

ACETYLGLUCOSAMINIDASE; BACTERIAL PROTEINS; BASE SEQUENCE; CLONING, MOLECULAR; DNA, BACTERIAL; DNA-BINDING PROTEINS; GLUCOSE; LACTOBACILLUS CASEI; MALTOSE; METHYLGALACTOSIDES; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOSPHATES; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; RESPONSE ELEMENTS; THIOGALACTOSIDES; TRANSFERASES;

BACTERIA (MICROORGANISMS); LACTOBACILLUS CASEI; POSIBACTERIA; PROKARYOTA;

EID: 0033996770     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.182.9.2582-2590.2000     Document Type: Article

References (59)

1. Bettenbrock, K., U. Siebers, P. Ehrenreich, and C.-A. Alpert. 1999. Lactobacillus casei 64H contains a phosphoenolpyruvate-dependent phosphotransferase system for uptake of galactose, as confirmed by analysis of ptsH and different gal mutants. J. Bacteriol. 181:225-230.
2. Brochu, D., and C. Vadeboncoeur. 1999. The HPr(Ser) kinase of Streptococcus salivarius: purification, properties, and cloning of the hprK gene. J. Bacteriol. 181:709-717.
3. Chassy, B. M., and J. Thompson. 1983. Regulation of lactose-phosphoenol-pyruvate-dependent phosphotransferase system and β-D-phosphogalactoside galactohydrolase activities in Lactobacillus casei. J. Bacteriol. 154:1195-1203.
4. 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.
5. Deutscher, J., B. Pevec, K. Beyreulher, 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.
6. Deutscher, J., J. Reizer, C. Fischer, A. Galinier, M. H. Saier, Jr., and M. Steinmetz. 1994. Loss of protein kinase-catalyzed phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, by mutation of the ptsH gene confers catabolite repression resistance to several catabolic genes of Bacillus subtilis. J. Bacteriol. 176:3336-3344.
7. 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.
8. Eisermann, R., J. Deutscher, G. Gonzy-Tréboul, and W. Hengstenberg. 1988. Site-directed mutagenesis with the ptsH gene of Bacillus subtilis. Isolation and characterization of heat-stable proteins altered at the ATP-dependent regulatory phosphorylation site. J. Biol. Chem. 263:17050-17054.
9. Faires, N., S. Tobisch, S. Bachem, I. Martin-Verstraete, M. Hecker, and J. Stülke. 1999. The catabolite control protein CcpA controls ammonium assimilation in Bacillus subtilis. J. Mol. Microbiol. Biotechnol. 1:141-148.
10. 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.
11. Galinier, A., J. Deutscher, and I. Martin-Verstraete. 1999 Phosphorylation of either Crh or HPr mediates catabolite repression and binding of CcpA to the cre of the Bacillus subtilis xyn operon. J. Mol. Biol. 286:307-314.
12. Galinier, A., J. Haiech, M.-C. Kilhoffer, M. Jaquinod, J. Stülke, J. Deutscher, and I. Martin-Verstraete. 1997. The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression. Proc. Natl. Acad. Sci. USA 94:8439-8444.
13. 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.
14. Gösseringer, R., E. Küster, A. Galinier, J. Deutscher, and W. Hillen. 1997. Cooperative and non-cooperative DNA binding modes of catabolite control protein CcpA from Bacillus megaterium result from sensing two different signals. J. Mol. Biol. 266:665-676.
15. Gunnewijk, M. G. W., P. W. Postma, and B. Poolman. 1999. Phosphorylation and functional properties of the IIA domain of the lactose transport protein of Streptococcus thermophilus. J. Bacteriol. 181:632-641.
16. Hausman, S. Z., J. Thompson, and J. London. 1984. Futile xylitol cycle in Lactobacillus casei. J. Bacteriol. 160:211-215.
17. 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.
18. Hueck, C. J., W. Hillen, and M. H. Saier, Jr. 1994. Analysis of a cis-active sequence mediating catabolite repression in Gram-positive bacteria. Res. Microbiol. 145:503-518.
19. Jault, J. M., S. Fieulaine, S. Nessler-Baudet, P. Gonzalo, J. Deutscher, A. Di Pietro, and A. Galinier. 2000. The HPr kinase from Bacillus subtilis is a homo-oligomeric enzyme which exhibits strong positive cooperatively for nucleotide and fructose 1,6-bisphosphate binding. J. Biol. Chem. 275:2009-2016.
20. Jones, B. E., V. Dossonnet, 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.
21. Kim, J.-H., M. I. Voskuil, and G. H. Chambliss. 1998. NADP, corepressor for the Bacillus catabolite control protein CcpA. Proc. Natl. Acad. Sci. USA 95:9590-9595.
22. Kravanja, M., R. Engelmann, V. Dossonnet, M. Blüggel, H. E. Meyer, R. Frank, A. Galinier, J. Deutscher, N. Schnell, and W. Hengstenberg. 1999. The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: the HPr kinase/phosphatase. Mol. Microbiol. 31:59-66.
23. Kunst, F., N. Ogasawara, I. Moszer, A. M. Albertini, G. Alloni, V. Azevedo, et al. 1997. The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390:249-256.
24. Küster, E., E. J. Luesink, W. M. de Vos, and W. Hillen. 1996 Immunological crossreactivity to the catabolite control protein CcpA from Bacillus megaterium is found in many Gram-positive bacteria. FEMS Microbiol. Lett. 139: 109-115.
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Leloup, L., S. D. Ehrlich, M. Zagorec, and F. Morel-Deville. 1997. Single-crossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsl and lacL. genes. Appl. Environ. Microbiol. 63:2117-2123.
27. Luesink, E. J., M. A. Beumer, O. P. Kuipers, and W. M. de Vos. 1999. Molecular characterization of the Lactococcus lactis ptsHI operon and analysis of the regulatory role of HPr. J. Bacteriol. 181:764-771.
28. Luesink, E. J., R. E. M. A. van Harpen, B. P. Grossiord, O. P. Kuipers, and W. M. de Vos. 1998. Transcriptional activation of the glycolytic las operon and catabolite repression of the gal operon in Lactococcus lactis are mediated by the catabolite control protein CcpA. Mol. Microbiol. 30:789-798.
29. Martin-Verstraete, I., J. Deutscher, and A. Galinier. 1999. Phosphorylation of HPr and Crh by HprK, early steps in the catabolite repression signalling pathway for the Bacillus subtilis levanase operon. J. Bacteriol. 181:2966-2969.
30. Martin-Verstraete, I., A. Galinier, E. Darbon, V. Quentin, V. Charrier, M.-C. Kilhoffer, J. Haiech, G. Rapoport, and J. Deutscher. 1999. The Q15H mutation enables Crh, a Bacillus subtilis HPr-like protein, to carry out some regulatory HPr functions, but does not make it an effective phosphocarrier for sugar transport. Microbiology 145:3195-3204.
31. Monedero, V. 1997. Elements implicated in catabolite repression in Lactobacillus casei. Ph.D. thesis. Universitat de València, Spain.
32. Monedero, V., M. J. Gosalbes, and G. Perez-Martinez. 1997. Catabolite repression in Lactobacillus casei ATCC 393 is mediated by CcpA. J. Bacteriol. 179:6657-6664.
33. Nicholson, W. L., and G. H. Chambliss. 1985. Isolation and characterization of a cis-acting mutation conferring catabolite repression resistance to α-amylase synthesis in Bacillus subtilis. J. Bacteriol. 161:875-881.
34. Posno, M., R. J. Leer, N. van Luijk, M. J. F. van Giezen, P. T. H. M. Heuvelmans, B. C. Lokman, and P. H. Pouwels. 1991. Incompatibility of Lactohacillus vectors with replicons derived from small cryptic Lactobacillus plasmids and segregational instability of the introduced vectors. Appl. Environ. Microbiol. 57:1822-1828.
35. Postma, P. W., J. W. Lengeler, and G. R. Jacobson. 1993. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57:543-594.
36. Presecan-Siedel, E., A. Galinier, R. Longin, J. Deutscher, A. Danchin, P. Glaser, and I. Martin-Verstraete. 1999. The catabolite regulation of the pta gene as part of the carbon flow pathways in Bacillus subtilis. J. Bacteriol. 181:6889-6897.
37. Qi, H.-Y., K. Sankaran, K. Gan, and H. C. Wu. 1995 Structure-function relationship of bacterial prolipoprotein diacylglyceryl transferase: functionally significant conserved regions. J. Bacteriol. 177:6820-6824.
38. Reizer, J., C. Hoischen, F. Titgemeyer, C. Rivolta, R. Rabus, J. Stülke, D. Karamata, M. H. Saier, Jr., and W. Hillen. 1998. A novel protein kinase that controls carbon catabolite repression in bacteria. Mol. Microbiol. 27:1157-1169.
39. Reizer, J., M. J. Novotny, W. Hengstenberg, and M. H. Saier, Jr. 1984. Properties of ATP-dependent protein kinase from Streptococcus pyogenes that phosphorylates a seryl residue in HPr, a phosphocarrier protein of the phosphotransferase system. J. Bacteriol. 160:333-340.
40. Reizer, J., M. J. Novotny, C. Panos, and M. H. Saier, Jr. 1983. Mechanism of inducer expulsion in Streptococcus pyogenes: a two-step process activated by ATP. J. Bacteriol. 156:354-361.
41. Reizer, J., and C. Panos. 1980. Regulation of β-galactoside phosphate accumulation in Streptococcus pyogenes by an expulsion mechanism. Proc. Natl. Acad. Sci. USA 77:5497-5501.
42. Reizer, J., A. Reizer, M. H. Saier, Jr., and G. R. Jacobson. 1992. A proposed link between nitrogen and carbon metabolism involving protein phosphorylation in bacteria. Protein Sci. 1:722-726.
43. Saier, M. H., Jr., S. Chauvaux, J. Deutscher, J. Reizer, and J.-J. Ye. 1995. Protein phosphorylation and regulation of carbon metabolism in Gram-negative versus Gram-positive bacteria. Trends Biochem. Sci. 20:267-271.
44. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
45. Schön, U., and W. Schumann. 1994. Construction of His6-tagging vectors allowing single-step purification of GroES and other polypeptides produced in Bacillus subtilis. Gene 147:91-94.
46. Thompson, J., and M. H. Saier, Jr. 1981. Regulation of thiomethylgalactoside 6-phosphate accumulation in Streptococcus lactis by exclusion and expulsion mechanisms. J. Bacteriol. 146:885-894.
47. Tobisch, S., D. Zühlke, J. Bernhardt, J. Stülke, and M. Hecker. 1999. Role of CcpA in regulation of the central pathways of carbon catabolism in Bacillus subtilis. J. Bacteriol. 181:6996-7004.
48. Toy, J., and A. L. Bognar. 1990. Cloning and expression of the gene encoding Lactobacillus casei folylpoly-y-glutamate synthetase in Escherichia coli and determination of its primary structure. J. Biol. Chem. 265:2492-2499.
49. Turinsky, A. J., F. J. Grundy, J.-H. Kim, G. H. Chambliss, and T. M. Henkin. 1998. Transcriptional activation of the Bacillus subtilis ackA gene requires sequences upstream of the promoter. J. Bacteriol. 180:5961-5967.
50. Veyrat, A., V. Monedero, and G. Perez-Martinez. 1994. Glucose transport by the phosphoenolpyruvate:mannose phosphotransferase system in Lactobacillus casei ATCC 393 and its role in carbon catabolite repression. Microbiology 140:1141-1149.
51. Viana, R., V. Monedero, V. Dossonnet, C. Vadeboncoeur, G. Perez-Martinez, and J. Deutscher. Enzyme I and HPr from Lactobacillus casei: their role in sugar transport, carbon catabolite repression and inducer exclusion. Mol. Microbiol., in press.
52. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982. Distantly related sequences in the alpha-and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
53. Wittekind, M., J. Reizer, J. Deutscher, M. H. Saier, Jr., 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.
54. Ye, J.-J., J. Minarcyk, and M. H. Saier, Jr. 1996. Inducer expulsion and the occurrence of an HPr(Ser-P)-activated sugar-phosphate phosphatase in Enterococcus faecalis and Streptococcus pyogenes. Microbiology 142:585-592.
55. Ye, J.-J., J. Reizer, X. Cui, and M. H. Saier, Jr. 1994. Inhibition of the phosphoenolpyruvate:lactose phosphotransferase system and activation of a cytoplasmic sugar-phosphate phosphatase in Lactococcus lactis by ATP-dependent metabolite-activated phosphorylation of serine 46 in the phosphocarrier protein HPr. J. Biol. Chem. 269:11837-11844.
56. + symporter of Lactobacillus brevis: cooperative binding of glucose and HPr(ser-P). J. Bacteriol. 177:1900-1902.
57. + symport permease of Lactobacillus brevis. Proc. Natl. Acad. Sci. USA 92:417-421.
58. Ye, J.-J., and M. H. Saier, Jr. 1995. Purification and characterization of a small membrane-associated sugar phosphate phosphatase that is allosterically activated by HPr(Ser-P) of the phosphotransferase system in Lactococcus lactis. J. Biol. Chem. 270:16740-16744.
59. Zalieckas, J. M., L. V. Wray, Jr., and S. H. Fisher. 1999. trans-acting factors affecting carbon catabolite repression of the hut operon in Bacillus subtilis. J. Bacteriol. 181:2883-2888.