Carbon catabolite repression of the maltose transporter revealed by X-ray crystallography

Nature

Volumn 499, Issue 7458, 2013, Pages 364-368

  Chen, Shanshuang ^a   Oldham, Michael L ^b   Davidson, Amy L ^c   Chen, Jue ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b Med Institute Inc Lafayette   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATASE; BACTERIAL ENZYME; CARBON; ENZYME IIA; MALTOSE; PROTEIN KINASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

CARBON; CATABOLISM; CONCENTRATION (COMPOSITION); CRYSTAL STRUCTURE; CYTOPLASM; DATA ACQUISITION; ENZYME ACTIVITY; GLUCOSE; GROWTH RATE; HYDROLYSIS; MEMBRANE; MICROBIAL ACTIVITY; MOLECULAR ANALYSIS; NUTRIENT UPTAKE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBON UTILIZATION; CATABOLITE REPRESSION; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN HYDROLYSIS; X RAY CRYSTALLOGRAPHY;

ATP-BINDING CASSETTE TRANSPORTERS; CARBON; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI;

EID: 84880511070     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12232     Document Type: Article

References (41)

1. Görke, B.& Stülke, J. Carbon catabolite repression in bacteria:many ways tomake the most out of nutrients. Nature Rev. Microbiol. 6, 613-624 (2008).
2. Deutscher, J., Francke, C.&Postma, P. W.Howphosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70, 939-1031 (2006).
3. Wang, G., Peterkofsky, A. & Clore, G. M. A novel membrane anchor function for the N-terminal amphipathic sequence of the signal-transducing protein IIAGlucose of the Escherichia coli phosphotransferase system. J. Biol. Chem. 275, 39811-39814 (2000).
4. Wang, G., Keifer, P. A. & Peterkofsky, A. Solution structure of the N-terminal amphitropic domain of Escherichia coli glucose-specific enzymeIIA inmembranemimetic micelles. Protein Sci. 12, 1087-1096 (2003).
5. Hogema, B. M. et al. Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of enzyme IIAGlc. Mol. Microbiol. 30, 487-498 (1998).
6. Khare, D., Oldham, M. L., Orelle, C., Davidson, A. L. & Chen, J. Alternating access in maltose transporter mediated by rigid-body rotations. Mol. Cell 33, 528-536 (2009).
7. Oldham, M. L., Khare, D., Quiocho, F. A., Davidson, A. L. & Chen, J. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450, 515-521 (2007).
8. Oldham, M. L. & Chen, J. Crystal structure of the maltose transporter in a pretranslocation intermediate state. Science 332, 1202-1205 (2011).
9. Monod, J., Wyman, J. & Changeux, J. P. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118 (1965).
10. Chen, J., Lu, G., Lin, J., Davidson, A. L. & Quiocho, F. A. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol. Cell 12, 651-661 (2003).
11. Dean, D. A., Reizer, J., Nikaido, H. & Saier, M. H. Jr. Regulation of the maltose transport system of Escherichia coli by the glucose-specific enzyme III of the phosphoenolpyruvate-sugar phosphotransferase system. Characterization of inducer exclusion-resistant mutants and reconstitution of inducer exclusion in proteoliposomes. J. Biol. Chem. 265, 21005-21010 (1990).
12. Kühnau, S., Reyes, M., Sievertsen, A., Shuman, H. A. & Boos, W. The activities of the Escherichia coli MalK protein in maltose transport, regulation, and inducer exclusion can be separated by mutations. J. Bacteriol. 173, 2180-2186 (1991).
13. Worthylake, D. et al. Three-dimensional structure of the Escherichia coli phosphocarrier protein IIIglc. Proc. Natl Acad. Sci. USA 88, 10382-10386 (1991).
14. Cai, M. et al. Solution structure of the phosphoryl transfer complex between the signal-transducing protein IIAGlucose and the cytoplasmic domain of the glucose transporter IICBGlucose of the Escherichia coli glucose phosphotransferase system. J. Biol. Chem. 278, 25191-25206 (2003).
15. Hurley, J. H. et al. Structure of the regulatory complex of Escherichia coli IIIGlc with glycerol kinase. Science 259, 673-677 (1993).
16. Wang, G. et al. Solution structure of the phosphoryl transfer complex between the signal transducing proteins HPr and IIAglucose of the Escherichia coli phosphoenolpyruvate:sugar phosphotransferase system. EMBO J. 19, 5635-5649 (2000).
17. Pelton, J. G., Torchia, D. A., Meadow, N. D. & Roseman, S. Structural comparison of phosphorylated and unphosphorylated forms of IIIGlc, a signal-transducing protein from Escherichia coli, using three-dimensional NMR techniques. Biochemistry 31, 5215-5224 (1992).
18. Dörschug, M., Frank, R., Kalbitzer, H. R., Hengstenberg, W. & Deutscher, J. Phosphoenolpyruvate-dependent phosphorylation site in enzyme IIIglc of the Escherichia coli phosphotransferase system. Eur. J. Biochem. 144, 113-119 (1984).
19. Blschke, B., Volkmer-Engert, R. & Schneider, E. Topography of the surface of the signal-transducing protein EIIAGlc that interacts with the MalK subunits of the maltose ATP-binding cassette transporter (MalFGK2) of Salmonella typhimurium. J. Biol. Chem. 281, 12833-12840 (2006).
20. Stein, A. et al. Functional characterization of the maltose ATP-binding-cassette transporter of Salmonella typhimurium by means of monoclonal antibodies directed against the MalK subunit. Eur. J. Biochem. 269, 4074-4085 (2002).
21. Meadow, N. D.&Roseman, S.Sugar transport by the bacterial phosphotransferase system. Isolation and characterization of a glucose-specific phosphocarrier protein (IIIGlc) fromSalmonella typhimurium. J. Biol. Chem. 257, 14526-14537 (1982).
22. Meadow, N. D., Savtchenko, R. S., Remington, S. J. & Roseman, S. Effects of mutations and truncations on the kinetic behavior of IIAGlc, a phosphocarrier and regulatory protein of the phosphoenolpyruvate phosphotransferase system of Escherichia coli. J. Biol. Chem. 281, 11450-11455 (2006).
23. Misko, T. P., Mitchell, W. J., Meadow, N. D. & Roseman, S. Sugar transport by the bacterial phosphotransferase system. Reconstitution of inducer exclusion in Salmonella typhimurium membrane vesicles. J. Biol. Chem. 262, 16261-16266 (1987).
24. van der Vlag, J., van Dam, K. & Postma, P. W. Quantification of the regulation of glycerol and maltose metabolism by IIAGlc of the phosphoenolpyruvatedependent glucose phosphotransferase system in Salmonella typhimurium. J. Bacteriol. 176, 3518-3526 (1994).
25. Scholte, B. J., Schuitema, A. R. & Postma, P. W. Isolation of IIIGlc of the phosphoenolpyruvate-dependent glucose phosphotransferase system of Salmonella typhimurium. J. Bacteriol. 148, 257-264 (1981).
26. Kadaba, N. S., Kaiser, J. T., Johnson, E., Lee, A. & Rees, D. C. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321, 250-253 (2008).
27. Gerber, S., Comellas-Bigler, M., Goetz, B. A.&Locher, K. P. Structural basis of transinhibition in a molybdate/tungstate ABC transporter. Science 321, 246-250 (2008).
28. Osumi, T.&Saier, M. H. Jr.Mechanismof regulation of the lactose permease by the phosphotransferase system in Escherichia coli: evidence for protein-protein interaction. Ann. Microbiol. 133, 269-273 (1982).
29. Osumi, T. & Saier, M. H. Jr. Regulation of lactose permease activity by the phosphoenolpyruvate:sugar phosphotransferase system: evidence for direct binding of the glucose-specific enzymeIII to the lactose permease. Proc. Natl Acad. Sci. USA 79, 1457-1461 (1982).
30. Saier, M. H. Jr, Novotny, M. J., Comeau-Fuhrman, D., Osumi, T. & Desai, J. D. Cooperative binding of the sugar substrates and allosteric regulatory protein (enzyme IIIGlc of the phosphotransferase system) to the lactose and melibiose permeases in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 155, 1351-1357 (1983).
31. Ujwal, S. & Bowie, J. U. Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J. Mol. Biol. 316, 1-6 (2002).
32. Ujwal, R. & Abramson, J. High-throughput crystallization of membrane proteins using the lipidic bicelle method. J. Vis. Exp. 59, e3383 (2012).
33. Rossmann, M. G. The molecular replacement method. Acta Crystallogr. A 46, 73-82 (1990).
34. Collaborative Computational Project, number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
35. Schröder, G. F., Levitt, M. & Brunger, A. T. Super-resolution biomolecular crystallography with low-resolution data. Nature 464, 1218-1222 (2010).
36. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
38. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
39. Alvarez, F. J., Orelle, C. & Davidson, A. L. Functional reconstitution of an ABC transporter in nanodiscs for use in electron paramagnetic resonance spectroscopy. J. Am. Chem. Soc. 132, 9513-9515 (2010).
40. Scharschmidt, B. F., Keeffe, E. B., Blankenship, N. M. & Ockner, R. K. Validation of a recording spectrophotometric method for measurement of membraneassociated Mg- and NaK-ATPase activity. J. Lab. Clin. Med. 93, 790-799 (1979).
41. Orelle, C., Ayvaz, T., Everly, R. M., Klug, C. S. & Davidson, A. L. Both maltose-binding protein and ATP are required for nucleotide-binding domain closure in the intact maltose ABC transporter. Proc. Natl Acad. Sci. USA 105, 12837-12842 (2008).