Molecular basis of ChvE function in sugar binding, sugar utilization, and virulence in Agrobacterium tumefaciens

Journal of Bacteriology

Volumn 191, Issue 18, 2009, Pages 5802-5813

  He, Fanglian ^a,b   Nair, Gauri R ^a,c   Soto, Cinque S ^a   Chang, Yehchung ^a,d   Hsu, Lillian ^a,e   Ronzone, Erik ^a   DeGrado, William F ^a   Binns, Andrew N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Bldg 142   (United States)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; CHEA KINASE; CHROMOSOME PROTEIN; CHVE PROTEIN; GALACTOSE; GALAPTIN; GLUCOSE; RIBOSE; SUGAR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONFORMATIONAL TRANSITION; CYTOPLASM; ESCHERICHIA COLI; FLUORESCENCE SPECTROSCOPY; GENE EXPRESSION; GENE MUTATION; GLUCOSE UTILIZATION; IMMUNOBLOTTING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RHIZOBIUM RADIOBACTER; SEQUENCE HOMOLOGY; SUGAR TRANSPORT;

ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; MODELS, MOLECULAR; MUTATION; PERIPLASMIC BINDING PROTEINS; RHIZOBIUM RADIOBACTER; VIRULENCE;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; VIR; VIRUSES;

EID: 69949097598     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00451-09     Document Type: Article

References (54)

1. Andujar-Sanchez, M., V. Jara-Perez, and A. Camara-Artigas. 2007. Thermodynamic determination of the binding constants of angiotensin-converting enzyme inhibitors by a displacement method. FEBS Lett. 581:3449-3454. (Pubitemid 47048191)
2. Ankenbauer, R. G., and E. W. Nester. 1990. Sugar-mediated induction of Agrobacterium tumefaciens virulence genes: structural specificity and activities of monosaccharides. J. Bacteriol. 172:6442-6446.
3. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
4. Berger, B. R., and P. J. Christie. 1993. The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J. Bacteriol. 175:1723-1734.
5. Binnie, R. A., H. Zhang, S. Mowbray, and M. A. Hermodson. 1992. Functional mapping of the surface of Escherichia coli ribose-binding protein: mutations that affect chemotaxis and transport. Protein Sci. 1:1642-1651.
6. Brencic, A., and S. C. Winans. 2005. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69:155-194.
7. Cangelosi, G. A., R. G. Ankenbauer, and E. W. Nester. 1990. Sugars induce the Agrobacterium virulence genes through a periplasmic binding protein and a transmembrane signal protein. Proc. Natl. Acad. Sci. USA 87:6708-6712.
8. Chang, C. H., and S. C. Winans. 1992. Functional roles assigned to the periplasmic, linker, and receiver domains of the Agrobacterium tumefaciens VirA protein. J. Bacteriol. 174:7033-7039.
9. Chilton, M. D., T. C. Currier, S. K. Farrand, A. J. Bendich, M. P. Gordon, and E. W. Nester. 1974. Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc. Natl. Acad. Sci. USA 71:3672-3676.
10. D'Auria, S., A. Ausili, A. Marabotti, A. Varriale, V. Scognamiglio, M. Staiano, E. Bertoli, M. Rossi, and F. Tanfani. 2006. Binding of glucose to the D-galactose/D-glucose-binding protein from Escherichia coli restores the native protein secondary structure and thermostability that are lost upon calcium depletion. J. Biochem. 139:213-221.
11. Doty, S. L., M. C. Yu, J. I. Lundin, J. D. Heath, and E. W. Nester. 1996. Mutational analysis of the input domain of the VirA protein of Agrobacterium tumefaciens. J. Bacteriol. 178:961-970.
12. Dwyer, M. A., and H. W. Hellinga. 2004. Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr. Opin. Struct. Biol. 14:495-504.
13. Eftink, M. R., and C. A. Ghiron. 1976. Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies. Biochemistry 15:672-680.
14. Eftink, M. R., and C. A. Ghiron. 1981. Fluorescence quenching studies with proteins. Anal. Biochem. 114:199-227.
15. Eym, Y., Y. Park, and C. Park. 1996. Genetically probing the regions of ribose-binding protein involved in permease interaction. Mol. Microbiol. 21:695-702.
16. Gao, R., and D. G. Lynn. 2005. Environmental pH sensing: resolving the VirA/VirG two-component system inputs for Agrobacterium pathogenesis. J. Bacteriol. 187:2182-2189.
17. Garfinkel, D. J., and E. W. Nester. 1980. Agrobacterium tumefaciens mutants affected in crown gall tumorigenesis and octopine catabolism. J. Bacteriol. 144:732-743.
18. Huang, M. L., G. A. Cangelosi, W. Halperin, and E. W. Nester. 1990. A chromosomal Agrobacterium tumefaciens gene required for effective plant signal transduction. J. Bacteriol. 172:1814-1822.
19. Jin, S., T. Roitsch, R. G. Ankenbauer, M. P. Gordon, and E. W. Nester. 1990. The VirA protein of Agrobacterium tumefaciens is autophosphorylated and is essential for vir gene regulation. J. Bacteriol. 172:525-530. (Pubitemid 20070357)
20. Kemner, J. M., X. Liang, and E. W. Nester. 1997. The Agrobacterium tumefaciens virulence gene chvE is part of a putative ABC-type sugar transport operon. J. Bacteriol. 179:2452-2458.
21. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-hostrange cloning vector pBBR1MCS, carrying different antibiotic- resistance cassettes. Gene 166:175-176.
22. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
23. Lakowicz, J. R. 1999. Principles of fluorescence spectroscopy. Plenum Press, New York, NY.
24. Leroux, B., M. F. Yanofsky, S. C. Winans, J. E. Ward, S. F. Ziegler, and E. W. Nester. 1987. Characterization of the virA locus of Agrobacterium tumefaciens: a transcriptional regulator and host range determinant. EMBO J. 6:849-856.
25. Martineau, P., W. Saurin, M. Hofnung, J. C. Spurlino, and F. A. Quiocho. 1990. Progress in the identification of interaction sites on the periplasmic maltose binding protein from E coli. Biochimie 72:397-402. (Pubitemid 20335935)
26. McCullen, C. A., and A. N. Binns. 2006. Agrobacterium tumefaciens and plant cell interactions and activities required for interkingdom macromolecular transfer. Annu. Rev. Cell Dev. Biol. 22:101-127.
27. McGowan, E. B., T. J. Silhavy, and W. Boos. 1974. Involvement of a tryptophan residue in the binding site of Escherichia coli galactose-binding protein. Biochemistry 13:993-999.
28. Miller, D. M., III, J. S. Olson, J. W. Pflugrath, and F. A. Quiocho. 1983. Rates of ligand binding to periplasmic proteins involved in bacterial transport and chemotaxis. J. Biol. Chem. 258:13665-13672.
29. Miller, D. M., III, J. S. Olson, and F. A. Quiocho. 1980. The mechanism of sugar binding to the periplasmic receptor for galactose chemotaxis and transport in Escherichia coli. J. Biol. Chem. 255:2465-2471.
30. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Mukhopadhyay, A., R. Gao, and D. G. Lynn. 2004. Integrating input from multiple signals: the VirA/VirG two-component system of Agrobacterium tumefaciens. ChemBioChem 5:1535-1542.
32. Nair, G. R. 2006. Novel insights into vir gene regulation in Agrobacterium tumefaciens. Ph.D. thesis. University of Pennsylvania, Philadelphia.
33. Neiditch, M. B., M. J. Federle, A. J. Pompeani, R. C. Kelly, D. L. Swem, P. D. Jeffrey, B. L. Bassler, and F. M. Hughson. 2006. Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126:1095-1108.
34. Neu, H. C., and L. A. Heppel. 1964. On the surface localization of enzymes in E. coli. Biochem. Biophys. Res. Commun. 17:215-219.
35. Oldham, M. L., D. Khare, F. A. Quiocho, A. L. Davidson, and J. Chen. 2007. Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450:515-521. (Pubitemid 350190241)
36. Ordal, G. W., and J. Adler. 1974. Properties of mutants in galactose taxis and transport. J. Bacteriol. 117:517-526.
37. Reference deleted.
38. Quiocho, F. A., and P. S. Ledvina. 1996. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol. Microbiol. 20:17-25.
39. Schafer, A., A. Tauch, W. Jager, J. Kalinowski, G. Thierbach, and A. Puhler. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73. (Pubitemid 24224965)
40. Reference deleted.
41. Shimoda, N., A. Toyoda-Yamamoto, S. Aoki, and Y. Machida. 1993. Genetic evidence for an interaction between the VirA sensor protein and the ChvE sugar-binding protein of Agrobacterium. J. Biol. Chem. 268:26552-26558. (Pubitemid 23361735)
42. Silhavy, T. J., and W. Boos. 1975. The "hidden ligand" of the galactose-binding protein. Eur. J. Biochem. 54:163-167.
43. Silva, J. L., E. W. Miles, and G. Weber. 1986. Pressure dissociation and conformational drift of the beta dimer of tryptophan synthase. Biochemistry 25:5780-5786.
44. Stulke, J., and W. Hillen. 1999. Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2:195-201.
45. Tam, R., and M. H. Saier, Jr. 1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57:320-346.
46. Toyoda-Yamamoto, A., N. Shimoda, and Y. Machida. 2000. Genetic analysis of the signal-sensing region of the histidine protein kinase VirA of Agrobacterium tumefaciens. Mol. Gen. Genet. 263:939-947.
47. Turk, S. C., R. P. van Lange, T. J. Regensburg-Tuink, and P. J. Hooykaas. 1994. Localization of the VirA domain involved in acetosyringone-mediated vir gene induction in Agrobacterium tumefaciens. Plant Mol. Biol. 25:899-907.
48. Vivian, J. T., and P. R. Callis. 2001. Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80:2093-2109.
49. Vyas, N. K., M. N. Vyas, and F. A. Quiocho. 1988. Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. Science 242:1290-1295.
50. Wang, Y., A. Mukhopadhyay, V. R. Howitz, A. N. Binns, and D. G. Lynn. 2000. Construction of an efficient expression system for Agrobacterium tumefaciens based on the coliphage T5 promoter. Gene 242:105-114.
51. Ward, L. D. 1985. Measurement of ligand binding to proteins by fluorescence spectroscopy. Methods Enzymol. 117:400-414.
52. Winans, S. C. 1990. Transcriptional induction of an Agrobacterium regulatory gene at tandem promoters by plant-released phenolic compounds, phosphate starvation, and acidic growth media. J. Bacteriol. 172:2433-2438.
53. Winans, S. C., R. A. Kerstetter, and E. W. Nester. 1988. Transcriptional regulation of the virA and virG genes of Agrobacterium tumefaciens. J. Bacteriol. 170:4047-4054.
54. Zhang, Y., C. Conway, M. Rosato, Y. Suh, and M. D. Manson. 1992. Maltose chemotaxis involves residues in the N-terminal and C-terminal domains on the same face of maltose-binding protein. J. Biol. Chem. 267:22813-22820.