Constitutive activation of two-component response regulators: Characterization of VirG activation in Agrobacterium tumefaciens

Journal of Bacteriology

Volumn 188, Issue 14, 2006, Pages 5204-5211

  Gao, Kong ^a   Mukhopadhyay, Aindrila ^a,b   Fang, Fang ^a   Lynn, David G ^a  

^a EMORY UNIVERSITY   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; PHOSPHATE; PROTEIN HISTIDINE KINASE; PROTEIN VIRG; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GENE EXPRESSION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RHIZOBIUM RADIOBACTER; SIGNAL TRANSDUCTION; VIRA GENE; VIRG GENE;

BACTERIAL PROTEINS; BASE SEQUENCE; CONSERVED SEQUENCE; DNA PRIMERS; GENE EXPRESSION REGULATION, BACTERIAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PLANTS; PLASMIDS; PROTEIN CONFORMATION; RHIZOBIUM RADIOBACTER; VIRULENCE;

AGROBACTERIUM; AGROBACTERIUM TUMEFACIENS;

EID: 33745895888     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00387-06     Document Type: Article

References (56)

1. Benda, C., C. Scheufler, N. T. de Marsac, and W. Gartner. 2004. Crystal structures of two cyanobacterial response regulators in apo- and phosphorylated form reveal a novel dimerization motif of phytochrome-associated response regulators. Biophys. J. 87:476-487.
2. Birck, C., Y. Chen, F. M. Hulett, and J.-P. Samama. 2003. The crystal structure of the phosphorylation domain in PhoP reveals a functional tandem association mediated by an asymmetric interface. J. Bacteriol. 185:254-261.
3. Birck, C., L. Mourey, P. Gouet, B. Fabry, J. Schumacher, P. Rousseau, D. Kahn, and J. P. Samama. 1999. Conformational changes induced by phosphorylation of the FixJ receiver domain. Structure 7:1505-1515.
4. Cangelosi, G. A., E. A. Best, G. Martinetti, and E. W. Nester. 1991. Genetic analysis of Agrobacterium. Methods Enzymol. 204:384-397.
5. Chamnongpol, S., and E. A. Groisman. 2000. Acetyl phosphate-dependent activation of a mutant PhoP response regulator that functions independently of its cognate sensor kinase. J. Mol. Biol. 300:291-305.
6. Chang, H. M., M. Y. Chen, Y. T. Shieh, M. J. Bibb, and C. W. Chen. 1996. The cutRS signal transduction system of Streptomyces lividans represses the biosynthesis of the polyketide antibiotic actinorhodin. Mol. Microbiol. 21:1075-1085.
7. Da Re, S., T. Tolstykh, P. M. Wolanin, and J. B. Stock. 2002. Genetic analysis of response regulator activation in bacterial chemotaxis suggests an intermolecular mechanism. Protein Sci. 11:2644-2654.
8. 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.
9. Gardino, A. K., B. F. Volkman, H. S. Cho, S. Y. Lee, D. E. Wemmer, and D. Kern. 2003. The NMR solution structure of BeF(3)(-)-activated Spo0F reveals the conformational switch in a phosphorelay system. J. Mol. Biol. 331:245-254.
10. Gubba, S., Y. H. Xie, and A. Das. 1995. Regulation of Agrobacterium tumefaciens virulence gene expression: isolation of a mutation that restores virGD52E function. Mol. Plant-Microbe Interact. 8:788-791.
11. Han, D. C., C. Y. Chen, Y. F. Chen, and S. C. Winans. 1992. Altered-function mutations of the transcriptional regulatory gene virG of Agrobacterium tumefaciens. J. Bacteriol. 174:7040-7043.
12. Han, D. C., and S. C. Winans. 1994. A mutation in the receiver domain of the Agrobacterium tumefaciens transcriptional regulator VirG increases its affinity for operator DNA. Mol. Microbiol. 12:23-30.
13. Jin, S., Y. Song, S. Q. Pan, and E. W. Nester. 1993. Characterization of a virG mutation that confers constitutive virulence gene expression in Agrobacterium. Mol. Microbiol. 7:555-562.
14. Jin, S. G., R. K. Prusti, T. Roitsch, R. G. Ankenbauer, and E. W. Nester. 1990. Phosphorylation of the VirG protein of Agrobacterium tumefaciens by the autophosphorylated VirA protein: essential role in biological activity of VirG. J. Bacteriol. 172:4945-4950.
15. Johnson, L. N., and R. J. Lewis. 2001 Structural basis for control by phosphorylation. Chem. Rev. 101:2209-2242.
16. Klose, K. E., D. S. Weiss, and S. Kustu. 1993. Glutamate at the site of phosphorylation of nitrogen-regulatory protein NTRC mimics aspartyl-phosphate and activates the protein. J. Mol. Biol. 232:67-78.
17. Kumari, S., C. M. Beatty, D. F. Browning, S. J. W. Busby, E. J. Simel, G. Hovel-Miner, and A. J. Wolfe. 2000. Regulation of acetyl coenzyme A synthetase in Escherichia coli. J. Bacteriol. 182:4173-4179.
18. Lan, C.-Y., and M. M. Igo. 1998. Differential expression of the OmpF and OmpC porin proteins in Escherichia coli K-12 depends upon the level of active OmpR. J. Bacteriol. 180:171-174.
19. Lee, K., M. W. Dudley, K. M. Hess, D. G. Lynn, R. D. Joerger, and A. N. Binns. 1992. Mechanism of activation of Agrobacterium virulence genes: identification of phenol-binding proteins. Proc. Natl. Acad. Sci. USA 89:8666-8670.
20. Lee, S.-Y., H. S. Cho, J. G. Pelton, D. Yan, E. A. Berry, and D. E. Wemmer. 2001. Crystal structure of activated CheY. Comparison with other activated receiver domains. J. Biol. Chem. 276:16425-16431.
21. Lee, S. Y., H. S. Cho, J. G. Pelton, D. Yan, R. K. Henderson, D. S. King, L. Huang, S. Kustu, E. A. Berry, and D. E. Wemmer. 2001. Crystal structure of an activated response regulator bound to its target. Nat. Struct. Biol. 8:52-56.
22. Lewis, R. J., J. A. Brannigan, K. Muchova, I. Barak, and A. J. Wilkinson. 1999. Phosphorylated aspartate in the structure of a response regulator protein. J. Mol. Biol. 294:9-15.
23. Lohrke, S. M., S. Nechaev, H. Yang, K. Severinov, and S. J. Jin. 1999. Transcriptional activation of Agrobacterium tumefaciens virulence gene promoters in Escherichia coli requires the A. tumefaciens RpoA gene, encoding the alpha subunit of RNA polymerase. J. Bacteriol. 181:4533-4539.
24. Lohrke, S. M., H. Yang, and S. Jin. 2001. Reconstitution of acetosyringone-mediated Agrobacterium tumefaciens virulence gene expression in the heterologous host Escherichia coli. J. Bacteriol. 183:3704-3711.
25. Lukat, G. S., B. H. Lee, J. M. Mottonen, A. M. Stock, and J. B. Stock. 1991. Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. J. Biol. Chem. 266:8348-8354.
26. Lukat, G. S., W. R. McCleary, A. M. Stock, and J. B. Stock. 1992. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci. USA 89:718-722.
27. Meyer, M. G., S. Park, L. Zeringue, M. Staley, M. McKinstry, R. I. Kaufman, H. Zhang, D. Van, N. Yennawar, H. Yennawar, G. K. Farber, and B. T. Nixon. 2001. A dimeric two-component receiver domain inhibits the sigma54-dependent ATPase in DctD. FASEB J. 15:1326-1328.
28. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
29. Mizuno, T. 1997. Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res. 4:161-168.
30. 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.
31. Nishino, K., and A. Yamaguchi. 2001. Overexpression of the response regulator evgA of the two-component signal transduction system modulates multidrug resistance conferred by multidrug resistance transporters. J. Bacteriol. 183:1455-1458.
32. Park, S., M. Meyer, A. D. Jones, H. P. Yennawar, N. H. Yennawar, and B. T. Nixon. 2002. Two-component signaling in the AAA + ATPase DctD: binding Mg2+ and BeF3- selects between alternate dimeric states of the receiver domain. FASEB J. 16:1964-1966.
33. Pazour, G. J., C. N. Ta, and A. Das. 1992. Constitutive mutations of Agrobacterium tumefaciens transcriptional activator virG. J. Bacteriol. 174:4169-4174.
34. Pruss, B. M., and A. J. Wolfe. 1994. Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli. Mol. Microbiol. 12:973-984.
35. Rodenburg, K. W., E. Scheeren-Groot, G. Vriend, and P. J. Hooykaas. 1994. The N-terminal domain of VirG of Agrobacterium tumefaciens: modelling and analysis of mutant phenotypes. Protein Eng. 7:905-909.
36. Scheeren-Groot, E. P., K. W. Rodenburg, A. den Dulk-Ras, S. C. Turk, and P. J. Hooykaas. 1994. Mutational analysis of the transcriptional activator VirG of Agrobacterium tumefaciens. J. Bacteriol. 176:6418-6426.
37. Silversmith, R. E., J. G. Smith, G. P. Guanga, J. T. Les, and R. B. Bourret. 2001. Alteration of a nonconserved active site residue in the chemotaxis response regulator CheY affects phosphorylation and interaction with CheZ. J. Biol. Chem. 276:18478-18484.
38. Simonovic, M., and K. Volz. 2001. A distinct meta-active conformation in the 1.1-A resolution structure of wild-type ApoCheY. J. Biol. Chem. 276:28637-28640.
39. Smith, J. G., J. A. Latiolais, G. P. Guanga, S. Citineni, R. E. Silversmith, and R. B. Bourret. 2003. Investigation of the role of electrostatic charge in activation of the Escherichia coli response regulator CheY. J. Bacteriol. 185:6385-6391.
40. Smith, J. G., J. A. Latiolais, G. P. Guanga, J. D. Pennington, R. E. Silversmith, and R. B. Bourret. 2004. A search for amino acid substitutions that universally activate response regulators. Mol. Microbiol. 51:887-901.
41. Sola, M., F. X. Gomis-Ruth, L. Serrano, A. Gonzalez, and M. Coll. 1999. Three-dimensional crystal structure of the transcription factor PhoB receiver domain. J. Mol. Biol. 285:675-687.
42. Stewart, R. 1993. Activating and inhibitory mutations in the regulatory domain of CheB, the methylesterase in bacterial chemotaxis. J. Biol. Chem. 268:1921-1930.
43. Stock, A. M., and A. H. West. 2003. Response regulator proteins and their interactions with histidine protein kinases, p. 237-271. In M. Inouye and R. Dutta (ed.), Histidine kinases in signal transduction. Academic Press, San Diego, Calif.
44. Tzfira, T., and V. Citovsky. 2002. Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol. 12:121-129.
45. Ueda, K., K. Miyake, S. Horinouchi, and T. Beppu. 1993. A gene cluster involved in aerial mycelium formation in Streptomyces griseus encodes proteins similar to the response regulators of two-component regulatory systems and membrane translocators. J. Bacteriol. 175:2006-2016.
46. Varughese, K. I. 2002. Molecular recognition of bacterial phosphorelay proteins. Curr. Opin. Microbiol. 5:142-148.
47. Volkman, B. F., D. Lipson, D. E. Wemmer, and D. Kern. 2001. Two-state allosteric behavior in a single-domain signaling protein. Science 291:2429-2433.
48. 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.
49. Watson, B., T. C. Currier, M. P. Gordon, M. D. Chilton, and E. W. Nester. 1975. Plasmid required for virulence of Agrobacterium tumefaciens. J. Bacteriol. 123:255-264.
50. West, A. H., and A. M. Stock. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26:369-376.
51. 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.
52. Winans, S. C., N. J. Mantis, C. Y. Chen, C. H. Chang, and D. C. Han. 1994. Host recognition by the VirA, VirG two-component regulatory proteins of Agrobacterium tumefaciens. Res. Microbiol. 145:461-473.
53. Wolfe, A. J. 2005. The acetate switch. Microbiol. Mol. Biol. Rev. 69:12-50.
54. Wolfe, A. J., D.-E. Chang, J. D. Walker, J. E. Seitz-Partridge, M. D. Vidaurri, C. F. Lange, B. M. Pruss, M. C. Henk, J. C. Larkin, and T. Conway. 2003. Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol. Microbiol. 48:977-988.
55. Zapf, J., M. Madhusudan, C. E. Grimshaw, J. A. Hoch, K. I. Varughese, and J. M. Whiteley. 1998. A source of response regulator autophosphatase activity: the critical role of a residue adjacent to the Spo0F autophosphorylation active site. Biochemistry 37:7725-7732.
56. Zhu, J., P. M. Oger, B. Schrammeijer, P. J. Hooykaas, S. K. Farrand, and S. C. Winans. 2000. The bases of crown gall tumorigenesis. J. Bacteriol. 182:3885-3895.