Structural biology: Specificity of the CheR2 methyltransferase in pseudomonas aeruginosa is directed by a C-terminal pentapeptide in the McpB chemoreceptor

Science Signaling

Volumn 7, Issue 320, 2014, Pages

  García Fontana, Cristina ^a,b   Lugo, Andrés Corral ^a   Krell, Tino ^a  

^a CSIC   (Spain)

^b Bio Iliberis R and D   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHER2 METHYLTRANSFERASE; METHYL ACCEPTING CHEMOTAXIS PROTEIN B; METHYLTRANSFERASE; PENTAPEPTIDE; PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; MEMBRANE PROTEIN; METHYL-ACCEPTING CHEMOTAXIS PROTEINS; OLIGOPEPTIDE; PROTEIN METHYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; CARBOXY TERMINAL SEQUENCE; CHEMORECEPTOR; CONTROLLED STUDY; ENZYME SPECIFICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN METHYLATION; PSEUDOMONAS AERUGINOSA; GENETICS; HUMAN; INDEL MUTATION; METABOLISM; METHYLATION; PHYSIOLOGY; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; HUMANS; INDEL MUTATION; MEMBRANE PROTEINS; METHYLATION; OLIGOPEPTIDES; PROTEIN METHYLTRANSFERASES; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; SUBSTRATE SPECIFICITY;

EID: 84898840393     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004849     Document Type: Article

References (46)

1. M. Y. Galperin, A census of membrane-bound and intracellular signal transduction proteins in bacteria: Bacterial IQ, extroverts and introverts. BMC Microbiol. 5, 35 (2005)
2. L. E. Ulrich, E. V. Koonin, I. B. Zhulin, One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 13, 52-56 (2005)
3. K. Wuichet, I. B. Zhulin, Origins and diversification of a complex signal transduction system in prokaryotes. Sci. Signal. 3, ra50 (2010)
4. G. L. Hazelbauer, J. J. Falke, J. S. Parkinson, Bacterial chemoreceptors: Highperformance signaling in networked arrays. Trends Biochem. Sci. 33, 9-19 (2008)
5. J. Yuan, R. W. Branch, B. G. Hosu, H. C. Berg, Adaptation at the output of the chemotaxis signalling pathway. Nature 484, 233-236 (2012)
6. N. Vladimirov, V. Sourjik, Chemotaxis: How bacteria use memory. Biol. Chem. 390, 1097-1104 (2009)
7. R. Hamer, P. Y. Chen, J. P. Armitage, G. Reinert, C. M. Deane, Deciphering chemotaxis pathways using cross species comparisons. BMC Syst. Biol. 4, 3 (2010)
8. J. Kato, H. E. Kim, N. Takiguchi, A. Kuroda, H. Ohtake, Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. J. Biosci. Bioeng. 106, 1-7 (2008)
9. J. Kato, T. Nakamura, A. Kuroda, H. Ohtake, Cloning and characterization of chemotaxis genes in Pseudomonas aeruginosa. Biosci. Biotechnol. Biochem. 63, 155-161 (1999)
10. Z. T. Güvener, D. F. Tifrea, C. S. Harwood, Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol. Microbiol. 61, 106-118 (2006)
11. J. W. Hickman, D. F. Tifrea, C. S. Harwood, A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. U. S. A. 102, 14422-14427 (2005)
12. N. B. Fulcher, P. M. Holliday, E. Klem, M. J. Cann, M. C. Wolfgang, The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulating adenylate cyclase activity. Mol. Microbiol. 76, 889-904 (2010)
13. C. S. Hong, M. Shitashiro, A. Kuroda, T. Ikeda, N. Takiguchi, H. Ohtake, J. Kato, Chemotaxis proteins and transducers for aerotaxis in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 231, 247-252 (2004)
14. S. Garvis, A. Munder, G. Ball, S. de Bentzmann, L. Wiehlmann, J. J. Ewbank, B. Tümmler, A. Filloux, Caenorhabditis elegans semi-automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence. PLOS Pathog. 5, e1000540 (2009)
15. G. Li, R. M. Weis, Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100, 357-365 (2000)
16. S. A. Simms, K. Subbaramaiah, The kinetic mechanism of S-adenosyl-L-methionine: Glutamylmethyltransferase from Salmonella typhimurium. J. Biol. Chem. 266, 12741-12746 (1991)
17. J. Wu, J. Li, G. Li, D. G. Long, R. M. Weis, The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 35, 4984-4993 (1996)
18. M. Li, G. L. Hazelbauer, The carboxyl-terminal linker is important for chemoreceptor function. Mol. Microbiol. 60, 469-479 (2006)
19. H. Okumura, S. Nishiyama, A. Sasaki, M. Homma, I. Kawagishi, Chemotactic adaptation is altered by changes in the carboxy-terminal sequence conserved among the major methyl-accepting chemoreceptors. J. Bacteriol. 180, 1862-1868 (1998)
20. S. Djordjevic, A. M. Stock, Chemotaxis receptor recognition by protein methyltransferase CheR. Nat. Struct. Biol. 5, 446-450 (1998)
21. A. N. Barnakov, L. A. Barnakova, G. L. Hazelbauer, Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proc. Natl. Acad. Sci. U. S. A. 96, 10667-10672 (1999)
22. H. Le Moual, T. Quang, D. E. Koshland Jr., Methylation of the Escherichia coli chemotaxis receptors: Intra-and interdimer mechanisms. Biochemistry 36, 13441-13448 (1997)
23. W. C. Lai, G. L. Hazelbauer, Carboxyl-terminal extensions beyond the conserved pentapeptide reduce rates of chemoreceptor adaptational modification. J. Bacteriol. 187, 5115-5121 (2005)
24. A. N. Barnakov, L. A. Barnakova, G. L. Hazelbauer, Comparison in vitro of a high-and a low-abundance chemoreceptor of Escherichia coli: Similar kinase activation but different methyl-accepting activities. J. Bacteriol. 180, 6713-6718 (1998)
25. B. Windisch, D. Bray, T. Duke, Balls and chains-A mesoscopic approach to tethered protein domains. Biophys. J. 91, 2383-2392 (2006)
26. E. Perez, A. M. Stock, Characterization of the Thermotoga maritima chemotaxis methylation system that lacks pentapeptide-dependent methyltransferase CheR: MCP tethering. Mol. Microbiol. 63, 363-378 (2007)
27. S. A. Simms, A. M. Stock, J. B. Stock, Purification and characterization of the S-adenosylmethionine:glutamyl methyltransferase that modifies membrane chemoreceptor proteins in bacteria. J. Biol. Chem. 262, 8537-8543 (1987)
28. X. Yi, R. M. Weis, The receptor docking segment and S-adenosyl-L- homocysteine bind independently to the methyltransferase of bacterial chemotaxis. Biochim. Biophys. Acta 1596, 28-35 (2002)
29. D. Shiomi, H. Okumura, M. Homma, I. Kawagishi, The aspartate chemoreceptor Tar is effectively methylated by binding to the methyltransferase mainly through hydrophobic interaction. Mol. Microbiol. 36, 132-140 (2000)
30. A. Ferrández, A. C. Hawkins, D. T. Summerfield, C. S. Harwood, Cluster II che genes from Pseudomonas aeruginosa are required for an optimal chemotactic response. J. Bacteriol. 184, 4374-4383 (2002)
31. J. R. Kirby, M. M. Saulmon, C. J. Kristich, G. W. Ordal, CheY-dependent methylation of the asparagine receptor, McpB, during chemotaxis in Bacillus subtilis. J. Biol. Chem. 274, 11092-11100 (1999)
32. D. Shiomi, I. B. Zhulin, M. Homma, I. Kawagishi, Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J. Biol. Chem. 277, 42325-42333 (2002)
33. M. N. Levit, J. B. Stock, Receptor methylation controls the magnitude of stimulusresponse coupling in bacterial chemotaxis. J. Biol. Chem. 277, 36760-36765 (2002)
34. M. R. Kehry, F. W. Dahlquist, The methyl-accepting chemotaxis proteins of Escherichia coli. Identification of the multiple methylation sites on methyl-accepting chemotaxis protein I. J. Biol. Chem. 257, 10378-10386 (1982)
35. P. Engström, G. L. Hazelbauer, Multiple methylation of methyl-accepting chemotaxis proteins during adaptation of E. coli to chemical stimuli. Cell 20, 165-171 (1980)
36. M. S. Springer, M. F. Goy, J. Adler, Sensory transduction in Escherichia coli: Two complementary pathways of information processing that involve methylated proteins. Proc. Natl. Acad. Sci. U. S. A. 74, 3312-3316 (1977)
37. U. K. Muppirala, S. Desensi, T. P. Lybrand, G. L. Hazelbauer, Z. Li, Molecular modeling of flexible arm-mediated interactions between bacterial chemoreceptors and their modification enzyme. Protein Sci. 18, 1702-1714 (2009)
38. M. D. Levin, T. S. Shimizu, D. Bray, Binding and diffusion of CheR molecules within a cluster of membrane receptors. Biophys. J. 82, 1809-1817 (2002)
39. M. Bains, L. Fernández, R. E. Hancock, Phosphate starvation promotes swarming motility and cytotoxicity of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78, 6762-6768 (2012)
40. J. L. Martin, F. M. McMillan, SAM (dependent) I AM: The S-adenosylmethioninedependent methyltransferase fold. Curr. Opin. Struct. Biol. 12, 783-793 (2002)
41. A. Hemsley, N. Arnheim, M. D. Toney, G. Cortopassi, D. J. Galas, A simple method for site-directed mutagenesis using the polymerase chain reaction. Nucleic Acids Res. 17, 6545-6551 (1989)
42. J. B. Stock, S. Clarke, D. E. Koshland Jr., The protein carboxylmethyltransferase involved in Escherichia coli and Salmonella typhimurium chemotaxis. Methods Enzymol. 106, 310-321 (1984)
43. J. E. Campillo, S. J. Ashcroft, Protein carboxymethylation in rat islets of Langerhans. FEBS Lett. 138, 71-75 (1982)
44. C. K. Stover, X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. Hancock, S. Lory, M. V. Olson, Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964 (2000)
45. F. W. Studier, B. A. Moffatt, Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113-130 (1986)
46. D. Hanahan, Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580 (1983).