Salmonella chemoreceptors McpB and McpC mediate a repellent response to L-cystine: A potential mechanism to avoid oxidative conditions

Molecular Microbiology

Volumn 84, Issue 4, 2012, Pages 697-711

  Lazova, Milena D ^a   Butler, Mitchell T ^b   Shimizu, Thomas S ^a   Harshey, Rasika M ^b  

^a FOM INSTITUTE AMOLF   (Netherlands)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID DERIVATIVE; CHEMOATTRACTANT; CYSTEINE; CYSTINE; ESTERASE; MEMBRANE RECEPTOR; METHYLTRANSFERASE; PROTEIN CHEB; PROTEIN CHER; PROTEIN KINASE; PROTEIN MCPB; PROTEIN MCPC; PROTEIN TSR; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHEMORECEPTOR; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VIVO STUDY; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA ENTERICA; WILD TYPE;

AGAR; BACTERIAL PROTEINS; CHEMOTAXIS; CULTURE MEDIA; CYSTINE; LOCOMOTION; SALMONELLA TYPHIMURIUM;

ESCHERICHIA COLI; SALMONELLA; SALMONELLA ENTERICA;

EID: 84860554052     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08051.x     Document Type: Article

References (65)

1. Adler, J. (1973) A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol 74: 77-91.
2. Alexander, R.P., Lowenthal, A.C., Harshey, R.M., and Ottemann, K.M. (2010) CheV: CheW-like coupling proteins at the core of the chemotaxis signaling network. Trends Microbiol 18: 494-503.
3. Alexandre, G., and Zhulin, I.B. (2001) More than one way to sense chemicals. J Bacteriol 183: 4681-4686.
4. Amann, E., Ochs, B., and Abel, K.J. (1988) Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69: 301-315.
5. Asquith, R.S., and Hirst, L. (1969) The photochemical degradation of cystine in aqueous solution in the presence of air. Biochim Biophys Acta 184: 345-357.
6. Baker, M.D., Wolanin, P.M., and Stock, J.B. (2006) Signal transduction in bacterial chemotaxis. Bioessays 28: 9-22.
7. Baptist, E.W., and Kredich, N.M. (1977) Regulation of L-cystine transport in Salmonella typhimurium. J Bacteriol 131: 111-118.
8. Barnakov, A.N., Barnakova, L.A., and Hazelbauer, G.L. (1999) Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proc Natl Acad Sci USA 96: 10667-10672.
9. Berg, H.C., and Block, S.M. (1984) A miniature flow cell designed for rapid exchange of media under high-power microscope objectives. J Gen Microbiol 130: 2915-2920.
10. Bespalov, V.A., Zhulin, I.B., and Taylor, B.L. (1996) Behavioral responses of Escherichia coli to changes in redox potential. Proc Natl Acad Sci USA 93: 10084-10089.
11. Bibikov, S.I., Biran, R., Rudd, K.E., and Parkinson, J.S. (1997) A signal transducer for aerotaxis in Escherichia coli. J Bacteriol 179: 4075-4079.
12. Bibikov, S.I., Miller, A.C., Gosink, K.K., and Parkinson, J.S. (2004) Methylation-independent aerotaxis mediated by the Escherichia coli Aer protein. J Bacteriol 186: 3730-3737.
13. Burkart, M., Toguchi, A., and Harshey, R.M. (1998) The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli. Proc Natl Acad Sci USA 95: 2568-2573.
14. Butler, J.D., Levin, S.W., Facchiano, A., Miele, L., and Mukherjee, A.B. (1993) Amino acid composition and N-terminal sequence of purified cystine binding protein of Escherichia coli. Life Sci 52: 1209-1215.
15. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
16. Ehrenberg, L., Harmsringdahl, M., Fedorcsak, I., and Granath, F. (1989) Kinetics of the copper-catalyzed and iron-catalyzed oxidation of cysteine by dioxygen. Acta Chem Scand 43: 177-187.
17. Feng, X., Baumgartner, J.W., and Hazelbauer, G.L. (1997) High- and low-abundance chemoreceptors in Escherichia coli: differential activities associated with closely related cytoplasmic domains. J Bacteriol 179: 6714-6720.
18. Feng, X., Lilly, A.A., and Hazelbauer, G.L. (1999) Enhanced function conferred on low-abundance chemoreceptor Trg by a methyltransferase-docking site. J Bacteriol 181: 3164-3171.
19. Frye, J., Karlinsey, J.E., Felise, H.R., Marzolf, B., Dowidar, N., McClelland, M., and Hughes, K.T. (2006) Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J Bacteriol 188: 2233-2243.
20. Gosink, K.K., Buron-Barral, M.C., and Parkinson, J.S. (2006) Signaling interactions between the aerotaxis transducer Aer and heterologous chemoreceptors in Escherichia coli. J Bacteriol 188: 3487-3493.
21. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
22. Hazelbauer, G.L., Falke, J.J., and Parkinson, J.S. (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33: 9-19.
23. Hedblom, M.L., and Adler, J. (1983) Chemotactic response of Escherichia coli to chemically synthesized amino acids. J Bacteriol 155: 1463-1466.
24. Karatan, E., Saulmon, M.M., Bunn, M.W., and Ordal, G.W. (2001) Phosphorylation of the response regulator CheV is required for adaptation to attractants during Bacillus subtilis chemotaxis. J Biol Chem 276: 43618-43626.
25. Kihara, M., and Macnab, R.M. (1981) Cytoplasmic pH mediates pH taxis and weak-acid repellent taxis of bacteria. J Bacteriol 145: 1209-1221.
26. Kondoh, H., Ball, C.B., and Adler, J. (1979) Identification of a methyl-accepting chemotaxis protein for the ribose and galactose chemoreceptors of Escherichia coli. Proc Natl Acad Sci USA 76: 260-264.
27. Lan, G., Schulmeister, S., Sourjik, V., and Tu, Y. (2011) Adapt locally and act globally: strategy to maintain high chemoreceptor sensitivity in complex environments. Mol Syst Biol 7: 475.
28. Lazova, M.D., Ahmed, T., Bellomo, D., Stocker, R., and Shimizu, T.S. (2011) Response rescaling in bacterial chemotaxis. Proc Natl Acad Sci USA 108: 13870-13875.
29. Li, J., Li, G., and Weis, R.M. (1997) The serine chemoreceptor from Escherichia coli is methylated through an inter-dimer process. Biochemistry 36: 11851-11857.
30. Li, M., and Hazelbauer, G.L. (2006) The carboxyl-terminal linker is important for chemoreceptor function. Mol Microbiol 60: 469-479.
31. Lux, R., Jahreis, K., Bettenbrock, K., Parkinson, J.S., and Lengeler, J.W. (1995) Coupling the phosphotransferase system and the methyl-accepting chemotaxis protein-dependent chemotaxis signaling pathways of Escherichia coli. Proc Natl Acad Sci USA 92: 11583-11587.
32. McGhie, E.J., Brawn, L.C., Hume, P.J., Humphreys, D., and Koronakis, V. (2009) Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 12: 117-124.
33. Maddock, J.R., and Shapiro, L. (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717-1723.
34. Manson, M.D., Blank, V., Brade, G., and Higgins, C.F. (1986) Peptide chemotaxis in E. coli involves the Tap signal transducer and the dipeptide permease. Nature 321: 253-256.
35. Meir, Y., Jakovljevic, V., Oleksiuk, O., Sourjik, V., and Wingreen, N.S. (2010) Precision and kinetics of adaptation in bacterial chemotaxis. Biophys J 99: 2766-2774.
36. Melton, T., Hartman, P.E., Stratis, J., Lee, T.L., and Davis, A.T. (1978) Chemotaxis of Salmonella typhimurium to amino acids and some sugars. J Bacteriol 133: 708-716.
37. Mesibov, R., and Adler, J. (1972) Chemotaxis toward amino acids in Escherichia coli. J Bacteriol 112: 315-326.
38. Miller, L.D., Russell, M.H., and Alexandre, G. (2009) Diversity in bacterial chemotactic responses and niche adaptation. Adv Appl Microbiol 66: 53-75.
39. Mowbray, S.L., and Koshland, D.E. (1987) Additive and independent responses in a single receptor: aspartate and maltose stimuli on the Tar protein. Cell 50: 171-180.
40. Neumann, S., Hansen, C.H., Wingreen, N.S., and Sourjik, V. (2010) Differences in signalling by directly and indirectly binding ligands in bacterial chemotaxis. EMBO J 29: 3484-3495.
41. Ohtsu, I., Wiriyathanawudhiwong, N., Morigasaki, S., Nakatani, T., Kadokura, H., and Takagi, H. (2010) The L-cysteine/L-cystine shuttle system provides reducing equivalents to the periplasm in Escherichia coli. J Biol Chem 285: 17479-17487.
42. Rosner, J.L., and Storz, G. (1997) Regulation of bacterial responses to oxidative stress. Curr Top Cell Regul 35: 163-177.
43. Russo, A.F., and Koshland, D.E. (1986) Identification of the tip-encoded receptor in bacterial sensing. J Bacteriol 165: 276-282.
44. Sano, G., Takada, Y., Goto, S., Maruyama, K., Shindo, Y., Oka, K., etal. (2007) Flagella facilitate escape of Salmonella from oncotic macrophages. J Bacteriol 189: 8224-8232.
45. Shimizu, T.S., Tu, Y., and Berg, H.C. (2010) A modular gradient-sensing network for chemotaxis in Escherichia coli revealed by responses to time-varying stimuli. Mol Syst Biol 6: 382.
46. Shinohara, K., and Kilpatrick, M. (1934) The stability of cystine in acid solution. J Biol Chem 105: 241-251.
47. Shiomi, D., Okumura, H., Homma, M., and Kawagishi, I. (2000) The aspartate chemoreceptor Tar is effectively methylated by binding to the methyltransferase mainly through hydrophobic interaction. Mol Microbiol 36: 132-140.
48. Sourjik, V., and Berg, H.C. (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99: 123-127.
49. Sourjik, V., and Berg, H.C. (2004) Functional interactions between receptors in bacterial chemotaxis. Nature 428: 437-441.
50. Sourjik, V., Vaknin, A., Shimizu, T.S., and Berg, H.C. (2007) In vivo measurement by FRET of pathway activity in bacterial chemotaxis. Methods Enzymol 423: 365-391.
51. Stevens, R., Stevems, L., and Price, N.C. (1983) The stabilities of various thiol compounds used in protein purifications. Biochem Educ 11: 70.
52. Stock, J.B., and Surette, M.G. (1996) Chemotaxis. Washington, DC: ASM Press, pp. 1103-1129.
53. Taylor, B.L., Zhulin, I.B., and Johnson, M.S. (1999) Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol 53: 103-128.
54. Tso, W.W., and Adler, J. (1974) Negative chemotaxis in Escherichia coli. J Bacteriol 118: 560-576.
55. Tu, Y., Shimizu, T.S., and Berg, H.C. (2008) Modeling the chemotactic response of Escherichia coli to time-varying stimuli. Proc Natl Acad Sci USA 105: 14855-14860.
56. Wadhams, G.H., and Armitage, J.P. (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5: 1024-1037.
57. Wang, Q., Suzuki, A., Mariconda, S., Porwollik, S., and Harshey, R.M. (2005) Sensing wetness: a new role for the bacterial flagellum. EMBO J 24: 2034-2042.
58. Wang, Q., Mariconda, S., Suzuki, A., McClelland, M., and Harshey, R.M. (2006) Uncovering a large set of genes that affect surface motility in Salmonella enterica serovar Typhimurium. J Bacteriol 188: 7981-7984.
59. Watts, K.J., Ma, Q., Johnson, M.S., and Taylor, B.L. (2004) Interactions between the PAS and HAMP domains of the Escherichia coli aerotaxis receptor Aer. J Bacteriol 186: 7440-7449.
60. Weerasuriya, S., Schneider, B.M., and Manson, M.D. (1998) Chimeric chemoreceptors in Escherichia coli: signaling properties of Tar-Tap and Tap-Tar hybrids. J Bacteriol 180: 914-920.
61. Wolfe, A.J., and Berg, H.C. (1989) Migration of bacteria in semisolid agar. Proc Natl Acad Sci USA 86: 6973-6977.
62. Yamamoto, K., and Imae, Y. (1993) Cloning and characterization of the Salmonella typhimurium-specific chemoreceptor Tcp for taxis to citrate and from phenol. Proc Natl Acad Sci USA 90: 217-221.
63. Yuan, J., and Berg, H.C. (2008) Resurrection of the flagellar rotary motor near zero load. Proc Natl Acad Sci USA 105: 1182-1185.
64. Zhou, Q., Ames, P., and Parkinson, J.S. (2009) Mutational analyses of HAMP helices suggest a dynamic bundle model of input-output signalling in chemoreceptors. Mol Microbiol 73: 801-814.
65. Zhou, Q., Ames, P., and Parkinson, J.S. (2011) Biphasic control logic of HAMP domain signalling in the Escherichia coli serine chemoreceptor. Mol Microbiol 80: 596-611.