Hypoxia-induced localization of chemotaxis-related signaling proteins in Vibrio cholerae

Molecular Microbiology

Volumn 95, Issue 5, 2015, Pages 780-790

  Hiremath, Geetha ^a,c   Hyakutake, Akihiro ^b,d   Yamamoto, Kentaro ^a   Ebisawa, Tatsuaki ^a   Nakamura, Tomoyuki ^a   Nishiyama, So ichiro ^a   Homma, Michio ^b   Kawagishi, Ikuro ^a  

^a HOSEI UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c Novozymes South Asia Pvt Ltd   (India)

^d Terumo Yamaguchi Corporation   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CHEA1 PROTEIN; CHEA2 PROTEIN; CHEW0 PROTEIN; CHEW1 PROTEIN; CHEY2 PROTEIN; CHEY3 PROTEIN; CYTOPLASM PROTEIN; MLP13 PROTEIN; MLP16 PROTEIN; MLP24 PROTEIN; PROTEIN HISTIDINE KINASE; RECEPTOR PROTEIN; REGULATOR PROTEIN; SODIUM AZIDE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; OXYGEN; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE;

AERATION; ARTICLE; BACTERIAL GROWTH; CELL ENERGY; CELLULAR DISTRIBUTION; CHEMOTAXIS; ENERGY METABOLISM; GROWTH INHIBITION; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PHYSIOLOGY;

VIBRIO CHOLERAE;

BACTERIAL PROTEINS; CHEMOTAXIS; ENERGY METABOLISM; GREEN FLUORESCENT PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; OXYGEN; PROTEIN KINASES; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE;

EID: 84924043218     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12887     Document Type: Article

References (48)

1. Alm, R.A., and Manning, P.A. (1990) Characterization of the hlyB gene and its role in the production of the El Tor haemolysin of Vibrio cholerae O1. Mol Microbiol 4: 413-425.
2. Ames, P., Studdert, C.A., Reiser, R.H., and Parkinson, J.S. (2002) Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99: 7060-7065.
3. Armitage, J.P. (1999) Bacterial tactic responses. Adv Microb Physiol 41: 229-289.
4. Banerjee, R., Das, S., Mukhopadhyay, K., Nag, S., Chakrabortty, A., and Chaudhuri, K. (2002) Involvement of in vivo induced cheY-4 gene of Vibrio cholerae in motility, early adherence to intestinal epithelial cells and regulation of virulence factors. FEBS Lett 532: 221-226.
5. Banno, S., Shiomi, D., Homma, M., and Kawagishi, I. (2004) Targeting of the chemotaxis methylesterase/deamidase CheB to the polar receptor-kinase cluster in an Escherichia coli cell. Mol Microbiol 53: 1051-1063.
6. 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.
7. Boin, M.A., and Häse, C.C. (2007) Characterization of Vibrio cholerae aerotaxis. FEMS Microbiol Lett 276: 193-201.
8. Bray, D., Levin, M.D., and Morton-Firth, C.J. (1998) Receptor clustering as a cellular mechanism to control sensitivity. Nature 393: 85-88.
9. Briegel, A., Li, X., Bilwes, A.M., Hughes, K.T., Jensen, G.J., and Crane, B.R. (2012) Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins. Proc Natl Acad Sci USA 109: 3766-3771.
10. Butler, S.M., and Camilli, A. (2004) Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc Natl Acad Sci USA 101: 5018-5023.
11. Butler, S.M., and Camilli, A. (2005) Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol 3: 611-620.
12. Butler, S.M., Nelson, E.J., Chowdhury, N., Faruque, S.M., Calderwood, S.B., and Camilli, A. (2006) Cholera stool bacteria repress chemotaxis to increase infectivity. Mol Microbiol 60: 417-426.
13. Everiss, K.D., Hughes, K.J., Kovach, M.E., and Peterson, K.M. (1994) The Vibrio cholerae acfB colonization determinant encodes an inner membrane protein that is related to a family of signal-transducing proteins. Infect Immun 62: 3289-3298.
14. Gardel, C.L., and Mekalanos, J.J. (1996) Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun 64: 2246-2255.
15. Gegner, J.A., Graham, D.R., Roth, A.F., and Dahlquist, F.W. (1992) Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell 70: 975-982.
16. Gestwicki, J.E., and Kiessling, L.L. (2002) Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415: 81-84.
17. Gosink, K.K., Kobayashi, R., Kawagishi, I., and Häse, C.C. (2002) Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J Bacteriol 184: 1767-1771.
18. BAD promoter. J Bacteriol 177: 4121-4130.
19. Hang, L., John, M., Asaduzzaman, M., Bridges, E.A., Vanderspurt, C., Kirn, T.J., etal. (2003) Use of in vivo-induced antigen technology (IVIAT) to identify genes uniquely expressed during human infection with Vibrio cholerae. Proc Natl Acad Sci USA 100: 8508-8513.
20. Harkey, C.W., Everiss, K.D., and Peterson, K.M. (1994) The Vibrio cholerae toxin-coregulated-pilus gene tcpI encodes a homolog of methyl-accepting chemotaxis proteins. Infect Immun 62: 2669-2678.
21. 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.
22. Heidelberg, J.F., Eisen, J.A., Nelson, W.C., Clayton, R.A., Gwinn, M.L., Dodson, R.J., etal. (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477-483.
23. Hiremath, G., Nishiyama, S., and Kawagishi, I. (2013) CheV1 plays an important role in chemotaxis of Vibrio cholerae. Int J Biosci Biochem Bioinforma 3: 71-74.
24. Hoffmann, C., Gaietta, G., Zurn, A., Adams, S.R., Terrillon, S., Ellisman, M.H., etal. (2010) Fluorescent labeling of tetracysteine-tagged proteins in intact cells. Nat Protoc 5: 1666-1677.
25. Homma, M., Shiomi, D., Homma, M., and Kawagishi, I. (2004) Attractant binding alters arrangement of chemoreceptor dimers within its cluster at a cell pole. Proc Natl Acad Sci USA 101: 3462-3467.
26. Hyakutake, A., Homma, M., Austin, M.J., Boin, M.A., Häse, C.C., and Kawagishi, I. (2005) Only one of the five CheY homologs in Vibrio cholerae directly switches flagellar rotation. J Bacteriol 187: 8403-8410.
27. Irieda, H., Homma, M., Homma, M., and Kawagishi, I. (2006) Control of chemotactic signal gain via modulation of a pre-formed receptor array. J Biol Chem 281: 23880-23886.
28. Kan, B., Habibi, H., Schmid, M., Liang, W., Wang, R., Wang, D., and Jungblut, P.R. (2004) Proteome comparison of Vibrio cholerae cultured in aerobic and anaerobic conditions. Proteomics 4: 3061-3067.
29. Kim, S.H., Wang, W., and Kim, K.K. (2002) Dynamic and clustering model of bacterial chemotaxis receptors: structural basis for signaling and high sensitivity. Proc Natl Acad Sci USA 99: 11611-11615.
30. Krishnan, H.H., Ghosh, A., Paul, K., and Chowdhury, R. (2004) Effect of anaerobiosis on expression of virulence factors in Vibrio cholerae. Infect Immun 72: 3961-3967.
31. Krukonis, E.S., and DiRita, V.J. (2003) From motility to virulence: sensing and responding to environmental signals in Vibrio cholerae. Curr Opin Microbiol 6: 186-190.
32. Lee, C.A. (1999) Vibrio cholerae TCP: a trifunctional virulence factor? Trends Microbiol 7: 391-392, discussion 393.
33. Lee, S.H., Butler, S.M., and Camilli, A. (2001) Selection for in vivo regulators of bacterial virulence. Proc Natl Acad Sci USA 98: 6889-6894.
34. Maddock, J.R., and Shapiro, L. (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717-1723.
35. Mekalanos, J.J., Swartz, D.J., Pearson, G.D., Harford, N., Groyne, F., and de Wilde, M. (1983) Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development. Nature 306: 551-557.
36. Merrell, D.S., Butler, S.M., Qadri, F., Dolganov, N.A., Alam, A., Cohen, M.B., etal. (2002) Host-induced epidemic spread of the cholera bacterium. Nature 417: 642-645.
37. Moorthy, S., and Watnick, P.I. (2005) Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol Microbiol 57: 1623-1635.
38. Nishiyama, S., Suzuki, D., Itoh, Y., Suzuki, K., Tajima, H., Hyakutake, A., etal. (2012) Mlp24 (McpX) of Vibrio cholerae implicated in pathogenicity functions as a chemoreceptor for multiple amino acids. Infect Immun 80: 3170-3178.
39. Rebbapragada, A., Johnson, M.S., Harding, G.P., Zuccarelli, A.J., Fletcher, H.M., Zhulin, I.B., and Taylor, B.L. (1997) The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc Natl Acad Sci USA 94: 10541-10546.
40. Schuster, S.C., Swanson, R.V., Alex, L.A., Bourret, R.B., and Simon, M.I. (1993) Assembly and function of a quaternary signal transduction complex monitored by surface plasmon resonance. Nature 365: 343-347.
41. Shiomi, D., Banno, S., Homma, M., and Kawagishi, I. (2005) Stabilization of polar localization of a chemoreceptor via its covalent modifications and its communication with a different chemoreceptor. J Bacteriol 187: 7647-7654.
42. Shiomi, D., I., Zhulin, B., Homma, M., and Kawagishi, I. (2002) Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J Biol Chem 277: 42325-42333.
43. Sourjik, V., and Berg, H.C. (2000) Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37: 740-751.
44. Sourjik, V., and Berg, H.C. (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99: 123-127.
45. Swulius, M.T., and Jensen, G.J. (2012) The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-Terminal yellow fluorescent protein tag. J Bacteriol 194: 6382-6386.
46. Taylor, B.L., and Zhulin, I.B. (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63: 479-506.
47. Wu, K., Walukiewicz, H.E., Glekas, G.D., Ordal, G.W., and Rao, C.V. (2011) Attractant binding induces distinct structural changes to the polar and lateral signaling clusters in Bacillus subtilis chemotaxis. J Biol Chem 286: 2587-2595.
48. Zhang, P., Khursigara, C.M., Hartnell, L.M., and Subramaniam, S. (2007) Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc Natl Acad Sci USA 104: 3777-3781.