HAMP domain structural determinants for signalling and sensory adaptation in Tsr, the Escherichia coli serine chemoreceptor

Molecular Microbiology

Volumn 91, Issue 5, 2014, Pages 875-886

  Ames, Peter ^a   Zhou, Qin ^a,b   Parkinson, John S ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI PROTEIN; PHOSPHOTRANSFERASE; PROTEIN HAMP; SERINE; TSR RECEPTOR; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMORECEPTOR; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME REGULATION; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; FLAGELLUM; HYDROPHOBICITY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN METHYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STEADY STATE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; ESCHERICHIA COLI; FLAGELLA; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84896726994     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12443     Document Type: Article

References (44)

1. Airola, M., Watts, K.J., and Crane, B.R. (2010) Structure of concatenated HAMP domains provides a mechanism for signal transduction. Structure 18: 436-448.
2. Airola, M.V., Sukomon, N., Samanta, D., Borbat, P.P., Freed, J.H., Watts, K.J., and Crane, B.R. (2013) HAMP domain conformers that propagate opposite signals in bacterial chemoreceptors. PLoS Biol 11: e1001479.
3. Ames, P., and Parkinson, J.S. (1994) Constitutively signaling fragments of Tsr, the Escherichia coli serine chemoreceptor. J Bacteriol 176: 6340-6348.
4. Ames, P., Yu, Y.A., and Parkinson, J.S. (1996) Methylation segments are not required for chemotactic signalling by cytoplasmic fragments of Tsr, the methyl-accepting serine chemoreceptor of Escherichia coli. Mol Microbiol 19: 737-746.
5. 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.
6. Ames, P., Zhou, Q., and Parkinson, J.S. (2008) Mutational analysis of the connector segment in the HAMP domain of Tsr, the Escherichia coli serine chemoreceptor. J Bacteriol 190: 6676-6685.
7. Appleman, J.A., and Stewart, V. (2003) Mutational analysis of a conserved signal-transducing element: the HAMP linker of the Escherichia coli nitrate sensor NarX. J Bacteriol 185: 89-97.
8. Aravind, L., and Ponting, C.P. (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176: 111-116.
9. 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.
10. Bolivar, F., Rodriguez, R., Greene, P.J., Betlach, M.C., Heyneker, H.L., and Boyer, H.W. (1977) Construction and characterization of new cloning vehicles. Gene 2: 95-113.
11. Briegel, A., Ames, P., Gumbart, J.C., Oikonomou, C.M., Parkinson, J.S., and Jensen, G.J. (2013) The mobility of two kinase domains in the Escherichia coli chemoreceptor array varies with signalling state. Mol Microbiol 89: 831-841.
12. Buron-Barral, M., Gosink, K.K., and Parkinson, J.S. (2006) Loss- and gain-of-function mutations in the F1-HAMP region of the Escherichia coli aerotaxis transducer Aer. J Bacteriol 188: 3477-3486.
13. Butler, S.L., and Falke, J.J. (1998) Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor. Biochemistry 37: 10746-10756.
14. Cantwell, B.J., Draheim, R.R., Weart, R.B., Nguyen, C., Stewart, R.C., and Manson, M.D. (2003) CheZ phosphatase localizes to chemoreceptor patches via CheA-short. J Bacteriol 185: 2354-2361.
15. Chang, A.C.Y., and Cohen, S.N. (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the p15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
16. Ferris, H.U., Dunin-Horkawicz, S., Mondejar, L.G., Hulko, M., Hantke, K., Martin, J., etal. (2011) The mechanisms of HAMP-mediated signaling in transmembrane receptors. Structure 19: 378-385.
17. Gosink, K.K., Zhao, Y., and Parkinson, J.S. (2011) Mutational analysis of N381, a key trimer contact residue in Tsr, the Escherichia coli serine chemoreceptor. J Bacteriol 193: 6452-6460.
18. Hazelbauer, G.L., and Lai, W.C. (2010) Bacterial chemoreceptors: providing enhanced features to two-component signaling. Curr Opin Microbiol 13: 124-132.
19. 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.
20. Hulko, M., Berndt, F., Gruber, M., Linder, J.U., Truffault, V., Schultz, A., etal. (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126: 929-940.
21. Kentner, D., Thiem, S., Hildenbeutel, M., and Sourjik, V. (2006) Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 61: 407-417.
22. Laemmli, U.K. (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680-685.
23. Mondejar, L.G., Lupas, A., Schultz, A., and Schultz, J.E. (2012) HAMP domain-mediated signal transduction probed with a mycobacterial adenylyl cyclase as a reporter. J Biol Chem 287: 1022-1031.
24. Mowery, P., Ostler, J.B., and Parkinson, J.S. (2008) Different signaling roles of two conserved residues in the cytoplasmic hairpin tip of Tsr, the Escherichia coli serine chemoreceptor. J Bacteriol 190: 8065-8074.
25. Parkinson, J.S. (1976) cheA, cheB, and cheC genes of Escherichia coli and their role in chemotaxis. J Bacteriol 126: 758-770.
26. Parkinson, J.S. (2010) Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases. Annu Rev Microbiol 64: 101-122.
27. Parkinson, J.S., and Houts, S.E. (1982) Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions. J Bacteriol 151: 106-113.
28. Shiomi, D., Zhulin, I.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.
29. Slocum, M.K., and Parkinson, J.S. (1985) Genetics of methyl-accepting chemotaxis proteins in Escherichia coli: null phenotypes of the tar and tap genes. J Bacteriol 163: 586-594.
30. Smith, R.A., and Parkinson, J.S. (1980) Overlapping genes at the cheA locus of Escherichia coli. Proc Natl Acad Sci USA 77: 5370-5374.
31. 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.
32. Starrett, D.J., and Falke, J.J. (2005) Adaptation mechanism of the aspartate receptor: electrostatics of the adaptation subdomain play a key role in modulating kinase activity. Biochemistry 44: 1550-1560.
33. Stewart, V., and Chen, L.L. (2010) The S helix mediates signal transmission as a HAMP domain coiled-coil extension in the NarX nitrate sensor from Escherichia coli K-12. J Bacteriol 192: 734-745.
34. Studdert, C.A., and Parkinson, J.S. (2004) Crosslinking snapshots of bacterial chemoreceptor squads. Proc Natl Acad Sci USA 101: 2117-2122.
35. Studdert, C.A., and Parkinson, J.S. (2005) Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc Natl Acad Sci USA 102: 15623-15628.
36. Swain, K.E., and Falke, J.J. (2007) Structure of the conserved HAMP domain in an intact, membrane-bound chemoreceptor: a disulfide mapping study. Biochemistry 46: 13684-13695.
37. Swain, K.E., Gonzalez, M.A., and Falke, J.J. (2009) Engineered socket study of signaling through a four-helix bundle: evidence for a yin-yang mechanism in the kinase control module of the aspartate receptor. Biochemistry 48: 9266-9277.
38. Watts, K.J., Johnson, M.S., and Taylor, B.L. (2008) Structure-function relationships in the HAMP and proximal signaling domains of the aerotaxis receptor Aer. J Bacteriol 190: 2118-2127.
39. Watts, K.J., Johnson, M.S., and Taylor, B.L. (2011) Different conformations of the kinase-on and kinase-off signaling states in the Aer HAMP domain. J Bacteriol 193: 4095-4103.
40. Williams, S.B., and Stewart, V. (1999) Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction. Mol Microbiol 33: 1093-1102.
41. Winston, S.E., Mehan, R., and Falke, J.J. (2005) Evidence that the adaptation region of the aspartate receptor is a dynamic four-helix bundle: cysteine and disulfide scanning studies. Biochemistry 44: 12655-12666.
42. Wu, J., Li, J., Li, G., Long, D.G., and Weis, R.M. (1996) The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 35: 4984-4993.
43. 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.
44. 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.