HAMP Domain Conformers That Propagate Opposite Signals in Bacterial Chemoreceptors

PLoS Biology

Volumn 11, Issue 2, 2013, Pages

  Airola, Michael V ^a,c   Sukomon, Nattakan ^a   Samanta, Dipanjan ^a   Borbat, Peter P ^a   Freed, Jack H ^a   Watts, Kylie J ^b   Crane, Brian R ^a  

^a Department of Obstetrics Gynecology   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HAMP DOMAIN PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; CHEMOTAXIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; GENE MUTATION; MUTANT; NONHUMAN; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; CHEMORECEPTOR CELLS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84874714706     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001479     Document Type: Article

References (40)

1. Szurmant H, White RA, Hoch JA, (2007) Sensor complexes regulating two-component signal transduction. Curr Opin Struct Biol 17: 706-715.
2. Letunic I, Doerks T, Bork P, (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40: D302-D305.
3. Parkinson JS, (2010) Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases. Annu Rev Microbiol 64: 101-122.
4. Hazelbauer GL, Falke JJ, Parkinson JS, (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33: 9-19.
5. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, et al. (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126: 929-940.
6. Ames P, Zhou Q, Parkinson JS, (2008) Mutational analysis of the connector segment in the HAMP domain of Tsr, the Escherichia coli serine chemoreceptor. J Bacteriol 190: 6676-6685.
7. Airola MV, Watts KJ, Bilwes AM, Crane BR, (2010) Structure of concatenated HAMP domains provides a mechanism for signal transduction. Structure 18: 436-448.
8. Ferris HU, Dunin-Horkawicz S, Mondéjar LG, Hulko M, Hantke K, et al. (2011) The mechanisms of HAMP-mediated signaling in transmembrane receptors. Structure 19: 378-385.
9. Ferris HU, Dunin-Horkawicz S, Hornig N, Hulko M, Martin J, et al. (2012) Mechanism of regulation of receptor histidine kinases. Structure 20: 56-66.
10. Swain KE, Falke JJ, (2007) Structure of the conserved HAMP domain in an intact, membrane-bound chemoreceptor: a disulfide mapping study. Biochemistry 46: 13684-13695.
11. Watts KJ, Johnson MS, Taylor BL, (2008) Structure-function relationships in the HAMP and proximal signaling domains of the aerotaxis receptor Aer. J Bacteriol 190: 2118-2127.
12. Falke JJ, Hazelbauer GL, (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26: 257-265.
13. Moukhametzianov R, Klare JP, Efremov R, Baeken C, Goppner A, et al. (2006) Development of the signal in sensory rhodopsin and its transfer to the cognate transducer. Nature 440: 115-119.
14. Hazelbauer GL, Lai WC, (2010) Bacterial chemoreceptors: providing enhanced features to two-component signaling. Curr Opin Microbiol 13: 124-132.
15. Chao X, Muff TJ, Park SY, Zhang S, Pollard AM, et al. (2006) A receptor-modifying deamidase in complex with a signaling phosphatase reveals reciprocal regulation. Cell 124: 561-571.
16. Zhou Q, Ames P, Parkinson JS, (2011) Biphasic control logic of HAMP domain signalling in the Escherichia coli serine chemoreceptor. Mol Microbiol 80: 596-611.
17. Dunin-Horkawicz S, Lupas AN, (2010) Comprehensive analysis of HAMP domains: implications for transmembrane signal transduction. J Mol Biol 397: 1156-1174.
18. Airola MV, Watts KJ, Crane BR, (2010) Identifying divergent HAMP domains and poly-HAMP chains. J Biol Chem 285: le7.
19. Watts KJ, Taylor BL, Johnson MS, (2011) PAS/poly-HAMP signalling in Aer-2, a soluble haem-based sensor. Mol Microbiol 79: 686-699.
20. Zhou Q, Ames P, Parkinson JS, (2009) Mutational analyses of HAMP helices suggest a dynamic bundle model of input-output signalling in chemoreceptors. Mol Microbiol 73: 801-814.
21. Linder JU, Schultz JE, (2010) Transmembrane receptor chimeras to probe HAMP domain function. Methods Enzymol 471: 115-123.
22. Mondéjar LG, Lupas A, Schultz A, Schultz JE, (2012) HAMP domain-mediated signal transduction probed with a mycobacterial adenylyl cyclase as a reporter. J Biol Chem 287: 1022-1031.
23. Stewart V, Chen LL, (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.
24. Swain KE, Gonzalez MA, Falke JJ, (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.
25. Ames P, Yu YA, Parkinson JS, (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.
26. Starrett DJ, Falke JJ, (2005) Adaptation mechanism of the aspartate receptor: electrostatics of the adaptation subdomain play a key role in modulating kinase activity. Biochemistry 44: 1550-1560.
27. Doebber M, Bordignon E, Klare JP, Holterhues J, Martell S, et al. (2008) Salt-driven equilibrium between two conformations in the HAMP domain from Natronomonas pharaonis-the language of signal transfer? J Biol Chem 283: 28691-28701.
28. Wang J, Sasaki J, Tsai A, Spudich JL, (2012) HAMP domain signal relay mechanism in a sensory rhodopsin-transducer complex. J Biol Chem 287: 21316-21325.
29. Appleman JA, Chen LL, Stewart V, (2003) Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases. J Bacteriol 185: 4872-4882.
30. Yu HS, Saw JH, Hou S, Larsen RW, Watts KJ, et al. (2002) Aerotactic responses in bacteria to photoreleased oxygen. FEMS Microbiol Lett 217: 237-242.
31. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. In: Carter CW Jr, Sweet RM, editors. Methods in enzymology, Volume 276: macromolecular crystallography, part A. pp. 307-326.
32. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
33. McRee DE, (1999) XtalView Xfit-a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125: 156-165.
34. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
35. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
36. Bhatnagar J, Borbat PP, Pollard AM, Bilwes AM, Freed JH, et al. (2010) Structure of the ternary complex formed by a chemotaxis receptor signaling domain, the CheA histidine kinase, and the coupling protein CheW as determined by pulsed dipolar ESR spectroscopy. Biochemistry 49: 3824-3841.
37. Borbat PP, Freed JH, (2007) Measuring distances by pulsed dipolar ESR spectroscopy: spin-labeled histidine kinases. Methods Enzymol 423: 52-116.
38. Park SY, Borbat PP, Gonzalez-Bonet G, Bhatnagar J, Pollard AM, et al. (2006) Reconstruction of the chemotaxis receptor-kinase assembly. Nat Struct Mol Biol 13: 400-407.
39. Chiang YW, Borbat PP, Freed JH, (2005) The determination of pair distance distributions by pulsed ESR using Tikhonov regularization. J Magn Reson 172: 279-295.
40. Chiang YW, Borbat PP, Freed JH, (2005) Maximum entropy: a complement to Tikhonov regularization for determination of pair distance distributions by pulsed ESR. J Magn Reson 177: 184-196.