Abstract
Aromatic tuning facilitates stimulus-independent modulation of receptor output. The methodology is based upon the affinity of amphipathic aromatic residues, namely Trp and Tyr, for the polar–hydrophobic interfaces found within biological membranes. Here, we describe the application of aromatic tuning within the aspartate chemoreceptor of Escherichia coli (Tar). We have also employed the method within other related proteins, such as sensor histidine kinases (SHKs), and therefore hope that other research groups find it useful to modulate signal output from their receptor of interest.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Draheim RR, Bormans AF, Lai RZ, Manson MD (2006) Tuning a bacterial chemoreceptor with protein-membrane interactions. Biochemistry 45(49):14655–14664
Norholm MH, von Heijne G, Draheim RR (2015) Forcing the issue: aromatic tuning facilitates stimulus-independent modulation of a two-component signaling circuit. ACS Synth Biol 4:474–481
Yusuf R, Draheim RR (2015) Employing aromatic tuning to modulate output from two-component signaling circuits. J Biol Eng 9:7
Lehning CE, Heidelberger JB, Reinhard J, Norholm MH et al (2017) A modular high-throughput in vivo screening platform based on chimeric bacterial receptors. ACS Synth Biol 6(7):1315–1326
Killian JA, Salemink I, de Planque MR, Lindblom G, Koeppe RE II et al (1996) Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane alpha-helical peptides: importance of hydrophobic mismatch and proposed role of tryptophans. Biochemistry 35:1037–1045
de Planque MR, Greathouse DV, Koeppe RE II, Schafer H, Marsh D et al (1998) Influence of lipid/peptide hydrophobic mismatch on the thickness of diacylphosphatidylcholine bilayers. A 2H NMR and ESR study using designed transmembrane alpha-helical peptides and gramicidin A. Biochemistry 37:9333–9345
de Planque MR, Boots JW, Rijkers DT, Liskamp RM, Greathouse DV et al (2002) The effects of hydrophobic mismatch between phosphatidylcholine bilayers and transmembrane alpha-helical peptides depend on the nature of interfacially exposed aromatic and charged residues. Biochemistry 41:8396–8404
de Planque MR, Bonev BB, Demmers JA, Greathouse DV, Koeppe RE II et al (2003) Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 42:5341–5348
Nilsson I, Saaf A, Whitley P, Gafvelin G, Waller C et al (1998) Proline-induced disruption of a transmembrane alpha-helix in its natural environment. J Mol Biol 284:1165–1175
Braun P, von Heijne G (1999) The aromatic residues Trp and Phe have different effects on the positioning of a transmembrane helix in the microsomal membrane. Biochemistry 38:9778–9782
Hessa T, Meindl-Beinker NM, Bernsel A, Kim H, Sato Y et al (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450(7172):1026–1030
Botelho SC, Enquist K, von Heijne G, Draheim RR (2015) Differential repositioning of the second transmembrane helices from E. coli Tar and EnvZ upon moving the flanking aromatic residues. Biochim Biophys Acta 1848:615–621
Draheim RR, Bormans AF, Lai RZ, Manson MD (2005) Tryptophan residues flanking the second transmembrane helix (TM2) set the signaling state of the Tar chemoreceptor. Biochemistry 44:1268–1277
Falke JJ, Hazelbauer GL (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26:257–265
Falke JJ, Erbse AH (2009) The piston rises again. Structure 17:1149–1151
Miller AS, Falke JJ (2004) Side chains at the membrane-water interface modulate the signaling state of a transmembrane receptor. Biochemistry 43:1763–1770
Isaac B, Gallagher GJ, Balazs YS, Thompson LK (2002) Site-directed rotational resonance solid-state NMR distance measurements probe structure and mechanism in the transmembrane domain of the serine bacterial chemoreceptor. Biochemistry 41:3025–3036
Hall BA, Armitage JP, Sansom MS (2011) Transmembrane helix dynamics of bacterial chemoreceptors supports a piston model of signalling. PLoS Comput Biol 7:e1002204
Wright GA, Crowder RL, Draheim RR, Manson MD (2011) Mutational analysis of the transmembrane helix 2-HAMP domain connection in the Escherichia coli aspartate chemoreceptor Tar. J Bacteriol 193:82–90
Adase CA, Draheim RR, Manson MD (2012) The residue composition of the aromatic anchor of the second transmembrane helix determines the signaling properties of the aspartate/maltose chemoreceptor Tar of Escherichia coli. Biochemistry 51:1925–1932
Adase CA, Draheim RR, Rueda G, Desai R, Manson MD (2013) Residues at the cytoplasmic end of transmembrane helix 2 determine the signal output of the TarEc chemoreceptor. Biochemistry 52:2729–2738
Berg HC, Block SM (1984) A miniature flow cell designed for rapid exchange of media under high-power microscope objectives. J Gen Microbiol 130:2915–2920
Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580
Ward SM, Delgado A, Gunsalus RP, Manson MD (2002) A NarX-Tar chimera mediates repellent chemotaxis to nitrate and nitrite. Mol Microbiol 44:709–719
Heininger A, Yusuf R, Lawrence R, Draheim RR (2016) Identification of transmembrane helix 1 (TM1) surfaces important for EnvZ signalling and dimerisation. Biochim Biophys Acta 1858:1868–1875
Lai RZ, Bormans AF, Draheim RR, Wright GA, Manson MD (2008) The region preceding the C-terminal NWETF pentapeptide modulates baseline activity and aspartate inhibition of Escherichia coli Tar. Biochemistry 47:13287–13295
Cohen SN, Chang AC, Hsu L (1972) Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A 69:2110–2114
Kuwajima G (1988) Construction of a minimum-size functional flagellin of Escherichia coli. J Bacteriol 170:3305–3309
Nyholm TK, Ozdirekcan S, Killian JA (2007) How protein transmembrane segments sense the lipid environment. Biochemistry 46:1457–1465
Acknowledgment
R.Y. was generously supported by the Indonesia Endowment Fund for Education, Ministry of Finance (S-4833/LPDP.3/2015). R.J.L. and L.V.E. received support from the University of Portsmouth. R.R.D. was supported with start-up funding from the Faculty of Science and from the Institute of Biological and Biomolecular Science (IBBS) at the University of Portsmouth.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Science+Business Media, LLC
About this protocol
Cite this protocol
Yusuf, R., Lawrence, R.J., Eke, L.V., Draheim, R.R. (2018). Tuning Chemoreceptor Signaling by Positioning Aromatic Residues at the Lipid–Aqueous Interface. In: Manson, M. (eds) Bacterial Chemosensing. Methods in Molecular Biology, vol 1729. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7577-8_14
Download citation
DOI: https://doi.org/10.1007/978-1-4939-7577-8_14
Published:
Publisher Name: Humana Press, New York, NY
Print ISBN: 978-1-4939-7576-1
Online ISBN: 978-1-4939-7577-8
eBook Packages: Springer Protocols