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Axial helix rotation as a mechanism for signal regulation inferred from the crystallographic analysis of the E. coli serine chemoreceptor.

Ferris HU, Zeth K, Hulko M, Dunin-Horkawicz S, Lupas AN
J Struct Biol 186 349-56 (2014)
Cited: 39 times
EuropePMC logo PMID: 24680785

Abstract

Bacterial chemotaxis receptors are elongated homodimeric coiled-coil bundles, which transduce signals generated in an N-terminal sensor domain across 15-20nm to a conserved C-terminal signaling subdomain. This signal transduction regulates the activity of associated kinases, altering the behavior of the flagellar motor and hence cell motility. Signaling is in turn modulated by selective methylation and demethylation of specific glutamate and glutamine residues in an adaptation subdomain. We have determined the structure of a chimeric protein, consisting of the HAMP domain from Archaeoglobus fulgidus Af1503 and the methyl-accepting domain of Escherichia coli Tsr. It shows a 21nm coiled coil that alternates between two coiled-coil packing modes: canonical knobs-into-holes and complementary x-da, a variant form related to the canonical one by axial rotation of the helices. Comparison of the obtained structure to the Thermotoga maritima chemoreceptor TM1143 reveals that they adopt different axial rotation states in their adaptation subdomains. This conformational change is presumably induced by the upstream HAMP domain and may modulate the affinity of the chemoreceptor to the methylation-demethylation system. The presented findings extend the cogwheel model for signal transmission to chemoreceptors.

Reviews - 3zx6 mentioned but not cited (1)

  1. Decoding the chemotactic signal. Thomas MA, Kleist AB, Volkman BF. J Leukoc Biol 104 359-374 (2018)

Articles - 3zx6 mentioned but not cited (9)

  1. The 3.2 Å resolution structure of a receptor: CheA:CheW signaling complex defines overlapping binding sites and key residue interactions within bacterial chemosensory arrays. Li X, Fleetwood AD, Bayas C, Bilwes AM, Ortega DR, Falke JJ, Zhulin IB, Crane BR. Biochemistry 52 3852-3865 (2013)
  2. In Situ Conformational Changes of the Escherichia coli Serine Chemoreceptor in Different Signaling States. Yang W, Cassidy CK, Ames P, Diebolder CA, Schulten K, Luthey-Schulten Z, Parkinson JS, Briegel A. mBio 10 e00973-19 (2019)
  3. Repurposing a chemosensory macromolecular machine. Ortega DR, Yang W, Subramanian P, Mann P, Kjær A, Chen S, Watts KJ, Pirbadian S, Collins DA, Kooger R, Kalyuzhnaya MG, Ringgaard S, Briegel A, Jensen GJ. Nat Commun 11 2041 (2020)
  4. Differential backbone dynamics of companion helices in the extended helical coiled-coil domain of a bacterial chemoreceptor. Bartelli NL, Hazelbauer GL. Protein Sci 24 1764-1776 (2015)
  5. Deciphering the Che2 chemosensory pathway and the roles of individual Che2 proteins from Pseudomonas aeruginosa. Orillard E, Watts KJ. Mol Microbiol 115 222-237 (2021)
  6. Methyltransferase CheR binds to its chemoreceptor substrates independent of their signaling conformation yet modifies them differentially. Li M, Hazelbauer GL. Protein Sci 29 443-454 (2020)
  7. Class III Histidine Kinases: a Recently Accessorized Kinase Domain in Putative Modulators of Type IV Pilus-Based Motility. Adebali O, Petukh MG, Reznik AO, Tishkov AV, Upadhyay AA, Zhulin IB. J Bacteriol 199 e00218-17 (2017)
  8. Concerted Differential Changes of Helical Dynamics and Packing upon Ligand Occupancy in a Bacterial Chemoreceptor. Gordon JB, Hoffman MC, Troiano JM, Li M, Hazelbauer GL, Schlau-Cohen GS. ACS Chem Biol 16 2472-2480 (2021)
  9. AlphaFold2 captures the conformational landscape of the HAMP signaling domain. Winski A, Ludwiczak J, Orlowska M, Madaj R, Kaminski K, Dunin-Horkawicz S. Protein Sci 33 e4846 (2024)


Reviews citing this publication (10)

  1. Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. Parkinson JS, Hazelbauer GL, Falke JJ. Trends Microbiol 23 257-266 (2015)
  2. Coiled Coils - A Model System for the 21st Century. Lupas AN, Bassler J. Trends Biochem Sci 42 130-140 (2017)
  3. Activation of transmembrane cell-surface receptors via a common mechanism? The "rotation model". Maruyama IN. Bioessays 37 959-967 (2015)
  4. The Structure and Topology of α-Helical Coiled Coils. Lupas AN, Bassler J, Dunin-Horkawicz S. Subcell Biochem 82 95-129 (2017)
  5. Bacterial chemoreceptors and chemoeffectors. Bi S, Lai L. Cell Mol Life Sci 72 691-708 (2015)
  6. Architecture and signal transduction mechanism of the bacterial chemosensory array: progress, controversies, and challenges. Falke JJ, Piasta KN. Curr Opin Struct Biol 29 85-94 (2014)
  7. Signal transduction in photoreceptor histidine kinases. Möglich A. Protein Sci 28 1923-1946 (2019)
  8. Transmembrane Signal Transduction in Two-Component Systems: Piston, Scissoring, or Helical Rotation? Gushchin I, Gordeliy V. Bioessays 40 (2018)
  9. Intraprotein signal transduction by HAMP domains: a balancing act. Schultz JE, Kanchan K, Ziegler M. Int J Med Microbiol 305 243-251 (2015)
  10. Recent structural advances in bacterial chemotaxis signalling. Riechmann C, Zhang P. Curr Opin Struct Biol 79 102565 (2023)

Articles citing this publication (19)

  1. The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis. Alva V, Nam SZ, Söding J, Lupas AN. Nucleic Acids Res 44 W410-5 (2016)
  2. Transmembrane protein sorting driven by membrane curvature. Strahl H, Ronneau S, González BS, Klutsch D, Schaffner-Barbero C, Hamoen LW. Nat Commun 6 8728 (2015)
  3. Both piston-like and rotational motions are present in bacterial chemoreceptor signaling. Yu D, Ma X, Tu Y, Lai L. Sci Rep 5 8640 (2015)
  4. Bacterial Chemoreceptor Dynamics: Helical Stability in the Cytoplasmic Domain Varies with Functional Segment and Adaptational Modification. Bartelli NL, Hazelbauer GL. J Mol Biol 428 3789-3804 (2016)
  5. Inverted signaling by bacterial chemotaxis receptors. Bi S, Jin F, Sourjik V. Nat Commun 9 2927 (2018)
  6. STAC--A New Domain Associated with Transmembrane Solute Transport and Two-Component Signal Transduction Systems. Korycinski M, Albrecht R, Ursinus A, Hartmann MD, Coles M, Martin J, Dunin-Horkawicz S, Lupas AN. J Mol Biol 427 3327-3339 (2015)
  7. Light-induced switching of HAMP domain conformation and dynamics revealed by time-resolved EPR spectroscopy. Klose D, Voskoboynikova N, Orban-Glass I, Rickert C, Engelhard M, Klare JP, Steinhoff HJ. FEBS Lett 588 3970-3976 (2014)
  8. Transmembrane Helices Tilt, Bend, Slide, Torque, and Unwind between Functional States of Rhodopsin. Ren Z, Ren PX, Balusu R, Yang X. Sci Rep 6 34129 (2016)
  9. Structure and Function of the Transmembrane Domain of NsaS, an Antibiotic Sensing Histidine Kinase in Staphylococcus aureus. Bhate MP, Lemmin T, Kuenze G, Mensa B, Ganguly S, Peters JM, Schmidt N, Pelton JG, Gross CA, Meiler J, DeGrado WF. J Am Chem Soc 140 7471-7485 (2018)
  10. Signaling and Adaptation Modulate the Dynamics of the Photosensoric Complex of Natronomonas pharaonis. Orekhov PS, Klose D, Mulkidjanian AY, Shaitan KV, Engelhard M, Klare JP, Steinhoff HJ. PLoS Comput Biol 11 e1004561 (2015)
  11. Stability and Conformation of a Chemoreceptor HAMP Domain Chimera Correlates with Signaling Properties. Sukomon N, Widom J, Borbat PP, Freed JH, Crane BR. Biophys J 112 1383-1395 (2017)
  12. Conformational shifts in a chemoreceptor helical hairpin control kinase signaling in Escherichia coli. Gao Q, Cheng A, Parkinson JS. Proc Natl Acad Sci U S A 116 15651-15660 (2019)
  13. Differential repositioning of the second transmembrane helices from E. coli Tar and EnvZ upon moving the flanking aromatic residues. Botelho SC, Enquist K, von Heijne G, Draheim RR. Biochim Biophys Acta 1848 615-621 (2015)
  14. Methylatable Signaling Helix Coordinated Inhibitory Receiver Domain in Sensor Kinase Modulates Environmental Stress Response in Bacillus Cereus. Chen JC, Liu JH, Hsu DW, Shu JC, Chen CY, Chen CC. PLoS One 10 e0137952 (2015)
  15. Structural signatures of Escherichia coli chemoreceptor signaling states revealed by cellular crosslinking. Flack CE, Parkinson JS. Proc Natl Acad Sci U S A 119 e2204161119 (2022)
  16. Protein design-scapes generated by microfluidic DNA assembly elucidate domain coupling in the bacterial histidine kinase CpxA. Clark IC, Mensa B, Ochs CJ, Schmidt NW, Mravic M, Quintana FJ, DeGrado WF, Abate AR. Proc Natl Acad Sci U S A 118 e2017719118 (2021)
  17. Conformational sampling of CpxA: Connecting HAMP motions to the histidine kinase function. Duclert-Savatier N, Bouvier G, Nilges M, Malliavin TE. PLoS One 13 e0207899 (2018)
  18. Employing aromatic tuning to modulate output from two-component signaling circuits. Yusuf R, Draheim RR. J Biol Eng 9 7 (2015)
  19. Structure of the native chemotaxis core signaling unit from phage E-protein lysed E. coli cells. Cassidy CK, Qin Z, Frosio T, Gosink K, Yang Z, Sansom MSP, Stansfeld PJ, Parkinson JS, Zhang P. mBio e0079323 (2023)


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