Skip to main content
SpringerLink
Log in

Manipulation of Bacterial Signaling Using Engineered Histidine Kinases

  • Protocol
  • First Online:
Histidine Phosphorylation

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2077))

Abstract

Two-component systems allow bacteria to respond to changes in environmental or cytosolic conditions through autophosphorylation of a histidine kinase (HK) and subsequent transfer of the phosphate group to its downstream cognate response regulator (RR). The RR then elicits a cellular response, commonly through regulation of transcription. Engineering two-component system signaling networks provides a strategy to study bacterial signaling mechanisms related to bacterial cell survival, symbiosis, and virulence, and to develop sensory devices in synthetic biology. Here we focus on the principles for engineering the HK to identify unknown signal inputs, test signal transmission mechanisms, design small molecule sensors, and rewire two-component signaling networks.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Gao R, Stock AM (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63:133–154. https://doi.org/10.1146/annurev.micro.091208.073214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Zschiedrich CP, Keidel V, Szurmant H (2016) Molecular mechanisms of two-component signal transduction. J Mol Biol 428(19):3752–3775. https://doi.org/10.1016/j.jmb.2016.08.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188(12):4169–4182. https://doi.org/10.1128/JB.01887-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lin YH, Pierce BD, Fang F, Wise A, Binns AN, Lynn DG (2014) Role of the VirA histidine autokinase of Agrobacterium tumefaciens in the initial steps of pathogenesis. Front Plant Sci 5:195. https://doi.org/10.3389/fpls.2014.00195

    Article  PubMed  PubMed Central  Google Scholar 

  5. Matamouros S, Hager KR, Miller SI (2015) HAMP domain rotation and tilting movements associated with signal transduction in the PhoQ sensor kinase. MBio 6(3):e00616–e00615. https://doi.org/10.1128/mBio.00616-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Schultz JE, Kanchan K, Ziegler M (2015) Intraprotein signal transduction by HAMP domains: a balancing act. Int J Med Microbiol 305(2):243–251. https://doi.org/10.1016/j.ijmm.2014.12.007

    Article  CAS  PubMed  Google Scholar 

  7. Diensthuber RP, Bommer M, Gleichmann T, Moglich A (2013) Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators. Structure 21(7):1127–1136. https://doi.org/10.1016/j.str.2013.04.024

    Article  CAS  PubMed  Google Scholar 

  8. Lesne E, Dupre E, Lensink MF, Locht C, Antoine R, Jacob-Dubuisson F (2018) Coiled-coil antagonism regulates activity of venus flytrap-domain-containing sensor kinases of the BvgS family. mBio 9(1):e02052–e02017. https://doi.org/10.1128/mBio.02052-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wang B, Zhao A, Novick RP, Muir TW (2014) Activation and inhibition of the receptor histidine kinase AgrC occurs through opposite helical transduction motions. Mol Cell 53(6):929–940. https://doi.org/10.1016/j.molcel.2014.02.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Marina A, Waldburger CD, Hendrickson WA (2005) Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24(24):4247–4259. https://doi.org/10.1038/sj.emboj.7600886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Albanesi D, Martin M, Trajtenberg F, Mansilla MC, Haouz A, Alzari PM, de Mendoza D, Buschiazzo A (2009) Structural plasticity and catalysis regulation of a thermosensor histidine kinase. Proc Natl Acad Sci U S A 106(38):16185–16190. https://doi.org/10.1073/pnas.0906699106

    Article  PubMed  PubMed Central  Google Scholar 

  12. Ferris HU, Zeth K, Hulko M, Dunin-Horkawicz S, Lupas AN (2014) Axial helix rotation as a mechanism for signal regulation inferred from the crystallographic analysis of the E. coli serine chemoreceptor. J Struct Biol 186(3):349–356. https://doi.org/10.1016/j.jsb.2014.03.015

    Article  CAS  PubMed  Google Scholar 

  13. Wang C, Sang J, Wang J, Su M, Downey JS, Wu Q, Wang S, Cai Y, Xu X, Wu J, Senadheera DB, Cvitkovitch DG, Chen L, Goodman SD, Han A (2013) Mechanistic insights revealed by the crystal structure of a histidine kinase with signal transducer and sensor domains. PLoS Biol 11(2):e1001493. https://doi.org/10.1371/journal.pbio.1001493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Mechaly AE, Sassoon N, Betton JM, Alzari PM (2014) Segmental helical motions and dynamical asymmetry modulate histidine kinase autophosphorylation. PLoS Biol 12(1):e1001776. https://doi.org/10.1371/journal.pbio.1001776

    Article  PubMed  PubMed Central  Google Scholar 

  15. Szurmant H, Bu L, Brooks CL 3rd, Hoch JA (2008) An essential sensor histidine kinase controlled by transmembrane helix interactions with its auxiliary proteins. Proc Natl Acad Sci U S A 105(15):5891–5896. https://doi.org/10.1073/pnas.0800247105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Goldberg SD, Clinthorne GD, Goulian M, DeGrado WF (2010) Transmembrane polar interactions are required for signaling in the Escherichia coli sensor kinase PhoQ. Proc Natl Acad Sci U S A 107(18):8141–8146. https://doi.org/10.1073/pnas.1003166107

    Article  PubMed  PubMed Central  Google Scholar 

  17. Utsumi R, Brissette RE, Rampersaud A, Forst SA, Oosawa K, Inouye M (1989) Activation of bacterial porin gene-expression by a chimeric signal transducer in response to aspartate. Science 245(4923):1246–1249. https://doi.org/10.1126/Science.2476847

    Article  CAS  PubMed  Google Scholar 

  18. Moglich A, Ayers RA, Moffat K (2009) Design and signaling mechanism of light-regulated histidine kinases. J Mol Biol 385(5):1433–1444. https://doi.org/10.1016/j.jmb.2008.12.017

    Article  CAS  PubMed  Google Scholar 

  19. Iniesta AA, Hillson NJ, Shapiro L (2010) Cell pole-specific activation of a critical bacterial cell cycle kinase. Proc Natl Acad Sci U S A 107(15):7012–7017. https://doi.org/10.1073/pnas.1001767107

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lopez D, Fischbach MA, Chu F, Losick R, Kolter R (2009) Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc Natl Acad Sci U S A 106(1):280–285. https://doi.org/10.1073/pnas.0810940106

    Article  PubMed  Google Scholar 

  21. Ganesh I, Ravikumar S, Lee SH, Park SJ, Hong SH (2013) Engineered fumarate sensing Escherichia coli based on novel chimeric two-component system. J Biotechnol 168(4):560–566. https://doi.org/10.1016/j.jbiotec.2013.09.003

    Article  CAS  PubMed  Google Scholar 

  22. Ganesh I, Ravikumar S, Yoo IK, Hong SH (2015) Construction of malate-sensing Escherichia coli by introduction of a novel chimeric two-component system. Bioprocess Biosyst Eng 38(4):797–804. https://doi.org/10.1007/s00449-014-1321-3

    Article  CAS  PubMed  Google Scholar 

  23. Ashenberg O, Rozen-Gagnon K, Laub MT, Keating AE (2011) Determinants of homodimerization specificity in histidine kinases. J Mol Biol 413(1):222–235. https://doi.org/10.1016/j.jmb.2011.08.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Skerker JM, Perchuk BS, Siryaporn A, Lubin EA, Ashenberg O, Goulian M, Laub MT (2008) Rewiring the specificity of two-component signal transduction systems. Cell 133(6):1043–1054. https://doi.org/10.1016/j.cell.2008.04.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Whitaker WR, Davis SA, Arkin AP, Dueber JE (2012) Engineering robust control of two-component system phosphotransfer using modular scaffolds. Proc Natl Acad Sci U S A 109(44):18090–18095. https://doi.org/10.1073/pnas.1209230109

    Article  PubMed  PubMed Central  Google Scholar 

  26. Krikos A, Conley MP, Boyd A, Berg HC, Simon MI (1985) Chimeric chemosensory transducers of Escherichia coli. Proc Natl Acad Sci U S A 82(5):1326–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Jin T, Inouye M (1994) Mutational analysis of the cytoplasmic linker region of Taz1-1, a Tar-Envz chimeric receptor in Escherichia coli. J Mol Biol 244(5):477–481. https://doi.org/10.1006/Jmbi.1994.1746

    Article  CAS  PubMed  Google Scholar 

  28. Zhu Y, Inouye M (2003) Analysis of the role of the EnvZ linker region in signal transduction using a chimeric Tar/EnvZ receptor protein, Tez1. J Biol Chem 278(25):22812–22819. https://doi.org/10.1074/jbc.M300916200

    Article  CAS  PubMed  Google Scholar 

  29. Moglich A, Ayers RA, Moffat K (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17(10):1282–1294. https://doi.org/10.1016/j.str.2009.08.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Harper SM, Christie JM, Gardner KH (2004) Disruption of the LOV-Jalpha helix interaction activates phototropin kinase activity. Biochemistry 43(51):16184–16192. https://doi.org/10.1021/bi048092i

    Article  CAS  PubMed  Google Scholar 

  31. Crosson S, Rajagopal S, Moffat K (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42(1):2–10. https://doi.org/10.1021/bi026978l

    Article  CAS  PubMed  Google Scholar 

  32. Bury A, Hellingwerf KJ (2018) Design, characterization and in vivo functioning of a light-dependent histidine protein kinase in the yeast Saccharomyces cerevisiae. AMB Express 8(1):53. https://doi.org/10.1186/s13568-018-0582-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Shivaji S, Prakash JS (2010) How do bacteria sense and respond to low temperature? Arch Microbiol 192(2):85–95. https://doi.org/10.1007/s00203-009-0539-y

    Article  CAS  PubMed  Google Scholar 

  34. Draheim RR, Bormans AF, Lai RZ, Manson MD (2006) Tuning a bacterial chemoreceptor with protein-membrane interactions. Biochemistry 45(49):14655–14664. https://doi.org/10.1021/bi061259i

    Article  CAS  PubMed  Google Scholar 

  35. 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(4):474–481. https://doi.org/10.1021/sb500261t

    Article  CAS  PubMed  Google Scholar 

  36. Lehning CE, Heidelberger JB, Reinhard J, Norholm MHH, Draheim RR (2017) A modular high-throughput in vivo screening platform based on chimeric bacterial receptors. ACS Synth Biol 6(7):1315–1326. https://doi.org/10.1021/acssynbio.6b00288

    Article  CAS  PubMed  Google Scholar 

  37. de Planque MR, Boots JW, Rijkers DT, Liskamp RM, Greathouse DV, Killian JA (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(26):8396–8404

    Article  PubMed  Google Scholar 

  38. de Planque MR, Goormaghtigh E, Greathouse DV, Koeppe RE 2nd, Kruijtzer JA, Liskamp RM, de Kruijff B, Killian JA (2001) Sensitivity of single membrane-spanning alpha-helical peptides to hydrophobic mismatch with a lipid bilayer: effects on backbone structure, orientation, and extent of membrane incorporation. Biochemistry 40(16):5000–5010

    Article  PubMed  Google Scholar 

  39. Crosson S, McGrath PT, Stephens C, McAdams HH, Shapiro L (2005) Conserved modular design of an oxygen sensory/signaling network with species-specific output. Proc Natl Acad Sci U S A 102(22):8018–8023. https://doi.org/10.1073/pnas.0503022102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ravikumar S, David Y, Park SJ, Choi JI (2018) A chimeric two-component regulatory system-based Escherichia coli biosensor engineered to detect glutamate. Appl Biochem Biotechnol 186:335–349. https://doi.org/10.1007/s12010-018-2746-y

    Article  CAS  PubMed  Google Scholar 

  41. Selvamani V, Ganesh I, Maruthamuthu MK, Eom GT, Hong SH (2017) Engineering chimeric two-component system into Escherichia coli from Paracoccus denitrificans to sense methanol. Biotechnol Bioproc E 22(3):225–230. https://doi.org/10.1007/s12257-016-0484-y

    Article  CAS  Google Scholar 

  42. Tabor JJ, Levskaya A, Voigt CA (2011) Multichromatic control of gene expression in Escherichia coli. J Mol Biol 405(2):315–324. https://doi.org/10.1016/j.jmb.2010.10.038

    Article  CAS  PubMed  Google Scholar 

  43. Daeffler KN, Galley JD, Sheth RU, Ortiz-Velez LC, Bibb CO, Shroyer NF, Britton RA, Tabor JJ (2017) Engineering bacterial thiosulfate and tetrathionate sensors for detecting gut inflammation. Mol Syst Biol 13(4):923. https://doi.org/10.15252/msb.20167416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Schrader J, Schilling M, Holtmann D, Sell D, Filho MV, Marx A, Vorholt JA (2009) Methanol-based industrial biotechnology: current status and future perspectives of methylotrophic bacteria. Trends Biotechnol 27(2):107–115. https://doi.org/10.1016/j.tibtech.2008.10.009

    Article  CAS  PubMed  Google Scholar 

  45. Ziolkowska JR (2014) Prospective technologies, feedstocks and market innovations for ethanol and biodiesel production in the US. Biotechnol Rep 4:94–98. https://doi.org/10.1016/j.btre.2014.09.001

    Article  Google Scholar 

  46. Ang J, Harris E, Hussey BJ, Kil R, McMillen DR (2013) Tuning response curves for synthetic biology. ACS Synth Biol 2(10):547–567. https://doi.org/10.1021/sb4000564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Batchelor E, Goulian M (2003) Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. Proc Natl Acad Sci U S A 100(2):691–696. https://doi.org/10.1073/pnas.0234782100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Landry BP, Palanki R, Dyulgyarov N, Hartsough LA, Tabor JJ (2018) Phosphatase activity tunes two-component system sensor detection threshold. Nat Commun 9(1):1433. https://doi.org/10.1038/s41467-018-03929-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Huynh TN, Noriega CE, Stewart V (2010) Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX. Proc Natl Acad Sci U S A 107(49):21140–21145. https://doi.org/10.1073/pnas.1013081107

    Article  PubMed  PubMed Central  Google Scholar 

  50. Huynh TN, Noriega CE, Stewart V (2013) Missense substitutions reflecting regulatory control of transmitter phosphatase activity in two-component signalling. Mol Microbiol 88(3):459–472. https://doi.org/10.1111/mmi.12195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Casino P, Rubio V, Marina A (2009) Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell 139(2):325–336. https://doi.org/10.1016/j.cell.2009.08.032

    Article  CAS  PubMed  Google Scholar 

  52. Zhu Y, Inouye M (2002) The role of the G2 box, a conserved motif in the histidine kinase superfamily, in modulating the function of EnvZ. Mol Microbiol 45(3):653–663

    Article  CAS  PubMed  Google Scholar 

  53. Sutton MA, Howard CM, Erisman JW, Billen G, Bleeker A, Grennfelt P, Van Grinsven H, Grizzetti B (2011) The European nitrogen assessment: sources, effects and policy perspectives. Cambridge University Press, Leiden

    Book  Google Scholar 

  54. Smanski MJ, Bhatia S, Zhao D, Park Y, Woodruff LBA, Giannoukos G, Ciulla D, Busby M, Calderon J, Nicol R, Gordon DB, Densmore D, Voigt CA (2014) Functional optimization of gene clusters by combinatorial design and assembly. Nat Biotechnol 32(12):1241–1249. https://doi.org/10.1038/nbt.3063

    Article  CAS  PubMed  Google Scholar 

  55. Casino P, Rubio V, Marina A (2010) The mechanism of signal transduction by two-component systems. Curr Opin Struct Biol 20(6):763–771. https://doi.org/10.1016/j.sbi.2010.09.010

    Article  CAS  PubMed  Google Scholar 

  56. Ferris HU, Dunin-Horkawicz S, Hornig N, Hulko M, Martin J, Schultz JE, Zeth K, Lupas AN, Coles M (2012) Mechanism of regulation of receptor histidine kinases. Structure 20(1):56–66. https://doi.org/10.1016/j.str.2011.11.014

    Article  CAS  PubMed  Google Scholar 

  57. Zitzewitz JA, Ibarra-Molero B, Fishel DR, Terry KL, Matthews CR (2000) Preformed secondary structure drives the association reaction of GCN4-p1, a model coiled-coil system. J Mol Biol 296(4):1105–1116. https://doi.org/10.1006/jmbi.2000.3507

    Article  CAS  PubMed  Google Scholar 

  58. Hidaka Y, Park H, Inouye M (1997) Demonstration of dimer formation of the cytoplasmic domain of a transmembrane osmosensor protein, EnvZ, of Escherichia coli using Ni-histidine tag affinity chromatography. FEBS Lett 400(2):238–242

    Article  CAS  PubMed  Google Scholar 

  59. Cochran AG, Kim PS (1996) Imitation of Escherichia coli aspartate receptor signaling in engineered dimers of the cytoplasmic domain. Science 271(5252):1113–1116

    Article  CAS  PubMed  Google Scholar 

  60. Wang Y, Gao R, Lynn DG (2002) Ratcheting up vir gene expression in Agrobacterium tumefaciens: coiled coils in histidine kinase signal transduction. Chembiochem 3(4):311–317

    Article  CAS  PubMed  Google Scholar 

  61. Gao R, Lynn DG (2007) Integration of rotation and piston motions in coiled-coil signal transduction. J Bacteriol 189(16):6048–6056. https://doi.org/10.1128/JB.00459-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wang B, Zhao A, Xie Q, Olinares PD, Chait BT, Novick RP, Muir TW (2017) Functional plasticity of the AgrC receptor histidine kinase required for staphylococcal virulence. Cell Chem Biol 24(1):76–86. https://doi.org/10.1016/j.chembiol.2016.12.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Winans SC (1992) Two-way chemical signaling in Agrobacterium-plant interactions. Microbiol Rev 56(1):12–31

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Doty SL, Yu MC, Lundin JI, Heath JD, Nester EW (1996) Mutational analysis of the input domain of the VirA protein of Agrobacterium tumefaciens. J Bacteriol 178(4):961–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. McLean BG, Greene EA, Zambryski PC (1994) Mutants of Agrobacterium VirA that activate vir gene expression in the absence of the inducer acetosyringone. J Biol Chem 269(4):2645–2651

    CAS  PubMed  Google Scholar 

  66. Reyes D, Andrey DO, Monod A, Kelley WL, Zhang G, Cheung AL (2011) Coordinated regulation by AgrA, SarA, and SarR to control agr expression in Staphylococcus aureus. J Bacteriol 193(21):6020–6031. https://doi.org/10.1128/JB.05436-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Childers WS, Xu Q, Mann TH, Mathews II, Blair JA, Deacon AM, Shapiro L (2014) Cell fate regulation governed by a repurposed bacterial histidine kinase. PLoS Biol 12(10):e1001979. https://doi.org/10.1371/journal.pbio.1001979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ozaki S, Schalch-Moser A, Zumthor L, Manfredi P, Ebbensgaard A, Schirmer T, Jenal U (2014) Activation and polar sequestration of PopA, a c-di-GMP effector protein involved in Caulobacter crescentus cell cycle control. Mol Microbiol 94(3):580–594. https://doi.org/10.1111/mmi.12777

    Article  CAS  PubMed  Google Scholar 

  69. Gao R, Lynn DG (2005) Environmental pH sensing: resolving the VirA/VirG two-component system inputs for Agrobacterium pathogenesis. J Bacteriol 187(6):2182–2189. https://doi.org/10.1128/JB.187.6.2182-2189.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Moglich A, Ayers RA, Moffat K (2010) Addition at the molecular level: signal integration in designed Per-ARNT-Sim receptor proteins. J Mol Biol 400(3):477–486. https://doi.org/10.1016/j.jmb.2010.05.019

    Article  CAS  PubMed  Google Scholar 

  71. Eswaramoorthy P, Dravis A, Devi SN, Vishnoi M, Dao HA, Fujita M (2011) Expression level of a chimeric kinase governs entry into sporulation in Bacillus subtilis. J Bacteriol 193(22):6113–6122. https://doi.org/10.1128/JB.05920-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Mann TH, Shapiro L (2018) Integration of cell cycle signals by multi-PAS domain kinases. bioRxiv. https://doi.org/10.1101/323444

  73. Eswaramoorthy P, Guo T, Fujita M (2009) In vivo domain-based functional analysis of the major sporulation sensor kinase, KinA, in Bacillus subtilis. J Bacteriol 191(17):5358–5368. https://doi.org/10.1128/JB.00503-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Rowland MA, Deeds EJ (2014) Crosstalk and the evolution of specificity in two-component signaling. Proc Natl Acad Sci U S A 111(15):5550–5555. https://doi.org/10.1073/pnas.1317178111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Chambonnier G, Roux L, Redelberger D, Fadel F, Filloux A, Sivaneson M, de Bentzmann S, Bordi C (2016) The hybrid histidine kinase LadS forms a multicomponent signal transduction system with the GacS/GacA two-component system in Pseudomonas aeruginosa. PLoS Genet 12(5):e1006032. https://doi.org/10.1371/journal.pgen.1006032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Goodman AL, Merighi M, Hyodo M, Ventre I, Filloux A, Lory S (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23(2):249–259. https://doi.org/10.1101/gad.1739009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Capra EJ, Laub MT (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66:325–347. https://doi.org/10.1146/annurev-micro-092611-150039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Atchley WR, Wollenberg KR, Fitch WM, Terhalle W, Dress AW (2000) Correlations among amino acid sites in bHLH protein domains: an information theoretic analysis. Mol Biol Evol 17(1):164–178. https://doi.org/10.1093/oxfordjournals.molbev.a026229

    Article  CAS  PubMed  Google Scholar 

  79. Fodor AA, Aldrich RW (2004) Influence of conservation on calculations of amino acid covariance in multiple sequence alignments. Proteins 56(2):211–221. https://doi.org/10.1002/prot.20098

    Article  CAS  PubMed  Google Scholar 

  80. Varughese KI, Tsigelny I, Zhao H (2006) The crystal structure of beryllofluoride Spo0F in complex with the phosphotransferase Spo0B represents a phosphotransfer pretransition state. J Bacteriol 188(13):4970–4977. https://doi.org/10.1128/JB.00160-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Podgornaia AI, Casino P, Marina A, Laub MT (2013) Structural basis of a rationally rewired protein-protein interface critical to bacterial signaling. Structure 21(9):1636–1647. https://doi.org/10.1016/j.str.2013.07.005

    Article  CAS  PubMed  Google Scholar 

  82. Bhattacharyya RP, Reményi A, Yeh BJ, Lim WA (2006) Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu Rev Biochem 75(1):655–680. https://doi.org/10.1146/annurev.biochem.75.103004.142710

    Article  CAS  PubMed  Google Scholar 

  83. Jin T, Inouye M (1993) Ligand binding to the receptor domain regulates the ratio of kinase to phosphatase activities of the signaling domain of the hybrid Escherichia coli transmembrane receptor, Taz1. J Mol Biol 232(2):484–492. https://doi.org/10.1006/jmbi.1993.1404

    Article  CAS  PubMed  Google Scholar 

  84. Skerker JM, Prasol MS, Perchuk BS, Biondi EG, Laub MT (2005) Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol 3(10):e334. https://doi.org/10.1371/journal.pbio.0030334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Townsend GE, Raghavan V, Zwir I, Groisman EA (2013) Intramolecular arrangement of sensor and regulator overcomes relaxed specificity in hybrid two-component systems. Proc Natl Acad Sci 110(2):E161–E169. https://doi.org/10.1073/pnas.1212102110

    Article  PubMed  Google Scholar 

  86. Capra EJ, Perchuk BS, Ashenberg O, Seid CA, Snow HR, Skerker JM, Laub MT (2012) Spatial tethering of kinases to their substrates relaxes evolutionary constraints on specificity. Mol Microbiol 86(6):1393–1403. https://doi.org/10.1111/mmi.12064

    Article  CAS  PubMed  Google Scholar 

  87. Tsokos CG, Perchuk BS, Laub MT (2011) A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev Cell 20(3):329–341. https://doi.org/10.1016/j.devcel.2011.01.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Eguchi Y, Okajima T, Tochio N, Inukai Y, Shimizu R, Ueda S, Shinya S, Kigawa T, Fukamizo T, Igarashi M, Utsumi R (2017) Angucycline antibiotic waldiomycin recognizes common structural motif conserved in bacterial histidine kinases. J Antibiot 70(3):251–258. https://doi.org/10.1038/ja.2016.151

    Article  CAS  Google Scholar 

  89. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612. https://doi.org/10.1002/jcc.20084

    Article  CAS  PubMed  Google Scholar 

  90. Jacobs C, Ausmees N, Cordwell SJ, Shapiro L, Laub MT (2003) Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol Microbiol 47(5):1279–1290

    Article  CAS  PubMed  Google Scholar 

  91. Cai SJ, Inouye M (2002) EnvZ-OmpR interaction and osmoregulation in Escherichia coli. J Biol Chem 277(27):24155–24161. https://doi.org/10.1074/jbc.M110715200

    Article  CAS  PubMed  Google Scholar 

  92. Gooderham WJ, Hancock RE (2009) Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev 33(2):279–294. https://doi.org/10.1111/j.1574-6976.2008.00135.x

    Article  CAS  PubMed  Google Scholar 

  93. Zimmermann L, Stephens A, Nam SZ, Rau D, Kubler J, Lozajic M, Gabler F, Soding J, Lupas AN, Alva V (2017) A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol 430:2237–2243. https://doi.org/10.1016/j.jmb.2017.12.007

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Kimberly A. Kowallis and Samuel W. Duvall contributed equally to this work.

Authors and Affiliations

  1. Department of Chemistry, University of Pittsburgh, Pittsburgh, PA, USA

    Kimberly A. Kowallis, Samuel W. Duvall, Wei Zhao & W. Seth Childers

  2. Chevron Science Center, University of Pittsburgh, Pittsburgh, PA, USA

    W. Seth Childers

Authors
  1. Kimberly A. Kowallis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samuel W. Duvall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. W. Seth Childers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to W. Seth Childers .

Editor information

Editors and Affiliations

  1. Department of Biochemistry, Centre for Proteome Research Institute of Integrative Biology, University of Liverpool, Liverpool, UK

    Claire E. Eyers

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Kowallis, K.A., Duvall, S.W., Zhao, W., Childers, W.S. (2020). Manipulation of Bacterial Signaling Using Engineered Histidine Kinases. In: Eyers, C. (eds) Histidine Phosphorylation. Methods in Molecular Biology, vol 2077. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-9884-5_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-9884-5_10

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-4939-9883-8

  • Online ISBN: 978-1-4939-9884-5

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation