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A distal arginine in oxygen-sensing heme-PAS domains is essential to ligand binding, signal transduction, and structure.

Dunham CM, Dioum EM, Tuckerman JR, Gonzalez G, Scott WG, Gilles-Gonzalez MA
Biochemistry 42 7701-8 (2003)
Cited: 37 times
EuropePMC logo PMID: 12820879

Abstract

To evaluate the contributions of the G(beta)-2 arginine to signal transduction in oxygen-sensing heme-PAS domains, we replaced this residue with alanine in Bradyrhizobium japonicum FixL and examined the results on heme-domain structure, ligand binding, and kinase regulation. In the isolated R220A BjFixL heme-PAS domain, the iron-histidine bond was increased in length by 0.31 A, the heme flattened even without a ligand, and the interaction of a presumed regulatory loop (the FG loop) with the helix of heme attachment was weakened. Binding of carbon monoxide was similar for ferrous BjFixL and R220A BjFixL. In contrast, the level of binding of oxygen was dramatically lower (K(d) approximately 1.5 mM) for R220A BjFixL, and this was manifested as 60- and 3-fold lower on- and off-rate constants, respectively. Binding of cyanide followed the same pattern as binding of oxygen. The catalytic activity was 3-4-fold higher in the "on-state" unliganded forms of R220A BjFixL than in the corresponding BjFixL species. Cyanide regulation of this activity was strongly impaired, but some inhibition was nevertheless preserved. Carbon monoxide and nitric oxide regulation, although weak in BjFixL, were abolished from R220A BjFixL. We conclude that the G(beta)-2 arginine assists in the binding of oxygen to BjFixL but does not accomplish this by stabilizing the oxy form. This arginine is not absolutely required for regulation, although it is important for shifting a pre-existing kinase equilibrium toward the inactive state on binding of regulatory ligands. These findings support a regulatory model in which the heme-PAS domain operates as an ensemble that couples to the kinase rather than a mechanism driven by a single central switch.

Reviews citing this publication (9)

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Articles citing this publication (28)

  1. DosT and DevS are oxygen-switched kinases in Mycobacterium tuberculosis. Sousa EH, Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA. Protein Sci 16 1708-1719 (2007)
  2. A GAF domain in the hypoxia/NO-inducible Mycobacterium tuberculosis DosS protein binds haem. Sardiwal S, Kendall SL, Movahedzadeh F, Rison SC, Stoker NG, Djordjevic S. J Mol Biol 353 929-936 (2005)
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  5. RcoM: a new single-component transcriptional regulator of CO metabolism in bacteria. Kerby RL, Youn H, Roberts GP. J Bacteriol 190 3336-3343 (2008)
  6. PAS/poly-HAMP signalling in Aer-2, a soluble haem-based sensor. Watts KJ, Taylor BL, Johnson MS. Mol Microbiol 79 686-699 (2011)
  7. The transcription regulator RcoM-2 from Burkholderia xenovorans is a cysteine-ligated hemoprotein that undergoes a redox-mediated ligand switch. Marvin KA, Kerby RL, Youn H, Roberts GP, Burstyn JN. Biochemistry 47 9016-9028 (2008)
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  9. Insights into heme-based O2 sensing from structure-function relationships in the FixL proteins. Rodgers KR, Lukat-Rodgers GS. J Inorg Biochem 99 963-977 (2005)
  10. Gas Sensing and Signaling in the PAS-Heme Domain of the Pseudomonas aeruginosa Aer2 Receptor. Garcia D, Orillard E, Johnson MS, Watts KJ. J Bacteriol 199 e00003-17 (2017)
  11. Architecture of the complete oxygen-sensing FixL-FixJ two-component signal transduction system. Wright GSA, Saeki A, Hikima T, Nishizono Y, Hisano T, Kamaya M, Nukina K, Nishitani H, Nakamura H, Yamamoto M, Antonyuk SV, Hasnain SS, Shiro Y, Sawai H. Sci Signal 11 eaaq0825 (2018)
  12. Subpicosecond oxygen trapping in the heme pocket of the oxygen sensor FixL observed by time-resolved resonance Raman spectroscopy. Kruglik SG, Jasaitis A, Hola K, Yamashita T, Liebl U, Martin JL, Vos MH. Proc Natl Acad Sci U S A 104 7408-7413 (2007)
  13. Strong ligand-protein interactions revealed by ultrafast infrared spectroscopy of CO in the heme pocket of the oxygen sensor FixL. Nuernberger P, Lee KF, Bonvalet A, Bouzhir-Sima L, Lambry JC, Liebl U, Joffre M, Vos MH. J Am Chem Soc 133 17110-17113 (2011)
  14. A proximal arginine R206 participates in switching of the Bradyrhizobium japonicum FixL oxygen sensor. Gilles-Gonzalez MA, Caceres AI, Sousa EH, Tomchick DR, Brautigam C, Gonzalez C, Machius M. J Mol Biol 360 80-89 (2006)
  15. pH dependence of cyanide binding to the ferric heme domain of the direct oxygen sensor from Escherichia coli and the effect of alkaline denaturation. Bidwai AK, Ok EY, Erman JE. Biochemistry 47 10458-10470 (2008)
  16. FxkR provides the missing link in the fixL-fixK signal transduction cascade in Rhizobium etli CFN42. Zamorano-Sánchez D, Reyes-González A, Gómez-Hernández N, Rivera P, Georgellis D, Girard L. Mol Plant Microbe Interact 25 1506-1517 (2012)
  17. Mutational analysis of conserved outer sphere arginine residues of chalcone synthase. Fukuma K, Neuls ED, Ryberg JM, Suh DY, Sankawa U. J Biochem 142 731-739 (2007)
  18. Plant Bio-Wars: Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore. Castano-Duque L, Helms A, Ali JG, Luthe DS. J Chem Ecol 44 727-745 (2018)
  19. Combining protein sequence, structure, and dynamics: A novel approach for functional evolution analysis of PAS domain superfamily. Dong Z, Zhou H, Tao P. Protein Sci 27 421-430 (2018)
  20. Critical roles of Asp40 at the haem proximal side of haem-regulated phosphodiesterase from Escherichia coli in redox potential, auto-oxidation and catalytic control. Watanabe M, Kurokawa H, Yoshimura-Suzuki T, Sagami I, Shimizu T. Eur J Biochem 271 3937-3942 (2004)
  21. A globin domain in a neuronal transmembrane receptor of Caenorhabditis elegans and Ascaris suum: molecular modeling and functional properties. Tilleman L, Germani F, De Henau S, Helbo S, Desmet F, Berghmans H, Van Doorslaer S, Hoogewijs D, Schoofs L, Braeckman BP, Moens L, Fago A, Dewilde S. J Biol Chem 290 10336-10352 (2015)
  22. Outer-sphere residues influence the catalytic activity of a chalcone synthase from Polygonum cuspidatum. Shen Y, Li X, Chai T, Wang H. FEBS Open Bio 6 610-618 (2016)
  23. Role of conserved F(alpha)-helix residues in the native fold and stability of the kinase-inhibited oxy state of the oxygen-sensing FixL protein from Sinorhizobium meliloti. Reynolds MF, Ackley L, Blizman A, Lutz Z, Manoff D, Miles M, Pace M, Patterson J, Pozzessere N, Saia K, Sato R, Smith D, Tarves P, Weaver M, Sieg K, Lukat-Rodgers GS, Rodgers KR. Arch Biochem Biophys 485 150-159 (2009)
  24. The Heme-Based Oxygen Sensor Rhizobium etli FixL: Influence of Auxiliary Ligands on Heme Redox Potential and Implications on the Enzyme Activity. Honorio-Felício N, Carepo MS, de F Paulo T, de França Lopes LG, Sousa EH, Diógenes IC, Bernhardt PV. J Inorg Biochem 164 34-41 (2016)
  25. Photoacoustic characterization of protein dynamics following CO photodetachment from fully reduced bovine cytochrome c oxidase. Oertling WA, Cornellison CD, Treff NR, Watanabe J, Pressler MA, Small JR. J Inorg Biochem 101 635-643 (2007)
  26. pH dependence of cyanide and imidazole binding to the heme domains of Sinorhizobium meliloti and Bradyrhizobium japonicum FixL. Bidwai AK, Ahrendt AJ, Sullivan JS, Vitello LB, Erman JE. J Inorg Biochem 153 88-102 (2015)
  27. Origins of aging mass loss in recombinant N-terminus and C-terminus deletion mutants of the heme-PAS biosensor domain BjFixLH(140-270). Satterlee JD. J Inorg Biochem 105 609-615 (2011)
  28. Photoacoustic Calorimetry Studies of O2-Sensing FixL and (R200, I209) Variants from Sinorhizobium meliloti Reveal Conformational Changes Coupled to Ligand Photodissociation from the Heme-PAS Domain. Mokdad A, Ang E, Desciak M, Ott C, Vilbert A, Beddow O, Butuc A, Larsen RW, Reynolds MF. Biochemistry 63 116-127 (2024)


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