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Two-component signaling in the AAA + ATPase DctD: binding Mg2+ and BeF3- selects between alternate dimeric states of the receiver domain.

Park S, Meyer M, Jones AD, Yennawar HP, Yennawar NH, Nixon BT
FASEB J 16 1964-6 (2002)
Cited: 37 times
EuropePMC logo PMID: 12368235

Abstract

A Crystallogral structure is described for the Mg2+-BeF3--bound receiver domain of Sinorhizobium meliloti DctD bearing amino acid substitution E121K. Differences between the apo- and ligand-bound active sites are similar to those reported for other receiver domains. However, the off and on states of the DctD receiver domain are characterized by dramatically different dimeric structures, which supports the following hypothesis of signal transduction. In the off state, the receiver domain and coiled-coil linker form a dimer that inhibits oligomerization of the AAA+ ATPase domain. In this conformation, the receiver domain cannot be phosphorylated or bind Mg2+ and BeF3-. Instead, these modifications stabilize an alternative dimeric conformation that repositions the subunits by approximately 20 A, thus replacing the a4-b5-a5 interface with an a4-b5 interface. Reoriented receiver domains permit the ATPase domain to oligomerize and stimulate open complex formation by the s54 form of RNA polymerase. NtrC, which shares 38% sequence identity with DctD, works differently. Its activated receiver domain must facilitate oligomerization of its ATPase domain. Significant differences exist in the signaling surfaces of the DctD and NtrC receiver domains that may help explain how triggering the common two-component switch can variously regulate assembly of a AAA+ ATPase domain.

Articles - 1l5y mentioned but not cited (7)

  1. Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Lee SY, De La Torre A, Yan D, Kustu S, Nixon BT, Wemmer DE. Genes Dev 17 2552-2563 (2003)
  2. Two variable active site residues modulate response regulator phosphoryl group stability. Thomas SA, Brewster JA, Bourret RB. Mol Microbiol 69 453-465 (2008)
  3. Matching biochemical reaction kinetics to the timescales of life: structural determinants that influence the autodephosphorylation rate of response regulator proteins. Pazy Y, Wollish AC, Thomas SA, Miller PJ, Collins EJ, Bourret RB, Silversmith RE. J Mol Biol 392 1205-1220 (2009)
  4. The aspartate-less receiver (ALR) domains: distribution, structure and function. Maule AF, Wright DP, Weiner JJ, Han L, Peterson FC, Volkman BF, Silvaggi NR, Ulijasz AT. PLoS Pathog 11 e1004795 (2015)
  5. Constitutive activation of two-component response regulators: characterization of VirG activation in Agrobacterium tumefaciens. Gao R, Mukhopadhyay A, Fang F, Lynn DG. J Bacteriol 188 5204-5211 (2006)
  6. A Variable Active Site Residue Influences the Kinetics of Response Regulator Phosphorylation and Dephosphorylation. Immormino RM, Silversmith RE, Bourret RB. Biochemistry 55 5595-5609 (2016)
  7. REC domain stabilizes the active heptamer of σ54-dependent transcription factor, FleR from Pseudomonas aeruginosa. Sahoo PK, Sheenu, Jain D. iScience 26 108397 (2023)


Reviews citing this publication (5)

  1. Bacterial response regulators: versatile regulatory strategies from common domains. Gao R, Mack TR, Stock AM. Trends Biochem Sci 32 225-234 (2007)
  2. The role of bacterial enhancer binding proteins as specialized activators of σ54-dependent transcription. Bush M, Dixon R. Microbiol Mol Biol Rev 76 497-529 (2012)
  3. Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Gao R, Stock AM. Curr Opin Microbiol 13 160-167 (2010)
  4. Structures and organisation of AAA+ enhancer binding proteins in transcriptional activation. Schumacher J, Joly N, Rappas M, Zhang X, Buck M. J Struct Biol 156 190-199 (2006)
  5. Bacterial enhancer-binding proteins: unlocking sigma54-dependent gene transcription. Rappas M, Bose D, Zhang X. Curr Opin Struct Biol 17 110-116 (2007)

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  1. Biological insights from structures of two-component proteins. Gao R, Stock AM. Annu Rev Microbiol 63 133-154 (2009)
  2. Mechanism of activation for transcription factor PhoB suggested by different modes of dimerization in the inactive and active states. Bachhawat P, Swapna GV, Montelione GT, Stock AM. Structure 13 1353-1363 (2005)
  3. Structural analysis and solution studies of the activated regulatory domain of the response regulator ArcA: a symmetric dimer mediated by the alpha4-beta5-alpha5 face. Toro-Roman A, Mack TR, Stock AM. J Mol Biol 349 11-26 (2005)
  4. The structural basis for regulated assembly and function of the transcriptional activator NtrC. De Carlo S, Chen B, Hoover TR, Kondrashkina E, Nogales E, Nixon BT. Genes Dev 20 1485-1495 (2006)
  5. Detection of allosteric signal transmission by information-theoretic analysis of protein dynamics. Pandini A, Fornili A, Fraternali F, Kleinjung J. FASEB J 26 868-881 (2012)
  6. Crystal structures of the response regulator DosR from Mycobacterium tuberculosis suggest a helix rearrangement mechanism for phosphorylation activation. Wisedchaisri G, Wu M, Sherman DR, Hol WG. J Mol Biol 378 227-242 (2008)
  7. The NMR solution structure of BeF(3)(-)-activated Spo0F reveals the conformational switch in a phosphorelay system. Gardino AK, Volkman BF, Cho HS, Lee SY, Wemmer DE, Kern D. J Mol Biol 331 245-254 (2003)
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  9. The Arabidopsis B-type response regulator 18 homomerizes and positively regulates cytokinin responses. Veerabagu M, Elgass K, Kirchler T, Huppenberger P, Harter K, Chaban C, Mira-Rodado V. Plant J 72 721-731 (2012)
  10. Dimer-induced signal propagation in Spo0A. Muchová K, Lewis RJ, Perecko D, Brannigan JA, Ladds JC, Leech A, Wilkinson AJ, Barák I. Mol Microbiol 53 829-842 (2004)
  11. The X-ray crystal structures of two constitutively active mutants of the Escherichia coli PhoB receiver domain give insights into activation. Arribas-Bosacoma R, Kim SK, Ferrer-Orta C, Blanco AG, Pereira PJ, Gomis-Rüth FX, Wanner BL, Coll M, Solà M. J Mol Biol 366 626-641 (2007)
  12. A new structural domain in the Escherichia coli RcsC hybrid sensor kinase connects histidine kinase and phosphoreceiver domains. Rogov VV, Rogova NY, Bernhard F, Koglin A, Löhr F, Dötsch V. J Mol Biol 364 68-79 (2006)
  13. Antisocial luxO Mutants Provide a Stationary-Phase Survival Advantage in Vibrio fischeri ES114. Kimbrough JH, Stabb EV. J Bacteriol 198 673-687 (2015)
  14. Interactions between strains govern the eco-evolutionary dynamics of microbial communities. Goyal A, Bittleston LS, Leventhal GE, Lu L, Cordero OX. Elife 11 e74987 (2022)
  15. Three-Dimensional Structure of Full-Length NtrX, an Unusual Member of the NtrC Family of Response Regulators. Fernández I, Cornaciu I, Carrica MD, Uchikawa E, Hoffmann G, Sieira R, Márquez JA, Goldbaum FA. J Mol Biol 429 1192-1212 (2017)
  16. Phosphorylation-independent dimer-dimer interactions by the enhancer-binding activator NtrC of Escherichia coli: a third function for the C-terminal domain. Yang XF, Ji Y, Schneider BL, Reitzer L. J Biol Chem 279 36708-36714 (2004)
  17. Structural mechanism of GAF-regulated σ(54) activators from Aquifex aeolicus. Batchelor JD, Lee PS, Wang AC, Doucleff M, Wemmer DE. J Mol Biol 425 156-170 (2013)
  18. Snapshots of Conformational Changes Shed Light into the NtrX Receiver Domain Signal Transduction Mechanism. Fernández I, Otero LH, Klinke S, Carrica MDC, Goldbaum FA. J Mol Biol 427 3258-3272 (2015)
  19. Regulation and action of the bacterial enhancer-binding protein AAA+ domains. Chen B, Sysoeva TA, Chowdhury S, Nixon BT. Biochem Soc Trans 36 89-93 (2008)
  20. The Third Transmembrane Domain of EscR Is Critical for Function of the Enteropathogenic Escherichia coli Type III Secretion System. Tseytin I, Madar A, Mitrovic B, Deng W, Finlay BB, Sal-Man N. mSphere 3 e00162-18 (2018)
  21. Use of restrained molecular dynamics to predict the conformations of phosphorylated receiver domains in two-component signaling systems. Foster CA, West AH. Proteins 85 155-176 (2017)
  22. The Role of the Small Export Apparatus Protein, SctS, in the Activity of the Type III Secretion System. Tseytin I, Mitrovic B, David N, Langenfeld K, Zarivach R, Diepold A, Sal-Man N. Front Microbiol 10 2551 (2019)
  23. Conformational Dynamics of Response Regulator RegX3 from Mycobacterium tuberculosis. Ahmad A, Cai Y, Chen X, Shuai J, Han A. PLoS One 10 e0133389 (2015)
  24. The W-Acidic Motif of Histidine Kinase WalK Is Required for Signaling and Transcriptional Regulation in Streptococcus mutans. Kong L, Su M, Sang J, Huang S, Wang M, Cai Y, Xie M, Wu J, Wang S, Foster SJ, Zhang J, Han A. Front Microbiol 13 820089 (2022)
  25. Subtle sequence differences between two interacting σ54 -dependent regulators lead to different activation mechanisms. Pacheco-Sánchez D, Marín P, Molina-Fuentes Á, Marqués S. FEBS J 289 7582-7604 (2022)


Related citations provided by authors (1)

  1. A dimeric two-component receiver domain inhibits the sigma54-dependent ATPase in DctD. Meyer MG, Park S, Zeringue L, Staley M, McKinstry M, Kaufman RI, Zhang H, Yan D, Yennawar N, Yennawar H, Farber GK, Nixon BT FASEB J. 15 1326-1328 (2001)

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