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Engagement of arginine finger to ATP triggers large conformational changes in NtrC1 AAA+ ATPase for remodeling bacterial RNA polymerase.

Chen B, Sysoeva TA, Chowdhury S, Guo L, De Carlo S, Hanson JA, Yang H, Nixon BT
Structure 18 1420-30 (2010)
Cited: 38 times
EuropePMC logo PMID: 21070941

Abstract

The NtrC-like AAA+ ATPases control virulence and other important bacterial activities through delivering mechanical work to σ54-RNA polymerase to activate transcription from σ54-dependent genes. We report the first crystal structure for such an ATPase, NtrC1 of Aquifex aeolicus, in which the catalytic arginine engages the γ-phosphate of ATP. Comparing the new structure with those previously known for apo and ADP-bound states supports a rigid-body displacement model that is consistent with large-scale conformational changes observed by low-resolution methods. First, the arginine finger induces rigid-body roll, extending surface loops above the plane of the ATPase ring to bind σ54. Second, ATP hydrolysis permits Pi release and retraction of the arginine with a reversed roll, remodeling σ54-RNAP. This model provides a fresh perspective on how ATPase subunits interact within the ring-ensemble to promote transcription, directing attention to structural changes on the arginine-finger side of an ATP-bound interface.

Reviews - 3m0e mentioned but not cited (2)

  1. 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)
  2. Bacterial Enhancer Binding Proteins-AAA+ Proteins in Transcription Activation. Gao F, Danson AE, Ye F, Jovanovic M, Buck M, Zhang X. Biomolecules 10 351 (2020)

Articles - 3m0e mentioned but not cited (11)

  1. Broad spectrum pro-quorum-sensing molecules as inhibitors of virulence in vibrios. Ng WL, Perez L, Cong J, Semmelhack MF, Bassler BL. PLoS Pathog 8 e1002767 (2012)
  2. Engagement of arginine finger to ATP triggers large conformational changes in NtrC1 AAA+ ATPase for remodeling bacterial RNA polymerase. Chen B, Sysoeva TA, Chowdhury S, Guo L, De Carlo S, Hanson JA, Yang H, Nixon BT. Structure 18 1420-1430 (2010)
  3. Nucleotide-induced asymmetry within ATPase activator ring drives σ54-RNAP interaction and ATP hydrolysis. Sysoeva TA, Chowdhury S, Guo L, Nixon BT. Genes Dev 27 2500-2511 (2013)
  4. Conserved phosphoryl transfer mechanisms within kinase families and the role of the C8 proton of ATP in the activation of phosphoryl transfer. Kenyon CP, Roth RL, van der Westhuyzen CW, Parkinson CJ. BMC Res Notes 5 131 (2012)
  5. A structural analysis of the AAA+ domains in Saccharomyces cerevisiae cytoplasmic dynein. Gleave ES, Schmidt H, Carter AP. J Struct Biol 186 367-375 (2014)
  6. Unique ATPase site architecture triggers cis-mediated synchronized ATP binding in heptameric AAA+-ATPase domain of flagellar regulatory protein FlrC. Dey S, Biswas M, Sen U, Dasgupta J. J Biol Chem 290 8734-8747 (2015)
  7. Allosteric communication in DNA polymerase clamp loaders relies on a critical hydrogen-bonded junction. Subramanian S, Gorday K, Marcus K, Orellana MR, Ren P, Luo XR, O'Donnell ME, Kuriyan J. Elife 10 e66181 (2021)
  8. Significant reduction in errors associated with nonbonded contacts in protein crystal structures: automated all-atom refinement with PrimeX. Bell JA, Ho KL, Farid R. Acta Crystallogr D Biol Crystallogr 68 935-952 (2012)
  9. The heptameric structure of the flagellar regulatory protein FlrC is indispensable for ATPase activity and disassembled by cyclic-di-GMP. Chakraborty S, Biswas M, Dey S, Agarwal S, Chakrabortty T, Ghosh B, Dasgupta J. J Biol Chem 295 16960-16974 (2020)
  10. Crystallization and preliminary X-ray analysis of the ATPase domain of the σ(54)-dependent transcription activator NtrC1 from Aquifex aeolicus bound to the ATP analog ADP-BeFx. Sysoeva TA, Yennawar N, Allaire M, Nixon BT. Acta Crystallogr Sect F Struct Biol Cryst Commun 69 1384-1388 (2013)
  11. SPARC: Structural properties associated with residue constraints. Neuwald AF, Yang H, Tracy Nixon B. Comput Struct Biotechnol J 20 1702-1715 (2022)


Reviews citing this publication (4)

  1. Mechanistic and Structural Insights into the Prion-Disaggregase Activity of Hsp104. Sweeny EA, Shorter J. J Mol Biol 428 1870-1885 (2016)
  2. Controlling the Revolving and Rotating Motion Direction of Asymmetric Hexameric Nanomotor by Arginine Finger and Channel Chirality. Guo P, Driver D, Zhao Z, Zheng Z, Chan C, Cheng X. ACS Nano 13 6207-6223 (2019)
  3. Modulating Salmonella Typhimurium's Response to a Changing Environment through Bacterial Enhancer-Binding Proteins and the RpoN Regulon. Hartman CE, Samuels DJ, Karls AC. Front Mol Biosci 3 41 (2016)
  4. Assessing heterogeneity in oligomeric AAA+ machines. Sysoeva TA. Cell Mol Life Sci 74 1001-1018 (2017)

Articles citing this publication (21)

  1. Insights into dynein motor domain function from a 3.3-Å crystal structure. Schmidt H, Gleave ES, Carter AP. Nat Struct Mol Biol 19 492-7, S1 (2012)
  2. The Hsp104 N-terminal domain enables disaggregase plasticity and potentiation. Sweeny EA, Jackrel ME, Go MS, Sochor MA, Razzo BM, DeSantis ME, Gupta K, Shorter J. Mol Cell 57 836-849 (2015)
  3. ATP binding to neighbouring subunits and intersubunit allosteric coupling underlie proteasomal ATPase function. Kim YC, Snoberger A, Schupp J, Smith DM. Nat Commun 6 8520 (2015)
  4. A central swivel point in the RFC clamp loader controls PCNA opening and loading on DNA. Sakato M, O'Donnell M, Hingorani MM. J Mol Biol 416 163-175 (2012)
  5. Bottom-up fabrication of a proteasome-nanopore that unravels and processes single proteins. Zhang S, Huang G, Versloot RCA, Bruininks BMH, de Souza PCT, Marrink SJ, Maglia G. Nat Chem 13 1192-1199 (2021)
  6. ATPase site architecture is required for self-assembly and remodeling activity of a hexameric AAA+ transcriptional activator. Joly N, Zhang N, Buck M. Mol Cell 47 484-490 (2012)
  7. An Arginine Finger Regulates the Sequential Action of Asymmetrical Hexameric ATPase in the Double-Stranded DNA Translocation Motor. Zhao Z, De-Donatis GM, Schwartz C, Fang H, Li J, Guo P. Mol Cell Biol 36 2514-2523 (2016)
  8. Structure, Regulation, and Inhibition of the Quorum-Sensing Signal Integrator LuxO. Boyaci H, Shah T, Hurley A, Kokona B, Li Z, Ventocilla C, Jeffrey PD, Semmelhack MF, Fairman R, Bassler BL, Hughson FM. PLoS Biol 14 e1002464 (2016)
  9. A common feature from different subunits of a homomeric AAA+ protein contacts three spatially distinct transcription elements. Zhang N, Joly N, Buck M. Nucleic Acids Res 40 9139-9152 (2012)
  10. 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)
  11. Spontaneous Reversions of an Evolutionary Trait Loss Reveal Regulators of a Small RNA That Controls Multicellular Development in Myxobacteria. Yu YN, Kleiner M, Velicer GJ. J Bacteriol 198 3142-3151 (2016)
  12. The structural basis for enhancer-dependent assembly and activation of the AAA transcriptional activator NorR. Bush M, Ghosh T, Sawicka M, Moal IH, Bates PA, Dixon R, Zhang X. Mol Microbiol 95 17-30 (2015)
  13. A key hydrophobic patch identified in an AAA⁺ protein essential for its in trans inhibitory regulation. Zhang N, Simpson T, Lawton E, Uzdavinys P, Joly N, Burrows P, Buck M. J Mol Biol 425 2656-2669 (2013)
  14. Subunit dynamics and nucleotide-dependent asymmetry of an AAA(+) transcription complex. Zhang N, Gordiyenko Y, Joly N, Lawton E, Robinson CV, Buck M. J Mol Biol 426 71-83 (2014)
  15. Hexameric assembly of the AAA+ protein McrB is necessary for GTPase activity. Nirwan N, Singh P, Mishra GG, Johnson CM, Szczelkun MD, Inoue K, Vinothkumar KR, Saikrishnan K. Nucleic Acids Res 47 868-882 (2019)
  16. Role of the σ54 Activator Interacting Domain in Bacterial Transcription Initiation. Siegel AR, Wemmer DE. J Mol Biol 428 4669-4685 (2016)
  17. Comment Breaking symmetry in multimeric ATPase motors. Sysoeva TA, Chowdhury S, Nixon BT. Cell Cycle 13 1509-1510 (2014)
  18. An ATPase R-finger leaves its print on transcriptional activation. Buck M, Hoover TR. Structure 18 1391-1392 (2010)
  19. Molecular basis of nucleotide-dependent substrate engagement and remodeling by an AAA+ activator. Darbari VC, Lawton E, Lu D, Burrows PC, Wiesler S, Joly N, Zhang N, Zhang X, Buck M. Nucleic Acids Res 42 9249-9261 (2014)
  20. REC domain stabilizes the active heptamer of σ54-dependent transcription factor, FleR from Pseudomonas aeruginosa. Sahoo PK, Sheenu, Jain D. iScience 26 108397 (2023)
  21. 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)


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