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Biomolecular NMR Assignments

, Volume 12, Issue 1, pp 91–94 | Cite as

NMR assignments of the N-terminal signaling domain of the TonB-dependent outer membrane transducer PupB

  • Jaime L. Jensen
  • Qiong Wu
  • Christopher L. Colbert
Article

Abstract

Outer membrane TonB-dependent transducers (TBDTs) actively transport ferric siderophore complexes from the extracellular environment into Gram-negative bacteria. They also participate in a cell-surface signaling regulatory pathway that results in upregulation of the transducer itself, in response to iron-deplete conditions. The TBDT PupB transports ferric pseudobactin, and signals through its N-terminal signaling domain (NTSD), while the TBDT homolog PupA is signaling-inactive. Here, we report the NMR chemical shift assignments of the PupB-NTSD. This information will provide the basis for structural characterization of the PupB-NTSD to further explore its signaling properties.

Keywords

Cell surface signaling Ton-B dependent transporters Pseudomonas Pseudobactin Nuclear magnetic resonance 

Notes

Acknowledgements

The authors thank Dr. John Bagu, NDSU Organic Spectroscopy lab, for assistance with in-house HSQC experiments and Dr. Sangita Sinha for critical reading of the manuscript. This research was supported in part by the National Institutes of Health (NIH) National Institutes of General Medical Science (NIGMS) (1R15 GM113227) to CLC, the NIH National Center for Research Resources (2P20 RR015566), and the NIH NIGMS (P30 GM103332). JLJ was supported by the North Dakota Experimental Program to Stimulate Competitive Research Doctoral Dissertation Assistantship (#FAR0025216). The Biomolecular NMR facility at UTSW acknowledges National Institutes of Health grants S10 RR026461-01 for its 600 MHz Agilent DD2 console and National Institutes of Health Grant 1S10OD018027-01 for its 800 MHz Agilent D22 console.

References

  1. Bax A, Ikura M (1991) An efficient 3D NMR technique for correlating the proton and 15N backbone amide resonances with the alpha-carbon of the preceding residue in uniformly 15N/13C enriched proteins. J Biomol Nmr 1:99–104CrossRefGoogle Scholar
  2. Bitter W, Marugg JD, de Weger LA, Tommassen J, Weisbeek PJ (1991) The ferric-pseudobactin receptor PupA of Pseudomonas putida WCS358: homology to TonB-dependent Escherichia coli receptors and specificity of the protein. Mol Microbiol 5:647–655CrossRefGoogle Scholar
  3. Brillet K, Journet L, Celia H, Paulus L, Stahl A, Pattus F, Cobessi D (2007) A beta strand lock exchange for signal transduction in TonB-dependent transducers on the basis of a common structural motif. Structure 15:1383–1391CrossRefGoogle Scholar
  4. Cavanagh J, Fairbrother WJ, Palmer AG, Rance M, Skelton NJ (2007) Protein NMR spectroscopy: principles and practice. Academic Press, New YorkGoogle Scholar
  5. Cobessi D, Celia H, Folschweiller N, Schalk IJ, Abdallah MA, Pattus F (2005) The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 angstroms resolution. J Mol Biol 347:121–134CrossRefGoogle Scholar
  6. Constantine KL, Goldfarb V, Wittekind M, Friedrichs MS, Anthony J, Ng SC, Mueller L (1993) Aliphatic 1H and 13C resonance assignments for the 26-10 antibody VL domain derived from heteronuclear multidimensional NMR spectroscopy. J Biomol Nmr 3:41–54CrossRefGoogle Scholar
  7. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) Nmrpipe—a multidimensional spectral processing system based on Unix pipes. J Biomol Nmr 6:277–293CrossRefGoogle Scholar
  8. Ferguson AD, Amezcua CA, Halabi NM, Chelliah Y, Rosen MK, Ranganathan R, Deisenhofer J (2007) Signal transduction pathway of TonB-dependent transporters. PNAS 104:513–518ADSCrossRefGoogle Scholar
  9. Garcia-Herrero A, Vogel HJ (2005) Nuclear magnetic resonance solution structure of the periplasmic signalling domain of the TonB-dependent outer membrane transporter FecA from Escherichia coli. Mol Microbiol 58:1226–1237CrossRefGoogle Scholar
  10. Ginzinger SW, Gerick F, Coles M, Heun V (2007) CheckShift: automatic correction of inconsistent chemical shift referencing. J Biomol Nmr 39:223–227CrossRefGoogle Scholar
  11. Ginzinger SW, Skocibusic M, Heun V (2009) CheckShift improved: fast chemical shift reference correction with high accuracy. J Biomol Nmr 44:207–211CrossRefGoogle Scholar
  12. Greenwald J, Nader M, Celia H, Gruffaz C, Geoffroy V, Meyer JM, Schalk IJ, Pattus F (2009) FpvA bound to non-cognate pyoverdines: molecular basis of siderophore recognition by an iron transporter. Mol Microbiol 72:1246–1259CrossRefGoogle Scholar
  13. Hantke K (1981) Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182:288–292CrossRefGoogle Scholar
  14. Harle C, Kim I, Angerer A, Braun V (1995) Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J 14:1430–1438Google Scholar
  15. Johnson BA (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278:313–352Google Scholar
  16. Johnson BA, Blevins RA (1994) NMR View: a computer program for the visualization and analysis of NMR data. J Biomol Nmr 4:603–614CrossRefGoogle Scholar
  17. Kadner RJ, McElhaney G (1978) Outer membrane-dependent transport systems in Escherichia coli: turnover of TonB function. J Bacteriol 134:1020–1029Google Scholar
  18. Koebnik R (2005) TonB-dependent trans-envelope signalling: the exception or the rule? Trends Microbiol 13:343–347CrossRefGoogle Scholar
  19. Koster M, van de Vossenberg J, Leong J, Weisbeek PJ (1993) Identification and characterization of the pupB gene encoding an inducible ferric-pseudobactin receptor of Pseudomonas putida WCS358. Mol Microbiol 8:591–601CrossRefGoogle Scholar
  20. Koster M, van Klompenburg W, Bitter W, Leong J, Weisbeek P (1994) Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J 13:2805–2813Google Scholar
  21. Shen Y, Delaglio F, Cornilescu G, Bax A (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol Nmr 44:213–223CrossRefGoogle Scholar
  22. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, Ulrich EL, Markley JL, Ionides J, Laue ED (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59:687–696CrossRefGoogle Scholar
  23. Wirth C, Meyer-Klaucke W, Pattus F, Cobessi D (2007) From the periplasmic signaling domain to the extracellular face of an outer membrane signal transducer of Pseudomonas aeruginosa: crystal structure of the ferric pyoverdine outer membrane receptor. J Mol Biol 368:398–406CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of Chemistry and BiochemistryNorth Dakota State UniversityFargoUSA
  2. 2.Department of BiophysicsUniversity of Texas Southwestern Medical CenterDallasUSA
  3. 3.Department of Pathology, Microbiology and ImmunologyVanderbilt UniversityNashvilleUSA

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