The proline-rich domain of TonB possesses an extended polyproline II-like conformation of sufficient length to span the periplasm of Gram-negative bacteria

Protein Science

Volumn 19, Issue 4, 2010, Pages 625-630

  Köhler, Silvia Domingo ^a   Annemarie Weber, S ^a   Howard, Peter ^b   Welte, Wolfram ^a   Drescher, Malte ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Active transport; DEER; EPR; Outer membrane; Polyproline II; TonB

Indexed keywords

PROLINE; PROTEIN TONB;

ARTICLE; CIRCULAR DICHROISM; CYTOPLASM; DOUBLE ELECTRON ELECTRON RESONANCE; ELECTRON SPIN RESONANCE; GRAM NEGATIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CIRCULAR DICHROISM; ELECTRON SPIN RESONANCE SPECTROSCOPY; GRAM-NEGATIVE BACTERIA; MEMBRANE PROTEINS; PEPTIDES; PERIPLASM; PROLINE;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 77950282521     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.345     Document Type: Article

References (39)

1. Wang CC, Newton A (1971) An additional step in the transport of iron defined by the TonB locus of Escherichia coli. J Biol Chem 246:2147-2151.
2. Hancock REW, Braun V (1976) Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and φ80 to Escherichia coli. J Bacteriol 125: 409-415.
3. Hilsenbeck JL, Park HJ, Chen G, Youn B, Postle K, Kang CH (2004) Crystal structure of th cytotoxic bacterial protein colicin B at 2.5 Å resolution. Mol Microbiol 51:711-720.
4. Salomón RA, Fariás RN (1995) The peptide antibiotic microcin 25 is imported through the TonB pathway and the SbmA protein. J Bacteriol 177:3323-3325.
5. Wandersman C, Stojiljkovic I (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr Opin Microbiol 3:215-220.
6. Cornelissen CN, Biswas GD, Tsai J, Paruchuri DK, Thompson SA, Sparling PF (1992) Gonococcal transferrin-binding protein 1 is required for transferrin utilization and its homologous to TonB-dependent outer membrane receptors. J Bacteriol 174:5788-5797.
7. Schauer K, Rodionov DA, de Reuse H (2008) New substrates for TonB-dependent transport: do we see the 'tip of the iceberg'. Trends Biochem Sci 33:330-338.
8. Higgs PI, Larsen RA, Postle K (2002) Quantification of known components of the Escherichia coli TonB energy transduction system: TonB, ExbB and FepA. Mol Microbiol 44:271-281.
9. Cascales E, Lioubes R, Sturgis JN (2001) The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol 42:795-807.
10. Braun V, Gaisser S, Herrmann C, Kampfenkel K, Killmann H, Traub I (1996) Energy coupled transport across the outer membrane of Escherichia coli: ExbB binds ExbD and TonB in vitro, and leucine 132 in the periplasmic region and aspartate 25 in the transmembrane region are important for ExbD activity. J Bacteriol 178:2836-12284
11. Higgs PI, Myers PS, Postle K (1998) Interactions in the TonB-dependent energy transduction complex: ExbB and ExbD form heteromultimers. J Bacteriol 180: 6031-6038.
12. Larson RA, Thomas MT, Wood GE, Postle K (1994) Partial suppression of an Escherichia coli TonB transmembrane domain mutation (DV17) by a missense mutation in ExbB. Mol Microbiol 13:627-640.
13. Garcia-Herrero A, Peacock RS, Howard SP, Vogel HJ (2007) The solution structure of the periplasmic domain of the TonB system ExbD protein reveals and unexpected structural homology with siderophore-binding proteins. Mol Microbiol 66:872-889.
14. Ferguson AD, Chakraborty R, Smith BS, Esser L, van der Helm D, Deisenhofer J (2002) Structural basis of gating by the outer membrane transporter FecA. Science 295:1715-1719.
15. Ködding J, Killig F, Polzer P, Howard PS, Diederichs K, Welte W (2005) Crystal structure of a 92-residue C-terminal fragment of TonB from Escherichia coli reveals significant conformational changes compared to structures of smaller TonB fragments. J Biol Chem 280:3022-3028.
16. Khursigara CM, De Crescenzo G, Pawelek PD, Coulton JW (2003) Enhanced binding of TonB to a ligand-loaded outer membrane receptor: role of the oligomeric state of TonB in formation of a functional FhuA-TonB complex. J Biol Chem 279:7405-7412.
17. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220.
18. Chimento DP, Mohanty AK, Kadner RJ, Wiener MC (2003) Substrate-induced transmembrane signaling in the cobalamin transporter BtuB. Nat Struct Biol 10: 394-401.
19. Peacock RS, Weljie AM, Howard SP, Price FD, Vogel HJ (2005) The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J Mol Biol 345:1185-1197.
20. Pawelek PD, Croteau N, Ng-Thow-Hing C, Khursigara CM, Moiseeva N, Allaire M, Coulton JW (2006) Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312:1399-1402.
21. Shultis DD, Purdy MD, Banchs CN, Wiener MC (2006) Outer membrane active transport: structure of the BtuB:TonB complex. Science 312:1396-1399.
22. Larsen RA, Letain TE, Postle K (2003) In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli. Mol Microbiol 49: 211-218.
23. Chang C, Mooser A, Plückthun A, Wlodawer A (2001) Crystal structure of the dimer C-terminal domain of TonB reveals a novel fold. J Biol Chem 276: 27535-27540.
24. Gumbart J, Wiener MC, Tajkhorshid E (2007) Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys J 93:496-504.
25. Larsen RA, Letain TE, Postle K (2003) In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli. Mol Microbiol 49:211-218.
26. Kaserer WA, Jiang X, Xiao Q, Scott DC, Bauler M, Copeland D, Newton SMC, Klebba PE (2008) Insight from TonB hybrid proteins into the mechanism of iron transport through the outer membrane. J Bacteriol 190:4001-4016.
27. Graham LL, Beveridge TJ, Naninga N (1991) Freeze-substitution of gram-negative eubacteria: general cell morphology and envelope profiles. J Bacteriol 173: 1623-1633.
28. Evans JS, Levine BA, Trayer IP, Dorman CJ, Higgins CF (1986) Sequence-imposed structural constraints in the TonB protein of E. coli. FEBS Lett 208:211-216.
29. Brewer S, Tolley M, Trayer IP, Barr GC, Dorman CJ, Hannavy K, Higgins CF, Evans JS, Levine BA, Wormald MR (1990) Structure and function of X-Pro dipeptide repeats in the TonB proteins of Salmonella typhimurium and Escherichia coli. J Mol Biol 216:883-895.
30. Postle K, Good RF (1983) DNA sequence of the Escherichia coli TonB gene. Proc Natl Acad Sci USA 80: 5235-5239.
31. Kay BK, Williamson MP, Sudol M (2000) The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14:231-241.
32. Adzhubei AA, Sternberg MJE (1993) Left-handed polyproline II helices commonly occur in globular proteins. J Mol Biol 229:472-493.
33. Milov AD, Maryasov AG, Tsvetkov YD (1998) Pulsed electron double resonance (PELDOR) and its applications in free-radicals research. Appl Magn Reson 15: 107-143.
34. Jeschke G (2002) Distance measurements in the nanometer range by pulse EPR. Chem Phys Chem 3: 927-932.
35. Larsen RG, Singel DJ (1993) Double electron-electron resonance spin-echo modulation: spectroscopic measurement of electron spin pair separations in orientationally disordered solids. J Chem Phys 98:5134-5146.
36. Jeschke G, Polyhach Y (2007) Distance measurements on spin-labelled biomacromolecules by pulsed electron paramagnetic resonance. Phys Chem Chem Phys 9: 1895-1910.
37. Schiemann O, Prisner TF (2007) Long-range distance determinations in biomacromolecules by EPR spectroscopy. Q Rev Biophys 40:1-53.
38. Ladias JAA (2007) Structural basis for polyproline recognition by the FE65 WW domain. J Mol Biol 372: 970-980.
39. Kakinoki S, Hirano Y, Oka M (2005) On the stability of polyproline-I and II structures of proline oligopeptides. Polym Bull 53:109-115.