High-resolution structures of the d-alanyl carrier protein (Dcp) DltC from Bacillus subtilis reveal equivalent conformations of apo- and holo-forms

FEBS Letters

Volumn 589, Issue 18, 2015, Pages 2283-2289

  Zimmermann, Stephan ^a,b   Pfennig, Sabrina ^a,c   Neumann, Piotr ^a,d   Yonus, Huma ^a   Weininger, Ulrich ^a,e   Kovermann, Michael ^a,f   Balbach, Jochen ^a   Stubbs, Milton T ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e LUND UNIVERSITY   (Sweden)

^f UMEÅ UNIVERSITY   (Sweden)

Author keywords

Abbreviations CP carrier protein; ACP acyl CP; ArCP aryl CP; Dcp d alanyl CP; FA fatty acid; NRP non ribosomal peptide; PCP peptidyl CP; PK polyketide; ppant 4 phosphopantetheine; rmsd root mean square deviation; SeMet selenomethionine

Indexed keywords

DLTC PROTEIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; PANTETHEINE PHOSPHATE; PEPTIDYL CARRIER PROTEIN; UNCLASSIFIED DRUG; APOPROTEIN; BACTERIAL PROTEIN; CARRIER PROTEIN; D-ALANYL CARRIER PROTEIN, BACTERIA;

ARTICLE; BACILLUS SUBTILIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PROCESSING; CHEMICAL STRUCTURE; CHEMISTRY; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BACILLUS SUBTILIS; POSIBACTERIA;

APOPROTEINS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 84938950821     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.07.008     Document Type: Article

References (45)

1. F.C. Neuhaus, and J. Baddiley A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in gram-positive bacteria Microbiol. Mol. Biol. Rev. 67 2003 686 723
2. J.G. Swoboda, J. Campbell, T.C. Meredith, and S. Walker Wall teichoic acid function, biosynthesis, and inhibition ChemBioChem 11 2010 35 45
3. A. Peschel, M. Otto, R.W. Jack, H. Kalbacher, G. Jung, and F. Gotz Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides J. Biol. Chem. 274 1999 8405 8410
4. L.V. Collins, S.A. Kristian, C. Weidenmaier, M. Faigle, K.P. Van Kessel, J.A. Van Strijp, F. Gotz, B. Neumeister, and A. Peschel Staphylococcus aureus strains lacking d-alanine modifications of teichoic acids are highly susceptible to human neutrophil killing and are virulence attenuated in mice J. Infect. Dis. 186 2002 214 219
5. M. Perego, P. Glaser, A. Minutello, M.A. Strauch, K. Leopold, and W. Fischer Incorporation of d-alanine into lipoteichoic acid and wall teichoic-acid in bacillus subtilis - identification of genes and regulation J. Biol. Chem. 270 1995 15598 15606
6. B.F. Volkman, Q.Y. Zhang, D.V. Debabov, E. Rivera, G.C. Kresheck, and F.C. Neuhaus Biosynthesis of d-alanyl-lipoteichoic acid: the tertiary structure of apo-d-alanyl carrier protein Biochemistry 40 2001 7964 7972
7. K.J. Weissman, and R. Muller Protein-protein interactions in multienzyme megasynthetases ChemBioChem 9 2008 826 848
8. A. Koglin, M.R. Mofid, F. Lohr, B. Schafer, V.V. Rogov, M.M. Blum, T. Mittag, M.A. Marahiel, F. Bernhard, and V. Dotsch Conformational switches modulate protein interactions in peptide antibiotic synthetases Science 312 2006 273 276
9. A. Koglin, F. Lohr, F. Bernhard, V.V. Rogov, D.P. Frueh, E.R. Strieter, M.R. Mofid, P. Guntert, G. Wagner, C.T. Walsh, M.A. Marahiel, and V. Dotsch Structural basis for the selectivity of the external thioesterase of the surfactin synthetase Nature 454 2008 907-U68
10. C.O. Rock, and J.L. Garwin Preparative enzymatic-synthesis and hydrophobic chromatography of acyl-acyl carrier protein J. Biol. Chem. 254 1979 7123 7128
11. A. Roujeinikova, C. Baldock, W.J. Simon, J. Gilroy, P.J. Baker, A.R. Stuitje, D.W. Rice, A.R. Slabas, and J.B. Rafferty X-ray crystallographic studies on butyryl-ACP reveal flexibility of the structure around a putative acyl chain binding site Structure 10 2002 825 835
12. G.A. Zornetzer, B.G. Fox, and J.L. Markley Solution structures of spinach acyl carrier protein with decanoate and stearate Biochemistry 45 2006 5217 5227
13. S.E. Evans, C. Williams, C.J. Arthur, S.G. Burston, T.J. Simpson, J. Crosby, and M.P. Crump An ACP structural switch: conformational differences between the Apo and Holo forms of the actinorhodin polyketide synthase acyl carrier protein ChemBioChem 9 2008 2424 2432
14. J. Crosby, and M.P. Crump The structural role of the carrier protein-active controller or passive carrier Nat. Prod. Rep. 29 2012 1111 1137
15. T. Weber, R. Baumgartner, C. Renner, M.A. Marahiel, and T.A. Holak Solution structure of PCP, a prototype for the peptidyl carrier domains of modular peptide synthetases Struct. Fold. Des. 8 2000 407 418
16. A.C. Goodrich, and D.P. Frueh A nuclear magnetic resonance method for probing molecular influences of substrate loading in nonribosomal peptide synthetase carrier proteins Biochemistry 54 2015 1154 1156
17. E.J. Drake, D.A. Nicolai, and A.M. Gulick Structure of the EntB multidomain nonribosomal peptide synthetase and functional analysis of its interaction with the EntE adenylation domain Chem. Biol. 13 2006 409 419
18. J.A. Sundlov, C. Shi, D.J. Wilson, C.C. Aldrich, and A.M. Gulick Structural and functional investigation of the intermolecular interaction between NRPS adenylation and carrier protein domains Chem. Biol. 19 2012 188 198
19. K. Haslinger, C. Redfield, and M.J. Cryle Structure of the terminal PCP domain of the non-ribosomal peptide synthetase in teicoplanin biosynthesis Proteins 83 2015 711 721
20. C.L. Allen, and A.M. Gulick Structural and bioinformatic characterization of an Acinetobacter baumannii type II carrier protein Acta Crystallogr. D Biol. Crystallogr. 70 2014 1718 1725
21. J.R. Lohman, M. Ma, M.E. Cuff, L. Bigelow, J. Bearden, G. Babnigg, A. Joachimiak, G.N. Phillips Jr., and B. Shen The crystal structure of BlmI as a model for nonribosomal peptide synthetase peptidyl carrier proteins Proteins 82 2014 1210 1218
22. P. Tufar, S. Rahighi, F.I. Kraas, D.K. Kirchner, F. Lohr, E. Henrich, J. Kopke, I. Dikic, P. Guntert, M.A. Marahiel, and V. Dotsch Crystal structure of a PCP/Sfp complex reveals the structural basis for carrier protein posttranslational modification Chem. Biol. 21 2014 552 562
23. U. Linne, A. Schafer, M.T. Stubbs, and M.A. Marahiel Aminoacyl-coenzyme A synthesis catalyzed by adenylation domains FEBS Lett. 581 2007 905 910
24. H. Yonus, P. Neumann, S. Zimmermann, J.J. May, M.A. Marahiel, and M.T. Stubbs Crystal structure of DltA: implications for the reaction mechanism of non-ribosomal peptide synthetase adenylation domains J. Biol. Chem. 283 2008 32484 32491
25. J.J. May, R. Finking, F. Wiegeshoff, T.T. Weber, N. Bandur, U. Koert, and M.A. Marahiel Inhibition of the d-alanine: d-alanyl carrier protein ligase from Bacillus subtilis increases the bacterium's susceptibility to antibiotics that target the cell wall FEBS J. 272 2005 2993 3003
26. W. Kabsch Xds Acta Crystallogr. Section D-Biol. Crystallogr. 66 2010 125 132
27. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
28. G.M. Sheldrick A short history of SHELX Acta Crystallogr. Section A 64 2008 112 122
29. T. Pape, and T.R. Schneider HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs J. Appl. Crystallogr. 37 2004 843 844
30. G. Langer, S.X. Cohen, V.S. Lamzin, and A. Perrakis Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 3 2008 1171 1179
31. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
32. P.V. Afonine, R.W. Grosse-Kunstleve, N. Echols, J.J. Headd, N.W. Moriarty, M. Mustyakimov, T.C. Terwilliger, A. Urzhumtsev, P.H. Zwart, and P.D. Adams Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr. D Biol. Crystallogr. 68 2012 352 367
33. A.J. Mccoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
34. S. Grzesiek, S.J. Stahl, P.T. Wingfield, and A. Bax The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR Biochemistry 35 1996 10256 10261
35. M. Tollinger, N.R. Skrynnikov, F.A. Mulder, J.D. Forman-Kay, and L.E. Kay Slow dynamics in folded and unfolded states of an SH3 domain J. Am. Chem. Soc. 123 2001 11341 11352
36. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
37. B.A. Johnson, and R.A. Blevins NMR View: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
38. J.S. Richardson, and D.C. Richardson Amino acid preferences for specific locations at the ends of alpha helices Science 240 1988 1648 1652
39. K.D. Parris, L. Lin, A. Tam, R. Mathew, J. Hixon, M. Stahl, C.C. Fritz, J. Seehra, and W.S. Somers Crystal structures of substrate binding to Bacillus subtilis holo-(acyl carrier protein) synthase reveal a novel trimeric arrangement of molecules resulting in three active sites Struct. Fold. Des. 8 2000 883 895
40. C.A. Mitchell, C. Shi, C.C. Aldrich, and A.M. Gulick Structure of PA1221, a nonribosomal peptide synthetase containing adenylation and peptidyl carrier protein domains Biochemistry 51 2012 3252 3263
41. M.M. Flocco, and S.L. Mowbray Planar stacking interactions of arginine and aromatic side-chains in proteins J. Mol. Biol. 235 1994 709 717
42. J.R. Gallagher, and S.T. Prigge Plasmodium falciparum acyl carrier protein crystal structures in disulfide-linked and reduced states and their prevalence during blood stage growth Proteins Struct. Funct. Bioinform. 78 2010 575 588
43. N.R. De Lay, and J.E. Cronan In vivo functional analyses of the type II acyl carrier proteins of fatty acid biosynthesis J. Biol. Chem. 282 2007 20319 20328
44. C.O. Rock, J.E. Cronan Jr., and I.M. Armitage Molecular properties of acyl carrier protein derivatives J. Biol. Chem. 256 1981 2669 2674
45. Y. Kim, E.L. Kovrigin, and Z. Eletr NMR studies of Escherichia coli acyl carrier protein: dynamic and structural differences of the apo- and holo-forms Biochem. Biophys. Res. Commun. 341 2006 776 783