Structural and functional investigation of the intermolecular interaction between NRPS adenylation and carrier protein domains

Chemistry and Biology

Volumn 19, Issue 2, 2012, Pages 188-198

  Sundlov, Jesse A ^a   Shi, Ce ^b   Wilson, Daniel J ^b   Aldrich, Courtney C ^b   Gulick, Andrew M ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NONRIBOSOMAL PEPTIDE SYNTHETASE; PANTETHEINE; THIOESTER;

ADENYLATION; ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ESTERIFICATION; GENE MUTATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE;

COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROLASES; KINETICS; LIGASES; MUTATION; PEPTIDE SYNTHASES; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84857523988     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2011.11.013     Document Type: Article

References (46)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. D. Chen, R. Wu, T.L. Bryan, and D. Dunaway-Mariano In vitro kinetic analysis of substrate specificity in enterobactin biosynthetic lower pathway enzymes provides insight into the biochemical function of the hot dog-fold thioesterase EntH Biochemistry 48 2009 511 513
3. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
4. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
5. E. Conti, T. Stachelhaus, M.A. Marahiel, and P. Brick Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S EMBO J. 16 1997 4174 4183 (Pubitemid 27298170)
6. 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
7. E.J. Drake, B.P. Duckworth, J. Neres, C.C. Aldrich, and A.M. Gulick Biochemical and structural characterization of bisubstrate inhibitors of BasE, the self-standing nonribosomal peptide synthetase adenylate-forming enzyme of acinetobactin synthesis Biochemistry 49 2010 9292 9305
8. L. Du, Y. He, and Y. Luo Crystal structure and enantiomer selection by D-alanyl carrier protein ligase DltA from Bacillus cereus Biochemistry 47 2008 11473 11480
9. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
10. E.A. Felnagle, J.J. Barkei, H. Park, A.M. Podevels, M.D. McMahon, D.W. Drott, and M.G. Thomas MbtH-like proteins as integral components of bacterial nonribosomal peptide synthetases Biochemistry 49 2010 8815 8817
11. M.A. Fischbach, and C.T. Walsh Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms Chem. Rev. 106 2006 3468 3496 (Pubitemid 44376945)
12. A.M. Gehring, K.A. Bradley, and C.T. Walsh Enterobactin biosynthesis in Escherichia coli: isochorismate lyase (EntB) is a bifunctional enzyme that is phosphopantetheinylated by EntD and then acylated by EntE using ATP and 2,3-dihydroxybenzoate Biochemistry 36 1997 8495 8503 (Pubitemid 27305132)
13. A.M. Gehring, I. Mori, and C.T. Walsh Reconstitution and characterization of the Escherichia coli enterobactin synthetase from EntB, EntE, and EntF Biochemistry 37 1998 2648 2659 (Pubitemid 28119342)
14. A.M. Gulick Conformational dynamics in the Acyl-CoA synthetases, adenylation domains of non-ribosomal peptide synthetases, and firefly luciferase ACS Chem. Biol. 4 2009 811 827
15. A.M. Gulick, V.J. Starai, A.R. Horswill, K.M. Homick, and J.C. Escalante-Semerena The 1.75 A crystal structure of acetyl-CoA synthetase bound to adenosine-5′-propylphosphate and coenzyme A Biochemistry 42 2003 2866 2873 (Pubitemid 36331530)
16. R.B. Kapust, J. Tözsér, J.D. Fox, D.E. Anderson, S. Cherry, T.D. Copeland, and D.S. Waugh Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency Protein Eng. 14 2001 993 1000 (Pubitemid 34137240)
17. T.A. Keating, C.G. Marshall, and C.T. Walsh Vibriobactin biosynthesis in Vibrio cholerae: VibH is an amide synthase homologous to nonribosomal peptide synthetase condensation domains Biochemistry 39 2000 15513 15521 (Pubitemid 32002778)
18. S. Khalil, and P.D. Pawelek Enzymatic adenylation of 2,3- dihydroxybenzoate is enhanced by a protein-protein interaction between Escherichia coli 2,3-dihydro-2,3-dihydroxybenzoate dehydrogenase (EntA) and 2,3-dihydroxybenzoate-AMP ligase (EntE) Biochemistry 50 2011 533 545
19. G. Kochan, E.S. Pilka, F. von Delft, U. Oppermann, and W.W. Yue Structural snapshots for the conformation-dependent catalysis by human medium-chain acyl-coenzyme A synthetase ACSM2A J. Mol. Biol. 388 2009 997 1008
20. A. Koglin, M.R. Mofid, F. Löhr, B. Schäfer, V.V. Rogov, M.M. Blum, T. Mittag, M.A. Marahiel, F. Bernhard, and V. Dötsch Conformational switches modulate protein interactions in peptide antibiotic synthetases Science 312 2006 273 276
21. J.R. Lai, M.A. Fischbach, D.R. Liu, and C.T. Walsh A protein interaction surface in nonribosomal peptide synthesis mapped by combinatorial mutagenesis and selection Proc. Natl. Acad. Sci. USA 103 2006 5314 5319
22. J.R. Lai, M.A. Fischbach, D.R. Liu, and C.T. Walsh Localized protein interaction surfaces on the EntB carrier protein revealed by combinatorial mutagenesis and selection J. Am. Chem. Soc. 128 2006 11002 11003 (Pubitemid 44300091)
23. D. Leduc, A. Battesti, and E. Bouveret The hotdog thioesterase EntH (YbdB) plays a role in vivo in optimal enterobactin biosynthesis by interacting with the ArCP domain of EntB J. Bacteriol. 189 2007 7112 7126 (Pubitemid 47525457)
24. J. Liu, K. Duncan, and C.T. Walsh Nucleotide sequence of a cluster of Escherichia coli enterobactin biosynthesis genes: identification of entA and purification of its product 2,3-dihydro-2,3-dihydroxybenzoate dehydrogenase J. Bacteriol. 171 1989 791 798
25. J. Liu, N. Quinn, G.A. Berchtold, and C.T. Walsh Overexpression, purification, and characterization of isochorismate synthase (EntC), the first enzyme involved in the biosynthesis of enterobactin from chorismate Biochemistry 29 1990 1417 1425 (Pubitemid 20063371)
26. F. Long, A.A. Vagin, P. Young, and G.N. Murshudov BALBES: a molecular-replacement pipeline Acta Crystallogr. D Biol. Crystallogr. 64 2008 125 132 (Pubitemid 350308686)
27. J.R. Luft, R.J. Collins, N.A. Fehrman, A.M. Lauricella, C.K. Veatch, and G.T. DeTitta A deliberate approach to screening for initial crystallization conditions of biological macromolecules J. Struct. Biol. 142 2003 170 179 (Pubitemid 36457899)
28. C.G. Marshall, M.D. Burkart, R.K. Meray, and C.T. Walsh Carrier protein recognition in siderophore-producing nonribosomal peptide synthetases Biochemistry 41 2002 8429 8437 (Pubitemid 34705497)
29. J.J. May, N. Kessler, M.A. Marahiel, and M.T. Stubbs Crystal structure of DhbE, an archetype for aryl acid activating domains of modular nonribosomal peptide synthetases Proc. Natl. Acad. Sci. USA 99 2002 12120 12125
30. 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. Cryst. 40 2007 658 674 (Pubitemid 47080256)
31. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255 (Pubitemid 27235885)
32. J. Neres, D.J. Wilson, L. Celia, B.J. Beck, and C.C. Aldrich Aryl acid adenylating enzymes involved in siderophore biosynthesis: fluorescence polarization assay, ligand specificity, and discovery of non-nucleoside inhibitors via high-throughput screening Biochemistry 47 2008 11735 11749
33. S.K. Olsen, A.D. Capili, X. Lu, D.S. Tan, and C.D. Lima Active site remodelling accompanies thioester bond formation in the SUMO E1 Nature 463 2010 906 912
34. C. Qiao, D.J. Wilson, E.M. Bennett, and C.C. Aldrich A mechanism-based aryl carrier protein/thiolation domain affinity probe J. Am. Chem. Soc. 129 2007 6350 6351 (Pubitemid 46799313)
35. K.N. Raymond, E.A. Dertz, and S.S. Kim Enterobactin: an archetype for microbial iron transport Proc. Natl. Acad. Sci. USA 100 2003 3584 3588 (Pubitemid 36418077)
36. A.S. Reger, R. Wu, D. Dunaway-Mariano, and A.M. Gulick Structural characterization of a 140 degrees domain movement in the two-step reaction catalyzed by 4-chlorobenzoate:CoA ligase Biochemistry 47 2008 8016 8025
37. F. Rusnak, W.S. Faraci, and C.T. Walsh Subcloning, expression, and purification of the enterobactin biosynthetic enzyme 2,3-dihydroxybenzoate-AMP ligase: demonstration of enzyme-bound (2,3-dihydroxybenzoyl)adenylate product Biochemistry 28 1989 6827 6835 (Pubitemid 19219869)
38. S.A. Sieber, and M.A. Marahiel Molecular mechanisms underlying nonribosomal peptide synthesis: approaches to new antibiotics Chem. Rev. 105 2005 715 738 (Pubitemid 40351638)
39. A.L. Sikora, D.J. Wilson, C.C. Aldrich, and J.S. Blanchard Kinetic and inhibition studies of dihydroxybenzoate-AMP ligase from Escherichia coli Biochemistry 49 2010 3648 3657
40. S.M. Soltis, A.E. Cohen, A. Deacon, T. Eriksson, A. González, S. McPhillips, H. Chui, P. Dunten, M. Hollenbeck, and I. Mathews New paradigm for macromolecular crystallography experiments at SSRL: automated crystal screening and remote data collection Acta Crystallogr. D Biol. Crystallogr. 64 2008 1210 1221
41. J.A. Sundlov, J.A. Garringer, J.M. Carney, A.S. Reger, E.J. Drake, W.L. Duax, and A.M. Gulick Determination of the crystal structure of EntA, a 2,3-dihydro-2,3-dihydroxybenzoic acid dehydrogenase from Escherichia coli Acta Crystallogr. D Biol. Crystallogr. 62 2006 734 740 (Pubitemid 43965899)
42. A. Tanovic, S.A. Samel, L.O. Essen, and M.A. Marahiel Crystal structure of the termination module of a nonribosomal peptide synthetase Science 321 2008 659 663
43. M.R. Webb A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems Proc. Natl. Acad. Sci. USA 89 1992 4884 4887
44. R. Wu, J. Cao, X. Lu, A.S. Reger, A.M. Gulick, and D. Dunaway-Mariano Mechanism of 4-chlorobenzoate:coenzyme a ligase catalysis Biochemistry 47 2008 8026 8039
45. 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
46. Z. Zhou, J.R. Lai, and C.T. Walsh Directed evolution of aryl carrier proteins in the enterobactin synthetase Proc. Natl. Acad. Sci. USA 104 2007 11621 11626 (Pubitemid 47175062)