Structural basis of the interaction of mbth-like proteins, putative regulators of nonribosomal peptide biosynthesis, with adenylating enzymes

Journal of Biological Chemistry

Volumn 288, Issue 3, 2013, Pages 1991-2003

  Herbst, Dominik A ^a   Boll, Björn ^a   Zocher, Georg ^a   Stehle, Thilo ^a,b   Heide, Lutz ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE; ADENYLATION; BIOSYNTHETIC GENE CLUSTER; DIRECT CONTACT; NONRIBOSOMAL PEPTIDE; POLYKETIDES; SIDE-CHAINS; STRUCTURAL BASIS; TRYPTOPHAN RESIDUES; VANCOMYCIN;

AMINO ACIDS; ANTIBIOTICS; BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES;

PROTEINS;

ALANINE; ALANINE 433; GLUTAMIC ACID; MBTH PROTEIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; POLYKETIDE; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN; STREPTOLYDIGIN; STRUCTURAL PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ADENYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; GENE MUTATION; MOLECULAR CLONING; NONRIBOSOMAL PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS;

ADENOSINE MONOPHOSPHATE; ALANINE; AMINO ACID SEQUENCE; AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; ASPARTIC ACID; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; PEPTIDE BIOSYNTHESIS, NUCLEIC ACID-INDEPENDENT; PEPTIDE SYNTHASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; TRYPTOPHAN;

EID: 84872734321     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.420182     Document Type: Article

References (53)

1. Baltz, R. H. (2011) Function of MbtH homologs in nonribosomal peptide biosynthesis and applications in secondary metabolite discovery. J. Ind. Microbiol. Biotechnol. 38, 1747-1760
2. Tatham, E., Chavadi, S., Mohandas, P., Edupuganti, U., Angala, S., Chatterjee, D., and Quadri, L. E. (2012) Production of mycobacterial cell wall glycopeptidolipids requires a member of the MbtH-like protein family. BMC Microbiol. 12, 118
3. Wolpert, M., Gust, B., Kammerer, B., and Heide, L. (2007) Effects of deletions of mbtH-like genes on clorobiocin biosynthesis in Streptomyces coelicolor. Microbiology 153, 1413-1423 (Pubitemid 46779997)
4. Lautru, S., Oves-Costales, D., Pernodet, J. L., and Challis, G. L. (2007) MbtH-like protein-mediated cross-talk between nonribosomal peptide antibiotic and siderophore biosynthetic pathways in Streptomyces coelicolor M145. Microbiology 153, 1405-1412 (Pubitemid 46779996)
5. Stegmann, E., Rausch, C., Stockert, S., Burkert, D., and Wohlleben, W. (2006) The small MbtH-like protein encoded by an internal gene of the balhimycin biosynthetic gene cluster is not required for glycopeptide production. FEMS Microbiol. Lett. 262, 85-92 (Pubitemid 44212893)
6. Imker, H. J., Krahn, D., Clerc, J., Kaiser, M., and Walsh, C. T. (2010) N-Acylation during glidobactin biosynthesis by the tridomain nonribosomal peptide synthetase module GlbF. Chem. Biol. 17, 1077-1083
7. Felnagle, E. A., Barkei, J. J., Park, H., Podevels, A. M., McMahon, M. D., Drott, D. W., and Thomas, M. G. (2010) MbtH-like proteins as integral components of bacterial nonribosomal peptide synthetases. Biochemistry 49, 8815-8817
8. Zhang, W., Heemstra, J. R., Jr., Walsh, C. T., and Imker, H. J. (2010) Activation of the pacidamycin PacL adenylation domain by MbtH-like proteins. Biochemistry 49, 9946-9947
9. McMahon, M. D., Rush, J. S., and Thomas, M. G. (2012) Analyses of MbtB, MbtE, and MbtF suggest revisions to the mycobactin biosynthesis pathway in Mycobacterium tuberculosis. J. Bacteriol. 194, 2809-2818
10. Zolova, O. E., and Garneau-Tsodikova, S. (2012) Importance of the MbtHlike protein TioT for production and activation of the thiocoraline adenylation domain of TioK. MedChemComm 3, 950-955
11. Boll, B., Taubitz, T., and Heide, L. (2011) The role of MbtH-like proteins in the adenylation of tyrosine during aminocoumarin and vancomycin biosynthesis. J. Biol. Chem. 286, 36281-36290
12. Gulick, A. M. (2009) Conformational dynamics in the Acyl-CoA synthetases, adenylation domains of nonribosomal peptide synthetases, and firefly luciferase. ACS Chem. Biol. 4, 811-827
13. Reger, A. S., Wu, R., Dunaway-Mariano, D., and Gulick, A. M. (2008) Structural characterization of a 140 degrees domain movement in the two-step reaction catalyzed by 4-chlorobenzoate:CoA ligase. Biochemistry 47, 8016-8025
14. Goyal, A., Yousuf, M., Rajakumara, E., Arora, P., Gokhale, R. S., and Sankaranarayanan, R. (2006) Crystallization and preliminary x-ray crystallographic studies of the N-terminal domain of FadD28, a fatty-acyl AMP ligase from Mycobacterium tuberculosis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62, 350-352
15. Arora, P., Goyal, A., Natarajan, V. T., Rajakumara, E., Verma, P., Gupta, R., Yousuf, M., Trivedi, O. A., Mohanty, D., Tyagi, A., Sankaranarayanan, R., and Gokhale, R. S. (2009) Mechanistic and functional insights into fatty acid activation in Mycobacterium tuberculosis. Nat. Chem. Biol. 5, 166-173
16. Drake, E. J., Cao, J., Qu, J., Shah, M. B., Straubinger, R. M., and Gulick, A. M. (2007) The 1.8 Å crystal structure of PA2412, an MbtH-like protein from the pyoverdine cluster of Pseudomonas aeruginosa. J. Biol. Chem. 282, 20425-20434 (Pubitemid 47099995)
17. Buchko, G. W., Kim, C. Y., Terwilliger, T. C., and Myler, P. J. (2010) Solution structure of Rv2377c-founding member of the MbtH-like protein family. Tuberculosis 90, 245-251
18. Horna, D. H., Gómez, C., Olano, C., Palomino-Schätzlein, M., Pineda-Lucena, A., Carbajo, R. J., Braña, A. F., Méndez, C., and Salas, J. A. (2011) Biosynthesis of the RNA polymerase inhibitor streptolydigin in Streptomyces lyticus. Tailoring modification of 3-methyl-aspartate. J. Bacteriol. 193, 2647-2651
19. Olano, C., Gómez, C., Pérez, M., Palomino, M., Pineda-Lucena, A., Carbajo, R. J., Braña, A. F., Méndez, C., and Salas, J. A. (2009) Deciphering biosynthesis of the RNA polymerase inhibitor streptolydigin and generation of glycosylated derivatives. Chem. Biol. 16, 1031-1044
20. Gómez, C., Horna, D. H., Olano, C., Palomino-Schätzlein, M., Pineda-Lucena, A., Carbajo, R. J., Braña, A. F., Méndez, C., and Salas, J. A. (2011) Amino acid precursor supply in the biosynthesis of the RNA polymerase inhibitor streptolydigin by Streptomyces lyticus. J. Bacteriol. 193, 4214-4223
21. Marsh, E. N. (2009) Insights into the mechanisms of adenosylcobalamin (coenzyme B12)-dependent enzymes from rapid chemical quench experiments. Biochem. Soc. Trans. 37, 336-342
22. Gómez, C., Olano, C., Palomino-Schätzlein, M., Pineda-Lucena, A., Carbajo, R. J., Braña, A. F., Méndez, C., and Salas, J. A. (2012) Novel compounds produced by Streptomyces lyticus NRRL 2433 engineered mutants altered in the biosynthesis of streptolydigin. J. Antibiot. 65, 341-348
23. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800
24. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
25. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., Mc-Coy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002) PHENIX. Building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954
26. Rossmann, M. G., and Blow, D. M. (1962) The detection of subunits within the crystallographic asymmetric unit. Acta Crystallogr. 15, 24-31
27. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
28. Conti, E., Stachelhaus, T., Marahiel, M. A., and Brick, P. (1997) Structural basis for the activation of phenylalanine in the nonribosomal biosynthesis of gramicidin S. EMBO J. 16, 4174-4183 (Pubitemid 27298170)
29. Stein, N. (2008) CHAINSAW. A program for mutating PDB files used as templates in molecular replacement. J. Appl. Crystallogr. 41, 641-643 (Pubitemid 351693895)
30. Terwilliger, T. (2000) Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56, 965-972 (Pubitemid 30622779)
31. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
32. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
33. Winn, M. D., Murshudov, G. N., and Papiz, M. Z. (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321 (Pubitemid 37531815)
34. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity. All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
35. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
36. Ten, L. (1973) Crystallographic fast Fourier transforms. Acta Crystallogr. A 29, 183-191
37. Schrödinger, L. L. C. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New York
38. Bond, C. S. (2003) TopDraw. A sketchpad for protein structure topology cartoons. Bioinformatics 19, 311-312 (Pubitemid 36181928)
39. Frishman, D., and Argos, P. (1995) Knowledge-based protein secondary structure assignment. Proteins 23, 566-579 (Pubitemid 26009520)
40. Holm, L., Kääriäinen, S., Rosenström, P., and Schenkel, A. (2008) Searching protein structure databases with DaliLite version 3. Bioinformatics 24, 2780-2781 (Pubitemid 352722625)
41. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
42. Stachelhaus, T., Mootz, H. D., and Marahiel, M. A. (1999) The specificityconferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 6, 493-505 (Pubitemid 29380764)
43. Röttig, M., Medema, M. H., Blin, K., Weber, T., Rausch, C., and Kohlbacher, O. (2011) NRPSpredictor2-a web server for predicting NRPS adenylation domain specificity. Nucleic Acids Res. 39, W362-W367
44. Rao, S. T., and Rossmann, M. G. (1973) Comparison of super-secondary structures in proteins. J. Mol. Biol. 76, 241-256
45. Holm, L., and Park, J. (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16, 566-567
46. Tanovic, A., Samel, S. A., Essen, L. O., and Marahiel, M. A. (2008) Crystal structure of the termination module of a nonribosomal peptide synthetase. Science 321, 659-663
47. Siddiqui, N., Tempel, W., Nedyalkova, L., Volpon, L., Wernimont, A. K., Osborne, M. J., Park, H. W., and Borden, K. L. (2012) Structural insights into the allosteric effects of 4EBP1 on the eukaryotic translation initiation factor eIF4E. J. Mol. Biol. 415, 781-792
48. Stanger, K., Steffek, M., Zhou, L., Pozniak, C. D., Quan, C., Franke, Y., Tom, J., Tam, C., Elliott, J. M., Lewcock, J. W., Zhang, Y., Murray, J., and Hannoush, R. N. (2012) Allosteric peptides bind a caspase zymogen and mediate caspase tetramerization. Nat. Chem. Biol. 8, 655-660
49. Changeux, J. P. (2012) Allostery and the Monod-Wyman-Changeux model after 50 years. Annu. Rev. Biophys. 41, 103-133
50. Gohara, D. W., and Di Cera, E. (2011) Allostery in trypsin-like proteases suggests new therapeutic strategies. Trends Biotechnol. 29, 577-585
51. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (Pubitemid 350162903)
52. Mitchell, C. A., Shi, C., Aldrich, C. C., and Gulick, A. M. (2012) Structure of PA1221, a nonribosomal peptide synthetase containing adenylation and peptidyl carrier protein domains. Biochemistry 51, 3252-3263
53. Sundlov, J. A., Shi, C., Wilson, D. J., Aldrich, C. C., and Gulick, A. M. (2012) Structural and functional investigation of the intermolecular interaction between NRPS adenylation and carrier protein domains. Chem. Biol. 19, 188-198