Interdomain and Intermodule Organization in Epimerization Domain Containing Nonribosomal Peptide Synthetases

ACS Chemical Biology

Volumn 11, Issue 8, 2016, Pages 2293-2303

  Chen, Wei Hung ^a   Li, Kunhua ^a   Guntaka, Naga Sandhya ^a   Bruner, Steven D ^a  

^a University of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APO PROTEIN; GRAMICIDIN A; GRAMICIDIN B; GRAMICIDIN S SYNTHETASE; HOLO PROTEIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; PANTETHEINE PHOSPHATE; PEPTIDYL CARRIER PROTEIN; UNCLASSIFIED DRUG; PEPTIDE SYNTHASE; PIPERAZINEDIONE;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; EPIMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; GENETICS; ISOMERISM; METABOLISM; SITE DIRECTED MUTAGENESIS;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DIKETOPIPERAZINES; ISOMERISM; MUTAGENESIS, SITE-DIRECTED; PEPTIDE SYNTHASES; PROTEIN CONFORMATION;

EID: 84983346275     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b00332     Document Type: Article

References (57)

1. Fischbach, M. A. and Walsh, C. T. (2006) Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms Chem. Rev. 106, 3468-3496 10.1021/cr0503097
2. Strieker, M., Tanović, A., and Marahiel, M. A. (2010) Nonribosomal peptide synthetases: structures and dynamics Curr. Opin. Struct. Biol. 20, 234-240 10.1016/j.sbi.2010.01.009
3. Meier, J. L. and Burkart, M. D. (2009) The chemical biology of modular biosynthetic enzymes Chem. Soc. Rev. 38, 2012-2045 10.1039/b805115c
4. Finking, R. and Marahiel, M. A. (2004) Biosynthesis of nonribosomal peptides Annu. Rev. Microbiol. 58, 453-488 10.1146/annurev.micro.58.030603.123615
5. Raymond, K. N., Dertz, E. A., and Kim, S. S. (2003) Enterobactin: an archetype for microbial iron transport Proc. Natl. Acad. Sci. U. S. A. 100, 3584-3588 10.1073/pnas.0630018100
6. Walsh, C. T. (2000) Molecular mechanisms that confer antibacterial drug resistance Nature 406, 775-781 10.1038/35021219
7. Wandersman, C. and Delepelaire, P. (2004) Bacterial iron sources: from siderophores to hemophores Annu. Rev. Microbiol. 58, 611-647 10.1146/annurev.micro.58.030603.123811
8. Kratzschmar, J., Krause, M., and Marahiel, M. A. (1989) Gramicidin-S biosynthesis operon containing the structural genes grsA and grsB has an open reading frame encoding a protein homologous to fatty-acid thioesterases J. Bacteriol. 171, 5422-5429
9. Marahiel, M. A., Stachelhaus, T., and Mootz, H. D. (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis Chem. Rev. 97, 2651-2674 10.1021/cr960029e
10. Mootz, H. D., Schwarzer, D., and Marahiel, M. A. (2002) Ways of assembling complex natural products on modular nonribosomal peptide synthetases ChemBioChem 3, 490-504 10.1002/1439-7633(20020603)3:6<490::AID-CBIC490>3.0.CO;2-N
11. Hur, G. H., Vickery, C. R., and Burkart, M. D. (2012) Explorations of catalytic domains in non-ribosomal peptide synthetase enzymology Nat. Prod. Rep. 29, 1074-1098 10.1039/c2np20025b
12. Peypoux, F., Bonmatin, J. M., and Wallach, J. (1999) Recent trends in the biochemistry of surfactin Appl. Microbiol. Biotechnol. 51, 553-563 10.1007/s002530051432
13. Radkov, A. D. and Moe, L. A. (2014) Bacterial synthesis of D-amino acids Appl. Microbiol. Biotechnol. 98, 5363-5374 10.1007/s00253-014-5726-3
14. Cava, F., Lam, H., de Pedro, M. A., and Waldor, M. K. (2011) Emerging knowledge of regulatory roles of D-amino acids in bacteria Cell. Mol. Life Sci. 68, 817-831 10.1007/s00018-010-0571-8
15. Linne, U., Doekel, S., and Marahiel, M. A. (2001) Portability of epimerization domain and role of peptidyl carrier protein on epimerization activity in nonribosomal peptide synthetases Biochemistry 40, 15824-15834 10.1021/bi011595t
16. Stachelhaus, T. and Walsh, C. T. (2000) Mutational analysis of the epimerization domain in the initiation module PheATE of gramicidin S synthetase Biochemistry 39, 5775-5787 10.1021/bi9929002
17. Tanner, M. E. (2002) Understanding Nature's strategies for enzyme-catalyzed racemization and epimerization racemization at an activated center Acc. Chem. Res. 35, 237-246 10.1021/ar000056y
18. Luo, L., Burkart, M. D., Stachelhaus, T., and Walsh, C. T. (2001) Substrate recognition and selection by the initiation module PheATE of gramicidin S synthetase J. Am. Chem. Soc. 123, 11208-11218 10.1021/ja0166646
19. Stachelhaus, T. and Walsh, C. T. (2000) Mutational analysis of the epimerization domain in the initiation module PheATE of gramicidin S synthetase Biochemistry 39, 5775-5787 10.1021/bi9929002
20. Linne, U. and Marahiel, M. A. (2000) Control of directionality in nonribosomal peptide synthesis: role of the condensation domain in preventing misinitiation and timing of epimerization Biochemistry 39, 10439-10447 10.1021/bi000768w
21. Keating, T. A., Marshall, C. G., Walsh, C. T., and Keating, A. E. (2002) The structure of VibH represents nonribosomal peptide synthetase condensation, cyclization and epimerization domains Nat. Struct. Biol. 9, 522-526 10.1038/nsb810
22. Samel, S. A., Czodrowski, P., and Essen, L. O. (2014) Structure of the epimerization domain of tyrocidine synthetase A Acta Crystallogr., Sect. D: Biol. Crystallogr. 70, 1442-1452 10.1107/S1399004714004398
23. Weissman, K. J. (2015) The structural biology of biosynthetic megaenzymes Nat. Chem. Biol. 11, 660-670 10.1038/nchembio.1883
24. Strieker, M., Tanović, A., and Marahiel, M. A. (2010) Nonribosomal peptide synthetases: structures and dynamics Curr. Opin. Struct. Biol. 20, 234-240 10.1016/j.sbi.2010.01.009
25. Winter, J. M. and Tang, Y. (2014) Natural products: getting a handle on peptides Nat. Chem. 6, 1037-1038 10.1038/nchem.2117
26. Winn, M., Fyans, J. K., Zhuo, Y., and Micklefield, J. (2016) Recent advances in engineering nonribosomal peptide assembly lines Nat. Prod. Rep. 33, 317-347 10.1039/C5NP00099H
27. Conti, E., Stachelhaus, T., Marahiel, M. A., and Brick, P. (1997) Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S EMBO J. 16, 4174-4183 10.1093/emboj/16.14.4174
28. Koglin, A., Mofid, M. R., Löhr, F., Schäfer, B., Rogov, V. V., Blum, M. M., Mittag, T., Marahiel, M. A., Bernhard, F., and Dötsch, V. (2006) Conformational switches modulate protein interactions in peptide antibiotic synthetases Science 312, 273-276 10.1126/science.1122928
29. Volkman, B. F., Zhang, Q., Debabov, D. V., Rivera, E., Kresheck, G. C., and Neuhaus, F. C. (2001) Biosynthesis of D-alanyl-lipoteichoic acid: the tertiary structure of apo D-alanyl carrier protein Biochemistry 40, 7964-7972 10.1021/bi010355a
30. Lohman, J. R., Ma, M., Cuff, M. E., Bigelow, L., Bearden, J., Babnigg, G., Joachimiak, A., Phillips, G. N., and Shen, B. (2014) The crystal structure of BlmI as a model for nonribosomal peptide synthetase peptidyl carrier proteins Proteins: Struct., Funct., Genet. 82, 1210-1218 10.1002/prot.24485
31. 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 10.1126/science.1159850
32. Liu, Y., Zheng, T., and Bruner, S. D. (2011) Structural basis for phosphopantetheinyl carrier domain interactions in the terminal module of nonribosomal peptide synthetases Chem. Biol. 18, 1482-1488 10.1016/j.chembiol.2011.09.018
33. 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 10.1016/j.chembiol.2011.11.013
34. 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 10.1021/bi300112e
35. Samel, S. A., Schoenafinger, G., Knappe, T. A., Marahiel, M. A., and Essen, L.-O. (2007) Structural and functional insights into a peptide bond-forming bidomain from a nonribosomal peptide synthetase Structure 15, 781-792 10.1016/j.str.2007.05.008
36. Drake, E. J., Miller, B. R., Shi, C., Tarrasch, J. T., Sundlov, J. A., Allen, C. L., Skiniotis, G., Aldrich, C. C., and Gulick, A. M. (2016) Structures of two distinct conformations of holo non-ribosomal peptide synthetases Nature 529, 235-238 10.1038/nature16163
37. Reimer, J. M., Aloise, M. N., Harrison, P. M., and Schmeing, T. M. (2016) Synthetic cycle of the initiation module of a formylating nonribosomal peptide synthetase Nature 529, 239-242 10.1038/nature16503
38. Hahn, M. and Stachelhaus, T. (2004) Selective interaction between nonribosomal peptide synthetases is facilitated by short communication-mediating domains Proc. Natl. Acad. Sci. U. S. A. 101, 15585-15590 10.1073/pnas.0404932101
39. 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 10.1016/j.chembiol.2011.11.013
40. Hur, G. H., Meier, J. L., Baskin, J., Codelli, J. A., Bertozzi, C. R., Marahiel, M. A., and Burkart, M. D. (2009) Crosslinking studies of protein-protein interactions in nonribosomal peptide biosynthesis Chem. Biol. 16, 372-381 10.1016/j.chembiol.2009.02.009
41. Quadri, L. E. N., Weinreb, P. H., Lei, M., Nakano, M. M., Zuber, P., and Walsh, C. T. (1998) Characterization of Sfp, a Bacillus subtilis phosphopantetheinyl transferase for peptidyl carrier protein domains in peptide synthetases Biochemistry 37, 1585-1595 10.1021/bi9719861
42. Kabsch, W. (2010) XDS Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 125-132 10.1107/S0907444909047337
43. 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. W., 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 CCP 4 suite and current developments Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 235-242 10.1107/S0907444910045749
44. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221 10.1107/S0907444909052925
45. Sheldrick, G. M. (2010) Experimental phasing with SHELXC /D /E: combining chain tracing with density modification Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 479-485 10.1107/S0907444909038360
46. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132 10.1107/S0907444904019158
47. The PyMOL Molecular Graphics System, Version 1.7.4 Schrödinger, LLC.
48. Laskowski, R. A. and Swindells, M. B. (2011) LigPlot+: multiple ligand-protein interaction diagrams for drug discovery J. Chem. Inf. Model. 51, 2778-2786 10.1021/ci200227u
49. Bergendahl, V., Linne, U., and Marahiel, M. A. (2002) Mutational analysis of the C-domain in nonribosomal peptide synthesis Eur. J. Biochem. 269, 620-629 10.1046/j.0014-2956.2001.02691.x
50. Kries, H., Wachtel, R., Pabst, A., Wanner, B., Niquille, D., and Hilvert, D. (2014) Reprogramming Nonribosomal Peptide Synthetases for "Clickable" Amino Acids Angew. Chem., Int. Ed. 53, 10105-10108 10.1002/anie.201405281
51. Leslie, A. G., Moody, P. C., and Shaw, W. V. (1988) Structure of chloramphenicol acetyltransferase at 1.75- angstrom resolution Proc. Natl. Acad. Sci. U. S. A. 85, 4133-4137 10.1073/pnas.85.12.4133
52. Nishina, Y., Sato, K., Tamaoki, H., Tanaka, T., Miura, R., and Shiga, K. (2003) Molecular mechanism of the drop in the pKa of a substrate analog bound to medium-chain acyl-CoA dehydrogenase: implications for substrate activation J. Biochem. 134, 835-842 10.1093/jb/mvg209
53. Koglin, A. and Walsh, C. T. (2009) Structural insights into nonribosomal peptide enzymatic assembly lines Nat. Prod. Rep. 26, 987-1000 10.1039/b904543k
54. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372, 774-797 10.1016/j.jmb.2007.05.022
55. Drake, E. J., Nicolai, D. A., and Gulick, A. M. (2006) Structure of the EntB multidomain nonribosomal peptide synthetase and functional analysis of its interaction with the EntE adenylation domain Chem. Biol. 13, 409-419 10.1016/j.chembiol.2006.02.005
56. Balibar, C. J., Vaillancourt, F. H., and Walsh, C. T. (2005) Generation of D amino acid residues in assembly of arthrofactin by dual condensation/epimerization domains Chem. Biol. 12, 1189-1200 10.1016/j.chembiol.2005.08.010
57. Rausch, C., Hoof, I., Weber, T., Wohlleben, W., and Huson, D. H. (2007) Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution BMC Evol. Biol. 7, 78 10.1186/1471-2148-7-78