Cyanobacterial polyketide synthase docking domains: A tool for engineering natural product biosynthesis

Chemistry and Biology

Volumn 20, Issue 11, 2013, Pages 1340-1351

  Whicher, Jonathan R ^a   Smaga, Sarah S ^a   Hansen, Douglas A ^a   Brown, William C ^a   Gerwick, William H ^c,d   Sherman, David H ^a,b   Smith, Janet L ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NATURAL PRODUCT; POLYKETIDE SYNTHASE; BIOLOGICAL PRODUCT; PEPTIDE SYNTHASE;

ARTICLE; BIOENGINEERING; BIOSYNTHESIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYANOBACTERIUM; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN ENGINEERING; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

CYANOBACTERIA;

BIOLOGICAL PRODUCTS; CRYSTALLOGRAPHY, X-RAY; CYANOBACTERIA; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PEPTIDE SYNTHASES; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY;

EID: 84888293028     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.09.015     Document Type: Article

References (49)

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.L. Akey, J.R. Razelun, J. Tehranisa, D.H. Sherman, W.H. Gerwick, and J.L. Smith Crystal structures of dehydratase domains from the curacin polyketide biosynthetic pathway Structure 18 2010 94 105
3. J.F. Aparicio, P. Caffrey, A.F. Marsden, J. Staunton, and P.F. Leadlay Limited proteolysis and active-site studies of the first multienzyme component of the erythromycin-producing polyketide synthase J. Biol. Chem. 269 1994 8524 8528
4. B.J. Beck, C.C. Aldrich, R.A. Fecik, K.A. Reynolds, and D.H. Sherman Iterative chain elongation by a pikromycin monomodular polyketide synthase J. Am. Chem. Soc. 125 2003 4682 4683
5. G. Bricogne, E. Blanc, M. Brandl, C. Flensburg, P. Keller, W. Paciorek, P. Roversi, A. Sharff, O.S. Smart, C. Vonrhein, and T.O. Womack BUSTER, Version 2.9 2011 Global Phasing Cambridge, UK
6. R.W. Broadhurst, D. Nietlispach, M.P. Wheatcroft, P.F. Leadlay, and K.J. Weissman The structure of docking domains in modular polyketide synthases Chem. Biol. 10 2003 723 731
7. T.J. Buchholz, T.W. Geders, F.E. Bartley 3rd, K.A. Reynolds, J.L. Smith, and D.H. Sherman Structural basis for binding specificity between subclasses of modular polyketide synthase docking domains ACS Chem. Biol. 4 2009 41 52
8. Z. Chang, N. Sitachitta, J.V. Rossi, M.A. Roberts, P.M. Flatt, J. Jia, D.H. Sherman, and W.H. Gerwick Biosynthetic pathway and gene cluster analysis of curacin A, an antitubulin natural product from the tropical marine cyanobacterium Lyngbya majuscula J. Nat. Prod. 67 2004 1356 1367
9. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
10. I.W. Davis, L.W. Murray, J.S. Richardson, and D.C. Richardson MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes Nucleic Acids Res. 32 Web Server issue 2004 W615 W619
11. J. DelProposto, C.Y. Majmudar, J.L. Smith, and W.C. Brown Mocr: a novel fusion tag for enhancing solubility that is compatible with structural biology applications Protein Expr. Purif. 63 2009 40 49
12. S. Donadio, M.J. Staver, J.B. McAlpine, S.J. Swanson, and L. Katz Modular organization of genes required for complex polyketide biosynthesis Science 252 1991 675 679
13. M.I. Donnelly, M. Zhou, C.S. Millard, S. Clancy, L. Stols, W.H. Eschenfeldt, F.R. Collart, and A. Joachimiak An expression vector tailored for large-scale, high-throughput purification of recombinant proteins Protein Expr. Purif. 47 2006 446 454
14. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797
15. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
16. 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
17. H.G. Floss Combinatorial biosynthesis - potential and problems J. Biotechnol. 124 2006 242 257
18. R.S. Gokhale, S.Y. Tsuji, D.E. Cane, and C. Khosla Dissecting and exploiting intermodular communication in polyketide synthases Science 284 1999 482 485
19. D.A. Hansen, C.M. Rath, E.B. Eisman, A.R. Narayan, J.D. Kittendorf, J.D. Mortison, Y.J. Yoon, and D.H. Sherman Biocatalytic synthesis of pikromycin, methymycin, neomethymycin, novamethymycin, and ketomethymycin J. Am. Chem. Soc. 135 2013 11232 11238
20. A. Keatinge-Clay Crystal structure of the erythromycin polyketide synthase dehydratase J. Mol. Biol. 384 2008 941 953
21. J.D. Kittendorf, and D.H. Sherman Developing tools for engineering hybrid polyketide synthetic pathways Curr. Opin. Biotechnol. 17 2006 597 605
22. J.D. Kittendorf, B.J. Beck, T.J. Buchholz, W. Seufert, and D.H. Sherman Interrogating the molecular basis for multiple macrolactone ring formation by the pikromycin polyketide synthase Chem. Biol. 14 2007 944 954
23. P. Kumar, Q. Li, D.E. Cane, and C. Khosla Intermodular communication in modular polyketide synthases: structural and mutational analysis of linker mediated protein-protein recognition J. Am. Chem. Soc. 125 2003 4097 4102
24. H.G. Menzella, and C.D. Reeves Combinatorial biosynthesis for drug development Curr. Opin. Microbiol. 10 2007 238 245
25. H.G. Menzella, R. Reid, J.R. Carney, S.S. Chandran, S.J. Reisinger, K.G. Patel, D.A. Hopwood, and D.V. Santi Combinatorial polyketide biosynthesis by de novo design and rearrangement of modular polyketide synthase genes Nat. Biotechnol. 23 2005 1171 1176
26. H.G. Menzella, J.R. Carney, and D.V. Santi Rational design and assembly of synthetic trimodular polyketide synthases Chem. Biol. 14 2007 143 151
27. 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
28. D.J. Newman, and G.M. Cragg Natural products as sources of new drugs over the last 25 years J. Nat. Prod. 70 2007 461 477
29. Z. Otwinowski, and V. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
30. B.A. Pfeifer, S.J. Admiraal, H. Gramajo, D.E. Cane, and C. Khosla Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli Science 291 2001 1790 1792
31. C.D. Reeves, S.L. Ward, W.P. Revill, H. Suzuki, M. Marcus, O.V. Petrakovsky, S. Marquez, H. Fu, S.D. Dong, and L. Katz Production of hybrid 16-membered macrolides by expressing combinations of polyketide synthase genes in engineered Streptomyces fradiae hosts Chem. Biol. 11 2004 1465 1472
32. M.D. Scholle, F.R. Collart, and B.K. Kay In vivo biotinylated proteins as targets for phage-display selection experiments Protein Expr. Purif. 37 2004 243 252
33. D.H. Sherman The Lego-ization of polyketide biosynthesis Nat. Biotechnol. 23 2005 1083 1084
34. J. Staunton, P. Caffrey, J.F. Aparicio, G.A. Roberts, S.S. Bethell, and P.F. Leadlay Evidence for a double-helical structure for modular polyketide synthases Nat. Struct. Biol. 3 1996 188 192
35. Y. Tang, C.Y. Kim, I.I. Mathews, D.E. Cane, and C. Khosla The 2.7-Angstrom crystal structure of a 194-kDa homodimeric fragment of the 6-deoxyerythronolide B synthase Proc. Natl. Acad. Sci. USA 103 2006 11124 11129
36. Y. Tang, A.Y. Chen, C.Y. Kim, D.E. Cane, and C. Khosla Structural and mechanistic analysis of protein interactions in module 3 of the 6-deoxyerythronolide B synthase Chem. Biol. 14 2007 931 943
37. T.C. Terwilliger Automated main-chain model building by template matching and iterative fragment extension Acta Crystallogr. D Biol. Crystallogr. 59 2003 38 44
38. M. Thattai, Y. Burak, and B.I. Shraiman The origins of specificity in polyketide synthase protein interactions PLoS Comput. Biol. 3 2007 1827 1835
39. S.Y. Tsuji, D.E. Cane, and C. Khosla Selective protein-protein interactions direct channeling of intermediates between polyketide synthase modules Biochemistry 40 2001 2326 2331
40. C.T. Walsh Combinatorial biosynthesis of antibiotics: challenges and opportunities ChemBioChem 3 2002 125 134
41. J.W. Wang, J.R. Chen, Y.X. Gu, C.D. Zheng, F. Jiang, H.F. Fan, T.C. Terwilliger, and Q. Hao SAD phasing by combination of direct methods with the SOLVE/RESOLVE procedure Acta Crystallogr. D Biol. Crystallogr. 60 2004 1244 1253
42. S.D. Weeks, M. Drinker, and P.J. Loll Ligation independent cloning vectors for expression of SUMO fusions Protein Expr. Purif. 53 2007 40 50
43. K.J. Weissman Single amino acid substitutions alter the efficiency of docking in modular polyketide biosynthesis ChemBioChem 7 2006 1334 1342
44. K.J. Weissman The structural basis for docking in modular polyketide biosynthesis ChemBioChem 7 2006 485 494
45. N. Wu, S.Y. Tsuji, D.E. Cane, and C. Khosla Assessing the balance between protein-protein interactions and enzyme-substrate interactions in the channeling of intermediates between polyketide synthase modules J. Am. Chem. Soc. 123 2001 6465 6474
46. N. Wu, D.E. Cane, and C. Khosla Quantitative analysis of the relative contributions of donor acyl carrier proteins, acceptor ketosynthases, and linker regions to intermodular transfer of intermediates in hybrid polyketide synthases Biochemistry 41 2002 5056 5066
47. Y. Xue, L. Zhao, H.W. Liu, and D.H. Sherman A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: architecture of metabolic diversity Proc. Natl. Acad. Sci. USA 95 1998 12111 12116
48. J. Yan, S. Gupta, D.H. Sherman, and K.A. Reynolds Functional dissection of a multimodular polypeptide of the pikromycin polyketide synthase into monomodules by using a matched pair of heterologous docking domains ChemBioChem 10 2009 1537 1543
49. J. Zheng, C.D. Fage, B. Demeler, D.W. Hoffman, and A.T. Keatinge-Clay The missing linker: A dimerization motif located within polyketide synthase modules ACS Chem. Biol. 8 2013 1263 1270