Evidence for a Protein-Protein Interaction Motif on an Acyl Carrier Protein Domain from a Modular Polyketide Synthase

Chemistry and Biology

Volumn 13, Issue 6, 2006, Pages 625-636

  Weissman, Kira J ^a   Hong, Hui ^a   Popovic, Bojana ^a   Meersman, Filip ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

CHEMBIO

Indexed keywords

ACYL CARRIER PROTEIN; BACTERIAL PROTEIN; ERYTHROMYCIN; PHOSPHOPANTETHEINYL TRANSFERASE; PHOSPHOTRANSFERASE; POLYKETIDE SYNTHASE;

ARTICLE; BACILLUS SUBTILIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY;

ACYL CARRIER PROTEIN; AMINO ACID MOTIFS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CONSERVED SEQUENCE; ERYTHROMYCIN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; POLYKETIDE SYNTHASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

EID: 33745200262     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2006.04.010     Document Type: Article

References (60)

1. Staunton J., and Weissman K.J. Polyketide biosynthesis: a millennium review. Nat. Prod. Rep. 18 (2001) 380-416
2. Walsh C.T. Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303 (2004) 1805-1810
3. Weissman K.J., and Leadlay P.F. Combinatorial biosynthesis of reduced polyketides. Nat. Rev. Microbiol. 3 (2005) 925-936
4. Tsai S.C., Miercke L.J., Krucinski J., Gokhale R., Chen J.C., Foster P.G., Cane D.E., Khosla C., and Stroud R.M. Crystal structure of the macrocycle-forming thioesterase domain of the erythromycin polyketide synthase: versatility from a unique substrate channel. Proc. Natl. Acad. Sci. USA 98 (2001) 14808-14813
5. Staunton J., Caffrey P., Aparicio J.F., Roberts G.A., Bethell S.S., and Leadlay P.F. Evidence for a double-helical structure for modular polyketide synthases. Nat. Struct. Biol. 3 (1996) 188-192
6. Worsham L.M., Earls L., Jolly C., Langston K.G., Trent M.S., and Ernst-Fonberg M.L. Amino acid residues of Escherichia coli acyl carrier protein involved in heterologous protein interactions. Biochemistry 42 (2003) 167-176
7. Asturias F.J., Chadick J.Z., Cheung I.K., Stark H., Witkowski A., Joshi A.K., and Smith S. Structure and molecular organization of mammalian fatty acid synthase. Nat. Struct. Mol. Biol. 12 (2005) 225-232
8. Schneider G. Enzymes in the biosynthesis of aromatic polyketide antibiotics. Curr. Opin. Struct. Biol. 15 (2005) 629-636
9. Findlow S.C., Winsor C., Simpson T.J., Crosby J., and Crump M.P. Solution structure and dynamics of oxytetracycline polyketide synthase acyl carrier protein from Streptomyces rimosus. Biochemistry 42 (2003) 8423-8433
10. Holak T.A., Kearsley S.K., Kim Y., and Prestegard J.H. Three-dimensional structure of acyl carrier protein determined by NMR pseudoenergy and distance geometry calculations. Biochemistry 27 (1988) 6135-6142
11. Kim Y., and Prestegard J.H. A dynamic model for the structure of acyl carrier protein in solution. Biochemistry 28 (1989) 8792-8797
12. Xu G.Y., Tam A., Lin L., Hixon J., Fritz C.C., and Powers R. Solution structure of B. subtilis acyl carrier protein. Structure (Camb) 9 (2001) 277-287
13. Reed M.A., Schweizer M., Szafranska A.E., Arthur C., Nicholson T.P., Cox R.J., Crosby J., Crump M.P., and Simpson T.J. The type I rat fatty acid synthase ACP shows structural homology and analogous biochemical properties to type II ACPs. Org. Biomol. Chem. 1 (2003) 463-471
14. Lambalot R.H., Gehring A.M., Flugel R.S., Zuber P., LaCelle M., Marahiel M.A., Reid R., Khosla C., and Walsh C.T. A new enzyme superfamily - the phosphopantetheinyl transferases. Chem. Biol. 3 (1996) 923-926
15. Zhang Y.-M., Rao M.S., Heath R.J., Price A.C., Olson A.J., Rock C.O., and White S.W. Identification and analysis of the acyl carrier protein (ACP) docking site on β-ketoacyl-ACP synthase III. J. Biol. Chem. 276 (2001) 8231-8238
16. Zhang Y.-M., Wu B., Zheng J., and Rock C.O. Key residues responsible for acyl carrier protein and β-ketoacyl-ACP reductase (FabG) interaction. J. Biol. Chem. 278 (2003) 52935-52943
17. Zhang Y.-M., Marrakchi H., White S.W., and Rock C.O. The application of computational methods to explore the diversity and structure of bacterial fatty acid synthase. Prog. Lipid Res. 44 (2003) 1-10
18. Hadfield A.T., Limpkin C., Tertasin W., Simpson T.J., Crosby J., and Crump M.P. The crystal structure of the actIII actinorhodin polyketide reductase: proposed mechanism for ACP and polyketide binding. Structure 12 (2004) 1865-1875
19. Gokhale R.S., Lau J., Cane D.E., and Khosla C. Functional orientation of the acyltransferase domain in a module of the erythromycin polyketide synthase. Biochemistry 37 (1998) 2524-2528
20. Joshi A.K., Rangan V.S., Witkowski A., and Smith S. Engineering of an active animal fatty acid synthase dimer with only one competent subunit. Chem. Biol. 10 (2003) 169-173
21. Weissman K.J., Hong H., Oliynyk M., Siskos A.P., and Leadlay P.F. Identification of a phosphopantetheinyl transferase for erythromycin biosynthesis in Saccharopolyspora erythraea. ChemBioChem 5 (2004) 116-125
22. Quadri L.E., Weinreb P.H., Lei M., Nakano M.M., Zuber P., and Walsh C.T. Characterization of Sfp, a Bacillus subtilis phosphopantetheinyl transferase for peptidyl carrier protein domains in peptide synthetases. Biochemistry 37 (1998) 1585-1595
23. Pfeifer B.A., Admiraal S.J., Gramajo H., Cane D.E., and Khosla C. Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science 291 (2001) 1790-1792
24. Flaman A.S., Chen J.M., Van Iderstine S.C., and Byers D.M. Site-directed mutagenesis of acyl carrier protein (ACP) reveals amino acid residues involved in ACP structure and acyl-ACP synthetase activity. J. Biol. Chem. 276 (2001) 35934-35939
25. Gong H., and Byers D.M. Glutamate-41 of Vibrio harveyi acyl carrier protein is essential for fatty acid synthase but not acyl-ACP synthetase activity. Biochem. Biophys. Res. Commun. 302 (2003) 35-40
26. Parris K.D., Lin L., Tam A., Mathew R., Hixon J., Stahl M., Fritz C.C., Seehra J., and Somers W.S. 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
27. Finking R., Mofid M.R., and Marahiel M.A. Mutational analysis of peptidyl carrier protein and acyl carrier protein synthase unveils residues involved in protein-protein recognition. Biochemistry 43 (2004) 8946-8956
28. Mofid M.R., Finking R., and Marahiel M.A. Recognition of hybrid peptidyl carrier proteins/acyl carrier proteins in nonribosomal peptide synthetase modules by the 4′-phosphopantetheinyl transferases AcpS and Sfp. J. Biol. Chem. 277 (2002) 17023-17031
29. Wong H.C., Liu G., Zhang Y.-M., Rock C.O., and Zheng Z. The solution structure of acyl carrier protein from Mycobacterium tuberculosis. J. Biol. Chem. 277 (2002) 15874-15880
30. Goldman-Fischman S., and Honig B. Structural genomics: computational methods for structure analysis. Protein Sci. 12 (2003) 1813-1821
31. st century. Curr. Opin. Chem. Biol. 15 (2005) 15-22
32. Shi J., Blundell T.L., and Mizuguchi K. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310 (2001) 243-257
33. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
34. Fischer D., Barret C., Bryson K., Elofsson A., Godzik A., Jones D., Karplus K.J., Kelley L.A., Maccallum R.M., Pawowski K., et al. CAFASP-1: critical assessment of fully automated structure prediction methods. Proteins Suppl. 3 (1999) 209-217
35. Kelley L.A., Maccallum R., and Sternberg M.J. Recognition of remote protein homologies using three-dimensional information to generate a position specific scoring matrix in the program 3D-PSSM. In: Istrail S., Pevzner P., and Waterman M. (Eds). RECOMB 99, Proceedings of the Third Annual Conference on Computational Molecular Biology (1999), The Association for Computing Machinery, New York 218-225
36. Kelley L.A., MacCallum R.M., and Sternberg M.J. Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299 (2000) 499-520
37. Sali A., Potterton L., Yuan F., van Vlijmen H., and Karplus M. Evaluation of comparative protein modeling by MODELLER. Proteins 23 (1995) 318-326
38. Caffrey P., Green B., Packman L.C., Rawlings B.J., Staunton J., and Leadlay P.F. An acyl-carrier-protein-thioesterase domain from the 6-deoxyerythronolide B synthase of Saccharopolyspora erythraea. High-level production, purification and characterisation in Escherichia coli. Eur. J. Biochem. 195 (1991) 823-830
39. Brikun I.A., Reeves A.R., Cernota W.H., Luu M.B., and Weber J.M. The erythromycin biosynthetic gene cluster of Aeromicrobium erythreum. J. Ind. Microbiol. Biotechnol. 31 (2004) 335-344
40. Byler D.M., and Susi H. Examination of the secondary structure of proteins by deconvoluted FTIR spectra. Biopolymers 25 (1996) 469-487
41. Jackson M., and Mantsch H.H. The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit. Rev. Biochem. Mol. Biol. 30 (1995) 95-120
42. Sreerama N., Venyaminov S.Y., and Woody R.W. Estimation of protein secondary structure from CD spectra: inclusion of denatured proteins with native protein in the analysis. Anal. Biochem. 287 (2000) 243-251
43. Whitmore L., and Wallace B.A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32 (2004) W668-W673
44. Yin J., Straight P.D., McLoughlin S.M., Zhou Z., Lin A.J., Golan D.E., Kelleher N.L., Kolter R., and Walsh C.T. Genetically encoded short peptide tag for versatile protein labeling by Sfp phosphopantetheinyl transferase. Proc. Natl. Acad. Sci. USA 102 (2005) 15815-15820
45. Mofid M.R., Finking R., Essen L.O., and Marahiel M.A. Structure-based mutational analysis of the 4′-phosphopantetheinyl transferase Sfp from Bacillus subtilis: carrier protein recognition and reaction mechanism. Biochemistry 43 (2004) 4128-4136
46. Flugel R.S., Hwangbo Y., Lambalot R.H., Cronan Jr. J.E., and Walsh C.T. Holo-(acyl carrier protein) synthase and phosphopantetheinyl transfer in Escherichia coli. J. Biol. Chem. 275 (2000) 959-968
47. Sánchez C., Du L., Edwards D.J., Toney M.D., and Shen B. Cloning and characterization of a phosphopantetheinyl transferase from Streptomyces verticillus ATCC15003, the producer of the hybrid peptide-polyketide antitumor drug bleomycin. Chem. Biol. 8 (2001) 725-738
48. McAllister K.A., Peery R.B., Meier T.I., Fischl A.S., and Zhao G. Biochemical and molecular analyses of the Streptococcus pneumoniae acyl carrier protein synthase, an enzyme essential for fatty acid biosynthesis. J. Biol. Chem. 275 (2000) 30864-30872
49. Lambalot R.H., and Walsh C.T. Cloning, overproduction, and characterization of the Escherichia coli holo-acyl carrier protein synthase. J. Biol. Chem. 270 (1995) 24658-24661
50. Maier T., Jenni S., and Ban N. Architecture of mammalian fatty acid synthase at 4.5 Å resolution. Science 311 (2006) 1258-1262
51. Ansari M.Z., Yadav G., Gokhale R.S., and Mohanty D. NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res. 32 (2004) W405-W413
52. In: Sambrook J., Fritsch E.F., and Maniatis T. (Eds). Molecular Cloning: A Laboratory Manual (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
53. Miguel R.N., Shi J., and Mizuguchi K. Protein fold recognition and comparative modeling using HOMSTRAD, JOY and FUGUE. In: Tsigelny I. (Ed). Protein Structure Prediction: Bioinformatic Approach (2002), International University Line [IUL] Publishers, La Jolla, CA 143-169
54. Mizuguchi K., Deane C.M., Blundell T.L., and Overington J.P. HOMSTRAD: a database of protein structure alignments for homologous families. Protein Sci. 7 (1998) 2469-2471
55. de Bakker P.I., DePristo M.A., Burke D.F., and Blundell T.L. Ab initio construction of polypeptide fragments: accuracy of loop decoy discrimination by an all-atom statistical potential and the AMBER force field with the Generalized Born solvation model. Proteins 51 (2003) 21-40
56. Deane C.M., and Blundell T.L. CODA: a combined algorithm for predicting the structurally variable regions of protein models. Protein Sci. 10 (2001) 599-612
57. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
58. Eisenberg D., Luthy R., and Bowie J.U. VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol. 277 (1997) 396-404
59. Li Y., Llewellyn N.M., Giri R., Huang F., and Spencer J.B. Biosynthesis of the unique amino acid side chain of butirosin: possible protective-group chemistry in an acyl carrier protein-mediated pathway. Chem. Biol. 12 (2005) 665-675
60. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 11 (1994) 4673-4680