Solution structure and dynamics of oxytetracycline polyketide synthase acyl carrier protein from Streptomyces rimosus

Biochemistry

Volumn 42, Issue 28, 2003, Pages 8423-8433

  Findlow, Stuart C ^a   Winsor, Claire ^a   Simpson, Thomas J ^b   Crosby, John ^b   Crump, Matthew P ^a,b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BIOSYNTHESIS; NUCLEAR MAGNETIC RESONANCE; PROTEINS; SIMULATED ANNEALING;

PROTEIN-PROTEIN INTERACTIONS;

BIOCHEMISTRY;

ACYL CARRIER PROTEIN; CARRIER PROTEIN; FATTY ACID SYNTHASE; OXYTETRACYCLINE; POLYKETIDE SYNTHASE; POLYKETIDE SYNTHASE ACYL CARRIER PROTEIN; POLYKETIDE SYNTHASE II; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME STRUCTURE; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; STREPTOMYCES; STREPTOMYCES RIMOSUS;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BINDING SITES; CARRIER PROTEINS; ESCHERICHIA COLI; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; OXYTETRACYCLINE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SOLUTIONS; STREPTOMYCES;

STREPTOMYCES; STREPTOMYCES RIMOSUS;

EID: 0038457084     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0342259     Document Type: Article

References (51)

1. Finlay, A. C., Hobby, G. L., P'an, S. Y., Regna, P. P., Routien, J. B., Seeley, D. B., Shull, G. M., Sobin, B. A., Solomons, I. A., Vinson, J. W., and Kane, J. H. (1950) Terramycin, a new antibiotic, Science 111, 85.
2. Hochstein, F. A., Stevens, C. R., Conover, L. H., Regna, P. F., Pasternack, R., Gordon, P. N., Pilgrim, F. J., Brunings, K. J., and Woodward, R. B. (1953) The structure of terramycin, J. Am. Chem. Soc. 75, 5455-5475.
3. Silver, L., and Bostian, K. (1990) Screening of natural products for antimicrobial agents, Eur. J. Clin. Microbiol. Infect. Dis. 9, 455-461.
4. O'Hagan, D. (1991) in The Polyketide Metabolites (Mellor, J., Ed.) Ellis Horwood Series in Organic Chemistry, Ellis Horwood Limited, Chichester, U.K.
5. Barden, T. C., Buckwalter, B. L., Testa, R. T., Petersen, P. J., and Lee, V. J. (1994) "Glycylcyclines". 3. 9-Aminodoxycycline-carboxamides, J. Med. Chem. 37, 3205-3211.
6. Eliopoulos, G. M., Wennersten, C. B., Cole, G., and Moellering, R. C. (1994) In vitro activities of two glycylcyclines against grampositive bacteria. Antimicrob. Agents Chemother. 38, 534-541.
7. Testa, R. T., Petersen, P. J., Jacobus, N. V., Sum, P. E., Lee, V. J., and Tally, F, P. (1993) In vitro and in vivo antibacterial activities of the glycylcyclines, a new class of semisynthetic tetracyclines, Antimicrob. Agents Chemother. 37, 2270-2277.
8. Kramer, P. J., Zawada, R. J. X., McDaniel, R., Hutchinson, C. R., Hopwood, D. A., and Khosla, C. J. (1997) Rational Design and Engineered Biosynthesis of a Novel 18-Carbon Aromatic Polyketide, J. Am. Chem. Soc. 119, 635-639.
9. Hopwood, D. A. (1997) Genetic contributions to understanding polyketide synthases, Chem. Rev. 97, 2465-2497.
10. Rawlings, M., and Cronan, J. E. (1992) The gene encoding Escherichia coli acyl carrier protein lies within a cluster of fatty acid biosynthetic genes, J. Biol. Chem. 267, 5751-5754.
11. Baerson, S. R., Vanderheiden, M. G., and Lamppa, G. K. (1994) Identification of domains in an Arabidopsis acyl carrier protein gene promoter required for maximal organ-specific expression, Plant Mol. Biol. 26, 1947-1959.
12. Lambalot, R. H., Gehring, A. M., Flugel, R. S., Zuber, P., LaCele, M., Marahiel, M. A., Reid, R., Khosla, C., and Walsh, C. T. (1996) A new enzyme superfamily - the phosphopantetheinyl transferases, Chem. Biol. 3, 923-936.
13. Crump, M. P., Crosby, J., Dempsey, C. E., Parkinson, J. A., Murray, M., Hopwood, D. A., and Simpson, T. J. (1997) Solution structure of the actinorhodin polyketide synthase acyl carrier protein from Streptomyces coelicolor, Biochemistry 36, 6000-6008.
14. Xu, G.-Y., Tam, A., Lin, L., Hixon, J., Fritz, C. C., and Powers, R. (2001) Solution structure of Bacillus subtilis acyl carrier protein, Structure 9, 277-287.
15. Kim, Y., and Prestegard, J. H. (1990). Refinement of the NMR structures for acyl carrier protein with scalar coupling data, Proteins 8, 377-385.
16. Wong, H. C., Liu, G., Zhang, Y.-M., Rock, C. O., and Zheng, J. (2002) The solution structure of acyl carrier protein from Mycobacterium tuberculosis, J. Biol. Chem. 277, 15874-15880.
17. Reed, M. A. C., Schweizer, M., Szafranska, A. E., Arthur, C., Nicholson, T. P., Cox, R. J., Crosby, J., Crump, M. P., and Simpson, T. J. (2003) The isolated acyl carrier protein domain from the type I rat fatty acid synthase shows considerable structural homology and analogous biochemical properties to type II acyl carrier proteins, Org. Biol. Chem. 3, 463-471.
18. 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.
19. Weber, T., Baumgartner, R., Renner, C., Marahiel, M. A., and Holak, T. A. (2000) Solution structure of PCP, a prototype for the peptidyl carrier domains of modular peptide synthetases, Struct. Folding Des. 8, 407-418.
20. Parris, K. D., Lin, L., Tam, A., Mathew, R., Hixon, J., Stahl, M., Fritz, C. C., Seehra, J., and Somers, W. S. (2000) 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, Structure Folding Des. 8, 883-895.
21. Zhang, Y. M., Rao, M. S., Heath, R. J., Price, A. C., Olson, A. J., Rock, C. O., and White, S. W. (2001) Identification and analysis of the acyl carrier protein (ACP) docking site on beta-ketoacyl-ACP synthase III, J. Biol. Chem. 276, 8231-8238.
22. Khosla, C., Ebertkhosla, S., and Hopwood, D. A. (1992) Targeted gene replacements in a Streptomyces polyketide synthase gene cluster - role for the acyl carrier protein, Mol. Microbiol. 6, 3237-3249.
23. Crosby, J., Byrom, K. J., Hitchman, T. S., Cox. R. J., Crump, M. P., Findlow, I. S., Bibb, M. J., and Simpson, T. J. (1998) Acylation of Streptomyces type II polyketide synthase acyl carrier proteins, FEBS Lett. 433, 132-138.
24. Florova, G., Kazanina, G., and Reynolds, K. A. (2002) Enzymes involved in fatty acid and polyketide biosynthesis in Streptomyces gIaucescens: role of FabH and FabD and their acyl carrier protein specificity, Biochemistry 41, 10462-10471.
25. Ritsema, T., Gehring, A. M., Stuitje, A. R., van der Drift, K. M., Dandal, I., Lambalot, R. H., Walsh, C. T., Thomas-Oates, J. E., Lugtenberg, B. J., and Spaink, H. P (1998) Functional analysis of an interspecies chimera of acyl carrier proteins indicates a specialized domain for protein recognition, Mol. Gen. Genet. 257, 641-648.
26. Matharu, A. L., Cox, R. J., Crosby, J., Byrom, K. J., and Simpson, T. J. (1998) MCAT is not required for in vitro polyketide synthesis in a minimal actinorhodin polyketide synthase from Streptomyces coelicolor, Chem. Biol. 5, 699-711.
27. Staunton, J., and Weissman, K. J. (2001) Polyketide biosynthesis: a millennium review, Nat. Prod. Rep. 18, 380-416.
28. Mofid, M. R., Finking, R., and Marahiel, M. A. (2002) 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, 17023-17031.
29. Petkovic, H., Thamchaipenet, A., Zhou, L. H., Hranueli, D., Raspor, P., Waterman, P. G., and Hunter, I. S. (1999) Disruption of an aromatase/cyclase from the oxytetracycline gene cluster of Streptomyces rimosus results in production of novel polyketides with shorter chain lengths, J. Biol. Chem. 274, 32829-32834.
30. Moore, B. S., and Hertweck, C. (2002) Biosynthesis and attachment of novel bacterial synthase starter units, Nat. Prod. Rep. 19, 70-99.
31. Hunter, I. S., and Hill, R. A. (1997) in Biotechnology of Antibiotics, 2nd ed. (Strohl, W. R., Ed.) pp 659-682, Marcel Decker Inc., New York.
32. Cox, R. J., Hitchman, T. S., Byrom, K. J., Findlow, I. S., Tanner, J. A., Crosby, J., and Simpson, T. J. (1997) Post-translational modification of heterologously expressed Streptomyces type II polyketide synthase acyl carrier proteins, FEBS Lett. 405, 267-772.
33. Kay, L. E. (1995) Pulsed field gradient multi-dimensional NMR methods for the study of protein structure and dynamics in solution, Prog. Biophys. Mol. Biol. 63, 277-299.
34. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-665.
35. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRpipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
36. Garrett, D. S., Powers, R., Gronenbom, A. M., and Clore, G. M. (1991) A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams, J. Magn. Reson. 95, 214-220.
37. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley and Sons, New York.
38. 15N-relaxation, Biochemistry 33, 5984-6003.
39. Abragam, A. (1961) Principles of Nuclear Magnetism, Clarendon, Oxford.
40. Lipari, G., and Szabo, A. (1982a) A model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules I. Theory and range of validity, J. Am. Chem. Soc. 104, 4545-4549.
41. Lipari, G., and Szabo, A. (1982b) A model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules II. Theory and range of validity, J. Am. Chem. Soc. 104, 4549-4570.
42. 1H NMR spectroscopy, Biochemistry 29, 7387-7401.
43. Clore, G. M., Szabo, A., Bax, A., Kay, L. E., Driscoll, P. C., and Gronenborn, A. M. (1990b) Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins, J. Am. Chem. Soc. 112, 4989-4991.
44. Lakowski, R. A., MacArthur, M. W., and Thornton, J. M. (1993) PROCHECK - a program to check the stereochemcial quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
45. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-5, 29-32.
46. Henry, G. D., and Sykes, B. D. (1995) Determination of the rotational-dynamics and pH-dependence of the hydrogen-exchange rates of the arginine guanidine group using NMR spectroscopy, J. Biomol. NMR 6, 59-66.
47. Neuhaus, D., and Williamson, M. (1989) The nuclear Overhauser effect in structural and conformational analysis. VCH publishers Inc. New York.
48. Worsham, L. M. S., Earls, L., Jolly, C., Langston, K. G., M. Trent, S., and Ernst-Fonberg, M. L. (2003) Amino acid residues of Escherichia coli acyl carrier protein involved in heterologous protein interactions, Biochemistry 42, 167-176.
49. Gong, H., and Byers, D. M. (2003) Glutamate-41 of Vibrio harveyi acyl carrier protein is essential for fatty acid synthase but not acyl-ACP synthetase activity. Biochem. Biophys. Res. Comm. 302, 35-40.
50. Mulder, F. A. A., Hon, B., Muhandiram, D. R., Dahlquist, F. W., and Kay, L. E. (2000) Flexibility and ligand exchange in a buried cavity mutant of T4 lysozyme studied by multinuclear NMR, Biochemistry 39, 12614-12622.
51. Andrec, M., Hil, R. B., and Prestegard, J. H. (1995) Amide exchange rates in Escherichia coli and acyl carrier protein: Correlation with protein structure and dynamics, Protein Sci. 4, 983-993.