Molecular basis of substrate promiscuity for the SAM-dependent O-methyltransferase NcsB1, involved in the biosynthesis of the enediyne antitumor antibiotic neocarzinostatin

Biochemistry

Volumn 48, Issue 40, 2009, Pages 9590-9598

  Cooke, Heather A ^a   Guenther, Elizabeth L ^a   Luo, Yinggang ^b   Shen, Ben ^b   Bruner, Steven D ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE STRUCTURE; ANTITUMOR ANTIBIOTICS; BIOCHEMICAL CHARACTERIZATION; BIOLOGICAL ACTIVITIES; BIOSYNTHETIC PATHWAY; BUILDING BLOCKES; CARRIER PROTEINS; COFACTORS; DUPLEX DNA; ENEDIYNES; HYDROCARBON CORES; IN-VITRO; MOLECULAR BASIS; NAPHTHOIC ACIDS; NATURAL PRODUCTS; O-METHYLTRANSFERASE; POLYKETIDES; S-ADENOSYLMETHIONINE; SITE DIRECTED MUTAGENESIS; SMALL MOLECULES; STRUCTURAL BASIS; SUBDOMAIN; SUBSTRATE DISCRIMINATION;

AMINES; AMINO ACIDS; ANTIBIOTICS; BIOCHEMISTRY; BIOSYNTHESIS; CARBOHYDRATES; ENZYME ACTIVITY; HYDROCARBONS; NUCLEIC ACIDS; ORGANIC ACIDS; SUBSTRATES;

ENZYMES;

ENEDIYNE; METHYLTRANSFERASE; PROTEIN NCSB1; UNCLASSIFIED DRUG; ZINOSTATIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; DRUG SYNTHESIS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

ANTIBIOTICS, ANTINEOPLASTIC; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENEDIYNES; NAPHTHOLS; PROTEIN BINDING; PROTEIN O-METHYLTRANSFERASE; S-ADENOSYLHOMOCYSTEINE; S-ADENOSYLMETHIONINE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; ZINOSTATIN;

EID: 70350059601     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901257q     Document Type: Article

References (48)

1. Shen, B., Liu, W., and Nonaka, K. (2003) Enediyne natural products: Biosynthesis and prospect towards engineering novel antitumor agents. Curr. Med. Chem. 10, 2317-2325.
2. Maeda, H., Aikawa, S., and Yamashita, A. (1975) Subcellular fate of protein antibiotic neocarzinostatin in culture of a lymphoid cell line from Burkitt's lymphoma. Cancer Res. 35, 554-559.
3. Liu, W., Ahlert, J., Gao, Q., Wendt-Pienkowski, E., Shen, B., and Thorson, J. S. (2003) Rapid PCR amplification of minimal enediyne polyketide synthase cassettes leads to a predictive familial classification model. Proc. Natl. Acad. Sci. U.S.A. 100, 11959-11963.
4. Liu, W., Nonaka, K., Nie, L., Zhang, J., Christenson, S. D., Bae, J., Van Lanen, S. G., Zazopoulos, E., Farnet, C. M., Yang, C. F., and Shen, B. (2005) The neocarzinostatin biosynthetic gene cluster from Streptomyces carzinostaticus ATCC 15944 involving two iterative type I polyketide synthases. Chem. Biol. 12, 293-302.
5. Udwary, D. W., Zeigler, L., Asolkar, R. N., Singan, V., Lapidus, A., Fenical, W., Jensen, P. R., andMoore, B. S. (2007) Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proc. Natl. Acad. Sci. U.S.A. 104, 10376-10381.
6. Liu, W., Christenson, S. D., Standage, S., and Shen, B. (2002) Biosynthesis of the enediyne antitumor antibiotic C-1027. Science 297, 1170-1173. (Pubitemid 36193350)
7. Van Lanen, S. G., Oh, T. J., Liu, W., Wendt-Pienkowski, E., and Shen, B. (2007) Characterization of the maduropeptin biosynthetic gene cluster from Actinomadura madurae ATCC 39144 supporting a unifying paradigm for enediyne biosynthesis. J. Am. Chem. Soc. 129, 13082-13094.
8. Ahlert, J., Shepard, E., Lomovskaya, N., Zazopoulos, E., Staffa, A., Bachmann, B. O., Huang, K., Fonstein, L., Czisny, A., Whitwam, R. E., Farnet, C. M., and Thorson, J. S. (2002) The calicheamicin gene cluster and its iterative type I enediyne PKS. Science 297, 1173-1176. (Pubitemid 36193351)
9. Povirk, L. F., Dattagupta, N., Warf, B. C., and Goldberg, I. H. (1981) Neocarzinostatin chromophore binds to deoxyribonucleic acid by intercalation. Biochemistry 20, 4007-4014. (Pubitemid 11012526)
10. Lee, S. H., and Goldberg, I. H. (1989) Sequence-specific, strand-selective, and directional binding of neocarzinostatin chromophore to oligodeoxyribonucleotides. Biochemistry 28, 1019-1026.
11. Kappen, L. S., Ellenberger, T. E., and Goldberg, I. H. (1987) Mechanism and base specificity of DNA breakage in intact cells by neocarzinostatin. Biochemistry 26, 384-390.
12. Zhang, J., Van Lanen, S. G., Ju, J., Liu, W., Dorrestein, P. C., Li, W., Kelleher, N. L., and Shen, B. (2008) A phosphopantetheinylating polyketide synthase producing a linear polyene to initiate enediyne antitumor antibiotic biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 105, 1460-1465.
13. Urbaniak, M. D., Bingham, J. P., Hartley, J. A., Woolfson, D. N., and Caddick, S. (2004) Design and synthesis of a nitrogen mustard derivative stabilized by apo-neocarzinostatin. J. Med. Chem. 47, 4710-4715.
14. Caddick, S., Muskett, F. W., Stoneman, R. G., and Woolfson, D. N. (2006) Synthetic ligands for apo-neocarzinostatin. J. Am. Chem. Soc. 128, 4204-4205.
15. Baker, J. R., Woolfson, D. N., Muskett, F. W., Stoneman, R. G., Urbaniak, M. D., and Caddick, S. (2007) Protein-small molecule interactions in neocarzinostatin, the prototypical enediyne chromoprotein antibiotic. ChemBioChem 8, 704-717.
16. Sthapit, B., Oh, T. J., Lamichhane, R., Liou, K., Lee, H. C., Kim, C. G., and Sohng, J. K. (2004) Neocarzinostatin naphthoate synthase: An unique iterative type I PKS from neocarzinostatin producer Streptomyces carzinostaticus. FEBS Lett. 566, 201-206. (Pubitemid 38625958)
17. Weitnauer, G., Muhlenweg, A., Trefzer, A., Hoffmeister, D., Sussmuth, R. D., Jung, G., Welzel, K., Vente, A., Girreser, U., and Bechthold, A. (2001) Biosynthesis of the orthosomycin antibiotic avilamycin A: Deductions from the molecular analysis of the avi biosynthetic gene cluster of Streptomyces viridochromogenes Tu57 and production of new antibiotics. Chem. Biol. 8, 569-581.
18. Jia, X. Y., Tian, Z. H., Shao, L., Qu, X. D., Zhao, Q. F., Tang, J., Tang, G. L., and Liu, W. (2006) Genetic characterization of the chlorothricin gene cluster as a model for spirotetronate antibiotic biosynthesis. Chem. Biol. 13, 575-585.
19. Zhao, Q., He, Q., Ding, W., Tang, M., Kang, Q., Yu, Y., Deng, W., Zhang, Q., Fang, J., Tang, G., and Liu, W. (2008) Characterization of the azinomycin B biosynthetic gene cluster revealing a different iterative type I polyketide synthase for naphthoate biosynthesis. Chem. Biol. 15, 693-705.
20. Cooke, H. A., Zhang, J., Griffin, M. A., Nonaka, K., Van Lanen, S. G., Shen, B., and Bruner, S. D. (2007) Characterization of NcsB2 as a promiscuous naphthoic acid/coenzyme A ligase integral to the biosynthesis of the enediyne antitumor antibiotic neocarzinostatin. J. Am. Chem. Soc. 129, 7728-7729.
21. Luo, Y., Lin, S., Zhang, J., Cooke, H. A., Bruner, S. D., and Shen, B. (2008) Regiospecific O-methylation of naphthoic acids catalyzed by NcsB1, an O-methyltransferase involved in the biosynthesis of the enediyne antitumor antibiotic neocarzinostatin. J. Biol. Chem. 283, 14694-14702.
22. Schubert, H. L., Blumenthal, R. M., and Cheng, X. (2003) Many paths to methyltransfer: A chronicle of convergence. Trends Biochem. Sci. 28, 329-335.
23. Vidgren, J., Svensson, L. A., and Liljas, A. (1994) Crystal structure of catechol O-methyltransferase. Nature 368, 354-358.
24. Martin, J. L., and McMillan, F. M. (2002) SAM (dependent) I AM: The S-adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol. 12, 783-793.
25. Madduri, K., Torti, F., Colombo, A. L., and Hutchinson, C. R. (1993) Cloning and sequencing of a gene encoding carminomycin 4-O-methyltransferase from Streptomyces peucetius and its expression in Escherichia coli. J. Bacteriol. 175, 3900-3904. (Pubitemid 23173353)
26. Jansson, A., Koskiniemi, H., Mantsala, P., Niemi, J., and Schneider, G. (2004) Crystal structure of a ternary complex of DnrK, a methyltransferase in daunorubicin biosynthesis, with bound products. J. Biol. Chem. 279, 41149-41156.
27. Jansson, A., Koskiniemi, H., Erola, A., Wang, J., Mantsala, P., Schneider, G., and Niemi, J. (2005) Aclacinomycin 10-hydroxylase is a novel substrate-assisted hydroxylase requiring S-adenosyl-L-methionine as cofactor. J. Biol. Chem. 280, 3636-3644.
28. Jansson, A., Niemi, J., Lindqvist, Y., Mantsala, P., and Schneider, G. (2003) Crystal structure of aclacinomycin-10-hydroxylase, a S-adenosyl-L- methionine-dependent methyltransferase homolog involved in anthracycline biosynthesis in Streptomyces purpurascens. J. Mol. Biol. 334, 269-280.
29. Oster, L. M., Lester, D. R., Terwisscha van Scheltinga, A., Svenda, M., van Lun, M., Genereux, C., and Andersson, I. (2006) Insights into cephamycin biosynthesis: The crystal structure of CmcI from Streptomyces clavuligerus. J. Mol. Biol. 358, 546-558.
30. Hou, X., Wang, Y., Zhou, Z., Bao, S., Lin, Y., and Gong, W. (2007) Crystal structure of SAM-dependent O-methyltransferase from pathogenic bacterium Leptospira interrogans. J. Struct. Biol. 159, 523-528.
31. Cho, J. H., Park, Y., Ahn, J. H., Lim, Y., and Rhee, S. (2008) Structural and functional insights into O-methyltransferase from Bacillus cereus. J. Mol. Biol. 382, 987-997.
32. Singh, S., McCoy, J. G., Zhang, C., Bingman, C. A., Phillips, G. N., Jr., and Thorson, J. S. (2008) Structure and mechanism of the rebeccamycin sugar 40-O-methyltransferase RebM. J. Biol. Chem. 283, 22628-22636.
33. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
34. 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.
35. Bailey, S. (1994) The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr. D50, 760-763.
36. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132. (Pubitemid 41742764)
37. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR system. Nat. Proc. 2, 2728-2733.
38. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D54, 905-921. (Pubitemid 28443603)
39. Vagin, A., and Teplyakov, A. (1997) MOLREP: An automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025.
40. Schuttelkopf, A. W., and van Aalten, D. M. F. (2004) PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D60, 1355-1363.
41. Kleywegt, G. J. (2007) Crystallographic refinement of ligand complexes. Acta Crystallogr. D63, 94-100.
42. Sippl, M. J., and Wiederstein, M. (2008) A note on difficult structure alignment problems. Bioinformatics 24, 426-427.
43. Sippl, M. J. (2008) On distance and similarity in fold space. Bioinformatics 24, 872-873.
44. Holm, L., Kaariainen, S., Rosenstrom, P., and Schenkel, A. (2008) Searching protein structure databases with DaliLite. Bioinformatics 24, 2780-2781. (Pubitemid 352722625)
45. Zubieta, C., He, X. Z., Dixon, R. A., and Noel, J. P. (2001) Structures of two natural product methyltransferases reveal the basis for substrate specificity in plant O-methyltransferases. Nat. Struct. Biol. 8, 271-279.
46. Parsons, J. F., Greenhagen, B. T., Shi, K., Calabrese, K., Robinson, H., and Ladner, J. E. (2007) Structural and functional analysis of the pyocyanin biosynthetic protein PhzM from Pseudomonas aeruginosa. Biochemistry 46, 1821-1828. (Pubitemid 46272946)
47. Zubieta, C., Kota, P., Ferrer, J. L., Dixon, R. A., and Noel, J. P. (2002) Structural basis for the modulation of lignin monomer methylation by caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase. Plant Cell 14, 1265-1277. (Pubitemid 34780432)
48. Van Lanen, S. G., Lin, S., and Shen, B. (2008) Biosynthesis of the enediyne antitumor antibiotic C-1027 involves a new branching point in chorismate metabolism. Proc. Natl. Acad. Sci. U.S.A. 105, 494-499.