Activity-Independent Discovery of Secondary Metabolites Using Chemical Elicitation and Cheminformatic Inference

ACS Chemical Biology

Volumn 10, Issue 11, 2015, Pages 2616-2623

  Pimentel Elardo, Sheila M ^a   Sørensen, Dan ^b   Ho, Louis ^a   Ziko, Mikaela ^b   Bueler, Stephanie A ^c   Lu, Stella ^d   Tao, Joe ^e   Moser, Arvin ^f   Lee, Richard ^f   Agard, David ^e   Fairn, Greg ^d   Rubinstein, John L ^a,c   Shoichet, Brian K ^e   Nodwell, Justin R ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Advanced Chemistry Development Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

9 METHYLSTREPTIMIDONE; ANTIBIOTIC AGENT; N [4 (4 CHLOROPHENOXY) PHENYL] ACETAMIDE; NONACTIN; OXOHYGROLIDIN; UNCLASSIFIED DRUG; ACETANILIDE DERIVATIVE; ANTIINFECTIVE AGENT; BIOLOGICAL PRODUCT; DIPHENYL ETHER DERIVATIVE; HEAT SHOCK PROTEIN 90; MACROLIDE; N-(4-(4-CHLOROPHENOXY)PHENYL)ACETAMIDE;

ARTICLE; BACTERIAL CELL; BIOLOGICAL ACTIVITY; CHEMICAL ELICITATION; CHEMICAL PHENOMENA; CHEMINFORMATIC INFERENCE; CONTROLLED STUDY; DRUG SCREENING; EPISTASIS; EUKARYOTIC CELL; GENE EXPRESSION; GENE SEQUENCE; GENOME; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; STREPTOMYCETACEAE; ACTINOBACTERIA; ANTAGONISTS AND INHIBITORS; BACTERIUM; BIOSYNTHESIS; CHEMISTRY; DRUG DEVELOPMENT; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; METABOLISM; PROCEDURES;

ACETANILIDES; ACTINOBACTERIA; ANTI-BACTERIAL AGENTS; BACTERIA; BIOLOGICAL PRODUCTS; CHROMATOGRAPHY, LIQUID; DRUG DISCOVERY; HSP90 HEAT-SHOCK PROTEINS; MACROLIDES; PHENYL ETHERS;

EID: 84947910327     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00612     Document Type: Article

References (50)

1. Bérdy, J. (2005) Bioactive microbial metabolites J. Antibiot. 58, 1-26 10.1038/ja.2005.1
2. Davies, J. (2011) How to discover new antibiotics: harvesting the parvome Curr. Opin. Chem. Biol. 15, 5-10 10.1016/j.cbpa.2010.11.001
3. Baltz, R. H. (2006) Marcel Faber Roundtable: is our antibiotic pipeline unproductive because of starvation, constipation or lack of inspiration? J. Ind. Microbiol. Biotechnol. 33, 507-513 10.1007/s10295-005-0077-9
4. Ito, T. and Masubuchi, M. (2014) Dereplication of microbial extracts and related analytical technologies J. Antibiot. 67, 353-360 10.1038/ja.2014.12
5. Nett, M., Ikeda, H., and Moore, B. S. (2009) Genomic basis for natural product biosynthetic diversity in the actinomycetes Nat. Prod. Rep. 26, 1362-1384 10.1039/b817069j
6. Blin, K., Medema, M. H., Kazempour, D., Fischbach, M. A., Breitling, R., Takano, E., and Weber, T. (2013) antiSMASH 2.0 - a versatile platform for genome mining of secondary metabolite producers Nucleic Acids Res. 41, W204-212 10.1093/nar/gkt449
7. Laureti, L., Song, L., Huang, S., Corre, C., Leblond, P., Challis, G. L., and Aigle, B. (2011) Identification of a bioactive 51-membered macrolide complex by activation of a silent polyketide synthase in Streptomyces ambofaciens Proc. Natl. Acad. Sci. U. S. A. 108, 6258-6263 10.1073/pnas.1019077108
8. Hosaka, T., Ohnishi-Kameyama, M., Muramatsu, H., Murakami, K., Tsurumi, Y., Kodani, S., Yoshida, M., Fujie, A., and Ochi, K. (2009) Antibacterial discovery in actinomycetes strains with mutations in RNA polymerase or ribosomal protein S12 Nat. Biotechnol. 27, 462-464 10.1038/nbt.1538
9. Murakami, T., Burian, J., Yanai, K., Bibb, M. J., and Thompson, C. J. (2011) A system for the targeted amplification of bacterial gene clusters multiplies antibiotic yield in Streptomyces coelicolor Proc. Natl. Acad. Sci. U. S. A. 108, 16020-16025 10.1073/pnas.1108124108
10. Yoon, V. and Nodwell, J. R. (2014) Activating secondary metabolism with stress and chemicals J. Ind. Microbiol. Biotechnol. 41, 415-424 10.1007/s10295-013-1387-y
11. Craney, A., Ahmed, S., and Nodwell, J. (2013) Towards a new science of secondary metabolism J. Antibiot. 66, 387-400 10.1038/ja.2013.25
12. McKenzie, N. L., Thaker, M., Koteva, K., Hughes, D. W., Wright, G. D., and Nodwell, J. R. (2010) Induction of antimicrobial activities in heterologous streptomycetes using alleles of the Streptomyces coelicolor gene absA1 J. Antibiot. 63, 177-182 10.1038/ja.2010.13
13. Gomez-Escribano, J. P. and Bibb, M. J. (2014) Heterologous expression of natural product biosynthetic gene clusters in Streptomyces coelicolor: from genome mining to manipulation of biosynthetic pathways J. Ind. Microbiol. Biotechnol. 41, 425-431 10.1007/s10295-013-1348-5
14. Typas, A., Nichols, R. J., Siegele, D. A., Shales, M., Collins, S. R., Lim, B., Braberg, H., Yamamoto, N., Takeuchi, R., Wanner, B. L., Mori, H., Weissman, J. S., Krogan, N. J., and Gross, C. A. (2008) High-throughput, quantitave analyses of genetic interactions in E. coli Nat. Methods 5, 781-787 10.1038/nmeth.1240
15. Ho, C. H., Magtanong, L., Barker, S. L., Gresham, D., Nishimura, S., Natarajan, P., Koh, J. L., Porter, J., Gray, C. A., Andersen, R. J., Giaever, G., Nislow, C., Andrews, B., Botstein, D., Graham, T. R., Yoshida, M., and Boone, C. (2009) A molecular barcoded yeast ORF library enables mode-of-action analysis of bioactive compounds Nat. Biotechnol. 27, 369-377 10.1038/nbt.1534
16. Craney, A., Ozimok, C., Pimentel-Elardo, S. M., Capretta, A., and Nodwell, J. R. (2012) Chemical perturbation of secondary metabolism demonstrates important links to primary metabolism Chem. Biol. 19, 1020-1027 10.1016/j.chembiol.2012.06.013
17. Thaker, M. N., Wang, W., Spanogiannopoulos, P., Waglechner, N., King, A. M., Medina, R., and Wright, G. D. (2013) Identifying producers of antibacterial compounds by screening for antibiotic resistance Nat. Biotechnol. 31, 922-927 10.1038/nbt.2685
18. Aoki, Y., Matsumoto, D., Kawaide, H., and Natsume, M. (2011) Physiological role of germicidins in spore germination and hyphal elongation in Streptomyces coelicolor A3(2) J. Antibiot. 64, 607-611 10.1038/ja.2011.59
19. Barona-Gómez, F., Lautru, S., Francou, F. X., Leblond, P., Pernodet, J. L., and Challis, G. L. (2006) Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877 Microbiology 152, 3355-3366 10.1099/mic.0.29161-0
20. Ahmed, S., Craney, A., Pimentel-Elardo, S. M., and Nodwell, J. R. (2013) A synthetic, species-specific activator of secondary metabolism and sporulation in Streptomyces coelicolor ChemBioChem 14, 83-91 10.1002/cbic.201200619
21. Kretschmer, A., Dorgerloh, M., Deeg, M., and Hagenmaier, H. (1985) The structures of novel insecticidal macrolides: bafilomycins D and E, and oxohygrolidin Agric. Biol. Chem. 49, 2509-2511 10.1271/bbb1961.49.2509
22. Saito, N., Kitame, F., Kikuchi, M., and Ishida, N. (1974) Studies on a new antiviral antibiotic, 9-methylstreptimidone. I. Physicochemical and biological properties J. Antibiot. 27, 206-214 10.7164/antibiotics.27.206
23. Jizba, J., Sedmera, P., Zima, J., Beran, M., Blumauerová, M., Kandybin, N. V., and Samoukina, G. V. (1991) Macrotetrolide antibiotics produced by Streptomyces globisporus Folia Microbiol. (Dordrecht, Neth.) 36, 437-443 10.1007/BF02884062
24. Asher, I. M., Phillies, G. D., Kim, B. J., and Stanley, H. E. (1977) Ion complexation in nonactin, monactin, and dinactin: a Raman spectroscopic study Biopolymers 16, 157-185 10.1002/bip.1977.360160112
25. Andrusiak, K., Piotrowski, J. S., and Boone, C. (2012) Chemical-genomic profiling: systematic analysis of the cellular targets of bioactive molecules Bioorg. Med. Chem. 20, 1952-1960 10.1016/j.bmc.2011.12.023
26. Smaczynska-de Rooij, I. I., Allwood, E. G., Aghamohammadzadeh, S., Hettema, E. H., Goldberg, M. W., and Ayscough, K. R. (2010) A role for the dynamin-like protein Vps1 during endocytosis in yeast J. Cell Sci. 123, 3496-3506 10.1242/jcs.070508
27. Vater, C. A., Raymond, C. K., Ekena, K., Howald-Stevenson, I., and Stevens, T. H. (1992) The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains J. Cell Biol. 119, 773-786 10.1083/jcb.119.4.773
28. Hama, H., Tall, G. G., and Horazdovsky, B. F. (1999) Vps9p is a guanine nucleotide exchange factor involved in vesicle-mediated vacuolar protein transport J. Biol. Chem. 274, 15284-15291 10.1074/jbc.274.21.15284
29. Conibear, E. and Stevens, T. H. (2000) Vps52p, Vps53p, and Vps54p form a novel multisubunit complex required for protein sorting at the yeast late Golgi Mol. Biol. Cell 11, 305-323 10.1091/mbc.11.1.305
30. Keiser, M. J., Roth, B. L., Armbruster, B. N., Ernsberger, P., Irwin, J. J., and Shoichet, B. K. (2007) Relating protein pharmacology by ligand chemistry Nat. Biotechnol. 25, 197-206 10.1038/nbt1284
31. Paolini, G. V., Shapland, R. H., van Hoorn, W. P., Mason, J. S., and Hopkins, A. L. (2006) Global mapping of pharmacological space Nat. Biotechnol. 24, 805-815 10.1038/nbt1228
32. Bender, A., Jenkins, J. L., Glick, M., Deng, Z., Nettles, J. H., and Davies, J. W. (2006) Bayes affinity fingerprints improve retrieval rates in virtual screening and define orthogonal bioactivity space: when are multitarget drugs a feasible concept? J. Chem. Inf. Model. 46, 2445-2456 10.1021/ci600197y
33. Reker, D., Perna, A. M., Rodrigues, T., Schneider, P., Reutlinger, M., Mönch, B., Koeberle, A., Lamers, C., Gabler, M., Steinmetz, H., Müller, R., Schubert-Zsilavecz, M., Werz, O., and Schneider, G. (2014) Revealing the macromolecular targets of complex natural products Nat. Chem. 6, 1072-1078 10.1038/nchem.2095
34. Antolín, A. A. and Mestres, J. (2015) Distant Polypharmacology among MLP Chemical Probes ACS Chem. Biol. 10, 395-400 10.1021/cb500393m
35. Yildirim, M. A., Goh, K. I., Cusick, M. E., Barabási, A. L., and Vidal, M. (2007) Drug-target network Nat. Biotechnol. 25, 1119-1126 10.1038/nbt1338
36. Bento, A. P., Gaulton, A., Hersey, A., Bellis, L. J., Chambers, J., Davies, M., Krüger, F. A., Light, Y., Mak, L., McGlinchey, S., Nowotka, M., Papadatos, G., Santos, R., and Overington, J. P. (2014) The ChEMBL bioactivity database: an update Nucleic Acids Res. 42, D1083-1090 10.1093/nar/gkt1031
37. Olah, M., Mracec, M., Ostopovici, L., Rad, R., Bora, A., Hadaruga, N., Olah, I., Banda, M., Simon, Z., Mracec, M., and Oprea, T. I. (2005) Wombat: world of molecular bioactivity, In Chemoinformatics in Drug Discovery (Oprea, T. I., Ed.), Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, FRG.
38. Hert, J., Keiser, M. J., Irwin, J. J., Oprea, T. I., and Shoichet, B. K. (2008) Quantifying the relationships among drug classes J. Chem. Inf. Model. 48, 755-765 10.1021/ci8000259
39. Keiser, M. J., Setola, V., Irwin, J. J., Laggner, C., Abbas, A. I., Hufeisen, S. J., Jensen, N. H., Kuijer, M. B., Matos, R. C., Tran, T. B., Whaley, R., Glennon, R. A., Hert, J., Thomas, K. L., Edwards, D. D., Shoichet, B. K., and Roth, B. L. (2009) Predicting new molecular targets for known drugs Nature 462, 175-181 10.1038/nature08506
40. DeGraw, A. J., Keiser, M. J., Ochocki, J. D., Shoichet, B. K., and Distefano, M. D. (2010) Prediction and evaluation of protein farnesyltransferase inhibition by commercial drugs J. Med. Chem. 53, 2464-2471 10.1021/jm901613f
41. Laggner, C., Kokel, D., Setola, V., Tolia, A., Lin, H., Irwin, J. J., Keiser, M. J., Cheung, C. Y., Minor, D. L., Roth, B. L., Peterson, R. T., and Shoichet, B. K. (2012) Chemical informatics and target identification in a zebrafish phenotypic screen Nat. Chem. Biol. 8, 144-146 10.1038/nchembio.732
42. Lounkine, E., Keiser, M. J., Whitebread, S., Mikhailov, D., Hamon, J., Jenkins, J. L., Lavan, P., Weber, E., Doak, A. K., Côté, S., Shoichet, B. K., and Urban, L. (2012) Large-scale prediction and testing of drug activity on side-effect targets Nature 486, 361-367 10.1038/nature11159
43. Lemieux, G. A., Keiser, M. J., Sassano, M. F., Laggner, C., Mayer, F., Bainton, R. J., Werb, Z., Roth, B. L., Shoichet, B. K., and Ashrafi, K. (2013) In silico molecular comparisons of C. elegans and mammalian pharmacology identify distinct targets that regulate feeding PLoS Biol. 11, e1001712 10.1371/journal.pbio.1001712
44. Ziemert, N., Lechner, A., Wietz, M., Millán-Aguinaga, N., Chavarria, K. L., and Jensen, P. R. (2014) Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora Proc. Natl. Acad. Sci. U. S. A. 111, E1130-1139 10.1073/pnas.1324161111
45. Abdelmohsen, U. R., Bayer, K., and Hentschel, U. (2014) Diversity, abundance and natural products of marine sponge-associated actinomycetes Nat. Prod. Rep. 31, 381-399 10.1039/c3np70111e
46. Pluskal, T., Castillo, S., Villar-Briones, A., and Oresic, M. (2010) MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data BMC Bioinf. 11, 395 10.1186/1471-2105-11-395
47. Moser, A., Elyashberg, M. E., Williams, A. J., Blinov, K. A., and Dimartino, J. C. (2012) Blind trials of computer-assisted structure elucidation software J. Cheminf. 4, 5 10.1186/1758-2946-4-5
48. Warde-Farley, D., Donaldson, S. L., Comes, O., Zuberi, K., Badrawi, R., Chao, P., Franz, M., Grouios, C., Kazi, F., Lopes, C. T., Maitland, A., Mostafavi, S., Montojo, J., Shao, Q., Wright, G., Bader, G. D., and Morris, Q. (2010) The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function Nucleic Acids Res. 38, W214-220 10.1093/nar/gkq537
49. Benlekbir, S., Bueler, S. A., and Rubinstein, J. L. (2012) Structure of the vacuolar-type ATPase from Saccharomyces cerevisiae at 11-Å resolution Nat. Struct. Mol. Biol. 19, 1356-1362 10.1038/nsmb.2422
50. Loetscher, H. R., deJong, C., and Capaldi, R. A. (1984) Modification of the F0 portion of the H+-translocating adenosinetriphosphatase complex of Escherichia coli by the water-soluble carbodiimide 1-ethyl-3[3-(dimethylamino)propyl]carbodiimide and effect on the proton channeling function Biochemistry 23, 4128-4134 10.1021/bi00313a018