Integrated compound profiling screens identify the mitochondrial electron transport Chain as the molecular target of the natural products manassantin, sesquicillin, and arctigenin

ACS Chemical Biology

Volumn 8, Issue 1, 2013, Pages 257-267

  Lai, Kevin ^a,c   Selinger, Douglas W ^a   Solomon, Jonathan M ^a   Wu, Hua ^a   Schmitt, Esther ^b   Serluca, Fabrizio C ^a   Curtis, Daniel ^a   Benson, John D ^a,d  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c Fate Therapeutics   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DIACETYL PHLOROGLUCINOL; ARCTIGENIN; FUMIGACHLORIN; MANASSANTIN; MANASSANTIN A; MANASSANTIN B; MUNDULONE; NALANTHALIDE; PLANT MEDICINAL PRODUCT; SESQUICILLIN; SESQUICILLIN A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; DRUG MECHANISM; DRUG TARGETING; ELECTRON TRANSPORT; EMBRYO; MITOCHONDRION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ZEBRA FISH;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; FURANS; GENE EXPRESSION PROFILING; LIGNANS; MITOCHONDRIAL MEMBRANES; MOLECULAR STRUCTURE; NAPHTHALENES; ZEBRAFISH;

DANIO RERIO;

EID: 84872521602     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300495e     Document Type: Article

References (39)

1. Grunwald, D. J. and Eisen, J. S. (2002) Headwaters of the zebrafish- emergence of a new model vertebrate Nat. Rev. Genet. 3, 717-724 (Pubitemid 34984260)
2. Wixon, J. (2000) Danio rerio, the zebrafish Yeast 17, 225-231
3. den Hertog, J. (2005) Chemical genetics: drug screens in zebrafish Biosci. Rep. 25, 289-297 (Pubitemid 41712659)
4. Peterson, R. T., Link, B. A., Dowling, J. E., and Schreiber, S. L. (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development Proc. Natl. Acad. Sci. U.S.A. 97, 12965-12969
5. Peterson, R. T., Mably, J. D., Chen, J.-N., and Fishman, M. C. (2001) Convergence of distinct pathways to heart patterning revealed by the small molecule concentramide and the mutation heart-and-soul Curr. Biol. 11, 1481-1491 (Pubitemid 32931009)
6. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D., and Peterson, R. T. (2007) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism Nat. Chem. Biol. 4, 33-41 (Pubitemid 350273653)
7. Stern, H. M., Murphey, R. D., Shepard, J. L., Amatruda, J. F., Straub, C. T., Pfaff, K. L., Weber, G., Tallarico, J. A., King, R. W., and Zon, L. I. (2005) Small molecules that delay S phase suppress a zebrafish bmyb mutant Nat. Chem. Biol. 1, 366-370
8. Schriemer, D. C., Kemmer, D., and Roberge, M. (2008) Design of phenotypic screens for bioactive chemicals and identification of their targets by genetic and proteomic approaches Comb. Chem. High Throughput Screening 11, 610-616
9. Yarrow, J. C., Feng, Y., Perlman, Z. E., Kirchhausen, T., and Mitchison, T. J. (2003) Phenotypic screening of small molecule libraries by high throughput cell imaging Comb. Chem. High Throughput Screening 6, 279-286 (Pubitemid 36612345)
10. Posakony, J., Hirao, M., and Bedalov, A. (2004) Identification and characterization of Sir2 inhibitors through phenotypic assays in yeast Comb. Chem. High Throughput Screening 7, 661-668 (Pubitemid 39371214)
11. Giaever, G., Shoemaker, D. D., Jones, T. W., Liang, H., Winzeler, E. A., Astromoff, A., and Davis, R. W. (1999) Genomic profiling of drug sensitivities via induced haploinsufficiency Nat. Genet. 21, 278-283 (Pubitemid 29124934)
12. Lum, P. Y., Armour, C. D., Stepaniants, S. B., Cavet, G., Wolf, M. K., Butler, J. S., Hinshaw, J. C., Garnier, P., Prestwich, G. D., Leonardson, A., Garrett-Engele, P., Rush, C. M., Bard, M., Schimmack, G., Phillips, J. W., Roberts, C. J., and Shoemaker, D. D. (2004) Discovering modes of action for therapeutic compounds using a genome-wide screen of yeast heterozygotes Cell 116, 121-137 (Pubitemid 38156189)
13. Koutsoukos, A. D., Rubinstein, L. V., Faraggi, D., Simon, R. M., Kalyandrug, S., Weinstein, J. N., Kohn, K. W., and Paull, K. D. (1994) Discrimination techniques applied to the NCI in vitro anti-tumour drug screen: Predicting biochemical mechanism of action Stat. Med. 13, 719-730 (Pubitemid 24106751)
14. Melnick, J. S., Janes, J., Kim, S., Chang, J. Y., Sipes, D. G., Gunderson, D., Jarnes, L., Matzen, J. T., Garcia, M. E., Hood, T. L., Beigi, R., Xia, G., Harig, R. A., Asatryan, H., Yan, S. F., Zhou, Y., Gu, X.-J., Saadat, A., Zhou, V., King, F. J., Shaw, C. M., Su, A. I., Downs, R., Gray, N. S., Schultz, P. G., Warmuth, M., and Caldwell, J. S. (2006) An efficient rapid system for profiling the cellular activities of molecular libraries Proc. Natl. Acad. Sci. U.S.A. 103, 3153-3158 (Pubitemid 43346440)
15. Lamb, J., Crawford, E. D., Peck, D., Modell, J. W., Blat, I. C., Wrobel, M. J., Lerner, J., Brunet, J.-P., Subramanian, A., Ross, K. N., Reich, M., Hieronymus, H., Wei, G., Armstrong, S. A., Haggarty, S. J., Clemons, P. A., Wei, R., Carr, S. A., Lander, E. S., and Golub, T. R. (2006) The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease Science 313, 1929-1935 (Pubitemid 44497995)
16. Perlman, Z. E., Slack, M. D., Feng, Y., Mitchison, T. J., Wu, L. F., and Altschuler, S. J. (2004) Multidimensional drug profiling by automated microscopy Science 306, 1194-1198 (Pubitemid 39489001)
17. MacDonald, M. L., Lamerdin, J., Owens, S., Keon, B. H., Bilter, G. K., Shang, Z., Huang, Z., Yu, H., Dias, J., Minami, T., Michnick, S. W., and Westwick, J. K. (2006) Identifying off-target effects and hidden phenotypes of drugs in human cells Nat. Chem. Biol. 2, 329-337 (Pubitemid 43787215)
18. Bantscheff, M., Eberhard, D., Abraham, Y., Bastuck, S., Boesche, M., Hobson, S., Mathieson, T., Perrin, J., Raida, M., Rau1, C., Reader, V., Sweetman, G., Bauer, A., Bouwmeester, T., Hopf, C., Kruse, U., Neubauer, G., Ramsden, N., Rick, J., Kuster, B., and Drewes, G. (2007) Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors Nat. Biotechnol. 25, 1035-1044 (Pubitemid 47517638)
19. Ong, S.-E., Schenone, M., Margolin, A. A., Li, X., Do, K., Doud, M. K., Mani, D. R., Kuai, L., Wang, X., Wood, J. L., Tolliday, N. J., Koehler, A. N., Marcaurelle, L. A., Golub, T. R., Gould, R. J., Schreiber, S. L., and Carr, S. A. (2009) Identifying the proteins to which small-molecule probes and drugs bind in cells Proc. Natl. Acad. Sci. U.S.A. 106, 4617-4622
20. Yildirim, M. A., Goh, K.-I., Cusick, M. E., Barabási, A.-L., and Vidal, M. (2007) Drug-target network Nat. Biotechnol. 25, 1119-1126 (Pubitemid 47538114)
21. Feng, Y., Mitchison, T. J., Bender, A., Young, D. W., and Tallarico, J. A. (2009) Multi-parameter phenotypic profiling: using cellular effects to characterize small-molecule compounds Nat. Rev. Drug Discovery 8, 567-578
22. Miyoshi, H. (1998) Structure-activity relationships of some complex I inhibitors Biochim. Biophys. Acta 1364, 236-244 (Pubitemid 28291842)
23. van Keulen, M. A. and Berden, J. A. (1985) Antimycin binds to a small subunit of the ubiquinol: cytochrome c oxidoreductase Biochim. Biophys. Acta 808, 32-38 (Pubitemid 15049506)
24. Lardy, H., Reed, P., and Lin, C. H. (1975) Antibiotic inhibitors of mitochondrial ATP synthesis Fed. Proc. 34, 1707-1710
25. Duax, W. L., Griffin, J. F., Langs, D. A., Smith, G. D., Grochulski, P., Pletnev, V., and Ivanov, V. (1996) Molecular structure and mechanisms of action of cyclic and linear ion transport antibiotics Biopolymers 40, 141-155
26. Jeong, H.-W., Lee, H.-J., Kho, Y.-H., Son, K.-H., Han, M. Y., Lim, J.-S., Lee, M.-Y., Han, D. C., Ha, J.-H., and Kwon, B. M. (2002) Biological effects of G1 phase arrest compound, sesquicillin, in human breast cancer cell lines Bioorg. Med. Chem. 10, 3129-3134 (Pubitemid 34855386)
27. Seo, B.-R., Lee, K.-W., Ha, J., Park, H.-J., Choi, J.-W., and Lee, K.-T. (2004) Saucernetin-7 isolated from Saururus chinensis inhibits proliferation of human promyelocytic HL-60 leukemia cells via G0/G1 phase arrest and induction of differentiation Carcinogenesis 25, 1387-1394 (Pubitemid 39172077)
28. Hossain, C. F., Kim, Y.-P., Baerson, S. R., Zhang, L., Bruick, R. K., Mohammed, K. A., Agarwal, A. K., Nagle, D. G., and Zhou, Y.-D. (2005) Saururus cernuus lignans-Potent small molecule inhibitors of hypoxia-inducible factor-1 Biochem. Biophys. Res. Commun. 333, 1026-1033 (Pubitemid 40854259)
29. Hodges, T. W., Hossain, C. F., Kim, Y.-P., Zhou, Y.-D., and Nagle, D. G. (2004) Molecular-targeted antitumor agents: the Saururus cernuus dineolignans manassantin B and 4- O -demethylmanassantin B are potent inhibitors of hypoxia-activated HIF-1 J. Nat. Prod. 67, 767-771 (Pubitemid 38702730)
30. Hwang, B. Y., Lee, J.-H., Nam, J. B., Hong, Y.-S., and Lee, J. J. (2003) Lignans from Saururus chinensis inhibiting the transcription factor NF-κB Phytochemistry 64, 765-771 (Pubitemid 37176411)
31. Rho, M.-C., Kwon, O. E., Kim, K., Lee, S. W., Chung, M. Y., Kim, Y. H., Hayashi, M., Lee, H. S., and Kim, Y.-K. (2003) Inhibitory effects of manassantin A and B isolated from the roots of Saururus chinensis on PMA-induced ICAM-1 expression Planta Med. 69, 1147-1149 (Pubitemid 38223359)
32. Peck, D., Crawford, E. D., Ross, K. N., Stegmaier, K., Golub, T. R., and Lamb, J. (2006) A method for high-throughput gene expression signature analysis Genome Biol. 7, R61
33. Robinson, B. H. (1996) Use of fibroblast and lymphoblast cultures for detection of respiratory chain defects Methods Enzymol. 264, 454-464
34. Nadanaciva, S., Bernal, A., Aggeler, R., Capaldi, R., and Will, Y. (2007) Target identification of drug induced mitochondrial toxicity using immunocapture based OXPHOS activity assays Toxicol. In Vitro 21, 902-911 (Pubitemid 46603229)
35. Huang, S.-L., Yu, R.-T., Gong, J., Feng, Y., Dai, Y.-L., Hu, F., Hu, Y.-H., Tao, Y.-D., and Leng, Y. (2012) Arctigenin, a natural compound, activates AMP-activated protein kinase via inhibition of mitochondria complex I and ameliorates metabolic disorders in ob/ob mice Diabetologia 55, 1469-1481
36. Lipinski, R. J., Dengler, E., Kiehn, M., Peterson, R. E., and Bushman, W. (2007) Identification and characterization of several dietary alkaloids as weak inhibitors of hedgehog signaling Toxicol. Sci. 100, 456-463 (Pubitemid 350131372)
37. 1B receptor inverse agonist 1′-methyl-5-[[2′-methyl-4′-(5-methyl-1,2,4-oxadiazol-3-yl) biphenyl-4-yl]carbonyl]-2,3,6,7-tetrahydrospiro[furo[2,3- f ]indole-3,4′- piperidine] (SB-224289) potently blocks terminal 5-HT autoreceptor function both in vitro and in vivo J. Med. Chem. 41, 1218-1235 (Pubitemid 28208177)
38. Marroquin, L. D., Hynes, J., Dykens, J. A., Jamieson, J. D., and Will, Y. (2007) Circumventing the Crabtree Effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants Toxicol. Sci. 97, 539-547 (Pubitemid 47073868)
39. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing J. R. Statist. Soc. B 57, 289-300