Thiol Probes to Detect Electrophilic Natural Products Based on Their Mechanism of Action

ACS Chemical Biology

Volumn 11, Issue 8, 2016, Pages 2328-2336

  Castro Falcón, Gabriel ^a   Hahn, Dongyup ^a   Reimer, Daniela ^a   Hughes, Chambers C ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGRAPHOLIDE; AROMATIC COMPOUND; BROMINE; CHLORINE; CYCLOMARIN A; CYSTEINE; CYTOTOXIC AGENT; EPONEMYCIN; EPOXOMICIN; ETOPOSIDE; NATURAL PRODUCT; PARTHENOLIDE; PENICILLIN G; SALINAMIDE A; SALINOSPORAMIDE A; THIOPHENOL; TIRANDALYDIGIN; TRIPTOLIDE; UNCLASSIFIED DRUG; WORTMANNIN; BIOLOGICAL PRODUCT; MOLECULAR PROBE; THIOL DERIVATIVE;

ANDROGRAPHIS PANICULATA; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIUM; CONTROLLED STUDY; CYTOTOXICITY; DRUG DETERMINATION; DRUG IDENTIFICATION; DRUG MECHANISM; ELECTROPHILICITY; ENZYME INHIBITION; HALOGENATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IC50; MASS SPECTROMETRY; MOLECULAR PROBE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; SALINISPORA TROPICA; STREPTOMYCES HYGROSCOPICUS; SUBSTITUTION REACTION; TALAROMYCES; TALAROMYCES WORTMANII; TANACETUM PARTHENIUM; X RAY CRYSTALLOGRAPHY; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; TUMOR CELL LINE;

BIOLOGICAL PRODUCTS; CELL LINE, TUMOR; CRYSTALLOGRAPHY, X-RAY; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR PROBES; SULFHYDRYL COMPOUNDS;

EID: 84983283319     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00924     Document Type: Article

References (68)

1. Newman, D. J. and Cragg, G. M. (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010 J. Nat. Prod. 75, 311-335 10.1021/np200906s
2. Cragg, G. M. and Newman, D. J. (2013) Natural products: A continuing source of novel drug leads Biochim. Biophys. Acta, Gen. Subj. 1830, 3670-3695 10.1016/j.bbagen.2013.02.008
3. Bentley, S. D., Chater, K. F., Cerdeño-Tárraga, A.-M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H., Harper, D., Bateman, A., Brown, S., Chandra, G., Chen, C. W., Collins, M., Cronin, A., Fraser, A., Goble, A., Hidalgo, J., Hornsby, T., Howarth, S., Huang, C.-H., Kieser, T., Larke, L., Murphy, L., Oliver, K., O'Neil, S., Rabbinowitsch, E., Rajandream, M.-A., Rutherford, K., Rutter, S., Seeger, K., Saunders, D., Sharp, S., Squares, R., Squares, S., Taylor, K., Warren, T., Wietzorrek, A., Woodward, J., Barrell, B. G., Parkhill, J., and Hopwood, D. A. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) Nature 417, 141-147 10.1038/417141a
4. Udwary, D. W., Zeigler, L., Asolkar, R. N., Singan, V., Lapidus, A., Fenical, W., Jensen, P. R., and Moore, 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 10.1073/pnas.0700962104
5. Zhang, H., Boghigian, B. A., Armando, J., and Pfeifer, B. A. (2011) Methods and options for the heterologous production of complex natural products Nat. Prod. Rep. 28, 125-151 10.1039/C0NP00037J
6. Ongley, S. E., Bian, X., Neilan, B. A., and Müller, R. (2013) Recent advances in the heterologous expression of microbial natural product biosynthetic pathways Nat. Prod. Rep. 30, 1121-38 10.1039/c3np70034h
7. Marfey, P. (1984) Determination of D-amino acids. II. Use of a bifunctional reagent, 1,5-difluoro-2,4-dinitrobenzene Carlsberg Res. Commun. 49, 591-596 10.1007/BF02908688
8. Carlson, E. E. and Cravatt, B. F. (2007) Enrichment tags for enhanced-resolution profiling of the polar metabolome J. Am. Chem. Soc. 129, 15780-15782 10.1021/ja0779506
9. Carlson, E. E. and Cravatt, B. F. (2007) Chemoselective probes for metabolite enrichment and profiling Nat. Methods 4, 429-435 10.1038/nmeth1038
10. Odendaal, A. Y., Trader, D. J., and Carlson, E. E. (2011) Chemoselective enrichment for natural products discovery Chem. Sci. 2, 760-764 10.1039/c0sc00620c
11. Jeon, H., Lim, C., Lee, J. M., and Kim, S. (2015) Chemical assay-guided natural product isolation via solid-supported chemodosimetric fluorescent probe Chem. Sci. 6, 2806-2811 10.1039/C5SC00360A
12. Miles, C. O., Sandvik, M., Nonga, H. E., Rundberget, T., Wilkins, A. L., Rise, F., and Ballot, A. (2012) Thiol derivatization for LC-MS identification of microcystins in complex matrices Environ. Sci. Technol. 46, 8937-8944 10.1021/es301808h
13. Cox, C. L., Tietz, J. I., Sokolowski, K., Melby, J. O., Doroghazi, J. R., and Mitchell, D. A. (2014) Nucleophilic 1,4-additions for natural product discovery ACS Chem. Biol. 9, 2014-2022 10.1021/cb500324n
14. Ross, C., Scherlach, K., Kloss, F., and Hertweck, C. (2014) The molecular basis of conjugated polyyne biosynthesis in phytopathogenic bacteria Angew. Chem., Int. Ed. 53, 7794-7798 10.1002/anie.201403344
15. Pérez, A. J., Wesche, F., Adihou, H., and Bode, H. B. (2016) Solid-phase enrichment and analysis of azide-labeled natural products: Fishing downstream of biochemical pathways Chem.-Eur. J. 22, 639-645 10.1002/chem.201503781
16. Rudolf, G. C., Koch, M. F., Mandl, F. A. M., and Sieber, S. A. (2015) Subclass-specific labeling of protein-reactive natural products with customized nucleophilic probes Chem.-Eur. J. 21, 3701-3707 10.1002/chem.201405009
17. Drahl, C., Cravatt, B. F., and Sorensen, E. J. (2005) Protein-reactive natural products Angew. Chem., Int. Ed. 44, 5788-5809 10.1002/anie.200500900
18. Gersch, M., Kreuzer, J., and Sieber, S. A. (2012) Electrophilic natural products and their biological targets Nat. Prod. Rep. 29, 659-682 10.1039/c2np20012k
19. Singh, J., Petter, R. C., Baillie, T. A., and Whitty, A. (2011) The resurgence of covalent drugs Nat. Rev. Drug Discovery 10, 307-317 10.1038/nrd3410
20. Sanderson, K. (2013) Irreversible kinase inhibitors gain traction Nat. Rev. Drug Discovery 12, 649-51 10.1038/nrd4103
21. Corey, E. J., Clark, D. A., Goto, G., Marfat, A., Mioskowski, C., Samuelsson, B., and Hammarstroem, S. (1980) Stereospecific total synthesis of a" slow reacting substance" of anaphylaxis, leukotriene C-1 J. Am. Chem. Soc. 102, 1436-1439 10.1021/ja00524a045
22. Corey, E. J., Albright, J. O., Barton, A. E., and Hashimoto, S. (1980) Chemical and enzymic syntheses of 5-HPETE, a key biological precursor of slow-reacting substance of anaphylaxis (SRS), and 5-HETE J. Am. Chem. Soc. 102, 1435-1436 10.1021/ja00524a044
23. Llinás, A., Donoso, J., Vilanova, B., Frau, J., Muñoz, F., and Page, M. I. (2000) Thiol-catalysed hydrolysis of benzylpenicillin J. Chem. Soc., Perkin Trans. 2, 1521-1525 10.1039/b001091j
24. Martinelli, M. J., Vaidyanathan, R., Khau, V. V., and Staszak, M. A. (2002) Reaction of cryptophycin 52 with thiols Tetrahedron Lett. 43, 3365-3367 10.1016/S0040-4039(02)00553-1
25. Oda, K. and Yoshida, A. (1997) Side chain substitution reaction of 2-arylsulfinyl and 2-arylsulfonyl intermediates for 1β-methylcarbapenems Tetrahedron Lett. 38, 5687-5690 10.1016/S0040-4039(97)01239-2
26. Naidu, B. N., Sorenson, M. E., Connolly, T. P., and Ueda, Y. (2003) Michael addition of amines and thiols to dehydroalanine amides: A remarkable rate acceleration in water J. Org. Chem. 68, 10098-10102 10.1021/jo034762z
27. Matsuura, F., Peters, R., Anada, M., Harried, S. S., Hao, J., and Kishi, Y. (2006) Unified total synthesis of pteriatoxins and their diastereomers J. Am. Chem. Soc. 128, 7463-7465 10.1021/ja0618954
28. Taubinger, A. A., Fenske, D., and Podlech, J. (2008) Synthesis of β,β-diamino acids from α-amino acid derived β-lactams Synlett 2008, 539-542 10.1055/s-2008-1032079
29. Schoof, S., Pradel, G., Aminake, M. N., Ellinger, B., Baumann, S., Potowski, M., Najajreh, Y., Kirschner, M., and Arndt, H. D. (2010) Antiplasmodial thiostrepton derivatives: Proteasome inhibitors with a dual mode of action Angew. Chem., Int. Ed. 49, 3317-3321 10.1002/anie.200906988
30. Csuk, R., Heinold, A., Siewert, B., Schwarz, S., Barthel, A., Kluge, R., and Ströhl, D. (2012) Synthesis and biological evaluation of antitumor-active arglabin derivatives Arch. Pharm. (Weinheim, Ger.) 345, 215-222 10.1002/ardp.201100065
31. Avonto, C., Taglialatela-scafati, O., Pollastro, F., Minassi, A., Di Marzo, V., De Petrocellis, L., and Appendino, G. (2011) An NMR spectroscopic method to identify and classify thiol- trapping agents: Revival of Michael acceptors for drug discovery? Angew. Chem., Int. Ed. 50, 467-471 10.1002/anie.201005959
32. Gerwick, W. H., Fenical, W., Van Engen, D., and Clardy, J. (1980) Isolation and structure of spatol, a potent inhibitor of cell replication from the brown seaweed Spatoglossum schmittii J. Am. Chem. Soc. 102, 7991-7993 10.1021/ja00547a055
33. Pettit, G. P., Herald, D. L., Gao, F., Sengupta, D., and Herald, C. L. (1991) Antineoplastic agents. 200. Absolute configuration of the bryostatins J. Org. Chem. 56, 1337-1340 10.1021/jo00003a086
34. Ondeyka, J. G., Helms, G. L., Hensens, O. D., Goetz, M. A., Zink, D. L., Tsipouras, A., Shoop, W. L., Slayton, L., Dombrowski, A. W., Polishook, J. D., Ostlind, D. A., Tsou, N. N., Ball, R. G., and Singh, S. B. (1997) Nodulisporic acid A, a novel and potent insecticide from a Nodulisporium sp. Isolation, structure determination, and chemical transformations J. Am. Chem. Soc. 119, 8809-8816 10.1021/ja971664k
35. Shigemori, H., Komaki, H., Yazawa, K., Mikami, Y., Nemoto, A., Tanaka, Y., Sasaki, T., In, Y., Ishida, T., and Kobayashi, J. (1998) Brasilicardin A. A novel tricyclic metabolite with potent immunosuppressive activity from actinomycete Nocardia brasiliensis J. Org. Chem. 63, 6900-6904 10.1021/jo9807114
36. Brady, S. F., Bondi, S. M., and Clardy, J. (2001) The guanacastepenes: A highly diverse family of secondary metabolites produced by an endophytic fungus J. Am. Chem. Soc. 123, 9900-9901 10.1021/ja016176y
37. Kwok, B. H. B., Koh, B., Ndubuisi, M. I., Elofsson, M., and Crews, C. M. (2001) The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits I-kappa B kinase Chem. Biol. 8, 759-766 10.1016/S1074-5521(01)00049-7
38. Xia, Y.-F., Ye, B.-Q., Li, Y.-D., Wang, J.-G., He, X.-J., Lin, X., Yao, X., Ma, D., Slungaard, A., Hebbel, R. P., Key, N. S., and Geng, J.-G. (2004) Andrographolide attenuates inflammation by inhibition of NF-kappa B activation through covalent modification of reduced cysteine 62 of p50 J. Immunol. 173, 4207-4217 10.4049/jimmunol.173.6.4207
39. Arcaro, A. and Wymann, M. P. (1993) Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses Biochem. J. 296, 297-301 10.1042/bj2960297
40. Norman, B. H., Shih, C., Toth, J. E., Ray, J. E., Dodge, J. A., Johnson, D. W., Rutherford, P. G., Schultz, R. M., Worzalla, J. F., and Vlahos, C. J. (1996) Studies on the mechanism of phosphatidylinositol 3-kinase inhibition by wortmannin and related analogs J. Med. Chem. 39, 1106-1111 10.1021/jm950619p
41. Wymann, M. P., Bulgarelli-Leva, G., Zvelebil, M. J., Pirola, L., Vanhaesebroeck, B., Waterfield, M. D., and Panayotou, G. (1996) Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys-802, a residue involved in the phosphate transfer reaction Mol. Cell. Biol. 16, 1722-1733 10.1128/MCB.16.4.1722
42. Walker, E. H., Pacold, M. E., Perisic, O., Stephens, L., Hawkins, P. T., Wymann, M. P., and Williams, R. L. (2000) Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine Mol. Cell 6, 909-919 10.1016/S1097-2765(05)00089-4
43. Yocum, R. R., Waxman, D. J., Rasmussen, J. R., and Strominger, J. L. (1979) Mechanism of penicillin action: penicillin and substrate bind covalently to the same active site serine in two bacterial D-alanine carboxypeptidases Proc. Natl. Acad. Sci. U. S. A. 76, 2730-2734 10.1073/pnas.76.6.2730
44. Feling, R. H., Buchanan, G. O., Mincer, T. J., Kauffman, C. A., Jensen, P. R., and Fenical, W. (2003) Salinosporamide A: A highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus Salinospora Angew. Chem., Int. Ed. 42, 355-357 10.1002/anie.200390115
45. Groll, M., Huber, R., and Potts, B. C. M. (2006) Crystal structures of salinosporamide A (NPI-0052) and B (NPI-0047) in complex with the 20S proteasome reveal important consequences of β-lactone ring opening and a mechanism for irreversible binding J. Am. Chem. Soc. 128, 5136-5141 10.1021/ja058320b
46. Flack, H. D. (1983) On enantiomorph-polarity estimation Acta Crystallogr., Sect. A: Found. Crystallogr. 39, 876-881 10.1107/S0108767383001762
47. McCallum, C., Kwon, S., Leavitt, P., Shen, D. M., Liu, W., and Gurnett, A. (2007) Triptolide binds covalently to a 90 kDa nuclear protein. Role of epoxides in binding and activity Immunobiology 212, 549-556 10.1016/j.imbio.2007.02.002
48. Titov, D. V., Gilman, B., He, Q.-L., Bhat, S., Low, W.-K., Dang, Y., Smeaton, M., Demain, A. L., Miller, P. S., Kugel, J. F., Goodrich, J. A., and Liu, J. O. (2011) XPB, a subunit of TFIIH, is a target of the natural product triptolide Nat. Chem. Biol. 7, 182-188 10.1038/nchembio.522
49. He, Q.-L., Titov, D. V., Li, J., Tan, M., Ye, Z., Zhao, Y., Romo, D., and Liu, J. O. (2015) Covalent modification of a cysteine residue in the XPB subunit of the general transcription factor TFIIH through single epoxide cleavage of the transcription inhibitor triptolide Angew. Chem., Int. Ed. 54, 1859-1863 10.1002/anie.201408817
50. Kim, K. B., Myung, J., Sin, N., and Crews, C. M. (1999) Proteasome inhibition by the natural products epoxomicin and dihydroeponemycin: Insights into specificity and potency Bioorg. Med. Chem. Lett. 9, 3335-3340 10.1016/S0960-894X(99)00612-5
51. Groll, M., Kim, K. B., Kairies, N., Huber, R., and Crews, C. M. (2000) Crystal structure of epoxomicin: 20S proteasome reveals a molecular basis for selectivity of α,β-epoxyketone proteasome inhibitors J. Am. Chem. Soc. 122, 1237-1238 10.1021/ja993588m
52. Meng, L., Kwok, B. H. B., Sin, N., and Crews, C. M. (1999) Eponemycin exerts its antitumor effect through the inhibition of proteasome function Cancer Res. 59, 2798-2801
53. Schorn, M., Zettler, J., Noel, J. P., Dorrestein, P. C., Moore, B. S., and Kaysser, L. (2014) Genetic basis for the biosynthesis of the pharmaceutically important class of epoxyketone proteasome inhibitors ACS Chem. Biol. 9, 301-309 10.1021/cb400699p
54. Renner, M., Shen, Y., Cheng, X., Jensen, P. R., Frankmoelle, W., Kauffman, C. A., Fenical, W., Lobkovsky, E., and Clardy, J. (1999) Cyclomarins A-C, new anti infl ammatory cyclic peptides produced by a marine bacterium (Streptomyces sp.) J. Am. Chem. Soc. 121, 11273-11276 10.1021/ja992482o
55. Schmitt, E. K., Riwanto, M., Sambandamurthy, V., Roggo, S., Miault, C., Zwingelstein, C., Krastel, P., Noble, C., Beer, D., Rao, S. P. S., Au, M., Niyomrattanakit, P., Lim, V., Zheng, J., Jeffery, D., Pethe, K., and Camacho, L. R. (2011) The natural product cyclomarin kills mycobacterium tuberculosis by targeting the ClpC1 subunit of the caseinolytic protease Angew. Chem., Int. Ed. 50, 5889-5891 10.1002/anie.201101740
56. Vasudevan, D., Rao, S. P. S., and Noble, C. G. (2013) Structural basis of mycobacterial inhibition by cyclomarin A J. Biol. Chem. 288, 30883-30891 10.1074/jbc.M113.493767
57. Bürstner, N., Roggo, S., Ostermann, N., Blank, J., Delmas, C., Freuler, F., Gerhartz, B., Hinniger, A., Hoepfner, D., Liechty, B., Mihalic, M., Murphy, J., Pistorius, D., Rottmann, M., Thomas, J. R., Schirle, M., and Schmitt, E. K. (2015) Gift from nature: Cyclomarin A kills mycobacteria and malaria parasites by distinct modes of action ChemBioChem 16, 2433-2436 10.1002/cbic.201500472
58. Trischman, J. A., Tapiolas, D. M., Jensen, P. R., Dwight, R., Fenical, W., Mckee, T. C., Ireland, C. M., Stout, T. J., and Clardy, J. (1994) Salinamides A and B: anti-inflammatory depsipeptides from a marine Streptomyces J. Am. Chem. Soc. 116, 757-758 10.1021/ja00081a042
59. Moore, B. S., Trischman, J. A., Seng, D., Kho, D., Jensen, P. R., and Fenical, W. (1999) Salinamides, antiinflammatory depsipeptides from a marine streptomycete J. Org. Chem. 64, 1145-1150 10.1021/jo9814391
60. Degen, D., Feng, Y., Zhang, Y., Ebright, K. Y., Ebright, Y. W., Gigliotti, M., Vahedian-Movahed, H., Mandal, S., Talaue, M., Connell, N., Arnold, E., Fenical, W., and Ebright, R. H. (2014) Transcription inhibition by the depsipeptide antibiotic salinamide A eLife 3, e02451 10.7554/eLife.02451
61. Hassan, H. M., Degen, D., Jang, K. H., Ebright, R. H., and Fenical, W. (2015) Salinamide F, new depsipeptide antibiotic and inhibitor of bacterial RNA polymerase from a marine-derived Streptomyces sp J. Antibiot. 68, 206-209 10.1038/ja.2014.122
62. Ziemert, N., Lechner, A., Wietz, M., Millán-Aguiñaga, 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-E1139 10.1073/pnas.1324161111
63. Brill, G. M., McAlpine, J. B., and Whittern, D. (1988) Tirandalydigin, a novel tetramic acid of the tirandamycin-streptolydigin type. II. Isolation and structural characterization J. Antibiot. 41, 36-44 10.7164/antibiotics.41.36
64. Karwowski, J. P., Jackson, M., Theriault, R. J., Barlow, G. J., Coen, L., Hensey, D. M., and Humphrey, P. E. (1992) Tirandalydigin, a novel tetramic acid of the tirandamycin-streptolydigin type. I. Taxonomy of the producing organism, fermentation and biological activity J. Antibiot. 45, 1125-1132 10.7164/antibiotics.45.1125
65. Omura, S., Fujimoto, T., Otoguro, K., Matsuzaki, K., Moriguchi, R., Tanaka, H., and Sasaki, Y. (1991) Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells J. Antibiot. 44, 113-116 10.7164/antibiotics.44.113
66. Reed, K. A., Manam, R. R., Mitchell, S. S., Xu, J., Teisan, S., Chao, T. H., Deyanat-Yazdi, G., Neuteboom, S. T. C., Lam, K. S., and Potts, B. C. M. (2007) Salinosporamides D-J from the marine actinomycete Salinispora tropica, bromosalinosporamide, and thioester derivatives are potent inhibitors of the 20S proteasome J. Nat. Prod. 70, 269-276 10.1021/np0603471
67. Dick, L. R., Cruikshank, A. A., Grenier, L., Melandri, F. D., Nunes, S. L., and Stein, R. L. (1996) Mechanistic studies on the inactivation of the proteasome by lactacystin J. Biol. Chem. 271, 7273-7276 10.1074/jbc.271.13.7273
68. Dick, L. R., Cruikshank, A. A., Destree, A. A., Grenier, L., McCormack, T. A., Melandri, F. D., Nunes, S. L., Palombella, V. J., Parent, L. A., Plamondon, L., and Stein, R. L. (1997) Mechanistic studies on the inactivation of the proteasome by lactacystin in cultured cells J. Biol. Chem. 272, 182-188 10.1074/jbc.272.1.182