Genetic basis for the biosynthesis of the pharmaceutically important class of epoxyketone proteasome inhibitors

ACS Chemical Biology

Volumn 9, Issue 1, 2014, Pages 301-309

  Schorn, Michelle ^a   Zettler, Judith ^d,e   Noel, Joseph P ^b   Dorrestein, Pieter C ^c   Moore, Bradley S ^a,c   Kaysser, Leonard ^a,d,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e German Center for Research in Infectious Disease (DZIF)   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARFILZOMIB; EPONEMYCIN; EPOXOMICIN; NONRIBOSOMAL PEPTIDE SYNTHETASE; PROTEASOME INHIBITOR; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BORTEZOMIB; CARMAPHYCIN; KETONE DERIVATIVE; MULTIFUNCTIONAL ENZYME; OXIDOREDUCTASE; TMC 86A; TMC 86B; TMC 89A; TMC 96;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; DNA SEQUENCE; DRUG IDENTIFICATION; DRUG SYNTHESIS; GENE CLUSTER; GENE LIBRARY; GENETIC LINKAGE; HETEROLOGOUS EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOMYCES ALBUS; STREPTOMYCES HYGROSCOPICUS; ACTINOBACTERIA; COMPLEX FORMATION; GENE; GENE EXPRESSION; GENE SEQUENCE; GENE SYNTHESIS; GENETIC CODE; MASS SPECTROMETRY; METABOLOMICS; NUCLEOTIDE SEQUENCE;

AMIDES; BASE SEQUENCE; GENES, BACTERIAL; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OLIGOPEPTIDES; PROTEASOME INHIBITORS; SERINE; STREPTOMYCES;

EID: 84900396854     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400699     Document Type: Article

References (50)

1. Ciechanover, A. (1994) The ubiquitin-proteasome proteolytic pathway. Cell 79, 13-21. (Pubitemid 24309509)
2. Lopes, U. G., Erhardt, P., Yao, R., and Cooper, G. M. (1997) p53-dependent induction of apoptosis by proteasome inhibitors. J. Biol. Chem. 272, 12893-12896. (Pubitemid 27216701)
3. Drexler, H. C. (1997) Activation of the cell death program by inhibition of proteasome function. Proc. Natl. Acad. Sci. U.S.A. 94, 855-860. (Pubitemid 27074411)
4. Grawert, M. A., and Groll, M. (2012) Exploiting natures rich source of proteasome inhibitors as starting points in drug development. Chem. Commun. (Camb.) 48, 1364-1378.
5. Hanada, M., Sugawara, K., Kaneta, K., Toda, S., Nishiyama, Y., Tomita, K., Yamamoto, H., Konishi, M., and Oki, T. (1992) Epoxomicin, a new antitumor agent of microbial origin. J. Antibiot. (Tokyo) 45, 1746-1752. (Pubitemid 23015454)
6. Sugawara, K., Hatori, M., Nishiyama, Y., Tomita, K., Kamei, H., Konishi, M., and Oki, T. (1990) Eponemycin, a new antibiotic active against B16 melanoma. I. Production, isolation, structure, and biological activity. J. Antibiot. (Tokyo) 43, 8-18. (Pubitemid 20043960)
7. Pereira, A. R., Kale, A. J., Fenley, A. T., Byrum, T., Debonsi, H. M., Gilson, M. K., Valeriote, F. A., Moore, B. S., and Gerwick, W. H. (2012) The carmaphycins: New proteasome inhibitors exhibiting an α,β-epoxyketone warhead from a marine cyanobacterium. Chembiochem 13, 810-817.
8. Koguchi, Y., Kohno, J., Suzuki, S., Nishio, M., Takahashi, K., Ohnuki, T., and Komatsubara, S. (2000) TMC-86A, B and TMC-96, new proteasome inhibitors from Streptomyces sp. TC 1084 and Saccharothrix sp. TC 1094. II. Physico-chemical properties and structure determination. J. Antibiot. (Tokyo) 53, 63-65. (Pubitemid 30088572)
9. Koguchi, Y., Nishio, M., Suzuki, S., Takahashi, K., Ohnuki, T., and Komatsubara, S. (2000) TMC-89A and B, new proteasome inhibitors from Streptomyces sp. TC 1087. J. Antibiot. (Tokyo) 53, 967-972.
10. Kuhn, D. J., Chen, Q., Voorhees, P. M., Strader, J. S., Shenk, K. D., Sun, C. M., Demo, S. D., Bennett, M. K., van Leeuwen, F. W., Chanan-Khan, A. A., and Orlowski, R. Z. (2007) Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 110, 3281-3290. (Pubitemid 350106321)
11. McCormack, P. L. (2012) Carfilzomib: In relapsed, or relapsed and refractory, multiple myeloma. Drugs 72, 2023-2032.
12. Curran, M. P., and McKeage, K. (2009) Bortezomib: A review of its use in patients with multiple myeloma. Drugs 69, 859-888.
13. Glenn, R. J., Pemberton, A. J., Royle, H. J., Spackman, R. W., Smith, E., Jennifer Rivett, A., and Steverding, D. (2004) Trypanocidal effect of α,β-epoxyketones indicates that trypanosomes are particularly sensitive to inhibitors of proteasome trypsin-like activity. Int. J. Antimicrob. Agents 24, 286-289.
14. Czesny, B., Goshu, S., Cook, J. L., and Williamson, K. C. (2009) The proteasome inhibitor epoxomicin has potent Plasmodium falciparum gametocytocidal activity. Antimicrob. Agents Chemother. 53, 4080-4085.
15. 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. (Pubitemid 30117471)
16. Rothberg, J. M., Hinz, W., Rearick, T. M., Schultz, J., Mileski, W., Davey, M., Leamon, J. H., Johnson, K., Milgrew, M. J., Edwards, M., Hoon, J., Simons, J. F., Marran, D., Myers, J. W., Davidson, J. F., Branting, A., Nobile, J. R., Puc, B. P., Light, D., Clark, T. A., Huber, M., Branciforte, J. T., Stoner, I. B., Cawley, S. E., Lyons, M., Fu, Y., Homer, N., Sedova, M., Miao, X., Reed, B., Sabina, J., Feierstein, E., Schorn, M., Alanjary, M., Dimalanta, E., Dressman, D., Kasinskas, R., Sokolsky, T., Fidanza, J. A., Namsaraev, E., McKernan, K. J., Williams, A., Roth, G. T., and Bustillo, J. (2011) An integrated semiconductor device enabling non-optical genome sequencing. Nature 475, 348-352.
17. Ross, A. C., Xu, Y., Lu, L., Kersten, R. D., Shao, Z., Al-Suwailem, A. M., Dorrestein, P. C., Qian, P. Y., and Moore, B. S. (2013) Biosynthetic multitasking facilitates thalassospiramide structural diversity in marine bacteria. J. Am. Chem. Soc. 135, 1155-1162.
18. Henke, W., Herdel, K., Jung, K., Schnorr, D., and Loening, S. A. (1997) Betaine improves the PCR amplification of GC-rich DNA sequences. Nucleic Acids Res. 25, 3957-3958. (Pubitemid 27420509)
19. Medema, M. H., Blin, K., Cimermancic, P., de Jager, V., Zakrzewski, P., Fischbach, M. A., Weber, T., Takano, E., and Breitling, R. (2011) antiSMASH: Rapid identification, annotation, and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 39, 339-346.
20. Kale, A. J., McGlinchey, R. P., Lechner, A., and Moore, B. S. (2011) Bacterial self-resistance to the natural proteasome inhibitor salinosporamide A. ACS Chem. Biol. 6, 1257-1264.
21. Kaysser, L., Bernhardt, P., Nam, S. J., Loesgen, S., Ruby, J. G., Skewes-Cox, P., Jensen, P. R., Fenical, W., and Moore, B. S. (2012) Merochlorins A-D, cyclic meroterpenoid antibiotics biosynthesized in divergent pathways with vanadium-dependent chloroperoxidases. J. Am. Chem. Soc. 134, 11988-11991.
22. Bierman, M., Logan, R., OBrien, K., Seno, E. T., Rao, R. N., and Schoner, B. E. (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116, 43-49.
23. Labeda, D. P., and Kroppenstedt, R. M. (2006) Goodfellowia gen. nov., a new genus of the Pseudonocardineae related to Actinoalloteichus, containing Goodfellowia coeruleoviolacea gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 56, 1203-1207. (Pubitemid 43940754)
24. Flett, F., Mersinias, V., and Smith, C. P. (1997) High efficiency intergeneric conjugal transfer of plasmid DNA from Escherichia coli to methyl DNA-restricting streptomycetes. FEMS Microbiol. Lett. 155, 223-229. (Pubitemid 28248232)
25. Lombo, F., Velasco, A., Castro, A., de la Calle, F., Brana, A. F., Sanchez-Puelles, J. M., Mendez, C., and Salas, J. A. (2006) Deciphering the biosynthesis pathway of the antitumor thiocoraline from a marine actinomycete and its expression in two streptomyces species. ChemBioChem 7, 366-376. (Pubitemid 43220952)
26. Bandeira, N., Tsur, D., Frank, A., and Pevzner, P. A. (2007) Protein identification by spectral networks analysis. Proc. Natl. Acad. Sci. U.S.A. 104, 6140-6145. (Pubitemid 47186062)
27. Guthals, A., Watrous, J. D., Dorrestein, P. C., and Bandeira, N. (2012) The spectral networks paradigm in high throughput mass spectrometry. Mol. Biosyst. 8, 2535-2544.
28. Watrous, J., Roach, P., Alexandrov, T., Heath, B. S., Yang, J. Y., Kersten, R. D., van der Voort, M., Pogliano, K., Gross, H., Raaijmakers, J. M., Moore, B. S., Laskin, J., Bandeira, N., and Dorrestein, P. C. (2012) Mass spectral molecular networking of living microbial colonies. Proc. Natl. Acad. Sci. U.S.A. 109, 1743-1752.
29. Nguyen, D. D., Wu, C. H., Moree, W. J., Lamsa, A., Medema, M. H., Zhao, X., Gavilan, R. G., Aparicio, M., Atencio, L., Jackson, C., Ballesteros, J., Sanchez, J., Watrous, J. D., Phelan, V. V., van de Wiel, C., Kersten, R. D., Mehnaz, S., De Mot, R., Shank, E. A., Charusanti, P., Nagarajan, H., Duggan, B. M., Moore, B. S., Bandeira, N., Palsson, B. O., Pogliano, K., Gutierrez, M., and Dorrestein, P. C. (2013) MS/ MS networking guided analysis of molecule and gene cluster families. Proc. Natl. Acad. Sci. U.S.A. 110, 2611-2620.
30. Challis, G. L., Ravel, J., and Townsend, C. A. (2000) Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem. Biol. 7, 211-224. (Pubitemid 30147205)
31. Stachelhaus, T., Mootz, H. D., and Marahiel, M. A. (1999) The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 6, 493-505. (Pubitemid 29380764)
32. Rausch, C., Hoof, I., Weber, T., Wohlleben, W., and Huson, D. H. (2007) Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution. BMC Evol. Biol. 7, 78.
33. Kraas, F. I., Giessen, T. W., and Marahiel, M. A. (2012) Exploring the mechanism of lipid transfer during biosynthesis of the acidic lipopeptide antibiotic CDA. FEBS Lett. 586, 283-288.
34. Wilkinson, S., and Lowe, L. A. (1964) Structure of polymyxin B1. Nature 202, 1211.
35. Powell, A., Borg, M., Amir-Heidari, B., Neary, J. M., Thirlway, J., Wilkinson, B., Smith, C. P., and Micklefield, J. (2007) Engineered biosynthesis of nonribosomal lipopeptides with modified fatty acid side chains. J. Am. Chem. Soc. 129, 15182-15191.
36. Revill, W. P., Bibb, M. J., Scheu, A. K., Kieser, H. J., and Hopwood, D. A. (2001) β-ketoacyl acyl carrier protein synthase III (FabH) is essential for fatty acid biosynthesis in Streptomyces coelicolor A3(2). J. Bacteriol. 183, 3526-3530. (Pubitemid 32448617)
37. Moore, B. S., and Hertweck, C. (2002) Biosynthesis and attachment of novel bacterial polyketide synthase starter units. Nat. Prod. Rep. 19, 70-99. (Pubitemid 34140334)
38. Thibodeaux, C. J., Chang, W. C., and Liu, H. W. (2012) Enzymatic chemistry of cyclopropane, epoxide, and aziridine biosynthesis. Chem. Rev. 112, 1681-1709.
39. Read, J. A., and Walsh, C. T. (2007) The lyngbyatoxin biosynthetic assembly line: Chain release by four-electron reduction of a dipeptidyl thioester to the corresponding alcohol. J. Am. Chem. Soc. 129, 15762-15763.
40. Hofvander, P., Doan, T. T., and Hamberg, M. (2011) A prokaryotic acyl-CoA reductase performing reduction of fatty acyl-CoA to fatty alcohol. FEBS Lett. 585, 3538-3543.
41. Gulder, T. A., Freeman, M. F., and Piel, J. (2011) The catalytic diversity of multimodular polyketide synthases: Natural product biosynthesis beyond textbook assembly rules. Top. Curr. Chem., DOI: 10.1007/128-2010-113.
42. Stein, M. L., Beck, P., Kaiser, M., Dudler, R., Becker, C. F., and Groll, M. (2012) One-shot NMR analysis of microbial secretions identifies highly potent proteasome inhibitor. Proc. Natl. Acad. Sci. U.S.A. 109, 18367-18371.
43. Krahn, D., Ottmann, C., and Kaiser, M. (2011) The chemistry and biology of syringolins, glidobactins, and cepafungins (syrbactins). Nat. Prod. Rep. 28, 1854-1867.
44. Sambrook, J., and Russell, D. W. (2001) Molecular Cloning. A Laboratory Manual, Cold Spring Harbor Laboratory Press, New York.
45. Kieser, T., Bibb, M., Buttner, M., Chater, K., and Hopwood, D. (2000) Practical Streptomyces Genetics, The John Innes Foundation, Norwich, U.K.
46. Patiny, L., and Borel, A. (2013) ChemCalc: A building block for tomorrows chemical infrastructure. J. Chem. Inf. Model 53, 1223-1228.
47. Frank, A. M., Bandeira, N., Shen, Z., Tanner, S., Briggs, S. P., Smith, R. D., and Pevzner, P. A. (2008) Clustering millions of tandem mass spectra. J. Proteome Res. 7, 113-122. (Pubitemid 351171122)
48. Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L., and Ideker, T. (2011) Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 27, 431-432.
49. Bibb, M. J., Findlay, P. R., and Johnson, M. W. (1984) The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of proteincoding sequences. Gene 30, 157-166. (Pubitemid 15201773)
50. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (Pubitemid 27359211)