Short pathways to complexity generation: Fungal peptidyl alkaloid multicyclic scaffolds from anthranilate building blocks

ACS Chemical Biology

Volumn 8, Issue 7, 2013, Pages 1366-1382

  Walsh, Christopher T ^a   Haynes, Stuart W ^a   Ames, Brian D ^a   Gao, Xue ^b   Tang, Yi ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOID; ANACINE; ANTHRANILATE SYNTHASE; ANTHRANILIC ACID DERIVATIVE; ASPERIFICIN C; ASPERLICIN C; ASPERLICIN D; ASPERLICIN E; CHAETOMININE; CYCLOPEPTINE; DEHYDROCYCLOPEPTINE; DIMETHYLALLYLTRANSFERASE; FISCALIN A; FISCALIN B; FISCALIN C; FUMIQUINAZOLINE A; FUMIQUINAZOLINE D; FUMIQUINAZOLINE DERIVATIVE; FUMIQUINAZOLINE F; NONRIBOSOMAL PEPTIDE SYNTHETASE; OXYGENASE; SERANYLTRYPINONE; SIBIROMYCIN; TOMAYMYCIN; TRYPTOPHAN SYNTHASE; UNCLASSIFIED DRUG; VERRUCINE A; VERRUCINE B;

ADENYLATION; ASPERGILLUS; CATALYSIS; CYCLIZATION; HYDROXYLATION; METABOLOME; NEOSARTORYA; NONHUMAN; OXIDATION; PENICILLIUM; PRIORITY JOURNAL; REVIEW;

ALKALOIDS; FUNGI; GLIOTOXIN; INDOLES; MOLECULAR STRUCTURE; ORTHO-AMINOBENZOATES; PEPTIDE SYNTHASES; PEPTIDES; PIPERAZINES; SPIRO COMPOUNDS;

EID: 84880519804     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb4001684     Document Type: Review

References (82)

1. Hanson, J. R. (2008) The Chemistry of Fungi, RSC Publishing, Cambridge, UK.
2. Sanchez, J. F., Somoza, A. D., Keller, N. P., and Wang, C. C. C. (2012) Advances in Aspergillus secondary metabolite research in the post-genomic era Nat. Prod. Rep. 29, 351-371
3. van den Berg, M. A., Albang, R., Albermann, K., Badger, J. H., Daran, J.-M., Driessen, A. J. M., Garcia-Estrada, C., Fedorova, N. D., Harris, D. M., Heijne, W. H. M., Joardar, V., Kiel, J. A. K. W., Kovalchuk, A., Martin, J. F., Nierman, W. C., Nijland, J. G., Pronk, J. T., Roubos, J. A., van der Klei, I. J., van Peij, N. N. M. E., Veenhuis, M., von Dohren, H., Wagner, C., Wortman, J., and Bovenberg, R. A. L. (2008) Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum Nat. Biotechnol. 26, 1161-1168
4. Hoffmeister, D. and Keller, N. P. (2007) Natural products of filamentous fungi: Enzymes, genes, and their regulation Nat. Prod. Rep. 24, 393-416
5. Lawen, A. and Zocher, R. (1990) Cyclosporin synthetase. The most complex peptide synthesizing multienzyme polypeptide so far described J. Biol. Chem. 265, 11355-11360
6. Dittmann, J., Wenger, R. M., Kleinkauf, H., and Lawen, A. (1994) Mechanism of cyclosporin A biosynthesis. Evidence for synthesis via a single linear undecapeptide precursor J. Biol. Chem. 269, 2841-2846
7. Byford, M. F., Baldwin, J. E., Shiau, C.-Y., and Schofield, C. J. (1997) The mechanism of ACV synthetase Chem. Rev. 97, 2631-2650
8. Weber, G. and Leitner, E. (1994) Disruption of the cyclosporin synthetase gene of Tolypocladium niveum Curr. Genet. 26, 461-467
9. Cacho, R. A., Jiang, W., Chooi, Y.-H., Walsh, C. T., and Tang, Y. (2012) Identification and characterization of the Echinocandin B biosynthetic gene cluster from Emericella rugulosa NRRL 11440 J. Am. Chem. Soc. 134, 16781-16790
10. Chen, S. C. A., Slavin, M. A., and Sorrell, T. C. (2011) Echinocandin antifungal drugs in fungal infections: A comparison Drugs 71, 11-41
11. Gardiner, D. M. and Howlett, B. J. (2005) Bioinformatic and expression analysis of the putative gliotoxin biosynthetic gene cluster of Aspergillus fumigatus FEMS Microbiol. Lett. 248, 241-248
12. Maiya, S., Grundmann, A., Li, S.-M., and Turner, G. (2006) The fumitremorgin gene cluster of Aspergillus fumigatus: Identification of a gene encoding brevianamide F synthetase Chembiochem 7, 1062-1069
13. Grundmann, A. and Li, S.-M. (2005) Overproduction, purification and characterization of FtmPT1, a brevianamide F prenyltransferase from Aspergillus fumigatus Microbiology 151, 2199-2207
14. Hayashi, H., Takiuchi, K., Murao, S., and Arai, M. (1989) Structure and insecticidal activity of new indole alkaloids, okaramines A and B, from Penicillium simplicissimum, Agr Biol. Chem. 53, 461-469
15. Walsh, C. T., Haynes, S. W., and Ames, B. D. (2012) Aminobenzoates as building blocks for natural product assembly lines Nat. Prod. Rep. 29, 37-59
16. McMurry, J. and Begley, T. (1995) The Organic Chemistry of Biological Pathways, Roberts & Company, Greenwood Village, CO.
17. Dunn, M. F., Niks, D., Ngo, H., Barends, T. R. M., and Schlichting, I. (2008) Tryptophan synthase: The workings of a channeling nanomachine Trends Biochem. Sci. 33, 254-264
18. Wintermeyer, W. and Rodnina, M. V. (2002) Biopolymers. Polyamides and Complex Proteinaceous Materials I; Ribosomal Protein Synthesis, Vol. 7, Wiley-VCH, Weinheim; Cambridge.
19. Walsh, C. T., O'Brien, R. V., and Khosla, C. (in press) Nonproteinogenic amino acid building blocks for nonribosomal peptide and hybrid polyketide scaffolds, Angew. Chem.
20. Hijarrubia, M. J., Aparicio, J. F., Casqueiro, J., and Martin, J. F. (2001) Characterization of the lys2 gene of Acremonium chrysogenum encoding a functional α-aminoadipate activating and reducing enzyme Mol. Gen. Genet. 264, 755-762
21. Ames, B. D., Liu, X., and Walsh, C. T. (2010) Enzymatic processing of fumiquinazoline F: A tandem oxidative-acylation strategy for the generation of multicyclic scaffolds in fungal indole alkaloid biosynthesis Biochemistry 49, 8564-8576
22. Haynes, S. W., Ames, B. D., Gao, X., Tang, Y., and Walsh, C. T. (2011) Unraveling terminal C-domain-mediated condensation in fungal biosynthesis of imidazoindolone metabolites Biochemistry 50, 5668-5679
23. Guo, H. and Rao, N. (2007) Chorismate-mutase-catalyzed claisen rearrangement. In The Claisen Rearrangement, pp 1-23, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim.
24. Romero, R. M., Roberts, M. F., and Phillipson, J. D. (1995) Anthranilate synthase in microorganisms and plants Phytochemistry 39, 263-276
25. Hurley, L. H. (1980) Elucidation and formulation of novel biosynthetic pathways leading to the pyrrolo[1,4]benzodaizepine antibiotics anthramycin, tomaymycin, and sibiromycin Acc. Chem. Res. 13, 263-269
26. Li, W., Chou, S., Khullar, A., and Gerratana, B. (2009) Cloning and characterization of the biosynthetic gene cluster for tomaymycin, an SJG-136 monomeric analog Appl. Environ. Microbiol. 75, 2958-2963
27. Li, W., Khullar, A., Chou, S., Sacramo, A., and Gerratana, B. (2009) Biosynthesis of sibiromycin, a potent antitumor antibiotic Appl. Environ. Microbiol. 75, 2869-2878
28. Barry, C. E., Nayar, P. G., and Begley, T. P. (1989) Phenoxazinone synthase: Mechanism for the formation of the phenoxazinone chromophore of actinomycin Biochemistry 28, 6323-6333
29. Mavrodi, D. V., Blankenfeldt, W., and Thomashow, L. S. (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation Annu. Rev. Phytopathol. 44, 417-445
30. Kunze, B., Hofle, G., and Reichenbach, H. (1987) The aurachins, new quinoline antibiotics from myxobacteria: Production, physico-chemical, and biological properties J. Antibiot. 40, 258-265
31. Höfle, G. and Kunze, B. (2008) Biosynthesis of aurachins A-L in Stigmatella aurantiaca: A feeding study J. Nat. Prod. 71, 1843-1849
32. Hu, J. L., Xue, Y. C., Xie, M. Y., Zhang, R., Otani, T., Minami, Y., Yamada, Y., and Marunaka, T. (1988) A new macromolecular antitumor antibiotic, C-1027. I. Discovery, taxonomy of producing organism, fermentation, and biological activity J. Antibiot. 41, 1575-1579
33. Liu, W., Christenson, S. D., Standage, S., and Shen, B. (2002) Biosynthesis of the enediyne antitumor antibiotic C-1027 Science 297, 1170-1173
34. 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
35. Ames, B. D. and Walsh, C. T. (2010) Anthranilate-activating modules from fungal nonribosomal peptide assembly lines Biochemistry 49, 3351-3365
36. Fedorova, N. D., Khaldi, N., Joardar, V. S., Maiti, R., Amedeo, P., Anderson, M. J., Crabtree, J., Silva, J. C., Badger, J. H., Albarraq, A., Angiuoli, S., Bussey, H., Bowyer, P., Cotty, P. J., Dyer, P. S., Egan, A., Galens, K., Fraser-Liggett, C. M., Haas, B. J., Inman, J. M., Kent, R., Lemieux, S., Malavazi, I., Orvis, J., Roemer, T., Ronning, C. M., Sundaram, J. P., Sutton, G., Turner, G., Venter, J. C., White, O. R., Whitty, B. R., Youngman, P., Wolfe, K. H., Goldman, G. H., Wortman, J. R., Jiang, B., Denning, D. W., and Nierman, W. C. (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus PLoS Genet. 4 10.1371/journal.pgen.1000046
37. Yu, X., Liu, Y., Xie, X., Zheng, X.-D., and Li, S.-M. (2012) Biochemical characterization of indole prenyltransferases: filling the last gap of prenylation positions by a 5-dimethylallyltryptophan synthase from Aspergillus clavatus J. Biol. Chem. 287, 1371-1380
38. Zou, H.-X., Xie, X.-L., Linne, U., Zheng, X.-D., and Li, S.-M. (2010) Simultaneous C7- and N1-prenylation of cyclo-L-Trp-L-Trp catalyzed by a prenyltransferase from Aspergillus oryzae Org. Biomol. Chem. 8, 3037-3044
39. Wollinsky, B., Ludwig, L., Xie, X., and Li, S.-M. (2012) Breaking the regioselectivity of indole prenyltransferases: Identification of regular C3-prenylated hexahydropyrrolo[2,3-b]indoles as side products of the regular C2-prenyltransferase FtmPT1 Org. Biomol. Chem. 10, 9262-9270
40. Yin, W.-B., Grundmann, A., Cheng, J., and Li, S.-M. (2009) Acetylaszonalenin biosynthesis in Neosartorya fischeri. Identification of the biosynthetic gene cluster by genomic mining and functional proof of the genes by biochemical investigation J. Biol. Chem. 284, 100-109
41. Gao, X., Haynes, S. W., Ames, B. D., Wang, P., Vien, L. P., Walsh, C. T., and Tang, Y. (2012) Cyclization of fungal nonribosomal peptides by a terminal condensation-like domain Nat. Chem. Biol. 8, 823-830
42. Clugston, S. L., Sieber, S. A., Marahiel, M. A., and Walsh, C. T. (2003) Chirality of peptide bond-forming condensation domains in nonribosomal peptide synthetases: The C5 domain of tyrocidine synthetase is a (D)C(L) catalyst Biochemistry 42, 12095-12104
43. Nover, L. and Luckner, M. (1969) On the biosynthesis of cyclopenin and cyclopenol, benzodiazepine alkaloids from Penicillium cyclopium westling Eur. J. Biochem. 10, 268-273
44. Lerbs, W. and Luckner, M. (1985) Cyclopeptine synthetase activity in surface cultures of Penicillium cyclopium J. Basic Microbiol. 25, 387-391
45. Gerlach, M., Schwelle, N., Lerbs, W., and Luckner, M. (1985) Enzymatic synthesis of cyclopeptine intermediates in the Penicillium Cyclopium Phytochem. 24, 1935-1939
46. Aboutabl, E. A. and Luckner, M. (1975) Cyclopeptine dehydrogenase in Penicillium cyclopium Phytochem. 14, 2573-2577
47. Richter, I. and Luckner, M. (1976) Cyclopenin m-hydroxylase-An enzyme of alkaloid metabolism in Penicillium cyclopium Phytochem. 15, 67-70
48. Nover, L. and Luckner, M. (1969) Mixed functional oxygenations during the biosynthesis of cyclopenin and cyclopenol, benzodiazepine alkaloids of Penicillium cyclopium westling. Incorporation of molecular oxygen and NIH-shift FEBS Lett. 3, 292-296
49. Voigt, S. and Luckner, M. (1977) Dehydrocyclopeptine epoxidase from Penicillium cyclopium Phytochem. 16, 1651-1655
50. Smith, H. W. and Rapoport, H. (1969) Mechanism of the transformation of cyclopenin to viridicatin J. Am. Chem. Soc. 91, 6083-6089
51. Framm, J., Nover, L., Azzouny, A. E., Richter, H., Winter, K., Werner, S., and Luckner, M. (1973) Cyclopeptin und dehydrocyclopeptin Eur. J. Biochem. 37, 78-85
52. Luckner, M., Winter, K., and Reisch, J. (1969) Zur bildung von chinolinalkaloiden in pflanzen Eur. J. Biochem. 7, 380-384
53. White, J. D. and Dimsdale, M. J. (1969) The conversion of cyclopenin into viridicatin J. Chem. Soc., Chem. Commun. 1285b-1286
54. Gao, X., Chooi, Y.-H., Ames, B. D., Wang, P., Walsh, C. T., and Tang, Y. (2011) Fungal indole alkaloid biosynthesis: Genetic and biochemical investigation of the tryptoquialanine pathway in Penicillium aethiopicum J. Am. Chem. Soc. 133, 2729-2741
55. Haynes, S. W., Gao, X., Tang, Y., and Walsh, C. T. (2013) Complexity generation in fungal peptidyl alkaloid biosynthesis: a two-enzyme pathway to the hexacyclic MDR export pump inhibitor ardeemin ACS Chem. Biol. 10.1021/cb3006787
56. Haynes, S. W., Gao, X., Tang, Y., and Walsh, C. T. (2012) Assembly of asperlicin peptidyl alkaloids from anthranilate and tryptophan: A two-enzyme pathway generates heptacyclic scaffold complexity in asperlicin E J. Am. Chem. Soc. 134, 17444-17447
57. Numata, A., Takahashi, C., Matsushita, T., Miyamoto, T., Kawai, K., Usami, Y., Matsumura, E., Inoue, M., Ohishi, H., and Shingu, T. (1992) Fumiquinazolines, novel metabolites of a fungus isolated from a saltfish Tetrahedron Lett. 33, 1621-1624
58. Takahashi, C., Matsushita, T., Doi, M., Minoura, K., Shingu, T., Kumeda, Y., and Numata, A. (1995) Fumiquinazolines A-G, novel metabolites of a fungus separated from a Pseudolabrus marine fish J. Chem. Soc., Perkin Trans. 1 2345-2353
59. Ames, B. D., Haynes, S. W., Gao, X., Evans, B. S., Kelleher, N. L., Tang, Y., and Walsh, C. T. (2011) Complexity generation in fungal peptidyl alkaloid biosynthesis: Oxidation of fumiquinazoline A to the heptacyclic hemiaminal fumiquinazoline C by the flavoenzyme Af12070 from Aspergillus fumigatus Biochemistry 50, 8756-8769
60. Larsen, T. O., Frydenvang, K., Frisvad, J. C., and Christophersen, C. (1998) UV-Guided isolation of alantrypinone, a novel Penicillium alkaloid J. Nat. Prod. 61, 1154-1157
61. Romero Ariza, M., Larsen, T. O., Petersen, B. O., Duus, J. O., Christophersen, C., and Barrero, A. F. (2001) A novel alkaloid serantrypinone and the spiro azaphilone daldinin D from Penicillium thymicola J. Nat. Prod. 64, 1590-1592
62. Fremlin, L. J., Piggott, A. M., Lacey, E., and Capon, R. J. (2009) Cottoquinazoline A and cotteslosins A and B, metabolites from an Australian marine-derived strain of Aspergillus versicolor J. Nat. Prod. 72, 666-670
63. Larsen, T. O., Petersen, B. O., and Duus, J. O. (2001) Lumpidin, a novel biomarker of some ochratoxin a producing Penicillia J. Agric. Food. Chem. 49, 5081-5084
64. Wong, S. M., Musza, L. L., Kydd, G. C., Kullnig, R., Gillum, A. M., and Cooper, R. (1993) Fiscalins: New substance P inhibitors produced by the fungus Neosartorya fischeri. Taxonomy, fermentation, structures, and biological properties J. Antibiot. (Tokyo) 46, 545-553
65. Karwowski, J. P., Jackson, M., Rasmussen, R. R., Humphrey, P. E., Poddig, J. B., Kohl, W. L., Scherr, M. H., Kadam, S., and McAlpine, J. B. (1993) 5-N-acetylardeemin, a novel heterocyclic compound which reverses multiple drug resistance in tumor cells. I. Taxonomy and fermentation of the producing organism and biological activity J. Antibiot. (Tokyo) 46, 374-379
66. Hochlowski, J. E., Mullally, M. M., Spanton, S. G., Whittern, D. N., Hill, P., and McAlpine, J. B. (1993) 5-N-acetylardeemin, a novel heterocyclic compound which reverses multiple drug resistance in tumor cells. II. Isolation and elucidation of the structure of 5-N-acetylardeemin and two congeners J. Antibiot. (Tokyo) 46, 380-386
67. Chou, T. C., Depew, K. M., Zheng, Y. H., Safer, M. L., Chan, D., Helfrich, B., Zatorska, D., Zatorski, A., Bornmann, W., and Danishefsky, S. J. (1998) Reversal of anticancer multidrug resistance by the ardeemins Proc. Natl. Acad. Sci. U.S.A. 95, 8369-8374
68. Buttachon, S., Chandrapatya, A., Manoch, L., Silva, A., Gales, L., Bruyère, C., Kiss, R., and Kijjoa, A. (2012) Sartorymensin, a new indole alkaloid, and new analogues of tryptoquivaline and fiscalins produced by Neosartorya siamensis (KUFC 6349) Tetrahedron 68, 3253-3262
69. Larsen, T. O., Franzyk, H., and Jensen, S. R. (1999) UV-Guided isolation of verrucines A and B, novel quinazolines from Penicillium verrucosum structurally related to anacine from Penicillium aurantiogriseum J. Nat. Prod. 62, 1578-1580
70. Jiao, R. H., Xu, S., Liu, J. Y., Ge, H. M., Ding, H., Xu, C., Zhu, H. L., and Tan, R. X. (2006) Chaetominine, a cytotoxic alkaloid produced by endophytic Chaetomium sp. IFB-E015 Org. Lett. 8, 5709-5712
71. Chang, R. S., Lotti, V. J., Monaghan, R. L., Birnbaum, J., Stapley, E. O., Goetz, M. A., Albers-Schonberg, G., Patchett, A. A., Liesch, J. M., and Hensens, O. D. (1985) A potent nonpeptide cholecystokinin antagonist selective for peripheral tissues isolated from Aspergillus alliaceus Science 230, 177-179
72. Goetz, M. A., Monaghan, R. L., Chang, R. S., Ondeyka, J., Chen, T. B., and Lotti, V. J. (1988) Novel cholecystokinin antagonists from Aspergillus alliaceus. I. Fermentation, isolation, and biological properties J. Antibiot. (Tokyo) 41, 875-877
73. Liesch, J. M., Hensens, O. D., Zink, D. L., and Goetz, M. A. (1988) Novel cholecystokinin antagonists from Aspergillus alliaceus II. Structure determination of asperlicins B, C, D, and E J. Antibiot. (Tokyo) 41, 878-881
74. Rahbaek, L., Breinholt, J., Frisvad, J. C., and Christophersen, C. (1999) Circumdatin A, B, and C: Three new benzodiazepine alkaloids isolated from a culture of the fungus Aspergillus ochraceus J. Org. Chem. 64, 1689-1692
75. Rahbaek, L. and Breinholt, J. (1999) Circumdatins D, E, and F: Further fungal benzodiazepine analogues from Aspergillus ochraceus J. Nat. Prod. 62, 904-905
76. Dai, J., Carte, B. K., Sidebottom, P. J., Sek Yew, A. L., Ng, S., Huang, Y., and Butler, M. S. (2001) Circumdatin G, a new alkaloid from the fungus Aspergillus ochraceus J. Nat. Prod. 64, 125-126
77. Lopez-Gresa, M. P., Gonzalez, M. C., Primo, J., Moya, P., Romero, V., and Estornell, E. (2005) Circumdatin H, a new inhibitor of mitochondrial NADH oxidase, from Aspergillus ochraceus J. Antibiot. (Tokyo) 58, 416-419
78. Zhang, D., Yang, X., Kang, J. S., Choi, H. D., and Son, B. W. (2008) Circumdatin I, a new ultraviolet-A protecting benzodiazepine alkaloid from a marine isolate of the fungus Exophiala J. Antibiot. (Tokyo) 61, 40-42
79. Ookura, R., Kito, K., Ooi, T., Namikoshi, M., and Kusumi, T. (2008) Structure revision of circumdatins A and B, benzodiazepine alkaloids produced by marine fungus Aspergillus ostianus, by X-ray crystallography J. Org. Chem. 73, 4245-4247
80. Sun, H. H., Barrow, C. J., Sedlock, D. M., Gillum, A. M., and Cooper, R. (1994) Benzomalvins, new substance P inhibitors from a Penicillium sp J. Antibiot. (Tokyo) 47, 515-522
81. Joshi, B. K., Gloer, J. B., Wicklow, D. T., and Dowd, P. F. (1999) Sclerotigenin: A new antiinsectan benzodiazepine from the sclerotia of Penicillium sclerotigenum J. Nat. Prod. 62, 650-652
82. Yeulet, S. E., Mantle, P. G., Bilton, J. N., Rzepa, H. S., and Sheppard, R. N. (1986) Auranthine, a new benzodiazepinone metabolite of Penicillium aurantiogriseum J. Chem. Soc., Perkin Trans. 1 1891-1894