Large-Scale Metabolomics Reveals a Complex Response of Aspergillus nidulans to Epigenetic Perturbation

ACS Chemical Biology

Volumn 10, Issue 6, 2015, Pages 1535-1541

  Albright, Jessica C ^a   Henke, Matthew T ^a   Soukup, Alexandra A ^c   McClure, Ryan A ^a   Thomson, Regan J ^a   Keller, Nancy P ^c   Kelleher, Neil L ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE; DRUG METABOLITE; FELLUTAMIDE DERIVATIVE; HISTONE DEACETYLASE; LIPOPEPTIDE; PROTEASOME; PROTEASOME INHIBITOR; STERIGMATOCYSTIN; UNCLASSIFIED DRUG; VORINOSTAT; FELLUTAMIDE B; FUNGAL PROTEIN; HISTONE DEACETYLASE INHIBITOR; SMALL INTERFERING RNA;

ARTICLE; ASPERGILLUS NIDULANS; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; DOWN REGULATION; DRUG ISOLATION; ENZYME ACTIVITY; ENZYME REPRESSION; EPIGENETICS; FUNGAL GENETICS; FUNGAL STRAIN; FUNGUS GROWTH; METABOLOME; METABOLOMICS; NONHUMAN; PENICILLIUM CHRYSOGENUM; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; QUANTITATIVE STUDY; UPREGULATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHEMISTRY; DNA METHYLATION; DRUG EFFECTS; ENZYMOLOGY; GENETIC EPIGENESIS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MULTIGENE FAMILY;

EMERICELLA NIDULANS; FUNGI;

ASPERGILLUS NIDULANS; DNA METHYLATION; EPIGENESIS, GENETIC; FUNGAL PROTEINS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; LIPOPEPTIDES; METABOLOME; METABOLOMICS; MULTIGENE FAMILY; RNA, SMALL INTERFERING;

EID: 84935007874     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00025     Document Type: Article

References (41)

1. Paláez, F. In Handbook of Industrial Mycology; An, Z., Ed.; Marcel Dekker: New York, 2005; p 49-92.
2. Yaegashi, J., Oakley, B. R., and Wang, C. C. (2014) Recent advances in genome mining of secondary metabolite biosynthetic gene clusters and the development of heterologous expression systems in Aspergillus nidulans J. Ind. Microbiol. Biotechnol. 41, 433-442
3. Giles, S. S., Soukup, A. A., Lauer, C., Shaaban, M., Lin, A., Oakley, B. R., Wang, C. C., and Keller, N. P. (2011) Cryptic Aspergillus nidulans antimicrobials Appl. Environ. Microbiol. 77, 3669-3675
4. Lim, F. Y., Sanchez, J. F., Wang, C. C., and Keller, N. P. (2012) Toward awakening cryptic secondary metabolite gene clusters in filamentous fungi Methods Enzymol. 517, 303-324
5. Nutzmann, H. W., Fischer, J., Scherlach, K., Hertweck, C., and Brakhage, A. A. (2013) Distinct amino acids of histone H3 control secondary metabolism in Aspergillus nidulans Appl. Environ. Microbiol. 79, 6102-6109
6. Shwab, E. K., Bok, J. W., Tribus, M., Galehr, J., Graessle, S., and Keller, N. P. (2007) Histone deacetylase activity regulates chemical diversity in Aspergillus Eukaryot. Cell 6, 1656-1664
7. Trojer, P., Brandtner, E. M., Brosch, G., Loidl, P., Galehr, J., Linzmaier, R., Haas, H., Mair, K., Tribus, M., and Graessle, S. (2003) Histone deacetylases in fungi: novel members, new facts Nucleic Acids Res. 31, 3971-3981
8. Bayram, O., Krappmann, S., Ni, M., Bok, J. W., Helmstaedt, K., Valerius, O., Braus-Stromeyer, S., Kwon, N. J., Keller, N. P., Yu, J. H., and Braus, G. H. (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism Science 320, 1504-1506
9. Cichewicz, R. H. (2010) Epigenome manipulation as a pathway to new natural product scaffolds and their congeners Nat. Prod. Rep. 27, 11-22
10. Lee, I., Oh, J. H., Shwab, E. K., Dagenais, T. R., Andes, D., and Keller, N. P. (2009) HdaA, a class 2 histone deacetylase of Aspergillus fumigatus, affects germination and secondary metabolite production Fungal Genet. Biol. 46, 782-790
11. Lin, J. Q., Zhao, X. X., Zhi, Q. Q., Zhao, M., and He, Z. M. (2013) Transcriptomic profiling of Aspergillus flavus in response to 5-azacytidine Fungal Genet Biol. 56, 78-86
12. Fisch, K. M., Gillaspy, A. F., Gipson, M., Henrikson, J. C., Hoover, A. R., Jackson, L., Najar, F. Z., Wagele, H., and Cichewicz, R. H. (2009) Chemical induction of silent biosynthetic pathway transcription in Aspergillus niger J. Ind. Microbiol. Biotechnol. 36, 1199-1213
13. Sarkar, A., Funk, A. N., Scherlach, K., Horn, F., Schroeckh, V., Chankhamjon, P., Westermann, M., Roth, M., Brakhage, A. A., Hertweck, C., and Horn, U. (2012) Differential expression of silent polyketide biosynthesis gene clusters in chemostat cultures of Aspergillus nidulans J. Biotechnol. 160, 64-71
14. Bergmann, S., Funk, A. N., Scherlach, K., Schroeckh, V., Shelest, E., Horn, U., Hertweck, C., and Brakhage, A. A. (2010) Activation of a silent fungal polyketide biosynthesis pathway through regulatory cross talk with a cryptic nonribosomal peptide synthetase gene cluster Appl. Environ. Microbiol. 76, 8143-8149
15. Szilagyi, M., Miskei, M., Karanyi, Z., Lenkey, B., Pocsi, I., and Emri, T. (2013) Transcriptome changes initiated by carbon starvation in Aspergillus nidulans Microbiology 159, 176-190
16. Maggio-Hall, L. A., Hammond, T. M., and Keller, N. P. Aspergillus nidulans as a model system to study secondary metabolism. Secondary Metabolism in Model Systems; Elsevier Science: 2004; Vol. 38, pp 197-222.
17. Zutz, C., Gacek, A., Sulyok, M., Wagner, M., Strauss, J., and Rychli, K. (2013) Small chemical chromatin effectors alter secondary metabolite production in Aspergillus clavatus Toxins (Basel) 5, 1723-1741
18. Asai, T., Yamamoto, T., Shirata, N., Taniguchi, T., Monde, K., Fujii, I., Gomi, K., and Oshima, Y. (2013) Structurally diverse chaetophenol productions induced by chemically mediated epigenetic manipulation of fungal gene expression Org. Lett. 15, 3346-3349
19. Chung, Y. M., Wei, C. K., Chuang, D. W., El-Shazly, M., Hsieh, C. T., Asai, T., Oshima, Y., Hsieh, T. J., Hwang, T. L., Wu, Y. C., and Chang, F. R. (2013) An epigenetic modifier enhances the production of anti-diabetic and anti-inflammatory sesquiterpenoids from Aspergillus sydowii Bioorg. Med. Chem. 21, 3866-3872
20. Henrikson, J. C., Hoover, A. R., Joyner, P. M., and Cichewicz, R. H. (2009) A chemical epigenetics approach for engineering the in situ biosynthesis of a cryptic natural product from Aspergillus niger Org. Biomol Chem. 7, 435-438
21. Graessle, S., Dangl, M., Haas, H., Mair, K., Trojer, P., Brandtner, E.-M., Walton, J. D., Loidl, P., and Brosch, G. (2000) Characterization of two putative histone deacetylase genes from Aspergillus nidulans Biochim. Biophys. Acta, Gene Struct. Expression 1492, 120-126
22. Lin, G., Li, D., Chidawanyika, T., Nathan, C., and Li, H. (2010) Fellutamide B is a potent inhibitor of the Mycobacterium tuberculosis proteasome Arch. Biochem. Biophys. 501, 214-220
23. Hines, J., Groll, M., Fahnestock, M., and Crews, C. M. (2008) Proteasome Inhibition by Fellutamide B Induces Nerve Growth Factor Synthesis Chem. Biol. 15, 501-512
24. Tribus, M., Bauer, I., Galehr, J., Rieser, G., Trojer, P., Brosch, G., Loidl, P., Haas, H., and Graessle, S. (2010) A novel motif in fungal class 1 histone deacetylases is essential for growth and development of Aspergillus Mol. Biol. cell 21, 345-353
25. Hoffmann, T., Krug, D., Huttel, S., and Muller, R. (2014) Improving Natural Products Identification through Targeted LC-MS/MS in an Untargeted Secondary Metabolomics Workflow Anal. Chem. 86, 10780-10788
26. Klitgaard, A., Iversen, A., Andersen, M. R., Larsen, T. O., Frisvad, J. C., and Nielsen, K. F. (2014) Aggressive dereplication using UHPLC-DAD-QTOF: screening extracts for up to 3000 fungal secondary metabolites Anal. Bioanal. Chem. 406, 1933-1943
27. El-Elimat, T., Figueroa, M., Ehrmann, B. M., Cech, N. B., Pearce, C. J., and Oberlies, N. H. (2013) High-resolution MS, MS/MS, and UV database of fungal secondary metabolites as a dereplication protocol for bioactive natural products J. Nat. Prod. 76, 1709-1716
28. Nielsen, K. F., Mansson, M., Rank, C., Frisvad, J. C., and Larsen, T. O. (2011) Dereplication of microbial natural products by LC-DAD-TOFMS J. Nat. Prod. 74, 2338-2348
29. Laatsch, H. Antibase 2011; Wiley VCH: Weinheim, Germany, 2011.
30. Sanchez, J. F., Chiang, Y. M., Szewczyk, E., Davidson, A. D., Ahuja, M., Elizabeth Oakley, C., Woo Bok, J., Keller, N., Oakley, B. R., and Wang, C. C. (2010) Molecular genetic analysis of the orsellinic acid/F9775 gene cluster of Aspergillus nidulans Mol. Biosyst. 6, 587-593
31. Ahuja, M., Chiang, Y. M., Chang, S. L., Praseuth, M. B., Entwistle, R., Sanchez, J. F., Lo, H. C., Yeh, H. H., Oakley, B. R., and Wang, C. C. (2012) Illuminating the diversity of aromatic polyketide synthases in Aspergillus nidulans J. Am. Chem. Soc. 134, 8212-8221
32. Brown, D. W., Yu, J. H., Kelkar, H. S., Fernandes, M., Nesbitt, T. C., Keller, N. P., Adams, T. H., and Leonard, T. J. (1996) Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans Proc. Natl. Acad. Sci. U.S.A. 93, 1418-1422
33. Dezotti, N. O. and Zucchi, T. M. (2001) Identification of Aspergillus nidulans genes essential for the accumulation of sterigmatocystin Fungal Genet. Biol. 34, 93-105
34. Yu, J. H. and Leonard, T. J. (1995) Sterigmatocystin biosynthesis in Aspergillus nidulans requires a novel type I polyketide synthase J. Bacteriol. 177, 4792-4800
35. Giltrap, A. M., Cergol, K. M., Pang, A., Britton, W. J., and Payne, R. J. (2013) Total Synthesis of Fellutamide B and Deoxy-Fellutamides B, C, and D Marine Drugs 11, 2382-2397
36. Shigemori, H., Wakuri, S., Yazawa, K., Nakamura, T., Sasaki, T., and Kobayashi, J. i. (1991) Fellutamides A and B, cytotoxic peptides from a marine fish-possessing fungus Penicillium fellutanum Tetrahedron 47, 8529-8534
37. Lee, Y. M., Kim, M. J., Li, H., Zhang, P., Bao, B., Lee, K. J., and Jung, J. H. (2013) Marine-derived Aspergillus species as a source of bioactive secondary metabolites Marine Biotechnol. 15, 499-519
38. Running, W. E. (1993) Chapman and Hall Dictionary of Natural-Products on Cd-Rom J. Chem. Inf. Comput. Sci. 33, 934-935
39. Palmer, J. M., Mallaredy, S., Perry, D. W., Sanchez, J. F., Theisen, J. M., Szewczyk, E., Oakley, B. R., Wang, C. C., Keller, N. P., and Mirabito, P. M. (2010) Telomere position effect is regulated by heterochromatin-associated proteins and NkuA in Aspergillus nidulans Microbiology 156, 3522-3531
40. Andersen, M. R., Nielsen, J. B., Klitgaard, A., Petersen, L. M., Zachariasen, M., Hansen, T. J., Blicher, L. H., Gotfredsen, C. H., Larsen, T. O., Nielsen, K. F., and Mortensen, U. H. (2013) Accurate prediction of secondary metabolite gene clusters in filamentous fungi Proc. Natl. Acad. Sci. U.S.A 110, E99-107
41. Caboche, S., Pupin, M., Leclere, V., Fontaine, A., Jacques, P., and Kucherov, G. (2008) NORINE: a database of nonribosomal peptides Nucleic Acids Res. 36, D326-331