Abstract
Chemical epigenetic manipulation was applied to the zoanthid-derived fungus Cochliobolus lunatus (TA26-46) with a histone deacetylation modifier (100 µmol L−1 nicotinamide), resulting in the isolation of a new 14-membered resorcylic acid lactone named 7′(Z)-zeaenol (1), together with six known analogues (2–7) from the treated broth. The planar structure of 1 was determined by comprehensive NMR spectroscopy and HRESIMS data. The absolute configuration of 1 was elucidated by ECD spectrum, 13C NMR shift calculations, and on the basis of biogenetic considerations. Compound 5 exhibited cytotoxic activity against the human tumor cell lines A549, HCT-116, HT-29, Hela, MCF-7, and K562 with the IC50 values ranging from 2.54 to 7.44 µmol L−1.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Appendino, G., Gibbons, S., Giana, A., Pagani, A., Grassi, G., Stavri, M., et al., 2008. Antibacterial cannabinoids from Cannabis sativa: A structure-activity study. Journal of Natural Products, 71(8): 1427–1430, DOI: https://doi.org/10.1021/np8002673.
Ayers, S., Graf, T. N., Adcock, A. F., Kroll, D. J., Matthew, S., Carcache de Blanco, E. J., et al., 2011. Resorcylic acid lactones with cytotoxic and NF-κB inhibitory activities and their structure-activity relationships. Journal of Natural Products, 74(5): 1126–1131, DOI: https://doi.org/10.1021/np200062x.
Bajwa, N., and Jennings, M. P., 2008. Syntheses of epi-aigialomycin D and deoxy-aigialomycin C via a diastereoselective ring closing metathesis macrocyclization protocol. Tetrahedron Letters, 49(2): 390–393, DOI: https://doi.org/10.1016/j.tetlet.2007.11.038.
Bharatiya, P., Rathod, P., Hiray, A., and Kate, A. S., 2021. Multifarious elicitors: Invoking biosynthesis of various bioactive secondary metabolite in fungi. Applied Biochemistry and Biotechnology, 193(3): 668–686, DOI: https://doi.org/10.3390/md20050302.
Bujaranipalli, S., and Das, S., 2016. First stereoselective total synthesis of paecilomycin G. Tetrahedron Letters, 57(25): 2800–2802, DOI: https://doi.org/10.1016/j.tetlet.2016.05.046.
Cao, F., Meng, Z. H., Mu, X., Yue, Y. F., and Zhu, H. J., 2019a. Absolute configuration of bioactive azaphilones from the marine-derived fungus Pleosporales sp. CF09–1. Journal of Natural Products, 82(2): 386–392, DOI: https://doi.org/10.1021/acs.jnatprod.8b01030.
Cao, F., Sun, T. T., Yang, J. K., Zhao, G. Z., Liu, Q. A., Hu, L. D., et al., 2019b. The absolute configuration of anti-Vibrio citrinin dimeric derivative by VCD, ECD and NMR methods. Natural Product Reports, 33(15): 2192–2199, DOI: https://doi.org/10.1080/14786419.2018.1493590.
Carroll, A. R., Copp, B. R., Davis, R. A., Keyzers, R. A., and Prinsep, M. R., 2019. Marine natural products. Natural Product Reports, 36(21): 122–173, DOI: https://doi.org/10.1039/C9NP00069K.
Chen, M., Zhang, W., Shao, C. L., Chi, Z. M., and Wang, C. Y., 2016. DNA methyltransferase inhibitor induced fungal biosynthetic products: Diethylene glycol phthalate ester oligomers from the marine-derived fungus Cochliobolus lunatus. Marine Biotechnology, 18(3): 409–417, DOI: https://doi.org/10.1007/s10126-016-9703-y.
Eisentraeger, A., Dott, W., Klein, J., and Hahn, S., 2003. Comparative studies on algal toxicity testing using fluorometric microplate and Erlenmeyer flask growth-inhibition assays. Ecotoxicology and Environmental Safety, 54(3): 346–354, DOI: https://doi.org/10.1016/S0147-6513(02)00099-4.
Ellestad, G. A., Lovell, F. M., Perkinson, N. A., Hargreaves, R. T., and McGahren, W. J., 1978. New zearalenone related macrolides and isocoumarins from an unidentified fungus. Journal of Organic Chemistry, 43(12): 2339–2343, DOI: https://doi.org/10.1021/jo00406a007.
Grimblat, N. S., Zanardi, M. M., and Sarotti, A. M., 2015. Beyond DP4: An improved probability for the stereochemical assignment of isomeric compounds using quantum chemical calculations of NMR shifts. Journal of Organic Chemistry, 80(24): 12526–12534, DOI: https://doi.org/10.1021/acs.joc.5b02396.
Guo, D. L., Qiu, L., Feng, D., He, X., Li, X. H., Cao, Z. X., et al., 2020. Three new ɑ-pyrone derivatives induced by chemical epigenetic manipulation of Penicillium herquei, an endophytic fungus isolated from Cordyceps sinensis. Natural Product Research, 34(7): 958–964, DOI: https://doi.org/10.1080/14786419.2018.1544974.
Hafez Ghoran, S., Taktaz, F., Ayatollahi, S. A., and Kijjoa, A., 2022. Anthraquinones and their analogues from marine-derived fungi: Chemistry and biological activities. Marine Drugs, 20(8): 1660–3397, DOI: https://doi.org/10.1007/s12010-020-03423-6.
Lai, D., Mao, Z., Dan, X., Zhang, X., and Yang, L., 2016. Hyalodendriellins A-F, new 14-membered resorcylic acid lactones from the endophytic fungus Hyalodendriella sp. Ponipodef12. RSC Advances, 6(110): 108989–109000, DOI: https://doi.org/10.1039/C6RA24009G.
Liu, Q. A., Shao, C. L., Gu, Y. C., Blum, M., Gan, L. S., Wang, K. L., et al., 2014. Antifouling and fungicidal resorcylic acid lactones from the sea anemone-derived fungus Cochliobolus lunatus. Journal of Agricultural and Food Chemistry, 62(14): 3183–3191, DOI: https://doi.org/10.1021/jf500248z.
Nagabhishek, S. N., and Madankumar, A., 2019. A novel apoptosis-inducing metabolite isolated from marine sponge symbiont Monascus sp. NMK7 attenuates cell proliferation, migration and ROS stress-mediated apoptosis in breast cancer cells. RSC Advances, 9(11): 5878–5890, DOI: https://doi.org/10.1039/C8RA09886G.
Repetto, G., Del Peso, A., and Zurita, J. L., 2008. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nature Protocols, 3(7): 1125–1131, DOI: https://doi.org/10.1038/nprot.2008.75.
Shao, C. L., Wu, H. X., Wang, C. Y., Liu, Q. A., Xu, Y., Wei, M. Y., et al., 2011. Potent antifouling resorcylic acid lactones from the gorgonian-derived fungus Cochliobolus lunatus. Journal of Natural Products, 74(4): 629–633, DOI: https://doi.org/10.1021/np100641b.
Skehan, P., Storeng, R., Scudiero, D., Monks, A., McMahon, J., Vistica, D., et al., 1990. New colorimetric cytotoxicity assay for anticancer-drug screening. Journal of the National Cancer Institute, 82(13): 1107–1112, DOI: https://doi.org/10.1093/jnci/82.13.1107.
Sugawara, F., Kim, K. W., Kobayashi, K., Uzawa, J., Yoshida, S., Murofushi, N., et al., 1992. Zearalenone derivatives produced by the fungus Drechslera portulacae. Phytochemistry, 31(6): 1987–1990, DOI: https://doi.org/10.1016/0031-9422(92)80346-G.
Tomm, H. A., Ucciferri, L., and Ross, A. C., 2019. Advances in microbial culturing conditions to activate silent biosynthetic gene clusters for novel metabolite production. Journal of Industrial Microbiology & Biotechnology, 46: 1381–1400, DOI: https://doi.org/10.1007/s10295-019-02198-y.
Wu, J. S., Shi, X. H., Zhang, Y. H., Yu, J. Y., Fu, X. M., Li, X., et al., 2019. Co-cultivation with 5-azacytidine induced new metabolites from the zoanthid-derived fungus Cochliobolus lunatus. Frontiers in Chemistry, 7: 763, DOI: https://doi.org/10.3389/fchem.2019.00763.
Xu, F., Wu, Y., Zhang, C., Davis, K. M., Moon, K., Bushin, L. B., et al., 2019. A genetics-free method for high-throughput discovery of cryptic microbial metabolites. Nature Chemical Biology, 15(2): 161, DOI: https://doi.org/10.1038/s41589-018-0193-2.
Xu, W. F., Wu, N. N., Wu, Y. W., Qi, Y. X., Wei, M. Y., Pineda, L. M., et al., 2022. Structure modification, antialgal, antiplasmodial, and toxic evaluations of a series of new marine-derived 14-membered resorcylic acid lactone derivatives. Marine Life Science & Technology, 4: 88–97, DOI: https://doi.org/10.1007/s42995-021-00103-0.
Xu, W. F., Xue, X. J., Qi, Y. X., Wu, N. N., Wang, C. Y., and Shao, C. L., 2021. Cochliomycin G, a 14-membered resorcylic acid lactone from a marine-derived fungus Cochliobolus lunatus. Natural Product Research, 35(3): 490–493, DOI: https://doi.org/10.1080/14786419.2019.1633646.
Zarins-Tutt, J. S., Barberi, T. T., Gao, H., Mearns-Spragg, A., Zhang, L., Newman, D. J., et al., 2016. Prospecting for new bacterial metabolites: A glossary of approaches for inducing, activating and upregulating the biosynthesis of bacterial cryptic or silent natural products. Natural Product Research, 33(1): 54–72, DOI: https://doi.org/10.1039/c5np00111k.
Zhang, R., Wang, H., Chen, B., Dai, H., Sun, J., Han, J., et al., 2022. Discovery of anti-MRSA secondary metabolites from a marine-derived fungus Aspergillus fumigatus. Marine Drugs, 20(5): 1660–3397, DOI: https://doi.org/10.3390/md20050302.
Zhang, W., Shao, C. L., Chen, M., Liu, Q. A., and Wang, C. Y., 2014. Brominated resorcylic acid lactones from the marine-derived fungus Cochliobolus lunatus induced by histone de-acetylase inhibitors. Tetrahedron Letters, 55(35): 4888–4891, DOI: https://doi.org/10.1016/j.tetlet.2014.06.096.
Zhang, X. Q., Spadafora, C., Pineda, L. M., Ng, M. G., Sun, J. H., Wang, W., et al., 2017. Discovery, semisynthesis, antiparasitic and cytotoxic evaluation of 14-membered resorcylic acid lactones and their derivatives. Scientific Reports, 7(1): 11822, DOI: https://doi.org/10.1038/s41598-017-12336-0.
Zhao, M., Yuan, L. Y., Guo, D. L., Ye, Y., DaWa, Z. M., Wang, X. L., et al., 2018. Bioactive halogenated dihydroisocoumarins produced by the endophytic fungus Lachnum palmae isolated from Przewalskia tangutica. Phytochemistry, 148: 97–103. DOI: https://doi.org/10.1016/j.phytochem.2018.01.018.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Nos. 81673350, 81703411, 417 76156), the National Science and Technology Major Project for Significant New Drugs Development, China (No. 2018ZX09735-004), the Fundamental Research Funds for the Central Universities of China (No. 201962002), and the Taishan Scholars Program, China.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Zhang, Z., Wang, J., Cao, F. et al. Histone Deacetylation Modifier Induced One New Resorcylic Acid Lactone 7′(Z)-zeaenol from the Zoanthid-Derived Fungus Cochliobolus lunatus. J. Ocean Univ. China 22, 198–204 (2023). https://doi.org/10.1007/s11802-020-4489-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-020-4489-y