Secondary metabolites from the marine-derived fungus Penicillium chrysogenum Y20-2, and their pro-angiogenic activity
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Yue-Zi Qiu
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Ke-Chun Liu
Abstract
A systematic chemical study of the secondary metabolites of the marine fungus, Penicillium chrysogenum (No. Y20-2), led to the isolation of 21 compounds, one of which is new (compound 3). The structures of the 21 compounds were determined by conducting extensive analysis of the spectroscopic data. The pro-angiogenic activity of each compound was evaluated using a zebrafish model. The results showed that compounds 7, 9, 16, and 17 had strong and dose-dependent pro-angiogenic effects, with compound 16 demonstrating the strongest pro-angiogenic activity, compounds 6, 12, 14, and 18 showing moderate activity, and compounds 8, 13, and 19 exhibiting relatively weak activity.
Funding source: The Project was Supported by the Foundation of Qilu University of Technology of Cultivating Subject for Biology and Biochemistry
Award Identifier / Grant number: No. ESIBBC202005
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Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: The Project was Supported by the Foundation (No. ESIBBC202005) of Qilu University of Technology of Cultivating Subject for Biology and Biochemistry.
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Conflict of interest statement: Authors declare no conflict of interest.
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Ethics Statement: The animal study was reviewed and approved by the Biology Institute, Qilu University of Technology of Animal Ethics Committee.
References
1. Altmann, KH. Drugs from the Oceans: marine natural products as leads for drug discovery. Chimia 2017;71:646–52. https://doi.org/10.2533/chimia.2017.646.Search in Google Scholar PubMed
2. Ameen, F, AlNadhari, S, Al-Homaidan, AA. Marine microorganisms as an untapped source of bioactive compounds. Saudi J Biol Sci 2021;28:224–31. https://doi.org/10.1016/j.sjbs.2020.09.052.Search in Google Scholar PubMed PubMed Central
3. Gulder, TA, Hong, H, Correa, J, Egereva, E, Wiese, J, Imhoff, JF, et al.. Isolation, structure elucidation and total synthesis of lajollamide A from the marine fungus Asteromyces cruciatus. Mar Drugs 2012;10:2912–35. https://doi.org/10.3390/md10122912.Search in Google Scholar PubMed PubMed Central
4. Yang, X, Liu, J, Mei, J, Jiang, R, Tu, S, Deng, H, et al.. Origins, structures, and bioactivities of secondary metabolites from marine-derived Penicillium fungi. Mini-Rev Med Chem 2021;21:2000–19. https://doi.org/10.2174/1389557521666210217093517.Search in Google Scholar PubMed
5. Li, P, Zhang, M, Li, H, Wang, R, Hou, H, Li, X, et al.. New prenylated indole homodimeric and pteridine alkaloids from the marine-derived fungus Aspergillus austroafricanus Y32-2. Mar Drugs 2021;19:98. https://doi.org/10.3390/md19020098.Search in Google Scholar PubMed PubMed Central
6. Fan, YQ, Li, PH, Chao, YX, Chen, H, Du, N, He, QX, et al.. Alkaloids with cardiovascular effects from the marine-derived fungus Penicillium expansum Y32. Mar Drugs 2015;13:6489–504. https://doi.org/10.3390/md13106489.Search in Google Scholar PubMed PubMed Central
7. Sitrin, RD, Chan, G, Dingerdissen, J, DeBrosse, C, Mehta, R, Roberts, G, et al.. Isolation and structure determination of Pachybasium cerebrosides which potentiate the antifungal activity of aculeacin. J Antibiot 1988;41:469–80. https://doi.org/10.7164/antibiotics.41.469.Search in Google Scholar PubMed
8. Yaoita, Y, Kohata, R, Kakuda, R, Machida, K, Kikuchi, M. Ceramide constituents from five mushrooms. Chem Pharm Bull 2002;50:681–4. https://doi.org/10.1248/cpb.50.681.Search in Google Scholar PubMed
9. Chen, YP, Wang, SL, Shen, YH, WU, Z-J. Chemical constituents from Ainsliaea glabra. Guihaia 2014;34:402–7.Search in Google Scholar
10. Liang, S, Chen, HS, Wang, HP, Jin, L, Qiao, LM, Jia, LU. Study on chemical constituents of Tabernaemontana divaricata (Ⅱ). Acad J Second Mil Med Univ 2007;28:425–6.Search in Google Scholar
11. Deng, S, Tian, C, Xiao, D. Studies on the chemical constituents of the sponge Riemna fortis from the south China sea. Chin J Mar Drugs 1999;3:4–6.Search in Google Scholar
12. Jian-ying, B, Zhi-bin, Z, Yi-wen, X, Ya, W, Ri-ming, Y, Du, Z. Antibacterial and antifungal secondary metabolites produced by endophytic actinomycete Streptomyces sp. PRh5 from Dongxiang wild rice. Nat Prod Res Dev 2018;30:1933–8, 2008.Search in Google Scholar
13. El-Amrani, M, Ebada, SS, Gad, HA, Proksch, P. Pestalotiopamide E and pestalotiopin B from an endophytic fungus Aureobasidium pullulans isolated from Aloe vera leaves. Phytochem Lett 2016;18:95–8. https://doi.org/10.1016/j.phytol.2016.09.006.Search in Google Scholar
14. Hahn, S, Stoilov, IL, Ha, TT, Raederstorff, D, Doss, GA, Li, HT, et al.. Biosynthetic studies of marine lipids. 17.1 the course of chain elongation and desaturation in long-chain fatty acids of marine sponges. J Am Chem Soc 1988;110:8117–24. https://doi.org/10.1021/ja00232a025.Search in Google Scholar
15. Searle, PA, Molinski, TF. Structure and absolute configuration of (R)-(E)-1-aminotridec-5-en-2-ol, an antifungal amino alcohol from the ascidian Didemnum sp. J Org Chem 1993;58:7578–80. https://doi.org/10.1021/jo00078a045.Search in Google Scholar
16. Zhao, CN, Yao, ZL, Yang, D, Ke, J, Wu, QL, Li, JK, et al.. Chemical constituents from Fraxinus hupehensis and their antifungal and herbicidal activities. Biomolecules 2020;10:74. https://doi.org/10.3390/biom10010074.Search in Google Scholar PubMed PubMed Central
17. Amagata, T, Usami, Y, Minoura, K, Ito, T, Numata, A. Cytotoxic substances produced by a fungal strain from a sponge: physico-chemical properties and structures. J Antibiot 1998;51:33–40. https://doi.org/10.7164/antibiotics.51.33.Search in Google Scholar PubMed
18. Hyun, KK, June, SY, Un, CS, Ro, LK. New cytotoxic δ-valerolactones from Cornus walteri. Bull Kor Chem Soc 2011;32:2443–5. https://doi.org/10.5012/bkcs.2011.32.7.2443.Search in Google Scholar
19. Göhrt, A, Zeeck, A, Hütter, K, Kirsch, R, Kluge, H, Thiericke, R. Secondary metabolites by chemical screening. 9 decarestrictines, a new family of inhibitors of cholesterol biosynthesis from Penicillium II. structure elucidation of the decarestrictines A to D. J Antibiot 1992;45:66–73. https://doi.org/10.7164/antibiotics.45.66.Search in Google Scholar PubMed
20. Pusecker, K, Laatsch, H, Helmke, E, Weyland, H. Dihydrophencomycin methyl ester, a new phenazine derivative from a marine Streptomycete. J Antibiot 1997;50:479–83. https://doi.org/10.7164/antibiotics.50.479.Search in Google Scholar PubMed
21. Ying, Y-M, Zhan, Z-J, Ding, Z-S, Shan, W-G. Bioactive metabolites from Penicillium sp. P-1, a fungal endophyte in Huperzia serrata. Chem Nat Compd 2011;47:541–4. https://doi.org/10.1007/s10600-011-9991-4.Search in Google Scholar
22. Nishikawa, Y, Nakamura, H, Ukai, N, Adachi, W, Hara, O. Tetraethylorthosilicate as a mild dehydrating reagent for the synthesis of N-formamides with formic acid. Tetrahedron Lett 2017;58:860–3. https://doi.org/10.1016/j.tetlet.2017.01.056.Search in Google Scholar
23. Davis, RA. Isolation and structure elucidation of the new fungal metabolite (-)-xylariamide A. J Nat Prod 2005;68:769–72. https://doi.org/10.1021/np050025h.Search in Google Scholar PubMed
24. Kawai, K, Nozawa, K, Nakajima, S, Iitaka, Y. Studies on fungal products. VII.1) the structures of meleagrin and 9-O-p-Bromobenzoylmeleagrin. Chem Pharm Bull 1984;32:94–8. https://doi.org/10.1248/cpb.32.94.Search in Google Scholar
25. Nozawa, K, Nakajima, S. Isolation of radicicol from Penicillium luteo-aurantium, and meleagrin, a new metabolite from Penicillium meleagrinum. J Nat Prod 1979;42:374–7. https://doi.org/10.1021/np50004a004.Search in Google Scholar
26. Overy, DP, Phipps, RK, Frydenvang, K, Larsen, TO. epi-Neoxaline, a chemotaxonomic marker for Penicillium tulipae. Biochem Syst Ecol 2006;34:345–8. https://doi.org/10.1016/j.bse.2005.10.010.Search in Google Scholar
27. Feng, Y, Han, JY, Zhang, Y, Xu, SU, Frank, E, Stephanie, G. Study on the alkaloids from two great white shark’s gill-derived Penicillium strains and their bioactivity. Chin J Mar Drugs 2016;35:16–22.Search in Google Scholar
28. Niu, XM, Li, SH, Peng, LY, Lin, ZW, Rao, GX, Sun, HD. Constituents from Limonia crenulata. J Asian Nat Prod Res 2001;3:299–311. https://doi.org/10.1080/10286020108040370.Search in Google Scholar PubMed
29. Gong, J, Tang, H, Liu, BS, Zhou, W, Zhang, W. Steroids from fungus Engyodontium album associated with the south China sea cucumber Holothuria nobilis Selenka. Acad J Second Mil Med Univ 2013;33:310–4. https://doi.org/10.3724/sp.j.1008.2013.00310.Search in Google Scholar
30. Fei, W, Jikai, L. The chemical constituents of basidiomycete Calodon suaveolens. Nat Prod Res Dev 2004;16:204–6.Search in Google Scholar
31. Liu, TF, Hua, T, Ling, L, Wei, G, Wen, Z. 5α,8α-epidioxy sterol components in gorgonian Muriceopsis flavida collected from the South China Sea. Acad J Second Mil Med Univ 2011;31:469–72. https://doi.org/10.3724/sp.j.1008.2011.00469.Search in Google Scholar
32. Chebaane, K, Guyot, U. Occurrence of erythro-docosasphinga-4,8-dienine, as an ester, in anemonia sulcata. Tetrahedron Lett 1986;27:1495–6.10.1016/S0040-4039(00)84294-XSearch in Google Scholar
33. Jackman, LM, Sternhell, S. Applications of nuclear magnetic resonance spectroscopy in organic chemistry. Ztschrift Für Physikalische Chemie; 1960;26:285–6. http://doi.org/10.1524/zpch.1960.26.3_4.285.10.1524/zpch.1960.26.3_4.285Search in Google Scholar
34. Bohlmann, F, Zeisberg, R, Klein, E. C-NMR-Spektren von monoterpenen. Org Magn Reson 1975;7:432–6.10.1002/mrc.1270070907Search in Google Scholar
35. Zhang, Y, Wang, S, Li, XM, Cui, CM, Feng, C, Wang, BG. New sphingolipids with a previously unreported 9-methyl-C20-sphingosine moiety from a marine algous endophytic fungus Aspergillus niger EN-13. Lipids 2007;42:759–64. https://doi.org/10.1007/s11745-007-3079-8.Search in Google Scholar PubMed
36. Barbazuk, WB, Korf, I, Kadavi, C, Heyen, J, Tate, S, Wun, E, et al.. The syntenic relationship of the zebrafish and human genomes. Genome Res 2000;10:1351–8. https://doi.org/10.1101/gr.144700.Search in Google Scholar PubMed PubMed Central
37. Yuan, X, Han, L, Fu, P, Zeng, H, Lv, C, Chang, W, et al.. Cinnamaldehyde accelerates wound healing by promoting angiogenesis via up-regulation of PI3K and MAPK signaling pathways. Lab Invest 2018;98:783–98. https://doi.org/10.1038/s41374-018-0025-8.Search in Google Scholar PubMed
38. Wang, Q, Tang, X, Liu, H, Luo, X, Sung, PJ, Li, P, et al.. New nardosinane and aristolane sesquiterpenoids with angiogenesis promoting activity from the marine soft coral Lemnalia sp. Mar Drugs 2020;18:171. https://doi.org/10.3390/md18030171.Search in Google Scholar PubMed PubMed Central
39. Feng, X, Li, Y, Wang, Y, Li, L, Little, PJ, Xu, SW, et al.. Danhong injection in cardiovascular and cerebrovascular diseases: pharmacological actions, molecular mechanisms, and therapeutic potential. Pharmacol Res 2019;139:62–75. https://doi.org/10.1016/j.phrs.2018.11.006.Search in Google Scholar PubMed
40. Li, Y, Liu, XJ, Wang, P, Gao, Y, Zhao, BN. Angiogenesis activity of Danhong injection in zebrafish. China J Tradit Chin Med Pharm 2016;31:2270–3.Search in Google Scholar
41. Tal, TL, McCollum, CW, Harris, PS, Olin, J, Kleinstreuer, N, Wood, CE, et al.. Immediate and long-term consequences of vascular toxicity during zebrafish development. Reprod Toxicol 2014;48:51–61. https://doi.org/10.1016/j.reprotox.2014.05.014.Search in Google Scholar PubMed
42. Raghunath, M, Sy Wong, Y, Farooq, M, Ge, R. Pharmacologically induced angiogenesis in transgenic zebrafish. Biochem Biophys Res Commun 2009;378:766–71. https://doi.org/10.1016/j.bbrc.2008.11.127.Search in Google Scholar PubMed
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Articles in the same Issue
- Frontmatter
- Research Article
- SOCSs: important regulators of host cell susceptibility or resistance to viral infection
- Review Article
- Essential oils of the ginger plants Meistera caudata and Conamomum vietnamense: chemical compositions, antimicrobial, and mosquito larvicidal activities
- Research Articles
- Secondary metabolites from the marine-derived fungus Penicillium chrysogenum Y20-2, and their pro-angiogenic activity
- Identification of tuliposides K–M in tulip bulbs via an enzyme reaction-based screening method using a tuliposide-converting enzyme
- Anti-SARS-CoV-2 in vitro potential of castor oil plant (Ricinus communis) leaf extract: in-silico virtual evidence
- GABase and glutaminase inhibitory activities of herbal extracts and acylated flavonol monoglycosides isolated from the leaves of Laurus nobilis L.
