| ORIGINAL ARTICLES |
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New piperazine derivatives helvamides B-C from the marine-derived fungus Penicillium velutinum ZK-14 uncovered by OSMAC (One Strain Many Compounds) strategy |
| Gleb V. Borkunov1,2, Elena V. Leshchenko1,2, Dmitrii V. Berdyshev1, Roman S. Popov1, Ekaterina A. Chingizova1, Nadezhda P. Shlyk2, Andrey V. Gerasimenko3, Natalya N. Kirichuk1, Yuliya V. Khudyakova1, Viktoria E. Chausova1, Alexandr S. Antonov1, Anatoly I. Kalinovsky1, Artur R. Chingizov1, Ekaterina A. Yurchenko1, Marina P. Isaeva1, Anton N. Yurchenko1 |
1. G. B. Elyakov Pacific Institute of Bioorganic Chemistry, Far Eastern Branch of the Russian Academy of Sciences, 159 Prospect 100-Letiya Vladivostoka, Vladivostok 690022, Russian Federation;
2. Far Eastern Federal University, Vladivostok 690922, Russian Federation;
3. Institute of Chemistry, Far Eastern Branch of the Russian Academy of Sciences, 159 Prospect 100-Letiya Vladivostoka, Vladivostok 690022, Russian Federation |
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Abstract Four extracts of the marine-derived fungus Penicillium velutinum J.F.H. Beyma were obtained via metal ions stress conditions based on the OSMAC (One Strain Many Compounds) strategy. Using a combination of modern approaches such as LC/UV, LC/MS and bioactivity data analysis, as well as in silico calculations, influence metal stress factors to change metabolite profiles Penicillium velutinum were analyzed. From the ethyl acetate extract of the P. velutinum were isolated two new piperazine derivatives helvamides B (1) and C (2) together with known saroclazin A (3) (4S,5R,7S)-4,11-dihydroxy-guaia-1(2),9(10)-dien (4). Their structures were established based on spectroscopic methods. The absolute configuration of helvamide B (1) as 2R,5R was determined by a combination of the X-ray analysis and by time-dependent density functional theory (TD-DFT) calculations of electronic circular dichroism (ECD) spectra. The cytotoxic activity of the isolated compounds against human prostate cancer PC-3 and human embryonic kidney HEK-293 cells and growth inhibition activity against yeast-like fungi Candida albicans were assayed.
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| Keywords
Penicillium velutinum
OSMAC strategy
Metal ions stress
LC/MS
Metabolite profile
Bioassay
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| Fund:This research was funded by Russian Science Foundation, grant number № 22-73-00190, https://rscf.ru/en/project/22-73-00190/. |
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Corresponding Authors:
Elena V. Leshchenko,E-mail:leshchenko.ev@dvfu.ru
E-mail: leshchenko.ev@dvfu.ru
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Issue Date: 01 August 2024
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[1] Jin L, Quan C, Hou X. Potential pharmacological resources: natural bioactive compounds from marine-derived fungi. Mar Drugs. 2016;14:76.
[2] Wang H-N, Sun S-S, Liu M-Z, Yan M-C, Liu Y-F, Zhu Z, et al. Natural bioactive compounds from marine fungi (2017-2020). J Asian Nat Prod Res. 2021;24:203-30.
[3] Pinedo-Rivilla C, Aleu J. Cryptic metabolites from marine-derived microorganisms using OSMAC and epigenetic approaches. Mar Drugs. 2022;20:84.
[4] Farinella VF, Kawafune ES, Tangerina MMP, Domingos HV, Costa-Lotufo LV. OSMAC strategy integrated with molecular networking for accessing griseofulvin derivatives from endophytic fungi of Moquiniastrum polymorphum (Asteraceae). Molecules. 2021;26:7316.
[5] Wolfender J-L, Nuzillard J-M, van der Hooft JJJ, Renault J-H. Accelerating metabolite identification in natural product research: toward an ideal combination of liquid chromatography-high-resolution tandem mass spectrometry and NMR profiling, in Silico databases, and chemometrics. Anal Chem. 2019;91:704-42.
[6] Wolfender J-L, Litaudon M, Touboul D. Innovative omics-based approaches for prioritisation and targeted isolation of natural products—new strategies for drug discovery. Narural Product Reports. 2019;36:855-68.
[7] Hawksworth DL, Lücking R. Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spect. 2017. https://doi.org/10.1128/microbiolspec.FUNK-0052-2016.
[8] Cheng Z, Liu W, Fan R, Han S, Li Y, Cui X, et al. Terpenoids from the deep-sea-derived fungus Penicillium thomii YPGA3 and their bioactivities. Mar Drugs. 2020;18:164.
[9] Cheng Z, Li Y, Xu W, Liu W, Liu L, Zhu D, et al. Three new cyclopiane-type diterpenes from a deep-sea derived fungus Penicillium sp. YPGA11 and their effects against human esophageal carcinoma cells. Bioorg Chem. 2019;91:103129.
[10] Ebel R. Terpenes from marine-derived fungi. Mar Drugs. 2010;8:2340-68.
[11] Jiang M, Wu Z, Guo H, Liu L. A Review of terpenes from marine-derived Fungi: 2015-2019. Mar Drugs. 2020;18:321.
[12] Chen HW, Jiang CX, Li J, Li N, Zang Y, Wu XY, et al. Beshanzoides A-D, unprecedented cycloheptanone-containing polyketides from Penicillium commune P-4-1, an endophytic fungus of the endangered conifer Abies beshanzuensis. RSC Adv. 2021;11:39781-9.
[13] Sobolevskaya MP, Leshchenko EV, Hoai TPT, Denisenko VA, Dyshlovoy SA, Kirichuk NN, et al. Pallidopenillines: polyketides from the alga-derived fungus Penicillium thomii Maire KMM 4675. J Nat Prod. 2016;79:3031-8.
[14] Iida M, Ooi T, Kito K, Yoshida S, Kanoh K, Shizuri Y, et al. Org Lett. 2008;10:845-8.
[15] Cheng Z, Xu W, Wang Y, Bai S, Liu L, Luo Z, et al. Two new meroterpenoids and two new monoterpenoids from the deep sea-derived fungus Penicillium sp YPGA11. Fitoterapia. 2019;133:120-4.
[16] Zhang P, Wei Q, Yuan X. Newly reported alkaloids produced by marine-derived Penicillium species (covering 2014-2018). Bioorg Chem. 2020;99: 103840.
[17] Youssef FS, Ashour ML, Singab AN, Wink M. A Comprehensive review of bioactive peptides from marine fungi and their biological significance. Mar Drugs. 2019;17:559.
[18] Dalsgaard PW, Larsen TO, Frydenvang K. Psychrophilin A and cycloaspeptide D, novel cyclic peptides from the psychrotolerant fungus Penicillium ribeum. J Nat Prod. 2004;67:878-81.
[19] 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.
[20] Honghua L, Yangi F, Fuhand S, Xiuli X. Recent updates on the antimicrobial compounds from marine-derived Penicillium fungi. Chem Biodiv. 2023;20:e202301278.
[21] Leshchenko EV, Antonov AS, Borkunov GV, Hauschild J, Zhuravleva OI, Khudyakova YV, et al. New Bioactive beta-resorcylic acid derivatives from the alga-derived fungus Penicillium antarcticum KMM 4685. Mar Drugs. 2023;21:178.
[22] Leshchenko EV, Antonov AS, Dyshlovoy SA, Berdyshev DV, Hauschild J, Zhuravleva OI, et al. Meroantarctines A-C, meroterpenoids with rearranged skeletons from the alga-derived fungus Penicillium antarcticum KMM 4685 with potent p-glycoprotein inhibitory activity. J Nat Prod. 2022;85:2746-52.
[23] Afiyatullov SS, Leshchenko EV, Berdyshev DV, Sobolevskaya MP, Antonov AS, Denisenko VA, et al. Zosteropenillines: polyketides from the marine-derived fungus Penicillium thomii. Mar Drugs. 2017;15:46.
[24] Zhuravleva OI, Oleinikova GK, Antonov AS, Kirichuk NN, Pelageev DN, Rasin AB, et al. New antibacterial chloro-containing polyketides from the alga-derived fungus Asteromyces cruciatus KMM 4696. Journal of Fungi. 2022;8:454.
[25] Zhuravleva OI, Chingizova EA, Oleinikova GK, Starnovskaya SS, Antonov AS, Kirichuk NN, et al. Anthraquinone derivatives and other aromatic compounds from marine fungus Asteromyces cruciatus KMM 4696 and their effects against Staphylococcus aureus. Mar Drugs. 2023;21:21080431.
[26] Chen Y, Jiang N, Wei YJ, Li X, Ge HM, Jiao RH, et al. Citrofulvicin, an antiosteoporotic polyketide from Penicillium velutinum. Org Lett. 2018;20:3741-4.
[27] Chen Y, Wei YJ, Jiang N, Ge HM, Jiao RH, Cheng X, et al. Spirocitromycetin, a fungal polyketide with an antiosteoporotic pharmacophore. J Nat Prod. 2022;85:1442-7.
[28] Wubshet SG, Nyberg NT, Tejesvi MV, Pirttilä AM, Kajula M, Mattila S, et al. Targeting high-performance liquid chromatography-high-resolution mass spectrometry-solid-phase extraction-nuclear magnetic resonance analysis with high-resolution radical scavenging profiles—Bioactive secondary metabolites from the endophytic fungus Penicillium namyslowskii. J Chromatogr A. 2013;1302:34-9.
[29] Dean FM, Eade RA, Moubasher R, Robertson A. The chemistry of fungi part XXVII. The structure of fulvic acid from Carpenteles brefeldianum. J Chem Soc 1957;3497-3510.
[30] Oxford A, Raistrick H. Studies in the biochemistry of microorganisms: fulvic acid, a new crystalline yellow pigment, a metabolic product of P. griseofulvum Dierckx, P. flexuosum Dale and P. Brefeldianum Dodge. Biochem J. 1935;39:1102-15.
[31] Hafez Ghoran S, Taktaz F, Ayatollahi SA. Anthraquinones and their analogues from marine-derived fungi: chemistry and biological activities. Mar Drugs. 2022;20:474.
[32] Noinart J, Buttachon S, Dethoup T, Gales L, Pereira JA, Urbatzka R, et al. A new ergosterol analog, a new bis-anthraquinone and anti-obesity activity of anthraquinones from the marine sponge-associated fungus Talaromyces stipitatus KUFA 0207. Mar Drugs. 2017;15:139.
[33] Kimura YK. New constitutents of roots of Polygonum cuspidatum. Planta Med. 1983;48:164-8.
[34] Saraiva N, Rodrigues B, Jimenez P, Guimarães L, Torres M, Rodrigues-Filho E, et al. Cytotoxic compounds from the marine-derived fungus Aspergillus sp. recovered from the sediments of the Brazilian coast. Nat Prod Rep. 2015;29:1545-50.
[35] Víctor Rodríguez Martín-Aragón, Mónica Trigal Martínez, Cristina Cuadrado, Antonio Hernández Daranas, Antonio Fernández Medarde, López JMS OSMAC approach and cocultivation for the induction of secondary metabolism of the fungus Pleotrichocladium opacum. ASC Omega 2023;8:39873-39885.
[36] Inamori Y, Kato Y, Kubo M, Kamiki T, Takemoto T. Studies on metabolites produced by Aspergillus terreus var. aureus. I. Chemical structures and antimicrobial activities of metabolites isolated from culture broth. Chem Pharm Bull (Tokyo). 1983;31:4543-8.
[37] Shaaban M, Abdel-Razek AS, Previtali V, Clausen MH, Gotfredsen CH, Laatsch H, et al. Sulochrins and alkaloids from a fennel endophyte Aspergillus sp. FVL2. Nat Prod Res. 2023;37:1310-20.
[38] Weihao C, Jiawen Z, Xin Q, Kai Z, Xiaoyan P, Xiuping L, et al. p-Terphenyls as anti-HSV-1/2 agents from a deep-sea-derived Penicillium sp. J Nat Prod. 2021;84:2822-31.
[39] Fukuda T, Furukawa T, Kobayashi K, Nagai K, Uchida R, Tomoda H Helvamide, a new inhibitor of sterol O-acyltransferase produced bythe fungus Aspergillus nidulans BF-0142. J. Antibiot. 2019;72:8:s41429-018-0101-8.
[40] Hui-Hui K, Mei-Jia Z, Li-Ying M, Xian-Guo R, De-Sheng L, Wei-Zhong L. Iizukines C-E from a saline soil fungus Aspergillus iizukae. Bioorg Chem. 2019;91:103167.
[41] Fujita T, Makishima D, Akiyama K. New convulsive compounds, brasiliamides A and B, from Penicillium brasilianum Batista JV-379. Biosci Biotechnol Biochem. 2002;66:1697-705.
[42] Fujita T, Hayashi H. New brasiliamide congeners, brasiliamides C, D and E, from Penicillium. Biosci Biotechnol Biochem. 2004;68:820-6.
[43] Yuan B, Liu D, Guan X, Yan Y, Zhang J, Zhang Y, et al. Piperazine ring formation by a single-module NRPS and cleavage by an α-KG-dependent nonheme iron dioxygenase in brasiliamide biosynthesis. Biotechnol Prod Process Eng. 2020;104:6149-59.
[44] Li F, Guo W, Wu L, Zhu T, Gu Q, Li D, et al. Saroclazines A-C, thio-diketopiperazines from mangrove-derived fungi Sarocladium kiliense HDN11-84. Arch Pharmacal Res. 2018;41:30-4.
[45] Li H, Peng SY, Yang DP, Bai B, Zhu LP, Mu CY, et al. Enantiomeric neolignans and a sesquiterpene from Solanum erianthum and their absolute configuration assignment. Chirality. 2016;28:259-63.
[46] Zhang CY, Luo L, Xia J, Song YN, Zhang LJ, Zhang M, et al. Sesquiterpenes and lignans from the flower buds of Daphne genkwa and their nitric oxide inhibitory activities. Nat Prod Res. 2018;32:2893-9.
[47] Wang W-J, Li D-Y, Li Y-C, Hua H-M, Ma E-L. Caryophyllene sesquiterpenes from the marine-derived fungus Ascotricha sp. ZJ-M-5 by the one strain-many compounds strategy. J Nat Prod. 2014;77:1367-71.
[48] Shi Y, Pan C, Auckloo BN, Chen X, Chen C-TA, Wang K, et al. Stress-driven discovery of a cryptic antibiotic produced by Streptomyces sp. WU20 from Kueishantao hydrothermal vent with an integrated metabolomics strategy. Appl Biochem Microbiol. 2017;101:1395-408.
[49] Gube M Fungal molecular response to heavy metal stress. Mycota 2016;47-68.
[50] Wysocki R. How Saccharomyces cerevisiae copes with toxic metals and metalloids. FEMS Microbiol Rev. 2010;34:925-51.
[51] Gräfe U, Ihn W, Tresselt D, Miosga N, Kaden U, Schlegel B, et al. Tolypocladin—a new metal-chelating 2-aza-anthraquinone from Tolypocladium inflatum. Biol Metals. 1990;3:39-44.
[52] Greenaway W. Relationship between mercury resistance and pigment production in Pyrenophora avenae. Trans Br Mycol Soc. 1971;56:37-44.
[53] Ibrahim SR, Alsiyud DF, Alfaeq AY, Mohamed SG, Mohamed GA, et al. Benzophenones-natural metabolites with great Hopes in drug discovery: structures. RSC Adv. 2023;13:23472-98.
[54] Marin B. Molecular phylogeny and classification of the mamiellophyceae class. nov. (Chlorophyta) based on sequence comparisons of the nuclear- and plastid-encoded rRNA operons. Protist. 2010;161:304-36.
[55] Fehling J, Green DH, Davidson K, Bolch CJ. Domoic acid production by Pseudo-nitzschia seriata (Bacillariophyceae) in scottish waters. J Phycol. 2004;40:622-30.
[56] Glass NL. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol. 1995;61:1323-30.
[57] Kumar S, Stecher G, Li M, Knyaz C. Tamura K MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547.
[58] Tamura K. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512-26.
[59] Nesterenko LE, Popov RS, Zhuravleva OI, Kirichuk NN, Chausova VE, Krasnov KS, et al. A study of the metabolic profiles of Penicillium dimorphosporum KMM 4689 which led to Its re-identification as Penicillium hispanicum. Fermentation. 2023;9:337.
[60] Chambers MC, MacLean B, Burke R, Amodei D, Ruderman DL, Neumann S, et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol. 2012;30:918-20.
[61] Pluskal T, Castillo S, Villar-Briones A, Orešič M. MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinform. 2010;11.
[62] Sheldrick GM. Crystal structure refinement with SHELXL. Acta Crystallogr Sect C Struct Chem. 2015;71:3-8.
[63] Sheldrick GM. SHELXT—integrated space-group and crystal-structure determination. Acta Crystallogr Sect A Found Crystallogr. 2015;71:3-8.
[64] Leutou AS, Yun K, Son BW. Induced production of 6,9-dibromoflavasperone, a new radical scavenging naphthopyranone in the marine-mudflat-derived fungus Aspergillus niger. Arch Pharm Res. 2016;39:806-10. |
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