Bioactive Bafilomycins and a New N-Arylpyrazinone Derivative from Marine-derived Streptomyces sp. HZP-2216E

Abstract

A MeOH extract prepared from culture of an actinomycete Streptomyces sp. HZP-2216E isolated from marine green algae Ulva pertusa was found to significantly inhibit proliferation of human glioma cells. Two different media were applied to culture this marine actinomycete, which produced two new compounds of 23-O-butyrylbafilomycin D and streptoarylpyrazinone A, together with known bafilomycin D, 9-hydroxybafilomycin D, and bafilomycin A₁. Structures of new compounds were determined by extensive NMR spectroscopic analyses and HRESIMS data. Bioactive assay indicated that all isolated bafilomycins significantly inhibited the proliferation of different glioma cell lines and the growth of methicillin-resistant Staphylococcus aureus with 23-O-butyrylbafilomycin D as the most active compound. Streptoarylpyrazinone A is a new N-arylpyrazinone derivative existing as a zwitterion, and this type of compounds was rarely found from natural resources.

Key words

marine Streptomyces sp. HZP-2216E - Ulva pertusa - Ulvaceae - bafilomycins - N-arylpyrazinone derivative - antiproliferative activity - antibacterial activity

• References

• 1 Molinski TF, Dalisay DS, Lievens SL, Saludes JP. Drug development from marine natural products. Nat Rev Drug Discov 2009; 8: 69-85
• 2 Gulder TA, Moore BS. Chasing the treasures of the sea-bacterial marine natural products. Curr Opin Microbiol 2009; 12: 252-260
• 3 Rateb ME, Ebel R. Secondary metabolites of fungi from marine habitats. Nat Prod Rep 2011; 28: 290-344
• 4 Bibi F, Faheem M, Azhar EI, Yasir M, Alvi SA, Kamal MA, Ullah I, Nasser MI. Bacteria from marine sponges: a source of new drugs. Curr Drug Metab 2017; 18: 11-15
• 5 König GM, Kehraus S, Seibert SF, Abdel-Lateff A, Müller D. Natural products from marine organisms and their associated microbes. Chembiochem 2006; 7: 229-238
• 6 Guan H, Wang S. Chinese Marine Materia Medica. Shanghai: Shanghai Scientific & Technical Publishers; 2009: 290-291
• 7 Qi H, Zhang Q, Zhao T, Chen R, Zhang H, Niu X, Li Z. Antioxidant activity of different sulfate content derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta) in vitro . Int J Biol Macromol 2005; 37: 195-199
• 8 Hong JK, Bong MH, Park JC, Moon HK, Kim DW, Lee SC, Lee JH. Antioxidant and immunomodulatory effects of Ulva pertusa kjellman on broiler chickens. J Anim Sci Tec 2011; 53: 419-428
• 9 Shi J, Cheng C, Zhao H, Jing J, Gong N, Lu W. In vivo anti-radiation activities of the Ulva pertusa polysaccharides and polysaccharide-iron (III) complex. Int J Biol Macromol 2013; 60: 341-346
• 10 Luo Z, Chen X, Wang X, Qu C, Zhang M, An W, Xiong S. Extraction and purification of anti-viral proteoglycan from Ulva pertusa and its activity against coxsackie virus B3. Shizhen Guoyi Guoyao 2010; 21: 1090-1093
• 11 Tabarsa M, Han JH, Kim CY, You SG. Molecular characteristics and immunomodulatory activities of water-soluble sulfated polysaccharides from Ulva pertusa . J Med Food 2012; 15: 135-144
• 12 Yu P, Zhang Q, Li N, Xu Z, Wang Y, Li Z. Polysaccharides from Ulva pertusa (Chlorophyta) and preliminary studies on their antihyperlipidemia activity. J Appl Phycol 2003; 15: 21-27
• 13 Li X, Fan X, Han L, Lou Q. Fatty acids of some algae from the Bohai Sea. Phytochemistry 2002; 59: 157-161
• 14 Xu J, Lu Q, Zhao Y. Studies on chemical constituents of green algae Ulva pertusa . China J Chin Materia Med 2007; 32: 1536-1538
• 15 Yamada K, Shizuri Y, Ishida Y, Shibata S. Cardiac inhibitory action of constituents of the marine green alga Ulva pertusa . J Pharma Sci 1983; 72: 945-946
• 16 Lu Q, Xu J, Zhao Y, Zhou C. Studies on chemical constituents of Ulva pertusa . Chin Pharma J 2008; 43: 582-584
• 17 Katayama T. Chemical studies on volatile constituents of sea-weed-II: On volatile acids of Ulva pertusa K. Nippon Suisan Gakkaishi 1955; 21: 416-419
• 18 Xin W, Ye X, Yu S, Lian XY, Zhang Z. New capoamycin-type antibiotics and polyene acids from marine Streptomyces fradiae PTZ0025. Mar Drugs 2012; 10: 2388-2402
• 19 Yu S, Ye X, Chen L, Lian XY, Zhang Z. Polyoxygenated 24,28-epoxyergosterols inhibiting the proliferation of glioma cells from sea anemone Anthopleura midori . Steroids 2014; 88: 19-25
• 20 Yu S, Ye X, Huang H, Peng R, Su Z, Lian XY, Zhang Z. Bioactive sulfated saponins from sea cucumber Holothuria moebii . Planta Med 2015; 81: 152-159
• 21 Chen L, Liang Y, Song T, Anjum K, Wang W, Yu S, Huang H, Lian XY, Zhang Z. Synthesis and bioactivity of tripolinolate A from Tripolium vulgare and its analogs. Bioorg Med Chem Lett 2015; 25: 2629-2633
• 22 Ye X, Anjum K, Song T, Wang W, Yu S, Huang H, Lian XY, Zhang Z. A new curvularin glycoside and its cytotoxic and antibacterial analogues from marine actinomycete Pseudonocardia sp. HS7. Nat Prod Res 2016; 30: 1156-1161
• 23 Liang Y, Xie X, Chen L, Yan S, Ye X, Anjum K, Huang H, Lian XY, Zhang Z. Bioactive polycyclic quinones from marine Streptomyces sp. 182SMLY. Mar Drugs 2016; 14: 10
• 24 Zhang F, Ye X, Chai W, Lian XY, Zhang Z. New metabolites and bioactive actinomycins from marine-derived Streptomyces sp. ZZ338. Mar Drugs 2016; 14: 181
• 25 Ye X, Anjum K, Song T, Wang W, Liang Y, Chen M, Huang H, Lian XY, Zhang Z. Antiproliferative cyclodepsipeptides from the marine actinomycete Streptomyces sp. P11-23B downregulating the tumor metabolic enzymes of glycolysis, glutaminolysis, and lipogenesis. Phytochemistry 2017; 135: 151-159
• 26 Kretschmer A, Dorgerloh M, Deeg M, Hagenmaier H. The structures of novel insecticidal macrolides: bafilomycins D and E, and oxohygrolidin. Agri Bio Chem 1985; 49: 2509-2511
• 27 Yu Z, Zhao L, Jiang C, Duan Y, Wong L, Carver KC, Schuler LA. Shen B. Bafilomycins produced by an endophytic actinomycete Streptomyces sp. YIM56209. J Antibiot 2011; 64: 159-162
• 28 Werner G, Hagenmaier H, Drautz H, Baumgartner A, Zahner H. Metabolic products of microorganisms. 224. Bafilomycins, a new group of macrolide antibiotics. Production, isolation, chemical structure and biological activity. J Antibiot 1984; 37: 110-117
• 29 Kim SD, Ryoo IJ, Kim CJ, Uramoto M, Yoo ID. The structure determination of a herbicidal compound, 3D5. J Microbiol Biotech 1993; 3: 51-56
• 30 Bowman EJ, Siebers A, Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 1988; 85: 972-976
• 31 Roush WR, Bannister TD, Wendt MD, Jablonowski JA, Scheidt KA. Studies on the synthesis of bafilomycin A (1): stereochemical aspects of the fragment assembly aldol reaction for construction of the C(13)–C(25) segment. J Org Chem 2002; 67: 4275-4283
• 32 Papini E, de Bernard M, Bugnoli M, Milia E, Rappuoli R, Montecucco C. Cell vacuolization induced by Helicobacter pylori: inhibition by bafilomycins A₁, B₁, C₁, and D. FEMS Microbiol Lett 1993; 113: 155-159
• 33 Tacara O, Sriamornsak P, Dass CR. Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol 2013; 65: 157-170