N-Acetylborrelidin B: a new bioactive metabolite from Streptomyces mutabilis sp. MII
-
Abdelaaty Hamed
Abstract
In the course of our screening program for new bioactive compounds, a naturally new 18-membered macrolide antibiotic, N-acetylborrelidin B (1) along with borrelidin (2) were obtained from the marine Streptomyces mutabilis sp. MII. The strain was isolated from a sediment sample collected in the Red Sea at the Hurghada Coast and characterized taxonomically. Additional nine diverse bioactive compounds were reported: 6-prenyl-indole-3-acetonitrile (3), sitosteryl-3β-d-glucoside, campesterol, ferulic acid, linoleic acid methyl ester, linoleic acid, N-acetylanthranilic acid, indole 3-acetic acid methyl ester, indole 3-carboxylic acid, and adenosine. Structure 1 was confirmed by in-depth NMR studies and by mass spectra, and comparison with related literature data. The antimicrobial activity of the strain extract and compounds 1 and 2 were studied using a panel of pathogenic microorganisms. The in vitro cytotoxicity of compounds 1 and 2 as well as the crude extract were tested against the human cervix carcinoma cell line (KB-3-1).
Acknowledgments
The authors are thankful to the NMR and MS Departments in Bielefeld University for the spectral measurements. We thank Carmela Michalek for biological activity testing, and Marco Wißbrock and Anke Nieß for technical assistances. DNA sequences were determined by the CeBiTec DNA sequencing core facility. The bioinformatics support of the BMBF-funded project “Bielefeld-Gießen Resource Center for Microbial Bioinformatics – BiGi (grant number 031A533)” within the German Network for Bioinformatics Infrastructure (de.NBI) is gratefully acknowledged. This research work was financed by the German Academic Exchange Service (DAAD) with funds from the German Federal Foreign Office in the frame of the Research Training Network “Novel Cytotoxic Drugs from Extremophilic Actinomycetes” (Project ID57166072).
References
1. Fenical W. Chemical studies of marine bacteria: developing a new resource. Chem Rev 1993;93:1673–83.10.1021/cr00021a001Search in Google Scholar
2. Fenical W, Jensen PR. Marine microorganisms: a new biomedical resource. In: Attaway DH, Zaborsky OR, editors. Marine Biotechnology. Pharmaceutical and Bioactive Natural Products, Vol. 1. New York, London: Plenum Press, 1993:419–59.10.1007/978-1-4899-2391-2_12Search in Google Scholar
3. Pietra F. Secondary metabolites from marine microorganisms: bacteria, protozoa, algae and fungi. Achievements and prospects. Nat Prod Rep 1997;14:453–64.10.1039/np9971400453Search in Google Scholar PubMed
4. Sánchez López JM, Martínez Insua M, Pérez Baz J, Fernández Puentes JL, Cañedo Hernández LM. New cytotoxic indolic metabolites from a marine Streptomyces. J Nat Prod 2003;66:863–4.10.1021/np0204444Search in Google Scholar PubMed
5. Hamed A, Abdel-Razek AS, Frese M, Wibberg D, El-Haddad AF, Ibrahim TM, et al. New oxaphenalene derivative from marine-derived Streptomyces griseorubens sp. ASMR4. Z Naturforsch 2017;72:53–62.10.1515/znb-2016-0145Search in Google Scholar
6. Zhang HW, Song YC, Tan RX. Biology and chemistry of endophytes. Nat Prod Rep 2006;23:753–71.10.1039/b609472bSearch in Google Scholar PubMed
7. Cragg GM, Newman DJ. Plants as a source of anti-cancer agents. J Ethnopharmacol 2005;100:72–9.10.1016/j.jep.2005.05.011Search in Google Scholar PubMed
8. Butler MS. The role of natural products in drug discovery. J Nat Prod 2004;67:2141–53.10.1021/np040106ySearch in Google Scholar PubMed
9. Strohl WR. Antimicrobials. In: Bull AT, editor. Microbial Diversity and Bioprospecting. USA: ASM Press, 2004:336–55.10.1128/9781555817770.ch31Search in Google Scholar
10. Song YC, Li H, Ye YH, Shan CY, Yang YM, Tan RX. Endophytic naphthopyrone metabolites are co-inhibitors of xanthine oxidase, sw1116 cell and some microbial growths. FEMS Microbiol Lett 2004;241:67–72.10.1016/j.femsle.2004.10.005Search in Google Scholar PubMed
11. Arasu MV, Duraipandiyan V, Ignacimuthu S. Antibacterial and antifungal activities of polyketide metabolite from marine Streptomyces sp. AP-123 and its cytotoxic effect. Chemosphere 2013;90:479–87.10.1016/j.chemosphere.2012.08.006Search in Google Scholar PubMed
12. Balachandran C, Duraipandiyan V, Emi N, Ignacimuthu S. Antimicrobial and cytotoxic properties of Streptomyces sp. (ERINLG-51) isolated from Southern Western Ghats. South Ind J Biol Sci 2015;1:7–14.10.22205/sijbs/2015/v1/i1/100436Search in Google Scholar
13. Faulkner D. Marine natural products. J Nat Prod Rep 2000;17: 7–55.10.1039/a809395dSearch in Google Scholar PubMed
14. Laatsch, H. Marine bacterial metabolites. In: Proksch P, Müller WE, editors. Frontiers in marine biotechnology. Norfolk, UK: Horizon Bioscience, 2006:225–88. ISBN 1-904933-18-1.Search in Google Scholar
15. El-Gendy MM, Shaaban M, Shaaban KA, El-Bondkly AM, Laatsch H. Essramycin: a first triazolopyrimidine antibiotic isolated from nature. J Antibiot 2008;61:149–57.10.1038/ja.2008.124Search in Google Scholar PubMed
16. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966;16:313–40.10.1099/00207713-16-3-313Search in Google Scholar
17. Shirling EB, Gottlieb D. Cooperative description of type cultures of Streptomyces. II – species description from first study. Int J Syst Bacteriol 1968;18:69–100.10.1099/00207713-18-2-69Search in Google Scholar
18. Shirling EB, Gottlieb D. Cooperative description of type cultures of Streptomyces. III – additional species description from first and second studies. Int J Syst Evol Micr 1968;18:279–345.10.1099/00207713-18-4-279Search in Google Scholar
19. Shirling EB, Gottlieb D. Cooperative description of type cultures of Streptomyces. IV – species description from 2nd, 3rd and 4th studies. Int J Syst Evol Micr 1969;19:391–512.10.1099/00207713-19-4-391Search in Google Scholar
20. Shirling EB, Gottlieb D. Cooperative description of type strain of Streptomyces. V – additional description. The 2nd, 3rd and 4th studies. Int J Syst Evol Micr 1972;22:265–300.10.1099/00207713-22-4-265Search in Google Scholar
21. Waksman SA. The Actinomycetes. Classification, Identification and Description of Genera and Species. Baltimore, USA: The Williams & Wilkins Co., 1961.Search in Google Scholar
22. Williams ST, Davies FL. Use of a scanning electron microscope for the examination of Actinomycetes. J Gen Microbiol 1967;48:171–7.10.1099/00221287-48-2-171Search in Google Scholar PubMed
23. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406–25.Search in Google Scholar
24. Nei M, Kumar S. Molecular evolution and phylogenetics. New York: Oxford University Press, 2000.10.1093/oso/9780195135848.001.0001Search in Google Scholar
25. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–4.10.1093/molbev/msw054Search in Google Scholar PubMed PubMed Central
26. Whitman W, Goodfellow M, Kämpfer P, Busse H-J, Trujillo M, Ludwig W, et al. Bergey’s manual of systematic bacteriology, the actinobacteria, 5, 2nd ed. New York: Springer, 2012.10.1007/978-0-387-68233-4Search in Google Scholar
27. Laatsch H. AntiBase – A data base for rapid structural determination of microbial natural products, and annual updates. Weinheim, Germany: Wiley-VCH, 2016.Search in Google Scholar
28. Dictionary of Natural Products on CD-ROM, Chapman & Hall Chemical Database, Boca Raton: CRC-Press, Taylor and Francis Group, 2016.Search in Google Scholar
29. The Chemical Abstracts by Scifinder Scholar (https://scifinder.cas.org/scifinder), search from July 2017.Search in Google Scholar
30. Schulze CJ, Bray WM, Loganzo F, Lam M-H, Szal T, Villalobos A, et al. Borrelidin B: isolation, biological activity, and implications for nitrile biosynthesis. J Nat Prod 2014;77:2570–4.10.1021/np500727gSearch in Google Scholar PubMed
31. Berger J, Jampolsky LM, Goldberg MW. Borrelidin, a new antibiotic with antiborrelia activity and penicillin enhancement properties. Arch Biochem 1949;22:476–8.Search in Google Scholar PubMed
32. Wakabayashi T, Kageyama R, Naruse N, Tsukahara N, Funahashi Y, Kitoh K, et al. Borrelidin is an angiogenesis inhibitor; disruption of angiogenic capillary vessels in a rat aorta matrix culture model. J Antibiot 1997;50:671–6.10.7164/antibiotics.50.671Search in Google Scholar PubMed
33. Azcárate IG, Marín-García P, Camacho N, Pérez-Benavente S, Puyet A, Diez A, et al. Insights into the preclinical treatment of blood-stage malaria by the antibiotic borrelidin. Br J Pharmacol 2013;169:645–58.10.1111/bph.12156Search in Google Scholar PubMed PubMed Central
34. Gafiuc D, Weiß M, Mylonas I, Brüning A. Borrelidin has limited anti-cancer effects in bcl-2 overexpressing breast cancer and leukemia cells and reveals toxicity in non-malignant breast epithelial cells. J Appl Toxicol 2014;34:1109–13.10.1002/jat.2946Search in Google Scholar PubMed
35. Sugawara A, Tanaka T, Hirose T, Ishiyama A, Iwatsuki M, Takahashi Y, et al. Borrelidin analogues with antimalarial activity: design, synthesis and biological evaluation against Plasmodium falciparum parasites. Bioorg Med Chem Lett 2013;23:2302–5.10.1016/j.bmcl.2013.02.075Search in Google Scholar PubMed
36. Wilkinson B, Gregory MA, Moss SJ, Carletti I, Sheridan RM, Kaja A, et al. Separation of anti-angiogenic and cytotoxic activities of borrelidin by modification at the C17 side chain. Bioorg Med Chem Lett 2006;16:5814–17.10.1016/j.bmcl.2006.08.073Search in Google Scholar PubMed
37. Moss SJ, Carletti I, Olano C, Sheridan RM, Ward M, Math V, et al. Biosynthesis of the angiogenesis inhibitor borrelidin: directed biosynthesis of novel analogues. Chem Commun 2006;14:2341–3.10.1039/B602931KSearch in Google Scholar
38. Kumar V, Bharti A, Gusain O, Bisht GS. An improved method for isolation of genomic DNA from filamentous actinomycetes. J Sci Engg Tech Mgt 2010;2:10–13.Search in Google Scholar
39. Yassin AF, Rainey FA, Burghardt J, Gierth D, Ungerechts J, Lux I, et al. A new actinomycete species, Nocardiopsis lucentensis. Int J Syst Bacteriol 1993;43:266–71.10.1099/00207713-43-2-266Search in Google Scholar
40. Kuster E, Williams ST. Production of hydrogen sulphide by Streptomycetes and methods for its detection. Appl Microbiol 1964;12:46–52.10.1128/am.12.1.46-52.1964Search in Google Scholar PubMed
41. Crawford DL, McCoy E. Cellulases of Thermomonospora fusca and Streptomycesthermodiastaticus. Appl Microbiol 1972;24:150–2.10.1128/am.24.1.150-152.1972Search in Google Scholar PubMed PubMed Central
42. Tresner HD, Hayes JA, Backus EJ. Differential tolerance of Streptomycetes to sodium chloride as a taxonomic aid. Appl Microbiol 1968;16:1134–6.10.1128/am.16.8.1134-1136.1968Search in Google Scholar PubMed PubMed Central
43. Bauer AW, Kirby WM, Sherris JC, Truck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966;45:493–6.10.1093/ajcp/45.4_ts.493Search in Google Scholar PubMed
44. Awantu AF, Lenta BN, Bogner T, Fongang YF, Ngouela S, Wansi JD, et al. Dialiumoside, an olean-18-ene triterpenoid from Dialium excelsum. Z Naturforsch 2011;66b:624–8.10.1515/znb-2011-0610Search in Google Scholar
45. Sammet B, Bogner T, Nahrwold M, Weiss C, Sewald N. Approaches for the synthesis of functionalized cryptophycins. J Org Chem 2010;75:6953–60.10.1021/jo101563sSearch in Google Scholar PubMed
Supplemental Material:
The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2017-0140).
©2018 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Three new coumarin types from aerial parts of Ammi majus L. and their cytotoxic activity
- Sesquiterpenes from the Saudi Red Sea: Litophyton arboreum with their cytotoxic and antimicrobial activities
- Biotechnology for bioenergy dedicated trees: meeting future energy demands
- Malusides, novel glucosylceramides isolated from apple pomace (Malus domestica)
- GC-MS characterization of n-hexane soluble fraction from dandelion (Taraxacum officinale Weber ex F.H. Wigg.) aerial parts and its antioxidant and antimicrobial properties
- N-Acetylborrelidin B: a new bioactive metabolite from Streptomyces mutabilis sp. MII
- Synthesis of methyl 4-dihydrotrisporate B and methyl trisporate B, morphogenetic factors of Zygomycetes fungi
- Volatiles from Cinnamomum cassia buds
- A new method for fast extraction and determination of chlorophylls in natural water
- Synthesis and biological evaluation of acyl derivatives of hydroxyflavones as potent antiproliferative agents against drug resistance cell lines
Articles in the same Issue
- Frontmatter
- Three new coumarin types from aerial parts of Ammi majus L. and their cytotoxic activity
- Sesquiterpenes from the Saudi Red Sea: Litophyton arboreum with their cytotoxic and antimicrobial activities
- Biotechnology for bioenergy dedicated trees: meeting future energy demands
- Malusides, novel glucosylceramides isolated from apple pomace (Malus domestica)
- GC-MS characterization of n-hexane soluble fraction from dandelion (Taraxacum officinale Weber ex F.H. Wigg.) aerial parts and its antioxidant and antimicrobial properties
- N-Acetylborrelidin B: a new bioactive metabolite from Streptomyces mutabilis sp. MII
- Synthesis of methyl 4-dihydrotrisporate B and methyl trisporate B, morphogenetic factors of Zygomycetes fungi
- Volatiles from Cinnamomum cassia buds
- A new method for fast extraction and determination of chlorophylls in natural water
- Synthesis and biological evaluation of acyl derivatives of hydroxyflavones as potent antiproliferative agents against drug resistance cell lines
