Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2019

Open Access 01-12-2019 | Glioblastoma | Research article

Cytotoxic activity of crude extracts from Datura stramonium’s fungal endophytes against A549 lung carcinoma and UMG87 glioblastoma cell lines and LC-QTOF-MS/MS based metabolite profiling

Published in: BMC Complementary Medicine and Therapies | Issue 1/2019

Login to get access

Abstract

Background

Endophytic fungi are a proven source of bioactive secondary metabolites that may provide lead compounds for novel drug discovery. In this study, crude extracts from fungal endophytes isolated from Datura stramonium were evaluated for cytotoxic activity on two human cancer cell lines.

Methods

Fungal endophytes were isolated from surface sterilized aerial parts of D. stramonium and identified using molecular, morphological and phylogenetic methods. Ethyl acetate crude extracts from these isolates were evaluated for cytotoxic activity on A549 lung carcinoma and UMG87 glioblastoma cell lines. Metabolite profiling was then performed by liquid chromatography coupled to quadrupole time-of-flight with tandem mass spectrometry (LC-QTOF-MS/MS) for the cytotoxic crude extract.

Results

Eleven fungal endophytes were identified from D. stramonium. Significant cytotoxicity was only observed from the crude extract of Alternaria sp. KTDL7 on UMG87 glioblastoma cells (IC50 = 21.49 μg/ml). Metabolite profiling of this crude extract tentatively revealed the presence of the following secondary metabolites: 1,8-dihydroxynaphthalene (1), anserinone B (2), phelligridin B (3), metacytofilin (4), phomopsidin (5) and vermixocin A (6). Compounds 2 and 3 have been shown to be cytotoxic in literature.

Conclusion

The findings in this study suggest that the crude extract of Alternaria sp. KTDL7 possesses compound(s) cytotoxic to glioblastoma multiforme cells. Future studies to isolate and characterize the cytotoxic compound(s) from this fungus could result in lead development of a fungal-based drug for glioblastoma multiforme treatment.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kumara PM, Shweta S, Vasanthakumari MM, Sachin N, Manjunatha BL, Jadhav SS, Ravikanth G, Ganeshaiah KN, Shaanker RU. Endophytes and plant secondary metabolite synthesis: molecular and evolutionary perspective. In: Verma VC, Gange AC, editors. Advances in endophytic research. Delhi: Springer India; 2014. p. 177–190. Kumara PM, Shweta S, Vasanthakumari MM, Sachin N, Manjunatha BL, Jadhav SS, Ravikanth G, Ganeshaiah KN, Shaanker RU. Endophytes and plant secondary metabolite synthesis: molecular and evolutionary perspective. In: Verma VC, Gange AC, editors. Advances in endophytic research. Delhi: Springer India; 2014. p. 177–190.
2.
go back to reference Shehata HR, Lyons EM, Jordan KS, Raizada MN. Relevance of in vitro agar based screens to characterize the anti-fungal activities of bacterial endophyte communities. BMC Microbiol. 2016;16:1–7.CrossRef Shehata HR, Lyons EM, Jordan KS, Raizada MN. Relevance of in vitro agar based screens to characterize the anti-fungal activities of bacterial endophyte communities. BMC Microbiol. 2016;16:1–7.CrossRef
3.
4.
go back to reference Alvin A, Miller KI, Neilan BA. Exploring the potential of endophytes from medicinal plants as sources of antimycobacterial compounds. Microbiol Res. 2014;169:483–95.CrossRefPubMedPubMedCentral Alvin A, Miller KI, Neilan BA. Exploring the potential of endophytes from medicinal plants as sources of antimycobacterial compounds. Microbiol Res. 2014;169:483–95.CrossRefPubMedPubMedCentral
5.
go back to reference Pansanit A, Pripdeevech P. Antibacterial secondary metabolites from an endophytic fungus, Arthrinium sp. MFLUCC16-1053 isolated from Zingiber cassumunar. Mycology. 2018;9:264–72.CrossRefPubMedPubMedCentral Pansanit A, Pripdeevech P. Antibacterial secondary metabolites from an endophytic fungus, Arthrinium sp. MFLUCC16-1053 isolated from Zingiber cassumunar. Mycology. 2018;9:264–72.CrossRefPubMedPubMedCentral
6.
go back to reference Chen L, Zhang Q, Jia M, Ming Q, Yue W, Rahman K, Qin L. Endophytic fungi with antitumor activities: their occurrence and anticancer compounds. Crit Rev Microbiol. 2014;42:454–73.PubMed Chen L, Zhang Q, Jia M, Ming Q, Yue W, Rahman K, Qin L. Endophytic fungi with antitumor activities: their occurrence and anticancer compounds. Crit Rev Microbiol. 2014;42:454–73.PubMed
7.
go back to reference Iranbakhsh A, Oshagi MA, Majd A. Distribution of atropine and scopolamine in different organs and stages of development in Datura stramonium L. (Solanaceae). Structure and ultrastructure of biosynthesizing cells. Acta Biol Cracov Ser Bot. 2006;48:13–8. Iranbakhsh A, Oshagi MA, Majd A. Distribution of atropine and scopolamine in different organs and stages of development in Datura stramonium L. (Solanaceae). Structure and ultrastructure of biosynthesizing cells. Acta Biol Cracov Ser Bot. 2006;48:13–8.
8.
go back to reference Soni P, Siddiqui AA, Dwivedi J, Soni V. Pharmacological properties of Datura stramonium L. as a potential medicinal tree: an overview. J Pharmacogn Phytochem. 2012;2:1002–8. Soni P, Siddiqui AA, Dwivedi J, Soni V. Pharmacological properties of Datura stramonium L. as a potential medicinal tree: an overview. J Pharmacogn Phytochem. 2012;2:1002–8.
9.
go back to reference Chávez D, Cui B, Hee-Byung CHB, García R, Mejía M, Farnsworth NR, Cordell GA, Pezzuto JM, Kinghorn AD. Reversal of multidrug resistance by tropane alkaloids from the stems of Erythroxylum rotundifolium. J Nat Prod. 2002;65:606–10.CrossRefPubMed Chávez D, Cui B, Hee-Byung CHB, García R, Mejía M, Farnsworth NR, Cordell GA, Pezzuto JM, Kinghorn AD. Reversal of multidrug resistance by tropane alkaloids from the stems of Erythroxylum rotundifolium. J Nat Prod. 2002;65:606–10.CrossRefPubMed
10.
go back to reference Mahdi T, Mohamed I, Yagi S. Endophytic fungal communities associated with ethno-medicinal plants from Sudan and their antimicrobial and antioxidant prospective. J For Pro Ind. 2014;3:248–56. Mahdi T, Mohamed I, Yagi S. Endophytic fungal communities associated with ethno-medicinal plants from Sudan and their antimicrobial and antioxidant prospective. J For Pro Ind. 2014;3:248–56.
11.
go back to reference Aydi R, Abdallah B, Jabnoun-khiareddine H, Nefzi A, Mokni-tlili S, Daami-remadi M. Endophytic bacteria from Datura stramonium for Fusarium wilt suppression and tomato growth promotion. J Microb Biochem Technol. 2006;8:30–41. Aydi R, Abdallah B, Jabnoun-khiareddine H, Nefzi A, Mokni-tlili S, Daami-remadi M. Endophytic bacteria from Datura stramonium for Fusarium wilt suppression and tomato growth promotion. J Microb Biochem Technol. 2006;8:30–41.
12.
go back to reference Lou J, Yu R, Wang X, Mao Z, Fu L, Liu Y, Zhou L. Alternariol 9-methyl ether from the endophytic fungus Alternaria sp . Samif01 and its bioactivities. Brazi J Microbiol. 2016;47:96–101.CrossRef Lou J, Yu R, Wang X, Mao Z, Fu L, Liu Y, Zhou L. Alternariol 9-methyl ether from the endophytic fungus Alternaria sp . Samif01 and its bioactivities. Brazi J Microbiol. 2016;47:96–101.CrossRef
13.
go back to reference Christhudas IVSN, Kumar PP, Agastian P. Antimicrobial activity and HPLC analysis of tropane alkaloids in Streptomyces spp. isolated from Datura stramonium L. Asian J Pharm Clin Res. 2012;5:1–5. Christhudas IVSN, Kumar PP, Agastian P. Antimicrobial activity and HPLC analysis of tropane alkaloids in Streptomyces spp. isolated from Datura stramonium L. Asian J Pharm Clin Res. 2012;5:1–5.
14.
go back to reference Christhudas IVSN, Kumar PP, Agastian P. In vitro α-glucosidase inhibition and antioxidative potential of an endophyte species (Streptomyces sp. Loyola UGC) isolated from Datura stramonium L. Curr Microbiol. 2013;67:69–76.CrossRef Christhudas IVSN, Kumar PP, Agastian P. In vitro α-glucosidase inhibition and antioxidative potential of an endophyte species (Streptomyces sp. Loyola UGC) isolated from Datura stramonium L. Curr Microbiol. 2013;67:69–76.CrossRef
15.
go back to reference Uche-okereafor N, Sebola T, Tapfuma K, Mekuto K, Green E, Mavumengwana V. Antibacterial activities of crude secondary metabolite extracts from Pantoea species obtained from the stem of Solanum mauritianum and their effects on two cancer cell lines. Int J Env Res Public Heal. 2019;16:1–12. Uche-okereafor N, Sebola T, Tapfuma K, Mekuto K, Green E, Mavumengwana V. Antibacterial activities of crude secondary metabolite extracts from Pantoea species obtained from the stem of Solanum mauritianum and their effects on two cancer cell lines. Int J Env Res Public Heal. 2019;16:1–12.
16.
go back to reference Alsohaili SA, Bani-hasan BM. Morphological and molecular identification of fungi isolated from different environmental sources in the northern eastern desert of Jordan. Jordan J Biol Sci. 2018;11:329–37. Alsohaili SA, Bani-hasan BM. Morphological and molecular identification of fungi isolated from different environmental sources in the northern eastern desert of Jordan. Jordan J Biol Sci. 2018;11:329–37.
17.
18.
go back to reference Mcginnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 2004;32:20–5.CrossRef Mcginnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 2004;32:20–5.CrossRef
19.
go back to reference Jeewon R, Ittoo J, Mahadeb D, Jaufeerally-Fakim Y, Wang H-K, Liu A-R. DNA based identification and phylogenetic characterisation of endophytic and saprobic fungi from Antidesma madagascariense, a medicinal plant in Mauritius. J Mycol. 2013;2013:1–10.CrossRef Jeewon R, Ittoo J, Mahadeb D, Jaufeerally-Fakim Y, Wang H-K, Liu A-R. DNA based identification and phylogenetic characterisation of endophytic and saprobic fungi from Antidesma madagascariense, a medicinal plant in Mauritius. J Mycol. 2013;2013:1–10.CrossRef
20.
21.
go back to reference Tan X, Zhou Y, Zhou X, Xia X, Wei Y, He L, Tang H, Yu L. Diversity and bioactive potential of culturable fungal endophytes of Dysosma versipellis; a rare medicinal plant endemic to China. Sci Rep. 2018;8:1–9.CrossRef Tan X, Zhou Y, Zhou X, Xia X, Wei Y, He L, Tang H, Yu L. Diversity and bioactive potential of culturable fungal endophytes of Dysosma versipellis; a rare medicinal plant endemic to China. Sci Rep. 2018;8:1–9.CrossRef
22.
go back to reference Ikechi-Nwogu CG, Elenwo EN. Comparative evaluation of growth media for the cultivation of fungal cultures. J Plant Pathol Microbiol. 2012;3:3–6.CrossRef Ikechi-Nwogu CG, Elenwo EN. Comparative evaluation of growth media for the cultivation of fungal cultures. J Plant Pathol Microbiol. 2012;3:3–6.CrossRef
23.
go back to reference Frisvad JC, Larsen TO, Vries RD, Meijer M, Houbraken J, Cabañes FJ, Ehrlich K, Samson RA. Secondary metabolite profiling, growth profiles and other tools for species recognition and important Aspergillus mycotoxins. Stud Mycol. 2007;9:31–7.CrossRef Frisvad JC, Larsen TO, Vries RD, Meijer M, Houbraken J, Cabañes FJ, Ehrlich K, Samson RA. Secondary metabolite profiling, growth profiles and other tools for species recognition and important Aspergillus mycotoxins. Stud Mycol. 2007;9:31–7.CrossRef
24.
go back to reference Song J, Ma Q, Hu M, Qian D, Wang B, He N. The inhibition of miR-144-3p on cell proliferation and metastasis by targeting TOP2A in HCMV-positive glioblastoma cells. Molecules. 2018;23:1–13. Song J, Ma Q, Hu M, Qian D, Wang B, He N. The inhibition of miR-144-3p on cell proliferation and metastasis by targeting TOP2A in HCMV-positive glioblastoma cells. Molecules. 2018;23:1–13.
25.
go back to reference Handayani D, Rivai H, Mulyana R, Suharti N, Rasyid R, Hertiani T. Antimicrobial and cytotoxic activities of endophytic fungi isolated from mangrove plant Sonneratia alba Sm. J Appl Pharm Sci. 2018;8:49–53.CrossRef Handayani D, Rivai H, Mulyana R, Suharti N, Rasyid R, Hertiani T. Antimicrobial and cytotoxic activities of endophytic fungi isolated from mangrove plant Sonneratia alba Sm. J Appl Pharm Sci. 2018;8:49–53.CrossRef
26.
go back to reference Tapfuma KI, Mekuto L, Makatini MM, Mavumengwana V. The LC-QTOF-MS/MS analysis data of detected metabolites from the crude extract of Datura stramonium leaves. Data Br. 2019;25:1–4. Tapfuma KI, Mekuto L, Makatini MM, Mavumengwana V. The LC-QTOF-MS/MS analysis data of detected metabolites from the crude extract of Datura stramonium leaves. Data Br. 2019;25:1–4.
27.
go back to reference Changwa R, Abia W, Msagati T, Nyoni H, Ndleve K, Njobeh P. Multi-mycotoxin occurrence in dairy cattle feeds from the gauteng province of South Africa: A pilot study using UHPLC-QTOF-MS/MS. Toxins (Basel). 2018;10:1–21.CrossRef Changwa R, Abia W, Msagati T, Nyoni H, Ndleve K, Njobeh P. Multi-mycotoxin occurrence in dairy cattle feeds from the gauteng province of South Africa: A pilot study using UHPLC-QTOF-MS/MS. Toxins (Basel). 2018;10:1–21.CrossRef
28.
go back to reference Hoffmann T, Krug D, Hüttel S, Müller R. Improving natural products identification through targeted LC-MS/MS in an untargeted secondary metabolomics workflow. Anal Chem. 2014;86:10780–8.CrossRefPubMed Hoffmann T, Krug D, Hüttel S, Müller R. Improving natural products identification through targeted LC-MS/MS in an untargeted secondary metabolomics workflow. Anal Chem. 2014;86:10780–8.CrossRefPubMed
29.
go back to reference Ruttkies C, Schymanski EL, Wolf S, Hollender J, Neumann S. MetFrag relaunched: incorporating strategies beyond in silico fragmentation. J Cheminform. 2016;8:1–16.CrossRef Ruttkies C, Schymanski EL, Wolf S, Hollender J, Neumann S. MetFrag relaunched: incorporating strategies beyond in silico fragmentation. J Cheminform. 2016;8:1–16.CrossRef
30.
go back to reference Li P, Wu Z, Wang Y. Biodiversity, phylogeny, and antifungal functions of endophytic fungi associated with Zanthoxylum bungeanum. Int J Mol Sci. 2016;17:1–24. Li P, Wu Z, Wang Y. Biodiversity, phylogeny, and antifungal functions of endophytic fungi associated with Zanthoxylum bungeanum. Int J Mol Sci. 2016;17:1–24.
31.
go back to reference Gordon JL, Brown MA, Reynolds MM. Cell-based methods for determination of efficacy for candidate therapeutics in the clinical Management of Cancer. Diseases. 2018;6:1–13.CrossRef Gordon JL, Brown MA, Reynolds MM. Cell-based methods for determination of efficacy for candidate therapeutics in the clinical Management of Cancer. Diseases. 2018;6:1–13.CrossRef
32.
go back to reference Wang P, Henning SM, Heber D. Limitations of MTT and MTS-based assays for measurement of antiproliferative activity of green tea polyphenols. PLoS One. 2010;5:1–10.CrossRef Wang P, Henning SM, Heber D. Limitations of MTT and MTS-based assays for measurement of antiproliferative activity of green tea polyphenols. PLoS One. 2010;5:1–10.CrossRef
33.
go back to reference Steenkamp V, Gouws MC. Cytotoxicity of six south African medicinal plant extracts used in the treatment of cancer. SA J Bot. 2006;72:630–3.CrossRef Steenkamp V, Gouws MC. Cytotoxicity of six south African medicinal plant extracts used in the treatment of cancer. SA J Bot. 2006;72:630–3.CrossRef
34.
go back to reference Suffness M, Pezzuto JM. Assays related to cancer drug discovery. In: Hostettmann K, editor. Methods in plant biochemistry: assays for bioactivity, vol. 6. London: Academic Press; 1990. p. 71–133. Suffness M, Pezzuto JM. Assays related to cancer drug discovery. In: Hostettmann K, editor. Methods in plant biochemistry: assays for bioactivity, vol. 6. London: Academic Press; 1990. p. 71–133.
35.
go back to reference Haar CP, Hebbar P, Wallace GC IV, Das A, Vandergrift WA III, Smith JA, Giglio P, Patel SJ, Ray SK, Banik NL. Drug resistance in glioblastoma: A mini review. Neurochem Res. 2012;37:1192–200.CrossRefPubMedPubMedCentral Haar CP, Hebbar P, Wallace GC IV, Das A, Vandergrift WA III, Smith JA, Giglio P, Patel SJ, Ray SK, Banik NL. Drug resistance in glioblastoma: A mini review. Neurochem Res. 2012;37:1192–200.CrossRefPubMedPubMedCentral
36.
go back to reference Wolf S, Schmidt S, Müller-hannemann M, Neumann S. In silico fragmentation for computer assisted identification of metabolite mass spectra. BMC Bioinformatics. 2010;11:1–12.CrossRef Wolf S, Schmidt S, Müller-hannemann M, Neumann S. In silico fragmentation for computer assisted identification of metabolite mass spectra. BMC Bioinformatics. 2010;11:1–12.CrossRef
37.
go back to reference Stierle A, Strobel G, Stierle S, Grothaus P, Bignami G. The search for a taxol-producing microorganism among the endophytic fungi of the Pacific yew. Taxus brevifolia J Nat Prod. 1995;58:1315–24.CrossRefPubMed Stierle A, Strobel G, Stierle S, Grothaus P, Bignami G. The search for a taxol-producing microorganism among the endophytic fungi of the Pacific yew. Taxus brevifolia J Nat Prod. 1995;58:1315–24.CrossRefPubMed
38.
go back to reference Ramalashmi K, Prasanna VK, Magesh K, Sanjana R, Siril JS. A potential surface sterilization technique and culture media for the isolation of endophytic bacteria from Acalypha indica and its antibacterial activity. J Med Plant Stud. 2018;6:181–4. Ramalashmi K, Prasanna VK, Magesh K, Sanjana R, Siril JS. A potential surface sterilization technique and culture media for the isolation of endophytic bacteria from Acalypha indica and its antibacterial activity. J Med Plant Stud. 2018;6:181–4.
39.
go back to reference Sun J, Awakawa T, Noguchi H, Abe I. Induced production of mycotoxins in an endophytic fungus from the medicinal plant Datura stramonium L. Bioorg Med Chem Lett. 2012;22:6397–400.CrossRefPubMed Sun J, Awakawa T, Noguchi H, Abe I. Induced production of mycotoxins in an endophytic fungus from the medicinal plant Datura stramonium L. Bioorg Med Chem Lett. 2012;22:6397–400.CrossRefPubMed
40.
go back to reference Puntscher H, Hankele S, Tillmann K, Attakpah E, Braun D, Kütt M, Del G, Aichinger G, Pahlke G, Höger H, Marko D, Warth B. First insights into Alternaria multi-toxin in vivo metabolism. Toxicol Lett. 2019;301:168–78.CrossRefPubMed Puntscher H, Hankele S, Tillmann K, Attakpah E, Braun D, Kütt M, Del G, Aichinger G, Pahlke G, Höger H, Marko D, Warth B. First insights into Alternaria multi-toxin in vivo metabolism. Toxicol Lett. 2019;301:168–78.CrossRefPubMed
41.
go back to reference Akimitsu K, Tsuge T, Kodama M, Yamamoto M, Otani H. Alternaria host-selective toxins: determinant factors of plant disease. J Gen Plant Pathol. 2014;80:109–22.CrossRef Akimitsu K, Tsuge T, Kodama M, Yamamoto M, Otani H. Alternaria host-selective toxins: determinant factors of plant disease. J Gen Plant Pathol. 2014;80:109–22.CrossRef
42.
go back to reference Thomma BPHJ. Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol. 2003;4:225–36.CrossRefPubMed Thomma BPHJ. Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol. 2003;4:225–36.CrossRefPubMed
43.
go back to reference Elgorban AM, Bahkali AH, Abdel-Wahab MA. Natural products of Alternaria sp., an endophytic fungus isolated from Salvadora persica from Saudi Arabia. Saudi J Biol Sci. 2018;xx:1–10. Elgorban AM, Bahkali AH, Abdel-Wahab MA. Natural products of Alternaria sp., an endophytic fungus isolated from Salvadora persica from Saudi Arabia. Saudi J Biol Sci. 2018;xx:1–10.
44.
go back to reference Yuan ZL, Zhang CL, LiN FC, Kubicek CP. Identity, diversity, and molecular phylogeny of the endophytic mycobiota in the roots of rare wild rice (Oryza granulate) from a nature reserve in Yunnan. China Appl Env Microbiol. 2010;76:1642–52.CrossRef Yuan ZL, Zhang CL, LiN FC, Kubicek CP. Identity, diversity, and molecular phylogeny of the endophytic mycobiota in the roots of rare wild rice (Oryza granulate) from a nature reserve in Yunnan. China Appl Env Microbiol. 2010;76:1642–52.CrossRef
45.
go back to reference Chand R, Kumar M, Kushwaha C, Shah K, Joshi AK. Role of melanin in release of extracellular enzymes and selection of aggressive isolates of Bipolaris sorokiniana in barley. Curr Microbiol. 2014;69:202–11.CrossRefPubMed Chand R, Kumar M, Kushwaha C, Shah K, Joshi AK. Role of melanin in release of extracellular enzymes and selection of aggressive isolates of Bipolaris sorokiniana in barley. Curr Microbiol. 2014;69:202–11.CrossRefPubMed
46.
go back to reference Li X, He X, Hou L, Ren Y, Wang S, Su F. Dark septate endophytes isolated from a xerophyte plant promote the growth of Ammopiptanthus mongolicus under drought condition. Sci Rep. 2018;8:1–11.CrossRef Li X, He X, Hou L, Ren Y, Wang S, Su F. Dark septate endophytes isolated from a xerophyte plant promote the growth of Ammopiptanthus mongolicus under drought condition. Sci Rep. 2018;8:1–11.CrossRef
47.
go back to reference Dufossé L. Microbial production of food grade pigments. Food Technol Biotech. 2006;44:313–21. Dufossé L. Microbial production of food grade pigments. Food Technol Biotech. 2006;44:313–21.
48.
go back to reference Venkatachalam M, Zelena M, Cacciola F, Ceslova L, Girard-valenciennes E, Clerc P, Dugo P, Mondello L, Fouillaud M, Rotondo A, Giu D, Dufossé L. Partial characterization of the pigments produced by the marine-derived fungus Talaromyces albobiverticillius 30548. Towards a new fungal red colorant for the food industry. J Food Compost Anal. 2018;67:8–47.CrossRef Venkatachalam M, Zelena M, Cacciola F, Ceslova L, Girard-valenciennes E, Clerc P, Dugo P, Mondello L, Fouillaud M, Rotondo A, Giu D, Dufossé L. Partial characterization of the pigments produced by the marine-derived fungus Talaromyces albobiverticillius 30548. Towards a new fungal red colorant for the food industry. J Food Compost Anal. 2018;67:8–47.CrossRef
49.
go back to reference Zhang X, Selvaraju K, Saei AA, D'Arcy P, Zubarev RA, Arnér ES, Linder S. Repurposing of auranofin: thioredoxin reductase remains a primary target of the drug. Biochimie. 2019;162:46–54.CrossRefPubMed Zhang X, Selvaraju K, Saei AA, D'Arcy P, Zubarev RA, Arnér ES, Linder S. Repurposing of auranofin: thioredoxin reductase remains a primary target of the drug. Biochimie. 2019;162:46–54.CrossRefPubMed
50.
go back to reference Lee JE, Kwon YJ, Baek HS, Ye DJ, Cho E, Choi HK, Oh KS, Chun YJ. Synergistic induction of apoptosis by combination treatment with mesupron and auranofin in human breast cancer cells. Arch Pharm Res. 2017;40:746–59.CrossRefPubMed Lee JE, Kwon YJ, Baek HS, Ye DJ, Cho E, Choi HK, Oh KS, Chun YJ. Synergistic induction of apoptosis by combination treatment with mesupron and auranofin in human breast cancer cells. Arch Pharm Res. 2017;40:746–59.CrossRefPubMed
51.
go back to reference Ye DJ, Kwon YJ, Baek HS, Cho E, Kwon TU, Chun YJ. Combination treatment with auranofin and nutlin-3a induces synergistic cytotoxicity in breast cancer cells. J Toxicol Environ Heal A. 2019;82:626–37.CrossRef Ye DJ, Kwon YJ, Baek HS, Cho E, Kwon TU, Chun YJ. Combination treatment with auranofin and nutlin-3a induces synergistic cytotoxicity in breast cancer cells. J Toxicol Environ Heal A. 2019;82:626–37.CrossRef
52.
go back to reference Hwang-Bo H, Lee WS, Nagappan A, Kim HJ, Panchanathan R, Park C, Chang SH, Kim ND, Leem SH, Chang YC, Kwon TK, Cheong JH, Kim GS, Jung JM, Shin SC, Hong SC, Choi YH. Morin enhances auranofin anticancer activity by up-regulation of DR4 and DR5 and modulation of Bcl-2 through reactive oxygen species generation in Hep3B human hepatocellular carcinoma cells. Phytother Res. 2019;33:1384–93.CrossRefPubMed Hwang-Bo H, Lee WS, Nagappan A, Kim HJ, Panchanathan R, Park C, Chang SH, Kim ND, Leem SH, Chang YC, Kwon TK, Cheong JH, Kim GS, Jung JM, Shin SC, Hong SC, Choi YH. Morin enhances auranofin anticancer activity by up-regulation of DR4 and DR5 and modulation of Bcl-2 through reactive oxygen species generation in Hep3B human hepatocellular carcinoma cells. Phytother Res. 2019;33:1384–93.CrossRefPubMed
53.
go back to reference Liu N, Guo Z, Xia X, Liao Y, Zhang F, Huang C, Liu Y, Deng X, Jiang L, Wang X, Liu J, Huang H. Auranofin lethality to prostate cancer includes inhibition of proteasomal deubiquitinases and disrupted androgen receptor signaling. Eur J Pharmacol. 2019;846:1–11.CrossRefPubMed Liu N, Guo Z, Xia X, Liao Y, Zhang F, Huang C, Liu Y, Deng X, Jiang L, Wang X, Liu J, Huang H. Auranofin lethality to prostate cancer includes inhibition of proteasomal deubiquitinases and disrupted androgen receptor signaling. Eur J Pharmacol. 2019;846:1–11.CrossRefPubMed
54.
go back to reference Park SH, Lee JH, Berek JS, Hu MC. Auranofin displays anticancer activity against ovarian cancer cells through FOXO3 activation independent of p53. Int J Oncol. 2014;45:1691–8.CrossRefPubMedPubMedCentral Park SH, Lee JH, Berek JS, Hu MC. Auranofin displays anticancer activity against ovarian cancer cells through FOXO3 activation independent of p53. Int J Oncol. 2014;45:1691–8.CrossRefPubMedPubMedCentral
55.
go back to reference Han Y, Chen P, Zhang Y, Lu W, Ding W, Luo Y, Wen S, Xu R, Liu P, Huang P. Synergy between auranofin and celecoxib against colon cancer in vitro and in vivo through a novel redox-mediated mechanism. Cancers. 2019;11:1–18.CrossRef Han Y, Chen P, Zhang Y, Lu W, Ding W, Luo Y, Wen S, Xu R, Liu P, Huang P. Synergy between auranofin and celecoxib against colon cancer in vitro and in vivo through a novel redox-mediated mechanism. Cancers. 2019;11:1–18.CrossRef
56.
go back to reference Skaga E, Skaga IØ, Grieg Z, Sandberg CJ, Langmoen IA, Mo EOV. The efficacy of a coordinated pharmacological blockade in glioblastoma stem cells with nine repurposed drugs using the CUSP9 strategy. J Cancer Res Clin Oncol. 2019;145:1495–507.CrossRefPubMedPubMedCentral Skaga E, Skaga IØ, Grieg Z, Sandberg CJ, Langmoen IA, Mo EOV. The efficacy of a coordinated pharmacological blockade in glioblastoma stem cells with nine repurposed drugs using the CUSP9 strategy. J Cancer Res Clin Oncol. 2019;145:1495–507.CrossRefPubMedPubMedCentral
57.
go back to reference Li H, Hu J, Wu S, Wang L, Cao X, Zhang X, Dai B, Cao M, Shao R, Zhang R, Majidi M, Ji L, Heymach JV, Wang M, Pan S, Minna J, Mehran RJ, Swisher SG, Roth JA, Fang B. Auranofin-mediated inhibition of PI3K/AKT/mTOR axis and anticancer activity in non-small cell lung cancer cells. Oncotarget. 2016;7:3548–58.PubMed Li H, Hu J, Wu S, Wang L, Cao X, Zhang X, Dai B, Cao M, Shao R, Zhang R, Majidi M, Ji L, Heymach JV, Wang M, Pan S, Minna J, Mehran RJ, Swisher SG, Roth JA, Fang B. Auranofin-mediated inhibition of PI3K/AKT/mTOR axis and anticancer activity in non-small cell lung cancer cells. Oncotarget. 2016;7:3548–58.PubMed
58.
go back to reference Sone Y, Nakamura S, Sasaki M, Hasebe F, Kim S-Y, Funa N. Bacterial enzymes catalyzing the synthesis of 1,8-dihydroxynaphthalene, a key precursor of dihydroxynaphthalene melanin, from Sorangium cellulosum. Appl Env Microbiol. 2018;84:1–13.CrossRef Sone Y, Nakamura S, Sasaki M, Hasebe F, Kim S-Y, Funa N. Bacterial enzymes catalyzing the synthesis of 1,8-dihydroxynaphthalene, a key precursor of dihydroxynaphthalene melanin, from Sorangium cellulosum. Appl Env Microbiol. 2018;84:1–13.CrossRef
59.
60.
go back to reference Fernandes C, Prados-rosales R, Silva BMA, Nakouzi-naranjo A, Zuzarte M, Chatterjee S, Stark RE, Casadevall A, Gonçalves T. Activation of melanin synthesis in Alternaria infectoria by antifungal drugs. Antimicrob Agents Chemother. 2016;60:1646–55.CrossRefPubMedCentral Fernandes C, Prados-rosales R, Silva BMA, Nakouzi-naranjo A, Zuzarte M, Chatterjee S, Stark RE, Casadevall A, Gonçalves T. Activation of melanin synthesis in Alternaria infectoria by antifungal drugs. Antimicrob Agents Chemother. 2016;60:1646–55.CrossRefPubMedCentral
61.
go back to reference Raman NM, Ramasamy S. Genetic validation and spectroscopic detailing of DHN-melanin extracted from an environmental fungus. Biochem Biophys Rep. 2017;12:98–107.PubMedPubMedCentral Raman NM, Ramasamy S. Genetic validation and spectroscopic detailing of DHN-melanin extracted from an environmental fungus. Biochem Biophys Rep. 2017;12:98–107.PubMedPubMedCentral
62.
go back to reference Wang HJ, Gloer KB, Gloer JB, Scott JA, Malloch D. Anserinones a and B: new antifungal and antibacterial benzoquinones from the coprophilous fungus Podospora anserina. J Nat Prod. 1997;60:629–31.CrossRefPubMed Wang HJ, Gloer KB, Gloer JB, Scott JA, Malloch D. Anserinones a and B: new antifungal and antibacterial benzoquinones from the coprophilous fungus Podospora anserina. J Nat Prod. 1997;60:629–31.CrossRefPubMed
63.
go back to reference Sarrocco S. Dung-inhabiting fungi: a potential reservoir of novel secondary metabolites for the control of plant pathogens. Pest Manag Sci. 2016;72:643–52.CrossRefPubMed Sarrocco S. Dung-inhabiting fungi: a potential reservoir of novel secondary metabolites for the control of plant pathogens. Pest Manag Sci. 2016;72:643–52.CrossRefPubMed
64.
go back to reference Shoemaker RH. Major events in the development, implementation and use of the NCI60 cell lines. Nat Rev Cancer. 2006;6:813–24.CrossRefPubMed Shoemaker RH. Major events in the development, implementation and use of the NCI60 cell lines. Nat Rev Cancer. 2006;6:813–24.CrossRefPubMed
65.
go back to reference Dewick PM. Medicinal natural products: a biosynthetic approach. 2nd ed. West Sussex: John Wiley & Sons Ltd; 2002. Dewick PM. Medicinal natural products: a biosynthetic approach. 2nd ed. West Sussex: John Wiley & Sons Ltd; 2002.
66.
go back to reference Silva DDD, Rapior S, Sudarman E, Hyde KD. Bioactive metabolites from macrofungi: ethnopharmacology, biological activities and chemistry. Fungal Divers. 2013;62:1–40.CrossRef Silva DDD, Rapior S, Sudarman E, Hyde KD. Bioactive metabolites from macrofungi: ethnopharmacology, biological activities and chemistry. Fungal Divers. 2013;62:1–40.CrossRef
67.
go back to reference Iijima M, Masuda T, Nakamura H, Naganawa H, Okami Y, Ishizuka M, Takeuchi T. Metacytofilin, a novel immunomodulator produced by Metarhizium sp. TA2759. J Antibiot. 1992;45:1553–6.CrossRef Iijima M, Masuda T, Nakamura H, Naganawa H, Okami Y, Ishizuka M, Takeuchi T. Metacytofilin, a novel immunomodulator produced by Metarhizium sp. TA2759. J Antibiot. 1992;45:1553–6.CrossRef
68.
go back to reference Wang X, Gong X, Li P, Lai D. Structural diversity and biological activities of cyclic depsipeptides from fungi. Molecules. 2018;23:1–49. Wang X, Gong X, Li P, Lai D. Structural diversity and biological activities of cyclic depsipeptides from fungi. Molecules. 2018;23:1–49.
69.
go back to reference Namikoshi M, Kobayashi H, Yoshimoto T, Hosoya T. Phomopsidin, a new inhibitor of microtubule assembly produced by Phomopsis sp. isolated from coral reef in Pohnpei. J Antibiot. 1997;50:890–2.CrossRef Namikoshi M, Kobayashi H, Yoshimoto T, Hosoya T. Phomopsidin, a new inhibitor of microtubule assembly produced by Phomopsis sp. isolated from coral reef in Pohnpei. J Antibiot. 1997;50:890–2.CrossRef
70.
go back to reference Liang ZQ, Cao N, Song ZK, Wang X. In vitro porcine brain tubulin assembly inhibition by water extract from a Chinese medicinal herb, Tripterygium hypoglaucum hutch. World J Gastroenterol. 2006;12:1133–5.CrossRefPubMedPubMedCentral Liang ZQ, Cao N, Song ZK, Wang X. In vitro porcine brain tubulin assembly inhibition by water extract from a Chinese medicinal herb, Tripterygium hypoglaucum hutch. World J Gastroenterol. 2006;12:1133–5.CrossRefPubMedPubMedCentral
71.
go back to reference Wu B, Ohlendorf B, Oesker V, Wiese J, Malien S, Schmaljohann R, Imhoff JF. Acetylcholinesterase inhibitors from a marine fungus Talaromyces sp. strain LF458. Mar Biotechnol. 2014;17:110–9.CrossRef Wu B, Ohlendorf B, Oesker V, Wiese J, Malien S, Schmaljohann R, Imhoff JF. Acetylcholinesterase inhibitors from a marine fungus Talaromyces sp. strain LF458. Mar Biotechnol. 2014;17:110–9.CrossRef
72.
go back to reference Nicoletti R, Ciavatta LM, Buommino E, Tufano MA. Antitumor extrolites produced by Penicillium species. Int J Biomed Pharm Sci. 2008;2:1–23. Nicoletti R, Ciavatta LM, Buommino E, Tufano MA. Antitumor extrolites produced by Penicillium species. Int J Biomed Pharm Sci. 2008;2:1–23.
73.
go back to reference Escrivá L, Oueslati S, Font G, Manyes L. Alternaria mycotoxins in food and feed: an overview. J Food Qual. 2017;2017:1–20.CrossRef Escrivá L, Oueslati S, Font G, Manyes L. Alternaria mycotoxins in food and feed: an overview. J Food Qual. 2017;2017:1–20.CrossRef
74.
go back to reference Vadlapudi V, Borah N, Yellusani KR, Gade S, Reddy P, Rajamanikyam M, Vempati LNS, Gubbala SP, Chopra P, Upadhyayula SM, Amanchy R. Aspergillus secondary metabolite database, a resource to understand the secondary metabolome of Aspergillus genus. Sci Rep. 2017;7:1–10.CrossRef Vadlapudi V, Borah N, Yellusani KR, Gade S, Reddy P, Rajamanikyam M, Vempati LNS, Gubbala SP, Chopra P, Upadhyayula SM, Amanchy R. Aspergillus secondary metabolite database, a resource to understand the secondary metabolome of Aspergillus genus. Sci Rep. 2017;7:1–10.CrossRef
75.
go back to reference Van Ngo T, Scarlett CJ, Bowyer MC, Ngo PD, Van Vuong Q. Impact of different extraction solvents on bioactive compounds and antioxidant capacity from the root of Salacia chinensis L. J Food Qual. 2017;2017:1–8.CrossRef Van Ngo T, Scarlett CJ, Bowyer MC, Ngo PD, Van Vuong Q. Impact of different extraction solvents on bioactive compounds and antioxidant capacity from the root of Salacia chinensis L. J Food Qual. 2017;2017:1–8.CrossRef
76.
go back to reference Samiee SM, Moazami N, Haghighi S, Mohseni FA, Bakhtiari MR. Screening of lovastatin production by filamentous fungi. Iran Biomed J. 2003;7:29–33. Samiee SM, Moazami N, Haghighi S, Mohseni FA, Bakhtiari MR. Screening of lovastatin production by filamentous fungi. Iran Biomed J. 2003;7:29–33.
Metadata
Title
Cytotoxic activity of crude extracts from Datura stramonium’s fungal endophytes against A549 lung carcinoma and UMG87 glioblastoma cell lines and LC-QTOF-MS/MS based metabolite profiling
Publication date
01-12-2019
Published in
BMC Complementary Medicine and Therapies / Issue 1/2019
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-019-2752-9

Other articles of this Issue 1/2019

BMC Complementary Medicine and Therapies 1/2019 Go to the issue