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Biologically Active Metabolites from Hungarian Mushrooms

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Biologically Active Metabolites from Hungarian Mushrooms University of Szeged Faculty of Pharmacy Graduate School of Pharmaceutical Sciences Department of Pharmacognosy From cyclic peptides to terphenyl quinones: biologically active metabolites from Hungarian mushrooms Ph.D. Thesis Bernadett Kovács Supervisors: Prof. Judit Hohmann Dr. Attila Ványolós Szeged, Hungary 2018 LIST OF PUBLICATIONS RELEATED TO THE THESIS I. Béni Z, Dékány M, Kovács B, Csupor-Löffler B, Zomborszki ZP, Kerekes E, Szekeres A, Urbán E, Hohmann J, Ványolós A Bioactivity-guided Isolation of Antibacterial and Antioxidant Metabolites from Tapinella atrotomentosa Molecules 23, 1082 (2018) II. Kovács B, Béni Z, Dékány M, Bózsity N, Zupkó I, Hohmann J, Ványolós A Isolation and Structure Determination of Antiproliferative Secondary Metabolites from the Potato Earthball Mushroom, Scleroderma bovista (Agaricomycetes). International Journal of Medicinal Mushrooms 20:(5) pp. 411-418. (2018) III. Kovács B, Béni Z, Dékány M, Orbán-Gyapai O, Sinka I, Zupkó I, Hohmann J, Ványolós A Chemical Analysis of the Edible Mushroom Tricholoma populinum: Steroids and Sulfyniladenosine Compounds Natural Product Communications 12:(10) pp. 1583-1584. (2017) IV. Ványolós A, Dékány M, Kovács B, Krámos B, Bérdi P, Zupkó I, Hohmann J, Béni Z Gymnopeptides A and B, Cyclic Octadecapeptides from the Mushroom Gymnopus fusipes Organic Letters 18:(11) pp. 2688-2691. (2016) V. Liktor-Busa E, Kovács B, Urbán E, Hohmann J, Ványolós A Investigation of Hungarian Mushrooms for Antibacterial Activity and Synergistic Effects with Standard Antibiotics against Resistant Bacterial Strains Letters in Applied Microbiology 62:(6) pp. 437-443. (2016) VI. Ványolós A, Kovács B, Bózsity N, Zupkó I, Hohmann J Antiproliferative Activity of Some Higher Mushrooms from Hungary against Human Cancer Cell Lines International Journal of Medicinal Mushrooms 17:(12) pp. 1145-1149. (2015) TABLE OF CONTENTS ABBREVIATIONS AND SYMBOLS ...................................................................................... 1 1. INTRODUCTION .................................................................................................................. 2 2. AIMS OF THE STUDY ......................................................................................................... 5 3. LITERATURE OVERVIEW ................................................................................................. 6 3.1. MORPHOLOGY AND CHEMISTRY OF INVESTIGATED SPECIES ...................... 6 3.1.1. Morphology and chemistry of Gymnopus fusipes .................................................... 6 3.1.2. Morphology and chemistry of Tricholoma populinum ............................................. 6 3.1.3. Morphology and chemistry of Scleroderma bovista ................................................. 7 3.1.4. Morphology and chemistry of Tapinella atrotomentosa .......................................... 8 4. MATERIALS AND METHODS ......................................................................................... 10 4.1. MUSHROOM MATERIALS ........................................................................................ 10 4.2. EXTRACTION .............................................................................................................. 11 4.2.1. Preparation of extracts for pharmacological screening ........................................... 11 4.2.2. Extraction of the mushroom materials for preparative work .................................. 11 4.3. PURIFICATION AND ISOLATION OF THE COMPOUNDS .................................. 12 4.3.1. Open-column chromatography (OCC) ................................................................... 12 4.3.2. Rotational planar chromatography (RPC) .............................................................. 12 4.3.3. Flash column chromatography (FCC)..................................................................... 12 4.3.4. High-performance liquid chromatography (HPLC) ................................................ 13 4.4. STRUCTURE DETERMINATION OF ISOLATED COMPOUNDS ......................... 14 4.5. MARFEY’S ANALYSIS (Hydrolysis and derivatization) ........................................... 15 4.6. LC-MS INVESTIGATION OF AMINO ACIDS ......................................................... 15 4.7. MOLECULAR MODELING ........................................................................................ 15 4.8. PHARMACOLOGICAL ASSAYS ............................................................................... 15 4.8.1. In vitro antiproliferative investigations (MTT assay) ............................................. 15 4.8.2. In vitro antimicrobial investigations of mushroom extracts ................................... 16 4.8.3. In vitro antimicrobial investigations of the isolated compounds ............................ 18 4.8.4. In vitro xanthine oxidase inhibitory investigation .................................................. 19 4.8.5. In vitro antioxidant activity investigation ............................................................... 20 5. RESULTS ............................................................................................................................. 21 5.1. SCREENING OF MUSHROOM SPECIES FOR ANTIPROLIFERATIVE ACTIVITY .............................................................................................................................................. 21 5.2. SCREENING OF MUSHROOM SPECIES FOR ANTIMICROBIAL ACTIVITY .... 21 5.3. ISOLATION OF COMPOUNDS FROM THE INVESTIGATED SPECIES .............. 24 5.3.1. Isolation of the compounds of G. fusipes ................................................................ 24 5.3.2. Isolation of the compounds of T. populinum .......................................................... 24 5.3.3. Isolation of the compounds of S. bovista ................................................................ 26 5.3.4. Isolation of the compounds of T. atrotomentosa .................................................... 27 5.4. CHARACTERIZATION AND STRUCTURE DETERMINATION OF THE ISOLATED COMPOUNDS ................................................................................................. 28 5.4.1. Compounds from the chloroform extract of G. fusipes .......................................... 28 5.4.2. Compounds from T. populinum .............................................................................. 31 5.4.3. Compounds from S. bovista .................................................................................... 32 5.4.4. Compounds from the chloroform extract of T. atrotomentosa ............................... 32 5.5. PHARMACOLOGICAL ACTIVITIES OF THE ISOLATED COMPOUNDS .......... 33 5.5.1. Antiproliferative effect of the cyclopeptides of G. fusipes ..................................... 33 5.5.2. Biological activity of the compounds of T. populium ............................................. 33 5.5.3. Antiproliferative activity of the secondary metabolites of S. bovista ..................... 34 5.5.4. Bioactivity of the compounds of T. atrotomentosa ................................................ 34 6. DISCUSSION ...................................................................................................................... 36 6.1. SCREENING STUDIES ............................................................................................... 36 6.2. INVESTIGATION OF G. FUSIPES, T. POPULINUM, S. BOVISTA, T. ATROTOMENTOSA ......................................................................................................... 37 6.3. ISOLATION OF THE BIOACTIVE COMPOUNDS .................................................. 37 6.4. STRUCTURE ELUCIDATION .................................................................................... 38 6.4.1. Cyclopeptides from Gymnopus fusipes ................................................................... 38 6.4.2. Steroids and sulfinyladenosine compounds from Tricholoma populinum.............. 39 6.4.3. Ceramide- and steroid-type compounds from Scleroderma bovista ....................... 40 6.4.4. Lactone and terphenylquinone derivatives from Tapinella atrotomentosa ............ 41 6.5. BIOLOGICAL ACTIVITIES OF THE COMPOUNDS OF THE INVESTIGATED SPECIES ............................................................................................................................... 42 7. SUMMARY ......................................................................................................................... 46 8. REFERENCES ..................................................................................................................... 48 ABBREVIATIONS AND SYMBOLS 1D one-dimensional 2D two-dimensional A2780 ovarian carcinoma cells A431 human skin epidermoid carcinoma cells AA amino acids COSY correlated spectroscopy δ chemical shift ESBL extended-spectrum beta-lactamase ESI–MS electrospray ionization mass spectrometry FCC flash column chromatography HeLa human cervix adenocarcinoma HMBC heteronuclear multiple-bond correlation spectroscopy HPLC high-performance liquid chromatography HR–MS high-resolution mass spectrometry HSQC heteronuclear single-quantum coherence spectroscopy JMOD J-modulated spin-echo experiment MCF-7 human breast adenocarcinoma cells MS mass spectrometry MTT 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide NMR nuclear magnetic resonance NOE nuclear Overhauser effect NOESY nuclear Overhauser effect spectroscopy NP normal-phase OCC open-column chromatography ROESY rotating-frame nuclear Overhauser effect correlation spectroscopy RP reversed-phase RPC
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