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Metabolite Profiling and Fingerprinting of Hypericum Species: a Comparison of MS and NMR Metabolomics

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Metabolite Profiling and Fingerprinting of Hypericum Species: a Comparison of MS and NMR Metabolomics Metabolomics (2014) 10:574–588 DOI 10.1007/s11306-013-0609-7 ORIGINAL ARTICLE Metabolite profiling and fingerprinting of Hypericum species: a comparison of MS and NMR metabolomics Andrea Porzel • Mohamed A. Farag • Julia Mu¨lbradt • Ludger A. Wessjohann Received: 16 August 2013 / Accepted: 15 November 2013 / Published online: 7 December 2013 Ó Springer Science+Business Media New York 2013 Abstract Hypericum perforatum, commonly known as comparable score plots in principal component analysis St. John’s wort, is a popular herbal supplement used for the were derived from both MS and NMR datasets, loading treatment of mild to moderate depression. The major sec- plots reveal, that different set of metabolites contribute for ondary metabolites of St. John’s wort extracts include species segregation in each dataset. Major peaks in 1H phenylpropanoids, flavonoids, xanthones, phloroglucinols, NMR and MS spectra contributing to species discrimina- and naphthodianthrones. There are over 400 species in the tion were assigned as those of hyperforins, lipids, chloro- genus Hypericum world-wide, most of which are little or genic and shikimic acid. Shikimic acid and its downstream not characterized in terms of phytochemical or pharma- phenylpropanoids were more enriched in H. perforatum, H. cological properties. Metabolomics techniques were used androsaemum, H. kouytchense and H. inodorum extracts; to investigate the natural product diversity within the genus whereas a novel hyperforin was found exclusively in H. Hypericum (Hypericaceae) and its correlation to bioactiv- polyphyllum. Next to H. perforatum, H. polyphyllum and ity, exemplified by cytotoxic properties. Utilizing nuclear H. tetrapterum show the highest levels of hypericins, and magnetic resonance (NMR) fingerprinting and mass spec- H. perforatum and H. polyphyllum are highest in trometry (MS) metabolic profiling techniques, MS and phloroglucinols, suggesting that the latter species might be NMR spectra of extracts from H. perforatum, H. poly- used as an alternative to St. John’s wort. However, the phyllum, H. tetrapterum, H. androsaemum, H. inodorum, major hyperforin-type compound in H. polyphyllum pos- H. undulatum and H. kouytchense were evaluated and sesses a novel constitution of yet unknown bioactivity. submitted to statistical multivariate analyses. Although Anti-cancer in vitro assays to evaluate the ability of extracts from Hypericum species in inhibiting prostate and colon cancer growth suggest that such bioactivity might be predicted by gross metabolic profiling. Electronic supplementary material The online version of this article (doi:10.1007/s11306-013-0609-7) contains supplementary Keywords H. perforatum Á H. polyphyllum Á material, which is available to authorized users. 1H NMR-based metabolomics Á LC–MS Á Hyperforin Á Anticancer activity prediction A. Porzel Á M. A. Farag Á J. Mu¨lbradt Á L. A. Wessjohann (&) Department of Bioorganic Chemistry, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120 Halle (Saale), Germany Abbreviations e-mail: [email protected] ESI Electrospray ionisation LC Liquid chromatography M. A. Farag Pharmacognosy Department, College of Pharmacy, Cairo MS Mass spectrometry University, Kasr El Aini St., P.B. 11562, Cairo, Egypt MSn Tandem mass spectrometry NMR Nuclear magnetic resonance Present Address: PDA Photodiode array detection J. Mu¨lbradt FB Biologie/Chemie, Universita¨t Bremen, NW2/Leobener Str., PCA Principal component analysis 28359 Bremen, Germany HCA Hierarchical cluster analysis 123 A comparison of MS and NMR metabolomics 575 1 Introduction annulatophenone, hypericophenonoside, otogirin, itali- dipyrone, chinesins, and sampsonines (Hillwig et al. 2008). In recent years, the use of herbs as dietary supplements has With regard to the concentrations of active components, increased dramatically in many countries. The World significant differences were found between different spe- Health Organization estimates (WHO Fact sheet No. 134, cies in Hypericum (Umek et al. 1999; Kitanov 2001). December 2008) that up to 80 % of the world’s population The increasing attention on St. John’s wort relies on its relies on traditional medicinal systems, and in many of efficacy as an antidepressant medicine, which has been these, herbal medicines play a key role in human health. demonstrated in numerous clinical trials challenging the Among these products, Hypericum perforatum (St. John’s conventional tricyclic antidepressants (Fornal et al. 2001; wort) is a very popular phytomedicine, recognized as one Gobbi and Mennini 2001). The antidepressant activity of of the top five herb remedies (Giese 1999). H. perforatum H. perforatum was first attributed to naphthodianthrones has been reported as an antidepressant, antiviral, antimi- hypericin, pseudohypericin, protohypericin and proto- crobial, anti-inflammatory, and a healing agent (Brolis pseudohypericin (Meruelo et al. 1988). Recent studies et al. 1998). It encompasses a myriad of natural product revealed that the phloroglucinol hyperforin and its deriva- groups (Fig. 1) including naphthodianthrones primarily tive adhyperforin, can also inhibit various neurotransmitter represented by hypericin and pseudohypericin, flavonoids receptors (Laakmann et al. 1998a, b). Additionally, flavo- such as hyperoside, rutin, quercetin and astilbin, and a third noids present in St. John’s wort extracts have been shown group of phloroglucinol derivatives such as hyperforin and to have anti-depressant activities (Butterweck et al. 1997). adhyperforin (Nahrstedt and Butterweck 1997). Other Moreover, hyperforin has been shown to display antibac- phloroglucinols already identified within Hypericum spe- terial activity (Schempp et al. 2002b) and was also pro- cies include, perforatumone, uliginosin, bromouliginosin, posed to act as a novel anticancer drug by induction of drummondins, saroaspidins, hyperbrasilols, paglucinol, apoptosis (Schempp et al. 2002a). a b d c Fig. 1 Major groups of natural products; phloroglucinols (a), naph- carbon numbering system for each compound is used throughout the thodianthrones (b) phenolic/organic acids (c) and flavonoids manuscript for NMR assignment, and thus is based on analogy rather (d) detected in Hypericum species discussed in the manuscript. The than IUPAC rules 123 576 A. Porzel et al. Up to now, H. perforatum has been the primary source For this study, a one pot extraction method compatible for the naphthodianthrones/phloroglucinols or dietary with both NMR and LC–MS metabolomics was developed. supplements containing Hypericum plant material. Other Extracts derived from seven Hypericum species were species such as H. hirsutum, H. maculatum, H. tetrapterum, evaluated using the aforementioned technology platforms, H. grandifolium, H. montanum and H. humifusum were and processed data were further subjected to multivariate also found to contain a certain amount of theses metabo- analysis using PCA and hierarchical cluster analysis (HCA) lites (Butterweck et al. 1997; Umek et al. 1999; Smelce- to help reveal for compositional differences among species. rovic and Spiteller 2006a, c; Bonkanka et al. 2008). Our focus on flowers was based on results revealing that Although there are many species present in nature, classi- among H. perforatum aerial organs, flower and floral bud fication of which might be intricate in terms of taxonomy, are distinct in having the highest levels of hyperforins and there are only few reports on the systematic untargeted hypericins (Bonkanka et al. 2008). Except for H. tet- metabolic analysis of other Hypericum species. For reliable rapterum, the additional species studied have not been differentiation and chemical analysis, a broad systematic chemically profiled previously. As well, previous phyto- method monitoring the whole set or at least the medicinally chemical analyses mostly aimed at targeted quantification relevant metabolites (metabolite profiling) is deemed of and analysis of metabolites already well characterized in H. interest. Also, chemical analyses that are based on the perforatum (Kusari et al. 2009; Sagratini et al. 2008; natural composition of metabolites, rather than detection of Smelcerovic and Spiteller 2006; Smelcerovic et al. 2006c). a single constituent, are favored as they cover additionally In this study, data collected using MS and NMR techniques or synergistically relevant components and can confirm the were found to be complementary, and only by combining efficacy of H. perforatum medical preparations (Politi et al. them, a clearer and quantitative interpretation of the Hy- 2009; Rasmussen et al. 2006; Poutaraud et al. 2001). pericum species metabolome could be achieved. This With the recent developments in plant metabolomics comparative metabolomic approach can also provide a new techniques, it is now possible to detect several hundred platform for global analyses of Hypericum pharmaceuticals metabolites simultaneously and to compare samples reli- and or other phytomedicines. ably to identify differences and similarities in an untargeted manner. To obtain the most complete metabolite profile, it is necessary to use a wide spectrum of extraction and 2 Experimental analytical techniques which are rapid, reproducible, stable in time and require only a very simple sample preparation. 2.1 Plant material Most commonly, metabolomics is heavily supported by mass spectrometry (MS). Nuclear magnetic resonance Hypericum perforatum and H. polyphyllum ‘Grandiflorum’ (NMR) has emerged as parallel technology that can pro- seedlings were obtained from
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