Abstract
Purpose
The goals of this study were to monitor the effect of drinking of herbal tea from Sideritis clandestina subsp. clandestina for 6 weeks on behavioral and oxidant/antioxidant parameters of adult male mice and also to evaluate its phytochemical composition.
Methods
The phytochemical profile of the Sideritis tea was determined by liquid chromatography-UV diode array coupled to ion-trap mass spectrometry with electrospray ionization interface. The effects of two doses of the herbal infusion (2 and 4% w/v, daily) intake on anxiety-like state in mice were studied by the assessment of their thigmotactic behavior. The oxidant/antioxidant status of brain (-Ce), liver and heart of adult male Balb-c mice following the consumption of Sideritis tea was also evaluated via the measurement of malondialdehyde (MDA) and reduced glutathione (GSH) levels using fluorometric assays. Our study was further extended to determine the antioxidant effects of the herbal tea on specific brain regions (cerebral cortex, cerebellum and midbrain).
Results
The identified compounds were classified into several natural product classes: quinic acid derivatives, iridoids, phenylethanol glycosides and flavonoids. Our results showed that only the 4% Sideritis tea exhibited anxiolytic-like properties as evidenced by statistically significant (p < 0.05) decrease in the thigmotaxis time and increase in the number of entries to the central zone in comparison with the control group. Consumption of both tea doses (2 and 4% w/v) elevated GSH (12 and 28%, respectively, p < 0.05) and decreased MDA (16 and 29%, p < 0.05) levels in brain (-Ce), while liver and heart remained unaffected. In regard to the effect of herbal tea drinking (2 and 4% w/v) on specific brain regions, it caused a significant increase in GSH of cerebellum (13 and 36%, respectively, p < 0.05) and midbrain (17 and 36%, p < 0.05). Similarly, MDA levels were decreased in cerebellum (45 and 79%, respectively, p < 0.05) and midbrain (50 and 63%, respectively, p < 0.05), whereas cerebral cortex remained unaffected.
Conclusions
Mountain tea drinking prevents anxiety-related behaviors and confers antioxidant protection to rodent’s tissues in a region-specific, dose-dependent manner, and its phytochemical constituents are shown for the first time.
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Abbreviations
- MDA:
-
Malondialdehyde
- GSH:
-
Reduced glutathione
- TBA:
-
Thiobarbituric acid
- BHT:
-
Butylated hydroxytoluene
- TCA:
-
Trichloroacetic acid
- LC/DAD/ESI-MSn :
-
Liquid chromatography/diode array detection/electrospray ion-trap tandem mass spectrometry
- NMR:
-
Nuclear magnetic resonance
References
Halliwell B (1992) Reactive oxygen species and the central-nervous-system. J Neurochem 59:1609–1623
Manach C, Scalbert A, Morand C, Rémésy C, Jiménez L (2004) Polyphenols: food sources and bioavailability. Am J Clin Nutr 79:727–747
Yao LH, Jiang YM, Shi J, Tomás-Barberán FA, Datta N, Singanusong R et al (2004) Flavonoids in food and their health benefits. Plant Foods Hum Nutr 59:113–122
Urquiaga I, Leighton F (2000) Plant polyphenol antioxidants and oxidative stress. Biol Res 33:55–64
Rammal H, Bouayed J, Younos C, Soulimani R (2008) Evidence that oxidative stress is linked to anxiety-related behaviour in mice. Brain Behav Immun 22:1156–1159
Kuloglu M, Atmaca M, Tezcan E, Ustundag B, Bulut S (2002) Antioxidant enzyme and malondialdehyde levels in patients with panic disorder. Neuropsychobiology 46:186–189
Bouayed J, Rammal H, Soulimani R (2009) Oxidative stress and anxiety relationship and cellular pathways. Oxid Med Cell Longev 2:63–67
Tomás-Barberán FA, Rejdali M, Harborne JB, Heywood VH (1988) External and vacuolar flavonoids from ibero-North African Sideritis species. A chemosystematic approach. Phytochemistry 27:165–170
Küpeli E, Şahin FP, Çaliş I, Yeşilada E, Ezer N (2007) Phenolic compounds of Sideritis ozturkii and their in vivo anti-inflammatory and antinociceptive activities. J Ethnopharmacol 112:356–360
Aligiannis N, Kalpoutzakis E, Chinou IB, Mitakou S, Gikas E, Tsarbopoulos A (2001) Composition and antimicrobial activity of the essential oils of five taxa of Sideritis from Greece. J Agric Food Chem 49:811–815
Aboutabl EA, Nassar MI, Elsakhawy FM, Maklad YA, Osman AF, El-Khrisy EAM (2002) Phytochemical and pharmacological studies on Sideritis taurica Stephan ex Wild. J Ethnopharmacol 82:177–184
Kassi E, Papoutsi Z, Fokialakis N, Messari I, Mitakou S, Moutsatsou P (2004) Greek plant extracts exhibit selective estrogen receptor modulator (SERM)-like properties. J Agric Food Chem 52:6956–6961
Rios JL, Mañez S, Paya M, Alcaraz MJ (1992) Antioxidant activity of flavonoids from Sideritis-Javalambrensis. Phytochemistry 31:1947–1950
Gabrieli CN, Kefalas PG, Kokkalou EL (2005) Antioxidant activity of flavonoids from Sideritis raeseri. J Ethnopharmacol 96:423–428
Tsaknis J, Lalas S (2005) Extraction and identification of natural antioxidant from Sideritis euboea (Mountain tea). J Agric Food Chem 53:6375–6381
Charami MT, Lazari D, Karioti A, Skaltsa H, Hadjipavlou-Litina D, Souleles C (2008) Antioxidant and antiinflammatory activities of Sideritis perfoliata subsp perfoliata (Lamiaceae). Phytother Res 22:450–454
Demirtas I, Ayhan B, Sahin A, Aksit H, Elmastas M, Telci I (2010) Antioxidant activity and chemical composition of Sideritis libanotica Labill ssp. linearis (Bentham) Borm. (Lamiaceae). Nat Prod Res 16:1512–1523
Celik I, Kaya MS (2011) The antioxidant role of Sideritis caesarea infusion against TCA toxicity in rats. Br J Nutr 105:663–668
Linardaki ZI, Vasilopoulou CG, Constantinou C, Iatrou G et al (2011) Differential antioxidant effects of consuming tea from Sideritis clandestina subsp. peloponnesiaca on Cerebral Regions of Adult Mice. J Med Food 14:1060–1064
Simon P, Dupuis R, Costentin J (1994) Thigmotaxis as an index of anxiety in mice-influence of dopaminergic transmissions. Behav Brain Res 61:59–64
Papandreou MA, Dimakopoulou A, Linardaki ZI, Cordopatis P, Klimis-Zacas D, Margarity M, Lamari FN (2009) Effect of a polyphenol-rich wild blueberry extract on cognitive performance of mice, brain antioxidant markers and acetylcholinesterase activity. Behav Brain Res 198:352–358
Mokrasch LC, Teschke EJ (1984) Glutathione content of cultured cells and rodent brain regions: a specific fluorometric assay. Anal Biochem 140:506–509
Petreska J, Stefova M, Ferreres F, Moreno DA, Tomas-Barberan FA, Stefkov G et al (2011) Potential bioactive phenolics of Macedonian Sideritis species used for medicinal “Mountain Tea”. Food Chem 125:13–20
Han J, Ye M, Guo H, Yang M, Wang BR, Guo DA (2007) Analysis of multiple constituents in a Chinese herbal preparation Shuang-Huang-Lian oral liquid by HPLC-DAD-ESI-MSn. J Pharm Biomed Anal 44:430–438
Hong JL, Qin XY, Shu P, Wu G, Wang QA, Qin MJ (2010) Analysis of catalpol derivatives by characteristic neutral losses using liquid chromatography combined with electrospray ionization multistage and time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 24:2680–2686
Quirantes-Piné R, Funes L, Micol V, Segura-Carretero A, Fernández-Gutiérrez A (2009) High-performance liquid chromatography with diode array detection coupled to electrospray time-of-flight and ion-trap tandem mass spectrometry to identify phenolic compounds from a lemon verbena extract. J Chromatogr A 1216:5391–5397
Ferreres F, Llorach R, Gil-Izquierdo A (2004) Characterization of the interglycosidic linkage in di-, tri-, tetra- and pentaglycosylated flavonoids and differentiation of positional isomers by liquid chromatography/electrospray ionization tandem mass spectrometry. J Mass Spectrom 39:312–321
Kirmizibekmez H, Montoro P, Piacente S, Pizza C, Donmez A, Calis I (2005) Identification by HPLC-PAD-MS and quantification by HPLC-PAD of phenylethanoid glycosides of five Phlomis species. Phytochem Anal 16:1–6
Karioti A, Bolognesi L, Vincieri FF, Bilia AR (2010) Analysis of the constituents of aqueous preparations of Stachys recta by HPLC-DAD and HPLC-ESI-MS. J Pharm Biomed Anal 53:15–23
Koleva II, Linssen JPH, van Beek TA, Evstatieva LN, Kortenska V, Handjieva N (2003) Antioxidant activity screening of extracts from Sideritis species (Labiatae) grown in Bulgaria. J Sci of Food Agric 83:809–819
Alipieva KI, Kostadinova EP, Evstatieva LN, Stefova M, Bankova VS (2009) An iridoid and a flavonoid from Sideritis lanata L. Fitoterapia 80:51–53
Świątek L, Lehmann D, Chaudhuri RK, Sticher O (1981) Occurrence of melittoside in the seeds of Plantago media. Phytochemistry 20:2023–2024
Küçükkurt I, Ince S, Keleş H, Akkol EK, Avci G, Yesilada E et al (2010) Beneficial effects of Aesculus hippocastanum L. seed extract on the body’s own antioxidant defense system on subacute administration. J Ethnopharmacol 129:18–22
MacEvilly CJ, Muller DPR (1996) Lipid peroxidation in neural tissues and fractions from vitamin E-deficient rats. Free Radical Biol Med 20:639–648
Haque AM, Hashimoto M, Katakura M, Tanabe Y, Hara Y, Shido O (2006) Long-term administration of green tea catechins improves spatial cognition learning ability in rats. J Nutr 136:1043–1047
Baldaçara L, Borgio JGF, de Lacerda ALT, Jackowski AP (2008) Cerebellum and psychiatric disorders. Rev Bras Psiquiatr 30:281–289
Avila MAV, Ruggiero RN, Cabral A, Brandão ML, Nobre MJ, Castilho VM (2008) Involvement of the midbrain tectum in the unconditioned fear promoted by morphine withdrawal. Eur J Pharmacol 590:217–223
Janga SC, Tzakos A (2009) Structure and organization of drug-target networks: insights from genomic approaches for drug discovery. Mol Biosyst 5:1536–1548
Yin F, Liu J, Zheng X, Guo L, Xiao H (2010) Geniposide induces the expression of heme oxygenase-1 via PI3K/Nrf2-signaling to enhance the antioxidant capacity in primary hippocampal neurons. Biol Pharm Bull 33:1841–1846
Kwon SH, Kim HC, Lee SY, Jang CG (2009) Loganin improves learning and memory impairments induced by scopolamine in mice. Eur J Pharmacol 619:44–49
Jeong EJ, Lee KY, Kim SH, Sung SH, Kim YC (2008) Cognitive-enhancing and antioxidant activities of iridoid glycosides from Scrophularia buergeriana in scopolamine-treated mice. Eur J Pharmacol 588:78–84
Kim SR, Koo KA, Sung SH, Ma CJ, Yoon JS, Kim YC (2003) Iridoids from Scrophularia buergeriana attenuate glutamate-induced neurotoxicity in rat cortical cultures. J Neurosci Res 74:948–955
Dimpfel W, Kler A, Kriesl E, Lehnfeld R (2007) Theogallin and L-theanine as active ingredients in decaffeinated green tea extract: II. Characterization in the freely moving rat by means of quantitative field potential analysis. J Pharm Pharmacol 59:1397–1403
Han J, Miyamae Y, Shigemori H, Isoda H (2010) Neuroprotective effect of 3, 5-di-O-caffeoylquinic acid on SH-SY5Y cells and senescence-accelerated-prone mice 8 through the up-regulation of phosphoglycerate kinase-1. Neuroscience 169:1039–1045
Nday CM, Drever BD, Salifoglou T, Platt B (2010) Aluminum does not enhance β-amyloid toxicity in rat hippocampal cultures. Brain Res 1352:265–276
Hur JY, Soh Y, Kim BH, Suk K, Sohn N, Kim HC et al (2001) Neuroprotective and neurotrophic effects of quinic acids from Aster scaber in PC12 cells. Biol Pharm Bull 24:921–924
Jang DS, Yoo NH, Kim NH, Lee YM, Kim CS, Kim J et al (2010) 3, 5-Di-O-caffeoyl-epi-quinic acid from the leaves and stems of Erigeron annuus inhibits protein glycation, aldose reductase, and cataractogenesis. Biol Pharm Bull 33:329–333
Yi LT, Li JM, Li YC, Pan Y, Xu Q, Kong LD (2008) Antidepressant-like behavioral and neurochemical effects of the citrus-associated chemical apigenin. Life Sci 82:741–751
Liu R, Zhang T, Yang H, Lan X, Ying J, Du G (2011) The flavonoid apigenin protects brain neurovascular coupling against amyloid-β25–35-induced toxicity in mice. J Alzheimers Dis 24:85–100
Ha SK, Lee P, Park JA, Oh HR, Lee SY, Park J-H et al (2008) Apigenin inhibits the production of NO and PGE2 in microglia and inhibits neuronal cell death in a middle cerebral artery occlusion-induced focal ischemia mice model. Neurochem Int 52:878–886
Jeyabal PVS, Syed MB, Venkataraman M, Sambandham JK, Sakthisekaran D (2005) Apigenin inhibits oxidative stress-induced macromolecular damage in N-nitrosodiethylamine (NDEA)-induced hepatocellular carcinogenesis in Wistar albino rats. Mol Carcinog 44:11–20
Singh JP, Selvendiran K, Banu SM, Padmavathi R, Sakthisekaran D (2004) Protective role of Apigenin on the status of lipid peroxidation and antioxidant defense against hepatocarcinogenesis in Wistar albino rats. Phytomedicine 11:309–314
Acknowledgments
We are grateful to Dr. Garbis S. for helpful discussions and comments. This work was partially supported by BIOFLORA, network of University of Patras and Esthir-Gkani Foundation, Ioannina. Special thanks are given to the Mass Spectrometry Unit of University of Ioannina for providing access to LC-MS/MS facilities and Mrs. Theodora Lamari for collecting the plant material. NMR data were recorded in the NMR center of the University of Ioannina.
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Catherine G. Vasilopoulou and Vassiliki G. Kontogianni contributed equally to this work.
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Vasilopoulou, C.G., Kontogianni, V.G., Linardaki, Z.I. et al. Phytochemical composition of “mountain tea” from Sideritis clandestina subsp. clandestina and evaluation of its behavioral and oxidant/antioxidant effects on adult mice. Eur J Nutr 52, 107–116 (2013). https://doi.org/10.1007/s00394-011-0292-2
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DOI: https://doi.org/10.1007/s00394-011-0292-2