Differences in bioactivity of three endemic Nepeta species arising from main terpenoid and phenolic constituents

Authors

  • Jasmina Milan Nestorović Živković Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade
  • Suzana Živković Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0003-0280-5884
  • Branislav Šiler Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0001-5831-6612
  • Neda Aničić Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade
  • Slavica Dmitrović Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-2621-1530
  • Aleksandra Divac Rankov Institute of Molecular Genetics and Genetic Engineering, University of Belgrade, Vojvode Stepe 444a, 11010 Belgrade
  • Zlatko Giba Institute of Botany, Faculty of Biology, University of Belgrade, Takovska 43, 11060 Belgrade
  • Danijela Mišić Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-5419-0773

Keywords:

Nepeta rtanjensis, Nepeta sibirica, Nepeta nervosa, nepetalactone, phenolic acids

Abstract

Methanol extracts of three endemic Nepeta species were analyzed for their main secondary metabolites, terpenes and phenolics, and further investigated for antioxidant capacity and embryonic toxicity in zebrafish. UHPLC/DAD/(±)HESI-MS/MS analysis showed that the dominant compound in N. rtanjensis was trans,cis-nepetalactone, the cis,trans isomer of this monoterpene lactone was dominant in N. sibirica, while nepetalactone was detected only in traces in N. nervosa. In all investigated species, rosmarinic acid was the dominant phenolic compound, while other identified phenolic acids (chlorogenic, neochlorogenic and caffeic) were present in considerably lower amounts. ABTS and DPPH assays showed that the methanol extracts of N. rtanjensis, N. sibirica and especially N. nervosa possessed strong antioxidant activities, with the FRAP assay revealing high ferric-reducing abilities for all three tested species. Such a strong antioxidant potential, especially as manifested in the DPPH and FRAP assays, can be attributed to phenolic acids, and in the first place to rosmarinic acid. Increased lethality of zebrafish embryos in any of the treatments was not observed, but several toxic effects on embryonic development were recorded, such as pericardial and yolk sac edema. As in other Nepeta species, the three studied endemic species possessed a great potential for food conservation or as medicinal supplements if applied in optimized concentrations; however, alternative sources of plant material (e.g. field cultivation) should be established bearing in mind their vulnerability in nature.

https://doi.org/10.2298/ABS170616026N

Received: June 16, 2017; Revised: July 20, 2017; Accepted: July 20, 2017; Published online: July 26, 2017

How to cite this article: Nestorović-Živković J, Živković S, Šiler B, Aničić N, Dmitrović S, Divac-Rankov A, Giba Z, Mišić D. Differences in bioactivity of three endemic Nepeta species arising from main terpenoid and phenolic constituents. Arch Biol Sci. 2018;70(1):63-76.

Downloads

Download data is not yet available.

Author Biographies

Jasmina Milan Nestorović Živković, Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade

Plant Physiology

Suzana Živković, Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade

Plant Physiology

Branislav Šiler, Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade

Plant Physiology

Neda Aničić, Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade

Plant Physiology

Slavica Dmitrović, Institute for Biological Research "Siniša Stanković" University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade

Plant Physiology

Danijela Mišić, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade

Plant Physiology

References

Yan X, Murphy BT., Hammond GB, Vinson JA, Neto CC. Antioxidant activities and antitumor screening of extracts from cranberry fruit (Vaccinium macrocarpon). J Agri Food Chem. 2002;50(21):5844-9.

Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: A review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol. 2009;7(1):65-74.

Tepe B, Daferera D, Tepe AS., Polissiou M, Sokmen A. Antioxidant activity of the essential oil and various extract of Nepeta flavida Hub.-Mor. from Turkey. Food Chem. 2007;103:1358-64.

Sarahroodi S, Jafari-Najafi R, Nasri S, Rahampur K, Maleki-Jamshid A, Esmaeili S. Effects of Nepeta menthoides aqueous extract on retention and retrieval of memory in mice. Pak J Biol Sci. 2012;15(22):1085-9.

Miceli N, Taviano MF, Giuffrida D, Trovato A, Tzakou O, Galati EM. Anti-inflammatory activity of extract and fractions from Nepeta sibthorpii Bentham. J Ethnopharmacol. 2005;97(2):261-6.

Aydin S, Demir T, Öztürk Y, Hüsnü K, Başer C. Analgesic activity of Nepeta italica L. Phytother Res. 1999;13:20-23.

Rigano D, Arnold NA, Conforti F, Menichini F, Formisano C, Piozzi F, Senatore F. Characterisation of the essential oil of Nepeta glomerata Montbret et Launcher ex Bentham from Lebanon and its biological activities. Nat Prod Res. 2011;25(6):614-26.

Bedoya LM, Palomino SS, Abad MJ, Bermejo P, Alcami J. Screening of selected plant extracts for in vitro inhibitory activity on human immunodeficiency virus. Phytother Res. 2002;16(6):550-4.

Nestorović J, Mišić D, Šiler B, Soković M, Glamoclija J, Ćirić A, Maksimović V, Grubišić D. Nepetalactone content in shoot cultures of three endemic Nepeta species and the evaluation of their antimicrobial activity. Fitoterapia 2010;81(6):621-625.

Mutlu S, Atic O, Esim N, Mete E. Essential oils of catmint (Nepeta meyeri Benth.) induce oxidative stress in early seedlings of various weed species. Acta Physiol Plant. 2011;33(3):943-51.

Dmitrović S, Perišić M, Stojić A, Živković, S, Boljević J, Nestorović Živković J, Aničić N, Ristić M, Mišić D. Essential oils of two Nepeta species inhibit growth and induce oxidative stress in ragweed (Ambrosia artemisiifolia L.) shoots in vitro. Acta Physiol Plant. 2015;37(3):64-97.

Nestorović Živković J, Dmitrović S, Jovanović V, Živković S, Božić D, Aničić N, Mišić D. Allelopathic potential of essential oil of N. rtanjensis. Allelopathy J. 2016;36(2):207-20.

Mišić D, Šiler B, Gašić U, Avramov S, Živković S, Nestorović Živković J, Milutinović M, Tešić Z. Simultaneous UHPLC/DAD/(+/-)HESI-MS/MS analysis of phenolic acids and nepetalactones in methanol extracts of Nepeta species: a possible application in chemotaxonomic studies. Phytochem Anal. 2015;26(1):72-85.

Liblikas I, Santangelo EM, Sandell J, Baeckström P, Svensson M, Jacobsson U, Unelius CR. Simplified isolation procedure and interconversion of the diastereomers of nepetalactone and nepetalactol. J Nat Prod. 2005;68(6):886-90.

Hardie J, Peace L, Pickett JA, Smiley DWM, Storer JR, Wadhams LJ. Sex pheromone stereochemistry and purity affect field catches of mail aphids. J Chem Ecol. 1997;23(11):2547-54.

Yazici SO, Özmen I, Celkoglu U, Öluzcel H, Genc H. In vitro antioxidant activities of extracts from some Nepeta species. Int J Health Nutr. 2012;3(1):8-12.

Chalchat JC, Gorunović MS, Petrović SD, Maksimović ZA. Composition of the essential oils of Nepeta rtanjensis Diklić et Milojević, Lamiaceae from Serbia. J Essent Oil Res. 2000;12:238-40.

Letchamo W, Korolyuk EA, Tkachev AV. Chemical screening of essential oil bearing flora of Siberia IV. Composition of the essential oil of Nepeta sibirica L. tops from Altai region. J Essent Oil Res. 2005;17: 487-9.

Blatter E. Beautiful Flowers of Kashmir. Vol 2. London: John Bale, Sons and Danielsson Limited Publishers,; 1928.

Lawrence BM. Chemical components of Labiatae oils and their exploitation. In: Harley RM, Reynolds T, editors. Advances in Labiatae Science. Royal Botanical Gardens; 1992. p. 399-436.

Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant. 1962;15:473-97.

Singleton VL, Rossi JA. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic. 1965;16:144-58.

Karadeniz F, Burdulu HS, Koca N, Soyer Y. Antioxidant activity of selected fruits and vegetables grown in Turkey. Turk J Agric For. 2005;29(4):297-303.

Šiler B, Živković S, Banjanac T, Cvetković J, Nestorović Živković J, Ćirić A, Soković M, Mišić D. Centauries as underestimated food additives: antioxidant and antimicrobial potential. Food Chem. 2014;147:367-76.

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorisation assay. Free Radic Biol Med. 1999;26(9-10):1231-7.

Brand-Williams W, Cuvelier ME, Berset C. Use of free radical method to evaluate antioxidant activity. Lebensm. Wiss. Technol. 1995;28(1):25-30.

Benzie IFF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “Antioxidant Power”: the FRAP assay. Anal Biochem. 1996;239(1):70-6.

Kimmel CB. Genetics and early development of zebrafish. Trends Genet. 1989;5(8):283-8.

Formisano C, Rigano D, Senatore F. Chemical constituens and biological activity of Nepeta species. Chem Biodivers. 2011;8(10):1783-817.

Kraujalis P, Rimantas P, Ragazinskiene O. Antoxidant activities and phenolic composition of extract from Nepeta plant species. In: Proceedings of the 6th Baltic Conference on Food Science and Technology FOODBALT-2011: Innovatops for food science and production; 2011 May 5-6; Jeglava, Latvia. Jelgava, Latvia: Faculty of Food Technology, University of Agriculture; 2011.

Hadi N, Sefidkon F, Shojaeiyan A, Šiler B, Jafari AA, Aničić N, Mišić D. Phenolics’ composition in four endemic Nepeta species from Iran cultivated under experimental field conditions: The possibility of the exploitation of Nepeta germplasm. Ind Crops Prod. 2017;95:475-84.

Pedersen JA. Distribution and taxonomic implication of some phenolics in the family Lamiaceae determined by ESR spectroscopy. Biochem Syst Ecol. 2000;28(3):229-53.

Takhtajan A. Subclass VIII. Lamiidae. In: Takhtajan A, editor. Flowering Plants. Berlin, Hamburg: Springer-Verlag;| 2009. p. 511-89.

Mišić D, Maksimović V, Todorović S, Grubišić D, Konjević R. Influence of carbohydrate source on Nepeta rtanjensis growth, morphogenesis and nepetalactone production in vitro. Isr J Plant Sci. 2005;53(2):103-8.

Sefidkon F, Jamzad Z. Essential oil composition of four Iranian Nepeta species (N. cephalotes, N. bornmuelleri, N. mirzayanii and N. bracteata). J Essent Oil Res. 2007;19(3):262-5.

Karaman S, Cӧmlekçioĝolu N. Essential oil composition of Nepeta cilici Boiss. Apud Bentham and Phlomis viscosa Poiret from Turkey. Int J Bot. 2007;3:122-6.

Senatore F, Arnold NA, Piozzi F. Composition of the essential oil of Nepeta curviflora Boiss. (Lamiaceae) from Lebanon. J Essent Oil Res. 2005;17(3):268-70.

Sajjadia SE, Mehregan I. Chemical constituents of the essential oil of Nepeta daenensis Boiss. J Essent Oil Res. 2005;17(5):563-64.

Potter JD. Vegetables, fruit and cancer. Lancet. 2005;366:527-30.

Tundis R, Nadjafi F, Menichini F. Angiotensin-converting enzyme inhibitory activity and antioxidant properties of Nepeta crassifolia Boiss & Buhse and Nepeta binaludensis Jamzad. Phytother Res. 2013;27:572-80.

Rice-Evans CA, Miller NJ, Paganga G. Antioxidant properties of phenolic compounds. Trends Plant Sci. 1997;2(4):152-9.

Chen JH, Ho CT. Antioxidant activities of caffeic acid and its related hydroxycinnamic acid compounds. J Agric Food Chem. 1997;45(7):2374-8.

Fadel O, Kirat KE, Morandat S. The natural antioxidant rosmarinic acid spontaneously penetrates membranes to inhibit lipid peroxidation in situ. Biochim Biophys Acta - Biomembranes. 2011;1808(12): 2973-80.

50. Tepe B. Antioxidant potentials and rosmarinic acid levels of the methanolic extracts of Salvia virgata (Jacq), Salvia staminea (Montbret & Aucher ex Bentham) and Salvia verbenaca (L.) from Turkey. Bioresour Technol. 2008;99(6):1584-8.

Proestos C, Boziaris IS, Nychas GJE, Komaitis M. Analysis of flavonoids and phenolic acids in Greek aromatic plants: Investigation of their antioxidant capacity and antimicrobial activity. Food Chem. 2006;95:664-71.

Mahboubi M, Kazempour N, Ghazian F, Taghizadeh M. Chemical composition, antioxidant and antimicrobial activity of Nepeta persica Boiss. essential oil. Herbapol. 2011;57(1):63-71.

Iacopini P, Baldi M, Storchi P, Sebastiani L. Catechin, epicatechin, quercetin, rutin and resveratrol in red grape: Content in vitro antioxidant activity and interactions. J Food Comp Anal. 2008;21(8):589-98.

Kratchanova M, Denev P, Ciz M, Mihailov AL. Evaluation of antioxidant activity of medicinal plants containing polyphenol compounds. Comparison of two extraction systems. Acta Bioch Pol. 2010;57(2):229-34.

Hill AJ, Teraoka H, Heidemann W, Peterson RE. Zebrafish as model vertebrate for investigating chemical toxicity. Toxicol Sci. 2005;86(1):6-19.

Xu Z, Zhang YL, Song C, Wu LL, Gao HW. Interactions of hydroxyapatite with proteins and its toxicological effect to zebrafish embryos development. PLoS One. 2012;7(4):e32818.

Hussain J, Jamila N, Gilani S, Abbas G, Ahmed S. Platelet aggregation, antiglycation, cytotoxic, phytotoxic and antimicrobial activities of extracts of Nepeta juncea. African J Biotechnol. 2009;8(6):935-40.

Gharbani P, Javazi H. The antioxidant, general toxicity and insecticidal activities of Nepeta scrophularioides Rech. f. extracts in different developmental stages. Pak J Pharm Sci. 2015;28(5):1905-09.

Baloch N, Nabi S, Bashir S, Al-Kahraman Y. In vitro antileishmanial, cytotoxic activity and phytochemical analysis of Nepeta praetervisa leaves extracts and its fractions. Int J Pharm Pharm Sci. 2013;5(4):475-8.

Skorić M, Gligorijević N, Čavić M, Todorović S, Janković R, Ristić M, Mišić D, Radulović S. Cytotoxic activity of Nepeta rtanjensis Diklić & Milojević essential oil and its mode of action. Ind Crops Prod. 2017;100:163-70.

Afshar AS, Nematpour FS, Meshkani M, Khafi A. Growth inhibition of human breast cancer cells and down-regulation of ODC1 and ADA genes by Nepeta binaloudensis. Rev Bras Farmacogn. 2017;27(1):84-90.

Ashkezary MD, Aboee-Mehrizi F, Moradi P. SiO2@antisense molecules covered by nepetalactone, extracted from Nepeta gloeocephala, inhibits ILK phosphorylation and downstream PKB/AKT signaling in HeLa cells. Cancer Gene Ther. 2017;24(1):28-32.

Shakeri A, Khakdan F, Soheili V, Sahebkar A, Rassam G, Asili J. Chemical composition, antibacterial activity, and cytotoxicity of essential oil from Nepeta ucrainica L. spp. kopetdaghensis. Ind Crops Prod. 2014;58:315-21.

Dar AB, Lone AM, Qurishi MA. Cytotoxic activity and GC-MS analysis of the constituents of essential oil of Nepeta govaniana (Wall. ex Benth) from Jammu and Kashmir. India Int J Her Med. 2014;2(2):58-60.

Spence R, Gerlach G, Lawrence C, Smith C. The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev. 2008;83(1):13-34.

Downloads

Published

2018-03-13

How to Cite

1.
Nestorović Živković JM, Živković S, Šiler B, Aničić N, Dmitrović S, Divac Rankov A, Giba Z, Mišić D. Differences in bioactivity of three endemic Nepeta species arising from main terpenoid and phenolic constituents. Arch Biol Sci [Internet]. 2018Mar.13 [cited 2024Mar.28];70(1):063-76. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/1881

Issue

Section

Articles

Most read articles by the same author(s)