The optimization growth of Dracocephalum forrestii in RITA® bioreactor, and preliminary screening of the biological activity of the polyphenol rich extract

Izabela Weremczuk-Jeżyna

Department of Biology and Pharmaceutical Botany, Medical University of Lodz, Muszyńskiego 1, 90-151 Lodz, Poland
https://orcid.org/0000-0002-1055-7617

Liwia Lebelt

Bioorganic Chemistry Laboratory, Faculty of Pharmacy, Medical University of Lodz, Lodz, Poland
https://orcid.org/0000-0003-2518-4953

Dorota Piotrowska

Bioorganic Chemistry Laboratory, Faculty of Pharmacy, Medical University of Lodz, Lodz, Poland
https://orcid.org/0000-0003-3792-8796

Weronika Gonciarz

Department of Immunology and Infectious Biology, Faculty of Biology and Environmental Protection, University of Lodz, Lodz, Poland
https://orcid.org/0000-0002-5231-5341

Magdalena Chmiela

Department of Immunology and Infectious Biology, Faculty of Biology and Environmental Protection, University of Lodz, Lodz, Poland
https://orcid.org/0000-0002-5447-2922

Izabela Grzegorczyk-Karolak

Department of Biology and Pharmaceutical Botany, Medical University of Lodz, Muszyńskiego 1, 90-151 Lodz, Poland
https://orcid.org/0000-0003-4793-4604


Abstract

Dracocephalum forrestii is a medicinal plant growing in China. The aim of the present study was to large-scale cultivation of D. forrestii transformed shoots in a temporary immersion system based on previously-optimized Murashige and Skoog (MS) medium supplemented with 0.5 mg/L N-benzyl-9-(2-tetrahydropyranyl)-adenine (BPA) and 0.2 mg/L indole-3-acetic acid (IAA) and physical (under blue LED) conditions. Shoot proliferation, and biomass and secondary metabolite accumulation in the shoots were assessed after a three-week growth period in a RITA® bioreactor. The levels of polyphenols in four types of extract (hydromethanolic extracts – mixtures with a 20%, 50%, and 80% methanol content and infusion) were determined using high-performance liquid chromatography (HPLC). Within three weeks, the culture increased its biomass 283-fold, with a proliferation ratio of 40.5 shoots or/and buds per explants. The most efficient solvent for extraction of phenolic compounds from raw material turned out to be 80% methanol solution; the highest polyphenol content was 40 mg/g DW (dry weight) with acacetin rhamnosyl-trihexoside (12.97 mg/g DW) and rosmarinic acid (10.68 mg/g DW) predominating. The intensive growth of the biomass of the culture allowed 570 mg of polyphenolic compounds to be obtained per liter of the medium. The antioxidant potential of extract of D. forrestii shoots was evaluated using three free radical-scavenging tests, and the inhibition of lipid peroxidation assay. In the study, the cytotoxic, antibacterial and antifungal potentials of the extract were also determined.

Keywords:

acacetin and apigenin glucoside, biological potential, large-scale cultivation, rosmarinic acid, RITA® bioreactor, transformed root culture

Abedini, A., Roumy, V., Mahieux, S., Biabiany, M., Standaert-Vitse, A., Rivière, C., Sahpaz, S., Bailleul, F., Neut, C., Hennebelle, T. (2013). Rosmarinic acid and its methyl ester as antimicrobial components of the hydromethanolic extract of Hyptis atrorubens Poit. (Lamiaceae). Evid. Based Complement. Alternat. Med., 604536. https://doi.org/ 10.1155/2013/604536 DOI: https://doi.org/10.1155/2013/604536

Ahmadian, M., Babaei, A., Shokri, S., Shakrir, H. (2017). Micropropagation of carnation (Dianthus caryophyllus L.) in liquid medium by temporary immersion bioreactor in comparison with solid culture. J. Genet. Eng. Biotechnol., 15(2), 309–315. https://doi.org/10.1016/j.jgeb.2017.07.005 DOI: https://doi.org/10.1016/j.jgeb.2017.07.005

Anwar, S., Shamsi, A., Shahbaaz, M., Qeen, A., Khan, P., Hasan, G.M., Islam, A., Alajmi, M.F., Hussain, A., Ahmad, F., Hassan I. (2020). Rosmarinic acid exhibits anticancer effects via MARK inhibition. Sci. Rep., 10, 10300. https://doi.org/10.1038/s41598-020-65648-z DOI: https://doi.org/10.1038/s41598-020-65648-z

Aprotosaie, A.C., Mihai, C.T., Vochita, G., Rotinberg, P., Trifan, A., Luca, S.A., Petreus, T., Gille, E., Miron, A. (2016). Antigenotoxic and antioxidant activities of a polyphenolic extract from European Dracocephalum moldavica L. Ind. Crops Prod., 79, 248–257. https://doi.org/10.1016/j.indcrop.2015.11.004 DOI: https://doi.org/10.1016/j.indcrop.2015.11.004

Aragón, C.E., Sánchez, C., Gonzalez-Olmedo, J., Escalona, M., Carvalho, L.K., Amâncio, S. (2014). Comparison of plantain plantlets propagated in temporary immersion bioreactors and gelled during in vitro growth and acclimatization. Biol. Plant., 58, 29–38. https://doi.org/10.1007/s10535-013-0381-6 DOI: https://doi.org/10.1007/s10535-013-0381-6

Blank, D.E., Alves, G.H., Nascente, P., Freitag, R.A., Clef, M.B. (2020). Bioactive compounds and antifungal activities of extracts of Lamiaceae species. J. Agric. Chem. Environ., 9(3), 85–96. https://doi.org/10.4236/jacen.2020.93008 DOI: https://doi.org/10.4236/jacen.2020.93008

Businge, E., Trifanova, A., Schneider, C., Rödel Egertdotter, U. (2017). Evaluation of new temporary immersion system for micropropagation of cultivars of Eucalyptus, Birch and Fir. Forests, 8(6), 196–205. https://doi.org/10.3390/f8060196 DOI: https://doi.org/10.3390/f8060196

Cai, Y., Luo, Q., Sun, M., Corke, H. (2004). Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci., 74(17), 2157–2184. https://doi.org/10.1016/j.lfs.2003.09.047 DOI: https://doi.org/10.1016/j.lfs.2003.09.047

Chaudhary, A., Sharma, S., Mittal, A., Gupta, S., Dua, A. (2020) Phytochemical and antioxidant profiling of Ocimmum sanctum. Food Sci. Technol., 57, 3852–3863. https://doi.org/10.1007/s13197-020-04417-2 DOI: https://doi.org/10.1007/s13197-020-04417-2

Chaves, J.O., Carrêa de Souza, M., Capelasso da Silva, L., Lachos-Perez, D., Torres-Mayanga, P.C., da Faresca Machado, A.P., Forster-Cameiro, T., Vázquez-Espinosa, M., González-de-Peredo, A.V., Barbero, G., Rostagno, M.A. (2020). Extraction of flavonoids from natural sources using modern techniques. Front. Chem., 8, 507887. https://doi.org/10.3389/fchem.2020.507887 DOI: https://doi.org/10.3389/fchem.2020.507887

DeRango-Adem, E.F., Blay, J. (2021). Does oral apigenin have real potential for a therapeutic effect in the context of human gastrointestinal and other cancers? Front. Pharmacol., 12, 681477. https://doi.org/10.3389/fphar.2021.681477 DOI: https://doi.org/10.3389/fphar.2021.681477

Dhanani, T., Shah, S., Gajbhiye, N.A., Kumar, S. (2017). Effect of extraction methods an yield phytochemical constituents and antioxidant activity of Withania somnifera. Arab. J. Chem., 10(1), S1103–S1199. https://doi.org/10.1016/j.arabjc.2013.02.015 DOI: https://doi.org/10.1016/j.arabjc.2013.02.015

Ekambram, S.P., Perumal, S.S., Balakrishnom A., Marappan, N., Gajendran, S.S., Viswannathan, V. (2016). Antibacterial synrgy between rosmarinic acid and antibiotics against methilicin resistant Saphylococcus aureus. J. Intercult. Ethnopharmacol., 5(4), 358–363. https://doi.org/10.5455/jice.20160906035020 DOI: https://doi.org/10.5455/jice.20160906035020

Elansary H.O., Szopa, A., Kubica P., Ekiert, H., Al-Mana F.A., Al-Yafrsi, M.A. (2020). Antioxidant and biological activities of Acacia saligna and Lawsonia inermis natural populations. Plants, 9(7), 908–925. https://doi.org/10.3390/plants9070908 DOI: https://doi.org/10.3390/plants9070908

Espinosa-Leal, C.A., Puente-Garza, CA., Gracía-Lara, S. (2018). In vitro plant tissue culture: Means for production of biological active compounds. Planta, 248, 1–18. https://doi.org/10.1007/s00425-018-2910-1 DOI: https://doi.org/10.1007/s00425-018-2910-1

Georgiev, V., Ivanov, I., Berkov, S., Pavlov, A. (2014a). Temporary immersion systems for Amaryllidaceae alkaloids biosynthesis by Pancratium maritimum L. shoot culture. J. Plant. Biochem. Biotechnol., 23, 389–398. https://doi.org/10.1007/s13562-013-0222-x DOI: https://doi.org/10.1007/s13562-013-0222-x

Georgiev, V., Schumann, A., Pavlow, A., Bley, T. (2014b). Temporary immersion system in plant biotechnology. Eng. Life. Sci., 14(6), 607–621. https://doi.org/10.1002/elsc.201300166 DOI: https://doi.org/10.1002/elsc.201300166

Grzegorczyk-Karolak, I., Staniewska, P., Lebelt, L., Piotrowska, D.G. (2022). Optimization of cultivation conditions of Salvia viridis L. shoots in the Plantform bioreactor to increase polyphenol production. Plant Cell Tissue Organ Cult., 149, 269–280.

https://doi.org/10.1007/s11240-021-02168-2 DOI: https://doi.org/10.1007/s11240-021-02168-2

Grzegorczyk-Karolak, I., Kiss, A.K. (2018). Determination of the phenolic profile and antioxidant properties of Salvia viridis L. shoots: a comparison of aqueous and hydroethanolic extracts. Molecules, 23(6), 1468–1495. https://doi.org/10.3390/molecules23061468 DOI: https://doi.org/10.3390/molecules23061468

Grzegorczyk-Karolak, I., Kuźma Ł., Wysokińska, H. (2015). The effect of cytokinin on shoot proliferation, secondary metabolite production and antioxidant potential in shoot cultures of Scutellaria alpina. Plant Cell Tissue Organ Cult., 122, 699–708.

https://doi.org/10.1007/s11240-015-0804-5 DOI: https://doi.org/10.1007/s11240-015-0804-5

Hashim, N., Shaari, A.R., Mamat, A.S., Ahmad, S. (2016). Effect of differences methanol concentration and extraction time on the antioxidant capacity, phenolics content and bioactive constituents of Orthosiphon stamineus extract. MATEC Web Conf., 78, 01004. DOI: https://doi.org/10.1051/matecconf/20167801004

Heydari, P., Yavari, M., Adibi, P., Asghari, G., Ghanadian, S.M., Dida, G., Khawesipour, F. (2019). Medicinal properties and active constituents of Dracocephalum kotschyi and significance in Iran: a systematic review. Evid. Based Complement. Altern. Med., 94655309. https://doi.org/10.1155/2019/9465309 DOI: https://doi.org/10.1155/2019/9465309

ISO 10993-5:2009 (2009). Biological evaluation of medical devices – Part. 5: Tests for in vitro cytotoxicity. ISO, Geneva, Switzerland.

Kamali, M., Khosroyar, S., Mohammadi, A. (2015). Antibacterial activity of various extracts from Dracocephalum kotschyi against food pathogenic microorganisms. Int. J. Pharm. Tech. Res., 8(9), 158–163.

Kamizela, A., Gawdzik, B., Urbaniak, M., Lechowicz, Ł., Białońska, A., Kutniewska, S., Gonciarz, W., Chmiela, M. (2019). New γ-halo-δ-lactones and δ-hydroxy-γ-lactones with strong cytotoxic activity. Molecules, 24(10), 1875. https://doi.org/10.3390/molecules24101875 DOI: https://doi.org/10.3390/molecules24101875

Khadije, R.K., Jahantigh, H.R., Bagheri, R., Kehkhaie, K.R. (2017). The effects of the ethanol extract of Dracocephalum moldavica (Badrashbu) against strains antibiotic-resistans Escherichia coli and Klebsiella pneumonia. Int. J. Infect., 5(1), e65295. https://doi.org/ 10.5812/iji.65295 DOI: https://doi.org/10.5812/iji.65295

Kang, K.-R., Kim, J.-S., Kim, T.-H., Seo, J.-Y., Park, J.-H., Lim, J.-W., Yu, S.-K., Kim, H.-J., Shin, S.-H., Park, B.-R., Kim, C.S., Kim D.K. (2020). Inhibition of cell growth and induction of apoptosis by acacetin in FaDu human pharyncal carcinoma cell. Int. J. Oral Biol., 45, 107–114. https://doi.org/10.11620/IJOB.2020.45.3.107 DOI: https://doi.org/10.11620/IJOB.2020.45.3.107

Kostić, M., Zlatković, B., Miladinović, B., Živanovič, S., Mihajilov-Krstev, T., Palvlovič, D., Kitić, D. (2015). Rosmarinic acid levels, phenolic contents, antioxidant and antimicrobial activities from Salvia verbenaca L. obtain with different solvents and procedures. J. Food Biochem., 39(2), 199–208. https://doi.org/10.1111/jfbc.12121 DOI: https://doi.org/10.1111/jfbc.12121

Krzemińska, M., Owczarek, A., Gonciarz, W., Chmiela, M., Olszewska, M.A., Grzegorczyk-Karolak, I. (2022). The antioxidant, cytotoxic and antimicrobial potential of phenolic acids- enriched extract of elicitated hairy roots of Salvia bulleyana. Molecules, 27(3), 992. https://doi.org/10.3390/molecules27030992 DOI: https://doi.org/10.3390/molecules27030992

Kunakhonnuruk, B., Inthima, P., Kongbangkerd, A. (2019). In vitro propagation of rheophytic orchid, Epipactis flava Seidenf. – a comparison of semi-solid, continuous immersion and temporary immersion systems. Biology, 8(4), 72. https://doi.org/10.3390/biology8040072 DOI: https://doi.org/10.3390/biology8040072

Lee, J.S., Lee, C.A., Kim, Y.H., Yun, S.J. (2014). Shorter wavelength blue light promotes growth of green perilla (Perilla frutescens). Int. J. Agric. Biol., 16, 1172–1182.

Li, G.-P., Zhao, J.-F., Yang, L.-J., Yang, X.-D., Li, L. (2007). New monoterpenoids from Dracocephalum forrestii aerial parts. Chem. Inform., 38(50). https://doi.org/10.1002/chin.200750193 DOI: https://doi.org/10.1002/chin.200750193

Li, S.-M., Yang, X.-W., Li, Y.-L., Shen, Y.-H., Feng, L., Wang, Y.-H., Zeng, H.-W., Liu, X.-H., Zhang, C.-S., Long, C.-L., Zhang, W.-D. (2009). Chemical constituents of Dracocephalum forrestii. Planta Med., 75(15), 1591–1596. https://doi.org/10.1055/s-0029-1185868 DOI: https://doi.org/10.1055/s-0029-1185868

Li, G.-P., Zhao, J.-F., Yang, L.-J., Yang, X.-D., Li, L. (2006). Three new triterpenoids from Dracocephalum forrestii. Helv. Chim. Acta, 89(12), 3018–3022. https://doi.org/10.1002/hlca.200690271 DOI: https://doi.org/10.1002/hlca.200690271

Lyam, P.T., Musa, M.L., Jamaleddine, Z.O., Okere, U.A., Odofin, W.T. (2012). The potential of temporary immersion bioreactors (TIBs) in meeting crop production demand in Nigeria. J. Biol. Life Sci., 3(1), 66–86. https://doi.org/10.5296/jbls.v3i1.1156 DOI: https://doi.org/10.5296/jbls.v3i1.1156

Manivannan, A., Soundararajan, P., Halimah, N., Ko, C.H., Jeong, B.R. (2015). Blue LED light enhances growth, phytochemical contents, and antioxidant enzyme activities of Rehmannia glutinosa cultured in vitro. Hortic. Environ. Biotechnol., 56, 105–113.

https://doi.org/10.1007/s13580-015-0114-1 DOI: https://doi.org/10.1007/s13580-015-0114-1

Meng, L., Gui, X., Yun, Z. (2019). A new method to extract oridonin and rosmarinic acid simultaneously from Rabdosia rubescens. Int. J. Food Eng., 15(9), 20190013. https://doi.org/10.1515/ijfe-2019-0013 DOI: https://doi.org/10.1515/ijfe-2019-0013

Moore, J., Yousef, M., Tsiani, E. (2016). Anticancer effects of rosemary (Rosmarinus officinalis L.) extract and rosemary extract polyphenols. Nutrients, 18(11), 731. https://doi.org/10.3390/nu8110731 DOI: https://doi.org/10.3390/nu8110731

Moradi, H., Ghavam, M., Tavili, A. (2020). Study of antioxidant activity and some herbal compounds of Dracocephalum kotschyi Boiss. In different ages of growth. Biotechnol. Rep., 25, e0048. https://doi.org/10.1016/j.btre.2019.e00408 DOI: https://doi.org/10.1016/j.btre.2019.e00408

Munteanu, I.G., Apetrei, C. (2021). Analytical methods used in determining antioxidant activity: a review. Int. J. Mol. Sci., 22(7), 3380–3410. https://doi.org/10.3390/ijms22073380 DOI: https://doi.org/10.3390/ijms22073380

Muniyandi, K., George, E., Mudili, V., Kalagatur, N.K., Anthuvan, A.J., Krishna, K., Thangaraj, P., Natarajan, G., (2017). Antioxidant and anticancer activities of Plectranthus stoksci Hook. f. leaf and stem extracts. Agric. Nat. Res., 51(2), 63–77. DOI: https://doi.org/10.1016/j.anres.2016.07.007

Murashige, T., Skoog, F. (1962). A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol. Plant., 15(3), 473–449. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x DOI: https://doi.org/10.1111/j.1399-3054.1962.tb08052.x

Nadeem, M., Imran, M., Gondal, T.A., Imran, A., Shahbaz, M., Amir, R.M., Sajid, M.W., Qaisrani, T.B., Atif, M., Hussain, G., Salehi, B., Ostrander, E.A., Martorell, M., Sharifi-Rad, J., Cho, W.C., Martins, N. (2019). Therapeutic potential of rosmarinic acid: a comprehensive review. Appl. Sci., 9(15), 3139. https://doi.org/10.3390/app9153139 DOI: https://doi.org/10.3390/app9153139

Olennikov, D.N., Chirikova, N.K., Okhlopkova, Z.M., Zulfuganov, I.S., (2013). Chemical composition and antioxidant activity of Tánara Ótó (Dracocepahlum palmatum Stephan), a medicinal plant used by North-Yakutian nomads. Molecules, 18(11), 14105–14121. https://doi.org/10.3390/molecules181114105 DOI: https://doi.org/10.3390/molecules181114105

Pan, M.-H., Lai, C.-S., Hsu, P.-C., Wang, Y.-J. (2005). Acacetin induces apoptosis in human gastric carcinoma cells accompanied by activation of caspase cascades and production of reactive oxygen species. J. Agric. Food Chem., 53(3), 620–630. https://doi.org/10.1021/jf048430m DOI: https://doi.org/10.1021/jf048430m

Picos-Solas, M.A., Heredia, J.B., Leyva-López, N., Ambriz-Pérez, D.L., Gutiérrez-Grijalva, E.P. (2021). Extraction process affect the composition and bioavailability of flavones from Lamiaceae plants: Comprehensive review. Processes, 9(9), 1675. https://doi.org/10.3390/pr9091675 DOI: https://doi.org/10.3390/pr9091675

Ray, J.X., Chaurasia, O.P., Vaipayee, P.K., Murugan, M.P., Bala, S.S. (2009). Antioxidative activity and phytochemical investigation on a high altitude medicinal plant Dracocephalum heterophyllum Benth. Pharmacon. J., 1, 246–251.

Scheckel, K.A., Degner, S.C., Romagnolo, D.F., (2008). Rosmarinic acid antagonizes activator protein-1-dependent activation of cyclooxygenase-2 expression in human cancer and nonmalignant cell lines. J. Nutr., 138(11), 2098–2105. https://doi.org/10.3945/jn.108.090431 DOI: https://doi.org/10.3945/jn.108.090431

Shaabani, M., Mousavi, S.H., Azizi, M., Ashraf Jafari, A. (2020). Cytotoxic and apoptogenic effects of Dracocephalum kotschyi Boiss., extracts against human glioblastoma U87 cells. Avic. J. Phytomed., 10(6), 594–603.

Smiljkovic, M., Stanisavljevic, D., Stojkovic, D., Petrovic, I., Vicentic, J.M., Popovic, J., Grdadolnik, S.G., Markovic, D., Sanković-Babić, S., Glamoclija, J., Stevanovic, M., Sokovic, M. (2017). Apigenin-7-O- glucoside versus apigenin insight into the modes of antiradical and cytotoxi actions. EXLI J., 16, 795–807. https://doi.org/10.17179/excli2017-300

Sonmezdag, A.S., Kelebek, H., Selli, S. (2018). Characterization of bioactive and volatile profiles of thyme (Thymus vulgaris L.) teas as affected by infusion times. J. Food Meas. Charact., 12, 2570–2580. https://doi.org/10.1007/s11694-018-9874-5 DOI: https://doi.org/10.1007/s11694-018-9874-5

Weremczuk-Jeżyna, I., Kuźma, Ł., Grzegorczyk-Karolak, I. (2021). The effect of different light treatments on morphogenesis, phenolic compound accumulation and antioxidant potential of Dracocephalum forrestii transformed shoots cultured in vitro. J. Photochem. Photobiol. B Biol., 224, 112329. https://doi.org/10.1016/j.jphotobiol.2021.112329 DOI: https://doi.org/10.1016/j.jphotobiol.2021.112329

Weremczuk-Jeżyna, I., Lisiecki, P., Gonciarz, W., Kuźma, Ł., Szemraj, M., Chmiela, M., Grzegorczyk-Karolak, I. (2020). Transformed shoots of Dracocephalum forrestii W.W. Smith from different bioreactor systems as a rich source of natural phenolic compounds. Molecules, 25(19), 4533. https://doi.org/10.3390/molecules25194533 DOI: https://doi.org/10.3390/molecules25194533

Weremczuk-Jeżyna, I., Skała, E., Kuźma, Ł., Kiss, A.K., Grzegorczyk-Karolak, I. (2019). The effect of purine-type cytokinin on the proliferation and production of phenolic compounds in transformed shoots of Dracocephalum forrestii. J. Biotechnol., 306, 125–133. https://doi.org/10.1016/j.jbiotec.2019.09.014 DOI: https://doi.org/10.1016/j.jbiotec.2019.09.014

Weremczuk-Jeżyna, I., Kuźma, Ł., Kiss, A.K., Grzegorczyk-Karolak, I. (2018). Effect of cytokinins on shoots proliferation and rosmarinic and salvianolic acid B production in shoot culture of Dracocephalum forrestii W.W. Smith. Acta Physiol. Plant., 40, 189–199. https://doi.org/10.1007/s11738-018-2763-z DOI: https://doi.org/10.1007/s11738-018-2763-z

Weremczuk-Jeżyna, I., Grzegorczyk-Karolak, I., Frydrych, B., Hantuszko-Konka, K., Gerszberg, A., Wysokińska, H. (2017). Rosmarinic acid accumulation and antioxidant potential of Dracocephalum moldavica cell suspension culture. Not. Bot. Hort. Agrobot. Cluj Napoca, 45(1), 2015–2017. https://doi.org/10.15835/nbha45110728 DOI: https://doi.org/10.15835/nbha45110728

Vassallo, A., Cioffi, G., De Simone, F., Braca, A., Sango, R., Vanella, A., Russo, A., De Tommasi, N. (2016). New flavonoid glycosides from Chrozophora senegalensis and their antioxidant activity. Nat. Prod. Commun., 1, 1089–1095. https://doi.org/10.1177/1934578X0600101204 DOI: https://doi.org/10.1177/1934578X0600101204

Xiao, Z., Liu, W., Mu, Y.-P., Zhang, H., Wang, X.-N., Zhao, C.-G., Chen, J.-M., Lu, P. (2020). Pharmacological effects of salvianolic acid B against oxidative damage. Front. Pharmacol., 11, 572373. https://doi.org/10.3389/fphar.2020.572373 DOI: https://doi.org/10.3389/fphar.2020.572373

Yaghoobi, M.M., Khaleghi, M., Rezanejad, H., Parsia, P. (2018). Antibiofilm activity of Dracocephalum polyachetum extract an methicillin-resistant Staphylococcus aureus. Avicenna J. Clin. Microbiol. Infect., 5(1), 61772. https://doi.org/10.5812/ajcmi.61772 DOI: https://doi.org/10.5812/ajcmi.61772

Yan, X., Qi, M., Li, P., Zhan, Y., Shao, H. (2017). Apigenin in cancer therapy: anticancer effects and mechanisms of action. Cell Biosci., 7, 50–66. https://doi.org/10.1186/s13578-017-0179-x DOI: https://doi.org/10.1186/s13578-017-0179-x

Zhang, B., Song, L., Bekele, L.M., Shi, J., Jia, Q., Zhang, B., Jin, L., Duns, G.J., Chen, J. (2018a). Optimizing factors a effecting development and propagation of Bletilla striata in a temporary immersion system. Sci. Hortic., 232, 121–126. https://doi.org/10.1016/j.scienta.2018.01.007 DOI: https://doi.org/10.1016/j.scienta.2018.01.007

Zhang, J., Zhang, X., Zhang, J., Li, M., Chen, D., Wu, T. (2018b). Minor compounds of the high purity salvianolic acid B freeze-dried powder from Salvia miltiorrhiza and antibacterial activity assessment. Nat. Prod. Res., 32(10), 1198–1202. https://doi.org/10.1080/14786419.2017.1323212 DOI: https://doi.org/10.1080/14786419.2017.1323212

Zheng, L., Labeke, M.C. (2017). Long-term effects of red- and blue – light emitting diodes on leaf anatomy and photosynthetic efficiency of three ornamental pot plants. Front. Plant. Sci., 8, 917. https://doi.org/10.3389/fpls.2017.00917 DOI: https://doi.org/10.3389/fpls.2017.00917

Ziani, B.E.C., Barros, L., Boumehina, A.Z., Bahari, K., Heleno, S.A., Alves, M.J., Ferreira, J.I. (2018). Profiling polyphenol composition by HPLC-DAD-ESI/MSn and antibacterial activity of infusion preparations obtained from four medicinal plants. Food Funct., 9(1), 720–725. https://doi.org/10.1039/c7fo01315a DOI: https://doi.org/10.1039/C7FO01315A

Download

Published
2023-04-28



Izabela Weremczuk-Jeżyna 
Department of Biology and Pharmaceutical Botany, Medical University of Lodz, Muszyńskiego 1, 90-151 Lodz, Poland https://orcid.org/0000-0002-1055-7617
Liwia Lebelt 
Bioorganic Chemistry Laboratory, Faculty of Pharmacy, Medical University of Lodz, Lodz, Poland https://orcid.org/0000-0003-2518-4953
Dorota Piotrowska 
Bioorganic Chemistry Laboratory, Faculty of Pharmacy, Medical University of Lodz, Lodz, Poland https://orcid.org/0000-0003-3792-8796
Weronika Gonciarz 
Department of Immunology and Infectious Biology, Faculty of Biology and Environmental Protection, University of Lodz, Lodz, Poland https://orcid.org/0000-0002-5231-5341
Magdalena Chmiela 
Department of Immunology and Infectious Biology, Faculty of Biology and Environmental Protection, University of Lodz, Lodz, Poland https://orcid.org/0000-0002-5447-2922
Izabela Grzegorczyk-Karolak 
Department of Biology and Pharmaceutical Botany, Medical University of Lodz, Muszyńskiego 1, 90-151 Lodz, Poland https://orcid.org/0000-0003-4793-4604



License

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

 

Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.

The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.