Exploring the biological potential of Cruciata taurica (Pall. ex Willd.) Ehrend.: Evaluating antibacterial, antioxidant, antidiabetic, and cytotoxic properties

محورهای موضوعی : Medicinal and Herbal Plants

Shiva Khalil-Moghaddam ¹ (Department of Biology, Yadegar-e-Imam Khomeini (RAH), Shahre Rey Branch, Islamic Azad University, Tehran, Iran )
Roya Moghimi ² (Department of Organic Chemistry, Faculty of Chemistry, University of Mazandaran, Babolsar, Iran)
Thomas Efferth ³ (Department of Pharmaceutical Biology, Institute of Pharmaceutical and Biomedical Sciences, Johannes Gutenberg University Mainz, Germany)
Sajedeh Mousavian ⁴ (Departmant of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran)

تاریخ دریافت : 1402/11/17 تاریخ پذیرش : 1403/03/28 تاریخ انتشار : 1403/06/31

کلید واژه: Bioactivity, Cancer, Cruciata taurica (Pall. ex Willd.) Ehrend., Cytotoxic, Ethnopharmacology, Multidrug resistance, Plant extract,

چکیده مقاله :

This study focused on the biological properties of Cruciata taurica, a plant found in the Irano-Turanian region, which has not been extensively studied in terms of its phytochemical and biological activities. The methanolic extract of the plant was obtained and its cytotoxic, antibacterial, antidiabetic, and antioxidant properties were investigated. The antibacterial activity of the fractions was evaluated using broth microdilution method, while the antioxidant properties were assessed through the DPPH assay and the cytotoxic properties were determined using the RRA assay. This study revealed that the residual aqueous fraction exhibited the highest extraction yield and the most potent antioxidant activity. The EtOAc fraction showed strong antibacterial activity against certain bacteria, while the n-hexane fraction exhibited greater antidiabetic effects. Additionally, the EtOAc fraction was found to be the most cytotoxic. Overall, the study suggested that C. taurica has potential therapeutic applications due to its various biological properties.

چکیده انگلیسی:

This study focused on the biological properties of Cruciata taurica, a plant found in the Irano-Turanian region, which has not been extensively studied in terms of its phytochemical and biological activities. The methanolic extract of the plant was obtained and its cytotoxic, antibacterial, antidiabetic, and antioxidant properties were investigated. The antibacterial activity of the fractions was evaluated using broth microdilution method, while the antioxidant properties were assessed through the DPPH assay and the cytotoxic properties were determined using the RRA assay. This study revealed that the residual aqueous fraction exhibited the highest extraction yield and the most potent antioxidant activity. The EtOAc fraction showed strong antibacterial activity against certain bacteria, while the n-hexane fraction exhibited greater antidiabetic effects. Additionally, the EtOAc fraction was found to be the most cytotoxic. Overall, the study suggested that C. taurica has potential therapeutic applications due to its various biological properties.

منابع و مأخذ:

Abd Elkader, A.M., Labib, S., Taha, T.F., Althobaiti, F., Aldhahrani, A., Salem, H.M., Saad, A., Ibrahim, F.M., 2022. Phytogenic compounds from avocado (Persea americana L.) extracts; antioxidant activity, amylase inhibitory activity, therapeutic potential of type 2 diabetes. Saudi J. Biol. Sci. 29, 1428-1433.
Abd Wahab, N.Z., Azizul, A., Ibrahim, N., 2020. Phytochemistry, cytotoxicity and antiviral activity of Catharanthus roseus. Iran. J. Microbiol. 12, 460.
Abdollahzadeh, E., Nematollahi, A., Hosseini, H., 2021. Composition of antimicrobial edible films and methods for assessing their antimicrobial activity: A review. Trends Food Sci. Technol. 110, 291-303.
Agati, G., Azzarello, E., Pollastri, S., Tattini, M., 2012. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. 196, 67-76.
Alam, M.W., Najeeb, J., Naeem, S., Usman, S.M., Nahvi, I., Alismail, F., Abuzir, A., Farhan, M., Nawaz, A., 2022a. Electrochemical methodologies for investigating the antioxidant potential of plant and fruit extracts: A review. Antioxidants 11, 1205.
Alam, S., Sarker, M.M.R., Sultana, T.N., Chowdhury, M.N.R., Rashid, M.A., Chaity, N.I., Zhao, C., Xiao, J., Hafez, E.E., Khan, S.A., 2022b. Antidiabetic phytochemicals from medicinal plants: Prospective candidates for new drug discovery and development. Front. Endocrinol. (Lausanne) 13.
Ansari, P., Akther, S., Hannan, J.M.A., Seidel, V., Nujat, N.J., Abdel-Wahab, Y.H.A., 2022. Pharmacologically active phytomolecules isolated from traditional antidiabetic plants and their therapeutic role for the management of diabetes mellitus. Molecules 27, 4278.
Atanasov, A.G., Zotchev, S.B., Dirsch, V.M., Orhan, I.E., Banach, M., Rollinger, J.M., Barreca, D., Weckwerth, W., Bauer, R., Bayer, E.A., Majeed, M., Bishayee, A., Bochkov, V., Bonn, G.K., Braidy, N., Bucar, F., Cifuentes, A., D’Onofrio, G., Bodkin, M., Diederich, M., Dinkova-Kostova, A.T., Efferth, T., El Bairi, K., Arkells, N., Fan, T.P., Fiebich, B.L., Freissmuth, M., Georgiev, M.I., Gibbons, S., Godfrey, K.M., Gruber, C.W., Heer, J., Huber, L.A., Ibanez, E., Kijjoa, A., Kiss, A.K., Lu, A., Macias, F.A., Miller, M.J.S., Mocan, A., Müller, R., Nicoletti, F., Perry, G., Pittalà, V., Rastrelli, L., Ristow, M., Russo, G.L., Silva, A.S., Schuster, D., Sheridan, H., Skalicka-Woźniak, K., Skaltsounis, L., Sobarzo-Sánchez, E., Bredt, D.S., Stuppner, H., Sureda, A., Tzvetkov, N.T., Vacca, R.A., Aggarwal, B.B., Battino, M., Giampieri, F., Wink, M., Wolfender, J.L., Xiao, J., Yeung, A.W.K., Lizard, G., Popp, M.A., Heinrich, M., Berindan-Neagoe, I., Stadler, M., Daglia, M., Verpoorte, R., Supuran, C.T., 2021. Natural products in drug discovery: Advances and opportunities. Nat. Rev. Drug Discov. 20, 200-216.
Avoseh, N.O., Lawal, O.A., Ogunwande, I.A., Ascrizzi, R., Flamini, G., Amoo, E., 2020. In vivo anti-inflammatory and anti-nociceptive activities, and chemical constituents of essential oil from the leaf of Gardenia jasminoides J. Ellis (Rubiaceae). Trends Phytochem. Res. 4, 203-212.
Behdarvand, N., Bikhof Torbati, M., Shaabanzadeh, M., 2020. Tamoxifen-loaded PLA/DPPE-PEG lipid-polymeric nanocapsules for inhibiting the growth of estrogen-positive human breast cancer cells through cell cycle arrest. J. Nanoparticle Res. 22, 262.
Borhan, M.Z., Norhidayah, A., Ahmad, R., Rusop, M., Abdullah, S., 2013. Production of herbal nanopowders: Effect of milling time. Adv. Mater. Res. 686, 3-7.
Borisov, M.I., 1974. Coumarins of the genera Asperula and Galium. Chem. Nat. Compd. 10, 78.
Bremer, B., Eriksson, T., 2009. Time tree of Rubiaceae: Phylogeny and dating the family, subfamilies, and tribes. Int. J. Plant Sci. 170, 766-793.
Chassagne, F., Samarakoon, T., Porras, G., Lyles, J.T., Dettweiler, M., Marquez, L., Salam, A.M., Shabih, S., Farrokhi, D.R., Quave, C.L., 2021. A systematic review of plants with antibacterial activities: A taxonomic and phylogenetic perspective. Front. Pharmacol. 11, 2069.
Chen, Y., Wu, Y., Gan, X., Liu, K., Lv, X., Shen, H., Dai, G., Xu, H., 2016. Iridoid glycoside from Cornus officinalis ameliorated diabetes mellitus-induced testicular damage in male rats: Involvement of suppression of the AGEs/RAGE/p38 MAPK signaling pathway. J. Ethnopharmacol. 194, 850-860.
Choudhury, H., Pandey, M., Hua, C.K., Mun, C.S., Jing, J.K., Kong, L., Ern, L.Y., Ashraf, N.A., Kit, S.W., Yee, T.S., Pichika, M.R., Gorain, B., Kesharwani, P., 2018. An update on natural compounds in the remedy of diabetes mellitus: A systematic review. J. Tradit. Complement. Med. 8(3), 361-376.
CLSI, W., 2006. Clinical and Laboratory Standards Institute Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. Approv. Stand. M7-A7, CLSI, Seventh Ed, PA, USA.
De Rosa, S., Mitova, M., Handjieva, N., Çalış, İ., 2002. Coumarin glucosides from Cruciata taurica. Phytochemistry 59, 447-450.
De Rosa, S., Mitova, M., Handjieva, N., Ersoz, T., Calis, I., 2003. Aromatic monoterpenoid glycosides from Cruciata taurica. Nat. Prod. Res. 17, 109-113.
Efferth, T., Konkimalla, V.B., Wang, Y.-F., Sauerbrey, A., Meinhardt, S., Zintl, F., Mattern, J., Volm, M., 2008. Prediction of broad spectrum resistance of tumors towards anticancer drugs. Clin. Cancer Res. 14, 2405-2412.
Ehrendorfer, F., Schönbeck-Temesy, E., 1982. Flora of Turkey and the East Aegean Islands.
Ergun, F., Küsmenoglu, Ş., Şener, B., 1984. High-performance liquid chromatographic determination of iridoids in Cruciata Taurica. J. Liq. Chromatogr. 7, 1685-1689.
Ehrendorfer, F., Schonbeck-Temesy, E., Puff, C., Rechinger, W., 2005. Rubiaceae. In: Rechinger, K H (ed.) Flora Iranica, No. 176-Graz, p. 443.
Eruygur, N., Buyukyildirim, T., Tetik Rama, S., Ayaz, F., Tekin, M., Tuzcu, M., Akcakavak, G., Abdullah Yilmaz, M., 2023. Phytochemical profiling and biological activity of Achillea sintenisii Hub.-Mor. Chem. Biodivers. 20, e202201258.
Ghagane, S.C., Puranik, S.I., Kumbar, V.M., Nerli, R.B., Jalalpure, S.S., Hiremath, M.B., Neelagund, S., Aladakatti, R., 2017. In vitro antioxidant and anticancer activity of Leea indica leaf extracts on human prostate cancer cell lines. Integr. Med. Res. 6, 79-87.
Goli, P.P., Torbati, M.B., Parivar, K., Khiavi, A.A., Yousefi, M., 2021. Preparation and evaluation of gemcitabin and cisplatin-entrapped Folate-PEGylated liposomes as targeting co-drug delivery system in cancer therapy. J. Drug Deliv. Sci. Technol. 65, 102756.
González-Castelazo, F., Soria-Jasso, L.E., Torre-Villalvazo, I., Cariño-Cortés, R., Muñoz-Pérez, V.M., Ortiz, M.I., Fernández-Martínez, E., 2023. Plants of the Rubiaceae family with effect on metabolic syndrome: Constituents, pharmacology, and molecular targets. Plants 12, 3583.
Huysmans, S., Dessein, S., Smets, E., Robbrecht, E., 2003. Pollen morphology of NW European representatives confirms monophyly of Rubieae (Rubiaceae). Rev. Palaeobot. Palynol. 127, 219-240.
Irobi, O.N., Daramola, S.O., 1994. Bactericidal properties of crude extracts of Mitracarpus villosus. J. Ethnopharmacol. 42, 39-43.
Karakas, F.P., Turker, A.U., Karakas, A., Mshvildadze, V., Pichette, A., Legault, J., 2017. In vitro cytotoxic, antibacterial, anti-inflammatory and antioxidant activities and phenolic content in wild-grown flowers of common daisy—A medicinal plant. J. Herb. Med. 8, 31-39.
Karou, S.D., Tchacondo, T., Ilboudo, D.P., Simpore, J., 2011. Sub-Saharan Rubiaceae: A review of their traditional uses, phytochemistry and biological activities. Pak. J. Biol. Sci. 14, 149-169.
Khadayat, K., Marasini, B.P., Gautam, H., Ghaju, S., Parajuli, N., 2020. Evaluation of the alpha-amylase inhibitory activity of Nepalese medicinal plants used in the treatment of diabetes mellitus. Clin. Phytosci. 6, 1-8.
Khalil-Moghaddam, S., Aliahmadi, A., Jalilian, N., Tabad, M.A., 2021. The study of antioxidant and cellular toxicity effects of methanol, ethyl acetate, aqueous and n-hexane extracts of symphytum kurdicum plant. J. Chem. Heal. Risks 11, 105-111.
Khan, M.I., Bouyahya, A., Hachlafi, N.E.L., Menyiy, N. El, Akram, M., Sultana, S., Zengin, G., Ponomareva, L., Shariati, M.A., Ojo, O.A., 2022. Anticancer properties of medicinal plants and their bioactive compounds against breast cancer: A review on recent investigations. Environ. Sci. Pollut. Res. 29, 24411-24444.
Kumar, A., Aswal, S., Chauhan, A., Semwal, R.B., Singh, R., Andola, H.C., Joshi, S.K., Semwal, D.K., 2022. Antidiabetic effect of aqueous-ethanol extract from the aerial parts of Artemisia roxburghiana. Nat. Prod. Res. 36, 1300-1305.
Kumar, A., Jaitak, V., 2019. Natural products as multidrug resistance modulators in cancer. Eur. J. Med. Chem. 176, 268-291.
Li, H., Yao, Y., Li, L., 2017. Coumarins as potential antidiabetic agents. J. Pharm. Pharmacol. 69, 1253-1264.
Liu, X., Wang, Y., Alizade, V., Khutsishvili, M., Atha, D., Borris, R.P., Clark, B.R., 2021. Cruciasides C-G, monoterpenoid glycosides from Cruciata articulata. Phytochemistry 189, 112821.
Lopez-Corona, A.V., Valencia-Espinosa, I., González-Sánchez, F.A., Sánchez-López, A.L., Garcia-Amezquita, L.E., Garcia-Varela, R., 2022. Antioxidant, anti-inflammatory and cytotoxic activity of phenolic compound family extracted from raspberries (Rubus idaeus): A general review. Antioxidants 11, 1192.
Luo, H., Vong, C.T., Chen, H., Gao, Y., Lyu, P., Qiu, L., Zhao, M., Liu, Q., Cheng, Z., Zou, J., 2019. Naturally occurring anti-cancer compounds: Shining from Chinese herbal medicine. Chin. Med. 14, 48.
Mazzola, P.G., Lopes, A.M., Hasmann, F.A., Jozala, A.F., Penna, T.C. V, Magalhaes, P.O., Rangel‐Yagui, C.O., Pessoa Jr, A., 2008. Liquid-liquid extraction of biomolecules: An overview and update of the main techniques. J. Chem. Technol. Biotechnol. Int. Res. Process. Environ. Clean Technol. 83, 143-157.
Méril-Mamert, V., Ponce-Mora, A., Sylvestre, M., Lawrence, G., Bejarano, E., Cebrián-Torrejón, G., 2022. Antidiabetic potential of plants from the Caribbean basin. Plants 11, 1360.
Mogana, R., Adhikari, A., Tzar, M.N., Ramliza, R., Wiart, C., 2020. Antibacterial activities of the extracts, fractions and isolated compounds from Canarium patentinervium Miq. against bacterial clinical isolates. BMC Complement. Med. Ther. 20, 55.
Mogole, L., Omwoyo, W., Mtunzi, F., 2020. Phytochemical screening, anti-oxidant activity and α-amylase inhibition study using different extracts of loquat (Eriobotrya japonica) leaves. Heliyon 6(8), e04736.
Molnár, J., Engi, H., Hohmann, J., Molnár, P., Deli, J., Wesolowska, O., Michalak, K., Wang, Q., 2010. Reversal of multidrug resistance by natural substances from plants. Curr. Top. Med. Chem. 10, 1757-1768.
Namjoyan, F., Dastjerdi, Z.M., Azemi, M.E., 2015. Alpha amylase inhibition activity of some plants extract of Teucrium species. Eur. J. Biol. Sci. 7, 26-31.
Ng, C.X., Affendi, M.M., Chong, P.P., Lee, S.H., 2022. The potential of plant-derived extracts and compounds to augment anticancer effects of chemotherapeutic drugs. Nutr. Cancer 74, 3058-3076.
Niño, J., Mosquera, O.M., Correa, Y.M., 2012. Antibacterial and antifungal activities of crude plant extracts from Colombian biodiversity. Rev. Biol. Trop. 60, 1535-1542.
Nyobe, J.C.N., Bikélé, D.M., Fodouop, M.B., Mpondo, E.M., Ndom, J.C., 2020. A new pyrrolidinyl-piperazine alkaloid derivative from Oxyanthus speciosus DC.(Rubiaceae). Trends Phytochem. Res. 4, 109-116.
Ouadja, B., Anani, K., Djeri, B., Ameyapoh, Y.O., Karou, D.S., 2018. Evaluation of the phytochemical composition, antimicrobial and anti-radical activities of Mitracarpus scaber (Rubiaceae). J. Med. plants Res. 12, 493-499.
Oyedemi, S.O., Oyedemi, B.O., Ijeh, I.I., Ohanyerem, P.E., Coopoosamy, R.M., Aiyegoro, O.A., 2017. Alpha-amylase inhibition and antioxidative capacity of some antidiabetic plants used by the traditional healers in Southeastern Nigeria. Sci. World J. 2017, 3592491.
Ranasinghe, S., Armson, A., Lymbery, A.J., Zahedi, A., Ash, A., 2023. Medicinal plants as a source of antiparasitics: An overview of experimental studies. Pathog. Glob. Health 1-19.
Rasouli, H., Hosseini-Ghazvini, S.M.-B., Adibi, H., Khodarahmi, R., 2017. Differential α-amylase/α-glucosidase inhibitory activities of plant-derived phenolic compounds: A virtual screening perspective for the treatment of obesity and diabetes. Food Funct. 8, 1942-1954.
Sai, K., Thapa, R., Devkota, H.P., Joshi, K.R., 2019. Phytochemical screening, free radical scavenging and α-amylase inhibitory activities of selected medicinal plants from Western Nepal. Medicines 6, 70.
Saifulazmi, N.F., Rohani, E.R., Harun, S., Bunawan, H., Hamezah, H.S., Nor Muhammad, N.A., Azizan, K.A., Ahmed, Q.U., Fakurazi, S., Mediani, A., 2022. A review with updated perspectives on the antiviral potentials of traditional medicinal plants and their prospects in antiviral therapy. Life 12, 1287.
Sak, K., 2014. Cytotoxicity of dietary flavonoids on different human cancer types. Pharmacogn. Rev. 8, 122.
Salim, M., Necattin, T., 2018. A survey on wild plants with ethnobotanical use in the Bahçe and Hasanbeyli districts of Osmaniye, Turkey. GSC Biol. Pharm. Sci. 05, 28-35.
Sartoratto, A., Machado, A.L.M., Delarmelina, C., Figueira, G.M., Duarte, M.C.T., Rehder, V.L.G., 2004. Composition and antimicrobial activity of essential oils from aromatic plants used in Brazil. Brazilian J. Microbiol. 35, 275-280.
Sbieh, R., Al-Lahham, S., Jaradat, N., 2022. Antioxidant, antimicrobial and cytotoxic properties of four different extracts derived from the aerial parts of Chiliadenus iphinoides. Eur. J. Integr. Med. 54, 102149.
Shah, S.B., Sartaj, L., Ali, F., Shah, S.I.A., Khan, M.T., 2018. Plant extracts are the potential inhibitors of α-amylase: A review. MOJ Bioequiv. Availab. 5, 270-273.
Singh, A.K., 2022. A review on plant extract-based route for synthesis of cobalt nanoparticles: Photocatalytic, electrochemical sensing and antibacterial applications. Curr. Res. Green Sustain. Chem. 100270.
Tava, A., Biazzi, E., Ronga, D., Avato, P., 2020. Identification of the volatile components of Galium verum L. and Cruciata leavipes Opiz from the Western Italian Alps. Molecules 25.
Tohma, H., Altay, A., Köksal, E., Gören, A.C., Gülçin, İ., 2019. Measurement of anticancer, antidiabetic and anticholinergic properties of sumac (Rhus coriaria): Analysis of its phenolic compounds by LC-MS/MS. J. Food Meas. Charact. 13, 1607-1619.
Tomou, E.-M., Papakyriakopoulou, P., Skaltsa, H., Valsami, G., Kadoglou, N.P.E., 2023. Bio-actives from natural products with potential cardioprotective properties: Isolation, identification, and pharmacological actions of apigenin, quercetin, and silibinin. Molecules 28, 2387.
Volm, M., Efferth, T., 2015. Role of P-glycoprotein for Resistance of Tumors to Anticancer Drugs: From bench to Bedside. Resistance to Targeted ABC Transporters in Cancer. pp. 1-26.
Wickramaratne, M.N., Punchihewa, J.C., Wickramaratne, D.B.M., 2016. In-vitro alpha amylase inhibitory activity of the leaf extracts of Adenanthera pavonina. BMC Complement. Altern. Med. 16, 1-5.
Wooster, T.J., Golding, M., Sanguansri, P., 2008. Impact of oil type on nanoemulsion formation and Ostwald ripening stability. Langmuir 24, 12758-12765.
Wonkam, A.K.N., Njanpa, C.A.N., Ateba, J.E.T., Fongang, Y.S.F., Awantu, A.F., Bankeu, J.J.K., Chouna, J.R., Boyom, F.F., Sewald, N., Lenta, B.N., 2022. Constituents of the ripe fruits of Nauclea latifolia Sm. (Rubiaceae) and their antileishmanial activities. Trends Phytochem. Res. 6(4), 292-300.
Yeshi, K., Turpin, G., Jamtsho, T., Wangchuk, P., 2022. Indigenous uses, phytochemical analysis, and anti-inflammatory properties of Australian tropical medicinal plants. Molecules 27, 3849.
Youmbi, L.M., Makong, Y.S.D., Mbaveng, A.T., Tankeo, S.B., Fotso, G.W., Ndjakou, B.L., Wansi, J.D., Beng, V.P., Sewald, N., Ngadjui, B.T., 2023. Cytotoxicity of the methanol extracts and compounds of Brucea antidysenterica (Simaroubaceae) towards multifactorial drug-resistant human cancer cell lines. BMC Complement. Med. Ther. 23, 48.
Yuan, M., Zhang, G., Bai, W., Han, X., Li, C., Bian, S., 2022. The role of bioactive compounds in natural products extracted from plants in cancer treatment and their mechanisms related to anticancer effects. Oxid. Med. Cell. Longev. 2022.
Zhang, J., Chu, W.-C., Li, L.-Z., 2023. Isolation and structure elucidation of antioxidant compounds from stem and root barks of Daphne giraldii. J. Asian Nat. Prod. Res. 1-10.
Zieneldien, T., Kim, J., Cao, C., 2022. The multifaceted role of neuroprotective plants in Alzheimer’s Disease treatment. Geriatrics 7, 24.