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Utilization of Dianthus Superbus L and Its Bioactive Compounds for Antioxidant, Anti-Influenza and Toxicological Effects T

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Utilization of Dianthus Superbus L and Its Bioactive Compounds for Antioxidant, Anti-Influenza and Toxicological Effects T Food and Chemical Toxicology 125 (2019) 313–321 Contents lists available at ScienceDirect Food and Chemical Toxicology journal homepage: www.elsevier.com/locate/foodchemtox Utilization of Dianthus superbus L and its bioactive compounds for antioxidant, anti-influenza and toxicological effects T ∗∗ Doo Hwan Kim, Gyun Seok Park, Arti Shivraj Nile, Young Deuk Kwon, Gansukh Enkhtaivan , ∗ Shivraj Hariram Nile Department of Bio-resources and Food Science, Konkuk University, Seoul, 143-701, South Korea ARTICLE INFO ABSTRACT Keywords: Dianthus superbus (DS) is a traditional medicinal herb well known for its medicinal and therapeutic potential and Dianthus superbus widely distributed in various Asian countries. The ethyl acetate (EA), butanol (Bu) and distilled water (DW) Anticancer extracts of DS assessed for extraction of bioactive compounds and their biological activities. The chemical fl Anti-in uenza analysis was done using LC-MS/MS and antioxidant, anticancer and antiviral activities were determined. EA Correlation study extracts showed strong anticancer activity with IC of 9.5, 13.8 and 69.9 μg/mL on SKOV, NCL-H1299 and Extraction 50 Caski cancer cell lines, respectively. The Bu extracts exhibited strongest antiviral activity with respect to both influenza A and B viruses with IC50 values of 4.97 and 3.9 μg/mL, respectively. Also the metabolic profile for EA, Bu and DW extracts shows high variations and influence precisely the antioxidant, anticancer and antiviral properties. The quercetin 3- rutinoside and isorhamnetin 3- glucoside showed higher neuraminidase inhibition activity in dose dependent manner. Molecular docking study revealed that flavonol glycosides have higher binding activities towards influenza polymerase membrane glycoprotein. Correlation study showed that flavonol glycosides were linked to anti-influenza activity and cyclic peptides with anticancer activities. This study pro- vides vital information for effective utilization of DS for medicinal, food and therapeutic purposes. 1. Introduction screening of natural drugs or compounds from medicinal plants for therapeutic applications against cancer and other diseases gained In recent years cancer and viral diseases predominantly leading paramount importance. Influenza virus referred to as “flu”, plays a cause of human death. About 12.7 million cancer patients were de- dangerous impact on children and elder people. Influenza vaccine tected in 2008, and approximately 7.98 million people died in 2010 due protection is extremely less or missing and gives only 35% protection to cancer (Jemal et al., 2011; Lozano et al., 2012). The various factors (Lozano et al., 2012). Additionally, influenza A and B viruses spread such as chewing of tobacco, obesity, a poor diet, stress, and lack of globally and generates mutations in human body which leads to de- physical exercise, infections, ionizing radiation, and environmental velopment of antigenic drift and shift after administration anti influ- pollutants leading to development of cancer in humans (Anand et al., enza drugs (Stephan et al., 2009). The studies showed that the pre- 2008). Occurrence of cancer risk is gaining significantly with age, food viously developed drugs such as Tamiflu (oseltamivir) couldn't inhibit habit and region wise as many cancers occurring more frequently in infection during the 2007–2008 seasonal influenza occurrence and even developed countries (Jemal et al., 2011). In the 20th century, many couldn't recognize binding to glycoproteins of the influenza virus anticancer treating treatments were developed such as chemotherapy membrane, hemagglutinin (HA) and neuraminidase (NA) (Choi et al., and radiation therapy, but these methods have strange side effects 2009). Hence, scientists need to discover more drugs and scientific leading to the loss of healthy cell count and body weight (Corrie and proof against influenza viral infections. There has been significant in- Pippa, 2008; Lee et al., 2012). Hence, research is important for crease in influenza outbreaks leaving thousands either infected or dead Abbreviations: ABTS, 2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt; Bu, Butanol; DMEM, Dulbecco's Modified Eagle's Medium; DPPH, 2,2 diphenyl-2-picrylhydrazyl; DS, Dianthus superbus var. longicalysinus; DW, Distilled water; EA, Ethyl acetate; Glu, glucoside; I, Isorhamnentin; K, Kaempferol; LC-MS, Liquid chromatography–mass spectrometry; MDCK, Madin-Darby Canine Kidney; MeOH, Methanol; PBS, Phosphate Buffered Saline; Q, Quercetin; RPMI-1640, Roswell Park Memorial Institute medium; Rha, Rhamnoside; Rut, Rutinoside; SRB, Sulforhodamine B; TFC, Total flavonoid content; TPC, Total polyphenol content ∗ Corresponding author. ∗∗ Co-corresponding author. E-mail addresses: [email protected] (G. Enkhtaivan), [email protected] (S.H. Nile). https://doi.org/10.1016/j.fct.2019.01.013 Received 26 October 2018; Received in revised form 7 December 2018; Accepted 12 January 2019 Available online 14 January 2019 0278-6915/ © 2019 Elsevier Ltd. All rights reserved. D.H. Kim et al. Food and Chemical Toxicology 125 (2019) 313–321 and many vaccines were used as a primary prophylaxis to control in- Different extraction solvents and techniques were used to study its fluenza virus infection. However, due to genetic changes occurred in biological potential and extracts were also evaluated for possible anti- life cycle of influenza virus during infection to human being there is oxidant potential using in vitro assays. Also, we investigated correla- limitation to control influenza pandemics in many regions by using tions between the extracted metabolites for their anticancer, antivirus available drugs of market (Kaiser et al., 2003; Gansukh et al., 2016). and antioxidant properties. Neuraminidase inhibitors such as oseltamivir and zanamivir are com- monly used to control the influenza virus infections but the seasonal 2. Materials and methods influenza crises revealed that some isolates of H1N1 were resistant towards these available commercial drugs (Deyde et al., 2009). Due to 2.1. Chemicals lack of scientific knowledge on aspects of anti-influenza drug devel- opment, safer, inexpensive, and low resistance drugs are needed for the Organic solvents used in extraction such as butanol, ethyl acetate protection of our society (Ozawa et al., 2011). Recent study reveled that and methanol were analytical grade and purchased from Sigma-Aldrich the DS crude leaf extract has been proved to have potent antiviral effect (St. Louis, MO, USA). Acetonitrile purchased from Merk, Drmstadt, against tobacco mosaic virus (Cho et al., 2000). Germany. Folin-ciocalteu's phenol reagent was obtained from Junsei Plants are always utilised as best source of food and for therapeutic Chemicals (Junsei chemical, Japan). 2,2′-Azino-bis(3-ethylbenzothia- purposes in human life due its high nutrients and secondary metabolites zoline-6-sulfonic acid) diammonium salt (ABTS), 2,2 diphenyl-2-pi- composition including flavonoids, phenolics, alkaloids and others crylhydrazyl (DPPH) used for antioxidant estimation and bioactive compounds. Depending on their metabolite content, different Sulforhodamine B (SRB) used for the anticancer study and quercetin, and a wide range of biological activities and mechanisms were observed berberine and gallic acid used as a control for studying anticancer ac- in the human body (Enkhtaivan et al., 2015). In modern day's drugs tivity were obtained from Sigma-Aldrich (Seoul, Korea). HPLC grade from natural origin mainly from folk medicinal plants were applied to distilled water purchased from Duksan Pure Chemicals CO., LTD (Seoul, prevent various infections including viral, bacterial and fungal with South Korea). promising disease control properties against cancer and diseases related to oxidation stress (Yu et al., 2012; Enkhtaivan et al., 2015). The plant 2.2. Cell lines and virus bioactive compounds help to reduce free radical effect as antioxidants and because the conventional wisdom is that antioxidants should lower Influenza viruses (APR/34/8 and B/LEE/40) and Madin-Darby cancer risk by neutralizing cell-damaging, cancer-causing free radicals Canine Kidney (MDCK), human ovary cancer cells (HeLa and SKOV) (Hawk et al., 2016). Dianthus superbus var. longicalysinus (DS) belongs to were provided by ATCC (Manassas, VA, USA). Lung cancer cell (NCL- a genus of Dianthus and the family Caryophyllaceae. DS commonly H1299) and cervix cancer cell (CaSki) were purchased from KCLB grows at high altitudes and is native to European, Asian countries and (Korean Cell line Bank, Seoul, South Korea). RPMI-1640, DMEM widely distributed in Mongolia (Flora GrEIF. 2010). Several species of medium (Dulbecco's Modified Eagle's Medium), fetal bovine serum, Dianthus have been considered medicinally important as they are antibiotic-antimytotic and trypsin-EDTA were supplied by Gibco BRL widely used to treat various infections and diseases in China, Korea, (Grand Island, NY, USA). The cell culture dish and 96 well plates were Iran and Mongolia for millennia (Mutlu et al., 2016; Yun et al., 2016). It purchased from Falcon (BD Bioscience, Franklin Lakes, NJ, USA). is also known as ‘Qumai’ in traditional Chinese medicine (TCM) and widely used to treat urethritis, diuretic, carbuncles, and carcinoma ef- 2.3. Extraction and fractionation of plant material fects, further it is widely used as natural agent for anti-inflammatory and urinary infections (López-Expósito et al., 2011; Yu et al., 2012). The dried plant sample (upper part of plant excluding root) of DS Dianthus
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