Characterization of Neuraminidase Inhibitors in Korean Papaver rhoeas Bee Pollen Contributing to Anti-Influenza Activities In Vitro

Abstract

Bee pollen is a granule-type material of agglutinated flower pollen made by worker honey bees with nectar and bee secretions. The resulting pollen is higher in nutritional value than untreated pollen, and is used as the primary source of protein for the bee hive. Bee pollen has been used in folk medicine from ancient times in many regions of the world for its medical properties to alleviate or cure conditions such as colds, flu, ulcers, and anemia [1]. Recently, biological effects such as antiox- [7], and antimutagenic [8] activities were also reported. Like other apicultural products, royal jelly, honey, and propolis, the chemical composition of bee pollen depends on the plant source, regional vegetation, season, and honeybee races at the site of collection. It is rich in carbohydrates, proteins, lipids, minerals, vitamins, and various organic compounds, including phenolic acids and flavonoids. Most flavonoids from bee pollen exist as glycosides and contain kaempferol or quercetin as aglycone parts. Other phenolic acids usually found in Abstract !The active constituents of Korean Papaver rhoeas bee pollen conferring neuraminidase inhibitory activities (H1N1, H3N2, and H5N1) were investigated. Six flavonoids and one alkaloid were isolated and characterized by nuclear magnetic resonance and mass spectrometry data. These included kaempferol-3-sophoroside (1), kaempferol-3-neohesperidoside (2), kaempferol-3-sambubioside (3), kaempferol-3-glucoside (4), quercetin-3-sophoroside (5), luteolin (6), and chelianthifoline (7). All compounds showed neuraminidase inhibitory activities with IC 50 values ranging from 10.7 to 151.1 µM. The most potent neuraminidase inhibitor was luteolin, which was the dominant content in the ethyl acetate fraction. All tested compounds displayed noncompetitive inhibition of H3N2 neuraminidase. Furthermore, compounds 1-7 all reduced the severity of virally induced cytopathic effects as determined by the Madin-Darby canine kidney cell-based assay showing antiviral activity with IC 50 values ranging from 10.7 to 33.4 µM (zanamivir: 58.3 µM). The active compounds were quantified by highperformance liquid chromatography, and the total amount of compounds 1-7 made up about 0.592 g/100 g bee pollen, contributing a rich resource of a natural antiviral product. Abbreviations

Potential anti-influenza effective plants used in Turkish folk medicine: A review

“… Vimalanathan and Hudson (2012) Origanum vulgare L. Not specified (Essential oil) Linalool (Essential oil) Linalool (Essential oil) Reduce visible cytopathic effects of influenza A/WS/33 virus activity by > 52.8%. Choi (2018) Papaver rhoeas L. Kaempferol-3-sophoroside, Kaempferol-3-neohesperidoside, Kaempferol-3-sambubioside, Kaempferol-3-glucoside, Quercetin-3-sophoroside, Luteolin, Chelianthifoline (Pollen) Display noncompetitive inhibition of H3N2 neuraminidase and reduce the severity of virally induced cytopathic effects Lee et al (2016) Peganum harmala L. Not specified (Seeds) Inhibit cytopathic effect of influenza virus Moradi et al (2017) Pimpinella anisum L. Not specified (Essential oil) Linalool (Essential oil) Linalool (Essential oil) Reduce visible cytopathic effects of influenza A/WS/33 virus activity by > 52.8%. Choi (2018) Portulaca oleracea L. Not specified (Aerial parts) Suppress the production of circulating H1N1 and H3N2 and inhibit the binding of virus to cells and decrease the viral load within 10 min to prevent viral infection Li et al (2019) Punica granatum L. Not specified (Seeds) Inhibit cytopathic effect of influenza virus Moradi et al (2017) Punica granatum L. Ellagic acid, Caffeic acid, Luteolin, and Punicalagin (Fruit juice) Suppress replication of influenza A virus and inhibit viral RNA replication and agglutination of chicken red blood cells by influenza virus Haidari et al (2009) Salvia fruticosa Mill.…”

Can network pharmacology identify the anti-virus and anti- inflammatory activities of Shuanghuanglian oral liquid used in Chinese medicine for respiratory tract infection?

“…Luteolin is proved to have significant protective effects of antivirus and anti-inflammatory in vivo. As a kind of neuraminidase inhibitors, luteolin could effectively inhibit the replication of the influenza virus and spread in the virus particle surface [44]. Also, luteolin possesses the ability to hinder acute respiratory syndrome coronavirus (SARS-CoV) to enter the host cells by binding avidly to the SARS-CoV inhibited protein [45].…”

Transcriptome Profiling of Two Ornamental and Medicinal Papaver Herbs

“…Therefore, Papaver species are used to retain the insect biodiversity in isolate settings [ 17 ]. Interestingly, the pollen collected by honey bees is used in folk medicine to treat various symptoms [ 18 ]. Other than these uses, Papaver plants are widely used as a raw material in industries to isolate alkaloid drug components [ 19 ], and so far, more than 170 alkaloids have been isolated from these species [ 20 ].…”