Effective inhibition of bacterial sialidases by phenolic acids and flavonoids

Year 2024, Volume: 11 Issue: 3, 514 - 521, 29.08.2024

Yana Gocheva , Milena Nikolova , Stephan Engıbarov Irina Lazarkevich Rumyana Eneva

https://doi.org/10.21448/ijsm.1408367

Abstract

As a pathogenicity factor in some microorganisms, sialidase is a key target for inactivation, as this would have curative and preventive effects on various diseases. Significant results are already achieved with viral sialidase inhibitors, while such studies on bacterial enzymes are scarce. Pure natural compounds representing phenols and flavonoids, were tested for their inhibitory effect on sialidases from Vibrio cholerae non-O1, Arthrobacter nicotianae and Oerskovia paurometabola. All three enzymes were isolated, purified beforehand and stored under suitable conditions. Quinic and gallic acids showed the highest inhibitory activity - 76 to 100% against the three sialidases. Fisetin had a significant inhibitory activity on two of the enzymes. The structurally related thymol and thymoquinone exerted from 80 to 100% inhibition on at least one of the enzymes. Catechin and rutin had significant inhibitory activity, varying from 49 to 100%, on some of the enzymes. Quercetin, known for its inhibitory effect on viral sialidases, had a lesser impact on the studied enzymes. The suppressive effect of quinic acid, rutin and fisetin on bacterial sialidases is observed for the first time.

Keywords

Bacterial sialidases, Inhibitors, Phenolic acids, Flavonoids

References

• Abrashev, I., Velcheva, P., Nikolov, P., & Kourteva, J. (1980). Substrate for colorimetric determination of enzyme activity. Bulgarian patent N 47647/IIR
• Abrashev, I., Dulguerova, G., Dolashka-Angelova, P., & Voelter, W. (2005). Purification and Characterization of a Novel Sialidase from a Strain of Arthrobacter nicotianae. Journal of Biochemistry, 137(3), 365-371. https://doi.org/10.1093/jb/mvi053
• Baell, J.B. (2016). Feeling nature’s PAINS: natural products, natural product drugs, and pan assay interference compounds (PAINS). Journal of Natural Products, 79(3), 616-628. https://doi.org/10.1021/acs.jnatprod.5b00947
• Brittan, J.L., Buckeridge, T.J., Finn, A., Kadioglu, A., & Jenkinson, H.F. (2012). Pneumococcal neuraminidase A: an essential upper airway colonization factor for Streptococcus pneumoniae. Molecular Oral Microbiology, 27(4), 270-283. https://doi.org/10.1111/j.2041-1014.2012.00658.x
• Chon, H. (2012). Medicinal Herbs and Plant Extracts for Influenza: Bioactivity, Mechanism of Anti-influenza Effects, and Modulation of Immune Responses. Studies in Natural Products Chemistry, Elsevier, https://doi.org/10.1016/B978-0-444-59530-0.00011-3
• Corfield, T. (1992). Bacterial sialidases - roles in pathogenicity and nutrition. Glycobiology, 2(6), 509-521. https://doi.org/10.1093/glycob/2.6.509
• Dubey, S., Ganeshpurkar, A., Ganeshpurkar, A., Bansal, D., & Dubey, N. (2017). Glycolytic enzyme inhibitory and antiglycation potential of rutin. Future Journal of Pharmaceutical Sciences, 3(2), 158-162. https://doi.org/10.1016/j.fjps.2017.05.005
• Eneva, R., Engibarov, A., Petrova, P., Abrashev, R., Strateva, T., Kolyovska, V., & Abrashev, I. (2015). High production of neuraminidase by a Vibrio cholerae non-O1 strain-the first possible alternative to toxigenic producers. Applied Biochemistry and Biotechnology, 176, 412-427. https://doi.org/10.1007/s12010-015-1584-4
• Eneva, R., Engibarov, S., Gocheva, Y., Mitova, S., Arsov, A., Petrov, K., Abrashev, R., Lazarkevich, I., & Petrova, P. (2022). Safe sialidase production by the saprophyte Oerskovia paurometabola: Gene sequence and enzyme purification. Molecules, 27(24), 8922. https://doi.org/10.3390/molecules27248922
• Escobar, A., Perez, M., Romanelli, G., & Blustein, G. (2020). Thymol bioactivity: A review focusing on practical applications. Arabian Journal of Chemistry, 13(12), 9243-9269. https://doi.org/10.1016/j.arabjc.2020.11.009
• Farina, V., & Brown, J.D. (2006), Tamiflu: The Supply Problem. Angewandte Chemie International Edition, 45(44) 7330-7334. https://doi.org/10.1002/anie.200602623
• Farkhondeh, T., Samarghandian, S., & Borji, A. (2017). An overview on cardioprotective and anti-diabetic effects of thymoquinone. Asian Pacific Journal of Tropical Medicine, 10(9), 849-854. https://doi.org/10.1016/j.apjtm.2017.08.020
• Ganeshpurkar, A., & Saluja, A.K. (2017). The pharmacological potential of rutin. Saudi Pharmaceutical Journal, 25(2), 149-164. https://doi.org/10.1016/j.jsps.2016.04.025
• Gattani, A., Kumar, A., Agrawal, A., Khan, M.H., Mahawar, M., Bag, S., Rajak, K.K., Singh, R.K., & Singh, P. (2020). An electrochemical impedance sensor for monitoring of gallic acid inhibited neuraminidase activity of PPR HN protein. Microchemical Journal, 158, 105229. https://doi.org/10.1016/j.microc.2020.105229
• Giacopuzzi, E., Bresciani, R., Schauer, R., Monti, E., Borsani, G. (2012) New insights on the sialidase protein family revealed by a phylogenetic analysis in Metazoa. PLoS One, 7(8), e44193. https://doi.org/10.1371/journal.pone.0044193
• Gonçalves, S., & Romano, A. (2017). Inhibitory properties of phenolic compounds against enzymes linked with human diseases. Phenolic Compounds-biological Activity, INTECH, http://dx.doi.org/10.5772/66844
• Grienke, U., Schmidtke, M., von Grafenstein, S., Kirchmair, J., Liedl, K.R., & Rollinger, J.M. (2012). Influenza neuraminidase: a druggable target for natural products. Natural Product Reports, 29(1), 11-36. https://doi.org/10.1039/C1NP00053E
• Haslam, E., & Cai, Y. (1994). Plant polyphenols (vegetable tannins): gallic acid metabolism. Natural Product Reports, 11, 41-66. https://doi.org/10.1039/NP9941100041
• Isemura, M. (2019). Catechin in human health and disease. Molecules, 24(3), 528. https://doi.org/10.3390/molecules24030528
• Kim, M., Kim, S.Y., Lee, H.W., Shin, J.S., Kim, P., Jung, Y.S., ... & Lee, C.K. (2013). Inhibition of influenza virus internalization by (−)-epigallocatechin-3-gallate. Antiviral Research, 100(2), 460-472. https://doi.org/10.1016/j.antiviral.2013.08.002
• Kowalczyk, A., Przychodna, M., Sopata, S., Bodalska, A., & Fecka, I. (2020). Thymol and thyme essential oil—new insights into selected therapeutic applications. Molecules, 25(18), 4125. https://doi.org/10.3390/molecules25184125
• Li, J., Sayeed, S., Robertson, S., Chen, J., McClane, B.A. (2011) Sialidases affect the host cell adherence and epsilon toxin-induced cytotoxicity of Clostridium perfringens type D strain CN3718. PLoS Pathogenes, 7(12), e1002429. https://doi.org/10.1371/journal.ppat.1002429
• Liu, A.L., Wang, H.D., Lee, S.M., Wang, Y.T., & Du, G.H. (2008). Structure–activity relationship of flavonoids as influenza virus neuraminidase inhibitors and their in vitro anti-viral activities. Bioorganic & Medicinal Chemistry, 16(15), 7141 7147. https://doi.org/10.1016/j.bmc.2008.06.049
• Meindl, P., Bodo, G., Palese, P., Schulman, J., & Tuppy, H. (1974). Inhibition of neuraminidase activity by derivatives of 2-deoxy-2, 3-dehydro-N-acetylneuraminic acid. Virology, 58(2), 457-463. https://doi.org/10.1016/0042-6822(74)90080-4
• Mercader, A.G., & Pomilio, A.B. (2010). QSAR study of flavonoids and biflavonoids as influenza H1N1 virus neuraminidase inhibitors. European Journal of Medicinal Chemistry, 45(5), 1724-1730. https://doi.org/10.1016/j.ejmech.2010.01.005
• Mueller, P., & Downard, K.M. (2015). Catechin inhibition of influenza neuraminidase and its molecular basis with mass spectrometry. Journal of Pharmaceutical and Biomedical Analysis, 111, 222-230. https://doi.org/10.1016/j.jpba.2015.03.014
• Rahman, M.M., Rahaman, M.S., Islam, M.R., Rahman, F., Mithi, F.M., Alqahtani, T., Almikhlafi, Alghamdi, S.Q., Alruwaili, A.S., Hossain, M.S., Ahmed, M., Das, R., Emran, T.B., & Uddin, M.S. (2021). Role of phenolic compounds in human disease: current knowledge and future prospects. Molecules, 27(1), 233. https://doi.org/10.3390/molecules27010233
• Rosas, E.C., Correa, L.B., & das Graças Henriques, M. (2019). Antiinflammatory properties of Schinus terebinthifolius and its use in arthritic conditions. In Bioactive food as dietary interventions for arthritis and related inflammatory diseases. Academic Press. https://doi.org/10.1016/B978-0-12-813820-5.00028-3
• Sadati, S.M., Gheibi, N., Ranjbar, S., & Hashemzadeh, M.S. (2019). Docking study of flavonoid derivatives as potent inhibitors of influenza H1N1 virus neuraminidase. Biomedical Reports, 10(1), 33-38. https://doi.org/10.3892/br.2018.1173
• Sahu, B.D., Kalvala, A.K., Koneru, M., Mahesh Kumar, J., Kuncha, M., Rachamalla, S.S., & Sistla, R. (2014). Ameliorative effect of fisetin on cisplatin-induced nephrotoxicity in rats via modulation of NF-κB activation and antioxidant defence. PloS one, 9(9), e105070. https://doi.org/10.1371/journal.pone.0105070
• Schauer, R., Kamerling, J.P. (2018), Exploration of the Sialic Acid Advances in Carbohydrate Chemistry and Biochemistry, Academic Press; https://doi.org/10.1016/bs.accb.2018.09.001
• Slack, T.J., Li, W., Shi, D., McArthur, J.B., Zhao, G., Li, Y., Xiao, A., Khedri, Z., Yu, H., Liu, Y., & Chen, X. (2018). Triazole-linked transition state analogs as selective inhibitors against V. cholerae sialidase. Bioorganic & Medicinal Chemistry, 26(21), 5751-5757. https://doi.org/10.1016/j.bmc.2018.10.028
• Son, Y.G., Kim, J.Y., Park, J.Y., Kim, K.D., Park, K.H., & Kim, J.Y. (2023). Inhibitory Potential of Quercetin Derivatives Isolated from the Aerial Parts of Siegesbeckia pubescens Makino against Bacterial Neuraminidase. Molecules, 28(14), 5365. https://doi.org/10.3390/molecules28145365
• Uchida, Y., Tsukada, Y., & Sugimori, T. (1977). Distribution of neuraminidase in Arthrobacter and its purification by affinity chromatography. The Journal of Biochemistry, 82(5), 1425-1433.
• Vuolo, M.M., Lima, V.S., & Maróstica Junior, M.R. (2019). Phenolic Compounds: Structure, classification, and antioxidant power. In Bioactive Compounds. Woodhead Publishing. https://doi.org/10.1016/B978-0-12-814774-0.00002-5
• Wang, G., Wang, Y., Yao, L., Gu, W., Zhao, S., Shen, Z., Lin, Z., Liu, W., & Yan, T. (2022). Pharmacological activity of quercetin: an updated review. Evidence-Based Complementary and Alternative Medicine, Article ID 3997190. https://doi.org/10.1155/2022/3997190