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Anticholinesterase, anti-α-glucosidase, antioxidant and antimicrobial effects of four Algerian propolis

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Abstract

This study aimed to investigate the functional properties of four Algerian propolis collected from El-Menia, Oum el Bouaghi, El Harrouch and Collo regions. The total bioactive content, antioxidant, anti-enzymatic and antimicrobial effects of the four propolis methanolic extracts were evaluated using in vitro assays. The highest amount of total phenolic (561.99 ± 3.50 μg GAE/mg E) and flavonoid content (76.98 ± 0.26 μg QE/mg E) was found in propolis from El-Menia. Antioxidant tests (DPPH, ABTS, CUPRAC and ferric reducing power) revealed the strong scavenging and reducing abilities of the extracts. Anti-enzymatic assays against acetylcholinesterase (AChE), butyrylcholinesterase (BChE) and α-glucosidase showed that all extracts possessed a potent inhibitory effect on α-glucosidase better than acarbose and revealed the ability of extracts to inhibit BChE more effectively than AChE. However, the extract of propolis from El Menia was the best inhibitor of the three key enzymes with IC50 values of 11.40 ± 0.58 µg/mL 16.06 ± 0.85 µg/mL and 71.29 ± 2.73 µg/mL against α-glucosidase, BChE and AChE, respectively. The antimicrobial assay indicated that all extracts were mainly active against Gram-positive bacteria and yeast and had bactericidal action in certain bacteria and bacteriostatic action in other ones. However, they had all fungistatic effect on C. albicans ATCC 10231. According to these results, Algerian propolis can be considered as a source of natural bioactive principles for dietary, pharmacological and medicinal applications.

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References

  1. A. Braakhuis, Nutrients (2019). https://doi.org/10.3390/nu11112705

    Article  PubMed  PubMed Central  Google Scholar 

  2. K. Pant, M. Thakur, H.K. Chopra, V. Nanda, M.J. Ansari, G. Pietramellara, S.I. Pathan, S.A. Alharbi, H.S. Almoallim, R. Datta, J King Saudi Univ. Sci. 33(4), 101405 (2021)

    Google Scholar 

  3. M. Oroian, F. Dranca, F. Ursachi, J. Food Sci. Technol. 57, 70–78 (2020)

    CAS  PubMed  Google Scholar 

  4. B.R. D’Arcy, Rural Industries Research and Development Corporation (Australia). Honeybee Research and Development, Antioxidants in Australian Floral Honeys: Identification of Health-enhancing Nutrient Components : A Report for the Rural Industries Research and Development Corporation (Rural Industries Research and Development Corporation, Barton, A.C.T., 2005), http://www.rirdc.gov.au/reports/HBE/05-040.pdf

  5. N. Segueni, A. Zellagui, F. Moussaoui, M. Lahouel, S. Rhouati, Arab. J. Chem. 9(Suppl. 1), S425–S428 (2016)

    CAS  Google Scholar 

  6. N. Segueni, A.A. Magid, M. Decarme, S. Rhouati, M. Lahouel, F. Antonicelli, C. Lavaud, W. Hornebeck, Planta Med. 77, 999–1004 (2011)

    CAS  PubMed  Google Scholar 

  7. A. Bouaroura, N. Segueni, J.G. Diaz, C. Bensouici, S. Akkal, S. Rhouati, Nat. Prod. Res. 34(22), 3257–3261 (2020)

    CAS  PubMed  Google Scholar 

  8. M. Debab, F. Toumi-Benali, M.M. Dif, Phytothérapie 15(4), 230–234 (2017)

    CAS  Google Scholar 

  9. N. Segueni, D. Evren, S. Akkal, O. Beraat Özçelik, S. Rhouati, Pak. J. Pharm. Sci. 30(4), 1417–1423 (2017)

    Google Scholar 

  10. H. Brihoum, M. Maiza, H. Sahali, M. Boulmeltout, G. Barratt, L. Benguedouar, M. Lahouel, Braz. J. Pharm. Sci. (2018). https://doi.org/10.1590/s2175-97902018000117396

    Article  Google Scholar 

  11. K. Boutabet, W. Kebsa, M. Alyane, M. Lahouel, Indian J. Nephrol. 21(2), 101–106 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. N. Nedji, W. Loucif-Ayad, Asian Pac. J. Trop. Dis. 4(6), 433–437 (2014)

    CAS  Google Scholar 

  13. M.Y. Boufadi, J. Soubhye, P. Van Antwerpen, J. Food Biochem. (2021). https://doi.org/10.1111/jfbc.13663

    Article  PubMed  Google Scholar 

  14. M. Debab, F. Toumi-Benali, H. Salem, Phytothérapie 17(4), 206–210 (2019)

    Google Scholar 

  15. E.K. Soltani, R. Cerezuela, N. Charef, S. Mezaache-Aichour, M.A. Esteban, M.M. Zerroug, Fish Shellfish Immunol. 62, 57–67 (2017)

    CAS  PubMed  Google Scholar 

  16. S. Boulechfar, A. Zellagui, A.E. Chemsa, C. Bensouici, N. Segueni, M. Lahouel, M. Öztürk, M.E. Duru, J. Biol. Act. Prod. Nat. 9(6), 434–444 (2019)

    CAS  Google Scholar 

  17. Y.K. Park, M. Ikegaki, Biosci. Biotech. Biochem. 62(11), 2230–2232 (1998)

    CAS  Google Scholar 

  18. V.L. Singleton, J.A. Rossi, Am. J. Enol. Vitic. 16(3), 144–158 (1965)

    CAS  Google Scholar 

  19. A. Djeridane, M. Yousfi, B. Nadjemi, D. Boutassouna, P. Stocker, N. Vidal, Food Chem. 97(4), 654–660 (2006)

    CAS  Google Scholar 

  20. L. Akhbariye, N. Zamindar, S. Nasiri, S. Paidari, M. Goli, H. Abbasi, J. Food Meas. Charact. (2021). https://doi.org/10.1007/s11694-021-01073-8

    Article  Google Scholar 

  21. M.S. Blois, Nature 181, 1119–1200 (1958)

    Google Scholar 

  22. R. Re, N. Pellegrini, A. Proteggente, A. Pannala, M. Yang, C. Rice-Evans, Free Radic. Biol. Med. 26(9–10), 1231–1237 (1999)

    CAS  PubMed  Google Scholar 

  23. R. Apak, K. Guclu, M. Ozyurek, S.E. Karademir, J. Agric. Food Chem. 52(26), 7970–7981 (2004)

    CAS  PubMed  Google Scholar 

  24. M. Oyaizu, Jpn. J. Nutr. 44(6), 307–315 (1986)

    CAS  Google Scholar 

  25. G.L. Ellman, K.D. Courtney, J.R.V. Andres, R.M. Featherstone, Biochem. Pharmacol. 7(2), 88–95 (1961)

    CAS  PubMed  Google Scholar 

  26. M. Öztürk, U. Kolak, G. Topçu, S. Öksüz, M.I. Choudhary, Food Chem. 126(1), 31–38 (2011)

    Google Scholar 

  27. S. Lordan, T.J. Smyth, A. Soler-Vila, C. Stanton, R.P. Ross, Food Chem. 141(3), 2170–2176 (2013)

    CAS  PubMed  Google Scholar 

  28. P.R. Murray, E.J. Baron, M.A. Pfaller, F.C. Tenover, R.H. Yolken, Manual of Clinical Microbiology, 6th edn. (ASM Press, Washington, 1995), pp. 457–464

    Google Scholar 

  29. N.M. Asl, H. Ahari, A.A.M. Moghanjoghi, S. Paidari, J. Food Meas. Charact. (2021). https://doi.org/10.1007/s11694-021-01082-7

    Article  Google Scholar 

  30. E.W. Koneman, S.D. Allen, W.M. Janda, P.C. Scherckenberger, W.C. Winn, Color Atlas and Textbook of Diagnostic Microbiology, 5th edn. (Lippincott-Raven, Philadelphia, 1997)

    Google Scholar 

  31. N. Krishnan, S. Ramanathan, S. Sasidharan, V. Murugaiyah, S.M. Mansor, Int. J. Pharmacol. 6(4), 510–514 (2010)

    Google Scholar 

  32. K.C. Hazen, J. Am. Acad. Dermatol. 38(5), S37-41 (1998)

    CAS  PubMed  Google Scholar 

  33. D. Lin, M. Xiao, J. Zhao, Z. Li, B. Xing, X. Li, M. Kong, L. Li, Q. Zhang, Y. Liu, Molecules 21(10), 1374 (2016)

    PubMed Central  Google Scholar 

  34. V. Lagouri, D. Prasianaki, F. Krysta, Int. J. Food Prop. 17(3), 511–522 (2014)

    CAS  Google Scholar 

  35. S. Misir, Y. Aliyazicioglu, S. Selim Demir, I. Turan, S.O. Yaman, O. Deger, Indian J. Pharm. Educ. Res. 52(1), 94–100 (2018)

    CAS  Google Scholar 

  36. M.D. Jobir, A. Belay, J. Apither. 7(2), 31–48 (2020)

    Google Scholar 

  37. V. Bankova, M. Popova, B. Trusheva, Chem. Cent. J. 8(1), 28 (2014)

    PubMed  PubMed Central  Google Scholar 

  38. A. Sorucu, H.H. Oruç, J. Food Meas. Charact. 13, 2461–2469 (2019)

    Google Scholar 

  39. N.E. Bayram, Y.C. Gerçek, S. Bayram, B. Toğar, J. Food Meas. Charact. (2019). https://doi.org/10.1007/s11694-019-00340-z

    Article  Google Scholar 

  40. J.B. Daleprane, D.S. Abdalla, Evid.-Based Compl. Altern. Med. (2013). https://doi.org/10.1155/2013/175135

    Article  Google Scholar 

  41. A. Rebiai, T. Lanez, M.L. Belfar, Int. J. Pharmacol. 7(1), 113–118 (2011)

    CAS  Google Scholar 

  42. A.L. Piccinelli, T. Mencherini, R. Celano, Z. Mouhoubi, A. Tamendjari, R. Aquino, L. Rastrelli, J. Agric. Food Chem. 61(21), 5080–5088 (2013)

    CAS  PubMed  Google Scholar 

  43. E.K. Soltani, K. Mokhnache, N. Charef, J. Drug Deliv. Ther. 10(1), 1–4 (2020)

    CAS  Google Scholar 

  44. M.I.N. Moreno, M.I. Isla, A.R. Sampietro, M.A. Vattunon, J. Ethnopharmacol. 71(1–2), 109–114 (2000)

    CAS  PubMed  Google Scholar 

  45. T. Hamasaka, S. Kumazawa, T. Fujimoto, T. Nakayama, Food Sci. Technol. Res. 10(1), 86–92 (2004)

    CAS  Google Scholar 

  46. S. Bendjabeur, O. Benchabane, C. Bensouici, M. Hazzit, A. Baaliouamer, A. Bitam, J. Food Meas. Charact. 12, 2278–2288 (2018)

    Google Scholar 

  47. I. Orhan, Q. Naz, M. Kartal, F. Tosun, B. Şener, Z. Naturforsch. C 62(9–10), 684–688 (2007)

    CAS  PubMed  Google Scholar 

  48. L.L. Chaillou, M.A. Nazareno, J. Sci. Food Agric. 89, 978–983 (2009)

    CAS  Google Scholar 

  49. S. El-Guendouz, S. Aazza, B. Lyoussi, M.D. Antunes, M.L. Faleiro, M.G. Miguel, Int. J. Food Sci. Technol. 51(8), 1762–1773 (2016)

    CAS  Google Scholar 

  50. N. Baltas, O. Yildiz, S. Kolayli, J. Enzyme Inhib. Med. Chem. 31(sup1), 52–55 (2016)

    CAS  PubMed  Google Scholar 

  51. F.K. Abd El-Hady, A.M.A. Souleman, I.G. Ibrahim, M.S. Abdel-Aziz, Z.A. El-Shahid, E.A. Ali, M.S.A. Der Elsarrag, Pharm. Lett. 8(19), 339–350 (2016)

    CAS  Google Scholar 

  52. A. Abirami, G. Nagarani, P. Siddhuraju, Food Sci. Hum. Well. 3(1), 16–25 (2014)

    Google Scholar 

  53. C. Proença, M. Freitas, D. Ribeiro, E.F.T. Oliveira, J.L.C. Sousa, S.M. Tomé, M.J. Ramos, A.M.S. Silva, P.A. Fernandes, E. Eduarda Fernandes, J. Enzyme Inhib. Med. Chem. 32(1), 1216–1228 (2017)

    PubMed  PubMed Central  Google Scholar 

  54. R.E.A. Taleb, N. Djebli, H. Chenini, H. Sahin, S. Kolayli, J. Food Biochem. 44(7), 1–13 (2020)

    Google Scholar 

  55. N. Ibrahim, N.F.S.M. Niza, M.M.M. Rodi, A.J. Zakaria, Z. Ismail, K.S. Mohd. Malaya, J. Anal. Sci. 20(2), 413–422 (2016)

    Google Scholar 

  56. M. Popova, B. Lyoussi, S. Aazza, D. Antunes, V. Bankova, G. Miguel, Nat. Prod. Commun. 10(11), 1961–1964 (2015)

    PubMed  Google Scholar 

  57. D.F. Pereira, L.H. Cazarolli, C. Lavado, V. Mengatto, M.S.R.B. Figueiredo, A. Guedes, M.G. Pizzolatti, F.R.M.B. Silva, Nutrition 27(11–12), 1161–1167 (2011)

    PubMed  Google Scholar 

  58. M.A. Asgar, Int. J. Food Prop. 16, 91–103 (2013)

    CAS  Google Scholar 

  59. Y.M. Boufadi, J. Soubhye, J. Nève, P. Van Antwerpen, A. Riazi, Int. J. Food Sci. Technol. 51(12), 2613–2620 (2016)

    CAS  Google Scholar 

  60. N. Mewari, P. Kumar, Pharm. Biol. 46(10–11), 819–822 (2008)

    CAS  Google Scholar 

  61. G. Chamandi, Z. Olama, H. Holail, Int. J. Curr. Microbiol. App. Sci. 4(4), 328–342 (2015)

    CAS  Google Scholar 

  62. S. Boisard, A. Le Ray, A. Landreau, M. Kemf, V. Cassisa, C. Flurin, P. Richomme, Evid.-Based Compl. Altern. Med. (2015). https://doi.org/10.1155/2015/319240

    Article  Google Scholar 

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Acknowledgements

Authors are grateful and thank the beekeepers Bilel Chellat, Yassine Hadjem, Hocine Semouma and Laidi Zaier who supplied Apis mellifera propolis samples from El-Menia, Oum el Bouaghi, El Harrouch and Collo regions, respectively. The financial support from Algerian Ministry of Higher Education and Scientific Research and DGRSDT is gratefully acknowledged.

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Authors and Affiliations

  1. Department of Biochemistry, Molecular and Cellular Biology, Faculty of Nature and Life Sciences, Mentouri University, 25000, Constantine, Algeria

    Safia Boulechfar

  2. Laboratory of Biomolecules and Plant Breeding, Department of Nature and Life Sciences, Faculty of Exact Sciences, Nature and Life Sciences, University of Larbi Ben Mhidi Oum El Bouaghi, Oum El Bouaghi, Algeria

    Safia Boulechfar & Amar Zellagui

  3. Research Center of Biotechnology, Ali Mendjli UV 03 BP E73, 25000, Constantine, Algeria

    Chawki Bensouici & Djeghim Hanene

  4. Department of Biotechnology, Faculty of Arts and Sciences, Aksaray University, 68100, Aksaray, Turkey

    Meltem Asan-Ozusaglam & Songul Tacer

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  1. Safia Boulechfar
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  2. Amar Zellagui
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  3. Chawki Bensouici
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Contributions

SB: data curation, formal analysis, investigation, visualization, writing-original draft, writing-review & editing. AZ: project administration, supervision, validation, visualization, writing-review & editing. CB: supervision, methodology, resources, data curation, validation, writing-review & editing. MA-O: supervision, methodology, resources, data curation, validation, writing-review & editing. ST: resources, data curation. HD: resources, data curation.

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Correspondence to Safia Boulechfar.

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Boulechfar, S., Zellagui, A., Bensouici, C. et al. Anticholinesterase, anti-α-glucosidase, antioxidant and antimicrobial effects of four Algerian propolis. Food Measure 16, 793–803 (2022). https://doi.org/10.1007/s11694-021-01203-2

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