Evaluation of potential anti-aging effects of Achillea phrygia Boiss. & Balansa (Asteraceae)

Year 2024, Volume: 11 Issue: 4, 646 - 657, 03.11.2024

Rukiye Boran Gülen , Nurdan Saraç , Aysel Uğur

https://doi.org/10.21448/ijsm.1401681

Abstract

This study aims to determine the anti-aging effects of Achillea phrygia, an endemic plant, by evaluating its sun protection factor (SPF) level, antioxidant activity, total phenolic content, extracellular matrix-degrading enzymes (ECM) inhibition, genotoxic/anti-genotoxic, and cytotoxic activities. The SPF level was assessed using an in vitro quantitative method, while antioxidant capacity was determined through DPPH, β-carotene, and hydroxyl-radical (H2O2) scavenging assays. The total phenolic content was quantitatively conducted using the Folin Ciocalteu reagent. The inhibition of ECM-degrading enzymes was determined using matrix metalloproteinase-1 (MMP-1), hyaluronidase, and elastase enzymes. Genotoxic/anti-genotoxic properties were assessed using the AMES Salmonella/microsome assay, and cytotoxicity effects were assessed through the MTT assay. The results indicated that A. phrygia showed moderate SPF activity (SPF = 4.013) and exhibited IC50 values of 0.183 ± 0.03, 0.079 ± 0.51, and 1.18 ± 0.35 mg/mL for DPPH, β-carotene, and hydroxyl-radicals, respectively. The total phenolic content was measured to be 23.56 ± 1.42 mg GAE/g dry extract. Furthermore, the extract demonstrated inhibition of MMP-1 (47.98%) and elastase (39.2%) activities. Importantly, it did not induce DNA damage and showed antigenotoxic activity ranging from 10% to 65.6%. The cytotoxicity assay revealed an IC50 value of 42.41±4.05 µg/mL. These findings suggest that A. phrygia could be utilized as a cosmetic ingredient in skincare products due to its ability to protect against UV radiation, exhibit antioxidant properties, prevent extracellular matrix degradation, and inhibit DNA damage.

Keywords

Achillea phrygia, Skin-care, Antioxidant, Enzyme inhibition, Anti-genotoxicity

References

• Afshari, M., Rahimmalek, M., & Miroliaei, M. (2018). Variation in polyphenolic profiles, antioxidant and antimicrobial activity of different Achillea species as natural sources of antiglycative compounds. Chemistry & Biodiversity, 15(8), e1800075.
• Agar, O.T., Dikmen, M., Ozturk, N., Yilmaz, M.A., Temel, H., & Turkmenoglu, F.P. (2015). Comparative studies on phenolic composition, antioxidant, wound healing and cytotoxic activities of selected Achillea L. species growing in Turkey. Molecules, 20(10), 17976-18000.
• Akyil, D., Oktay, S., Liman, R., Eren, Y., & Konuk, M. (2012). Genotoxic and mutagenic effects of aqueous extract from aerial parts of Achillea teretifolia. Turkish Journal of Biology, 36(4), 441-448.
• Alnuqaydan, A.M., & Sanderson, B.J. (2016). Toxicity and Genotoxicity of Beauty Products on Human Skin Cells In Vitro. Journal of Clinical Toxicology, 6(4), 1 9. https://doi.org/10.4172/2161-0495.1000315
• Anlaş, C., Bakirel, T., Ustuner, O., Ustun-Alkan, F., Diren-Sigirci, B., Koca-Caliskan, U., Mancak-Karakus, M., Dogan, U., Ak, S., Akpulat, H.A. (2023). In vitro biological activities and preliminary phytochemical screening of different extracts from Achillea sintenisii Hub- Mor. Arabian Journal of Chemistry, 16(1), 104426
• Anlaş, C., Bakirel, T., Çalişkan, U.K., Dönmez, C., Alkan, F.Ü., & Keleş, O.Ü. (2022). In vitro cytotoxicity and genotoxicity screening of Cuscuta arvensis Beyr. and Achillea wilhelmsii C. Koch. Journal of Research in Veterinary Medicine, 41(2), 143-149.
• Aronson, J.K. (2016). Asteraceae. Meyler's Side Effects of Drugs (Sixteenth Edition). The International Encyclopedia of Adverse Drug Reactions and Interactions. Elsevier.
• Barak, T.H., Kurt-Celep, I., Dilek-Tepe, H., Bardakcı, H., Akaydın, G., Yesilada, E., & Celep, E. (2023). In vitro assessment of dermatological activity potential of Achillea clypeolata Sm. in H2O2-treated human dermal fibroblasts. South African Journal of Botany, 160, 1-8.
• Barda, C., Grafakou, M. E., Tomou, E. M., & Skaltsa, H. (2021). Phytochemistry and evidence-based traditional uses of the genus Achillea L.: an update (2011–2021). Scientia Pharmaceutica, 89(4), 50.
• Barrantes, E., & Guinea, M. (2003). Inhibition of collagenase and metalloproteinases by aloins and aloe gel. Life Sciences, 72, 843–850. https://doi.org/10.1016/S0024-3205(02)02308-1
• Başer, K.H.C. (2016). Essential Oils of Achillea Species of Turkey. Natural Volatiles and Essential Oils, 3(1), 1–14.
• Becker, L.C., Bergfeld, W.F., Belsito, D.V., Hill, R.A., Klaassen, C.D., Liebler, D.C., Marks, J.G., Shank, R.C., Slaga, T.J., Snyder, P.W., & Andersen, F.A. (2016). Safety Assessment of Achillea millefolium as used in cosmetics. International Journal of Toxicology, 35(3), 5-15. https://doi.org/10.1177/1091581816677717
• Cefali, L.C., Ataide, J.A., Moriel, P., Foglio, M.A., & Mazzola, P.G. (2016). Plant‐based active photoprotectants for sunscreens. International Journal of Cosmetic Science, 38(4), 346-353.
• Choquenet, B., Couteau, C., Paparis, E., & Coiffard, L.J.M. (2008). quercetin and rutin as potential sunscreen agents: determination of efficacy by an in vitro method. Journal of Natural Products, 71, 1117–1118. https://doi.org/10.1021/np7007297
• Deniz, L., Serteser, A., & Kargıoglu, M. (2010). Local names and ethnobotanical features of some plants in Usak University (Usak) and its near vicinity. AKÜ Fen Bilimleri Dergisi, 10, 57–72.
• Doğan, M., Taşkın, D., Ermanoğlu, M., & Arabacı, T. (2022). Characterization of nanoparticles containing Achillea phrygia and their antioxidant and antiproliferative properties. Cumhuriyet Science Journal, 43(1), 27-32. https://doi.org/10.17776/csj.1056496
• Düsman, E., Almeida, I.V.D., Coelho, A.C., Balbi, T.J., Düsman Tonin, L.T., & Vicentini, V. E.P. (2013). Antimutagenic effect of medicinal plants Achillea millefolium and Bauhinia forficata in vivo. Evidence-Based Complementary and Alternative Medicine, 2013.
• Ebrahimabadi, A.H., Mazoochi, A., Kashi, F.J., Djafari-Bidgoli, Z., & Batooli, H. (2010). Essential oil composition and antioxidant and antimicrobial properties of the aerial parts of Salvia eremophila Boiss. from Iran. Food and Chemical Toxicology, 48(5), 1371–1376. https://doi.org/10.1016/j.fct.2010.03.003
• Eruygur, N., Buyukyildirim, T., Tetik Rama, S., Ayaz, F., Tekin, M., Tuzcu, M., ... & Abdullah Yilmaz, M. (2023). Phytochemical profiling and biological activity of Achillea sintenisii Hub.‐Mor. Chemistry & Biodiversity, 20(6), e202201258.
• FDA. (2013). Food and Drug Administration. Sunscreen drug products for over-the-counter human use. Code of Federal Regulations. Title 21, v. 5.
• Fibrich, B.D., & Lall, N. (2018). Chapter 3: Fighting the Inevitable: Skin Aging and Plants, in: Lall N, (Ed), Medicinal Plants for Holistic Health and Well-Being, in: Academic Press, United Kingdom. pp: 77–115.
• Gaweł-Bęben, K., Strzępek-Gomółka, M., Czop, M., Sakipova, Z., Głowniak, K., & Kukula-Koch, W. (2020). Achillea millefolium L. and Achillea biebersteinii Afan. hydroglycolic extracts–bioactive ingredients for cosmetic use. Molecules, 25(15), 3368.
• Huber-Morath, A. (1975). Achillea L. In: Davis PH. (eds.). Flora of Turkey and the East Aegean Islands, in: Edinburgh: Edinburgh Univ Press pp. 224–52.
• Hussein, A.A., Al-Ezzy, R.M., & Abdallah, M.T. (2019). Biochemical, enzymatic, and immunological study on antimutagenic Achillea millefolium methanolic extract in vivo. Journal of Pharmacy and Pharmacology, 7, 69-74.
• Jaradat, N.A., Zaid, A.N., Hussen, F., Issa, L., Altamimi, M., Fuqaha, B., Nawahda, A., & Assadi, M. (2018). Phytoconstituents, antioxidant, sun protection and skin anti-wrinkle effects using four solvents fractions of the root bark of the traditional plant Alkanna tinctoria (L.). European Journal of Integrative Medicine, 21, 88 93. https://doi.org/10.1016/j.eujim.2018.07.003
• Krutmann, J. (2001). New developments in photoprotection of human skin. Skin Pharmacology and Physiology, 14, 401–407. https://doi.org/10.1159/000056374
• Küpeli, E., Erdogan Orhan, I., Küsmenoğlu, Ş., & Yesilada, E. (2007). Evaluation of anti-inflammatory and antinocicptive activity of five Anatolian Achillea species. Turkish Journal of Pharmaceutical Sciences, 4, 89-99.
• Lee, J-H., Zhou, H.Y., Cho, S.Y., Kim, Y.S., Lee, Y.S., & Jeong, C.S. (2007). Anti-inflammatory mechanisms of apigenin: inhibition of cyclooxygenase-2 expression, adhesion of monocytes to human umbilical vein endothelial cells, and expression of cellular adhesion molecules. Archives of Pharmacal Research, 30, 1318 – 1327. https://doi.org/10.1007/BF02980273
• Lee, K-K., Kim, J-H., Cho, J-J., & Choi, J-D. (1999). Inhibitory effects of 150 plant extracts on elastase activity, and their anti-inflammatory effects. International Journal of Cosmetic Science, 21, 71–82. https://doi.org/10.1046/j.1467-2494.1999.181638.x
• Lephart, E.D. (2016). Skin aging and oxidative stress: Equol’s anti-aging effects via biochemical and molecular mechanisms. Ageing Research Reviews, 31, 36–54. https://doi.org/10.1016/j.arr.2016.08.001
• Lim, H., & Kim, H. (2007). Inhibition of Mammalian Collagenase, Matrix Metalloproteinase -1, by Naturally - Occurring Flavonoids. Planta Medica, 73, 12671274. https://doi.org/10.1055/s-2007-990220
• Madan, K., & Nanda, S. (2018). In-vitro evaluation of antioxidant, anti-elastase, anti-collagenase, anti-hyaluronidase activities of safranal and determination of its sun protection factor in skin photoaging. Bioorganic Chemistry, 77, 159167. https://doi.org/10.1016/j.bioorg.2017.12.030
• Maron, D.M., & Ames, B.N. (1983). Revised methods for the Salmonella mutagenicity test. Mutation Research/Environmental Mutagenesis and Related Subjects, 113(3-4), 173–215. https://doi.org/10.1016/0165-1161(83)90010-9
• Masaki, H. (2010). Role of antioxidants in the skin: Anti-aging effects. Japanese Society for Investigative Dermatology, 58, 85–90. https://doi.org/10.1016/j.jdermsci.2010.03.003
• Meena, S.N., & Mohandass, C. (2019). in Advances in Biological Science Research. A Practical Approach (Elsevier), pp. 469–484.
• Millis, A.J.T., Hoyle, M., McCue, H.M., & Martini, H. (1992). Differential expression of metalloproteinase and tissue inhibitor of metalloproteinase genes in aged human fibroblasts. Experimental Cell Research, 201, 373–379. https://doi.org/10.1016/0014-4827(92)90286-H
• Mohammadhosseini, M., Sarker, S.D., & Akbarzadeh, A. (2017). Chemical composition of the essential oils and extracts of Achillea species and their biological activities: A review. Journal of Ethnopharmacology, 199, 257-315.
• Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods, 65(1-2), 55-63.
• Pientaweeratch, S., Panapisal, V., & Tansirikongkol, A. (2016). Antioxidant, anti-collagenase and anti-elastase activities of Phyllanthus emblica, Manilkara zapota and silymarin: an in vitro comparative study for anti-aging applications. Pharmaceutical Biology, 54, 1865–1872 https://doi.org/10.3109/13880209.2015.1133658
• Ramos-e-Silva, M., Celem, L.R., Ramos-e-Silva, S., & Fucci-da-Costa, A.P. (2013). Anti-aging cosmetics: Facts and controversies. Clinics in Dermatology, 31(6), 750–758. https://doi.org/10.1016/j.clindermatol.2013.05.013
• Rauter, A.P., Dias, C., Martins, A., Branco, I., Neng, N.R., Nogueira, J.M., … Waltho, J.P. (2012). Non-toxic Salvia sclareoides Brot. extracts as a source of functional food ingredients: Phenolic profile, antioxidant activity and prion binding properties. Food Chemistry, 132, 1930–1935. https://doi.org/10.1016/j.foodchem.2011.12.028
• Saewan, N., & Jimtaisong, A. (2013). Photoprotection of natural flavonoids. Journal of Applied Pharmaceutical Science, 3(9), 129-141. https://doi.org/10.7324/JAPS.2013.3923
• Salehi, B., Selamoglu, Z., Sevindik, M., Fahmy, N.M., Al-Sayed, E., El-Shazly, … Büsselberg, D. (2020). Achillea spp.: A comprehensive review on its ethnobotany, phytochemistry, phytopharmacology and industrial applications. Cellular and Molecular Biology, 25, 78-103.
• Saraf, S., & Kaur, C.D. (2010). In vitro sun protection factor determination of herbal oils used in cosmetics. Pharmacognosy Research, 2, 22. https://doi.org/10.4103/0974-8490.60586
• Singleton, V.L., Orthofer, R., & Lamuel-Raventos, R.M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Method Enzym. 299, 152–78.
• Sun, X., Zhang, J., Mi, Y., Chen, Y., Tan, W., Li, Q., Dong, F., & Guo, Z. (2020). Synthesis, characterization, and the antioxidant activity of the acetylated chitosan derivatives containing sulfonium salts. International Journal of Biological Macromolecules, 152, 349–358. https://doi.org/10.1016/j.ijbiomac.2020.02.177
• Wölfle, U., Heinemann, A., Esser, P.R., Haarhaus, B., Martin, S.F., & Schempp, C.M. (2012). Luteolin prevents solar radiation-induced matrix metalloproteinase-1 activation in human fibroblasts: A role for p38 mitogen-activated protein kinase and interleukin-20 released from keratinocytes. Rejuvenation Research, 15, 466–475. https://doi.org/10.1089/rej.2011.1309
• Zengin, G., Bulut, G., Mollica, A., Haznedaroglu, M.Z., Dogan, A., & Aktumsek, A. (2017a). Bioactivities of Achillea phrygia and Bupleurum croceum based on the composition of phenolic compounds: In vitro and in silico approaches. Food and Chemical Toxicology, 107, 597–608. https://doi.org/10.1016/j.fct.2017.03.037
• Zengin, G., Aktumsek, A., Ceylan, R., Uysal, S., Mocan, A., Guler, G. O., ... Soković, M. (2017b). Shedding light on the biological and chemical fingerprints of three Achillea species (A. biebersteinii, A. millefolium and A. teretifolia). Food & Function, 8(3), 1152-1165.
• Zhang, C-H., Yu, Y., Liang,,Y-Z., Chen, X-Q., (2015). Purification, partial characterization and antioxidant activity of polysaccharides from Glycyrrhiza uralensis. International Journal of Biological Macromolecules, 79, 681–686. https://doi.org/10.1016/j.ijbiomac.2015.05.060