Abstract
In the present study, we investigated cytogenetic and oxidative [total antioxidant capacity (TAC), total oxidant status (TOS)] effects of methanol and water extracts of Cladonia chlorophaea (Flörke ex Sommerf.) Sprengel, Dermatocarpon miniatum (L.) W.Mann and Parmelia saxatilis (L.) Ach. on cultured human lymphocytes. In addition, different phenolic compounds in the extracts were quantified by high performance liquid chromatography (HPLC) analysis. As a result of HPLC analysis, methanol extracts of all lichen species tested had higher phenolic compounds. Likewise, methanol extracts of each lichen increased TAC levels in lymphocytes more than water extracts. The TOS levels of the cells treated with different concentrations (1–100 mg/L) of the extracts decreased due to the increasing concentration of the extracts. Genotoxicity experiments revealed that the tested lichen extracts did not significantly increase (p > 0.05) the level of genotoxicity on human peripheral lymphocyte culture compared to the negative control group. The results showed that C. chlorophaea, D. miniatum and P. saxatilis lichens, which were found to be a rich source of phenolic compounds, might be of interest in the pharmaceutical and food industries.
Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
1. Ureshino, H, Shindo, T, Kimura, S. Role of cancer immunology in chronic myelogenous leukemia. Leuk Res 2020;88:106273. https://doi.org/10.1016/j.leukres.2019.106273.Search in Google Scholar
2. Olszowski, T, Janiszewska-Olszowska, J, Sporniak-Tutak, K. Non-specific defence factors in the course of dental caries. Pediatr Pol 2010;85:265–8. https://doi.org/10.1016/s0031-3939(10)70034-2.Search in Google Scholar
3. Muhl, A, Liebert, F. No impact of a phytogenic feed additive on digestion and unspecific immune reaction in piglets. J Anim Physiol Anim Nutr 2007;91:426–31. https://doi.org/10.1111/j.1439-0396.2006.00671.x.Search in Google Scholar
4. Allard-Chamard, H, Mahajan, VS. The future of clinical immunology laboratory testing. Clin Lab Med 2019;39:699–708. https://doi.org/10.1016/j.cll.2019.07.014.Search in Google Scholar
5. Britten, CM, Walter, S, Janetzki, S. Immunological monitoring to rationally guide AAV gene therapy. Front Immunol 2013;4:273. https://doi.org/10.3389/fimmu.2013.00273.Search in Google Scholar
6. Arancibia, S, Campo, MD, Nova, E, Salazar, F, Becker, MI. Enhanced structural stability of Concholepas hemocyanin increases its immunogenicity and maintains its non-specific immunostimulatory effects. Eur J Immunol 2012;42:688–99. https://doi.org/10.1002/eji.201142011.Search in Google Scholar
7. Shalini, KS, Yengkhom, O, Subramani, PA, Dinakaran, MR. Polysaccharide fraction of the hemi-parasitic mistletoe, Dendrophthoe falcata (L) ettingsh leaves enhances innate immune responses and disease resistance in Oreochromis niloticus (Linnaeus). Int J Res Pharm Sci 2019;10:56–64.10.1016/j.fsi.2019.03.008Search in Google Scholar
8. Venkatalakshmi, P, Vadivel, V, Brindha, P. Role of phytochemicals as immunomodulatory agents: a review. Int J Green Pharm 2016;10:1–18.Search in Google Scholar
9. Karatas, M, Dogan, M, Emsen, B, Aasim, M. Determination of in vitro free radical scavenging activities of various extracts from in vitro propagated Ceratophyllum demersum L. Fresenius Environ Bull 2015;24:2946–52.Search in Google Scholar
10. Zugic, A, Tadic, V, Savic, S. Nano-and microcarriers as drug delivery systems for usnic acid: review of literature. Pharmaceutics 2020;12:156. https://doi.org/10.3390/pharmaceutics12020156.Search in Google Scholar
11. Furmanek, Ł, Czarnota, P, Seaward, MRD. Antifungal activity of lichen compounds against dermatophytes: a review. J Appl Microbiol 2019;127:308–25. https://doi.org/10.1111/jam.14209.Search in Google Scholar
12. Radice, M, Manfredini, S, Ziosi, P, Dissette, V, Buso, P, Fallacara, A, et al.. Herbal extracts, lichens and biomolecules as natural photo-protection alternatives to synthetic UV filters. A systematic review. Fitoterapia 2016;114:144–62. https://doi.org/10.1016/j.fitote.2016.09.003.Search in Google Scholar
13. Emsen, B, Yildirim, E, Aslan, A, Anar, M, Ercisli, S. Insecticidal effect of the extracts of Cladonia foliacea (Huds.) Willd. and Flavoparmelia caperata (L.) Hale against adults of the grain weevil, Sitophilus granarius (L.) (Coleoptera: Curculionidae). Egypt J Biol Pest Contr 2012;22:145–9.Search in Google Scholar
14. Verma, N, Behera, BC. Future directions in the study of pharmaceutical potential of lichens. In: Lichen secondary metabolites: bioactive properties and pharmaceutical potential. Cham: Springer International Publishing; 2015:179–202 pp.10.1007/978-3-319-13374-4_8Search in Google Scholar
15. Purvis, OW, Coppins, BJ, Hawksworth, DL, James, PW, Moore, DM. The lichen flora of Great Britain and Ireland. London: Natural History Museum Publications in Association with the British Lichen Society; 1992:710 p.Search in Google Scholar
16. Wirth, V. Die Flechten Baden Württembergs. Stuttgart: Ulmer; 1995:1006 p.Search in Google Scholar
17. Rodríguez-Delgado, MA, Malovaná, S, Pérez, JP, Borges, T, García Montelongo, FJ. Separation of phenolic compounds by high-performance liquid chromatography with absorbance and fluorimetric detection. J Chromatogr A 2001;912:249–57. https://doi.org/10.1016/S0021-9673(01)00598-2.Search in Google Scholar
18. Emsen, B. The antioxidant and antigenotoxic potential of Peltigera canina and Umbilicaria nylanderiana based on their phenolic profile. Farmacia 2019;67:912–21. https://doi.org/10.31925/farmacia.2019.5.24.Search in Google Scholar
19. Kaufmann, SHE. Immunology’s coming of age. Front Immunol 2019;10:684. https://doi.org/10.3389/fimmu.2019.00684.Search in Google Scholar
20. Fang, T, Wu, X, Cao, W, Jia, G, Zhao, H, Chen, X, et al.. Effects of dietary fiber on the antioxidant capacity, immune status, and antioxidant-relative signaling molecular gene expression in rat organs. RSC Adv 2017;7:19611–20. https://doi.org/10.1039/c7ra02464a.Search in Google Scholar
21. Cavuldak, ÖA, Vural, N, Akay, MA, Anlı, RE. Optimization of ultrasound-assisted water extraction conditions for the extraction of phenolic compounds from black mulberry leaves (Morus nigra L.). J Food Process Eng 2019;42:e13132. https://doi.org/10.1111/jfpe.13132.Search in Google Scholar
22. Gollucke, APB. Recent applications of grape polyphenols in foods, beverages and supplements. Recent Pat Food Nutr Agric 2010;2:105–9.10.2174/1876142911002020105Search in Google Scholar
23. Zavarzina, AG, Nikolaeva, TN, Demin, VV, Lapshin, PV, Makarov, MI, Zavarzin, AA, et al.. Water-soluble phenolic metabolites in lichens and their potential role in soil organic matter formation at the pre-vascular stage. Eur J Soil Sci 2019;70:736–50. https://doi.org/10.1111/ejss.12822.Search in Google Scholar
24. Emsen, B, Ozdemir, O, Engin, T, Togar, B, Cavusoglu, S, Turkez, H. Inhibition of growth of U87MG human glioblastoma cells by Usnea longissima Ach. An Acad Bras Cienc 2019;91:e20180994. https://doi.org/10.1590/0001-3765201920180994.Search in Google Scholar
25. de Souza, ARC, Stefanov, S, Bombardelli, MCM, Corazza, ML, Stateva, RP. Assessment of composition and biological activity of Arctium lappa leaves extracts obtained with pressurized liquid and supercritical CO2 extraction. J Supercrit Fluids 2019;152:104573. https://doi.org/10.1016/j.supflu.2019.104573.Search in Google Scholar
26. Ghate, NB, Chaudhuri, D, Sarkar, R, Sajem, AL, Panja, S, Rout, J, et al.. An antioxidant extract of tropical lichen, Parmotrema reticulatum, induces cell cycle arrest and apoptosis in breast carcinoma cell line MCF-7. PloS One 2013;8:e82293. https://doi.org/10.1371/journal.pone.0082293.Search in Google Scholar
27. Colak, S, Geyikoğlu, F, Aslan, A, Deniz, GY. Effects of lichen extracts on haematological parameters of rats with experimental insulin-dependent diabetes mellitus. Toxicol Ind Health 2014;30:878–87. https://doi.org/10.1177/0748233712466130.Search in Google Scholar
28. Fernández-Moriano, C, Divakar, PK, Crespo, A, Gómez-Serranillos, MP. Protective effects of lichen metabolites evernic and usnic acids against redox impairment-mediated cytotoxicity in central nervous system-like cells. Food Chem Toxicol 2017;105:262–77. https://doi.org/10.1016/j.fct.2017.04.030.Search in Google Scholar
29. Turkez, H, Aydin, E, Aslan, A. Role of aqueous Bryoria capillaris (Ach.) extract as a genoprotective agent on imazalil-induced genotoxicity in vitro. Toxicol Ind Health 2014;30:33–9. https://doi.org/10.1177/0748233712448119.Search in Google Scholar
30. Ari, F, Aztopal, N, Oran, S, Bozdemir, S, Celikler, S, Ozturk, S, et al.. Parmelia sulcata Taylor and Usnea filipendula Stirt induce apoptosis-like cell death and DNA damage in cancer cells. Cell Prolif 2014;47:457–64. https://doi.org/10.1111/cpr.12123.Search in Google Scholar
31. Shrestha, G, El-naggar, AM, Clair, LLS, Neill, KLO. Anticancer activities of selected species of North American lichen extracts. Phytother Res 2015;29:100–7. https://doi.org/10.1002/ptr.5233.Search in Google Scholar
32. Legouin, B, Lohézic-Le Dévéhat, F, Ferron, S, Rouaud, I, Le Pogam, P, Cornevin, L, et al.. Specialized metabolites of the lichen Vulpicida pinastri act as photoprotective agents. Molecules 2017;22:1162. https://doi.org/10.3390/molecules22071162.Search in Google Scholar
33. Mishra, T, Shukla, S, Meena, S, Singh, R, Pal, M, Upreti, DK, et al.. Isolation and identification of cytotoxic compounds from a fruticose lichen Roccella montagnei, and it’s in silico docking study against CDK-10. Rev Bras Farmacogn 2017;27:724–8. https://doi.org/10.1016/j.bjp.2017.07.006.Search in Google Scholar
34. Ahmed, E, Elkhateeb, W, Taie, H, Rateb, M, Fayad, W. Biological capacity and chemical composition of secondary metabolites from representatives Japanese lichens. J Appl Pharmaceut Sci 2017;7:98–103. https://doi.org/10.7324/JAPS.2017.70113.Search in Google Scholar
Supplementary material
The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2020-0135).
© 2020 Walter de Gruyter GmbH, Berlin/Boston
