Abstract
The present study aims at assessing the efficacies of olivetoric acid (OA) and physodic acid (PA) isolated from Pseudevernia furfuracea (L.) Zopf (Parmeliaceae) in human lymphocytes (HLs) in vitro. 3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide and lactate dehydrogenase assays were performed to establish cytotoxicity in HLs. Besides, oxidative stress and genotoxicity were monitored by estimating the changes of total oxidative stress (TOS) and 8-hydroxy-2′-deoxyguanosine (8-OH-dG) levels, respectively, in HLs. At the same time, OA- and PA-induced total antioxidant capacity (TAC) levels in HLs were determined. Although especially low concentrations of OA (IC50=109.94 mg/L) and PA (IC50=665.49 mg/L) did not show cytotoxic effect at high levels in HLs, it was revealed that cytotoxicity was significantly (p<0.05) associated with oxidative stress and genotoxicity via correlation analysis. While TOS level in HLs did not statistically (p>0.05) increase in the presence of all treatments (0.5–100 mg/L) of PA, TAC level was increased by PA applications in certain concentrations (0.5–10 mg/L). Overall, the obtained data indicate that OA and especially PA as lichen compounds that do not cause oxidative stress can be a new resource of therapeutics as recognized in the present study with their high antioxidant features.
References
1. Gago-Dominguez M, Castelao JE. Lipid peroxidation and renal cell carcinoma: further supportive evidence and new mechanistic insights. Free Radic Biol Med 2006;40:721–33.10.1016/j.freeradbiomed.2005.09.026Search in Google Scholar PubMed
2. Ray PD, Huang B-W, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012;24:981–90.10.1016/j.cellsig.2012.01.008Search in Google Scholar PubMed PubMed Central
3. Poljsak B, Suput D, Milisav I. Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxid Med Cell Longev 2013:956792.10.1155/2013/956792Search in Google Scholar PubMed PubMed Central
4. Valenzuela BA, Sanhueza J, Nieto S. Natural antioxidants in functional foods: from food safety to health benefits. Grasas Y Aceites 2003;54:295–303.10.3989/gya.2003.v54.i3.245Search in Google Scholar
5. Fki I, Allouche N, Sayadi S. The use of polyphenolic extract, purified hydroxytyrosol and 3,4-dihydroxyphenyl acetic acid from olive mill wastewater for the stabilization of refined oils: a potential alternative to synthetic antioxidants. Food Chem 2005;93:197–204.10.1016/j.foodchem.2004.09.014Search in Google Scholar
6. Ahmad SR, Gokulakrishnan P, Giriprasad R, Yatoo MA. Fruit-based natural antioxidants in meat and meat products: a review. Crit Rev Food Sci Nutr 2015;55:1503–13.10.1080/10408398.2012.701674Search in Google Scholar PubMed
7. Moukette BM, Pieme CA, Njimou JR, Biapa CP, Marco B, Ngogang JY. In vitro antioxidant properties, free radicals scavenging activities of extracts and polyphenol composition of a non-timber forest product used as spice: Monodora myristica. Biol Res 2015;48:15.10.1186/s40659-015-0003-1Search in Google Scholar PubMed PubMed Central
8. 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
9. Mondal A, Bennett LL. Resveratrol enhances the efficacy of sorafenib mediated apoptosis in human breast cancer MCF7 cells through ROS, cell cycle inhibition, caspase 3 and PARP cleavage. Biomed Pharmacother 2016;84:1906–14.10.1016/j.biopha.2016.10.096Search in Google Scholar PubMed
10. Brodo IM, Sharnoff SD, Sharnoff S. About the lichens in: Lichens of North America. New Haven: Yale University Press, 2001:3–113.10.29173/bluejay5827Search in Google Scholar
11. Boustie J, Grube M. Lichens–a promising source of bioactive secondary metabolites. Plant Genet Resour 2005;3:273–87.10.1079/PGR200572Search in Google Scholar
12. Gökalsın B, Sesal NC. Lichen secondary metabolite evernic acid as potential quorum sensing inhibitor against Pseudomonas aeruginosa. World J Microbiol Biotechnol 2016;32:150.10.1007/s11274-016-2105-5Search in Google Scholar PubMed
13. Karabulut G, Ozturk S. Antifungal activity of Evernia prunastri, Parmelia sulcata, Pseudevernia furfuracea var. furfuracea. Pakistan J Bot 2015;47:1575–9.Search in Google Scholar
14. Sokolov DN, Zarubaev VV, Shtro AA, Polovinka MP, Luzina OA, Komarova NI, et al. Anti-viral activity of (−)– and (+)– usnic acids and their derivatives against influenza virus A(H1N1)2009. Bioorg Med Chem Lett 2012;22:7060–4.10.1016/j.bmcl.2012.09.084Search in Google Scholar PubMed
15. Schmeda-Hirschmann G, Tapia A, Lima B, Pertino M, Sortino M, Zacchino S, et al. A new antifungal and antiprotozoal depside from the andean lichen Protousnea poeppigii. Phyther Res 2008;22:349–55.10.1002/ptr.2321Search in Google Scholar PubMed
16. Emsen B, Yildirim E, Aslan A. Insecticidal activities of extracts of three lichen species on Sitophilus granarius (L.) (Coleoptera: Curculionidae). Plant Prot Sci 2015;51:156–61.10.17221/101/2014-PPSSearch in Google Scholar
17. de Castro Fonseca J, de Oliveira YS, Bezerra BP, Ellena J, Honda NK, Silva CV, et al. Diffractaic acid: crystalline structure and physicochemical characterization. Spectrochim Acta Part A Mol Biomol Spectrosc 2016;165:26–32.10.1016/j.saa.2016.04.030Search in Google Scholar PubMed
18. Melo MG, Araújo AA, Rocha CP, Almeida EM, Siqueira R de S, Bonjardim LR, et al. Purification, physicochemical properties, thermal analysis and antinociceptive effect of atranorin extracted from Cladina kalbii. Biol Pharm Bull 2008;31:1977–80.10.1248/bpb.31.1977Search in Google Scholar PubMed
19. Morita H, Tsuchiya T, Kishibe K, Noya S, Shiro M, Hirasawa Y. Antimitotic activity of lobaric acid and a new benzofuran, sakisacaulon a from Stereocaulon sasakii. Bioorganic Med Chem Lett 2009;19:3679–81.10.1016/j.bmcl.2009.03.170Search in Google Scholar PubMed
20. Emsen B, Aslan A, Togar B, Turkez H. In vitro antitumor activities of the lichen compounds olivetoric, physodic and psoromic acid in rat neuron and glioblastoma cells. Pharm Biol 2016;54:1748–62.10.3109/13880209.2015.1126620Search in Google Scholar PubMed
21. Fernández-Moriano C, Divakar PK, Crespo A, Gómez-Serranillos MP. Neuroprotective activity and cytotoxic potential of two Parmeliaceae lichens: identification of active compounds. Phytomedicine 2015;22:847–55.10.1016/j.phymed.2015.06.005Search in Google Scholar PubMed
22. Basile A, Rigano D, Loppi S, Di Santi A, Nebbioso A, Sorbo S, et al. Antiproliferative, antibacterial and antifungal activity of the lichen Xanthoria parietina and its secondary metabolite parietin. Int J Mol Sci 2015;16:7861–75.10.3390/ijms16047861Search in Google Scholar PubMed PubMed Central
23. Emsen B, Turkez H, Togar B, Aslan A. Evaluation of antioxidant and cytotoxic effects of olivetoric and physodic acid in cultured human amnion fibroblasts. Hum Exp Toxicol 2017;36:376–85.10.1177/0960327116650012Search in Google Scholar PubMed
24. Araújo AA, de Melo MG, Rabelo TK, Nunes PS, Santos SL, Serafini MR, et al. Review of the biological properties and toxicity of usnic acid. Nat Prod Res 2015;29:2167–80.10.1080/14786419.2015.1007455Search in Google Scholar PubMed
25. 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.Search in Google Scholar
26. Wirth V. Die Flechten Baden Württembergs, vol. 1–2. Stuttgart: Ulmer, 1995:1006.Search in Google Scholar
27. Asahina Y, Shibata S. Chemistry of lichen substances. Tokyo: Japan Society for the Promotion of Science, 1971:240.Search in Google Scholar
28. Berridge MV, Herst PM, Tan AS. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Annu Rev 2005;11:127–52.10.1016/S1387-2656(05)11004-7Search in Google Scholar PubMed
29. Haslam G, Wyatt D, Kitos PA. Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities. Cytotechnology 2000;32:63–75.10.1023/A:1008121125755Search in Google Scholar PubMed
30. Wolterbeek HT, van der Meer AJ. Optimization, application, and interpretation of lactate dehydrogenase measurements in microwell determination of cell number and toxicity. Assay Drug Dev Technol 2005;3:675–82.10.1089/adt.2005.3.675Search in Google Scholar PubMed
31. Gan W, Nie B, Shi F, Xu XM, Qian JC, Takagi Y, et al. Age-dependent increases in the oxidative damage of DNA, RNA, and their metabolites in normal and senescence-accelerated mice analyzed by LC-MS/MS: urinary 8-oxoguanosine as a novel biomarker of aging. Free Radic Biol Med 2012;52:1700–7.10.1016/j.freeradbiomed.2012.02.016Search in Google Scholar PubMed
32. van Andel T, van Onselen S, Myren B, Towns A, Quiroz D. “The medicine from behind”: the frequent use of enemas in western African traditional medicine. J Ethnopharmacol 2015;174:637–43.10.1016/j.jep.2015.06.040Search in Google Scholar PubMed
33. Al-Farga A, Zhang H, Siddeeg A, Shamoon M, Chamba MV, Al-Hajj N. Proximate composition, functional properties, amino acid, mineral and vitamin contents of a novel food: alhydwan (Boerhavia elegana Choisy) seed flour. Food Chem 2016;211:268–73.10.1016/j.foodchem.2016.05.016Search in Google Scholar PubMed
34. Arun M, Satish S, Anima P. Phytopharmacological profile of Jasminum grandiflorum Linn. (Oleaceae). Chin J Integr Med 2016;22:311–20.10.1007/s11655-015-2051-3Search in Google Scholar PubMed
35. Emsen B, Dogan M, Aasim M, Yildirim E. Insecticidal activity of in vitro propagated aquatic plant Ceratophyllum demersum L. against granary weevil Sitophilus granarius L. (Coleoptera: Curculionidae). Egypt J Biol Pest Control 2016;26:619–24.Search in Google Scholar
36. Emsen B, Kocabas A, Kaya A, Cinar S, Aasim M, Sadi G. In vitro cytotoxicity, antibacterial and antioxidant properties of various extracts from Schizophyllum commune Fr. Fresenius Environ Bull 2017;26:1144–53.Search in Google Scholar
37. Bayram S, Ecem BN, Gerçek YC, Öz GC, Sorkun K. Anticytotoxic and antimutagenic effects of propolis on human lymphocytes in vitro. Mellifera 2016;16:38–46.Search in Google Scholar
38. 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;30:33–9.10.1177/0748233712448119Search in Google Scholar PubMed
39. Cardile V, Graziano AC, Avola R, Piovano M, Russo A. Potential anticancer activity of lichen secondary metabolite physodic acid. Chem Biol Interact 2017;263:36–45.10.1016/j.cbi.2016.12.007Search in Google Scholar PubMed
40. Studzińska-Sroka E, Piotrowska H, Kucińska M, Murias M, Bylka W. Cytotoxic activity of physodic acid and acetone extract from Hypogymnia physodes against breast cancer cell lines. Pharm Biol 2016;54:2480–5.10.3109/13880209.2016.1160936Search in Google Scholar PubMed
41. Kosanić M, Manojlović N, Janković S, Stanojković T, Ranković B. Evernia prunastri and Pseudoevernia furfuraceae lichens and their major metabolites as antioxidant, antimicrobial and anticancer agents. Food Chem Toxicol 2013;53:112–8.10.1016/j.fct.2012.11.034Search in Google Scholar PubMed
42. Xin L, Wang J, Fan G, Wu Y, Guo S. Activation of HSPA1A promoter by environmental pollutants: an early and rapid response to cellular damage. Environ Toxicol Pharmacol 2015;39:1027–33.10.1016/j.etap.2015.03.011Search in Google Scholar PubMed
43. Dinter D, Gajski G, Domijan A-M, Garaj-Vrhovac V. Cytogenetic and oxidative status of human lymphocytes after exposure to clinically relevant concentrations of antimalarial drugs atovaquone and proguanil hydrochloride in vitro. Fundam Clin Pharmacol 2015;29:575–85.10.1111/fcp.12153Search in Google Scholar PubMed
44. Turkez H, Aydin E, Aslan A. An antidote for imazalil-induced genotoxicity in vitro: the lichen, Dermatocarpon intestiniforme (Körber) Hasse. Acta Biol Hung 2012;63:354–61.10.1556/ABiol.63.2012.3.5Search in Google Scholar PubMed
45. Aslan A, Agar G, Alpsoy L, Kotan E, Ceker S. Protective role of methanol extracts of two lichens on oxidative and genotoxic damage caused by AFB1 in human lymphocytes in vitro. Toxicol Ind Health 2012;28:505–12.10.1177/0748233711416944Search in Google Scholar PubMed
46. Nardemir G, Yanmis D, Alpsoy L, Gulluce M, Agar G, Aslan A. Genotoxic, antigenotoxic and antioxidant properties of methanol extracts obtained from Peltigera horizontalis and Peltigera praetextata. Toxicol Ind Health 2015;31:602–13.10.1177/0748233713480207Search in Google Scholar PubMed
47. Kang S, Lee SH, Shim YN, Oh MJ, Lee NR, Park S. Antioxidant capacity of anthocyanin-rich fruits and vegetables and changes of quality characteristics of black carrot added pudding according to storage. J Appl Biol Chem 2016;59:273–80.10.3839/jabc.2016.047Search in Google Scholar
48. Álvarez R, Araya H, Navarro-Lisboa R, de Dicastillo CL. Evaluation of polyphenol content and antioxidant capacity of fruits and vegetables using a modified enzymatic extraction. Food Technol Biotechnol 2016;54:462–7.10.17113/ftb.54.04.16.4497Search in Google Scholar PubMed PubMed Central
49. Polat Z, Aydin E, Turkez H, Aslan A. In vitro risk assessment of usnic acid. Toxicol Ind Health 2016;32:468–75.10.1177/0748233713504811Search in Google Scholar PubMed
50. 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;30:878–87.10.1177/0748233712466130Search in Google Scholar PubMed
51. Reddy RG, Veeraval L, Maitra S, Chollet-Krugler M, Tomasi S, Dévéhat FL, et al. Lichen-derived compounds show potential for central nervous system therapeutics. Phytomedicine 2016;23:1527–34.10.1016/j.phymed.2016.08.010Search in Google Scholar PubMed
52. Pavlovic V, Stojanovic I, Jadranin M, Vajs V, Djordjević I, Smelcerovic A, et al. Effect of four lichen acids isolated from Hypogymnia physodes on viability of rat thymocytes. Food Chem Toxicol 2013;51:160–4.10.1016/j.fct.2012.04.043Search in Google Scholar PubMed
Supplementary Material:
The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2017-0209).
©2018 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Research Articles
- PFGE: a tool for examination of heterogeneity between the bacterial spot-causing xanthomonads of tomato plants in Bulgaria
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- Letter
- Chemical composition and antifungal activity of essential oils from four Asteraceae plants grown in Egypt
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Articles in the same Issue
- Frontmatter
- Research Articles
- PFGE: a tool for examination of heterogeneity between the bacterial spot-causing xanthomonads of tomato plants in Bulgaria
- Applications of magnetoliposomes with encapsulated doxorubicin for integrated chemotherapy and hyperthermia of rat C6 glioma
- Effect of the Arctic terrestrial plant Ranunculus hyperboreus on LPS-induced inflammatory response via MAPK pathways
- Cyanidin-3-rutinoside protects INS-1 pancreatic β cells against high glucose-induced glucotoxicity by apoptosis
- Research for the lichen Usnea barbata metabolites
- Shape-controlled synthesis of three-dimensional zinc oxide nanoflowers for disinfection of food pathogens
- Effects of two lichen acids isolated from Pseudevernia furfuracea (L.) Zopf in cultured human lymphocytes
- Letter
- Chemical composition and antifungal activity of essential oils from four Asteraceae plants grown in Egypt
- Research note
- Effect of yeast extract addition to a mineral salts medium containing hydrolyzed plant xylan on fungal pullulan production