Synergistic gastroprotective and antioxidative effects of natural olive oil and usnic acid isolated from Usnea longissima, a lichen species in Anatolia (Türkiye), in the indomethacin ulcer model created in rats

Year 2023, , 196 - 209, 15.12.2023

Fehmi Odabasoglu , Serkan Uyanık , Fadime Atalay Dumlu , Özlem Aydın Berktaş , Ali Aslan

https://doi.org/10.31797/vetbio.1351161

Abstract

Usnea longissima, a medically important lichen growing up in forests in Anatolia (Turkey). In this study, the gastroprotective effect of usnic acid (UA) was investigated using an indomethacin (IND)-induced gastric ulcer model in rats. While 25, 50, 100 and 200 mg/kg UA doses were dissolved in 2 ml of olive oil (OO) and administered to rats, only OO was given to one group. In addition, lansoprazole (LAN) and ranitidine (RAN) and IND were dissolved in water and administered to rat groups. IND administration caused very high levels of damage to rat stomachs. On the other hand, when four doses of UA, OO, RAN and LAN were administered, it was determined that hyperemias in the stomach of rats was significantly reduced. After macroscopic analysis of gastric tissues, the activities of superoxide dismutase (SOD), catalase (CAT), myeloperoxidase (MPO) and nitric oxide synthase (iNOS and cNOS) enzymes as well as glutathione (GSH) and lipid peroxidation (LPO) levels were determined in these tissues. After IND application, it was detected increases in MPO, CAT and iNOS activities in gastric tissues and decreases in SOD, cNOS and GSH amounts. Four doses of UA, OO, RAN and LAN applications reversed the trend, bringing them closer to healthy levels.

Keywords

Indomethacin, iNOS, gastroprotective effect, myeloperoxidase, usnic acid, olive oil

References

• Aebi, H. (1984). Catalase. Methods Enzymology, 105, 121-126.
• Ahmadjian, V. (1993). The lichen symbiosis. Wiley, New York, pp. 1-6.
• Ahmed, M.A.E., Mohanad, M., Ahmed, A.A.E., Aboulhoda, B.E., & El-Awdan, S.A. (2021). Mechanistic insights into the protective effects of chlorogenic acid against indomethacin-induced gastric ulcer in rats: Modulation of the cross talk between autophagy and apoptosis signaling. Life Sciences, 275, 119370. https://doi.org/10.1016/j.lfs.2021.119370
• Anwar, H.M., Georgy, G.S., Hassan, A.A., & Gad, A.M. (2021). Honokiol mitigates gastric ulcer induced by indomethacin in rats via suppression of inflammatory biomarkers and reactive oxygen species. Egyptian Journal of Chemistry, 64(11), 6439-6447. https://doi.org/10.21608/EJCHEM.2021.78917.3860
• Atalay, F., Odabasoglu, F., Halici, M., Cadirci, E., Aydin, O., Halici, Z., & Cakir, A. (2016). N-acetyl cysteine has both gastro-protective and anti-inflammatory effects in experimental rat models: its gastro-protective effect is related to its in vivo and in vitro antioxidant properties. Journal of Cellular Biochemistry, 117(2), 308-319. https://doi.org/10.1002 /jcb.25193
• Atalay, F., Odabasoglu, F., Halici, M., Cakir, A., Cadirci, E., Aslan, A., Berktas, O.A., & Kazaz, C. (2015). Gastroprotective and antioxidant effects of Lobaria pulmonaria and its metabolite Rhizonyl Alcohol on indomethacin-induced gastric ulcer. Chemistry & Biodiversity, 12(11),1756-1767. https:// doi.org/10.1002/cbdv.201400432
• Bayir, Y., Odabasoglu, F., Cakir, A., Aslan, A., Suleyman. H., Halici, M., & Kazaz, C. (2006). The inhibition of gastric mucosal lesion, oxidative stress and neutrophil-infiltration in rats by the lichen constituent diffractaic acid. Phytomedicine, 13, 584-590. https://doi.org/10.1016/j.phymed.2005.07.002
• Berktas, O.A., Odabasoglu, F., Dumlu, F.A., Kutlu, Z., Cadirci, E., Halici, M., Ozturk, F., & Cakir, A. (2021). Gastroprotective and antioxidant effects of the cinnamon, cumin, sumac on ındomethacin ınduced gastric ulcer in rats. European Journal of Food Science and Technology, 5(2), 147-166.
• Bi, W.P., Man, H.B., & Man, M.Q. (2014). Efficacy and safety of herbal medicines in treating gastric ulcer: A review. World Journal of Gastroenterology, 20(45), 17020–17028. https://doi.org/10.3748/wjg.v20.i45. 17020
• Bozkurt, I., Dilek, E., Erol, H.S., Çakir, A., Hamzaoğlu, E., Koç, M., Keles, O.N., & Halici, M.B. (2017). Investigation on the effects of pomiferin from Maclura pomifera on indomethacin-induced gastric ulcer: An experimental study in rats. Medicinal Chemistry Research, 26, 2048-2056. https://doi.org/10.1007/ s00044-017-1913-y
• Bradley, P.P., Priebat, D.A., Christensen, R.D., & Rothstein, G. (1982). Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. Journal of Investigative Dermatology, 78, 206-209. https://doi.org/10.1111/1523-1747. ep12506462
• Brij, L., & Upreti, D.K. (1995). Ethnobotanical notes on three Indian lichens. Lichenologist, 27, 77-79.
• Coskun, T., Yegen, B.C., Alican, I., Peker, O., & Kartel, H. (1996). Cold restraint stress-induced gastric mucosal dysfunction-role of nitric oxide. Digestive Diseases and Sciences, 41, 956-963. https:// doi.org/10.1007/BF02091537
• Culberson, C.F. (1969). Chemical and botanical guide to lichen products, The University of North Carolina Press, Chapel Hill. p. 1-628.
• De la Lastra, C.A., Barranco, M.D., Motilva, V., & Herrerías, J.M. (2001). Mediterranean diet and health: biological importance of olive oil. Current Pharmaceutical Design, 23, 933-950. https://doi. org/10.2174/1381612013397654
• Dejban, P., Eslami, F., Rahimi, N., Takzare, N., Jahansouz, M., & Dehpour, A.R. (2020). Involvement of nitric oxide pathway in the anti-inflammatory effect of modafinil on indomethacin-, stress-, and ethanol -induced gastric mucosal injury in rat. European Journal of Pharmacology, 887, 173579. https://doi.org/10.1016/j.ejphar.2020.173579
• Halici, M., Odabasoglu, F., Suleyman, H., Cakir, A., Aslan, A., & Bayir, Y. (2005). Effects of water extract of Usnea longissima on antioxidant enzyme activity and mucosal damage caused by indomethacin in rats. Phytomedicine, 12, 656-662. https://doi.org/10.1016/j. phymed.2004.06.021
• Halici, M., Kufrevioglu, O.I., Odabasoglu, F., Halici, Z., Cakir, A., & Aslan, A. (2011). The ethanol-water extract of Ramalina capitata has gastroprotective and antioxidative properties: an experimental study in rats with indomethacin-induced gastric injuries. Journal of Food Biochemistry, 35(1), 11-26. https://doi.org/10. 1111/j.1745-4514.2010.00363.x
• Hanci, N., Odabasoglu, F., Dumlu, F.A., Berktas, O.A., Kutlu, Z., Halici, M., & Halici, Z. (2018). Sesame oil has gastroprotective and anti-oxidative properties: An experimental study in rats with indomethacin-induced gastric ulcers. European Journal of Food Science and Technology, 2(2), 53-68.
• Huneck, S., & Yoshimura, I. (1996). Identification of Lichen Substances. Springer-Verlag, Berlin. p. 251.
• Huneck, S. (1999). The significance of lichens and their metabolites. Naturwissenschaften, 86, 559-570.
• Kaplan, K.A., Odabasoglu, F., Halici. Z., Halici, M., Cadirci, E., Atalay, F., Aydin, O., & Cakir, A. (2012). Alpha-lipoic acid protects against indomethacin-induced gastric oxidative toxicity by modulating antioxidant system. Journal of Food Science, 77(11), 224-230. https://doi.org/10.1111/j. 1750-3841.2012.02920.x
• Karakus, B., Odabasoglu, F., Cakir, A., Halici, Z., Bayir, Y., Halici, M., Aslan, A., & Suleyman, H. (2009). The effects of methanol extract of Lobaria pulmonaria, a lichen species, on indometacin-induced gastric mucosal damage, oxidative stress and neutrophil infiltration. Phyto Research, 23(5), 635-639. https://doi.org/10.1002/ptr.2675
• Knowles, R.G., Merrett, M., Salter, M., & Moncada, S. (1990). Differential induction of brain, lung and liver nitric oxide synthase by endotoxin in the rat. Biochemical Journal, 270,833-836. https://doi.org/10. 1042/bj2700833
• Konturek, S.J., Brzozowski, T., Majka, J., Pytko-Polonczyk, J., & Stachura, J. (1993). Inhibition of nitric oxide synthase delays healing of chronic gastric ulcers. European Journal of Pharmacology, 239, 215-217. https://doi.org/10.1016/0014-2999(93)90997-v
• Lanas, A., Carrera-Lasfuentes, P., Arguedas, Y., García, S., Bujanda, L., Calvet, X., Ponce, J., Perez-Aísa, Á., Castro, M., Muñoz, M., Sostres, C., & García-Rodríguez., L. (2015). Risk of upper and lower gastrointestinal bleeding in patients taking nonsteroidal antiinflammatory drugs, antiplatelet agents, or anticoagulants. Clinical Gastroenterology and Hepatology, 13(5), 906-912. https://doi.org/10. 1016/j.cgh.2014.11.007
• Miraj, S., Pourafzali, S., & Ahmadabadi Rafiei, Z. (2020). Effect of olive oil in preventing the development of pressure ulcer grade one in intensive care unit patients. International Journal of Preventive Medicine, 11,23(1-5). https://doi.org/10.4103/ijpvm. IJPVM_545_18
• Morsy, M.A., & El-Moselhy, M.A. (2013). Mechanisms of the protective effects of curcumin against indomethacin-induced gastric ulcer in rats. Pharmacology, 91, 267-274. https://doi.org/10.1159/ 000350190
• Nishida, K., Ohta, Y., & Ishiguro, I. (1998). Contribution of NO synthases to neutrophil infiltration in the gastric mucosal lesions in rats with water immersion restraint stress. FEBS Letter, 425, 243-248. https://doi.org/10.1016/s0014-5793(98)00237-3
• Odabasoglu, F., Cakir, A., Suleyman, H., Aslan, A., Bayir, Y., Halici, M., & Kazaz, C. (2006). Gastroprotective and antioxidant effects of usnic acid on indomethacin-induced gastric ulcer in rats. Journal of Ethnopharmacology, 103(1),59-65. https://doi.org/ 10.1016/j.jep.2005.06.043
• Odabasoglu, F., Halici, Z., Cakir, A., Halici, M., Aygun, H., Suleyman, H., Cadirci, E., & Atalay, F. (2008). Beneficial effects of vegetable oils (corn, olive and sunflower oils) and a-tocopherol on anti-inflammatory and gastrointestinal profiles of indomethacin in rats. European Journal of Pharmacology, 591(1-3),300-306. https://doi.org/10. 1016/j.ejphar.2008.06.075
• Odabasoglu, F., Yildirim, O.S., Aygun, H., Halici, Z., Halici, M., Erdogan, F., Cadirci, E., Cakir, A., Okumus, Z., Aksakal, B., Aslan, A., Unal, D., & Bayir, Y. (2012). Diffractaic acid, a novel proapoptotic agent, induces with olive oil both apoptosis and antioxidative systems in Ti-implanted rabbits. European Journal of Pharmacology. 674 (2-3), 171-178. https://doi.org/10.1016/j.ejphar.2011.11.019
• Odabasoglu, F., Yildirim, O.S., Aygun, H., Halici, Z., Halici, M., Atalay, F., Cadirci, E., Can, I., Cakir, A., Berktas, O.A., Aslan, A., Bayir, Y., Erdogan, F., & Aksakal, B. (2019). The effect of usnic acid supplementation on rabbit’s tissues surrounding implant apoptosis and some enzyme activities. Global Drugs and Therapeutics, 4, 1-7. https://doi.org/10. 15761/GDT.1000168
• Odabasoglu, F. (2001). Likenler. Pharma Sark, 3, 16-19.
• Ogaly, H.A., Alsherbiny, M.A., El Badawy, S.A., Abd- Elsalam, R.M., Li, C.G., & Azouz, A.A. (2021). Gastroprotective effects and metabolomic profiling of Chasteberry fruits against indomethacin-induced gastric injury in rats. Journal of Functional Foods, 86, 104732.
• Ohkawa, H., Ohishi, H., & Yagi, K. (1979). Assay for lipid peroxide in animal tissues by thiobarbutiric acid reaction. Analytical Biochemistry, 95,351-358. https://doi.org/10.1016/0003-2697(79)90738-3 Rojas-Martínez, R., Arrieta, J., Cruz-Antonio, L., Arrieta-Baez, D., Vel´azquez-M´endez, A., & S´anchez-Mendoza, M. (2013). Dillapiole, isolated from Peperomia pellucida, shows gastroprotector activity against ethanol-induced gastric lesions in Wistar rats. Molecule, 18, 11327-11337. https://doi.org/10.3390/molecules180911327
• Safak, B., Ciftci, I.H., Ozdemir, M., Kiyildi, N., Cetinkaya, Z., Aktepe, O.C, Altindis., M., & Asik, G. (2019). In vitro anti-Helicobacter pylori activity of usnic acid. Phytotherapy Research, 23, 955-957. https://doi.org/10.1002/ptr.2690
• Sedlak, J., & Lindsay, R.H. (1968). Estimation of total, proteinbound, and nonprotein sulfhydryls groups in tissue with Ellman’s reagent. Analytical Biochemistry, 25,192-205. https://doi.org/10.1016/0003-2697(68) 90092-4
• Solárová, Z., Liskova, A., Samec, M., Kubatka, P., Büsselberg, D., & Solár, P. (2020). Anticancer potential of lichens’secondary metabolites. Biomolecule, 10(87), 1-32. https://doi.org/10.3390/ biom10010087
• Suleyman, H., Odabasoglu, F., Aslan, A., Cakir, A., Karagoz, Y., Gocer, F., Halici, M., & Bayir, Y. (2003). Antiinflammatory and antiulcer effects of aqueous extract of Lobaria pulmonaria. Phytomedicine, 10, 552-557. https://doi.org/10.1078/ 094471103322331539
• Sun, Y., Larry, W.O., & Ying, L. (1988). A simple method for clinical assay of superoxide dismutase. Clinical Chemistry, 34(3), 497-500.
• Tahir, M., Rahman, A., & Khushtara, M. (2022). Gastroprotective effect of Hyssopus officinalis L. leaves via reduction of oxidative stress in indomethacin-induced gastric ulcer in experimental rats. Drug and Chemical Toxicology, 45(1), 291-300. https://doi.org/10.1080/01480545.2019.1685537
• Takeuchi, K., Yasuhiro, T., Asada, Y., & Sugawa, Y. (1998). Role of nitric oxide in pathogenesis of aspirin-induced gastric mucosal damage in rats. Digestion, 59, 298-307. https://doi.org/10.1159/000007506
• Valcheva-Kuzmanova, S., Denev, P., Eftimov, M., Georgieva, A., Kuzmanova, V., Kuzmanov, A., Kuzmanov, K., & Tzaneva, M. (2019). Protective effects of Aronia melanocarpa juices either alone or combined with extracts from Rosa canina or Alchemilla vulgaris in a rat model of indomethacin-induced gastric ulcers. Food and Chemical Toxicology, 132, 110739. https://doi.org/10.1016/j.fct.2019.110739
• Wei, Y., Ren, S., Wang, J., Wang, Y., Cui, Y., Tian, M., Wang, R., Liu, H., & Zhao, Y. (2021). Dehydroevodiamine ameliorates indomethacin-induced gastric injury via inhibition of ERK and p38 signaling pathway. Phytomedicine, 93,153764. https://doi.org/10.1016/j.phymed.2021.153764
• Yazici, K., & Aslan, A. (2003). Lichens from the regions of Gumushane, Erzincan and Bayburt (Turkey). Cryptogamie Mycologie, 24, 287-300.
• Yingshu, Z., Mingfu, W., & Baojun, X. (2021). A comprehensive review on secondary metabolites and health-promoting effects of edible lichen. Journal of Functional Foods, 80, 104283. https://doi.org/10. 1016/j.jff.2020.104283