Reduction of paw edema and liver oxidative stress in carrageenan-induced acute inflammation by Lobaria pulmonaria and Parmelia caperata, lichen species, in mice
Abstract
Abstract. Paw edema volume reduction is a useful marker in determining the anti-inflammatory effect of drugs and plant extracts in carrageenan-induced acute inflammation. In this study, the anti-inflammatory effect of Lobaria pulmonaria (LP) and Parmelia caperata (PC), two lichen species, was examined in carrageenan-induced mouse paw edema test. Compared to the controls in carrageenan-induced inflammation (n = 5/group), our results showed that pretreatment by single oral doses with PC extract (50–500 mg/kg) gives better results than LP extract (50–500 mg/kg) in terms of anti-edematous activity, as after 4 h of carrageenan subplantar injection, paw edema formation was inhibited at 82–99% by PC while at 35–49% by LP. The higher anti-inflammatory effect of PC, at all doses, was also observed on the time-course of carrageenan-induced paw edema, displaying profile closely similar to that obtained with diclofenac (25 mg/kg), an anti-inflammatory drug reference (all p < 0.001). Both LP and PC, at all doses, significantly ameliorated liver catalase (CAT) activity (all p < 0.05). However, superoxide dismutase (SOD) activity, glutathione peroxidase (GPx) activity and glutathione (GSH) levels were found increased in liver of PC- compared to LP-carrageenan-injected mice. Our findings demonstrated on one hand higher preventive effects of PC compared to LP in a mouse carrageenan-induced inflammatory model and suggested, on the other hand, that anti-inflammatory effects elicited by the two lichens were closely associated with the amelioration in the endogenous antioxidant status of liver.
References
1 (2014) Lichens: chemistry and biological activities. Stud Nat Prod Chem. 43, 223–257.
2 (2008) Lichen Biology, Cambridge University Press. 486 pp.
3 (2001) Guide des lichens: 350 espèces de lichens d’Europe, Delachaux et Niestlé Ed. 304 pp.
4 (1993) Guide des lichens, 376 pp., Lechevalier Ed.
5 (1993) Identification of lichen substances by a standardized high-performance liquid chromatographic method. J Chromatogr. A. 646 (2): 417–427.
6 (2007) Lichen secondary metabolites from the cultured lichen mycobionts of Teloschistes chrysophthalmus and Ramalina celastri and their antiviral activities. Z Naturforsch C. 62 (7–8): 543–549.
7 (2008) Biochemistry and secondary metabolites. In: Lichen biology (Nash, T.H., III, ed), pp. 104–133. Cambridge University Press.
8 (2008) Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimate metabolite production, and PKS genes. Nat Prod Rep. 25, 188–200.
9 (2011) Variable responses of different human cancer cells to the lichen compounds parietin, atranorin, usnic acid and gyrophoric acid. Toxicol Vitr. 25, 37–44.
10 (1996) Identification of lichen substances. pp. 304–349., Springer, Berlin Heidelberg.
11 (2010) Lichens as a potential natural source of bioactive compounds: a review. Phytochem Rev. 9 (2): 303–314.
12 (1996) Biochemistry and secondary metabolites. In: Lichen biology(Nash, T.H., ed), pp. 154–181. Cambridge University Press.
13 (2011) Bioactive lichen metabolites: alpine habitats as an untapped source. Phytochem Rev. 10 (3): 287–307.
14 (2013) Lichens: a promising source of antibiotic and anticancer drugs. Phytochem Rev. 12, 229–244.
15 (2017) Antibacterial activities of natural lichen compounds against Streptococcus gordonii and Porphyromonas gingivalis. Fitoterapia. 121, 164–169.
16 (1999) Lichen metabolites 2. Antiproliferative and cytotoxic activity of gyrophoric, usnic and diffractaic acids on human keratinocyte growth. J Nat Prod. 62 (6): 821–823.
17 (2003) Anti-inflammatory and antiulcerogenic effects of the aqueous extract of Lobaria pulmonaria (L.) Hoffm. Phytomedicine. 10, 552–557.
18 (2005) Antioxidant activity, reducing power and total phenolic content of some lichen species. Fitoterapia. 76, 216–219.
19 (2009) The effects of methanol extract of Lobaria pulmonaria, a lichen species, on indometacin-induced gastric mucosal damage, oxidative stress and neutrophil infiltration. Phytother Res. 23 (5): 635–639.
20 (2011) Antioxidant phenolics from Lobaria pulmonaria (L.) Hoffm. and Usnea longissima Ach. lichen species. Turk J Chem. 35, 647–661.
21 (2010) Medicinal lichens of India. In: Drugs from plants (Trivedi, P.C., ed), pp. 1–38., Avishkar Publishers, Distributors, Jaipur, India.
22 (2015) Lichens used in traditional medicine, p. 27–80. In: Lichen secondary metabolites: Bioactive properties and pharmaceutical potential. (Rankovic B., ed), (pp. 202). Springer (ISBN: 978-3-319-13373-7).
23 (2012) Chemical composition, antioxidant, and antimicrobial activities of lichen Umbilicaria cylindrica (L.) Delise (Umbilicariaceae). Evid Based Complement Alternat Med. 2012, 431452. doi: 10.1155/2012/452431.
24 (2013) Guide des lichens de France : Lichens des arbres, 239 pp. Belin.
25 (2013) Contribution à l’étude de la biodiversité des lichens dans le Parc National de Taza, thèse de magister, 100 pp., Université Mohamed Seddiki Ben yahia, Jijel, Algérie.
26 (1962) Carrageenan-induced edema in hind paw of the rat as an assay for anti-inflammatory drugs. Proc Soc Exp Biol Med. 111, 544–547.
27 (2003) Dietary supplementation of curcumin enhanced antioxidant and phase II metabolizing enzymes in ddY male mice: Possible role in protection against chemical carcinogenesis and toxicity. Pharmacol Toxicol. 92, 33–38.
28 (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72, 248–254.
29 (1971) Assay of superoxide dismutase. Anal Biochem. 44, 276–87.
30 (1984) Catalase in vitro. Methods Enzymol. 105, 121–126.
31 (1988) Ribonucleotide reductase activity and growth of glutathione-depleted mouse leukemia L 1210 cells in vitro. Cancer Lett. 40, 257–264.
32 (1984) Assays of glutathione peroxidase. Methods Enzymol. 105, 114–121.
33 (2004) What is “inflammation”? Are we ready to move beyond Celsus? Br J Sports Med. 38, 248–249.
34 (2004) What do we mean by the term “inflammation”? A contemporary basic science update for sports medicine. Br J Sports Med. 38, 372–380.
35 (2007) Amiadorane has anti-inflammatory and antioxidative properties: an experimental study in rats with carrageenan-induced paw edema. Eur J Pharmacol. 566, 215–221.
36 (2013) Anti-inflammatory effects of an aqueous extract of Welsh onion green leaves in mice. Food Chem. 138, 751–756.
37 (1996) Nitric oxide: a key mediator in the early and late phase of carrageenan-induced rat paw inflammation. Br J Pharmacol. 118, 829–838.
38 (2004) Carrageenan-induced mouse paw oedema is biphasic, age-weight dependent and displays differential nitric oxide cyclooxygenase-2 expression. Br J Pharmacol. 142, 331–338.
39 (2015) Effects of endocrine disrupters on immune function and inflammation. In: Endocrine Disruption and Human Health (P.D. Darbre, ed), pp. 257–272. Elsevier.
40 (2000) Evaluated serum leptin concentrations induced by experimental acute inflammation. Life Sci. 67 (20): 2433–2441.
41 (1969) Biphasic development of carrageenan edema in rats. J. Pharmacol Exp Ther. 166, 96–103.
42 (1971) Studies on the mediators of the acute inflammatory response induced in rats in different sites by carrageenan and turpentine. J Pathol. 104, 15–29.
43 (1999) Role of oxygen radicals and arachidonic acid metabolites in the reverse passive arthus reaction and carrageenin paw edema in the rat. Br J Pharmacol. 110, 896–902.
44 (1998) Regulation of cyclooxygenase gene expression in rat smooth muscle cells by catalase. Biochem Pharmacol. 55, 1621–1631.
45 (2007) Antiinflammatory and antioxidant activities of Desmodium gangeticum fractions in carrageenan-induced inflamed rats. Phytother Res. 21, 975–979.
46 (2010) Evaluation of anti-inflammatory and antioxidant activities of Peltigera rufescens lichen species in acute and chronic inflammation models. J Nat Med. 64, 42–49.
47 (2017) In vivo analgesic, anti-inflammatory and antioxidant potentials of Achillea odorata from north Algeria. S Afr J Bot. 112, 307–313.
48 (2017) Anti-inflammatory, analgesic and antioxidant effects of phenolic compound from Algerian Mentha rotundifolia L. leaves on experimental animals. S Afr J Bot. 113, 77–83.
49 (2000) Immunotoxicology: role of inflammation in chemical-induced hepatotoxicity. Int J Immunopharmacol. 22 (12): 1143–1147.
50 (2012) Dietary derived antioxidants: implications on health, pp. 1–22. Chapter invited for the book “Nutrition, Well-Being and Health”, pp. 224 (ISBN 978-953-51-0125-3), Bouayed J & Bohn T, Eds., Intech, Rijeka, Croatia.
51 (2010) Effects of reduced glutathione on nitric oxide level, total antioxidant and oxidant capacity and adenosine deaminase activity. Eur Rev Med Pharmacol Sci. 14, 19–23.
52 (2011) Glutathione is a Physiologic Reservoir of Neuronal Glutamate. Biochem Biophys Res Commun. 409 (4): 596–602.
53 (2016) Evaluation of Parmotrema reticulatum taylor for antibacterial and antiinflammatory activities. Indian J Pharm Sci. 78 (1): 94–102.
54 (2017) 2-Pentadecyl-2-oxazoline, the oxazoline of pea, modulates carrageenan-induced acute Inflammation. Front Pharmacol. 8, 308. doi: 10.3389/fphar.2017.00308.
55 (2018) Lichens as a source of chemical compounds with anti-inflammatory activity. Herba Pol. 64 (1): 56–64.
56 (2015) The immunostimulating role of lichen polysaccharides: a review. Phytother Res. 29 (3): 317–22.
57 (2005) Effects of lichen heteroglycans on proliferation and IL-10 secretion by rat spleen cells and IL-10 and TNF-alpha secretion by rat peritoneal macrophages in vitro. Phytomedicine. 12 (6–7): 461–7.
58 (1998) Antiproliferative effects of lichen-derived inhibitors of 5-lipoxygenase on malignant cell-lines and mitogen-stimulated lymphocytes. J Pharm Pharmacol. 50, 107–115.
59 (1982) Depside as potent inhibitor of prostaglandin biosynthesis: a new active site model for fatty acid cyclooxygenase. Prostaglandins. 24 (1): 21–34.
60 (2000) Anti-inflammatory activity of (+)-usnic acid. Fitoterapia. 71 (5): 564–566.
61 (2012) Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites. Phytomedicine. 19 (13): 1166–1172.