Gamma-Terpinene Modulates Acute Inflammatory Response in Mice

Theresa Raquel de Oliveira Ramalho; Maria Talita Pacheco de Oliveira; Ana Luisa de Araujo Lima; Claudio Roberto Bezerra-Santos; Marcia Regina Piuvezam

doi:10.1055/s-0035-1546169

Planta Medica, Inhaltsverzeichnis

Planta Med 2015; 81(14): 1248-1254
DOI: 10.1055/s-0035-1546169

Biological and Pharmacological Activity

Original Papers

Georg Thieme Verlag KG Stuttgart · New York

Gamma-Terpinene Modulates Acute Inflammatory Response in Mice

Autor*innen

Theresa Raquel de Oliveira Ramalho

¹Universidade Federal da Paraíba, Centro de Ciências Exatas e da Natureza, Programa de Pós-Graduação em Biologia Celular e Molecular, João Pessoa, Paraíba, Brasil
Maria Talita Pacheco de Oliveira

¹Universidade Federal da Paraíba, Centro de Ciências Exatas e da Natureza, Programa de Pós-Graduação em Biologia Celular e Molecular, João Pessoa, Paraíba, Brasil
Ana Luisa de Araujo Lima

²Universidade Federal da Paraíba, Centro de Ciências da Saúde, Programa de Pós-Graduação em Produtos Naturais e Sintéticos Bioativos, João Pessoa, Paraíba, Brasil
Claudio Roberto Bezerra-Santos

³Universidade Federal da Paraíba, Departamento de Fisiologia e Patologia, Laboratório de Imunofarmacologia, João Pessoa, Paraíba, Brasil
Marcia Regina Piuvezam

¹Universidade Federal da Paraíba, Centro de Ciências Exatas e da Natureza, Programa de Pós-Graduação em Biologia Celular e Molecular, João Pessoa, Paraíba, Brasil

²Universidade Federal da Paraíba, Centro de Ciências da Saúde, Programa de Pós-Graduação em Produtos Naturais e Sintéticos Bioativos, João Pessoa, Paraíba, Brasil

³Universidade Federal da Paraíba, Departamento de Fisiologia e Patologia, Laboratório de Imunofarmacologia, João Pessoa, Paraíba, Brasil

Abstract

The monoterpene gamma-terpinene is a natural compound present in essential oils of a wide variety of plants, including the Eucalyptus genus, which has been reported to possess anti-inflammatory activity. The goal of this study was to evaluate the effect of gamma-terpinene on several in vivo experimental models of acute inflammation. Swiss mice were pretreated with gamma-terpinene and subjected to protocols of paw edema with different phlogistic agents such as carrageenan, prostaglandin-E₂, histamine, or bradykinin. The microvascular permeability was measured by intraperitoneal injection of acetic acid and measuring the amount of protein extravasation. Carrageenan-induced peritonitis was used to analyze the effect of gamma-terpinene on inflammatory cell migration and cytokine production. We also developed an acute lung injury protocol to define the anti-inflammatory effect of gamma-terpinene. Mice pretreated with gamma-terpinene displayed reduced paw edema induced by carrageenan from 1–24 h after challenge. A similar reduction was observed when gamma-terpinene was administered after stimulation with PGE₂, bradykinin, and histamine. Treatment with gamma-terpinene also inhibited fluid extravasation in the acetic acid model of microvascular permeability. In a carrageenan-induced peritonitis model, gamma-terpinene treatment reduced neutrophil migration as well as the production of interleukin-1β and tumor necrosis factor-α when compared to nontreated animals, and in the acute lung injury protocol, gamma-terpinene diminished the neutrophil migration into lung tissue independently of the total protein extravasation in the lung. These data demonstrate that, in different models of inflammation, treatment with gamma-terpinene alleviated inflammatory parameters such as edema and pro-inflammatory cytokine production, as well as cell migration into the inflamed site, and that this monoterpene has anti-inflammatory properties.

Key words

gamma-terpinene - mice - acute inflammation - mediators

Volltext

Referenzen

References
1 Medzhitov R. Inflammation 2010: new adventures of an old flame. Cell 2010; 140: 771-776
2 Yang Y, Tang LO, Wei W. Prostanoids receptors signaling in different diseases/cancers progression. J Recept Signal Transduct Res 2013; 33: 14-27
3 Noursadeghi M, Cohen J. Immunopathogenesis of severe sepsis. J R Coll Physicians Lond 2000; 34: 432-436
4 Hargreaves DC, Medzhitov R. Innate sensors of microbial infection. J Clin Immunol 2005; 25: 503-510
5 Filgueiras LR, Martins JO, Serezani CH, Capelozzi VL, Montes MBA, Jancar S. Sepsis-induced acute lung injury (ALI) is milder in diabetic rats and correlates with impaired NFkB activation. PLoS One 2012; 7: e44987
6 Yoshimura A, Suzuki M, Sakaguchi R, Hanada T, Yasukawa H. SOCS, inflammation, and autoimmunity. Front Immunol 2012; 3: 20
7 Terpstra ML, Aman MD, Van Nieuw Amerongen GP, Groeneveld AB. Plasma biomarkers for acute respiratory distress syndrome: A systematic review and meta-analysis. Crit Care Med 2014; 42: 691-700
8 Johnson ER, Matthay MA. Acute lung injury: epidemiology, pathogenesis, and treatment. J Aerosol Med Pulm Drug Deliv 2010; 23: 243-252
9 Schimmer BP, Parker KL. Hormônio adrenocorticotrópico; esteroides adrenocorticais e seus análogos sintéticos; inibidores da síntese e das ações dos hormônios adrenocorticais. In: MGH, editor Goodman & Gilman: as bases farmacológicas da terapêutica. Rio de Janeiro: McGraw and Hill; 2003: 10
10 Pereira NP, Miguel OG, Miguel MD. Composição química do óleo fixo obtido dos frutos secos da [Chamomilla recutita (L.) Rauschert] produzida no município de Mandirituba, PR. Rev Bras Farmacogn 2005; 15: 334-337
11 Zakaria ZA, Patahuddin H, Mohamad AS, Israf DA, Sulaiman MR. In vivo anti-nociceptive and anti-inflammatory activities of the aqueous extract of the leaves of Piper sarmentosum . J Ethnopharmacol 2010; 128: 42-48
12 Lima MS, Quintans-Junior LJ, Santana WAK, Martins Kaneto C, Pereira Soares MB, Villareal CF. Anti-inflammatory effects of carvacrol: Evidence for a key role of interleukin-10. Eur J Pharmacol 2013; 14: 112-117
13 Guimarães AG, Quintans JS, Quintans-Junior LJ. Monoterpenes with analgesic activity – a systematic review. Phytother Res 2013; 27: 1-15
14 Siveen KS, Kuttan G. Thujone inhibits lung metastasis induced by B16F-10 melanoma cells in C57BL/6 mice. Can J Physiol Pharmacol 2011; 89: 691-703
15 Chagas ACS, Passos WM, Prates HT, Leite RM, Furlong J, Pereira Fortes IC. Acaricide effect of Eucalyptus spp. essential oils and concentrated emulsion on Boophilus microplus . Braz J Vet Res Anim Sci 2002; 39: 247-253
16 Kim KN, Ko YJ, Yang HM, Ham YM, Roh SW, Jeon YJ, Ahn G, Kang MC, Yoon WJ, Kim D, Oda T. Anti-inflammatory effect of essential oil and its constituents from fingered citron (Citrus medica L. var. sarcodactylis) through blocking JNK, ERK and NF-κB signaling pathways in LPS-activated RAW 264.7 cells. Food Chem Toxicol 2013; 57: 126-131
17 Béjaoui A, Chaabane H, Jemli M, Boulila A, Boussaid M. Essential oil composition and antibacterial activity of Origanum vulgare subsp. glandulosum Desf. at different phenological stages. J Med Food 2013; 16: 1115-1120
18 Tao N, Jia L, Zhou H. Anti-fungal activity of Citrus reticulata Blanco essential oil against Penicillium italicum and Penicillium digitatum . Food Chem 2014; 153: 265-272
19 Öztürk M. Anticholinesterase and antioxidant activities of Savoury (Satureja thymbra L.) with identified major terpenes of the essential oil. Food Chem 2012; 134: 48-54
20 Milde J, Elstner EF, Grassmann J. Synergistic inhibition of low-density lipoprotein oxidation by rutin, γ-terpinene, and ascorbic acid. Phytomedicine 2004; 11: 105-113
21 Damas J, Remacle-Volon G. Influence of a long-acting bradykinin antagonist, Hoe 140, on some acute inflammatory reactions in the rat. Eur J Pharmacol 1992; 211: 81-86
22 Handy RL, Moore PK. A comparison of the effects of L-NAME, 7-NI and L-NIL on carrageenan-induced hindpaw oedema and NOS activity. Br J Pharmacol 1998; 123: 1119-1126
23 Medeiros MV, Binhara IM, Moreno H, Zats R, De Nucci G, Antunes E. Effect of chronic nitric oxide synthesis inhibition on the inflammatory responses induced by carrageenan in rats. Eur J Pharmacol 1995; 285: 109-114
24 Vaz ZR, Cechinel V, Yunes RA, Calixto JB. Antinociceptive action of 2-(-4bromobenzoyl)-3-methy-4–6-dimethoxybenzofuran, a novel xanthoxyline derivative of chemical and thermal models of nociception in mice. J Pharmacol Exp Ther 1996; 278: 304-312
25 Hajhashemi V, Sajjadj SE, Zomorodkia M. Antinociceptive and anti-inflammatory activities of Bunium persicum essential oil, hydroalcoholic and polyphenolic extracts in animal models. Pharm Biol 2011; 49: 146-151
26 Claudino RF, Kassuya CAL, Ferreira J, Calixto JB. Pharmacological and molecular characterization of the mechanisms involved in prostaglandin E2-induced mouse paw edema. J Pharmacol Exp Ther 2006; 318: 611-618
27 Morimoto K, Shirata N, Taketomi Y, Tsuchiya S, Segi-Nishida E, Inazumi T, Kabashima K, Tanaka S, Murakami M, Narumiya S, Sugimoto Y. Prostaglandin E2-EP3 signaling induces inflammatory swelling by mast cell activation. J Immunol 2014; 192: 1130-1137
28 Trabold R, Eros C, Zweckberger K, Relton H, Nussberger J, Müller-Esterl W, Bader M, Whalley E, Plesnila N. The role of bradykinin B(1) and B(2) receptors for secondary brain damage after traumatic brain injury in mice. J Cereb Blood Flow Metab 2010; 30: 130-139
29 Falhout M, Deraedt R, Jougney S, Delevalcee F. Release of prostaglandin E and F in an algogenic reaction and its inhibition. Eur J Pharmacol 1980; 51: 17-24
30 Collier HO, Dinneen LC, Johnson CA, Schneider C. The abdominal constriction response and its suppression by analgesic drugs in the mouse. Br J Pharmacol Chemother 1968; 32: 295-310
31 Deraedt R, Jougney S, Delevalcee F, Flahaut M. Release of prostaglandin E and F in an algogenic reaction and its inhibition. Eur J Pharmacol 1980; 51: 17-24
32 Malech HL, Gallin JI. Current concepts: immunology-neutrophils in human diseases. N Engl J Med 1987; 317: 687-694
33 Salvemini D, Mazzon E, Dugo L, Riley DP, Serraino I, Caputi AP, Cuzzocrea S. Pharmacological manipulation of the inflammatory cascade by superoxide dismutase mimetic. Br J Pharmacol 2001; 132: 815-827
34 Loram LC, Fuller A, Fick LG, Cartmell T, Poole S, Mitchell D. Cytokine profiles during carrageenan-induced inflammatory hyperalgesia in rat muscle and hind paw. J Pain 2007; 8: 127-136
35 Omote K, Hazama K, Kawamata T, Kawamata M, Nakayaka Y, Toriyabe M, Namiki A. Peripheral nitric oxide in carrageenan-induced inflammation. Brain Res 2001; 912: 171-175
36 Juergens UR, Stober M, Vetter H. Inhibition of cytokine production and arachidonic acid metabolism by eucalyptol (1, 8-cineole) in human blood monocytes in vitro . Eur J Med Res 1998; 17: 508-510
37 Hirahara K, Poholek A, Vahedi G, Laurence A, Kanno Y, Milner JD, OʼShea JJ. Mechanisms underlying helper T-cell plasticity: Implications for immune-mediated disease. J Allergy Clin Immunol 2013; 131: 1276-1287