Anti-Inflammatory and Antinociceptive Activities of an Acid Fraction of the Seeds of Carpotroche Brasiliensis (Raddi) (Flacourtiaceae)

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Anti-Inflammatory and Antinociceptive Activities of an Acid Fraction of the Seeds of Carpotroche Brasiliensis (Raddi) (Flacourtiaceae) Brazilian Journal of Medical and Biological Research (2005) 38: 1095-1103 Anti-inflammatory and antinociceptive activities of C. brasiliensis 1095 ISSN 0100-879X Anti-inflammatory and antinociceptive activities of an acid fraction of the seeds of Carpotroche brasiliensis (Raddi) (Flacourtiaceae) J.A. Lima1, A.S. Oliveira1, 1Departamento de Química Orgânica, Instituto de Química, A.L.P. de Miranda2, 2Laboratório de Avaliação e Síntese de Substâncias Bioativas, C.M. Rezende1 Departamento de Fármacos, Faculdade de Farmácia, and A.C. Pinto1 Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil Abstract Correspondence Carpotroche brasiliensis is a native Brazilian tree belonging to the Key words A.C. Pinto Oncobeae tribe of Flacourtiaceae. The oil extracted from its seeds • Carpotroche brasiliensis Departamento de Química Orgânica contains as major constituents the same cyclopentenyl fatty acids • Flacourtiaceae Instituto de Química, UFRJ hydnocarpic (40.5%), chaulmoogric (14.0%) and gorlic (16.1%) acids • Cyclopentenyl fatty acids Centro de Tecnologia, Bloco A found in the better known chaulmoogra oil prepared from the seeds of • Anti-inflammatory effect 21945-970 Rio de Janeiro, RJ • various species of Hydnocarpus (Flacourtiaceae). These acids are Analgesic Brasil • Antinociceptive effect Fax: +55-21-2562-7256 known to be related to the pharmacological activities of these plants E-mail: [email protected] and to their use as anti-leprotic agents. Although C. brasiliensis oil has been used in the treatment of leprosy, a disease that elicits inflamma- Research supported by FAPERJ (No. tory responses, the anti-inflammatory and analgesic activities of the E-26/171.379/2001), CNPq-PIBIC, oil and its constituents have never been characterized. We describe the Fundação Universitária José Bonifácio, anti-inflammatory and antinociceptive activities of C. brasiliensis and PRONEX. seed oil in acute and chronic models of inflammation and in peripheral and central nociception. The mixture of acids from C. brasiliensis administered orally by gavage showed dose-dependent (10-500 mg/ Received August 3, 2004 kg) anti-inflammatory activity in carrageenan-induced rat paw edema, Accepted April 29, 2005 inhibiting both the edema by 30-40% and the associated hyperalgesia. The acid fraction (200 mg/kg) also showed significant antinociceptive activity in acetic acid-induced constrictions (57% inhibition) and formalin-induced pain (55% inhibition of the second phase) in Swiss mice. No effects were observed in the hot-plate (100 mg/kg; N = 10), rota-road (200 mg/kg; N = 9) or adjuvant-induced arthritis (50 mg/kg daily for 7 days; N = 5) tests, the latter a chronic model of inflamma- tion. The acid fraction of the seeds of C. brasiliensis which contains cyclopentenyl fatty acids is now shown to have significant oral anti- inflammatory and peripheral antinociceptive effects. Braz J Med Biol Res 38(7) 2005 1096 J.A. Lima et al. Introduction in the therapy of the inflammatory reactions of leprosy and other immune inflammatory Carpotroche brasiliensis (Raddi) Endl. diseases like rheumatoid arthritis (6). It was (syn. Mayna brasiliensis Raddi) is a native also demonstrated that prostaglandin E2 Brazilian tree belonging to the Oncobeae (PGE2) plays a regulatory role in the im- tribe of Flacourtiaceae, which occurs in the mune response to Mycobacterium leprae (7). high altitude forests of the states of Rio de Although C. brasiliensis oil has been Janeiro, Minas Gerais, Espírito Santo, Ba- used in the treatment of leprosy, the anti- hia, São Paulo, and Piauí. It is commonly inflammatory and analgesic activities of the known as sapucainha and has several other oil and its constituents have never been char- local popular names such as canudeiro, acterized. babado fruit, comona fruit, cotia fruit, lep- We report here the results of a study of rosy fruit, monkey fruit, mata-piolho, papo the anti-inflammatory, anti-arthritic and an- de anjo, pau de anjo, pau de cachimbo, pau algesic activities of the cyclopentenyl fatty de cotia, pau de lepra, and ruchuchu (1). The acid mixture from C. brasiliensis. oil extracted from the seeds, whose major fatty acids are hydnocarpic, chaulmoogric Material and Methods and gorlic acids (2,3), has parasiticidal and anti-leprotic properties (Figure 1) (1,2,4,5). Plant material and preparation of the acid This class of cyclopentenyl fatty acids seems fraction of C. brasiliensis to be restricted to the seed oils of two tribes of the Flacourtiaceae family, Oncobeae and Fruits of C. brasiliensis were collected in Pangieae (3). C. brasiliensis oil, like the July 2001 at Serra do Caparaó, MG, Brazil. better known chaulmoogra oil prepared from A voucher specimen was deposited in the the seeds of various Flacourtiaceae, was used herbarium of the Museu Nacional of the in medicine for the treatment of leprosy until Federal University of Rio de Janeiro (R- 1940 when diaminodiphenyl sulfone began 203170). to be used with better results (4). The acid fraction of C. brasiliensis was Leprosy is a disease characterized by a obtained by maceration and extraction of the spectrum of clinical and immunological dried seeds (30.3 g) with 260 ml isopropanol/ manifestations, including inflammation and dichloromethane (2:1). After filtration, con- pain. One of the major modifications in the centration and extraction with 100 ml chloro- inflammatory reactions observed in leprosy form/methanol (1:2), the organic fraction was seems to be the increase in tumor necrosis concentrated under vacuum. The resulting oil factor-α (TNF-α) synthesis. Drugs that in- was then saponified by heating under reflux hibit TNF-α production, such as thalido- with 100 ml 10% (w/v) ethanolic potassium mide, have demonstrated a beneficial effect hydroxide for 3 h. After ethanol evaporation and addition of 150 ml water, the aqueous Figure 1. Chemical structures of the major cyclopentenyl fatty COOH phase was acidified with 100 ml 10% (v/v) acids from seeds of Carpotroche aqueous hydrochloric acid. The free acids were Gorlic acid brasiliensis. extracted into diethyl ether to provide the acid COOH fraction in 29% (w/w) yield after concentra- Chaulmoogric acid tion and drying over sodium sulfate (8). The chemical composition of the acidic fraction COOH was established by high-resolution gas chro- matography (HRGC; Agilent 6890, Avondale, Hydnocarpic acid PA, USA), HRGC-mass spectrometry (HRGC- Braz J Med Biol Res 38(7) 2005 Anti-inflammatory and antinociceptive activities of C. brasiliensis 1097 MS; Agilent 6890 gas chromatograph coupled Carrageenan-induced rat paw edema and to an Agilent 6973 mass-selective detector; hyperalgesia after methylation with a 30% solution of diazomethane in diethyl ether) and by 1H- and Anti-inflammatory activity was deter- 13C-NMR analyses of the mixture (Bruker mined in vivo using the carrageenan-induced DRX-300, Rheinstetten, Germany) (9,10). rat paw edema test (12). The acid fraction HRGC (FID at 280ºC) and HRGC-MS (ion- from Carpotroche seeds was administered ization energy at 70 eV, ion source at 200ºC) orally at doses of 10, 50, 100, 200, and 500 were carried out on a DB-5 (J&W, Folsom, mg/kg (0.1 ml/20 g) as a suspension in EtOH/ CA, USA) capillary column (12 m x 0.25 µm Tween 80/H2O (2:2:20, v/v/v; vehicle) 1 h x 0.22 mm). Helium was used as carrier gas before carrageenan. Control animals received (1.3 ml/min) and the injection port in the an equal volume of vehicle. Animals were splitless mode at 270ºC (0.5 min). Oven tem- then injected subplantarly with either 0.1 ml perature was programmed from 120oC (3oC/ of 1% carrageenan solution in saline (0.1 min) to 280oC (15 min). The compounds ob- mg/paw) or sterile saline (0.9% NaCl) into served are reported in terms of relative areas. one of the hind paws. Paw volumes were measured every hour up to 4 h after subplantar Animals injection using a glass plethysmometer coupled to a peristaltic pump. The edema Wistar rats (120-200 g) and Swiss albino was considered to be the difference in vol- mice (18-25 g) of both sexes were obtained ume between the carrageenan- and saline- from the LASSBio breeding unit (Faculty of treated paws. Anti-inflammatory activity was Pharmacy, UFRJ, Brazil). The animals were reported as percent inhibition of the edema maintained under standardized conditions, compared with the vehicle control group. with only water ad libitum for 12 h before Ulcerogenic effects in rats were investigated the experiment. Animal experiments were (13). Briefly, animals were euthanized and performed according to the “Principles of the stomachs excised along the greater cur- Laboratory Animal Care and Use in Re- vature for visualization of gastric lesions search” (Colégio Brasileiro de Experimen- with a stereomicroscope. tação Animal - COBEA/Instituto Brasileiro Carrageenan-evoked hyperalgesia was Carlos Chagas Filho - IBCCFo, Brazil), based quantified in separate groups of animals as a on international guidelines for the care and measure of the nociceptive response to a use of laboratory animals and ethical guide- thermal stimulus using the hot-plate test with lines for the investigation of experimental the temperature adjusted to 51 ± 1ºC (14). pain in conscious animals (11). The withdrawal latency of each hind paw was determined and hyperalgesia defined as Reagents a decrease in the ∆ latency (s) calculated as the difference between carrageenan and sa- Acetic acid, indomethacin, Tween 80, etha- line paw latency times. The withdrawal la- nol and all other chemicals were purchased tency of the saline-injected paws remained from Merck (Darmstadt, Germany). Arabic stable (11.2 ± 0.9 s), as did the withdrawal gum was from Sigma (St. Louis, MO, USA), latency of non-injected paws (data not carrageenan was from Cialgas (Taboão da shown). The C. brasiliensis seed acid frac- Serra, SP, Brazil) and morphine sulfate was tion was administered orally by gavage at a from Cristália (Itapira, SP, Brazil).
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