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Heliopsis Longipes: Anti-Arthritic Activity Evaluated in a Freund's G Model BJP 317 1–6 ARTICLE IN PRESS Revista Brasileira de Farmacognosia xxx (2016) xxx–xxx ww w.elsevier.com/locate/bjp Original Article 1 Heliopsis longipes: anti-arthritic activity evaluated in a Freund’s 2 adjuvant-induced model in rodents a,∗ b 3 Q1 Carolina Escobedo-Martínez , Silvia Laura Guzmán-Gutiérrez , a c a 4 María de los Milagros Hernández-Méndez , Julia Cassani , Alfonso Trujillo-Valdivia , a d 5 Luis Manuel Orozco-Castellanos , Raúl G. Enríquez a 6 Departamento de Farmacia, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Guanajuato, Mexico b 7 Catedrática CONACyT, Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, México, DF, Mexico c 8 Departamento de Sistemas Biológicos, Universidad Autónoma Metropolitana Unidad Xochimilco, México, DF, Mexico d 9 Instituto de Química, Universidad Nacional Autónoma de México, México, DF, Mexico 10 a b s t r a c t 11 a r t i c l e i n f o 12 13 Article history: This study assesses the anti-arthritic effect of the affinin-enriched (spilanthol, main alkamide) hexane 14 Received 26 June 2016 extract from the roots of Heliopsis longipes (A. Gray) S.F. Blake, Asteraceae, on a Freund adjuvant-induced 15 Accepted 5 September 2016 arthritis model in rodents. The extract was orally administered at a dose of 2, 6.6, or 20 mg/kg; a significant 16 Available online xxx edema-inhibitory activity in the acute and chronic phases was observed with a dose of 2 and 20 mg/kg, 17 respectively. The extract showed higher anti-inflammatory and anti-arthritic effects than the reference 18 Keywords: drug phenylbutazone (80 mg/kg). Moreover, the extract prevented the occurrence of secondary lesions 19 Heliopsis longipes associated to this pharmacological model. 20 Affinin 21 Anti-arthritic © 2016 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. This is an open 22 Complete Freund adjuvant access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 23 Spilanthol 24 Introduction ideal, Freund’s adjuvant-induced rat arthritis shares several traits 43 with human arthritis, and its sensitivity to evaluate anti-arthritic 44 25 Rheumatoid arthritis (RA) is an idiopathic auto-immune dis- agents was the basis for its choice as the model to assess the activ- 45 26 ease, characterized by symmetrical synovitis in large and small ity of the Heliopsis longipes (A. Gray) S.F. Blake, Asteraceae, hexane 46 27 joints that may lead to progressive articular damage and disability extract (Ekambaram et al., 2010; Tanushree and Saikat, 2013). 47 28 (Mendoza-Vázquez et al., 2013). Analgesic and anti-inflammatory RA prevalence in developed countries is 0.5–2%, with an annual 48 29 drugs, including steroids, are used to suppress the symptoms. New incidence of 12–1200 per 100,000 inhabitants. The female:male 49 30 therapies, like those targeting the tumor necrosis factor alpha ratio is 2–3:1, and the peak age range of onset is 30–55 years 50 31 (infliximab) or the anti-CD20 therapy (rituximab), which inhibit old, but it could occur at any age. In Mexico, RA affects 1.6% of 51 32 the underlying immune process, have been proposed. However, all general population, being the main reason for consultation at the 52 33 these drugs have several undesired effects. Recent research aims to Rheumatology Service (Mendoza-Vázquez et al., 2013; Guía de 53 34 discover long-acting anti-inflammatory drugs with minimal side Práctica Clínica, Diagnóstico y Tratamiento de Artritis Reumatoide 54 35 effects (Ekambaram et al., 2010). A number of animal models are del Adulto, México: Secretaría de Salud, 2009). 55 36 used to evaluate potentially useful compounds against RA, and the H. longipes is a perennial herb, endemic in a region comprising 56 37 choice of a particular model depends on the immunological prop- parts of Sierra de Alvarez and Sierra Gorda, near the triple border of 57 38 erties being observed in the model and their relation with the San Luis Potosi, Guanajuato and Queretaro, in Central Mexico. The 58 39 human disease. Among the available models is collagen-induced common names for this plant are chilcuague, pelitre, golden root, 59 40 or adjuvant-induced (e.g., Freund’s adjuvant) arthritis in rodents, and Aztec root (Cilia-López et al., 2008). The paralyzing and toxic 60 41 spontaneous arthritis induced by TNF-␣ or genetic models, like the action against flies and other insects of H. longipes root extracts 61 42 transgenic animal model. While no RA model can be considered was discovered as similar as that of pyrethrins during World War 62 II (Acree et al., 1945). 63 Fortunately, chilcuague did not become extinct after the expor- 64 ∗ tation boom, even though its wild population was severely reduced. 65 Corresponding author. 66 E-mail: [email protected] (C. Escobedo-Martínez). To date, land plots solely dedicated to the cultivation of this species, http://dx.doi.org/10.1016/j.bjp.2016.09.003 0102-695X/© 2016 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: Escobedo-Martínez, C., et al. Heliopsis longipes: anti-arthritic activity evaluated in a Freund’s adjuvant- induced model in rodents. Revista Brasileira de Farmacognosia (2016), http://dx.doi.org/10.1016/j.bjp.2016.09.003 G Model BJP 317 1–6 ARTICLE IN PRESS 2 C. Escobedo-Martínez et al. / Revista Brasileira de Farmacognosia xxx (2016) xxx–xxx 67 disseminated either by seed or by cutting, can be found between Among the recent studies on H. longipes is the assessment of 119 68 Guanajuato and Queretaro; the root is fully developed after 2–3 ethanolic extract and affinin as potential anti-mutagenic and anti- 120 69 years (García-Chávez et al., 2004). It is the most economically carcinogenic agents. The anti-mutagenic properties of affinin were 121 70 important species in its genus; its root is used in the region as evaluated by adding it to several mutagens, either with or without 122 71 a cooking condiment, and it is added to alcoholic beverages to S9 metabolic activation, in Salmonella typhimurium (TA98, TA100, 123 72 improve taste. In traditional medicine, chilcuague root is used to and TA102 strains) cultures. Affinin significantly decreased the 124 73 treat respiratory diseases, as an anesthetic to treat tooth and mus- point mutations induced by 2-aminoanthracene (2AA) (40%) and 125 74 cular aches, to treat buccal lesions, and as an anti-parasitic (Cilia decreased the DNA oxidative damage induced by norfloxacin (NOR) 126 75 López, 2007). Several alkamides have been isolated from H. longipes, (37–50%). Additionally, it showed antioxidant properties capable 127 76 but affinin, also known as spilanthol ((2E,6Z,8E)-N-isobutyl-2,6,8- of reducing the rate of 2AA- and NOR-induced mutation in S. 128 77 decatrienamide), was identified as the main alkamide in the plant typhimurium TA98 and TA102, respectively, which could be rele- 129 78 (Molina-Torres et al., 1996; García-Chávez et al., 2004; Hernández vant to treat some pain symptoms related to anti-radical activity 130 79 et al., 2009). The oily substance causes intense lip numbness and (Arriga-Alba et al., 2013). 131 80 tingling within a few minutes after placed in the mouth, and it 81 also stimulates salivation (Correa et al., 1971). H. longipes is also Materials and methods 132 82 reported to produce analgesia and anti-inflammation in human 83 dental and oral pathologies (Colvard et al., 2006). Additionally, it Plant material 133 84 has been reported that H. longipes dichloromethane extract showed 85 analgesic activity, as demonstrated in vitro by releasing of gamma- H. longipes (A. Gray). S.F. Blake, Asteraceae, roots were collected 134 86 aminobutyric acid (GABA) in mouse brain slices; the increase in on February 16, 2014, 2:14:59 pm, within the boundaries of a land 135 87 GABA release in a region of cerebral cortex leads to sustained ◦ ◦ plot in Beltran community (N 21 16.427 , W 100 0.2672 ) at 1780 m 136 88 analgesia, favoring a descendent inhibition of nociceptive spinal above sea level, Xichu municipality, in Guanajuato, Mexico. After 137 89 neurons (Ríos et al., 2007). proper identification, five plant specimens were deposited in the 138 90 With regard to anti-inflammatory activity, Hernández et al. Isidro Palacios herbarium (SLPM), at the Universidad Autónoma de 139 91 (2009) evaluated H. longipes ethanolic extract and purified affinin San Luis (No. 048150). 140 92 on mouse ear edema induced by either arachidonic acid (AA) 93 or phorbol 12-myristate 13-acetate (PMA), demonstrating a sig- 141 94 nificant anti-inflammatory effect. DE50 values of 0.8 mg/ear and Extraction 95 1.2 mg/ear were obtained, respectively, in the AA-induced edema 142 96 model; nimesulide (1 mg/ear) was used as reference drug. In Dry, ground H. longipes roots (1285 g) were macerated for three 143 97 the PMA-induced edema model, the ethanolic extract and affinin consecutive times: First component extraction was performed 144 98 showed a dose-dependent anti-inflammatory effect with DE50 val- with 2.5 l of hexane for 2 h; then, the recovered extract solu- 145 99 ues of 2 mg/ear and 1.3 mg/ear, respectively, using indometacin tion (1750 ml) was evaporated, yielding a dark yellow, viscous oil 146 100 (3 mg/ear) as reference drug. (26.386 g, labeled as Hl-A). A second maceration was performed on 147 101 On the other hand, Cilia-López et al.
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