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Iridoids and Amino Acid Derivatives from the Paraguayan Crude Drug Adenocalymma Marginatum (Ysypó Hû)

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Iridoids and Amino Acid Derivatives from the Paraguayan Crude Drug Adenocalymma Marginatum (Ysypó Hû) molecules Article Iridoids and Amino Acid Derivatives from the Paraguayan Crude Drug Adenocalymma marginatum (ysypó hû) Guillermo Schmeda-Hirschmann 1,* , Alberto Burgos-Edwards 1, Felipe Jiménez-Aspee 2 , Daniel Mieres-Castro 1, Cristina Theoduloz 3, Lisa Pormetter 1, Ramon Fogel 4, Claudia Céspedes 4 , Nelida Soria 4 and Sintya Valdez 4 1 Laboratorio de Química de Productos Naturales, Instituto de Química de Recursos Naturales, Universidad de Talca, Campus Lircay, Talca 3460000, Chile; [email protected] (A.B.-E.); [email protected] (D.M.-C.); [email protected] (L.P.) 2 Departamento de Ciencias Básicas Biomédicas, Facultad de Ciencias de la Salud, Universidad de Talca, Campus Lircay, Talca 3460000, Chile; [email protected] 3 Laboratorio de Cultivo Celular, Facultad de Ciencias de la Salud, Universidad de Talca, Campus Lircay, Talca 3460000, Chile; [email protected] 4 Centro de Estudios Rurales Interdisciplinarios, Oliva 1019, Edificio Lider V, Piso 17, oficina 172, Asunción 01421, Paraguay; [email protected] (R.F.); [email protected] (C.C.); [email protected] (N.S.); [email protected] (S.V.) * Correspondence: [email protected]; Tel.: +56-712-200-288 Received: 5 December 2019; Accepted: 27 December 2019; Published: 1 January 2020 Abstract: The crude drug ysypó hû (Adenocalymma marginatum DC., Bignoniaceae) is used traditionally by the Guarani of Eastern Paraguayan as a male sexual enhancer. The aim of the present study was to identify the main constituents of the crude drug and to evaluate the in vitro inhibitory activity towards the enzyme phosphodiesterase-5 (PDE-5). The main compounds were isolated by counter-current chromatography (CCC). The metabolites were identified by spectroscopic and spectrometric means. The chemical profiling of the extracts was assessed by high-performance liquid chromatography coupled to mass spectrometry (HPLC-MS/MS). The crude extract and main isolated compounds were tested for their PDE-5 inhibitory activity using commercial kits. The iridoid theviridoside and 4-hydroxy-1-methylproline were isolated as the main constituent of the crude drug. Four chlortheviridoside hexoside derivatives were detected for the first time as natural products. Chemical profiling by HPLC-MS/MS led to the tentative identification of nine iridoids, six phenolics, and five amino acids. The crude extracts and main compounds were inactive towards PDE-5 at concentrations up to 500 µg/mL. Iridoids and amino acid derivatives were the main compounds occurring in the Paraguayan crude drug. The potential of ysypó hû as a male sexual enhancer cannot be discarded, since other mechanisms may be involved. Keywords: Adenocalymma marginatum; Bignoniaceae; counter-current chromatography; iridoids; amino acid derivatives; Guarani medicine; Paraguayan crude drug 1. Introduction The Guarani Amerindians inhabited large parts of eastern South America before the European conquest. The group included the Tupi and Guarani people, living from the costs of the Atlantic Ocean to the subtropical forests of Paraguay and eastern Argentina. The Tupi–Guarani Amerindians are closely related, sharing a common language and playing a relevant role in the South American traditional medicine and culture [1]. Paraguayan traditional medicine has strong roots in Guarani Molecules 2020, 25, 180; doi:10.3390/molecules25010180 www.mdpi.com/journal/molecules Molecules 2020, 25, 180 2 of 16 Molecules 2019, 24, x 2 of 16 culture and has provided the world with relevant food and medicinal plants, including the tea mate (Ilex(Ilex paraguariensisparaguariensis)[) 2[2],], thethe sweetsweet herbherb steviastevia (“kaa(“kaa hee”,hee”,Stevia Stevia rebaudianarebaudiana)[) 3[3],], andand hundredshundreds ofof medicinalmedicinal plants plants widely widely used used in in South South America. America. TheThe use use of of medicinal medicinal plants plants by theby the Guarani Guarani people people was describedwas described by Pedro by dePedro Montenegro de Montenegro (1770), during(1770), theduring Spanish the JesuitSpanish Missions Jesuit Missions in Paraguay in Paraguay [4]. Plant [4]. and Plant animal and drugs animal were drugs selected were based selected on empiricalbased on knowledgeempirical knowledge and the self-experience and the self-experience of the healers. of Thethe healers. use of sexual The use enhancers of sexual by enhancers the Guarani by peoplethe Guarani is not common.people is not However, common. fertility However, control fertility was widespread, control was with widespread, plants used with as contraceptiveplants used as andcontraceptive as abortifacients and as [5abortifacients]. The Bignoniaceae [5]. The AdenocalymmaBignoniaceae Adenocalymma marginatum (Cham.) marginatum DC. (Figure(Cham.)1) DC. is commonly(Figure 1) knownis commonly as “ysyp óknownhû” (black as “ysypó vine) by hû” the Pai(black Tavytera vine) andby Mbythe áPaiAmerindians, Tavytera and who Mbyá live inAmerindians, northeastern who Paraguay. live in The northeastern plant has the Paraguay. synonyms TheAdenocalymma plant has marginatumthe synonymsvar. Adenocalymma marginatum, A.marginatum marginatum var.var. marginatum, polystachyum A. DC, marginatum and the basionym var. polystachyumBignonia marginata DC, andCham. the [6basionym]. The plant, Bignonia fresh ormarginata in decoction, Cham. is recommended[6]. The plant, fresh to improve or in decoction, fecundity is and recommended as a male sexual to improve enhancer fecundity [7,8]. The and crude as a drugmale includes sexual enhancer the aerial [7,8]. parts The of the crude plant drug (leaves includes and stem) the butaerial consists parts mainlyof the plant of stems. (leaves The and root stem) was includedbut consists in this mainly study of for stems. comparison The root purposes. was included For the in preparationthis study for of thecomparison drug, the purposes. stem and For leaves the arepreparation powdered, of and the adrug, handful the isstem placed and in leaves 1 L water are po andwdered, boiled forand 3–5 a handful min. After is placed cooling, in the1 L decoctionwater and isboiled taken for orally 3–5 (aboutminutes. 200 After mL) twocooling, times the a day,decoction as long is as taken necessary. orally The(about preparation 200 mL) two is also times included a day, inas mate long tea, as necessary. where mate The is thepreparation carrier of theis also medicinal included plants in mate [2]. Ittea, is alsowhere used mate to relieveis the carrier rheumatism of the andmedicinal as anti-diarrheic plants [2]. [7It, 8is]. also used to relieve rheumatism and as anti-diarrheic [7,8]. A B C Figure 1. The Paraguayan crude drug “ysypó hû” (Adenocalymma marginatum). (A) flowering plant; (BFigure) aerial 1. parts; The Paraguayan (C) root and crude stem. drug “ysypó hû” (Adenocalymma marginatum). (A) flowering plant; (B) aerial parts; (C) root and stem. The use of plants and animal parts as sexual enhancers is a known practice worldwide [9]. Since ancientThe times, use of several plants naturaland animal products parts as have sexual been enhancers used as is sexual a known enhancers practice for worldwide the treatment [9]. Since of erectileancient dysfunction, times, several including natural yohimbineproducts have from beenPausinystalia used as yohimbe sexual (Rubiaceae),enhancers for forskolin the treatment from the of erectile dysfunction , including yohimbine from Pausinystalia yohimbe (Rubiaceae), forskolin from the Indian herb Plectranthus barbatus (Lamiaceae), or the “Peruvian Viagra” Lepidium meyenii (Brassicaceae), among many others [10]. They are popularly considered safe and “natural”, and no Molecules 2020, 25, 180 3 of 16 Indian herb Plectranthus barbatus (Lamiaceae), or the “Peruvian Viagra” Lepidium meyenii (Brassicaceae), among many others [10]. They are popularly considered safe and “natural”, and no strict regulation is applied to control their sale. Unfortunately, a study published in 2015 showed that 61% of a total of 150 supplements were altered with synthetic phosphodiesterase-5 (PDE-5) inhibitors, including the commercial drug sildenalfil, or structurally modified analogs [11]. We recently reported the chemical composition and potential male sexual enhancer activity of Campsiandra angustifolia, Minquartia guianensis, Swartzia polyphylla, and Tynanthus panurensis, as well as from two traditional preparations of the Peruvian Amazon. In our experiment, C. angustifolia was found to be a potent inhibitor of PDE-5 in vitro [12]. The occurrence of the iridoids ipolamiide, strictoloside, and theviridoside in leaves of A. marginatum from Rio Grande do Sul (southern Brazil) has been reported [13]. However, no information is available on the chemical composition of the Paraguayan crude drug, nor on the male sexual enhancement capacity of A. marginatum. Hence, the aims of the present study were to isolate and characterize the main secondary metabolites from the Paraguayan crude drug ysypó hû. Additionally, the potential male sexual enhancer capacity was evaluated by the in vitro inhibitory capacity of this traditional preparation towards the enzyme phosphodiesterase-5. 2. Results and Discussion 2.1. CCC Isolation of the Main Compounds from Ysypó Hû The TLC analysis of the crude drug extracts (Table1 and Figure2) showed that the main compounds were UV inactive and were visualized only after spraying with p-anisaldehyde/sulfuric acid and heating. The semi-purified fractions 8–15 from the Sephadex of the stem extract were worked up to obtain the main compounds using counter-current chromatography
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