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8-Oxo-9-Dihydromakomakine Isolated from Aristotelia Chilensis Induces Vasodilation in Rat Aorta: Role of the Extracellular Calcium Influx

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8-Oxo-9-Dihydromakomakine Isolated from Aristotelia Chilensis Induces Vasodilation in Rat Aorta: Role of the Extracellular Calcium Influx molecules Article 8-Oxo-9-Dihydromakomakine Isolated from Aristotelia chilensis Induces Vasodilation in Rat Aorta: Role of the Extracellular Calcium Influx Fredi Cifuentes 1, Javier Palacios 2,*, Adrián Paredes 3,4 , Chukwuemeka R. Nwokocha 5 and Cristian Paz 6,* 1 Laboratorio de Fisiología Experimental, Instituto Antofagasta, Universidad de Antofagasta, Antofagasta 1270300, Chile; [email protected] 2 Facultad Ciencias de la Salud, Instituto de EtnoFarmacología (IDE), Universidad Arturo Prat, Iquique 1110939, Chile 3 Laboratorio de Química Biológica, Instituto Antofagasta, Universidad de Antofagasta, Antofagasta 1270300, Chile; [email protected] 4 Departamento de Química, Facultad de Ciencias Básicas, Universidad de Antofagasta, Antofagasta 1270300, Chile 5 Department of Basic Medical Sciences Physiology Section, Faculty of Medical Sciences, The University of the West Indies, Mona, Kingston 7, KGN, Jamaica (W.I.); [email protected] 6 Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería, Universidad de La Frontera, Temuco 4780000, Chile * Correspondence: [email protected] (J.P.); [email protected] (C.P.); Tel.: +56-57-2526910 (J.P.); +56-45-2235424 (C.P.) Academic Editor: John C. D’Auria Received: 1 November 2018; Accepted: 17 November 2018; Published: 21 November 2018 Abstract: 8-Oxo-9-dihydromakomakine is a tetracyclic indole alkaloid extracted from leaves of the Chilean tree Aristotelia chilensis. The present study investigated the effects of this alkaloid on vascular response in tissues isolated from aortic segments obtained from normotensive rats. Our results showed that 8-oxo-9-dihydromakomakine induced a dose-dependent relaxation of aortic rings pre-contracted with phenylephrine (PE; 10−6 M). The vasorelaxation induced by 8-oxo-9-dihydromakomakine in rat aortic rings is independent of endothelium. The pre-incubation of aortic rings with 8-oxo-9-dehydromakomakine (10−4 M) significantly reduced the contractile response to KCl (p < 0.001) more than PE (p < 0.05). The highest dose of 8-oxo-9-dehydromakomakine (10−4 M) drastically reduced the contraction to KCl (6·10−2 M), but after that, PE (10−6 M) caused contraction (p < 0.05) in the same aortic rings. The addition of 8-oxo-9-dihydromakomakine (10−5 M) decreased the contractile response to tetraethylammonium (a voltage-dependent potassium channels blocker; −3 TEA; 5 × 10 M; p < 0.01) and BaCl2 (a non-selective inward rectifier potassium channel blocker; 5 × 10−3 M; p < 0.001) in rat aorta. 8-oxo-9-dihydromakomakine (10−5 M) decreased the contractile response to PE in rat aorta in the presence or absence of ouabain (an inhibitor of Na,K-ATPase; 10−3 M; p < 0.05). These results could indicate that 8-oxo-9-dihydromakomakine partially reduces plasma membrane depolarization-induced contraction. In aortic rings depolarized by PE, 8-oxo-9-dihydromakomakine inhibited the contraction induced by the influx of extracellular Ca2+ in a Ca2+ free solution (p < 0.01). 8-oxo-9-dihydromakomakine reduced the contractile response to agonists of voltage-dependent calcium channels type L (Bay K6844; 10−8 M; p < 0.01), likely decreasing the influx of extracellular Ca2+ through the voltage-dependent calcium channels. This study provides the first qualitative analysis indicating that traditional folk medicine Aristotelia chilensis may be protective in the treatment of cardiovascular pathologies. Keywords: Aristotelia chilensis Molina Stuntz; vascular activity; endothelium-independent; indole alkaloid; 8-oxo-9-dihydromakomakine; voltage-dependent calcium channels Molecules 2018, 23, 3050; doi:10.3390/molecules23113050 www.mdpi.com/journal/molecules Molecules 2018, 23, x FOR PEER REVIEW 2 of 11 Keywords: Aristotelia chilensis Molina Stuntz; vascular activity; endothelium-independent; indole Moleculesalkaloid;2018 8-oxo-9-dihydromakomakine;, 23, 3050 voltage-dependent calcium channels 2 of 11 1. Introduction 1. Introduction Maqui (Aristotelia chilensis (Molina) Stuntz, Elaeocarpaceae) is a Chilean native tree sacred to the Aristotelia chilensis Elaeocarpaceae AraucanianMaqui ( people. Nowadays,(Molina) maqui Stuntz,fruits have aroused special) is a Chilean interest native due treeto their sacred beneficial to the Araucanianproperties people.for human Nowadays, health, maquisuch as fruits antioxid haveant, aroused cardioprotective, special interest anti-inflammatory, due to their beneficial and propertiesenzymatic for activities human [1–3]. health, These such asbioactivities antioxidant, could cardioprotective, be useful for anti-inflammatory,the treatment of vascular and enzymatic diseases activitiessuch as hypertension, [1–3]. These myocardial bioactivities ischemia, could be and useful cerebral for the infarction, treatment which of vascular have become diseases worldwide such as hypertension,epidemics in myocardialmodern society ischemia, [4]. and cerebral infarction, which have become worldwide epidemics in modernAristotelia society chilensis [4]. produce various active components including a high concentration of flavonoidsAristotelia in fruits chilensis [1,2].produce Chemical various analysis active have componentsreported that includingmaqui leaves a high consists concentration of non-iridoid of flavonoidsmonoterpene in fruits indole [1 ,2alkaloids]. Chemical and analysis polyphenolic have reported compounds that maqui[5,6]. It leaves is known consists that of several non-iridoid pure monoterpenecompounds indolefrom alkaloidsplants may and polyphenolicmodulate the compounds vascular [5response,,6]. It is knownand therefore that several act pure as compoundsantihypertensives. from plants In fact, may some modulate flavonoids the vascular (quercetin response, or myricetin) and therefore cause vasoconstriction act as antihypertensives. because In fact, some flavonoids (quercetin or myricetin) cause vasoconstriction because they activate Cav1.2 they activate Cav1.2 channel, while flavonols (kaempferol and galangin), a flavone (chrysin), and an channel, while flavonols (kaempferol and galangin), a flavone (chrysin), and an isoflavone (genistein) isoflavone (genistein) inhibit Cav3.1 channel by producing vasorelaxation [7]. In addition, galangin inhibit Cav3.1 channel by producing vasorelaxation [7]. In addition, galangin and chrysin can inhibit and chrysin can inhibit Cav1.2 channel [8]. Cav1.2However, channel [there8]. are a paucity of data and studies about the vascular response of alkaloids from A. chilensisHowever,. In thereorder areto have a paucity a more of comprehensive data and studies idea about of the the pharmacological vascular response activity of alkaloids of alkaloids from A.produced chilensis .by In A. order chilensis to have on athe more cardiovascular comprehensive system, idea the of the main pharmacological component of activityleaves of of maqui alkaloids was producedpurified and by A.chemically chilensis oncharacterized the cardiovascular by NMR system, spectroscopy the main as 8-oxo-9-dihydromakomakine. component of leaves of maqui Then, was purifiedits activity and was chemically determined characterized by the induction by NMR of spectroscopytension change as in 8-oxo-9-dihydromakomakine. vascular tissue isolated from Then,aortic itssegments activity wasobtained determined from normotensive by the induction rats. of The tension potential change mechanisms in vascular tissuewere isolatedevaluated from from aortic the segmentsendothelium obtained and nitric from oxide normotensive (NO) production, rats. The togeth potentialer with mechanisms the role of werecytosolic evaluated calcium, from and the its endotheliummodulation by and calcium nitric oxidechannels, (NO) pota production,ssium channels, together and with Na,K-ATPase. the role of cytosolic calcium, and its modulation by calcium channels, potassium channels, and Na,K-ATPase. 2. Results 2. Results 2.1.2.1. 8-Oxo-9-Dihydromakomakine8-Oxo-9-Dihydromakomakine Induced Induced Vasodilation Vasodilation in in Rat Rat Aorta Aorta 8-Oxo-9-dehydromakomakine8-Oxo-9-dehydromakomakine induced vascular vascular relaxation relaxation on on aortic aortic rings rings pre-contracted pre-contracted with −6 withPE (10 PE M). (10− 6In M).fact, In8-oxo-9-dehydromakomakine fact, 8-oxo-9-dehydromakomakine caused relaxation caused relaxationin intact aorta in intact and aortaendothelium-denuded and endothelium-denuded aorta (Figure aorta (Figure1A). 1A).This This result result was was confirmedconfirmed becausebecause −4 8-oxo-9-dehydromakomakine8-oxo-9-dehydromakomakine alsoalso producedproduced relaxationrelaxation inin aortic aortic rings rings pre-incubated pre-incubated with with 10 10−4 MM N!ω-nitro-L-arginine methyl ester (L-NAME) (Figure 1B). N -nitro-L-arginine methyl ester (L-NAME) (Figure1B). Figure 1. Vasorelaxation effect of 8-oxo-9-dihydromakomakine in intact (Endo) and Figure 1. Vasorelaxation effect of 8-oxo-9-dihydromakomakine in intact− (Endo) and denuded-endothelium (Endo-denuded) aortic rings (A), and in presence of 10 4 M L-NAME denuded-endothelium (Endo-denuded) aortic rings (A), and in presence of 10−4 M L-NAME in the in the intact aorta (B). Values are mean ± standard error of the mean of 6 experiments. Two-way intact aorta (B). Values are mean ± standard error of the mean of 6 experiments. Two-way ANOVA ANOVA followed by Bonferroni’s post-hoc test. followed by Bonferroni’s post-hoc test. MoleculesMolecules 20182018,,23 23,, 3050x FOR PEER REVIEW 33 ofof 1111 Molecules 2018, 23, x FOR PEER REVIEW 3 of 11 2.2. 8-Oxo-9-Dihydromakomakine Reduced the Contractile
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