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UHPLC-MS Chemical Fingerprinting and Antioxidant, Antiproliferative, and Enzyme Inhibition Potential of Gaultheria Pumila Berries

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UHPLC-MS Chemical Fingerprinting and Antioxidant, Antiproliferative, and Enzyme Inhibition Potential of Gaultheria Pumila Berries H OH metabolites OH Article UHPLC-MS Chemical Fingerprinting and Antioxidant, Antiproliferative, and Enzyme Inhibition Potential of Gaultheria pumila Berries Carlos Fernández-Galleguillos 1, Luisa Quesada-Romero 2,*, Adrián Puerta 3, José M. Padrón 3 , Ernane Souza 4, Javier Romero-Parra 5 and Mario J. Simirgiotis 1,6,* 1 Instituto de Farmacia, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, Valdivia 5090000, Chile; [email protected] 2 Facultad de Ciencias Para el Cuidado de la Salud, Universidad San Sebastián, Valdivia 5090000, Chile 3 BioLab, Instituto Universitario de Bio-Orgánica Antonio González (IUBO-AG), Universidad de La Laguna, 38206 La Laguna, Spain; [email protected] (A.P.); [email protected] (J.M.P.) 4 The Lloyd L. Gregory School of Pharmacy, Palm Beach Atlantic University, West Palm Beach, FL 33401, USA; [email protected] 5 Departamento de Química Orgánica y Fisicoquímica, Facultad de Ciencias Químicas y Farmacéuticas, Universidad de Chile, Olivos 1007, Casilla 233, Santiago 6640022, Chile; [email protected] 6 Center for Interdisciplinary Studies on the Nervous System (CISNe), Universidad Austral de Chile, Valdivia 5090000, Chile * Correspondence: [email protected] (L.Q.-R.); [email protected] (M.J.S.); Tel.: +56-632632811 (L.Q.-R.) Citation: Fernández-Galleguillos, C.; Quesada-Romero, L.; Puerta, A.; Abstract: Gaultheria pumila (Ericaceae) (known as Chaura or Mutilla) is a Chilean native small Padrón, J.M.; Souza, E.; shrub that produces berry fruits consumed by local Mapuche people. In this study, the chemical Romero-Parra, J.; Simirgiotis, M.J. fingerprinting and antioxidant, enzyme inhibition, and antiproliferative activities of the berries UHPLC-MS Chemical Fingerprinting were investigated for the first time. Thirty-six metabolites were identified in the fruits by ultra-high and Antioxidant, Antiproliferative, performance liquid chromatography-photodiode array detection, hyphenated with Orbitrap mass and Enzyme Inhibition Potential of spectrometry analysis (UHPLC-DAD-Orbitrap-MS). Metabolites, included anthocyanins, pheno- Gaultheria pumila Berries. Metabolites lic acids, flavonoids, iridoids, diterpenes, and fatty acids. Moderate inhibitory activities against 2021, 11, 523. https://doi.org/ acetylcholinesterase (7.7 ± 0.3 µg/mL), butyrylcholinesterase (34.5 ± 0.5 µg/mL), and tyrosinase 10.3390/metabo11080523 (3.3 ± 0.2 µg/mL) enzymes were found. Moreover, selected major compounds were subjected to docking assays in light of their experimental inhibition. Results indicated that hydrogen bonding, Academic Editor: Hirokazu π π Gaultheria pumila Kawagishi – interaction, and a salt bridge interaction contributed significantly. berries showed a total phenolic content of 189.2 ± 0.2 mg of gallic acid equivalents/g, total flavonoid content Received: 19 July 2021 of 51.8 ± 0.1 mg quercetin equivalents/g, and total anthocyanin content of 47.3 ± 0.2 mg of cianydin- Accepted: 3 August 2021 3-glucoside equivalents/g. Antioxidant activity was assessed using DPPH (92.8 ± 0.1 µg/mL), FRAP Published: 7 August 2021 (134.1 ± 0.1 µmol Trolox equivalents/g), and ORAC (4251.6 ± 16.9 µmol Trolox equivalents/g) assays. Conversely, Gaultheria pumila showed a scarce antiproliferative potential against several Publisher’s Note: MDPI stays neutral solid human cancer cells. Our findings suggest that Gaultheria pumila berries have several bioactive with regard to jurisdictional claims in metabolites with inhibitory effects against acetylcholinesterase, butyrylcholinesterase, and tyrosinase, published maps and institutional affil- and have the potential for use in food supplements. iations. Keywords: gaultheria; phenolics; enzyme inhibition; native berries; antioxidant Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. 1. Introduction This article is an open access article The human consumption of native berries has been increasing worldwide in part due distributed under the terms and to their potential impact on health promotion and disease prevention. Fruit berries from conditions of the Creative Commons a variety of species have been associated with a reduction in the risk of cardiovascular, Attribution (CC BY) license (https:// neurodegenerative, and inflammatory diseases, as well as potential benefits against some creativecommons.org/licenses/by/ forms of cancer [1]. The effects against reactive oxygen species (ROS) have been described 4.0/). Metabolites 2021, 11, 523. https://doi.org/10.3390/metabo11080523 https://www.mdpi.com/journal/metabolites Metabolites 2021, 11, x 2 of 23 Metabolites 2021, 11, 523 2 of 22 forms of cancer [1]. The effects against reactive oxygen species (ROS) have been described asas the the main main antioxidant antioxidant protective protective mechanism mechanism [2]. [2]. Chile Chile possesses possesses a a high high biodiversity biodiversity of of nativenative berries, berries, which which are are mainly mainly found found in in the the central-southern central-southern region region of of the the country country and and includeinclude different different genuses genuses such such as as AristoteliaAristotelia,, FragariaFragaria,, BerberisBerberis,, UgniUgni,, and and GaultheriaGaultheria,, among among others.others. The The phytochemical phytochemical and and biological biological activi activitiesties of of plants plants belonging belonging to to those those genuses genuses havehave been been reported reported previously previously [3]. [3]. TheThe GaultheriaGaultheria genusgenus (Ericaceae) (Ericaceae) includes includes approximately approximately 135 135 species, species, many many of of which which havehave been been used used in in traditional traditional medicine medicine to to trea treatt several several diseases diseases [4]. [4]. Some Some of of their their chemical chemical constituentsconstituents and and pharmacological pharmacological properties properties ha haveve been been extensively extensively investigated investigated [5]. [5]. An- An- tioxidant,tioxidant, antibacterial, antibacterial, anti-inflammatory, anti-inflammatory, anticancer, anticancer, and and enzyme enzyme inhibitory inhibitory properties properties havehave been been reported reported in in the the scientific scientific literature literature [6–9]. [6–9]. In In Chile, Chile, the the genus genus GaultheriaGaultheria isis dis- dis- tributedtributed from from the the central central region region (Región (Región Metr Metropolitana)opolitana) to to the the extreme extreme south south (Región (Región de de Magallanes),Magallanes), and and twelve twelve species species have have been been formally formally registered registered including including G.G. angustifolia angustifolia, , G.G. antarctica antarctica,, G.G. cespitosa cespitosa,, G.G. insana insana,, G.G. mucronata mucronata, ,G.G. nubigena nubigena, ,G.G. phyllireifolia phyllireifolia, ,G.G. poeppigii poeppigii, , G.G. tenuifolia tenuifolia, ,G.G. renjifoana renjifoana,, G.G. racemulosa racemulosa,, andand G. G. pumila pumila [10].[10]. Some Some of of these these plants plants are are edible edible speciesspecies ( (G.G. tenuifolia tenuifolia, ,G.G. phillyreifolia phillyreifolia,, G.G. poeppigii poeppigii,, G.G. mucronata mucronata,, and and G.G. pumila pumila).). AnthocyaninsAnthocyanins and and iridoids iridoids with with important important antioxidant antioxidant activities activities have have been been isolated isolated fromfrom the the native native berries berries of of G.G. phillyreifolia phillyreifolia andand G.G. poeppigii poeppigii [11].[11]. The The quantitative quantitative and and quali- qual- tativeitative profiles profiles of of phenolic phenolic compounds compounds from from different different colored colored genotypes genotypes of of G.G. poeppigii poeppigii berriesberries and and their antioxidants activitiesactivities havehave been been evaluated evaluated [12 [12].]. Anthocyanins, Anthocyanins, proantho- proan- thocyanidins,cyanidins, phenylpropanoids, phenylpropanoids, iridoids, iridoids, and and flavonols flavonols have have been been isolated isolated from fromG. tenuifoliaG. tenu- ifoliaberries berries [13]. [13]. The anthocyaninThe anthocyanin profiles, profiles, total tota anthocyaninl anthocyanin content, content, and antioxidant and antioxidant activities ac- tivitiesfrom G. from mucronata G. mucronataand G. antarcticaand G. antarcticahave also have been also described been described [14], as well [14], as as the well flavonols as the flavonolsand hydroxycinnamic and hydroxycinnamic acid profiles acid [15 profiles]. In addition, [15]. In addition, morphometric morphometric analysis and analysis the chemi- and thecal characterizationchemical characterization (total anthocyanin (total anthocyanin content and content pectin) ofand red, pectin) pink,and of red, white pink,G. pumila and whiteberries G. have pumila been berries investigated have been [16 investigated]. [16]. GaultheriaGaultheria pumila pumila isis a a native native small small bush bush (2–3 (2–3 cm cm tall) tall) that that produces produces a a tasty, tasty, aromatic, aromatic, andand flavored flavored fruit fruit popularly popularly known known as as “Chaur “Chaura”a” or or “Mutilla” “Mutilla” and and is is consumed consumed by by local local MapucheMapuche communities communities (Figure (Figure 1).1). FigureFigure 1. 1. GaultheriaGaultheria pumila pumila (Ericaceae)(Ericaceae) shrub shrub in inParque Parque Nacional Nacional Conguillío Conguill (left)ío (left and) andGaultheriaGaultheria pu- milapumila berriesberries
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