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1 an Integrated Approach for the Valorization of Mango Seed Kernel: Efficient Extraction

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1 an Integrated Approach for the Valorization of Mango Seed Kernel: Efficient Extraction 1 An integrated approach for the valorization of mango seed kernel: efficient extraction 2 solvent selection, phytochemical profiling and antiproliferative activity assessment. 3 4 Diego Ballesteros-Vivas1,2a, Gerardo Alvarez-Rivera2a, Sandra Johanna Morantes Medina3 5 Andrea del Pilar Sánchez Camargo1, Elena Ibánez2, Fabián Parada-Alfonso1, Alejandro 6 Cifuentes2* 7 8 1 High Pressure Laboratory, Department of Chemistry, Faculty of Science, Universidad 9 Nacional de Colombia, Carrera 30 #45-03, Bogotá D.C., 111321, Colombia. 10 2 Laboratory of Foodomics, Institute of Food Science Research, CIAL, CSIC, Nicolás Cabrera 11 9, 28049 Madrid, Spain. 12 3 Unit of Basic Oral Investigation (UIBO), School of Dentistry, Universidad El Bosque, Av. 13 Carrera 9 #131 A-02, Bogotá D.C., 110121, Colombia. 14 15 a These two authors contributed equally to this work. 16 17 *Corresponding author: 18 Prof. Dr. Alejandro Cifuentes, Laboratory of Foodomics, Institute of Food Science Research, 19 CIAL (CSIC), Nicolás Cabrera 9, 28049 Madrid, Spain, e-mail: [email protected], Tel.: +34 20 910017955; fax: +34 910017905. 21 22 Keywords: 23 Mangifera indica L.; fruit by-products; Hansen solubility parameters; Pressurized-liquid 24 extraction; LC-Q-TOF; GC-Q-TOF; High-resolution mass spectrometry; antiproliferative 25 activity; HT-29 cell line; CCD-18Co cell line. 26 1 27 ABSTRACT 28 A novel valorization strategy is proposed in this work for the sustainable utilization of a major 29 mango processing waste (i.e. mango seed kernel, MSK), integrating green pressurized-liquid 30 extraction (PLE), bioactive assays and comprehensive HRMS-based phytochemical 31 characterization to obtain bioactive-rich fractions with high antioxidant capacity and 32 antiproliferative activity against human colon cancer cells. Thus, a two steps PLE procedure 33 was proposed to recover first the non-polar fraction (fatty acids and lipids) and second the polar 34 fraction (polyphenols). Efficient selection of the most suitable solvent for the second PLE step 35 (ethanol/ethyl acetate mixture) was based on the Hansen solubility parameters (HSP) approach. 36 A comprehensive GC- and LC-Q-TOF-MS/MS profiling analysis allowed the complete 37 characterization of the lipidic and phenolic fractions obtained under optimal condition (100% 38 EtOH at 150°C), demonstrating the abundance of oleic and stearic acids, as well as bioactive 39 xanthones, phenolic acids, flavonoids, gallate derivatives and gallotannins. The obtained MSK- 40 extract exhibited higher antiproliferative activity against human colon adenocarcinoma cell line 41 HT-29 compared to traditional extraction procedures described in literature for MSK utilization 42 (e.g. Soxhlet), demonstrating the great potential of the proposed valorization strategy as a 43 valuable opportunity for mango processing industry to deliver a value-added product to the 44 market with health promoting properties. 45 46 47 48 49 50 51 2 52 1. INTRODUCTION 53 Mango (Mangifera indica L.) is one of the most important tropical fruit crops, with an annual 54 production of more than 38 million tonnes (Mitra, 2016). The commercial importance of mango 55 fruit is due, among other reasons, to its sensorial quality attributes, high nutritional value and 56 functional compounds content (Ediriweera, Tennekoon, & Samarakoon, 2017; Gentile et al., 57 2019; Ribeiro & Schieber, 2010). Colombia plays an increasing role in world mango 58 production with cultivars such as ‘Sugar mango’, recognized by its sensorial qualities 59 (Corrales-Bernal, Maldonado, Urango, Franco, & Rojano, 2014). The industrial mango 60 processing generates about 40–60% of fruit wastes (12–15% of peels and 15–20% of kernels 61 seeds); none of them currently used for commercial purposes (Nawab, Alam, Haq, & Hasnain, 62 2016). Recently, several researches about the chemical composition and bioactive potential of 63 mango seed kernel (MSK) have been reviewed (Jahurul et al., 2015; Torres-León et al., 2016). 64 MSK contains important families of health-promoting compounds including fatty acids and 65 triacylglycerols (Lieb et al., 2018), gallotanins (Luo et al., 2014), xanthones (e.g. mangiferin) 66 (Barreto et al., 2008), flavonoids and phenolic acids, among others (Dorta, González, Lobo, 67 Sánchez-Moreno, & de Ancos, 2014; Lopez-Cobo et al., 2017). Polyphenolic compounds from 68 mango have been reported to have a strong antioxidant activity (Barreto et al., 2008; Soong & 69 Barlow, 2006; Sultana, Hussain, Asif, & Munir, 2012), and exhibit bioactivity in cancer cell 70 line models, including breast, liver, leukemia, cervix, prostate, lung and colon (Abdullah, 71 Mohammed, Rasedee, & Mirghani, 2015; Abdullah, Mohammed, Rasedee, Mirghani, & Al- 72 Qubaisi, 2015; Luo et al., 2014; Timsina & Nadumane, 2015). In particular, mangiferin (2-β- 73 D-glucopyranosyl-1,3,6,7-tetrahydroxy-9H-xanthen-9-one) has been reported as one of the 74 most bioactive phytochemicals in mango; in both in vitro and in vivo models (Imran et al., 75 2017). 3 76 Considering the bioactive potential of MSK, the development of green valorization strategies 77 to obtain polyphenolic-rich extracts from this valuable biowaste, pose a great challenge and a 78 unique opportunity for mango processing industry to deliver a value-added product to the 79 market with health promoting properties. Thus, strategies based on efficient extraction solvent 80 selection and use of new green extraction processes can help fulfilling the goals of the green 81 extraction of natural products (Chemat, Vian, & Cravotto, 2012). Hansen solubility parameters 82 (HSP) was shown to be a useful predictive model to ascertain the solubility of solutes, such as 83 secondary metabolites, in different solvents through their affinity and miscibility estimation. 84 In terms of new green extraction processes, Pressurized Liquid Extraction (PLE) is a 85 recognized environmentally friendly technique due to its higher extraction efficiency, lower 86 solvent consumption, short extraction time and the possibility of using green solvents (Ameer, 87 Shahbaz, & Kwon, 2017; Herrero, Castro-Puyana, Mendiola, & Ibañez, 2013). Several 88 research works have been conducted employing the joint strategy involving HSP+PLE to 89 target bioactive compounds recovery from natural sources (Ballesteros-Vivas et al., 2019; 90 Damergi et al., 2017; Sánchez-Camargo et al., 2017; Srinivas, King, Monrad, Howard, & 91 Hansen, 2009). 92 In this context, the present research aimed to develop an integrated valorization strategy, 93 involving HSP approach and sequential PLE procedure, in vitro antioxidant assays and 94 comprehensive characterization with advanced analytical techniques (liquid chromatography 95 and gas chromatography coupled to high resolution mass spectrometry) to obtain mangiferin 96 and other phenolic compounds from ‘sugar MSK’ with selective antiproliferative activity 97 against human colon adenocarcinoma cell line HT-29. An integrated process scheme of the 98 proposed MSK valorization strategy is shown in Figure 1. 99 100 4 101 2. MATERIAL AND METHODS 102 2.1 Samples and reagents 103 Sugar mango fruits were purchased from a local market in Bogotá D.C., Colombia in February 104 2018. Mango fruit by-products were obtained after mechanical pulping process. Seeds were 105 split into coat and kernel (endosperm). ‘Sugar MSK’ (5.3% moisture content) was dried at 106 room temperature in the darkness during 48 h, subsequently ground to fine powder and stored 107 at -20 °C until its use. 108 Gallic acid, quercetin, trolox, 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS), 109 2,2-diphenyl-1-picrylhydrazyl (DPPH), 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium 110 bromide (MTT), RPMI-1640 cell culture medium, streptomycin (0.1 mg/mL), penicillin (100 111 U/mL) potassium acetate, ammonium acetate, sodium carbonate, formic acid, potassium 112 persulfate, aluminum chloride, were purchased from Sigma-Aldrich (Madrid, Spain). Fetal 113 bovine serum (Gibco) and 0.05% trypsin-EDTA (Gibco) were purchased from Thermo Fisher 114 Scientific (Rockford, IL). Merck (Darmstadt, Germany) provided the Folin-Ciocalteu phenol 115 reagent. Solvents employed were HPLC-grade. Acetonitrile, chloroform, ethanol and methanol 116 were acquired from VWR Chemicals (Barcelona, Spain), whereas ethyl acetate by Scharlau 117 (Barcelona, Spain). Ultrapure water was obtained from a Millipore system (Billerica, MA, 118 USA). For the UPLC-q-TOF-MS analyses, MS grade ACN and water from LabScan (Dublin, 119 Ireland) were employed. 120 121 2.2 Hansen Solubility Parameters estimation 122 HSP for mangiferin and green solvents, including ethanol, ethyl acetate, ethyl lactate and (+)- 123 limonene, were estimated using HSPiP® software v 5.0 at normal conditions, following the 124 methodology previously reported by Sánchez-Camargo et al (Sánchez-Camargo et al., 2017). 125 Briefly, the SMILES (Simplified molecular input line syntax) of mangiferin 5 126 [C1=C2C(=CC(=C1O)O)OC3=CC(=C(C(=C3C2=O)O)C4C(C(C(C(O4)CO)O)O)O)O] was 127 break into corresponding functional groups using Yamamoto-molecular break (Y-MB) method 128 and then HSP parameters were estimated by “Do It Yourself” tool. Subsequently, the affinity 129 between the mangiferin and the green solvents was measured by Ra or “distance” term using 130 their HSPs values through “Solvent optimizer” tool (the smaller Ra corresponding to the greater 131 affinity between solvent and solute). The variation of Ra at different temperatures (25-150 °C) 132 was also
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