Black Bean (Phaseolus vulgaris L.) Polyphenolic Extract Exerts Antioxidant and Antiaging Potential
Abstract
:1. Introduction
2. Results
2.1. Conventional Leaching and SFE Extraction
2.2. Tentative Dentification of Phenolic Compounds by ESI-QTOF
2.3. Antioxidant Capacity
2.4. Tyrosinase Inhibitory Potential
2.5. Elastase Inhibitory Potential
2.6. Molecular Docking (In Silico Assay)
3. Discussion
4. Materials and Methods
4.1. Materials
4.2. Conventional Leaching Extraction
4.3. Supercritical CO2 Fluids Extraction
4.4. Determination of Total Phenolic Compounds
4.5. Determination of Total Anthocyanins
4.6. Phenolic Compounds Purification
4.7. Identification of Phenolic Compounds by ESI-QTOF
4.8. ABTS Assay
4.9. DPPH Assay
4.10. Tyrosinase Inhibition Assay
4.11. Elastase Inhibition Assay
4.12. Molecular Docking (In Silico Analysis)
4.13. Statistical Analysis
5. Conclusions
6. Patents
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kim, D.U.; Chung, H.C.; Kim, C.; Hwang, J.K. Oral Intake of Boesenbergia Pandurata Extract Improves Skin Hydration, Gloss, and Wrinkling: A Randomized, Double-Blind, and Placebo-Controlled Study. J. Cosmet. Dermatol. 2017, 16, 512–519. [Google Scholar] [CrossRef] [PubMed]
- Xiong, Z.-M.; O’Donovan, M.; Sun, L.; Choi, J.Y.; Ren, M.; Cao, K. Anti-Aging Potentials of Methylene Blue for Human Skin Longevity. Sci. Rep. 2017, 7, 1–12. [Google Scholar] [CrossRef]
- Cho, Y.H.; Bahuguna, A.; Kim, H.H.; Kim, D.; Kim, H.J.; Yu, J.M.; Jung, H.G.; Jang, J.Y.; Kwak, J.H.; Park, G.H.; et al. Potential Effect of Compounds Isolated from Coffea Arabica against UV-B Induced Skin Damage by Protecting Fibroblast Cells. J. Photochem. Photobiol. B Biol. 2017, 174, 323–332. [Google Scholar] [CrossRef] [PubMed]
- Hernandez, D.F.; Cervantes, E.L.; Diego, A.; Luna-Vital, L.M. Food-Derived Bioactive Compounds with Anti-Aging Potential for Nutricosmetic and Cosmeceutical Products. Crit. Rev. Food Sci. Nutr. 2020, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Wittenauer, J.; MäcKle, S.; Sußmann, D.; Schweiggert-Weisz, U.; Carle, R. Inhibitory Effects of Polyphenols from Grape Pomace Extract on Collagenase and Elastase Activity. Fitoterapia 2015, 101, 179–187. [Google Scholar] [CrossRef]
- Şöhretoğlu, D.; Sari, S.; Barut, B.; Özel, A. Tyrosinase Inhibition by Some Flavonoids: Inhibitory Activity, Mechanism by in Vitro and in Silico Studies. Bioorg. Chem. 2018, 81, 168–174. [Google Scholar] [CrossRef]
- Chiocchio, I.; Mandrone, M.; Sanna, C.; Maxia, A.; Tacchini, M.; Poli, F. Screening of a Hundred Plant Extracts as Tyrosinase and Elastase Inhibitors, Two Enzymatic Targets of Cosmetic Interest. Ind. Crops Prod. 2018, 122, 498–505. [Google Scholar] [CrossRef]
- Quideau, S.; Deffieux, D.; Douat-casassus, C.; Pouysegu, L. Natural Products Plant Polyphenols: Chemical Properties, Biological Activities, and Synthesis. Angew. Chem. 2011, 50, 586–621. [Google Scholar] [CrossRef]
- Mojica, L.; Meyer, A.; Berhow, M.A.; de Mejía, E.G. Bean Cultivars (Phaseolus Vulgaris L.) Have Similar High Antioxidant Capacity, in Vitro Inhibition of α-Amylase and α-Glucosidase While Diverse Phenolic Composition and Concentration. Food Res. Int. 2015, 69, 38–48. [Google Scholar] [CrossRef]
- Hu, S.; Zhang, X.; Chen, F.; Wang, M. Dietary Polyphenols as Photoprotective Agents against UV Radiation. J. Funct. Foods 2017, 30, 108–118. [Google Scholar] [CrossRef]
- Molino, A.; Mehariya, S.; Di, G.; Larocca, V.; Martino, M.; Paolo, G.; Marino, T.; Chianese, S.; Balducchi, R.; Musmarra, D. Recent Developments in Supercritical Fluid Extraction of Bioactive Compounds from Microalgae: Role of Key Parameters, Technological Achievements and Challenges. J. CO2 Util. 2020, 36, 196–209. [Google Scholar] [CrossRef]
- Garcia-Vaquero, M.; Rajauria, G.; Tiwari, B. Conventional Extraction Techniques: Solvent Extraction; Elsevier Inc.: Amsterdam, The Netherlands, 2020; ISBN 9780128179437. [Google Scholar]
- Hsieh-Lo, M.; Castillo-Herrera, G.; Mojica, L. Black Bean Anthocyanin-Rich Extract from Supercritical and Pressurized Extraction Increased In Vitro Antidiabetic Potential, While Having Similar Storage Stability. Foods 2020, 9, 655. [Google Scholar] [CrossRef]
- del Garcia-Mendoza, M.P.; Espinosa-Pardo, F.A.; Baseggio, A.M.; Barbero, G.F.; Maróstica Junior, M.R.; Rostagno, M.A.; Martínez, J. Extraction of Phenolic Compounds and Anthocyanins from Juçara (Euterpe Edulis Mart.) Residues Using Pressurized Liquids and Supercritical Fluids. J. Supercrit. Fluids 2017, 119, 9–16. [Google Scholar] [CrossRef]
- Alcázar-Valle, M.; Lugo-Cervantes, E.; Mojica, L.; Morales-Hernández, N.; Reyes-Ramírez, H.; Enríquez-Vara, J.N.; García-Morales, S. Bioactive Compounds, Antioxidant Activity, and Antinutritional Content of Legumes: A Comparison between Four Phaseolus Species. Molecules 2020, 25, 3528. [Google Scholar] [CrossRef] [PubMed]
- Alfaro-Diaz, A.; Urías-Silvas, J.E.; Loarca-Piña, G.; Gaytan-Martínez, M.; Prado-Ramirez, R.; Mojica, L. Techno-Functional Properties of Thermally Treated Black Bean Protein Concentrate Generated through Ultrafiltration Process. LWT 2021, 136, 110296. [Google Scholar] [CrossRef]
- Escobedo, A.; Loarca-Piña, G.; Gaytan-Martínez, M.; Orozco-Avila, I.; Mojica, L. Autoclaving and Extrusion Improve the Functional Properties and Chemical Composition of Black Bean Carbohydrate Extracts. J. Food Sci. 2020, 85, 2783–2791. [Google Scholar] [CrossRef]
- Gross, J.H. Direct Analysis in Real Time-a Critical Review on DART-MS. Anal. Bioanal. Chem. 2014, 406, 63–80. [Google Scholar] [CrossRef]
- Carbas, B.; Machado, N.; Oppolzer, D.; Ferreira, L.; Queiroz, M.; Brites, C.; Rosa, E.A.S.; Barros, A.I.R.N.A. Nutrients, Antinutrients, Phenolic Composition, and Antioxidant Activity of Common Bean Cultivars and Their Potential for Food Applications. Antioxidants 2020, 9, 186. [Google Scholar] [CrossRef] [Green Version]
- Pratheeshkumar, P.; Son, Y.O.; Wang, X.; Divya, S.P.; Joseph, B.; Hitron, J.A.; Wang, L.; Kim, D.; Yin, Y.; Roy, R.V.; et al. Cyanidin-3-Glucoside Inhibits UVB-Induced Oxidative Damage and Inflammation by Regulating MAP Kinase and NF-ΚB Signaling Pathways in SKH-1 Hairless Mice Skin. Toxicol. Appl. Pharmacol. 2014, 280, 127–137. [Google Scholar] [CrossRef] [Green Version]
- Luthria, D.L.; Pastor-Corrales, M.A. Phenolic Acids Content of Fifteen Dry Edible Bean (Phaseolus vulgaris L.) Varieties. J. Food Compos. Anal. 2006, 19, 205–211. [Google Scholar] [CrossRef]
- Mojica, L.; Berhow, M.; Gonzalez de Mejia, E. Black Bean Anthocyanin-Rich Extracts as Food Colorants: Physicochemical Stability and Antidiabetes Potential. Food Chem. 2017, 229, 628–639. [Google Scholar] [CrossRef]
- Yang, Q.; Gan, R.; Ge, Y.; Zhang, D.; Corke, H. Polyphenols in Common Beans (Phaseolus vulgaris L.): Chemistry, Analysis, and Factors Affecting Composition. Compr. Rev. Food Sci. Food Saf. 2018, 1–22. [Google Scholar] [CrossRef] [Green Version]
- Jiao, X.; Zhang, X.; Zhang, Q.; Gao, N.; Li, B.; Meng, X. Optimation of Enrichment and Purification of Polyphenols from Blueberries (Vaccinium Spp.) by Macroporous Resins XAD-7HP. Emirates J. Food Agric. 2017, 29, 581–588. [Google Scholar] [CrossRef] [Green Version]
- Mat Saad, H.; Tan, C.H.; Lim, S.H.; Manickam, S.; Sim, K.S. Evaluation of Anti-Melanogenesis and Free Radical Scavenging Activities of Five Artocarpus Species for Cosmeceutical Applications. Ind. Crops Prod. 2021, 161, 113184. [Google Scholar] [CrossRef]
- Rittié, L.; Fisher, G.J. Natural and Sun-Induced Aging of Human Skin. Cold Spring Harb. Perspect. Med. 2015, 5, 18–26. [Google Scholar] [CrossRef] [PubMed]
- Jabłońska-Trypuć, A.; Matejczyk, M.; Rosochacki, S. Matrix Metalloproteinases (MMPs), the Main Extracellular Matrix (ECM) Enzymes in Collagen Degradation, as a Target for Anticancer Drugs. J. Enzym. Inhib. Med. Chem. 2016, 31, 177–183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kusumawati, I.; Indrayanto, G. Natural Antioxidants in Cosmetics, 1st ed.; Elsevier B.V.: Amsterdam, The Netherlands, 2013; Volume 40, ISBN 9780444596031. [Google Scholar]
- Burger, P.; Landreau, A.; Azoulay, S.; Michel, T.; Fernandez, X. Skin Whitening Cosmetics: Feedback and Challenges in the Development of Natural Skin Lighteners. Cosmetics 2016, 3, 36. [Google Scholar] [CrossRef] [Green Version]
- Mukherjee, P.K.; Biswas, R.; Sharma, A.; Banerjee, S.; Biswas, S.; Katiyar, C.K. Validation of Medicinal Herbs for Anti-Tyrosinase Potential. J. Herb. Med. 2018. [Google Scholar] [CrossRef]
- Ersoy, E.; Eroglu Ozkan, E.; Boga, M.; Yilmaz, M.A.; Mat, A. Anti-Aging Potential and Anti-Tyrosinase Activity of Three Hypericum Species with Focus on Phytochemical Composition by LC–MS/MS. Ind. Crops Prod. 2019, 141. [Google Scholar] [CrossRef]
- Athipornchai, A.; Jullapo, N. Tyrosinase Inhibitory and Antioxidant Activities of Orchid (Dendrobium Spp.). S. Afr. J. Bot. 2018, 119, 188–192. [Google Scholar] [CrossRef]
- Abdul Karim, A.; Azlan, A.; Ismail, A.; Hashim, P.; Abd Gani, S.S.; Zainudin, B.H.; Abdullah, N.A. Phenolic Composition, Antioxidant, Anti-Wrinkles and Tyrosinase Inhibitory Activities of Cocoa Pod Extract. BMC Complementary Altern. Med. 2014, 14, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.; Lee, W.W.; Cui, Y.R.; Ahn, G.; Jeon, Y.J. Protective Effect of Green Tea Catechin against Urban Fine Dust Particle-Induced Skin Aging by Regulation of NF-ΚB, AP-1, and MAPKs Signaling Pathways. Environ. Pollut. 2019, 252, 1318–1324. [Google Scholar] [CrossRef] [PubMed]
- Pientaweeratch, S.; Panapisal, V.; Tansirikongkol, A. Antioxidant, Anti-Collagenase and Anti-Elastase Activities of Phyllanthus Emblica, Manilkara Zapota and Silymarin: An in Vitro Comparative Study for Anti-Aging Applications. Pharm. Biol. 2016, 54, 1865–1872. [Google Scholar] [CrossRef] [Green Version]
- Eun Lee, K.; Bharadwaj, S.; Yadava, U.; Gu Kang, S. Evaluation of Caffeine as Inhibitor against Collagenase, Elastase and Tyrosinase Using in Silico and in Vitro Approach. J. Enzym. Inhib. Med. Chem. 2019, 34, 927–936. [Google Scholar] [CrossRef] [Green Version]
- Johnson, M.H.; De Mejia, E.G.; Fan, J.; Lila, M.A.; Yousef, G.G. Anthocyanins and Proanthocyanidins from Blueberry-Blackberry Fermented Beverages Inhibit Markers of Inflammation in Macrophages and Carbohydrate-Utilizing Enzymes in Vitro. Mol. Nutr. Food Res. 2013, 57, 1182–1197. [Google Scholar] [CrossRef]
- Nenadis, N.; Wang, L.F.; Tsimidou, M.; Zhang, H.Y. Estimation of Scavenging Activity of Phenolic Compounds Using the ABTS + Assay. J. Agric. Food Chem. 2004, 52, 4669–4674. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, M.J.; Pereira, C.A.; Oliveira, M.; Neng, N.R.; Nogueira, J.M.F.; Zengin, G.; Mahomoodally, M.F.; Custódio, L. Sea Rose (Armeria Pungens (Link) Hoffmanns. & Link) as a Potential Source of Innovative Industrial Products for Anti-Ageing Applications. Ind. Crops Prod. 2018, 121, 250–257. [Google Scholar] [CrossRef]
- San Pablo-Osorio, B.; Mojica, L.; Urías-Silvas, J.E. Chia Seed (Salvia hispanica L.) Pepsin Hydrolysates Inhibit Angiotensin-Converting Enzyme by Interacting with Its Catalytic Site. J. Food Sci. 2019, 84, 1170–1179. [Google Scholar] [CrossRef]
Extraction Method | Cosolvent | Total Phenolic Compounds (mg GAE/g Coat) | Anthocyanins (mg C3GE/g Coat) |
---|---|---|---|
SFE | H2O-100% | 63.77 ± 3.16 a | 6.76 ± 0.37 a |
SFE | H2O-EtOH 50% | 66.60 ± 7.41 a | 7.30 ± 0.64 a |
Leaching | H2O-100% | 44.04 ±1.39 b | 3.50 ± 0.35 b |
Leaching | H2O-EtOH 50% | 59.83 ± 4.86 a | 5.87 ± 0.21 c |
Sample | Tentative Identification | Elemental Formula Compound | Ion | m/z Experimental | m/z Theoretical | Tentative Error ppm |
---|---|---|---|---|---|---|
Leaching Crude Extract | Quercetin-3-D-Galactoside | C21H20O12 | [M-H]− | 463.1211 | 463.1211 * | 0 |
Malvidin-3-Glucoside | C23H25O12 | [M+H]+ | 331.0715 | 331.0641 * | −22.3 | |
Delphinidin 3-Glucoside | C21H20O12 | [M+H]+ | 303.0402 | 303.0402 * | 0 | |
Cyanidin 3-Glucoside | C21H21O11+ | [M-H]− | 447.1285 | 447.1242 * | −9.61 | |
Petunidin-3-O-β-Glucoside | C22H23O12 | [M-H]− | 447.1285 | 447.1033 | - | |
Gallic acid | C7H6O5 | [M-H]− | 169.0686 | 169.0606 | - | |
Sinapic acid | C11H12O5 | [M-H]− | 223.0993 | 223.0607 | - | |
Genistein | C15H10O5 | [M-H]− | 269.021 | 269.0455 | - | |
Protocatechuic acid | C7H6O4 | [M-H]− | 153.0649 | 153.0188 | - | |
Rutin | C27H30O16 | [M-H]− | 609.1525 | 609.1461 | - | |
Naringenin | C15H12O5 | [M-H]− | 271.0737 | 271.0612 | - | |
Catechin | C15H14O6 | [M-H]− | 289.1219 | 289.0712 | - | |
Glycitein | C16H12O5 | [M+H]+ | 285.0356 | 285.0749 | - | |
Myricetin | C15H10O8 | [M-H]− | 317.0705 | 317.0303 | - | |
Ferulic acid | C10H10O4 | [M-H]− | 193.0635 | 193.0506 | - | |
Daidzin | C21H20O9 | [M-H]− | 415.09 | 415.1 | - | |
p-coumaric acid | C9H8O3 | [M-H]− | 163.1649 | 163.0395 | - | |
Caffeic acid | C15H10O4 | [M-H]− | 179.1075 | 179.0345 | - | |
Rosmarinic acid | C18H16O8 | [M-H]− | 359.1975 | 359.0767 | - | |
Leaching Pure Extract | Quercetin-3-D-Galactoside | C21H20O12 | [M-H]− | 463.1255 | 463.1211 * | −9.5 |
Malvidin-3-Glucoside | C23H25O12 | [M+H]+ | 331.0715 | 331.0641 * | −22.3 | |
Delphinidin 3-Glucoside | C21H20O12 | [M+H]+ | 303.0438 | 303.0402 * | −11.8 | |
Cyanidin 3-Glucoside | C21H21O11+ | [M-H]− | 447.1328 | 447.1242 * | −9.61 | |
Petunidin-3-O- β -Glucoside | C22H23O12 | [M-H]− | 447.1422 | 447.1033 | - | |
Gallic acid | C7H6O5 | [M-H]− | 169.0713 | 169.0606 | - | |
Protocatechuic acid | C7H6O4 | [M-H]− | 153.07 | 153.0188 | - | |
Rutin | C27H30O16 | [M-H]− | 609.1423 | 609.1461 | - | |
Naringenin | C15H12O5 | [M-H]− | 271.0737 | 271.0612 | - | |
Rosmarinic acid | C18H16O8 | [M-H]− | 359.2091 | 359.0767 | - | |
Catechin | C15H14O6 | [M-H]− | 289.1184 | 289.0712 | - | |
Glycitein | C16H12O5 | [M+H]+ | 285.0356 | 285.0749 | - | |
Myricetin | C15H10O8 | [M-H]− | 317.0823 | 317.0303 | - | |
Ferulic acid | C10H10O4 | [M-H]− | 193.1005 | 193.0506 | - | |
SFE Crude Extract | Quercetin-3-D-Galactoside | C21H20O12 | [M-H]− | 463.0462 | 463.0876 * | 89.4 |
Cyanidin 3-Glucoside | C21H21O11+ | [M-H]− | 447.0592 | 447.1242 * | 145.3 | |
Gallic acid | C7H6O5 | [M-H]− | 169.0207 | 169.0606 | - | |
Caffeic acid | C15H10O4 | [M-H]− | 179.0829 | 179.0345 | - | |
Daidzin | C21H20O9 | [M-H]− | 415.0513 | 415.1 | - | |
Sinapic acid | C11H12O5 | [M-H]− | 223.0014 | 223.0607 | - | |
Naringenin | C15H12O5 | [M-H]− | 271.0333 | 271.0612 | - | |
Rosmarinic acid | C18H16O8 | [M-H]− | 359.1432 | 359.0767 | - | |
Catechin | C15H14O6 | [M-H]− | 289.0766 | 289.0712 | - | |
Myricetin | C15H10O8 | [M-H]− | 317.0568 | 317.0303 | - | |
Ferulic acid | C10H10O4 | [M-H]− | 193.0436 | 193.0506 | - | |
SFE Pure Extract | Quercetin-3-D-Galactoside | C21H20O12 | [M-H]− | 463.0462 | 463.0872 * | 89.4 |
Cyanidin 3-Glucoside | C21H21O11+ | [M-H]− | 447.0679 | 447.1242 * | 125.9 | |
Gallic acid | C7H6O5 | [M-H]− | 169.0367 | 169.0606 | - | |
Caffeic acid | C15H10O4 | [M-H]− | 179.0801 | 179.0345 | - | |
Daidzin | C21H20O9 | [M-H]− | 415.06 | 415.1 | - | |
Sinapic acid | C11H12O5 | [M-H]− | 223.0443 | 223.0607 | - | |
Naringenin | C15H12O5 | [M-H]− | 271.0333 | 271.0612 | - | |
Rosmarinic acid | C18H16O8 | [M-H]− | 359.1432 | 359.0767 | - | |
Catechin | C15H14O6 | [M-H]− | 289.0662 | 289.0712 | - | |
Myricetin | C15H10O8 | [M-H]− | 317.0239 | 317.0303 | - | |
Ferulic acid | C10H10O4 | [M-H]− | 193.0721 | 193.0506 | - |
Phenolic Compounds Identified | Predicted Binding Affinity | |
---|---|---|
Tyrosinase (kcal/mol) | Elastase (kcal/mol) | |
Quercetin-3-D-Galactoside | −7.6 | −4.8 |
Malvidin-3-Glucoside | −7.8 | −5.5 |
Delphinidin-3-Glucoside | −7.1 | −5.8 |
Cyanidin-3-Glucoside | −7.7 | −3.4 |
Petunidin-3-O-β-Glucoside | −7.7 | −5.7 |
Gallic acid | −5.9 | −5.7 |
Sinapic acid | −5.9 | −4.7 |
Genistein | −6.9 | −5.6 |
Protocatechuic acid | −5.8 | −5.3 |
Rutin | −8.5 | −2.4 |
Naringenin | −6.8 | −6.7 |
Catechin | −6.8 | −6.9 |
Glycetin | −7.0 | −5.1 |
Myricetin | −6.9 | −6.5 |
Ferulic acid | −5.3 | −5.2 |
Daidzin | −6.6 | −4.2 |
p-coumaric acid | −5.5 | −5.0 |
Caffeic acid | −5.7 | −5.2 |
Rosmarinic acid | −5.9 | −6.8 |
Kojic acid | −5.5 | - |
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Fonseca-Hernández, D.; Lugo-Cervantes, E.D.C.; Escobedo-Reyes, A.; Mojica, L. Black Bean (Phaseolus vulgaris L.) Polyphenolic Extract Exerts Antioxidant and Antiaging Potential. Molecules 2021, 26, 6716. https://doi.org/10.3390/molecules26216716
Fonseca-Hernández D, Lugo-Cervantes EDC, Escobedo-Reyes A, Mojica L. Black Bean (Phaseolus vulgaris L.) Polyphenolic Extract Exerts Antioxidant and Antiaging Potential. Molecules. 2021; 26(21):6716. https://doi.org/10.3390/molecules26216716
Chicago/Turabian StyleFonseca-Hernández, David, Eugenia Del Carmen Lugo-Cervantes, Antonio Escobedo-Reyes, and Luis Mojica. 2021. "Black Bean (Phaseolus vulgaris L.) Polyphenolic Extract Exerts Antioxidant and Antiaging Potential" Molecules 26, no. 21: 6716. https://doi.org/10.3390/molecules26216716