Antioxidant Scavenging of the Superoxide Radical by Yerba Mate (Ilex paraguariensis) and Black Tea (Camellia sinensis) Plus Caffeic and Chlorogenic Acids, as Shown via DFT and Hydrodynamic Voltammetry
Abstract
:1. Introduction
2. Results and Discussion
2.1. DFT Scavenging of Superoxide via Caffeic Acid Catechol Moiety
2.2. DFT Scavenging of Superoxide via Chlorogenic Acid Catechol Moiety
2.3. DFT Scavenging of Superoxide via the Acidic Proton of Chlorogenic Acid
2.4. DFT Scavenging of Superoxide via the Acidic Proton of Caffeic Acid
2.5. Experimental Superoxide Measurement Using RRDE to Scavenge the Title Compounds
3. Materials and Methods
3.1. Materials for RRDE Solutions
3.2. Hydrodynamic Voltammetry (RRDE)
3.3. Computational Study
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Petrovska, B.B. Historical review of medicinal plants’ usage. Pharmacogn. Rev. 2012, 6, 1–5. [Google Scholar] [CrossRef]
- Food and Agriculture Organization of the United Nations. Tea: Commodity in Focus. Available online: https://www.fao.org/markets-and-trade/commodities/tea/en/ (accessed on 27 May 2024).
- Jiang, J.; Lu, G.; Wang, Q.; Wei, S. The analysis and identification of charred suspected tea remains unearthed from warring state period Tomb. Sci. Rep. 2021, 11, 16557. [Google Scholar] [CrossRef] [PubMed]
- Aaqil, M.; Peng, C.; Kamal, A.; Nawaz, T.; Zhang, F.; Gong, J. Tea harvesting and processing techniques and its effect on phytochemical profile and final quality of black tea: A review. Foods 2023, 12, 4467. [Google Scholar] [CrossRef] [PubMed]
- Munim Khan, M.R.; Islam, M.A.; Uddin, R.; Kalam, M.A.; Baishakh, N.N.; Barua, P.; Rahman Talukder, M.H.; Ahmad, I. Biochemical investigation of Bangladeshi black tea and their correlation to organoleptic quality evaluation. Heliyon 2023, 9, e16802. [Google Scholar] [CrossRef]
- Wang, S.; Qiu, Y.; Gan, R.Y.; Zhu, F. Chemical constituents and biological properties of Pu-erh tea. Food Res. Int. 2022, 154, 110899. [Google Scholar] [CrossRef] [PubMed]
- Gawron-Gzella, A.; Chanaj-Kaczmarek, J.; Cielecka-Piontek, J. Yerba mate a long but current history. Nutrients 2021, 13, 3706. [Google Scholar] [CrossRef]
- Liguori, I.; Russo, G.; Curcio, F.; Bulli, G.; Aran, L.; Della-Morte, D.; Gargiulo, G.; Testa, G.; Cacciatore, F.; Bonaduce, D.; et al. Oxidative stress, aging, and diseases. Clin. Interv. Aging 2018, 13, 757–772. [Google Scholar] [CrossRef]
- Anik, M.I.; Mahmud, N.; Masud, A.A.; Khan, M.I.; Islam, M.N.; Uddin, S.; Hossain, M.K. Role of reactive oxygen species in aging and age-related diseases: A review. ACS Appl. Bio Mater. 2022, 5, 4028–4054. [Google Scholar] [CrossRef]
- Wang, L.; Pan, X.; Jiang, L.; Chu, Y.; Gao, S.; Jiang, X.; Zhang, Y.; Chen, Y.; Luo, S.; Peng, C. the biological activity mechanism of chlorogenic acid and its applications in food industry: A review. Front. Nutr. 2022, 9, 943911. [Google Scholar] [CrossRef]
- Chen, H.; Yu, F.; Kang, J.; Li, Q.; Warusawitharana, H.K.; Li, B. Quality chemistry, physiological functions, and health benefits of organic acids from tea (Camellia sinensis). Molecules 2023, 28, 2339. [Google Scholar] [CrossRef]
- Espíndola, K.M.M.; Ferreira, R.G.; Narvaez, L.E.M.; Silva Rosario, A.C.R.; da Silva, A.H.M.; Silva, A.G.B.; Vieira, A.P.O.; Monteiro, M.C. Chemical and pharmacological aspects of caffeic acid and its activity in hepatocarcinoma. Front. Oncol. 2019, 9, 541. [Google Scholar] [CrossRef] [PubMed]
- Manivel, P.; Chen, X. Chlorogenic, Caffeic, and Ferulic Acids and Their Derivatives in Foods. In Handbook of Dietary Phytochemicals; Xiao, J., Sarker, S.D., Asakawa, Y., Eds.; Springer Nature: Singapore, 2021. [Google Scholar] [CrossRef]
- Del Rio, D.; Rodriguez-Mateos, A.; Spencer, J.P.E.; Tognolini, M.; Borges, G.; Crozier, A. Dietary (poly)phenolics in human health: Structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid. Redox Signal 2013, 18, 1818–1892. [Google Scholar] [CrossRef]
- Sova, M.; Saso, L. Natural sources, pharmacokinetics, biological activities and health benefits of hydroxycinnamic acids and their metabolites. Nutrients 2020, 12, 2190. [Google Scholar] [CrossRef] [PubMed]
- El-Seedi, H.R.; El-Said, A.M.A.; Khalifa, S.A.M.; Göransson, U.; Bohlin, L.; Borg-Karlson, A.-K.; Verpoorte, R. Biosynthesis, natural sources, dietary intake, pharmacokinetic properties, and biological activities of hydroxycinnamic acids. J. Agric. Food Chem. 2012, 60, 10877–10895. [Google Scholar] [CrossRef] [PubMed]
- Silva, H.; Lopes, N.M.F. Cardiovascular effects of caffeic acid and its derivatives: A comprehensive review. Front. Physiol. 2020, 11, 595516. [Google Scholar] [CrossRef] [PubMed]
- Silva, R.B.; Santos, N.; Martins, N.; Ferreira, D.; Barbosa, F.; Souza, V.O.; Kinoshita, Â.; Baffa, O.; Del-Bel, E.; Santos, A. Caffeic acid phenethyl ester protects against the dopaminergic neuronal loss induced by 6-hydroxydopamine in rats. Neuroscience 2013, 233, 86–94. [Google Scholar] [CrossRef]
- Saija, A.; Tomaino, A.; Lo Cascio, R.; Trombetta, D.; Proteggente, A.; De Pasquale, A.; Uccella, N.; Bonina, F. Ferulic and caffeic acids as potential protective agents against photooxidative skin damage. J. Sci. Food Agric. 1999, 79, 476–480. [Google Scholar] [CrossRef]
- Zielińska, D.; Zieliński, H.; Laparra-Llopis, J.M.; Szawara-Nowak, D.; Honke, J.; Giménez-Bastida, J.A. Caffeic acid modulates processes associated with intestinal inflammation. Nutrients 2021, 13, 554. [Google Scholar] [CrossRef]
- Wei, X.; Zhao, L.; Ma, Z.; Holtzman, D.M.; Yan, C.; Dodel, R.C.; Hampel, H.; Oertel, W.; Farlow, M.R.; Du, Y. Caffeic acid phenethyl ester prevents neonatal hypoxic-ischaemic brain injury. Brain 2004, 127, 2629–2635. [Google Scholar] [CrossRef]
- Cliford, M.N.; Johnston, K.L.; Knigh, S.; Kuhnert, N. Hierarchical scheme for LC-MSn identification of chlorogenic acids. J. Agric. Food Chem. 2003, 51, 2900–2911. [Google Scholar] [CrossRef]
- Clifford, M.N.; Ramirez-Martinez, J.R. Chlorogenic acids and purine alkaloids contents on mate (Ilex paraguariensis) leaf and beverage. Food Chem. 1990, 35, 13–21. [Google Scholar] [CrossRef]
- Filip, R.; Lotito, S.B.; Ferraro, G.; Fraga, C.G. Antioxidant activity of Ilex paraguariensis and related species. Nutr. Res. 2000, 20, 1437–1446. [Google Scholar] [CrossRef]
- Bastos, D.H.M.; Ishimotoa, E.Y.; Marques, M.O.M.; Ferri, A.F.; Torres, E.A.F.S. Essential oil and antioxidant activity of green mate and mate tea (Ilex paraguariensis) infusions. J. Food Compos. Anal. 2006, 19, 538–543. [Google Scholar] [CrossRef]
- Rząsa-Duran, E.; Kryczyk-Poprawa, A.; Drabicki, D.; Podkowa, A.; Sułkowska-Ziaja, K.; Szewczyk, A.; Kała, K.; Opoka, W.; Zięba, P.; Fidurski, M.; et al. Yerba mate as a source of elements and bioactive compounds with antioxidant activity. Antioxidants 2022, 11, 371. [Google Scholar] [CrossRef]
- Caruso, F.; Pedersen, J.Z.; Incerpi, S.; Belli, S.; Sakib, R.; Rossi, M. Interaction between Vitamins C and E when scavenging the superoxide radical shown by hydrodynamic voltammetry and DFT. Biophysica 2024, 4, 310–326. [Google Scholar] [CrossRef]
- Gugliucci, A. Antioxidant effects of Ilex paraguariensis: Induction of decreased oxidability of human LDL in vivo. Biochem. Biophys. Res. Commun. 1996, 224, 338–344. [Google Scholar] [CrossRef]
- Schinella, G.R.; Troiani, G.; Dávila, V.; Buschiazzo, P.M.; Tournier, H.A. Antioxidant effects of an aqueous extract of Ilex paraguariensis. Biochem. Biophys. Res. Commun. 2000, 269, 257–360. [Google Scholar] [CrossRef]
- Tan, H.P.; Ye, S.R.; Chen, L.; Zou, Y. Determination overview of organic acids in tea. China Meas. Test. Technol. 2008, 6, 77–80. [Google Scholar]
- Atoui, A.K.; Mansouri, A.; Boskou, G.; Panagiotis, K. Tea and herbal infusions: Their antioxidant activity and phenolic profile. Food Chem. 2005, 89, 27–36. [Google Scholar] [CrossRef]
- Zhang, C.; Suen, C.L.; Yang, C.; Quek, S.Y. Antioxidant capacity and major polyphenol composition of teas as affected by geographical location, plantation elevation and leaf grade. Food Chem. 2018, 244, 109–119. [Google Scholar] [CrossRef]
- Zhao, C.N.; Tang, G.Y.; Cao, S.Y.; Xu, X.Y.; Gan, R.Y.; Liu, Q.; Mao, Q.Q.; Shang, A.; Li, H.B. Phenolic profiles and antioxidant activities of 30 tea infusions from green, black, oolong, white, yellow and dark teas. Antioxidants 2019, 8, 215. [Google Scholar] [CrossRef]
- Sato, Y.; Itagaki, S.; Kurokawa, T.; Ogura, J.; Kobayashi, M.; Hirano, T.; Sugawara, M.; Iseki, K. In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. Int. J. Pharm. 2011, 403, 136–138. [Google Scholar] [CrossRef] [PubMed]
- Gülçin, I. Antioxidant activity of caffeic acid (3,4-dihydroxycinnamic acid). Toxicology 2006, 217, 213–220. [Google Scholar] [CrossRef] [PubMed]
- Zhao, M.; Zhu, D.; Sun-Waterhouse, D.; Su, G.; Lin, L.; Wang, X.; Dong, Y. In vitro and in vivo studies on adlay-derived seed extracts: Phenolic profiles, antioxidant activities, serum uric acid suppression, and xanthine oxidase inhibitory effects. J. Agric. Food Chem. 2014, 62, 7771–7778. [Google Scholar] [CrossRef] [PubMed]
- Amorati, R.; Valgimigli, L. Advantages and limitations of common testing methods for antioxidants. Free Radic. Res. 2015, 49, 633–649. [Google Scholar] [CrossRef] [PubMed]
- Huang, D.; Ou, B.; Prior, R.L. The chemistry behind antioxidant capacity assays. J. Agric. Food Chem. 2005, 53, 1841–1856. [Google Scholar] [CrossRef]
- Caruso, F.; Incerpi, S.; Pedersen, J.; Belli, S.; Kaur, S.; Rossi, M. Aromatic polyphenol π-π interactions with superoxide radicals contribute to radical scavenging and can make polyphenols mimic superoxide dismutase activity. Curr. Issues Mol. Biol. 2022, 44, 5209–5220. [Google Scholar] [CrossRef]
- Yu, S.; Caruso, F.; Belli, S.; Rossi, M. Scavenging of superoxide in aprotic solvents of four isoflavones that mimic superoxide dismutase. Int. J. Mol. Sci. 2023, 24, 3815. [Google Scholar] [CrossRef]
- Okoye, I.; Yu, S.; Caruso, F.; Rossi, M. X-ray structure determination, antioxidant voltammetry studies of butein and 2′,4′-dihydroxy-3,4-dimethoxychalcone. Computational studies of 4 structurally related 2′,4′-diOH chalcones to examine their antimalarial activity by binding to falcipain-2. Molecules 2021, 26, 6511. [Google Scholar] [CrossRef]
- Le Bourvellec, C.; Hauchard, D.; Darchen, A.; Burgot, J.L.; Abasq, M.L. Validation of a new method using the reactivity of electrogenerated superoxide radical in the antioxidant capacity determination of flavonoids. Talanta 2008, 75, 1098–1103. [Google Scholar] [CrossRef]
- Belli, S.; Rossi, M.; Molasky, N.; Middleton, L.; Caldwell, C.; Bartow-McKenney, C.; Duong, M.; Chiu, J.; Gibbs, E.; Caldwell, A.; et al. Effective and novel application of superoxide radical scavenging by natural phenolic antioxidants. Antioxidants 2019, 8, 14. [Google Scholar] [CrossRef] [PubMed]
- Sukma, R.M.; Iswantini, D.; Nurhidayat, N.; Rafi, M.; Ariyanti, D. Antioxidant determining using electrochemical method. Chemistry 2023, 5, 1921–1941. [Google Scholar] [CrossRef]
- Ye, N.; Belli, S.; Caruso, F.; Roy, G.; Rossi, M. Antioxidant studies by hydrodynamic voltammetry and DFT, quantitative analyses by HPLC-DAD of clovamide, a natural phenolic compound found in Theobroma Cacao L. beans. Food Chem. 2021, 341, 128260. [Google Scholar] [CrossRef] [PubMed]
- Caruso, F.; Rossi, M.; Kaur, S.; Garcia-Villar, E.; Molasky, N.; Belli, S.; Sitek, J.D.; Gionfra, F.; Pedersen, J.Z.; Incerpi, S. Antioxidant properties of embelin in cell culture. Electrochemistry and theoretical mechanism of scavenging. potential scavenging of superoxide radical through the cell membrane. Antioxidants 2020, 9, 382. [Google Scholar] [CrossRef] [PubMed]
- Sakib, R.; Caruso, F.; Belli, S.; Rossi, M. Azadiradione, a component of Neem Oil, behaves as a superoxide dismutase mimic when scavenging the superoxide radical, as shown using DFT and hydrodynamic voltammetry. Biomedicines 2023, 11, 3091. [Google Scholar] [CrossRef]
- Rossi, M.; Caruso, F.; Kwok, L.; Lee, G.; Caruso, A.; Gionfra, F.; Candelotti, E.; Belli, S.; Molasky, N.; Raley-Susman, K.M.; et al. Protection by extra virgin olive oil against oxidative stress in vitro and in vivo. Chemical and biological studies on the health benefits due to a major component of the Mediterranean diet. PLoS ONE 2017, 12, e0189341. [Google Scholar] [CrossRef]
- Sakib, R.; Caruso, F.; Aktar, S.; Belli, S.; Kaur, S.; Hernandez, M.; Rossi, M. Antioxidant properties of thymoquinone, thymohydroquinone and black cumin (Nigella sativa l.) seed oil: Scavenging of superoxide radical studied using cyclic voltammetry, DFT and single crystal X-ray diffraction. Antioxidants 2023, 12, 607. [Google Scholar] [CrossRef]
- Caruso, F.; Berinato, M.; Hernandez, M.; Belli, S.; Smart, C.; Rossi, M. Antioxidant properties of bee propolis and an important component, galangin, described by X-ray crystal structure, DFT-D and hydrodynamic voltammetry. PLoS ONE 2022, 17, e0267624. [Google Scholar] [CrossRef]
- Delley, B.J. From molecules to solids with the DMol3 approach. J. Chem. Phys. 2000, 113, 7756–7764. [Google Scholar] [CrossRef]
- Perdew, J.P.; Chevary, J.A.; Vosko, S.H.; Jackson, K.A.; Pederson, M.R.; Singh, D.J.; Fiolhais, C. Atoms, molecules, solids, and surfaces: Applications of the generalized gradient approximation for exchange and correlation. Phys. Rev. 1992, 46, 6671–6687. [Google Scholar] [CrossRef]
- Becke, A.D. Density-functional exchange-energy approximation with correct asymptotic behavior. Phys. Rev. A 1988, 38, 3098–3100. [Google Scholar] [CrossRef] [PubMed]
- Grimme, S. Semiempirical GGA-type density functional constructed with a long-range dispersion correction. J. Comput. Chem. 2006, 27, 1787–1799. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.; Yang, W.; Parr, R.G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 1988, 37, 785–789. [Google Scholar] [CrossRef] [PubMed]
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Caruso, F.; Sakib, R.; Belli, S.; Caruso, A.; Rossi, M. Antioxidant Scavenging of the Superoxide Radical by Yerba Mate (Ilex paraguariensis) and Black Tea (Camellia sinensis) Plus Caffeic and Chlorogenic Acids, as Shown via DFT and Hydrodynamic Voltammetry. Int. J. Mol. Sci. 2024, 25, 9342. https://doi.org/10.3390/ijms25179342
Caruso F, Sakib R, Belli S, Caruso A, Rossi M. Antioxidant Scavenging of the Superoxide Radical by Yerba Mate (Ilex paraguariensis) and Black Tea (Camellia sinensis) Plus Caffeic and Chlorogenic Acids, as Shown via DFT and Hydrodynamic Voltammetry. International Journal of Molecular Sciences. 2024; 25(17):9342. https://doi.org/10.3390/ijms25179342
Chicago/Turabian StyleCaruso, Francesco, Raiyan Sakib, Stuart Belli, Alessio Caruso, and Miriam Rossi. 2024. "Antioxidant Scavenging of the Superoxide Radical by Yerba Mate (Ilex paraguariensis) and Black Tea (Camellia sinensis) Plus Caffeic and Chlorogenic Acids, as Shown via DFT and Hydrodynamic Voltammetry" International Journal of Molecular Sciences 25, no. 17: 9342. https://doi.org/10.3390/ijms25179342