Characterization of Extractable and Non-Extractable Phenols and Betalains in Berrycactus (Myrtillocactus geometrizans) and Its Chemoprotective Effect in Early Stage of Colon Cancer In Vivo
Abstract
1. Introduction
2. Materials and Methods
2.1. Fruit Sample
2.2. Extractable Phenolics
2.3. Non-Extractable Phenolics
2.4. Total Phenolic, Flavonoid, and Condensed Tannins
2.5. Betanin and Vulgaxanthines
2.6. Dietary Fiber
2.7. Antioxidant Capacity Determination
2.8. Identification of Bioactive Compounds by UPLC-QTOF-MSE
2.9. In Vivo Experimental Design
2.10. Histologic Analysis
2.11. β-Glucoronidase Activity Determination
2.12. Short-Chain Fatty Acids in Feces
2.13. Statistical Analysis
3. Results and Discussion
3.1. Betalains and Dietary Fiber
3.2. Phenolics in Extractable and Non-Extractable Polyphenols
3.3. Polyphenol Profile of EP and NEP by UPLC-QToF MS
3.4. Antioxidant Capacity of EP and NEP
3.5. In Vivo Model
3.6. Quantification of ACF in Distal Colonic Tissue
3.7. β-Glucoronidase Activity
3.8. Production of Short-Chain Fatty Acids
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Extractable Polyphenols | Non-Extractable Polyphenols | |||||
---|---|---|---|---|---|---|
H2SO4 | HCl | |||||
1 M | 4 M | 1 M | 4 M | |||
TP | (mg GAE/100 g) | 958.7 ± 26 a | 1804.8 ± 3.7 b | 1447.7 ± 3.7 c | 2070.1 ± 14.1 d | 2008.1 ± 25.4 e |
TF | (mg CE/100 g) | 397.1 ± 13 a | 802.2 ± 2.2 b | 1339.6 ± 85 c | 1431.0 ± 26 d | 1114.3 ± 11 d |
CT | (mg CE/100 g) | 120.9 ± 4 a | 163.2 ± 3.7 b | 103.1 ± 3.7 c | 114.3 ± 11 d | 98.7 ± 3.5 c |
Family | Component Name | Retention Time (min) | Molecular Formula | Observed m/z | Adducts | Fragments | Extractable Polyphenols (EPs) | Non-Extractable Polyphenols (NEPs) | |
---|---|---|---|---|---|---|---|---|---|
HCl | |||||||||
1 M | 4 M | ||||||||
Flavonols | Kaempferol rutinoside | 3.79 | C27H30O15 | 593.1517 | [M-H]− | 284.02482, 151.05667 | 15.14 ± 3.10 d | 3.84 ± 0.16 c | 4.27 ± 0.15 b |
Myricetin * | 3.99 | C15H10O8 | 317.0315 | [M-H]− | 179.03553, 151.04052 | ND | ND | ND | |
Quercetin rhamnosyl- rhamnosyl-hexoside | 4.44 | C33H40O20 | 755.2054 | [M-H]− | 609.14759, 300.02792, 151.00426 | 150.48 ± 0.73 i | 40.74 ± 0.04 e | 20.21 ± 0.15 d | |
Kaempferol rhamnosyl- hexoside-rhamnoside | 5.14 | C33H40O19 | 739.2113 | [M-H]− | 447.09479, 431.19371, 284.03324, 151.06481 | 12.02 ± 0.00 d | 2.53 ± 0.03 c | 0.89 ± 0.05 a | |
Quercetin rutinoside * | 5.35 | C27H30O16 | 609.1479 | [M-H]− | 300.02817, 151.00450 | 44.82 ± 0.06 h | 5.24 ± 7.41 c | 5.72 ± 0.13 b | |
Kaempferol dihexoside | 5.61 | C27H30O16 | 609.1482 | [M-H]− | 447.09449, 284.03222, 151.09310 | 9.13 ± 0.86 c | 4.58 ± 0.15 c | 7.80 ± 0.12 c | |
Kaempferol hexoside | 6.22 | C21H20O11 | 447.0954 | [M-H]− | 285.04134, 151.07177 | 8.66 ± 0.01 c | 1.32 ± 0.01 b | 1.21 ± 0.0 a | |
(Iso)-rhamnetin hexoside | 7.50 | C22H22O12 | 477.1062 | [M-H]− | 284.97552, 151.00421 | 4.74 ± 0.00 b | 2.45 ± 0.00 c | 1.02 ± 0.0 a | |
Isorhamnetin * | 9.99 | C16H12O7 | 315.0504 | [M-H]− | 315.05231, 300.02842, 285.04171, 151.00472 | ND | 0.34 ± 0.00 a | 0.24 ± 0.02 a | |
Quercetin * | 11.02 | C15H10O7 | 301.0365 | [M-H]− | 178.99924, 151.00423, 107.01432 | ND | 2.62 ± 0.02 c | 4.46 ± 0.18 b | |
Hydroxybenzoic acids | Dihydroxybenzoic acid isomer I | 1.84 | C7H6O4 | 153.0187 | [M-H]− | 137.02375, 109.02909 | ND | 2.50 ± 0.08 c | 1.16 ±0.01 a |
Methyl gallic acid | 2.23 | C8H8O4 | 183.0290 | [M-H]− | 169.04992 | ND | 2.85 ± 0.20 c | 1.62 ± 0.04 a | |
Hydroxybenzoic acid isomer I | 2.71 | C7H6O3 | 137.0243 | [M-H]− | 109.02171 | 7.78 ± 0.13 b | ND | ND | |
Dihydroxybenzoic acid hexoside | 2.82 | C13H16O9 | 315.0716 | [M-H]− | 153.01914, 137.02446, 109.02949 | 31.19 ± 2.42 g | 3.09 ± 0.07 c | 1.77 ± 0.04 a | |
Dihydroxybenzoic acid isomer II * | 2.84 | C7H6O4 | 153.0194 | [M-H]− | 137.03907, 109.02967 | ND | 3.36 ± 0.02 c | 1.47 ± 0.08 a | |
Hydroxybenzoic acid hexoside | 3.01 | C13H16O8 | 299.0773 | [M-H]− | 137.02452 | 21.28 ± 0.07 f | 3.38 ± 0.08 c | 0.98 ± 0.02 a | |
Gallic acid * | 3.07 | C7H6O5 | 169.0144 | [M-H]− | 125.0469 | ND | 3.02 ± 0.02 c | 8.57 ± 019 c | |
Hydroxybenzoic acid isomer II * | 3.22 | C7H6O3 | 137.0247 | [M-H]− | 109.02969 | 7.09 ± 0.42 b | 76.01 ± 0.72 f | 31.99 ±0.25 c | |
Hydroxybenzoic acid isomer III | 4.19 | C7H6O3 | 137.0251 | [M-H]− | 109.02996 | 5.70 ± 0.34 b | ND | ND | |
Vanillic acid * | 4.69 | C8H8O4 | 167.0357 | [M-H]− | 139.04067, 109.02987 | 4.35 ± 0.04 b | 9.91 ± 0.02 d | 7.04 ± 0.01 c | |
Hydroxycinnamic acids | Caffeic acid hexoside | 3.23 | C15H18O9 | 341.0878 | [M-H]− | 179.03506, 135.04525 | 16.06 ± 0.27 e | 5.01 ± 1.73 c | 5.37 ± 0.06 b |
Coumaroyl hexoside | 3.40 | C15H18O8 | 325.0933 | [M-H]− | 163.04038, 119.05054 | 4.21 ± 0.12 b | 0.92 ± 0.12 a | 1.12 ± 0.10 a | |
Ferulic acid hexoside | 3.66 | C16H20O9 | 355.1037 | [M-H]− | 193.05082, 178.02736, 134.03761 | 22.53 ± 1.32 f | 4.6 ± 0.05 c | ND | |
Coumaroylquinic acid | 4.61 | C16H18O8 | 337.0939 | [M-H]− | 191.05682, 163.05624 | 5.79 ± 1.25 b | ND | ND | |
Caffeic acid * | 4.80 | C9H8O4 | 179.0357 | [M-H]− | 109.02989 | ND | 2.13 ± 0.02 c | 0.31 ± 0.44 a | |
p-Coumaric acid * | 5.11 | C9H8O3 | 163.0408 | [M-H]− | 119.05085 | 8.75 ± 0.40 c | 1.62 ± 0.00 b | 1.00 ± 0.01 a | |
Ferulic acid * | 5.19 | C10H10O4 | 193.0515 | [M-H]− | 178.02806, 134.03809 | 3.27 ± 0.62 b | 0.64 ± 0.00 b | 1.12 ± 0.05 a | |
Sinapic acid hexoside | 5.23 | C17H22O10 | 385.1153 | [M-H]− | 223.09660, 209.08182 | 24.30 ± 0.11 f | 2.48 ± 0.05 c | 1.94 ± 0.07 a | |
Coumaroyl malic acid | 5.43 | C13H12O7 | 279.0519 | [M-H]− | 163.04082, 119.05093 | 4.55 ± 0.03 b | 2.12 ± 0.24 c | ND | |
Betalains | Betanidin | 2.80 | C18H16N2O8 | 389.0965 | [M+H]+ | 345.10744 | 7 ± 0.11 b | ND | ND |
Proline-betaxanthin (indicaxanthin) | 2.72 | C14H16N2O6 | 309.1068 | [M+H]+ | 389.09606 | 35.71 ± 0.18 g | ND | ND | |
Betanidin β-hexoside (betanin) * | 2.66 | C24H26N2O13 | 551.1486 | [M+H]+ | 389.09643 | 157.64 ± 3.01 i | ND | ND | |
Isobetanidin β-hexoside (isobetanin) | 3.67 | C24H26N2O13 | 551.1481 | [M+H]+ | 265.09656 | 1.98 ± 0.29 a | ND | ND |
Non-Extractable Polyphenols (μmol TE/g GL) | |||||
---|---|---|---|---|---|
Extractable Polyphenols (μmol TE/g GL) | H2SO4 | HCl | |||
1 M | 4 M | 1 M | 4 M | ||
DPPH | 40.0 ± 1.5 a | 376.6 ± 9 b | 394.2 ± 12.2 b | 452 ± 13 c | 357.2 ± 10.6 b |
FRAP | 105.7 ± 3.3 a | 614.7 ± 20 b | 841.4 ± 30 c | 1199 ± 38 d | 1159 ± 22 d |
TEAC | 100.8 ± 3.6 a | 1445.8 ± 34 b | 1037.9 ± 44 c | 1560 ± 66 d | 525.9 ± 51 e |
ORAC | 140.5 ± 5.5 a | 509.3 ± 22 b | 302.7 ± 11 c | 1620.8 ± 63 d | 1464 ± 56 e |
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Godínez-Santillán, R.I.; Kuri-García, A.; Ramírez-Pérez, I.F.; Herrera-Hernández, M.G.; Ahumada-Solórzano, S.M.; Guzmán-Maldonado, S.H.; Vergara-Castañeda, H.A. Characterization of Extractable and Non-Extractable Phenols and Betalains in Berrycactus (Myrtillocactus geometrizans) and Its Chemoprotective Effect in Early Stage of Colon Cancer In Vivo. Antioxidants 2024, 13, 1112. https://doi.org/10.3390/antiox13091112
Godínez-Santillán RI, Kuri-García A, Ramírez-Pérez IF, Herrera-Hernández MG, Ahumada-Solórzano SM, Guzmán-Maldonado SH, Vergara-Castañeda HA. Characterization of Extractable and Non-Extractable Phenols and Betalains in Berrycactus (Myrtillocactus geometrizans) and Its Chemoprotective Effect in Early Stage of Colon Cancer In Vivo. Antioxidants. 2024; 13(9):1112. https://doi.org/10.3390/antiox13091112
Chicago/Turabian StyleGodínez-Santillán, Rosa Iris, Aarón Kuri-García, Iza Fernanda Ramírez-Pérez, María Guadalupe Herrera-Hernández, Santiaga Marisela Ahumada-Solórzano, Salvador Horacio Guzmán-Maldonado, and Haydé Azeneth Vergara-Castañeda. 2024. "Characterization of Extractable and Non-Extractable Phenols and Betalains in Berrycactus (Myrtillocactus geometrizans) and Its Chemoprotective Effect in Early Stage of Colon Cancer In Vivo" Antioxidants 13, no. 9: 1112. https://doi.org/10.3390/antiox13091112
APA StyleGodínez-Santillán, R. I., Kuri-García, A., Ramírez-Pérez, I. F., Herrera-Hernández, M. G., Ahumada-Solórzano, S. M., Guzmán-Maldonado, S. H., & Vergara-Castañeda, H. A. (2024). Characterization of Extractable and Non-Extractable Phenols and Betalains in Berrycactus (Myrtillocactus geometrizans) and Its Chemoprotective Effect in Early Stage of Colon Cancer In Vivo. Antioxidants, 13(9), 1112. https://doi.org/10.3390/antiox13091112