Comparative Chemical Analysis of Eight Punica granatum L. Peel Cultivars and Their Antioxidant and Anti-Inflammatory Activities
Abstract
:1. Introduction
2. Materials and Methods
2.1. Samples
2.2. Reagents
2.3. Peels Extraction
2.4. Qualitative Profiling of Pomegranate Peels Hydroalcoholic Extracts
2.5. Quantitative Analysis
2.6. DPPH Assay
2.7. ABTS Assay
2.8. Cell Viability Assay
2.9. Antioxidant Activity in M0 Macrophages
2.10. Cytokine Production and Enzyme-Linked Immunosorbent Assay (ELISA)
2.11. Bioinformatics Analyses
3. Results
3.1. LC-MS/MS-Based Quali-Quantitative Analysis
3.2. Antioxidant Activity
3.3. Anti-Inflammatory Activity
3.4. Bioinformatics Analyses
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Sample | Collection Area | Cultivars | Company |
---|---|---|---|
M1 | Benevento, Campania region | Dente di cavallo | Caruso |
M2 | Palomonte, Campania region | Dente di cavallo | Rosso Granato |
M3 | Sicignano degli Alburni, Campania region | Wonderful | Rosso Granato |
M4 | Palomonte, Campania region | Wonderful One | Rosso Granato |
M5 | Aiello del Sabato, Campania region | Granato di Aiello del Sabato | Giovomel |
M6 | Pietrelcina, Campania region | Dente di cavallo | Salgliocca |
M7 | Acri, Calabria region | Dente di cavallo | Cofone |
M8 | Tursi, Basilicata region | Dente di cavallo | Francolino |
M9 | Forchia, Campania region | Hicaz | ErarslanFarm |
M10 | Caserta, Campania region | Wonderful precoce | Luce |
M11 | Altavilla silentina, Campania region | Dente di cavallo | De Matteis |
M12 | Altavilla silentina, Campania region | Mollar de Elche | De Matteis |
M13 | Telese, Campania region | Parfianka | Troiano |
M14 | Grottaminarda, Campania region | Wonderful | Bruno |
tR (min) | [M-H]2−/[M-H]− | MS2 | Compound | MSI Status a | |
---|---|---|---|---|---|
1 | 2.1 | 481.0632 | 300.9991, 275.0185 | HHDP b-hexoside 1 | 2 |
2 | 2.8 | 481.0632 | 300.9991, 275.0185 | HHDP-hexoside 2 | 2 |
3 | 3.0 | 331.0680 | 271.0449, 211.0239, 169.0143 | Galloyl-hexoside 1 | 2 |
4 | 3.5 | 331.0680 | 271.0449, 211.0239, 169.0143 | Galloyl-hexoside 2 | 2 |
5 | 3.9 | 649.0705 | 300.9991, 497.0575 | Galloyl-HHDP-gluconate | 2 |
6 | 4.0 | 633.0752 | 481.0630, 300.9991, 249.0407, 275.0185 | HHDP-galloyl-hexoside | 2 |
7 | 4.2 | 169.0138 | 125.0249 | Gallic acid | 1 |
8 | 4.3 | 331.0680 | 271.0449, 211.0239, 169.0143 | Galloyl-hexoside 3 | 2 |
9 | 4.4 | 483.0798 | 331.0671, 313.0566, 169.0143 | Digalloyl-hexoside | 2 |
10 | 4.6–4.8 | 781.0555 | 721.0330, 600.9907, 475.0361 | Punicalin | 1 |
11 | 4.9 | 483.0798 | 331.0671, 313.0566, 169.0143 | Digalloyl-hexoside isomer | 2 |
12 | 5.7 | 633.0752 | 481.0630, 300.9991, 249.0407, 275.0185 | HHDP-galloyl-hexoside isomer | 2 |
13 | 6.0 | 391.0321/783.0712 | 765.0588, 721.0330, 481.0630, 300.9991 | Casuariin | 2 |
14 | 6.1 | 541.0272/1083.0630 | 807.0330, 721.0330, 600.9907, 510.0260, 275.0185 | Punicalagin isomer 1 | 2 |
15 | 6.5 | 649.0705 | 300.9991, 497.0575 | Galloyl-HHDP-gluconate | 2 |
16 | 6.8 | 541.0272/1083.0630 | 807.0330, 721.0330, 600.9907, 510.0260, 275.0185 | Punicalagin isomer 2 | 2 |
17 | 7.1 | 483.0798 | 331.0671, 313.0566, 169.0143 | Digalloyl-hexoside isomer | 2 |
18 | 7.2 | 466.0299/933.0679 | 915.0552, 781.0550, 721.0330, 600.9907, 300.9991 | Castalagin | 2 |
19 | 7.8 | 391.0321/783.0712 | 631.0589, 481.0630, 300.9991 | Pedunculagin | 2 |
20 | 7.9 | 707.0647/1415.1368 | 783.0690, 613.0480, 633.0739, 300.9991 | Di (HHDPgalloyl-hexoside)-pentoside | 2 |
21 | 8.3 | 305.0675 | 125.0249, 137.0250 | Gallocatechin | 2 |
22 | 8.4 | 466.0299/933.0679 | 781.0550, 631.0589, 450.9945, 425.0153, 300.9991, 275.0185 | 2-O-Galloylpunicalin | 2 |
23 | 12.9 | 541.0272/1083.0630 | 781.0550, 600.9907, 300.9991, 275.0185 | Punicalagin A | 1 |
24 | 14.3 | 391.0318/783.0708 | 631.0589, 481.0630, 300.9991 | Pedunculagin isomer | 2 |
25 | 14.5 | 951.0767 | 907.0867, 783.0690, 605.0800, 481.0630, 300.9991 | Trisgalloyl HHDP-hexoside | 2 |
26 | 15.3 | 632.0670/1265.1423 | 783.0690, 481.0630 | Pedunculagin-I-der | 2 |
27 | 16.2 | 392.0392/785.0859 | 300.9991, 275.0185, 249.0407, 169.0143 | Digallolyl HHDP-hexoside | 2 |
28 | 16.3 | 541.0272/1083.0630 | 781.0550, 600.9907, 300.9991, 275.0185 | Punicalagin B | 1 |
29 | 17.4 | 799.0657 | 781.0550, 479.0476, 300.9991 | Granatin A | 2 |
30 | 18.2 | 467.0374/935.0822 | 917.0711, 783.0690, 633.0739, 571.0740 | Galloyl-bis-HHDP-hexoside (casuarinin) | 2 |
31 | 18.3 | 400.0371/801.0814 | 649.0681, 499.0724, 347.0623, 300.9991 | Punigluconin | 2 |
32 | 18.4 | 783.0718/1567.1511 | 765.0588, 300.9991 | Digalloyl triHHDP-dihexoside | 2 |
33 | 19.2 | 392.0392/785.0859 | 300.9991, 275.0185, 249.0407, 169.0143 | Digallolyl-HHDP-hexoside | 2 |
34 | 19.2 | 542.0355/1085.0795 | 783.0690, 765.0588, 300.9991 | Digalloyl-gallagyl-hexoside | 2 |
35 | 19.6 | 542.0355/1085.0795 | 783.0690 765.0588, 300.9991 | Digalloyl-gallagyl-hexoside isomer | 2 |
36 | 19.8 | 633.0752 | 481.0630, 300.9991, 249.0407, 275.0185 | HHDP galloyl-hexoside isomer | 2 |
37 | 20.6 | 463.0530 | 300.9991 | Ellagic acid hexoside | 2 |
38 | 22.7 | 951.0767 | 933.0668, 765.0588, 613.0480, 445.0425, 300.9991 | Trisgalloyl HHDP-hexoside | 2 |
39 | 23.6 | 787.1035 | 635.0883, 617.0779, 465.0671, 447.0562 | Tetragalloyl-hexoside isomer 1 | 2 |
40 | 23.7 | 392.0392/785.0859 | 300.9991, 275.0185, 249.0407, 169.0143 | Digallolyl HHDP hexoside | 2 |
41 | 23.8 | 433.0428 | 299.9917, 300.9991 | Ellagic acid-pentoside | 2 |
42 | 24.0 | 447.0580 | 300.9991, 300.9991 | Ellagic acid-deoxyhexoside | 2 |
43 | 24.2 | 787.1035 | 635.0883, 617.0779, 465.0671, 447.0562 | Tetragalloyl-hexoside isomer 2 | 2 |
44 | 24.6 | 787.1035 | 635.0883, 617.0779, 465.0671, 447.0562 | Tetragalloyl-hexoside isomer 3 | 2 |
45 | 24.7 | 609.1458 | 301.0356 | Rutin | 1 |
46 | 24.8 | 300.9995 | 257.0094, 229.0146, 185.0249 | Ellagic acid | 1 |
47 | 25.5 | 463.0902 | 301.0356 | Quercetin-hexoside | 2 |
48 | 26.3 | 939.1158 | 787.1030, 635.0883 | Pentagalloyl-hexoside | 2 |
49 | 26.8 | 593.1534 | 447.0948, 285.0400 | Kaempferol-rutinoside | 2 |
50 | 27.8 | 447.0948 | 285.0400 | Kaempferol-hexoside | 2 |
51 | 28.4 | 431.0999 | 269.0447 | Apigenin 7-O-glucoside | 1 |
52 | 28.7 | 431.0999 | 269.0447 | Apigenin-hexoside | 2 |
53 | 29.1 | 417.0843 | 285.0400 | Kaempferol-pentoside | 2 |
54 | 29.8 | 447.0948 | 285.0400 | Luteolin 7-O-glucoside | 1 |
55 | 29.9 | 417.0843 | 285.0400 | Kaempferol pentoside isomer | 2 |
Cyanidin 3-O-glucoside | Delphinidin 3-O-glucoside | Ellagic Acid | Gallic Acid | Punicalagin | Punicalin | |
---|---|---|---|---|---|---|
M1 | 0.15 ± 0.02 | nd | 13.20 ± 1.89 a | 0.55 ± 0.10 a | 87.86 ± 20.16 a | 4.22 ± 0.11 a |
M2 | 0.13 ± 0.01 | nd | 7.07 ± 2.29 bc | 0.71 ± 0.01 ac | 72.91 ± 18.59 a | 3.43 ± 0.41 a |
M3 | 0.35 ± 0.01 | nd | 8.19 ± 1.68 acd | 0.75 ± 0.02 ad | 93.86 ± 22.66 a | 3.85 ± 0.29 a |
M4 | 0.34 ± 0.01 | nd | 5.65 ± 1.39 bde | 0.65 ± 0.02 a | 58.16 ± 9.72 a | 2.27 ± 0.22 a |
M5 | 0.17 ± 0.01 | nd | 11.55 ± 0.69 af | 0.77 ± 0.04 a | 107.28 ± 3.86 ac | 3.70 ± 0.11 a |
M6 | 0.14 ± 0.01 | nd | 13.80 ± 2.51 a | 1.52 ± 0.06 b | 85.16 ± 11.90 a | 6.73 ± 0.46 ab |
M7 | 0.14 ± 0.01 | nd | 14.67 ± 0.92 a | 0.68 ± 0.01 ah | 142.38 ± 4.16 bd | 6.58 ± 0.74 ab |
M8 | 0.12 ± 0.01 | nd | 12.66 ± 1.76 a | 0.96 ± 0.01 bcdh | 112.79 ± 5.01 acd | 4.22 ± 0.45 a |
M9 | 0.47 ± 0.05 | nd | 7.15 ± 0.56 bdfg | 0.47 ± 0.01 afi | 85.04 ± 6.85 a | 4.04 ± 0.66 a |
M10 | 0.44 ± 0.03 | nd | 4.60 ± 0.30 bdh | 0.36 ± 0.01 afi | 89.79 ± 1.57 a | 3.02 ± 0.21 a |
M11 | 0.13 ± 0.01 | nd | 11.96 ± 0.68 acg | 0.20 ± 0.03 bdgij | 83.35 ± 6.90 a | 3.43 ± 0.61 a |
M12 | 0.11 ± 0.01 | nd | 8.64 ± 0.54 aceghi | 0.41 ± 0.01 af | 80.65 ± 2.42 a | 3.30 ± 0.27 a |
M13 | 1.99 ± 0.05 | 0.52 ± 0.08 | 4.62 ± 0.1 bdi | 0.33 ± 0.01 ae | 52.38 ± 5.99 a | 2.36 ± 0.23 a |
M14 | 0.61 ± 0.07 | nd | 5.87 ± 0.40 bdi | 0.56 ± 0.01 ac | 59.32 ± 5.37 a | 2.50 ± 0.27 a |
Sample | DPPH TEAC mM | ABTS TEAC mM |
---|---|---|
M1 | 45.8 ± 4.1 a | 7.4 ± 0.2 a |
M2 | 53.3 ± 5.3 ac | 8.4 ± 0.1 b |
M3 | 72.8 ± 6.1 b | 10.3 ± 0.1 bc |
M4 | 49.7 ± 6.1 ad | 10.2 ± 0.1 bc |
M5 | 67.4 ± 4.5 a | 7.6 ± 0.2 a |
M6 | 45.3 ± 3.6 a | 8.5 ± 0.1 b |
M7 | 63.1 ± 3.9 bc | 10.2 ± 0.1 bc |
M8 | 59.6 ± 5.5 bcd | 8.4 ± 0.1 b |
M9 | 60.6 ± 5.4 bcd | 9.4 ± 0.2 bcd |
M10 | 59.2 ± 5.1 bcde | 10.2 ± 0.1 bc |
M11 | 48.3 ± 2.3 ae | 9.3 ± 0.2 bcd |
M12 | 47.3 ± 6.8 a | 8.2 ± 0.2 b |
M13 | 40.1 ± 5.9 a | 9.4 ± 0.1 bcd |
M14 | 70.0 ± 9.1 b | 13.3 ± 0.2 bcde |
(A) | |||||||||||
ABTS TEAC | DPPH Assay | ||||||||||
ρ | |||||||||||
Granatin | −0.485 *** | −0.557 *** | |||||||||
Trisgalloyl iso 2 | −0.469 *** | −0.491 *** | |||||||||
HHDP iso 2 | −0.464 *** | 0.180 | |||||||||
Casuarinin | −0.441 ** | −0.137 | |||||||||
Digalloyl HHDP iso 3 | −0.364 ** | −0.160 | |||||||||
Galloyl-hexoside iso 1 | −0.351 ** | 0.260 | |||||||||
Ellagic acid | −0.319 * | −0.436 ** | |||||||||
Pedunculagin | −0.313 * | 0.103 | |||||||||
Galloyl-hexoside iso 3 | −0.312 * | −0.084 | |||||||||
HHDP iso 1 | −0.303 * | −0.035 | |||||||||
Digalloyl iso 3 | −0.288 * | 0.243 | |||||||||
Pedunculagin iso 2 | −0.269 * | 0.373 | |||||||||
Galloyl-hexoside iso 3 | −0.260 | −0.141 | |||||||||
Galloyl-hexoside iso 3 | −0.260 | −0.141 | |||||||||
(B) | |||||||||||
IL-1β | IL-6 | TNF-α | |||||||||
ρ | |||||||||||
Galloyl-hexoside iso 2 | −0.900 *** | 0.022 | −0.374 ** | ||||||||
Pedunculagin | −0.728 *** | −0.057 | −.591 *** | ||||||||
HHDP iso 2 | −0.677 *** | 0.083 | −0.323 * | ||||||||
Pedunculagin iso 2 | −0.673 *** | 0.042 | −0.310 * | ||||||||
Punicalagin iso 2 | −0.600 *** | −0.060 | −0.634 *** | ||||||||
Pedunculagin iso 1 | −0.588 *** | −0.096 | −0.295 * | ||||||||
Trisgalloyl iso 1 | −0.582 *** | −0.085 | −0.460 *** | ||||||||
Galloyl-gluconate iso 2 | −0.555 *** | −0.222 | −0.359 ** | ||||||||
Galloylpunicalin | −0.544 *** | −0.092 | −0.576 *** | ||||||||
Digalloyl | −0.520 *** | −0.112 | −0.436 ** | ||||||||
Digalloyl HHDP iso 2 | −0.518 *** | 0.131 | −0.273 * | ||||||||
Castalagin | −0.515 *** | −0.127 | −0.615 *** | ||||||||
Casuarinin | −0.499 *** | −0.248 | −0.454 *** | ||||||||
Punicalagin iso 1 | −0.489 *** | −0.241 | −0.703 *** | ||||||||
Galloyl-gluconate iso 1 | −0.446 ** | −0.296 * | −0.382 ** | ||||||||
Ellagic acid deoxy | −0.438 ** | −0.361 ** | −0.545 *** | ||||||||
Ellagic acid pentoside | −0.429 ** | −0.356 ** | −0.504 *** | ||||||||
Digalloyl gallagyl iso 1 | −0.416 ** | −0.381 ** | −0.109 | ||||||||
Digalloyl gallagyl iso 2 | −0.410 ** | −0.402 ** | −0.108 | ||||||||
Digalloyl HHDP iso 3 | −0.403 ** | −0.500 *** | −0.221 | ||||||||
Casuariin | −0.395 ** | −0.298 * | −0.133 | ||||||||
Galloyl-hexoside iso 3 | −0.268 * | −0.470 *** | −0.038 | ||||||||
Ellagic acid hexoside | −0.217 | −0.329 * | −0.485 *** | ||||||||
Digalloyl iso 2 | −0.127 | −0.376 ** | −0.376 ** |
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Parisi, V.; Santoro, V.; Donadio, G.; Bellone, M.L.; Diretto, G.; Sandri, C.; Mensitieri, F.; De Tommasi, N.; Dal Piaz, F.; Braca, A. Comparative Chemical Analysis of Eight Punica granatum L. Peel Cultivars and Their Antioxidant and Anti-Inflammatory Activities. Antioxidants 2022, 11, 2262. https://doi.org/10.3390/antiox11112262
Parisi V, Santoro V, Donadio G, Bellone ML, Diretto G, Sandri C, Mensitieri F, De Tommasi N, Dal Piaz F, Braca A. Comparative Chemical Analysis of Eight Punica granatum L. Peel Cultivars and Their Antioxidant and Anti-Inflammatory Activities. Antioxidants. 2022; 11(11):2262. https://doi.org/10.3390/antiox11112262
Chicago/Turabian StyleParisi, Valentina, Valentina Santoro, Giuliana Donadio, Maria Laura Bellone, Gianfranco Diretto, Carla Sandri, Francesca Mensitieri, Nunziatina De Tommasi, Fabrizio Dal Piaz, and Alessandra Braca. 2022. "Comparative Chemical Analysis of Eight Punica granatum L. Peel Cultivars and Their Antioxidant and Anti-Inflammatory Activities" Antioxidants 11, no. 11: 2262. https://doi.org/10.3390/antiox11112262