The Antioxidant Properties of Salvia verbenaca Extract Contribute to Its Intestinal Antiinflammatory Effects in Experimental Colitis in Rats
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals and Reagents
2.2. Plant Material and Preparation of the Extract
2.3. Chemical Composition of S. verbenaca Using High-Performance Liquid Chromatography-Mass Spectrometry Condition
2.4. Total Phenolic Content and Antioxidant Capacity Assays
2.5. In Vitro Studies
2.6. Animals and Experimental Design
2.7. Analysis of Gene Expression by RT-qPCR
2.8. Statistics
3. Results
3.1. Chemical Characterization of S. verbenaca
3.2. Antioxidant Capacity of S. verbenaca
3.3. Immunomodulatory Properties of S. verbenaca in Murine Intestinal Epithelial Cells
3.4. Intestinal Anti-Inflammatory Effect of S. verbenaca in TNBS-Induced Colitis in Rats
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Score | Criteria |
---|---|
0 | No damage |
1 | Hyperemia, no ulcers |
2 | Linear ulcer with no significant inflammation |
3 | Linear ulcer with inflammation at one site |
4 | Two or more sites of ulceration/inflammation |
5 | Two or more major sites of ulceration and inflammation or one site of ulceration/inflammation extending along the length of the colon |
6–10 | If damage covers along the length of the colon, the score is increased by 1 for each additional centimeter of involvement |
Gene | Organism | Sequence 5′–3′ | Annealing T °C | Accesion Number |
---|---|---|---|---|
Gapdh | Mouse/Rat | FW: CCATCACCATCTTCCAGGAG RV: CCTGCTTCACCACCTTCTTG | 60 | NM_001289726.1 |
Il6 | Mouse | FW: TAGTCCTTCCTACCCCAATTTCC RV: TTGGTCCTTAGCCACTCCTTCC | 60 | NM_031168.2 |
Icam-1 | Mouse | FW: CAGTCCGCTGTGCTTTGAGA RV: CGGAAACGAATACACGGTGAT | 62 | NC_000075.7 |
Mip-2 | Mouse | FW: CAGTGAGCTGCGCTGTCCAATG RV: CAGTTAGCCTTGCCTTTGTTCAG | 57 | NC_000071.7 |
Muc2 | Mouse | FW: GCAGTCCTCAGTGGCACCTC RV: CACCGTGGGGCTACTGGAGAG | 60 | NC_000073.7 |
Tnfα | Mouse | FW: AACTAGTGGTGCCAGCCGAT RV: CTTCACAGAGCAATGACTCC | 60 | NM_001278601.1 |
Cinc-1 | Rat | FW: GGCAGGGATTCACTTCAAGA RV: GCCATCGGTGCAATCTATCT | 60 | NC_051349.1 |
Icam-1 | Rat | FW: AGGTATCCATCCATCCCACA RV: AGTGTCTCATTGCCACGGAG | 60 | NC_051343.1 |
Il1β | Rat | FW: GATCTTTGAAGAAGAGCCCG RV: AACTATGTCCCGACCATTGC | 59 | NC_051338.1 |
Il6 | Rat | FW: CTTCCCTACTTCACAAGTC RV: CTCCATTAGGAGAGCATTG | 60 | NC_051339.1 |
Il12a | Rat | FW: ACGCTACCTCCTCTTCTTG RV: ATGTCGTCCGTGGTCTTC | 60 | NC_051337.1 |
Il17 | Rat | FW: TGGACTCTGAGCCGCAATGAGG RV: GACGCATGGCGGACAATAGAGG | 60 | NC_051344.1 |
Il23 | Rat | FW: ATCCAGTGTGGTGATGGTTGTG RV: TGTCCGAGTCCAGCAGGTG | 60 | NC_051342.1 |
iNos | Rat | FW: AAGAGACGCACAGGCAGAGG RV: AGCAGGCACACGCAATGAT | 60 | NC_051345.1 |
Mcp-1 | Rat | FW: CACTATGCAGGTCTCTGTCACG RV: CTGGTCACTTCTACAGAAGTGC | 60 | NC_051345.1 |
Muc-2 | Rat | FW: ACCACCATTACCACCACCTCAG RV: CGATCACCACCATTGCCACTG | 60 | NC_051336.1 |
Muc-3 | Rat | FW: CACAAAGGCAAGAGTCCAGA RV: ACTGTGCTTGGTGCTGAATG | 60 | NC_051347.1 |
Villin | Rat | FW: TGTGGAACTGGCAGGGAG RV: GGGGTGGGTCTTGAGGTATT | 59 | NC_051344.1 |
Peak | RT | Measured m/z | Molecular Formula | Proposed Compounds | Main Fragments |
---|---|---|---|---|---|
1 | 1.01 | 195.0538 | C6H12O7 | Gluconic acid | NF |
2 | 1.14 | 133.0165 | C4H6O5 | Malic acid | NF |
3 | 1.28 | 191.0226 | C6H8O7 | Citric acid | NF |
4 | 1.58 | 96.9610 | - | Sulfate | NF |
5 | 1.73 | 96.9610 | - | Sulfate | NF |
6 | 2.20 | 191.0559 | C7H12O6 | Quinic acid | NF |
7 | 2.39 | 395.0965 | C18H20O10 | Acetylisobiflorin | 179 |
8 | 2.74 | 315.0723 | C13H16O9 | Gentisoyl glucoside | 152, 108 |
9 | 2.85 | 551.1058 | C24H24O15 | Phloroscorbinol hexaacetate | NF |
10 | 3.19 | 153.0188 | C7H6O4 | Dihydroxybenzoic acid | 109 |
11 | 3.38 | 181.0502 | C9H10O4 | Dihydrocaffeic acid isomer 1 | 135 |
12 | 3.67 | 175.0608 | C7H12O5 | Isopropylmalic acid | NF |
13 | 4.35 | 391.0667 | C18H16O10 | Pentahydroxy trimethoxy flavone isomer 1 | 347, 303 |
14 | 4.55 | 325.0927 | C15H18O8 | p-Coumaric acid glucoside | 163 |
15 | 4.72 | 391.0661 | C18H16O10 | Pentahydroxy trimethoxy flavone isomer 2 | 347, 303 |
16 | 5.66 | 475.0886 | C22H20O12 | Chrysoeriol glucuronide | 299, 227 |
17 | 6.22 | 475.1833 | C21H32O12 | Cistanoside E | 179, 135 |
18 | 6.32 | 181.0504 | C9H10O4 | Dihydrocaffeic acid isomer 2 | NF |
19 | 6.80 | 179.0346 | C9H8O4 | Caffeic acid | 135 |
20 | 7.34 | 593.1158 | C30H26O13 | O-coumaroyl orientin | NF |
21 | 7.65 | 639.1199 | C27H28O18 | Quercetin glucosyl-glucuronide isomer 1 | 463, 300 |
22 | 7.89 | 405.0834 | C19H18O10 | Glucopyranosyl-trihydroxy-9H-xanthen-9-one | 273, 317, 387 |
23 | 8.12 | 639.1157 | C27H28O18 | Quercetin glucosyl-glucuronide isomer 2 | 299 |
24 | 8.20 | 589.0826 | C19H26O21 | Unknown 1 | |
25 | 8.28 | 783.1637 | C33H36O22 | Quercetin glucoside derivative | 607, 505, 463, 300, 545 |
26 | 8.48 | 353.0876 | C16H18O9 | Caffeoyl quinic acid | 191, 179 |
27 | 8.63 | 347.0777 | C17H16O8 | Dihydroxy tetramethoxyxanthone | NF |
28 | 8.78 | 655.1288 | C31H28O16 | Acetylated flavonol glycoside isomer 1 | 285, 461, 447 |
29 | 8.86 | 329.0774 | C14H18O9 | Flavonol derivative | 285 |
30 | 8.92 | 655.1292 | C31H28O16 | Acetylated flavonol glycoside isomer 2 | 285, 461 |
31 | 8.96 | 655.1299 | C31H28O16 | Acetylated flavonol glycoside isomer 3 | 285, 461, 447 |
32 | 9.02 | 637.1058 | C27H26O18 | Luteolin diglucuronide | 351, 285 |
33 | 9.10 | 571.1082 | C27H24O14 | Yunnaneic acid E isomer 1 | 197, 285, 135, 527, 241, 329, 439 |
34 | 9.23 | 571.1083 | C27H24O14 | Yunnaneic acid E isomer 2 | 197, 135, 285, 347, 527, 241, 483, 439 |
35 | 9.29 | 539.1189 | C27H24O12 | Yunnaneic acid D | 297, 179, 197, 161, 135, 359 |
36 | 9.35 | 415.1953 | C20H32O9 | Yunnaneic acid derivative 1 | 329, 179, 161, 297 |
37 | 9.47 | 597.1263 | C29H26O14 | Yunnaneic acid F | 197, 135, 329, 179 |
38 | 9.63 | 309.0616 | C14H14O8 | Feruloylmalic acid | 193, 134 |
39 | 9.71 | 555.1157 | C27H24O13 | Salvianolic acid K isomer 1 | 197, 135, 329, 179 |
40 | 9.76 | 585.1273 | C28H26O14 | Naringenin digalloylglucopyranoside isomer 1 | 271 |
41 | 9.79 | 585.1244 | C28H26O14 | Naringenin digalloylglucopyranoside isomer 2 | 271 |
42 | 9.84 | 585.1221 | C28H26O14 | Naringenin digalloylglucopyranoside isomer 3 | 271 |
43 | 9.87 | 461.0740 | C21H18O12 | Luteolin glucuronide | 285 |
44 | 9.95 | 361.0938 | C18H18O8 | Crotepoxide | 273, 241 |
45 | 10.03 | 527.1208 | C26H24O12 | Yunnaneic acid derivative 2 isomer 1 | 135, 197, 179, 285 |
46 | 10.15 | 719.1629 | C36H32O16 | Sagerinic acid | 359, 161, 197, 179 |
47 | 10.24 | 527.1198 | C26H24O12 | Yunnaneic acid derivative 2 isomer 2 | 285, 197, 135, 241, 179, 439 |
48 | 10.33 | 717.1479 | C33H34O18 | Salvianolic acid L | 359, 161, 197 |
49 | 10.49 | 511.1293 | C26H24O11 | Salvianolic acid A hydrate | 269, 197, 135, 179 |
50 | 10.58 | 343.0924 | C22H16O4 | Unknown 2 | |
51 | 10.64 | 555.1153 | C27H24O13 | Salvianolic acid K isomer 2 | 359, 161, 135, 493, 401, 537 |
52 | 10.74 | 711.3987 | C37H60O13 | Hydroxytormentic acid derivative isomer 1 | 503 |
53 | 10.87 | 533.1302 | C25H26O13 | Yunnaneic acid derivative 3 isomer 1 | 197 |
54 | 10.93 | 541.1365 | C27H26O12 | Yunnaneic acid derivative 4 | 197, 509, 135, 179 |
55 | 10.95 | 533.1315 | C25H26O13 | Yunnaneic acid derivative 3 isomer 2 | 197 |
56 | 10.99 | 537.1053 | C27H22O12 | Lithospermic acid A | 295, 161, 359, 135, 197, 493 |
57 | 11.06 | 651.2319 | C31H40O15 | Martynoside | 175, 475 |
58 | 11.17 | 373.0936 | C19H18O8 | Methyl rosmarinate isomer 1 | 197, 161 |
59 | 11.21 | 373.0917 | C19H18O8 | Methyl rosmarinate isomer 2 | 135, 175, 197 |
60 | 11.38 | 711.3966 | C37H60O13 | Hydroxytormentic acid derivative isomer 2 | 503 |
61 | 11.43 | 481.1125 | C25H22O10 | Silybin | 301, 283 |
62 | 11.62 | 493.1144 | C26H22O10 | Salvianolic acid A | 295 |
63 | 11.71 | 479.0992 | C25H20O10 | Dehydrosilybin | 299, 281 |
64 | 11.76 | 491.0985 | C26H20O10 | Salvianolic acid C | 293 |
65 | 11.99 | 327.2151 | C18H32O5 | Trihydroxyoctadecadienoic acid | NF |
66 | 12.19 | 695.4023 | C37H60O12 | Unknown 3 | |
67 | 12.47 | 329.2330 | C18H34O5 | Pinellic acid | NF |
68 | 12.57 | 523.1242 | C27H24O11 | Salvianolic acid derivative | 135, 179, 491, 359 |
69 | 12.77 | 345.1717 | C20H26O5 | Rosmanol isomer 1 | NF |
70 | 13.56 | 307.1909 | C18H28O4 | Unknown 4 | |
71 | 14.20 | 345.1702 | C20H26O5 | Rosmanol isomer 2 | 301, 283 |
72 | 14.32 | 311.2206 | C18H32O4 | Octadecenedioic acid | NF |
73 | 14.74 | 331.1918 | C20H28O4 | Carnosic acid | 287, 244 |
74 | 14.99 | 721.3674 | C34H58O16 | Palmitoleic-linolenicglucoside | 397, 277, 415, 235 |
75 | 15.80 | 293.2116 | C18H30O3 | Hydroxylinolenic acid isomer 1 | NF |
76 | 15.82 | 293.2119 | C18H30O3 | Hydroxylinolenic acid isomer 2 | NF |
77 | 16.39 | 295.2276 | C18H32O3 | Hydroxylinoleic acid | NF |
78 | 16.68 | 455.3168 | C29H44O4 | Diosgenin acetate | NF |
79 | 17.22 | 471.3479 | C30H48O4 | Maslinic acid isomer 1 | NF |
80 | 17.36 | 471.3485 | C30H48O4 | Maslinic acid isomer 2 | NF |
Method | Value |
---|---|
Folin–Ciocalteu (mg GAE/g d.e.) | 166 ± 4 |
FRAP (mmol eq. FeSO4/g d.e.) | 2.6 ± 0.1 |
TEAC (mmol eq. Trolox/g d.e.) | 0.73 ± 0.02 |
ORAC (mmol eq. Trolox/g d.e.) | 0.92 ± 0.03 |
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Vezza, T.; Molina-Tijeras, J.A.; Rodríguez-Nogales, A.; Garrido-Mesa, J.; Cádiz-Gurrea, M.d.l.L.; Segura-Carretero, A.; González-Tejero, M.R.; Rodríguez-Cabezas, M.E.; Gálvez, J.; Algieri, F. The Antioxidant Properties of Salvia verbenaca Extract Contribute to Its Intestinal Antiinflammatory Effects in Experimental Colitis in Rats. Antioxidants 2023, 12, 2071. https://doi.org/10.3390/antiox12122071
Vezza T, Molina-Tijeras JA, Rodríguez-Nogales A, Garrido-Mesa J, Cádiz-Gurrea MdlL, Segura-Carretero A, González-Tejero MR, Rodríguez-Cabezas ME, Gálvez J, Algieri F. The Antioxidant Properties of Salvia verbenaca Extract Contribute to Its Intestinal Antiinflammatory Effects in Experimental Colitis in Rats. Antioxidants. 2023; 12(12):2071. https://doi.org/10.3390/antiox12122071
Chicago/Turabian StyleVezza, Teresa, Jose Alberto Molina-Tijeras, Alba Rodríguez-Nogales, Jose Garrido-Mesa, María de la Luz Cádiz-Gurrea, Antonio Segura-Carretero, María Reyes González-Tejero, María Elena Rodríguez-Cabezas, Julio Gálvez, and Francesca Algieri. 2023. "The Antioxidant Properties of Salvia verbenaca Extract Contribute to Its Intestinal Antiinflammatory Effects in Experimental Colitis in Rats" Antioxidants 12, no. 12: 2071. https://doi.org/10.3390/antiox12122071