Volatile Composition, Antimicrobial Activity, and In Vitro Innate Immunomodulatory Activity of Echinacea purpurea (L.) Moench Essential Oils
Abstract
:1. Introduction
2. Results and Discussion
2.1. Chemical Composition
2.2. Enantiomeric Distribution
2.3. Antimicrobial Activity of E. purpurea EO
2.4. Innate Immunomodulatory Activity of E. purpurea EO and Its Components
3. Materials and Methods
3.1. Materials
3.2. Essential Oil Extraction
3.3. Gas Chromatography-Mass Spectrometry (GC–MS) Analysis
3.4. Gas Chromatography–Flame Ionization Detection (GC–FID) Analysis
3.5. Enantiomeric Analysis by Chiral Gas Chromatography–Mass Spectrometry (CGC–MS)
3.6. Isolation of Human Neutrophils
3.7. Cell Culture
3.8. Ca2+ Mobilization Assay
3.9. Chemotaxis Assay
3.10. Cytotoxicity Assays
3.11. Antimicrobial Activity
3.12. Molecular Modeling
3.13. Statistical Analysis
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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RIexp a | Compound | E1 | E2 | E3 | E4 | E5 | Average | SD |
---|---|---|---|---|---|---|---|---|
881 | 2-Butyl furan | - | - | - | 0.06 | - | 0.06 | - |
924 | α-Thujene | - | - | - | 0.05 | - | 0.05 | - |
932 | α-Pinene | 1.86 | 2.71 | 1.52 | 2.58 | 1.77 | 2.09 | 0.53 |
949 | Camphene | - | - | - | 0.05 | - | 0.05 | - |
971 | Sabinene | 0.28 | 0.54 | 0.26 | 0.48 | 0.28 | 0.37 | 0.13 |
977 | β-Pinene | 1.70 | 2.82 | 1.64 | 2.65 | 1.64 | 2.09 | 0.59 |
988 | Myrcene | 0.62 | 0.86 | 0.76 | 0.73 | 0.57 | 0.71 | 0.12 |
1007 | α-Phellandrene | 8.95 | 11.86 | 8.66 | 12.09 | 8.62 | 10.04 | 1.78 |
1024 | p-Cymene | 1.62 | 3.17 | 1.57 | 3.01 | 1.65 | 2.20 | 0.81 |
1028 | Limonene | 0.40 | 0.63 | 0.44 | 0.56 | 0.39 | 0.48 | 0.11 |
1030 | β-Phellandrene | 0.08 | 0.13 | 0.09 | 0.11 | 0.07 | 0.10 | 0.02 |
1330 | Bicycloelemene | - | - | 0.10 | - | 0.08 | 0.09 | 0.01 |
1335 | δ-Elemene | - | - | 0.08 | 0.07 | - | 0.08 | 0.01 |
1345 | α-Cubebene | - | - | 0.10 | 0.05 | 0.10 | 0.08 | 0.03 |
1367 | α-Ylangene | - | - | 0.14 | - | 0.14 | 0.14 | - |
1374 | α-Copaene | 0.88 | 0.89 | 0.81 | 0.77 | 0.93 | 0.86 | 0.06 |
1386 | β-Cubebene | 0.45 | 0.46 | 0.44 | - | 0.47 | 0.46 | 0.01 |
1388 | β-Elemene | 1.55 | 1.77 | 1.60 | 2.07 | 1.56 | 1.71 | 0.22 |
1405 | β-Maaliene | - | - | - | - | 0.07 | 0.07 | - |
1409 | α-Gurjunene | - | - | - | 0.08 | - | 0.08 | - |
1419 | β-Caryophyllene | 6.31 | 6.57 | 6.23 | 6.60 | 6.52 | 6.45 | 0.17 |
1428 | β-Copaene | 0.78 | 0.61 | 0.66 | - | 0.66 | 0.68 | 0.07 |
1429 | γ-Elemene | - | - | - | 0.16 | - | 0.16 | - |
1431 | trans-α-Bergamotene | 0.62 | 0.61 | 0.55 | 1.02 | 0.62 | 0.68 | 0.19 |
1447 | Z-Muurola-3,5-diene | - | - | 0.09 | 0.09 | 0.12 | 0.10 | 0.02 |
1447 | Isogermacrene D | - | - | - | 0.11 | - | 0.11 | - |
1449 | E-Muurola-3,5-diene | 0.14 | - | 0.14 | 0.12 | 0.12 | 0.13 | 0.01 |
1454 | α-Humulene | 1.90 | 1.91 | 1.85 | 1.86 | 1.83 | 1.87 | 0.03 |
1458 | allo-Aromadendrene | 0.15 | 0.20 | 0.21 | 0.28 | 0.17 | 0.20 | 0.05 |
1460 | Z-Muurola-4(14),5-diene | 0.29 | - | 0.14 | - | 0.27 | 0.23 | 0.08 |
1465 | Z-Cadina-1(6),4-diene | - | 0.23 | - | 0.19 | - | 0.21 | 0.03 |
1472 | Citronellol isobutanoate | 1.03 | 1.23 | 1.44 | 1.09 | - | 1.20 | 0.18 |
1474 | Dodecenol | 0.72 | - | - | - | 0.92 | 0.82 | 0.14 |
1476 | E-Cadina-1(6),4-diene | 0.40 | 0.20 | 0.49 | 0.81 | 0.32 | 0.44 | 0.23 |
1479 | γ-Curcumene | 3.42 | 7.44 | 6.44 | 2.79 | 5.05 | 5.03 | 1.96 |
1484 | Germacrene D | 45.07 | 33.13 | 43.84 | 41.35 | 45.65 | 41.81 | 5.12 |
1488 | β-Selinene | 0.27 | 0.21 | 0.26 | 0.44 | 0.25 | 0.29 | 0.09 |
1492 | 1-Pentadecene | - | 0.81 | - | 0.55 | 1.09 | 0.82 | 0.27 |
1494 | Bicyclogermacrene | 1.73 | 1.55 | 1.53 | 1.93 | 1.20 | 1.59 | 0.27 |
1496 | E-Muurola-4(14),5-diene | 0.54 | 0.41 | 1.16 | 0.23 | - | 0.59 | 0.40 |
1497 | α-Muurolene | 1.19 | 0.91 | 1.33 | - | 1.23 | 1.17 | 0.18 |
1501 | β-Cadinene | 0.18 | 0.13 | 0.20 | 0.24 | 0.17 | 0.18 | 0.04 |
1506 | E,E-α-Farnesene | - | - | 0.09 | - | - | 0.09 | - |
1509 | Shyobunone | 0.17 | 0.18 | 0.88 | 0.10 | 0.07 | 0.28 | 0.34 |
1510 | Cubebol | 0.16 | 0.19 | - | - | - | 0.18 | 0.02 |
1512 | γ-Cadinene | 0.94 | 0.73 | 0.89 | 0.77 | 0.85 | 0.84 | 0.09 |
1517 | δ-Cadinene | 3.89 | 3.03 | 4.14 | 2.99 | 3.34 | 3.48 | 0.52 |
1524 | Isoshyobunone | - | - | - | 0.39 | 0.21 | 0.30 | 0.13 |
1524 | Zonarene | - | - | - | 0.29 | - | 0.29 | - |
1531 | E-Cadina-1,4-diene | 0.20 | 0.16 | 0.21 | - | 0.19 | 0.19 | 0.02 |
1535 | α-Cadinene | 0.27 | 0.21 | 0.23 | 0.23 | 0.23 | 0.23 | 0.02 |
1543 | α-Elemol | 0.12 | 0.16 | - | - | - | 0.14 | 0.03 |
1556 | α-Cadinol | 2.08 | 1.77 | 1.62 | 1.87 | 1.96 | 1.86 | 0.18 |
1557 | Germacrene B | 0.33 | 0.33 | 0.34 | 0.39 | 0.32 | 0.34 | 0.03 |
1560 | E-Nerolidol | 0.66 | 0.56 | 0.58 | 0.41 | 0.58 | 0.56 | 0.09 |
1566 | 1,5-Epoxy salvial-4(14)-ene | 0.42 | 0.39 | 0.28 | 0.41 | 0.39 | 0.38 | 0.06 |
1576 | Germacrene D-4-ol | 1.14 | 1.33 | 0.80 | 1.06 | 1.00 | 1.07 | 0.19 |
1580 | Caryophyllene oxide | 0.82 | 1.14 | 0.60 | 1.63 | 0.75 | 0.99 | 0.41 |
1583 | β-Copaen-4-α-ol | 0.23 | 0.23 | 0.19 | - | 0.23 | 0.22 | 0.02 |
1591 | Salvial-4(14)-en-1-one | 0.27 | 0.23 | 0.19 | 0.28 | 0.28 | 0.25 | 0.04 |
1608 | Humulene epoxide II | 0.30 | 0.35 | 0.11 | 0.29 | 0.18 | 0.25 | 0.10 |
1616 | Junenol | 0.38 | 0.32 | - | - | - | 0.35 | 0.04 |
1621 | Widdrol isomer | 0.25 | 0.31 | 0.29 | - | 0.39 | 0.31 | 0.06 |
1626 | 1-epi-Cubenol | 0.20 | 0.17 | 0.14 | - | 0.17 | 0.17 | 0.02 |
1641 | δ-Cadinol | 0.33 | 0.24 | 0.16 | - | - | 0.24 | 0.09 |
1642 | τ-Cadinol | - | - | - | - | 0.60 | 0.60 | - |
1644 | τ-Muurolol | - | - | - | - | 0.96 | 0.96 | - |
1646 | epi-α-Cadinol | 0.73 | 0.57 | 0.58 | 0.60 | - | 0.62 | 0.07 |
1649 | epi-α-Muurolol | 0.83 | 0.62 | 0.76 | 0.75 | - | 0.74 | 0.09 |
1653 | Eudesm-4(15),7-dien-1 a-ol | 0.08 | 0.20 | - | - | - | 0.14 | 0.08 |
1657 | 7E-Tetradecenol | - | 0.16 | - | - | - | 0.16 | - |
1679 | epi-α-Bisabolol | - | 0.13 | - | - | - | 0.13 | - |
1679 | Germacra-4(15),5,10(14)-trien-1-α-ol | 0.22 | 0.13 | - | - | - | 0.18 | 0.06 |
1685 | Germacra-4(15),5,10(14)-trien-1-β-ol | 0.21 | 0.18 | - | - | - | 0.20 | 0.02 |
1688 | Shyobunol | 1.26 | 1.64 | - | - | - | 1.45 | 0.27 |
1773 | 14-oxy-α-Muurolene | - | - | - | 0.10 | - | 0.10 | - |
1828 | Z-Thujopsenic acid | 0.26 | 0.26 | 0.14 | 0.37 | 0.27 | 0.26 | 0.08 |
1839 | Phytone | 0.12 | 0.15 | 0.08 | 0.13 | 0.15 | 0.13 | 0.03 |
2293 | Tricosane | - | - | - | 0.03 | - | 0.03 | - |
2493 | Pentacosane | - | - | - | 0.04 | - | 0.04 | - |
2692 | Heptacosane | - | - | - | 0.05 | - | 0.05 | - |
2891 | Nonacosane | - | - | - | 0.03 | - | 0.03 | - |
Unidentified | 0.00 | 1.94 | 1.93 | 1.52 | 2.35 |
Chiral Compounds | Average (%) | SD | |
---|---|---|---|
(+) | (−) | ||
α-Pinene | 4.11 | 95.89 | 2.71 |
Sabinene | 20.43 | 79.57 | 4.15 |
β-Pinene | 1.23 | 98.77 | 0.41 |
α-Phellandrene | 100.00 | 0.00 | 0.00 |
Limonene | 49.21 | 50.79 | 10.80 |
α-Copaene | 100.00 | 0.00 | 0.00 |
β-Phellandrene | 48.37 | 51.63 | 0.10 |
β-Elemene | 23.30 | 76.70 | 1.24 |
β-Caryophyllene | 0.00 | 100.00 | 0.00 |
Germacrene D | 9.50 | 90.50 | 2.45 |
δ-Cadinene | 98.60 | 1.40 | 0.82 |
Bacterial Species | MIC (μg/mL) |
---|---|
Citrobacter freundii | 312.5 ± 0.49 |
Escherichia coli | 625.0 ± 0.32 |
Klebsiella pneumoniae | 312.5 ± 0.34 |
Bacillus cereus | 312.5 ± 0.43 |
Pseudomonas aeruginosa | 312.5 ± 0.44 |
Shigella flexneri | 312.5 ± 0.14 |
Staphylococcus aureus | 1250.0 ± 0.28 |
Stroptococcus pyogenes | 625.0 ± 0.21 |
Alcaligenes faecalis | 312.5 ± 0.38 |
Staphylococcus epidermidis | 625.0 ± 0.29 |
Shigella sonnei | 312.5 ± 0.24 |
Enterococcus faecalis | 312.5 ± 0.30 |
Essential Oil or Pure Compound | Activation of [Ca2+]i | Inhibition of fMLF-Induced [Ca2+]i | Chemotaxis | Cytotoxicity (at 24 h) | Cytotoxicity (at 90 min) |
---|---|---|---|---|---|
EC50 (μg/mL) | IC50 (μg/mL) | IC50 (μg/mL) | IC50 (μg/mL) | ||
Echinacea EO | 19.9 ± 4.5 | 1.8 ± 0.6 | 1.7 ± 0.7 | 25–30% (at 50 μg/mL) | n.t. |
EC50 (μM) | IC50 (μM) | IC50 (μM) | IC50 (μM) | ||
β-Caryophyllene | N.A. | 0.13 ± 0.02 | 17.6 ± 5.7 * | n.t. | n.t. |
(+)-δ-Cadinene | 24.6 ± 6.7 | 0.48 ± 0.1 | 7.2 ± 1.6 | n.t. | n.t. |
α-Phellandrene | 20.8 ± 7.5 | 7.9 ± 1.1 | 19.4 ± 1.5 | 35% at 50 μM | n.t. |
Germacrene D | 21.7 ± 7.1 | 1.9 ± 0.1 | 5.4 ± 2.3 * | n.t. | n.t. |
Rank | PDB ID | Target Name | Fit Score |
---|---|---|---|
1 | 1J96 | Aldo-keto reductase family 1 member C2 | 2.974 |
2 | 1REU | Bone morphogenetic protein 2 | 2.948 |
3 | 1PME | Mitogen-activated protein kinase 1 | 2.918 |
4 | 1P49 | Steryl-sulfatase | 2.905 |
5 | 1F40 | Peptidyl-prolyl cis-trans isomerase FKBP1A | 2.901 |
6 | 1E7E | Serum albumin | 2.874 |
7 | 1SHJ | Caspase-7 | 2.842 |
8 | 2PIN | Thyroid hormone receptor beta | 2.837 |
9 | 2P3G | MAP kinase-activated protein kinase 2 | 2.804 |
10 | 1L6L | Apolipoprotein A-II | 2.763 |
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Dosoky, N.S.; Kirpotina, L.N.; Schepetkin, I.A.; Khlebnikov, A.I.; Lisonbee, B.L.; Black, J.L.; Woolf, H.; Thurgood, T.L.; Graf, B.L.; Satyal, P.; et al. Volatile Composition, Antimicrobial Activity, and In Vitro Innate Immunomodulatory Activity of Echinacea purpurea (L.) Moench Essential Oils. Molecules 2023, 28, 7330. https://doi.org/10.3390/molecules28217330
Dosoky NS, Kirpotina LN, Schepetkin IA, Khlebnikov AI, Lisonbee BL, Black JL, Woolf H, Thurgood TL, Graf BL, Satyal P, et al. Volatile Composition, Antimicrobial Activity, and In Vitro Innate Immunomodulatory Activity of Echinacea purpurea (L.) Moench Essential Oils. Molecules. 2023; 28(21):7330. https://doi.org/10.3390/molecules28217330
Chicago/Turabian StyleDosoky, Noura S., Liliya N. Kirpotina, Igor A. Schepetkin, Andrei I. Khlebnikov, Brent L. Lisonbee, Jeffrey L. Black, Hillary Woolf, Trever L. Thurgood, Brittany L. Graf, Prabodh Satyal, and et al. 2023. "Volatile Composition, Antimicrobial Activity, and In Vitro Innate Immunomodulatory Activity of Echinacea purpurea (L.) Moench Essential Oils" Molecules 28, no. 21: 7330. https://doi.org/10.3390/molecules28217330