Essential Oils of Gardenia jasminoides J. Ellis and Gardenia jasminoides f. longicarpa Z.W. Xie & M. Okada Flowers: Chemical Characterization and Assessment of Anti-Inflammatory Effects in Alveolar Macrophage
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Material, Essential Oil Preparation, and Chemicals
2.2. Identification of the Constituents of the Essential Oil
2.3. Cell Culture and Chemical Treatment
2.4. Cell Viability Assay
2.5. Measurement of Nitric Oxide Levels, PGE2, and TNF-α
2.6. Statistical Analysis
3. Result
3.1. The Main Constituents of the Gardenia Flower Essential Oils
3.2. Effects of Gardenia Essential Oils on the Viability of MH-S Cells
3.3. Effects of Gardenia Essential Oils on the NO, TNF-α, and PGE2 Secretion of MH-S Cells
3.4. Anti-Inflammatory Effects of Two Main Ingredients of Gardenia Essential Oils
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Barnes, P.J. Chronic obstructive pulmonary disease. In Reference Module in Biomedical Sciences; Elsevier: Amsterdam, Netherlands, 2014. [Google Scholar] [CrossRef]
- Chan, K.Y.; Li, X.; Chen, W.; Song, P.; Wong, N.W.K.; Poon, A.N.; Jian, W.; Soyiri, I.N.; Cousens, S.; Adeloye, D.; et al. Prevalence of chronic obstructive pulmonary disease (COPD) in China in 1990 and 2010. J. Glob. Health 2017, 7, 020704. [Google Scholar] [CrossRef] [PubMed]
- Vlahos, R.; Bozinovski, S. Role of alveolar macrophages in chronic obstructive pulmonary disease. Front. Immunol. 2014, 5, 435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, D.; He, S.; Liu, B.; Liu, C. MiR-27-3p regulates TLR2/4-dependent mouse alveolar macrophage activation by targetting PPARgamma. Clin. Sci. 2018, 132, 943–958. [Google Scholar] [CrossRef]
- Thammason, H.; Khetkam, P.; Pabuprapap, W.; Suksamrarn, A.; Kunthalert, D. Ethyl rosmarinate inhibits lipopolysaccharide-induced nitric oxide and prostaglandin E2 production in alveolar macrophages. Eur. J. Pharmacol. 2018, 824, 17–23. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Xiao, C.; Liang, Y.; Weng, Z.; Yang, W. Research Advances in COPD Drugs and Novel Targets. Nano LIFE 2021, 11, 2140008. [Google Scholar] [CrossRef]
- Knobloch, J.; Hag, H.; Jungck, D.; Urban, K.; Koch, A. Resveratrol impairs the release of steroid-resistant cytokines from bacterial endotoxin-exposed alveolar macrophages in chronic obstructive pulmonary disease. Basic Clin. Pharmacol. Toxicol. 2011, 109, 138–143. [Google Scholar] [CrossRef]
- Jiang, Z.; Zhu, L. Update on molecular mechanisms of corticosteroid resistance in chronic obstructive pulmonary disease. Pulm. Pharmacol. Ther. 2016, 37, 1–8. [Google Scholar] [CrossRef]
- Valente, J.; Zuzarte, M.; Liberal, J.; Goncalves, M.J.; Lopes, M.C.; Cavaleiro, C.; Cruz, M.T.; Salgueiro, L. Margotia gummifera essential oil as a source of anti-inflammatory drugs. Ind. Crop. Prod. 2013, 47, 86–91. [Google Scholar] [CrossRef]
- Bigliani, M.C.; Rossetti, V.; Grondona, E.; Lo Presti, S.; Paglini, P.M.; Rivero, V.; Zunino, M.P.; Ponce, A.A. Chemical compositions and properties of Schinus areira L. essential oil on airway inflammation and cardiovascular system of mice and rabbits. Food Chem. Toxicol. 2012, 50, 2282–2288. [Google Scholar] [CrossRef]
- Cardia, G.F.E.; Silva-Filho, S.E.; Silva, E.L.; Uchida, N.S.; Cavalcante, H.A.O.; Cassarotti, L.L.; Salvadego, V.E.C.; Spironello, R.A.; Bersani-Amado, C.A.; Cuman, R.K.N. Effect of lavender (Lavandula angustifolia) essential oil on acute inflammatory response. Evid. Based Complement. Altern. 2018, 2018, 1413940. [Google Scholar] [CrossRef] [Green Version]
- Wu, Y.N.; Xu, Y.; Yao, L. Anti-inflammatory and anti-allergic effects of German chamomile (Matricaria chamomilla L.). J. Essent. Oil Bear. Plants 2012, 15, 75–83. [Google Scholar] [CrossRef]
- Pimentel, S.P.; Barrella, G.E.; Casarin, R.C.V.; Cirano, F.R.; Casati, M.Z.; Foglio, M.A.; Figueira, G.M.; Ribeiro, F.V. Protective effect of topical Cordia verbenacea in a rat periodontitis model: Immune-inflammatory, antibacterial and morphometric assays. BMC Complement. Altern. Med. 2012, 12, 224. [Google Scholar] [CrossRef] [Green Version]
- Moraes, T.M.; Kushima, H.; Moleiro, F.C.; Santos, R.C.; Rocha, L.R.M.; Marques, M.O.; Vilegas, W.; Hiruma-Lima, C.A. Effects of limonene and essential oil from Citrus aurantium on gastric mucosa: Role of prostaglandins and gastric mucus secretion. Chem.-Biol. Interact. 2009, 180, 499–505. [Google Scholar] [CrossRef]
- Rufino, A.T.; Ribeiro, M.; Judas, F.; Salgueiro, L.; Lopes, M.C.; Cavaleiro, C.; Mendes, A.F. Anti-inflammatory and chondroprotective activity of (+)-alpha-pinene: Structural and enantiomeric selectivity. J. Nat. Prod. 2014, 77, 264–269. [Google Scholar] [CrossRef]
- Peana, A.T.; D’Aquila, P.S.; Panin, F.; Serra, G.; Pippia, P.; Moretti, M.D.L. Anti-inflammatory activity of linalool and linalyl acetate constituents of essential oils. Phytomedicine 2002, 9, 721–726. [Google Scholar] [CrossRef]
- Ma, J.Q.; Xu, H.; Wu, J.; Qu, C.F.; Sun, F.L.; Xu, S.D. Linalool inhibits cigarette smoke-induced lung inflammation by inhibiting NF-kappa B activation. Int. J. Immunopharmacol. 2015, 29, 708–713. [Google Scholar] [CrossRef] [PubMed]
- Arigesavan, K.; Sudhandiran, G. Carvacrol exhibits anti-oxidant and anti-inflammatory effects against 1, 2-dimethyl hydrazine plus dextran sodium sulfate induced inflammation associated carcinogenicity in the colon of Fischer 344 rats. Biochem. Biophys. Res. Commun. 2015, 461, 314–320. [Google Scholar] [CrossRef]
- Ehrnhofer-Ressler, M.M.; Fricke, K.; Pignitter, M.; Walker, J.M.; Walker, J.; Rychlik, M.; Somoza, V. Identification of 1,8-cineole, borneol, camphor, and thujone as anti-inflammatory compounds in a Salvia officinalis L. infusion using human gingival fibroblasts. J. Agr. Food Chem. 2013, 61, 3451–3459. [Google Scholar] [CrossRef] [PubMed]
- Rocha, N.F.M.; de Oliveira, G.V.; de Araujo, F.Y.R.; Rios, E.R.V.; Carvalho, A.M.R.; Vasconcelos, L.F.; Macedo, D.S.; Soares, P.M.G.; De Sousa, D.P.; de Sousa, F.C.F. (-)-alpha-Bisabolol-induced gastroprotection is associated with reduction in lipid peroxidation, superoxide dismutase activity and neutrophil migration. Eur. J. Pharm. Sci. 2011, 44, 455–461. [Google Scholar] [CrossRef] [PubMed]
- Juergens, L.J.; Racké, K.; Tuleta, I.; Stoeber, M.; Juergens, U.R. Anti-inflammatory effects of 1,8-cineole (eucalyptol) improve glucocorticoid effects in vitro: A novel approach of steroid-sparing add-on therapy for COPD and asthma? Synergy 2017, 5, 1–8. [Google Scholar] [CrossRef]
- Shen, Y.; Sun, Z.; Guo, X. Citral inhibits lipopolysaccharide-induced acute lung injury by activating PPAR-gamma. Eur. J. Pharmacol. 2015, 747, 45–51. [Google Scholar] [CrossRef] [PubMed]
- Ballabeni, V.; Tognolini, M.; Giorgio, C.; Bertoni, S.; Bruni, R.; Barocelli, E. Ocotea quixos Lam. essential oil: In vitro and in vivo investigation on its anti-inflammatory properties. Fitoterapia 2010, 81, 289–295. [Google Scholar] [CrossRef]
- Rogerio, A.P.; Andrade, E.L.; Leite, D.F.P.; Figueiredo, C.P.; Calixto, J.B. Preventive and therapeutic anti-inflammatory properties of the sesquiterpene alpha-humulene in experimental airways allergic inflammation. Br. J. Pharmacol. 2009, 158, 1074–1087. [Google Scholar] [CrossRef] [Green Version]
- Boskabady, M.H.; Mahtaj, L.G. Lung inflammation changes and oxidative stress induced by cigarette smoke exposure in guinea pigs affected by Zataria multiflora and its constituent, carvacrol. BMC Complement. Altern. Med. 2015, 15, 39. [Google Scholar] [CrossRef] [Green Version]
- Mamber, S.W.; Gurel, V.; Lins, J.; Ferri, F.; Beseme, S.; McMichael, J. Effects of cannabis oil extract on immune response gene expression in human small airway epithelial cells (HSAEpC): Implications for chronic obstructive pulmonary disease (COPD). J. Cannabis Res. 2020, 2, 5. [Google Scholar] [CrossRef] [Green Version]
- Hsieh, Y.S.; Shin, Y.K.; Han, A.Y.; Kwon, S.; Seol, G.H. Linalyl acetate prevents three related factors of vascular damage in COPD-like and hypertensive rats. Life Sci. 2019, 232, 116608. [Google Scholar] [CrossRef]
- Worth, H.; Schacher, C.; Dethlefsen, U. Concomitant therapy with Cineole (Eucalyptole) reduces exacerbations in COPD: A placebo-controlled double-blind trial. Respir. Res. 2009, 10, 69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ni, Y.; Li, L.; Zhang, W.; Lu, D.; Zang, C.; Zhang, D.; Yu, Y.; Yao, X. Discovery and LC-MS characterization of new crocins in gardeniae fructus and their neuroprotective potential. J. Agric. Food Chem. 2017, 65, 2936–2946. [Google Scholar] [CrossRef] [PubMed]
- Lu, D.; Zhang, W.Y.; Jiang, Y.N.; Zhang, Y.; Pan, D.B.; Zhang, D.; Yao, X.S.; Yu, Y. Two new triterpenoids from Gardenia jasminoides fruits. Nat. Prod. Res. 2019, 33, 2789–2794. [Google Scholar] [CrossRef]
- Ma, W.-W.; Tao, Y.; Wang, Y.-Y.; Peng, I.F. Effects of Gardenia jasminoides extracts on cognition and innate immune response in an adult Drosophila model of Alzheimer’s disease. Chin. J. Nat. Med. 2017, 15, 899–904. [Google Scholar] [CrossRef]
- Jia, Q.; Huang, B.; Liu, L.; Gong, B.; Zhu, P. The populationdynamics of root-knot nematode and its effect on soil microenvironment in the Gardania jasminoides ‘Longicarpa’ plantation. South Chin. Forest Sci. 2019, 47, 33–36. [Google Scholar] [CrossRef]
- Khalid, K.A.; Essa, E.F.; Ismaiel, H.M.H.; Elsayed, A.A.A. Effects of geographical locations on essential oil composition of navel orange leaves and flowers. J. Essent. Oil Bear. Plants 2020, 23, 139–148. [Google Scholar] [CrossRef]
- Riccardo, N.; Maria, G.A. Citrus bergamia, Risso: The peel, the juice and the seed oil of the bergamot fruit of Reggio Calabria (South Italy). Emir. J. Food Agric. 2020, 32, 522–532. [Google Scholar] [CrossRef]
- Giuffrè, A.M.; Labate, M.L.C.; Ursino, D.; Gioffrè, G. The peel essential oil composition of bergamot fruit (Citrus bergamia, Risso) of Reggio Calabria (Italy): A review. Emir. J. Food Agric. 2020, 32, 835–845. [Google Scholar] [CrossRef]
- Inan, M.; Kirpik, M.; Kaya, D.A.; Kirici, S. Effect of harvest time on essential oil composition of Thymbra spicata L. growing in flora of Adyaman. Adv. Environ. Biol. 2011, 5, 356–358. [Google Scholar]
- Alizadeh, A.; Khoshkhui, M.; Javidnia, K.; Firuzi, O.; Khalighi, A. Effects of fertilizer on yield, essential oil composition, total phenolic content and antioxidant activity in Satureja hortensis L. (Lamiaceae) cultivated in Iran. J. Med. Plants Res. 2010, 4, 33–40. [Google Scholar]
- Chaichana, J.; Niwatananun, W.; Somna, S.; Vejabhikul, S.; Chansakaow, S. Volatile constituents and biological activities of Gardenia jasminoides. J. Health Res. 2009, 23, 141–145. [Google Scholar]
- Zhang, N.; Luo, M.; He, L.; Yao, L. Chemical composition of essential oil from flower of ‘Shanzhizi’ (Gardenia jasminoides Ellis) and involvement of serotonergic system in its anxiolytic effect. Molecules 2020, 25, 4702. [Google Scholar] [CrossRef]
- Cai, Y.M.; Cui, X.F.; Liu, Y.Y. Summary of research on materia medica in southern Yunnan. J. Med. Pharm. Chin. Min. 1997, S1, 90–91. [Google Scholar]
- Ma, T.T.; Li, X.F.; Li, W.X.; Yang, Y.; Huang, C.; Meng, X.M.; Zhang, L.; Li, J. Geniposide alleviates inflammation by suppressing MeCP2 in mice with carbon tetrachloride-induced acute liver injury and LPS-treated THP-1 cells. Int. Immunopharmacol. 2015, 29, 739–747. [Google Scholar] [CrossRef]
- Yu, Y.; Xie, Z.-L.; Gao, H.; Ma, W.-W.; Dai, Y.; Wang, Y.; Zhong, Y.; Yao, X.-S. Bioactive Iridoid Glucosides from the Fruit of Gardenia jasminoides. J. Nat. Prod. 2009, 72, 1459–1464. [Google Scholar] [CrossRef] [PubMed]
- Xiao, W.; Li, S.; Wang, S.; Ho, C.T. Chemistry and bioactivity of Gardenia jasminoides. J. Food Drug Anal. 2017, 25, 43–61. [Google Scholar] [CrossRef] [Green Version]
- Avoseh, N.O.; Lawal, O.A.; Ogunwande, I.A.; Ascrizzi, R.; Elizabeth, A. In vivo anti-inflammatory and anti-nociceptive activities, and chemical constituents of essential oil from the leaf of Gardenia jasminoides J. Ellis (Rubiaceae). Trends Phytochem. Res. 2020, 4, 203–212. [Google Scholar]
- Zhang, N.; Yao, L. Anxiolytic effect of essential oils and their constituents: A review. J. Agric. Food Chem. 2019, 67, 13790–13808. [Google Scholar] [CrossRef] [PubMed]
- Hao, J.R.; Yao, L.; Yuan, G.X.; Zhu, J.W. Comparison on the biological character and the composition of essential oil from lavender for essential oil and for ornamental. J. Shanghai Jiaotong Univ. 2006, 24, 146–151. [Google Scholar]
- Al Faraj, A.; Shaik, A.S.; Afzal, S.; Al Sayed, B.; Halwani, R. MR imaging and targeting of a specific alveolar macrophage subpopulation in LPS-induced COPD animal model using antibody-conjugated magnetic nanoparticles. Int. J. Nanomed. 2014, 9, 1491–1503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, M.G.; Kim, S.M.; Min, J.H.; Kwon, O.K.; Park, M.H.; Park, J.W.; Ahn, H.I.; Hwang, J.Y.; Oh, S.R.; Lee, J.W.; et al. Anti-inflammatory effects of linalool on ovalbumin-induced pulmonary inflammation. Int. Immunopharmacol. 2019, 74, 9. [Google Scholar] [CrossRef] [PubMed]
- Batista, P.A.; Werner, M.F.D.; Oliveira, E.C.; Burgos, L.; Pereira, P.; Brum, L.F.D.; Story, G.M.; Santos, A.R.S. The antinociceptive effect of (-)-linalool in models of chronic inflammatory and neuropathic hypersensitivity in mice. J. Pain 2010, 11, 1222–1229. [Google Scholar] [CrossRef]
- Peana, A.T.; Marzocco, S.; Popolo, A.; Pinto, A. (-)-Linalool inhibits in vitro NO formation: Probable involvement in the antinociceptive activity of this monoterpene compound. Life Sci. 2006, 78, 719–723. [Google Scholar] [CrossRef] [PubMed]
- Du, Y.H.; Feng, R.Z.; Li, Q.; Wei, Q.; Yin, Z.Q.; Zhou, L.J.; Tao, C.; Jia, R.Y. Anti-inflammatory activity of leaf essential oil from Cinnamomum longepaniculatum (Gamble) N. Chao. Int. J. Clin. Exp. Med. 2014, 7, 5612–5620. [Google Scholar]
- Raymundo, L.J.; Guilhon, C.C.; Alviano, D.S.; Matheus, M.E.; Antoniolli, A.R.; Cavalcanti, S.C.; Alves, P.B.; Alviano, C.S.; Fernandes, P.D. Characterisation of the anti-inflammatory and antinociceptive activities of the Hyptis pectinata (L.) Poit essential oil. J. Ethnopharmacol. 2011, 134, 725–732. [Google Scholar] [CrossRef] [PubMed]
- Sun, Z.; Wang, H.; Wang, J.; Zhou, L.; Yang, P. Chemical composition and anti-Inflammatory, cytotoxic and antioxidant activities of essential oil from leaves of Mentha piperita grown in China. PLoS ONE 2014, 9, e114767. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tung, Y.T.; Yen, P.L.; Lin, C.Y.; Chang, S.T. Anti-inflammatory activities of essential oils and their constituents from different provenances of indigenous cinnamon (Cinnamomum osmophloeum) leaves. Pharm. Biol. 2010, 48, 1130–1136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xian, Y.F.; Li, Y.C.; Ip, S.P.; Lin, Z.X.; Lai, X.P.; Su, Z.R. Anti-inflammatory effect of patchouli alcohol isolated from Pogostemonis Herba in LPS-stimulated RAW264.7 macrophages. Exp. Ther. Med. 2011, 2, 545–550. [Google Scholar] [CrossRef] [PubMed] [Green Version]
No. | Retention Time (min) | Name | Peak Area (%) | |
---|---|---|---|---|
GJE | GJLE | |||
1 | 14.35 | Linalool | 34.65 | 6.56 |
2 | 17.19 | α-Terpineol | 6.27 | 2.40 |
3 | 18.41 | Nerol | 1.96 | 0.64 |
4 | 19.66 | Geraniol | 5.79 | 1.93 |
5 | 21.78 | cis-3-Hexenyl tiglate | 3.13 | 8.02 |
6 | 21.99 | Hexyl tiglate | 2.39 | 1.23 |
7 | 28.00 | α-Farnesene | 10.24 | 32.45 |
8 | 28.34 | Octyl (E)-2-methylbut-2-enoate | 0.70 | 0.52 |
9 | 29.50 | (+)-trans-Nerolidol | - | 0.53 |
10 | 29.66 | 3-Hexen-1-ol, benzoate, (Z)- | - | 1.76 |
11 | 29.82 | Benzoic acid, hexyl ester | - | 0.66 |
12 | 29.92 | (3E,7E)-4,8,12-Trimethyltrideca-1,3,7,11-tetraene | - | 0.90 |
13 | 31.79 | tau-Cadinol | 1.77 | 2.40 |
14 | 32.17 | α-Cadinol | 0.68 | 0.74 |
15 | 32.30 | α-Terpinyl acetate | 1.19 | - |
16 | 33.51 | Geranyl angelate | 1.89 | 0.55 |
17 | 36.57 | 8-Hydroxylinalool | 1.67 | 1.23 |
18 | 40.67 | Cembrene A | 5.77 | 0.97 |
19 | 40.86 | Verticillol | 1.01 | 0.97 |
20 | 41.55 | n-Hexadecanoic acid | 1.33 | 5.70 |
21 | 42.10 | 3,7,11,15-Tetramethylhexadeca-1,6,10,14-tetraen-3-ol | - | 1.17 |
22 | 45.10 | Benzoic acid, [(E,E)-3,7,11-trimethyl-2,6,10-dodecatrien-1-yl] ester | - | 1.11 |
23 | 45.87 | trans-Geranylgeraniol | - | 1.03 |
24 | 45.69 | 9,12-Octadecadienoic acid (Z,Z)- | - | 1.44 |
25 | 48.44 | Tricosane | 1.93 | 0.90 |
26 | 52.66 | Pentacosane | 2.96 | 3.68 |
27 | 56.37 | Heptacosane | - | 0.53 |
28 | 58.77 | Squalene | - | 0.64 |
Sum | 85.33 | 72.64 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, N.; Bian, Y.; Yao, L. Essential Oils of Gardenia jasminoides J. Ellis and Gardenia jasminoides f. longicarpa Z.W. Xie & M. Okada Flowers: Chemical Characterization and Assessment of Anti-Inflammatory Effects in Alveolar Macrophage. Pharmaceutics 2022, 14, 966. https://doi.org/10.3390/pharmaceutics14050966
Zhang N, Bian Y, Yao L. Essential Oils of Gardenia jasminoides J. Ellis and Gardenia jasminoides f. longicarpa Z.W. Xie & M. Okada Flowers: Chemical Characterization and Assessment of Anti-Inflammatory Effects in Alveolar Macrophage. Pharmaceutics. 2022; 14(5):966. https://doi.org/10.3390/pharmaceutics14050966
Chicago/Turabian StyleZhang, Nan, Ying Bian, and Lei Yao. 2022. "Essential Oils of Gardenia jasminoides J. Ellis and Gardenia jasminoides f. longicarpa Z.W. Xie & M. Okada Flowers: Chemical Characterization and Assessment of Anti-Inflammatory Effects in Alveolar Macrophage" Pharmaceutics 14, no. 5: 966. https://doi.org/10.3390/pharmaceutics14050966
APA StyleZhang, N., Bian, Y., & Yao, L. (2022). Essential Oils of Gardenia jasminoides J. Ellis and Gardenia jasminoides f. longicarpa Z.W. Xie & M. Okada Flowers: Chemical Characterization and Assessment of Anti-Inflammatory Effects in Alveolar Macrophage. Pharmaceutics, 14(5), 966. https://doi.org/10.3390/pharmaceutics14050966