Ethyl Acetate Fractions of Papaver rhoeas L. and Papaver nudicaule L. Exert Antioxidant and Anti-Inflammatory Activities
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and Sample Preparation
2.2. Cell Culture and Reagents
2.3. Cell Viability Assays
2.4. Nitric Oxide Assays
2.5. 2,2-Diphenyl-1-picrylhydrazyl (DPPH) Free Radical Scavenging Activity
2.6. GSH/GSSG Ratio
2.7. Measurement of Intracellular ROS
2.8. Real-Time Quantitative PCR
2.9. Preparation of Nuclear and Cytosolic Extracts
2.10. Western Blotting Analysis
2.11. Enzyme-Linked Immunosorbent Assay (ELISA) Assays
2.12. Statistical Analysis
2.13. Investigation and Identification of Bioactivity-Specific Metabolites
3. Results
3.1. EtOAc Fractions of P. nudicaule and P. rhoeas Reduce the LPS-Induced NO and PGE2
3.2. EtOAc Fractions of P. nudicaule and P. rhoeas Reduced LPS-Induced Inflammatory Cytokines and Inhibited the LPS-Mediated Activation of NF-κB and STAT3
3.3. EtOAc Fractions of P. nudicaule and P. rhoeas Reduce Oxidative Stress
3.4. EtOAc Fractions of P. nudicaule and P. rhoeas Increases the Expression of Antioxidant Regulators by Activating Nrf2
3.5. Investigation and Identification of Bioactivity-Specific Metabolites
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Simpson, J.L.; Phipps, S.; Gibson, P.G. Inflammatory mechanisms and treatment of obstructive airway diseases with neutrophilic bronchitis. Pharmacol. Ther. 2009, 124, 86–95. [Google Scholar] [CrossRef] [PubMed]
- Bone, R.C.; Grodzin, C.J.; Balk, R.A. Sepsis: A new hypothesis for pathogenesis of the disease process. Chest 1997, 112, 235–243. [Google Scholar] [CrossRef] [PubMed]
- Rock, K.L.; Kono, H. The inflammatory response to cell death. Annu. Rev. Pathol. 2008, 3, 99–126. [Google Scholar] [CrossRef] [PubMed]
- Kaplan, M.J. Management of cardiovascular disease risk in chronic inflammatory disorders. Nat. Rev. Rheumatol. 2009, 5, 208–217. [Google Scholar] [CrossRef]
- Amor, S.; Peferoen, L.A.; Vogel, D.Y.; Breur, M.; van der Valk, P.; Baker, D.; van Noort, J.M. Inflammation in neurodegenerative diseases—An update. Immunology 2014, 142, 151–166. [Google Scholar] [CrossRef]
- Murray, P.J.; Wynn, T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11, 723–737. [Google Scholar] [CrossRef]
- Jones, D.P. Redefining oxidative stress. Antioxid. Redox Signal. 2006, 8, 1865–1879. [Google Scholar] [CrossRef]
- Brune, B.; Dehne, N.; Grossmann, N.; Jung, M.; Namgaladze, D.; Schmid, T.; von Knethen, A.; Weigert, A. Redox control of inflammation in macrophages. Antioxid. Redox Signal. 2013, 19, 595–637. [Google Scholar] [CrossRef] [Green Version]
- Loboda, A.; Damulewicz, M.; Pyza, E.; Jozkowicz, A.; Dulak, J. Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: An evolutionarily conserved mechanism. Cell. Mol. Life Sci. 2016, 73, 3221–3247. [Google Scholar] [CrossRef] [Green Version]
- De, S.; Manna, A.; Kundu, S.; De Sarkar, S.; Chatterjee, U.; Sen, T.; Chattopadhyay, S.; Chatterjee, M. Allylpyrocatechol Attenuates Collagen-Induced Arthritis via Attenuation of Oxidative Stress Secondary to Modulation of the MAPK, JAK/STAT, and Nrf2/HO-1 Pathways. J. Pharmacol. Exp. Ther. 2017, 360, 249–259. [Google Scholar] [CrossRef] [Green Version]
- Huang, Y.; Li, W.; Su, Z.Y.; Kong, A.N. The complexity of the Nrf2 pathway: Beyond the antioxidant response. J. Nutr. Biochem. 2015, 26, 1401–1413. [Google Scholar] [CrossRef]
- Bujak, T.; Zagorska-Dziok, M.; Ziemlewska, A.; Niziol-Lukaszewska, Z.; Wasilewski, T.; Hordyjewicz-Baran, Z. Antioxidant and Cytoprotective Properties of Plant Extract from Dry Flowers as Functional Dyes for Cosmetic Products. Molecules 2021, 26, 2809. [Google Scholar] [CrossRef]
- Selen Isbilir, S.; Sagiroglu, A. An Assessment of In Vitro Antioxidant Activities of Different Extracts from Papaver rhoeas L. Leaves. Int. J. Food Prop. 2012, 15, 1300–1308. [Google Scholar] [CrossRef] [Green Version]
- Kalav, Y.N.; Sariyar, G. Alkaloids from Turkish Papaver rhoeas. Planta Med. 1989, 55, 488. [Google Scholar] [CrossRef]
- Çoban, İ.; Toplan, G.G.; Özbek, B.; Gürer Ç, U.; Sarıyar, G. Variation of alkaloid contents and antimicrobial activities of Papaver rhoeas L. growing in Turkey and northern Cyprus. Pharm. Biol. 2017, 55. [Google Scholar] [CrossRef] [Green Version]
- El, S.N.; Karakaya, S. Radical scavenging and iron-chelating activities of some greens used as traditional dishes in Mediterranean diet. Int. J. Food Sci. Nutr. 2004, 55, 67–74. [Google Scholar]
- Huang, Z.; He, J.; Xia, D.; Zhong, X.-J.; Li, X.; Sun, L.-X.; Cai, S.-Z. Evaluation of physiological responses and tolerance to low-temperature stress of four Iceland poppy (Papaver nudicaule) varieties. J. Plant. Interact. 2016, 11, 117–123. [Google Scholar] [CrossRef] [Green Version]
- Hedrick, U.P. Sturtevant’s Edible Plants of the World; Southwest School of Botanical Medicine: Ithaca, NY, USA, 1 July 1972. [Google Scholar]
- Todorova, T.; Pesheva, M.; Gregan, F.; Chankova, S. Antioxidant, antimutagenic, and anticarcinogenic effects of Papaver rhoeas L. extract on Saccharomyces cerevisiae. J. Med. Food 2015, 18, 460–467. [Google Scholar] [CrossRef]
- Saeed-Abadi, S.; Ranjbaran, M.; Jafari, F.; Najafi-Abedi, A.; Rahmani, B.; Esfandiari, B.; Delfan, B.; Mojabi, N.; Ghahramani, M.; Sahraei, H. Effects of Papaver rhoeas (L.) extract on formalin-induced pain and inflammation in mice. Pak. J. Biol. Sci. 2012, 15, 1041–1044. [Google Scholar] [CrossRef] [Green Version]
- Sahraei, H.; Fatemi, S.M.; Pashaei-Rad, S.; Faghih-Monzavi, Z.; Salimi, S.H.; Kamalinegad, M. Effects of Papaver rhoeas extract on the acquisition and expression of morphine-induced conditioned place preference in mice. J. Ethnopharmacol. 2006, 103, 420–424. [Google Scholar] [CrossRef]
- Song, K.; Oh, J.H.; Lee, M.Y.; Lee, S.G.; Ha, I.J. Molecular Network-Guided Alkaloid Profiling of Aerial Parts of Papaver nudicaule L. Using LC-HRMS. Molecules 2020, 25, 2636. [Google Scholar] [CrossRef] [PubMed]
- Katarzyna, J.; Karolina, J.; Patrycja, K.; Mateusz, B.; Izabela, G. Mineral Composition and Antioxidant Potential in the Common Poppy (Papaver rhoeas L.) Petal Infusions. Biol. Trace Elem. Res. 2021, 199, 371–381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Osanloo, N.; Najafi-Abedi, A.; Jafari, F.; Javid, F.; Pirpiran, M.; Memar Jafari, M.R.; Mousavi Khosravi, S.A.; Rahimzadeh Behzadi, M.; Ranjbaran, M.; Sahraei, H. Papaver rhoeas L. Hydroalcoholic Extract Exacerbates Forced Swimming Test-Induced Depression in Mice. Basic Clin. Neurosci. 2016, 7, 195–202. [Google Scholar] [CrossRef] [PubMed]
- Hasplova, K.; Hudecova, A.; Miadokova, E.; Magdolenova, Z.; Galova, E.; Vaculcikova, L.; Gregan, F.; Dusinska, M. Biological activity of plant extract isolated from Papaver rhoeas on human lymfoblastoid cell line. Neoplasma 2011, 58, 386–391. [Google Scholar] [CrossRef]
- Pourmotabbed, A.; Rostamian, B.; Manouchehri, G.; Pirzadeh-Jahromi, G.; Sahraei, H.; Ghoshooni, H.; Zardooz, H.; Kamalnegad, M. Effects of Papaver rhoeas extract on the expression and development of morphine-dependence in mice. J. Ethnopharmacol. 2004, 95, 431–435. [Google Scholar] [CrossRef]
- Gürbüz, İ.; Üstün, O.; Yesilada, E.; Sezik, E.; Kutsal, O. Anti-ulcerogenic activity of some plants used as folk remedy in Turkey. J. Ethnopharmacol. 2003, 88, 93–97. [Google Scholar] [CrossRef]
- Oh, J.H.; Yun, M.; Park, D.; Ha, I.J.; Kim, C.K.; Kim, D.W.; Kim, E.O.; Lee, S.G. Papaver nudicaule (Iceland poppy) alleviates lipopolysaccharide-induced inflammation through inactivating NF-κB and STAT3. BMC Complement. Altern. Med. 2019, 19, 90. [Google Scholar] [CrossRef]
- Lim, S.L.; Park, S.Y.; Kang, S.; Park, D.; Kim, S.H.; Um, J.Y.; Jang, H.J.; Lee, J.H.; Jeong, C.H.; Jang, J.H.; et al. Morusin induces cell death through inactivating STAT3 signaling in prostate cancer cells. Am. J. Cancer Res. 2015, 5, 289–299. [Google Scholar]
- Bogdan, C. Nitric oxide synthase in innate and adaptive immunity: An update. Trends Immunol. 2015, 36, 161–178. [Google Scholar] [CrossRef]
- Ricciotti, E.; FitzGerald, G.A. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 986–1000. [Google Scholar] [CrossRef]
- Park, M.H.; Hong, J.T. Roles of NF-κB in Cancer and Inflammatory Diseases and Their Therapeutic Approaches. Cells 2016, 5, 15. [Google Scholar] [CrossRef]
- Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M.T.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39, 44–84. [Google Scholar] [CrossRef]
- He, G.; Karin, M. NF-kappaB and STAT3-key players in liver inflammation and cancer. Cell Res. 2011, 21, 159–168. [Google Scholar] [CrossRef] [Green Version]
- Ory, L.; Nazih, E.H.; Daoud, S.; Mocquard, J.; Bourjot, M.; Margueritte, L.; Delsuc, M.A.; Bard, J.M.; Pouchus, Y.F.; Bertrand, S.; et al. Targeting bioactive compounds in natural extracts-Development of a comprehensive workflow combining chemical and biological data. Anal. Chim. Acta 2019, 1070, 29–42. [Google Scholar] [CrossRef]
- Nothias, L.F.; Nothias-Esposito, M.; da Silva, R.; Wang, M.; Protsyuk, I.; Zhang, Z.; Sarvepalli, A.; Leyssen, P.; Touboul, D.; Costa, J.; et al. Bioactivity-Based Molecular Networking for the Discovery of Drug Leads in Natural Product Bioassay-Guided Fractionation. J. Nat. Prod. 2018, 81, 758–767. [Google Scholar] [CrossRef] [Green Version]
- Schmidt, J.; Boettcher, C.; Kuhnt, C.; Kutchan, T.M.; Zenk, M.H. Poppy alkaloid profiling by electrospray tandem mass spectrometry and electrospray FT-ICR mass spectrometry after [ring-13C6]-tyramine feeding. Phytochemistry 2007, 68, 189–202. [Google Scholar] [CrossRef]
- Oh, J.H.; Ha, I.J.; Lee, M.Y.; Kim, E.O.; Park, D.; Lee, J.H.; Lee, S.G.; Kim, D.W.; Lee, T.H.; Lee, E.J.; et al. Identification and metabolite profiling of alkaloids in aerial parts of Papaver rhoeas by liquid chromatography coupled with quadrupole time-of-flight tandem mass spectrometry. J. Sep. Sci. 2018, 41, 2517–2527. [Google Scholar] [CrossRef] [Green Version]
- Hussain, S.P.; He, P.; Subleski, J.; Hofseth, L.J.; Trivers, G.E.; Mechanic, L.; Hofseth, A.B.; Bernard, M.; Schwank, J.; Nguyen, G.; et al. Nitric oxide is a key component in inflammation-accelerated tumorigenesis. Cancer Res. 2008, 68, 7130–7136. [Google Scholar] [CrossRef] [Green Version]
- Sharma, J.N.; Al-Omran, A.; Parvathy, S.S. Role of nitric oxide in inflammatory diseases. Inflammopharmacology 2007, 15, 252–259. [Google Scholar] [CrossRef]
- Liu, T.; Zhang, L.; Joo, D.; Sun, S.C. NF-kappaB signaling in inflammation. Signal Transduct. Target. Ther. 2017, 2. [Google Scholar] [CrossRef] [Green Version]
- Finkel, T. Signal transduction by reactive oxygen species. J. Cell Biol. 2011, 194, 7–15. [Google Scholar] [CrossRef] [Green Version]
- Poljsak, B.; Suput, D.; Milisav, I. Achieving the balance between ROS and antioxidants: When to use the synthetic antioxidants. Oxidative Med. Cell. Longev. 2013, 2013, 956792. [Google Scholar] [CrossRef]
- Tonelli, C.; Chio, I.I.C.; Tuveson, D.A. Transcriptional Regulation by Nrf2. Antioxid. Redox Signal. 2018, 29, 1727–1745. [Google Scholar] [CrossRef] [Green Version]
- Yu, M.; Li, H.; Liu, Q.; Liu, F.; Tang, L.; Li, C.; Yuan, Y.; Zhan, Y.; Xu, W.; Li, W.; et al. Nuclear factor p65 interacts with Keap1 to repress the Nrf2-ARE pathway. Cell Signal. 2011, 23, 883–892. [Google Scholar] [CrossRef]
- Hayes, J.D.; McMahon, M.; Chowdhry, S.; Dinkova-Kostova, A.T. Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid. Redox Signal. 2010, 13, 1713–1748. [Google Scholar] [CrossRef]
- Niu, X.; Fan, T.; Li, W.; Xing, W.; Huang, H. The anti-inflammatory effects of sanguinarine and its modulation of inflammatory mediators from peritoneal macrophages. Eur. J. Pharmacol. 2012, 689, 262–269. [Google Scholar] [CrossRef]
- Wang, Q.; Dai, P.; Bao, H.; Liang, P.; Wang, W.; Xing, A.; Sun, J. Anti-inflammatory and neuroprotective effects of sanguinarine following cerebral ischemia in rats. Exp. Ther. Med. 2017, 13, 263–268. [Google Scholar] [CrossRef] [Green Version]
- Yu, J.; Zhao, L.; Liu, L.; Yang, F.; Zhu, X.; Cao, B. Tetrahydropalmatine protects rat pulmonary endothelial cells from irradiation-induced apoptosis by inhibiting oxidative stress and the calcium sensing receptor/phospholipase C-gamma1 pathway. Free Radic Res. 2016, 50, 611–626. [Google Scholar] [CrossRef]
- Wang, Y.; Zhu, W.; Lu, D.; Zhang, C.; Wang, Y. Tetrahydropalmatine attenuates MSU crystal-induced gouty arthritis by inhibiting ROS-mediated NLRP3 inflammasome activation. Int. Immunopharmacol. 2021, 100, 108107. [Google Scholar] [CrossRef]
- Wu, S.Z.; Xu, H.C.; Wu, X.L.; Liu, P.; Shi, Y.C.; Pang, P.; Deng, L.; Zhou, G.X.; Chen, X.Y. Dihydrosanguinarine suppresses pancreatic cancer cells via regulation of mut-p53/WT-p53 and the Ras/Raf/Mek/Erk pathway. Phytomedicine 2019, 59, 152895. [Google Scholar] [CrossRef]
- Kim, D.H.; Lee, J.H.; Park, S.; Oh, S.S.; Kim, S.; Kim, D.W.; Park, K.H.; Kim, K.D. 6-Acetonyl-5,6-dihydrosanguinarine (ADS) from Chelidonium majus L. triggers proinflammatory cytokine production via ROS-JNK/ERK-NFkappaB signaling pathway. Food Chem. Toxicol. 2013, 58, 273–279. [Google Scholar] [CrossRef] [PubMed]
Species | Flower Color | Abbreviation of Ethanolic Extract | Abbreviation of EtOAc Fraction From Each Ethanolic Extracts |
---|---|---|---|
Papaver rhoeas | Red | RA | RA-Fr |
Papaver nudicaule | White | NW | NW-Fr |
Papaver nudicaule | Pink | NP | NP-Fr |
Papaver nudicaule | Scarlet | NS | NS-Fr |
Papaver nudicaule | Yellow | NY | NY-Fr |
Papaver nudicaule | Orange | NO | NO-Fr |
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Kim, H.; Han, S.; Song, K.; Lee, M.Y.; Park, B.; Ha, I.J.; Lee, S.-G. Ethyl Acetate Fractions of Papaver rhoeas L. and Papaver nudicaule L. Exert Antioxidant and Anti-Inflammatory Activities. Antioxidants 2021, 10, 1895. https://doi.org/10.3390/antiox10121895
Kim H, Han S, Song K, Lee MY, Park B, Ha IJ, Lee S-G. Ethyl Acetate Fractions of Papaver rhoeas L. and Papaver nudicaule L. Exert Antioxidant and Anti-Inflammatory Activities. Antioxidants. 2021; 10(12):1895. https://doi.org/10.3390/antiox10121895
Chicago/Turabian StyleKim, Hail, Sanghee Han, Kwangho Song, Min Young Lee, BeumJin Park, In Jin Ha, and Seok-Geun Lee. 2021. "Ethyl Acetate Fractions of Papaver rhoeas L. and Papaver nudicaule L. Exert Antioxidant and Anti-Inflammatory Activities" Antioxidants 10, no. 12: 1895. https://doi.org/10.3390/antiox10121895
APA StyleKim, H., Han, S., Song, K., Lee, M. Y., Park, B., Ha, I. J., & Lee, S.-G. (2021). Ethyl Acetate Fractions of Papaver rhoeas L. and Papaver nudicaule L. Exert Antioxidant and Anti-Inflammatory Activities. Antioxidants, 10(12), 1895. https://doi.org/10.3390/antiox10121895