Effect of Green and Brown Propolis Extracts on the Expression Levels of MicroRNAs, MRNAs and Proteins, Related to Oxidative Stress and Inflammation

Overview

Journal Nutrients

Date 2017 Oct 5

PMID 28974022

Citations 19

Authors

Vincenzo Zaccaria

Valeria Curti

Arianna Di Lorenzo

Alessandra Baldi

Cristina Maccario

Sabrina Sommatis

Roberto Mocchi

Maria Daglia

Affiliations

Soon will be listed here.

Abstract

A large body of evidence highlights that propolis exerts many biological functions that can be ascribed to its antioxidant and anti-inflammatory components, including different polyphenol classes. Nevertheless, the molecular mechanisms are yet unknown. The aim of this study is to investigate the mechanisms at the basis of propolis anti-inflammatory and antioxidant activities. The effects of two brown and green propolis extracts-chemically characterized by RP-HPLC-PDA-ESI-MSn-on the expression levels of miRNAs associated with inflammatory responses (miR-19a-3p and miR-203a-3p) and oxidative stress (miR-27a-3p and miR-17-3p), were determined in human keratinocyte HaCat cell lines, treated with non-cytotoxic concentrations. The results showed that brown propolis, whose major polyphenolic components are flavonoids, induced changes in the expression levels of all miRNAs, and was more active than green propolis (whose main polyphenolic components are hydroxycinnamic acid derivatives) which caused changes only in the expression levels of miR-19a-3p and miR-27a-3p. In addition, only brown propolis was able to modify (1) the expression levels of mRNAs, the target of the reported miRNAs, which code for Tumor Necrosis Factor-α (TNF-α), Nuclear Factor, Erythroid 2 Like 2 (NFE2L2) and Glutathione Peroxidase 2 (GPX2), and (2) the protein levels of TNF-α and NFE2L2. In conclusion, brown and green propolis, which showed different metabolite profiles, exert their biological functions through different mechanisms of action.

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References

Park Y, Alencar S, Aguiar C . Botanical origin and chemical composition of Brazilian propolis. J Agric Food Chem. 2002; 50(9):2502-6. DOI: 10.1021/jf011432b. View

Kuropatnicki A, Szliszka E, Krol W . Historical aspects of propolis research in modern times. Evid Based Complement Alternat Med. 2013; 2013:964149. PMC: 3655583. DOI: 10.1155/2013/964149. View

Abo-Salem O, El-Edel R, Harisa G, El-Halawany N, Ghonaim M . Experimental diabetic nephropathy can be prevented by propolis: Effect on metabolic disturbances and renal oxidative parameters. Pak J Pharm Sci. 2009; 22(2):205-10. View

Kumazaki M, Shinohara H, Taniguchi K, Yamada N, Ohta S, Ichihara K . Propolis cinnamic acid derivatives induce apoptosis through both extrinsic and intrinsic apoptosis signaling pathways and modulate of miRNA expression. Phytomedicine. 2014; 21(8-9):1070-7. DOI: 10.1016/j.phymed.2014.04.006. View

Machado B, Dantas Silva R, Barreto G, Costa S, da Silva D, Brandao H . Chemical Composition and Biological Activity of Extracts Obtained by Supercritical Extraction and Ethanolic Extraction of Brown, Green and Red Propolis Derived from Different Geographic Regions in Brazil. PLoS One. 2016; 11(1):e0145954. PMC: 4706314. DOI: 10.1371/journal.pone.0145954. View

Zhao L, Pu L, Wei J, Li J, Wu J, Xin Z . Brazilian Green Propolis Improves Antioxidant Function in Patients with Type 2 Diabetes Mellitus. Int J Environ Res Public Health. 2016; 13(5). PMC: 4881123. DOI: 10.3390/ijerph13050498. View

Liu R, Li J, Song J, Sun J, Li Y, Zhou S . Pinocembrin protects human brain microvascular endothelial cells against fibrillar amyloid-β(1-40) injury by suppressing the MAPK/NF-κB inflammatory pathways. Biomed Res Int. 2014; 2014:470393. PMC: 4135138. DOI: 10.1155/2014/470393. View

Cui-Ping Z, Shuai H, Wen-ting W, Shun P, Xiao-ge S, Ya-Jing L . Development of high-performance liquid chromatographic for quality and authenticity control of Chinese propolis. J Food Sci. 2014; 79(7):C1315-22. DOI: 10.1111/1750-3841.12510. View

Curti V, Di Lorenzo A, Rossi D, Martino E, Capelli E, Collina S . Enantioselective Modulatory Effects of Naringenin Enantiomers on the Expression Levels of miR-17-3p Involved in Endogenous Antioxidant Defenses. Nutrients. 2017; 9(3). PMC: 5372878. DOI: 10.3390/nu9030215. View

10.

Martinotti S, Ranzato E . Propolis: a new frontier for wound healing?. Burns Trauma. 2016; 3:9. PMC: 4964312. DOI: 10.1186/s41038-015-0010-z. View

11.

Barros M, Lemos M, Maistro E, Leite M, Sousa J, Bastos J . Evaluation of antiulcer activity of the main phenolic acids found in Brazilian Green Propolis. J Ethnopharmacol. 2008; 120(3):372-7. DOI: 10.1016/j.jep.2008.09.015. View

12.

Wu Z, Zhu A, Takayama F, Okada R, Liu Y, Harada Y . Brazilian green propolis suppresses the hypoxia-induced neuroinflammatory responses by inhibiting NF-κB activation in microglia. Oxid Med Cell Longev. 2013; 2013:906726. PMC: 3747398. DOI: 10.1155/2013/906726. View

13.

Kurek-Gorecka A, Rzepecka-Stojko A, Gorecki M, Stojko J, Sosada M, Swierczek-Zieba G . Structure and antioxidant activity of polyphenols derived from propolis. Molecules. 2013; 19(1):78-101. PMC: 6271064. DOI: 10.3390/molecules19010078. View

14.

Bufalo M, Bordon-Graciani A, Conti B, Golim M, Sforcin J . The immunomodulatory effect of propolis on receptors expression, cytokine production and fungicidal activity of human monocytes. J Pharm Pharmacol. 2014; 66(10):1497-504. DOI: 10.1111/jphp.12279. View

15.

Tiveron A, Rosalen P, Franchin M, Lacerda R, Bueno-Silva B, Benso B . Chemical Characterization and Antioxidant, Antimicrobial, and Anti-Inflammatory Activities of South Brazilian Organic Propolis. PLoS One. 2016; 11(11):e0165588. PMC: 5089781. DOI: 10.1371/journal.pone.0165588. View

16.

Eldutar E, Kandemir F, Kucukler S, Caglayan C . Restorative effects of Chrysin pretreatment on oxidant-antioxidant status, inflammatory cytokine production, and apoptotic and autophagic markers in acute paracetamol-induced hepatotoxicity in rats: An experimental and biochemical study. J Biochem Mol Toxicol. 2017; 31(11). DOI: 10.1002/jbt.21960. View

17.

Cuevas A, Saavedra N, Cavalcante M, Salazar L, Abdalla D . Identification of microRNAs involved in the modulation of pro-angiogenic factors in atherosclerosis by a polyphenol-rich extract from propolis. Arch Biochem Biophys. 2014; 557:28-35. DOI: 10.1016/j.abb.2014.04.009. View

18.

Lahouel M, Boulkour S, Segueni N, Fillastre J . [The flavonoids effect against vinblastine, cyclophosphamide and paracetamol toxicity by inhibition of lipid-peroxydation and increasing liver glutathione concentration]. Pathol Biol (Paris). 2004; 52(6):314-22. DOI: 10.1016/j.patbio.2004.01.001. View

19.

Chen B, Lu Y, Chen Y, Cheng J . The role of Nrf2 in oxidative stress-induced endothelial injuries. J Endocrinol. 2015; 225(3):R83-99. DOI: 10.1530/JOE-14-0662. View

20.

Khayyal M, El-Hazek R, El-Ghazaly M . Propolis aqueous extract preserves functional integrity of murine intestinal mucosa after exposure to ionizing radiation. Environ Toxicol Pharmacol. 2015; 40(3):901-6. DOI: 10.1016/j.etap.2015.09.006. View