Research Article
BibTex RIS Cite

Solvation Methods Affect the Amount of Active Components in the Extract of Propolis as well as Its Anti-Inflammatory Activity in THP-1 Cells

Year 2023, Volume: 82 Issue: 2, 132 - 141, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1247199

Abstract

Objective: Propolis has been found to have various effects, including antioxidant and anti-inflammatory properties, according to studies. In this recent research, we discovered that reducing allergenic compounds in propolis through biotransformation using specific Lactobacillus plantarum strains enhanced its anti-inflammatory qualities. The study aimed to identify the extraction methods and solvents that had the most significant anti-inflammatory effects and assess how L. plantarum strains biotransformation of propolis affected these qualities in THP-1 cell line cultures.

Materials and Methods: Propolis samples were biotransformed with different concentrations (1.5%, 2.5%, 3.5%) of several L. plantarum strains (ISLG-2, ATCC®8014, visbyvac) before extraction using various solvents (ethanol, polyethylene glycol-PEG, water) and ultrasound treatments (300 W/40 Hz for 5, 10, 15 min). Liquid chromatography-mass spectrometer/mass spectrometry was used for phenolic analysis of the samples. ELISA test kits were employed to assess NF-kβ, IL-1α, IL-1β, IL-6, IL-10, TNF-α, IFN-γ , COX-1 in the cell culture supernatant.

Results: Results showed that, except for NF-kβ, all cytokine levels decreased in four separate propolis samples. Caffeic acid, kaempferol, ferulic acid, quercetin, pelargonin, and naringenin were the key physiologically active components associated with the anti-inflammatory activity of propolis. The biotransformation process to reduce allergen compounds did not alter propolis’s anti-inflammatory properties.

Conclusion: In samples that were dissolved in water, dissolved in ethanol+biotransformed with L. plantarum ATCC®8014, dissolved in water+biotransformed with L. plantarum ATCC®8014, and dissolved in water+sonicated for 15 min and biotransformed with L. plantarum ATCC®8014, the maximum anti-inflammatory effect of propolis was assessed.

Supporting Institution

TUBITAK (The Scientific and Technological Research Council of Turkey)

Project Number

116Z223

Thanks

The authors greatly appreciated to Ege University Children Hospital Metabolism Laboratory for their technical assistance.

References

  • Tan HY, Wang, N Lis, Hong M, Wang, X, Feng Y. The reactive oxygen species in macrophage polarization: Reflecting its dual role in progression and treatment of human diseases. Oxid Med Cell Longev. 2016;2795090. doi:10.1155/2016/2795090 google scholar
  • Hausen BM, Wollenweber E, Senff H, Post B. The sensitizing properties of 1,1-dimethylallyl caffeic acid ester. Propolis Aller (II). 1987;17(3):171-177. google scholar
  • Chanput W, Mes J, Vreeburg RAM, Savelkoul HFJ, Wichers HJ. Transcription profiles of LPS-stimulated THP-1 monocytes and macrophages: A tool to study inflammation modulating effects of food-derived compounds. Food Funct. 2010;1(3):254-261. google scholar
  • De Mendonca ICG, Porto ICC de M, do Nascimento TG, de Souza NS, Oliveira JM, Arruda RE dos S. Brazilian red propolis: Phytochemical screening, antioxidant activity and effect against cancer cells. BMC Complement Altern Med. 2015;15:357. doi:10.1186/s12906-015-0888-9 google scholar
  • Chen L, Deng H, Cui H, et al. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget. 2018;9(6):7204-7218. google scholar
  • Italiani P, Boraschi D. From monocytes to M1/M2 macrophages: Phenotypical vs. functional differentiation. Front Immunol. 2014;5:514. doi:10.3389/fimmu.2014.00514 google scholar
  • Ahn MR, Kunimasa K, Kumazawa S, et al. Correlation be-tween antiangiogenic activity and antioxidant activity of various components from propolis. Molecular Nut Food Res.2009;53(5): 643-651. google scholar
  • Bankova V, Popova M, Trusheva B. Propolis volatile compounds: Chemical diversity and biological activity: A review. Chem Cent J. 2014;8:28. doi:10.1186/1752-153X-8-28 google scholar
  • Sabbione AC, Luna-Vital D, Scilingo A, Anonb MC, Mej^a EG. Amaranth peptides decreased the activity and expression of cellu-lar tissue factor on LPS activated THP-1 human monocytes. Food Funct. 2018;9:3823-3834. google scholar
  • Walgrave SE, Warshaw EM, Glesne LA. Allergic contact der-matitis from propolis. Dermatitis. 2015;16:209-215. google scholar
  • Chanput W, Mes JJ., Wichers HJ. THP-1 cell line: An in vitro cell model for immune modulation approach. Int Immunopharmacol. 2014;23:37-45. google scholar
  • Touzani S, Embaslat W, Imtara H, et al. In vitro evaluation of the potential use of propolis as a multitarget therapeu-tic product: Physicochemical properties, chemical composition, and immunomodulatory, antibacterial, and anticancer properties. Biomed Res Int. 2019;2019:4836378. doi:10.1155/2019/4836378 google scholar
  • Basista-Soltys K. Allergy to propolis in beekeepers-A literatüre review. Occup Med Health Aff. 2013;1-105. google scholar
  • Alliboni A, D’Andrea A, Massanisso P. Propolis specimens from different locations of central Italy: Chemical profiling and gas chromatography-mass spectrometry (GC-MS) quantitative analy-sis of the allergenic esters benzyl cinnamate and benzyl salicylate. J Agric Food Chem. 2011;59(1):282-288. google scholar
  • Borrelli F, Maffia P, Pinto L, et al. Phytochemical compounds involved in the anti-inflammatory effect of propolis extract. Fi-toterapia. 2002;73:53-63. google scholar
  • Galeotti F, Maccari F, Fachini A., Volpi N. Chemical compo-sition and antioxidant activity of propolis prepared in different forms and in different solvents useful for finished products. Foods. 2018:7(3):41. doi:10.3390/foods7030041 google scholar
  • Chanput W, Mes JJ, Wichers HJ. THP-1 cell line: An in vitro cell model for immune modulation approach. Inter Immunopharmaco. 2014;23:37-45. google scholar
  • Memmedov H., Oktay LM., Durmaz B. et al. Propolis prevents inhibition of apoptosis by potassium bromate in CCD 841 human colon cell. Cell Biochem Func. 2020; 38(4):510-519. google scholar
  • Aldemir O, Yıldırım HK, Sozmen, EY. Antioxidant and antiinflammatory effects of biotechnologically transformed propolis. J Food Process Preserv. 2018;42(6):e13642. doi: 10.1111/jfpp.13642 google scholar
  • Woo KJ, Jeong YJ, Inoue H, Parka JW, Kwon TK. Chrysin sup-presses lipopolysaccharide-induced cyclooxygenase-2 expression through the inhibition of nuclear factor for IL-6 (NF-IL6) DNA-binding activity. FEBS Letters. 2005;579:705-711. google scholar
  • Yıldırım HK, Canbay E, Öztürk Ş, Aldemir O, Sözmen EY. Bio-transformation of propolis phenols by L. plantarum as a strategy for reduction of allergens. Food Sci Biotechnol. 2018;27(6):1727-1733. google scholar
  • Öztürk Ş, Durmaz B, Memmedov, H, et al. Effect of ferulic acid on cytokine release in human leukemia monocytic cells induced with lipopolysaccharides. Ege J Med. 2021:60(1):39-50. google scholar
  • Memmedov H, Oktay LM, Durmaz B, Günel NS, Yıldırım HK, Sözmen EY. Propolis prevents inhibition of apoptosis by potas-sium bromate in CCD 841 human colon cell. Cell Biochem Func. 2020;38(4):510-519. google scholar
  • Ferreres F, Gomes NGM, Valentâo P. Leaves and stem bark from Allophylus africanus P. Beauv: An approach to anti-inflammatory properties and characterization of their flavonoit profile. Food Chem Toxicol. 2018;118:430-438. google scholar
  • Rajendran P, Rengarajan T, Natarajan N, Rajendran P, Yutaka N, Ikuo N. Kaempferol, a potential cytostatic and cure for inflamma-tory disorders. Eur JMed Chem. 2014;86:103-112. google scholar
  • Touzani S, Embaslat W, Imtara H, et al. In vitro evaluation of the potential use of propolis as a multitarget therapeu-tic product: Physicochemical properties, chemical composition, and immunomodulatory, antibacterial, and anticancer properties. BioMed Res Int. 2019;2019:4836378. doi:10.1155/2019/4836378 google scholar
  • Lund ME, To J, O’Brien BA, Donnelly S. The choice of phorbol 12-myristate 13-acetate differentiation protocol influences the re-sponse of THP-1 macrophages to a pro-inflammatory stimulus. J Immunol Methods. 2016;430:64-70. google scholar
  • Bueno-Silva B, Kawamoto D Ando-Suguimoto E, et al. Brazil-ian red propolis attenuates inflammatory signaling cascade in LPS activated macrophages. Plos One. 2015;10(12): e0144954. doi.org/10.1371/journal.pone.0144954 google scholar
  • Castro C, Mura F, Valenzuela G, et al. Identification of phenolic compounds by HPLC-ESI-MS/MS and antioxidant activity from Chilean propolis. Food Res Int. 2014:64:873-879. google scholar
  • Giambartolomei GH, Dennis VA, Lasater BL, Murthy PK, Philipp M.T. Autocrine and exocrine regulation of interleukin-10 produc-tion in THP-1 cells stimulated with Borrelia burgdorferi lipopro-teins. Infect Immun. 2002;70(4):1881-1888. google scholar
  • Bachiega TF, Orsatti CL, Pagliarone AC, Sforcin JM. The effects of propolis and its isolated compounds on cytokine production by murine macrophages. Phytother Res. 2012;26:1308-1313. google scholar
  • Silva JC, Rodrigues S, Fes X, Estevinho LM. Antimicrobial ac-tivity, phenolic profile and role in the inflammation of propolis. Food Chem Toxicol. 2012;50(5):1790-1795. google scholar
  • Nakayama M, Kayagaki N, Yamaguchi N, Okumura K, Yagita H. Involvement of TWEAK in interferon gamma-stimulated mono-cyte cytotoxicity. J Exp Med. 2000:192(9):1373-1380. google scholar
  • Ribeiro MNS, Nascimento FRF. Mechanisms of action underlying the anti- inflammatory and immunomodulatory effects of propo-lis: A brief review. Braz J Pharmacogn. 2012;22(1):208-219. google scholar
  • Paracatu LC, Quinello CM, Faria G. Caffeic acid phenethyl ester: Consequences of its hydrophobicity in the oxidative functions and cytokine release by leukocytes. Evid Based Complement Alternat Med. 2014;2014:793629. doi:10.1155/2014/793629 google scholar
  • Szliszka E, Kucharska AZ, Sokol-Ltowska A, Mertas A, Czuba ZP, Krol W. Chemical composition and anti-inflammatory ef-fect of ethanolic extract of Brazilian green propolis on activated J774A.1 macrophages. Evid Based Complement Alternat Med. 2013;2013:976415. doi:10.1155/2013/976415 google scholar
  • Burdock GA. Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol.1998;36:347-363. google scholar
Year 2023, Volume: 82 Issue: 2, 132 - 141, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1247199

Abstract

Project Number

116Z223

References

  • Tan HY, Wang, N Lis, Hong M, Wang, X, Feng Y. The reactive oxygen species in macrophage polarization: Reflecting its dual role in progression and treatment of human diseases. Oxid Med Cell Longev. 2016;2795090. doi:10.1155/2016/2795090 google scholar
  • Hausen BM, Wollenweber E, Senff H, Post B. The sensitizing properties of 1,1-dimethylallyl caffeic acid ester. Propolis Aller (II). 1987;17(3):171-177. google scholar
  • Chanput W, Mes J, Vreeburg RAM, Savelkoul HFJ, Wichers HJ. Transcription profiles of LPS-stimulated THP-1 monocytes and macrophages: A tool to study inflammation modulating effects of food-derived compounds. Food Funct. 2010;1(3):254-261. google scholar
  • De Mendonca ICG, Porto ICC de M, do Nascimento TG, de Souza NS, Oliveira JM, Arruda RE dos S. Brazilian red propolis: Phytochemical screening, antioxidant activity and effect against cancer cells. BMC Complement Altern Med. 2015;15:357. doi:10.1186/s12906-015-0888-9 google scholar
  • Chen L, Deng H, Cui H, et al. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget. 2018;9(6):7204-7218. google scholar
  • Italiani P, Boraschi D. From monocytes to M1/M2 macrophages: Phenotypical vs. functional differentiation. Front Immunol. 2014;5:514. doi:10.3389/fimmu.2014.00514 google scholar
  • Ahn MR, Kunimasa K, Kumazawa S, et al. Correlation be-tween antiangiogenic activity and antioxidant activity of various components from propolis. Molecular Nut Food Res.2009;53(5): 643-651. google scholar
  • Bankova V, Popova M, Trusheva B. Propolis volatile compounds: Chemical diversity and biological activity: A review. Chem Cent J. 2014;8:28. doi:10.1186/1752-153X-8-28 google scholar
  • Sabbione AC, Luna-Vital D, Scilingo A, Anonb MC, Mej^a EG. Amaranth peptides decreased the activity and expression of cellu-lar tissue factor on LPS activated THP-1 human monocytes. Food Funct. 2018;9:3823-3834. google scholar
  • Walgrave SE, Warshaw EM, Glesne LA. Allergic contact der-matitis from propolis. Dermatitis. 2015;16:209-215. google scholar
  • Chanput W, Mes JJ., Wichers HJ. THP-1 cell line: An in vitro cell model for immune modulation approach. Int Immunopharmacol. 2014;23:37-45. google scholar
  • Touzani S, Embaslat W, Imtara H, et al. In vitro evaluation of the potential use of propolis as a multitarget therapeu-tic product: Physicochemical properties, chemical composition, and immunomodulatory, antibacterial, and anticancer properties. Biomed Res Int. 2019;2019:4836378. doi:10.1155/2019/4836378 google scholar
  • Basista-Soltys K. Allergy to propolis in beekeepers-A literatüre review. Occup Med Health Aff. 2013;1-105. google scholar
  • Alliboni A, D’Andrea A, Massanisso P. Propolis specimens from different locations of central Italy: Chemical profiling and gas chromatography-mass spectrometry (GC-MS) quantitative analy-sis of the allergenic esters benzyl cinnamate and benzyl salicylate. J Agric Food Chem. 2011;59(1):282-288. google scholar
  • Borrelli F, Maffia P, Pinto L, et al. Phytochemical compounds involved in the anti-inflammatory effect of propolis extract. Fi-toterapia. 2002;73:53-63. google scholar
  • Galeotti F, Maccari F, Fachini A., Volpi N. Chemical compo-sition and antioxidant activity of propolis prepared in different forms and in different solvents useful for finished products. Foods. 2018:7(3):41. doi:10.3390/foods7030041 google scholar
  • Chanput W, Mes JJ, Wichers HJ. THP-1 cell line: An in vitro cell model for immune modulation approach. Inter Immunopharmaco. 2014;23:37-45. google scholar
  • Memmedov H., Oktay LM., Durmaz B. et al. Propolis prevents inhibition of apoptosis by potassium bromate in CCD 841 human colon cell. Cell Biochem Func. 2020; 38(4):510-519. google scholar
  • Aldemir O, Yıldırım HK, Sozmen, EY. Antioxidant and antiinflammatory effects of biotechnologically transformed propolis. J Food Process Preserv. 2018;42(6):e13642. doi: 10.1111/jfpp.13642 google scholar
  • Woo KJ, Jeong YJ, Inoue H, Parka JW, Kwon TK. Chrysin sup-presses lipopolysaccharide-induced cyclooxygenase-2 expression through the inhibition of nuclear factor for IL-6 (NF-IL6) DNA-binding activity. FEBS Letters. 2005;579:705-711. google scholar
  • Yıldırım HK, Canbay E, Öztürk Ş, Aldemir O, Sözmen EY. Bio-transformation of propolis phenols by L. plantarum as a strategy for reduction of allergens. Food Sci Biotechnol. 2018;27(6):1727-1733. google scholar
  • Öztürk Ş, Durmaz B, Memmedov, H, et al. Effect of ferulic acid on cytokine release in human leukemia monocytic cells induced with lipopolysaccharides. Ege J Med. 2021:60(1):39-50. google scholar
  • Memmedov H, Oktay LM, Durmaz B, Günel NS, Yıldırım HK, Sözmen EY. Propolis prevents inhibition of apoptosis by potas-sium bromate in CCD 841 human colon cell. Cell Biochem Func. 2020;38(4):510-519. google scholar
  • Ferreres F, Gomes NGM, Valentâo P. Leaves and stem bark from Allophylus africanus P. Beauv: An approach to anti-inflammatory properties and characterization of their flavonoit profile. Food Chem Toxicol. 2018;118:430-438. google scholar
  • Rajendran P, Rengarajan T, Natarajan N, Rajendran P, Yutaka N, Ikuo N. Kaempferol, a potential cytostatic and cure for inflamma-tory disorders. Eur JMed Chem. 2014;86:103-112. google scholar
  • Touzani S, Embaslat W, Imtara H, et al. In vitro evaluation of the potential use of propolis as a multitarget therapeu-tic product: Physicochemical properties, chemical composition, and immunomodulatory, antibacterial, and anticancer properties. BioMed Res Int. 2019;2019:4836378. doi:10.1155/2019/4836378 google scholar
  • Lund ME, To J, O’Brien BA, Donnelly S. The choice of phorbol 12-myristate 13-acetate differentiation protocol influences the re-sponse of THP-1 macrophages to a pro-inflammatory stimulus. J Immunol Methods. 2016;430:64-70. google scholar
  • Bueno-Silva B, Kawamoto D Ando-Suguimoto E, et al. Brazil-ian red propolis attenuates inflammatory signaling cascade in LPS activated macrophages. Plos One. 2015;10(12): e0144954. doi.org/10.1371/journal.pone.0144954 google scholar
  • Castro C, Mura F, Valenzuela G, et al. Identification of phenolic compounds by HPLC-ESI-MS/MS and antioxidant activity from Chilean propolis. Food Res Int. 2014:64:873-879. google scholar
  • Giambartolomei GH, Dennis VA, Lasater BL, Murthy PK, Philipp M.T. Autocrine and exocrine regulation of interleukin-10 produc-tion in THP-1 cells stimulated with Borrelia burgdorferi lipopro-teins. Infect Immun. 2002;70(4):1881-1888. google scholar
  • Bachiega TF, Orsatti CL, Pagliarone AC, Sforcin JM. The effects of propolis and its isolated compounds on cytokine production by murine macrophages. Phytother Res. 2012;26:1308-1313. google scholar
  • Silva JC, Rodrigues S, Fes X, Estevinho LM. Antimicrobial ac-tivity, phenolic profile and role in the inflammation of propolis. Food Chem Toxicol. 2012;50(5):1790-1795. google scholar
  • Nakayama M, Kayagaki N, Yamaguchi N, Okumura K, Yagita H. Involvement of TWEAK in interferon gamma-stimulated mono-cyte cytotoxicity. J Exp Med. 2000:192(9):1373-1380. google scholar
  • Ribeiro MNS, Nascimento FRF. Mechanisms of action underlying the anti- inflammatory and immunomodulatory effects of propo-lis: A brief review. Braz J Pharmacogn. 2012;22(1):208-219. google scholar
  • Paracatu LC, Quinello CM, Faria G. Caffeic acid phenethyl ester: Consequences of its hydrophobicity in the oxidative functions and cytokine release by leukocytes. Evid Based Complement Alternat Med. 2014;2014:793629. doi:10.1155/2014/793629 google scholar
  • Szliszka E, Kucharska AZ, Sokol-Ltowska A, Mertas A, Czuba ZP, Krol W. Chemical composition and anti-inflammatory ef-fect of ethanolic extract of Brazilian green propolis on activated J774A.1 macrophages. Evid Based Complement Alternat Med. 2013;2013:976415. doi:10.1155/2013/976415 google scholar
  • Burdock GA. Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol.1998;36:347-363. google scholar
There are 37 citations in total.

Details

Primary Language English
Subjects Biochemistry and Cell Biology (Other)
Journal Section Research Articles
Authors

Burak Durmaz 0000-0002-6383-6724

Latife Merve Oktay 0000-0002-8012-0445

Hikmet Memmedov 0000-0002-8012-0445

Nur Selvi Günel 0000-0002-6383-6724

Hatice Kalkan Yıldırım 0000-0001-9698-9682

Eser Y. Sözmen 0000-0002-6383-6724

Project Number 116Z223
Publication Date December 21, 2023
Submission Date February 3, 2023
Published in Issue Year 2023 Volume: 82 Issue: 2

Cite

AMA Durmaz B, Oktay LM, Memmedov H, Selvi Günel N, Kalkan Yıldırım H, Y. Sözmen E. Solvation Methods Affect the Amount of Active Components in the Extract of Propolis as well as Its Anti-Inflammatory Activity in THP-1 Cells. Eur J Biol. December 2023;82(2):132-141. doi:10.26650/EurJBiol.2023.1247199