Skip to main content
Top
Published in: Clinical Reviews in Allergy & Immunology 3/2013

01-06-2013

The Immunomodulatory and Anticancer Properties of Propolis

Authors: Godfrey Chi-Fung Chan, Ka-Wai Cheung, Daniel Man-Yuen Sze

Published in: Clinical Reviews in Allergy & Immunology | Issue 3/2013

Login to get access

Abstract

Propolis, a waxy substance produced by the honeybee, has been adopted as a form of folk medicine since ancient times. It has a wide spectrum of alleged applications including potential anti-infection and anticancer effects. Many of the therapeutic effects can be attributed to its immunomodulatory functions. The composition of propolis can vary according to the geographic locations from where the bees obtained the ingredients. Two main immunopotent chemicals have been identified as caffeic acid phenethyl ester (CAPE) and artepillin C. Propolis, CAPE, and artepillin C have been shown to exert summative immunosuppressive function on T lymphocyte subsets but paradoxically activate macrophage function. On the other hand, they also have potential antitumor properties by different postulated mechanisms such as suppressing cancer cells proliferation via its anti-inflammatory effects; decreasing the cancer stem cell populations; blocking specific oncogene signaling pathways; exerting antiangiogenic effects; and modulating the tumor microenvironment. The good bioavailability by the oral route and good historical safety profile makes propolis an ideal adjuvant agent for future immunomodulatory or anticancer regimens. However, standardized quality controls and good design clinical trials are essential before either propolis or its active ingredients can be adopted routinely in our future therapeutic armamentarium.
Literature
1.
go back to reference Burdock GA (1998) Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol 36:347–363PubMedCrossRef Burdock GA (1998) Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol 36:347–363PubMedCrossRef
2.
go back to reference Marcucci MC, Ferreres F, Garcia-Viguera C, Bankova VS, De Castro SL, Dantas AP et al (2001) Phenolic compounds from Brazilian propolis with pharmacological activities. J Ethnopharmacol 74:105–112PubMedCrossRef Marcucci MC, Ferreres F, Garcia-Viguera C, Bankova VS, De Castro SL, Dantas AP et al (2001) Phenolic compounds from Brazilian propolis with pharmacological activities. J Ethnopharmacol 74:105–112PubMedCrossRef
3.
go back to reference Salatino A, Teixeira EW, Negri G, Message D (2005) Origin and chemical variation of Brazilian propolis. Evid Based Complement Alternat Med 2:33–38PubMedCrossRef Salatino A, Teixeira EW, Negri G, Message D (2005) Origin and chemical variation of Brazilian propolis. Evid Based Complement Alternat Med 2:33–38PubMedCrossRef
4.
go back to reference Castaldo S, Capasso F (2002) Propolis, an old remedy used in modern medicine. Fitoterapia 73(Suppl 1):S1–S6PubMedCrossRef Castaldo S, Capasso F (2002) Propolis, an old remedy used in modern medicine. Fitoterapia 73(Suppl 1):S1–S6PubMedCrossRef
5.
go back to reference Banskota AH, Tezuka Y, Adnyana IK, Midorikawa K, Matsushige K, Message D et al (2000) Cytotoxic, hepatoprotective and free radical scavenging effects of propolis from Brazil, Peru, the Netherlands and China. J Ethnopharmacol 72:239–246PubMedCrossRef Banskota AH, Tezuka Y, Adnyana IK, Midorikawa K, Matsushige K, Message D et al (2000) Cytotoxic, hepatoprotective and free radical scavenging effects of propolis from Brazil, Peru, the Netherlands and China. J Ethnopharmacol 72:239–246PubMedCrossRef
6.
go back to reference Borrelli F, Maffia P, Pinto L, Ianaro A, Russo A, Capasso F et al (2002) Phytochemical compounds involved in the anti-inflammatory effect of propolis extract. Fitoterapia 73(Suppl 1):S53–S63PubMedCrossRef Borrelli F, Maffia P, Pinto L, Ianaro A, Russo A, Capasso F et al (2002) Phytochemical compounds involved in the anti-inflammatory effect of propolis extract. Fitoterapia 73(Suppl 1):S53–S63PubMedCrossRef
7.
go back to reference Pereira AS, Norsell M, Cardoso JN, Aquino Neto FR, Ramos MF (2000) Rapid screening of polar compounds in Brazilian propolis by high-temperature high-resolution gas chromatography–mass spectrometry. J Agric Food Chem 48:5226–5230PubMedCrossRef Pereira AS, Norsell M, Cardoso JN, Aquino Neto FR, Ramos MF (2000) Rapid screening of polar compounds in Brazilian propolis by high-temperature high-resolution gas chromatography–mass spectrometry. J Agric Food Chem 48:5226–5230PubMedCrossRef
8.
go back to reference Pileggi R, Antony K, Johnson K, Zuo J, Shannon Holliday L (2009) Propolis inhibits osteoclast maturation. Dent Traumatol 25:584–588PubMedCrossRef Pileggi R, Antony K, Johnson K, Zuo J, Shannon Holliday L (2009) Propolis inhibits osteoclast maturation. Dent Traumatol 25:584–588PubMedCrossRef
9.
go back to reference van Ketel WG, Bruynzeel DP (1992) Occupational dermatitis in an accordion repairer. Contact Dermatitis 27:186PubMedCrossRef van Ketel WG, Bruynzeel DP (1992) Occupational dermatitis in an accordion repairer. Contact Dermatitis 27:186PubMedCrossRef
10.
go back to reference Han SK, Yamauchi K, Park HK (2001) Effect of nitrite and propolis preservative on volatile basic nitrogen changes in meat products. Microbios 105:71–75PubMed Han SK, Yamauchi K, Park HK (2001) Effect of nitrite and propolis preservative on volatile basic nitrogen changes in meat products. Microbios 105:71–75PubMed
11.
go back to reference Bankova V, Boudourova-Krasteva G, Sforcin JM, Frete X, Kujumgiev A, Maimoni-Rodella R et al (1999) Phytochemical evidence for the plant origin of Brazilian propolis from Sao Paulo state. Z Naturforsch C 54:401–405PubMed Bankova V, Boudourova-Krasteva G, Sforcin JM, Frete X, Kujumgiev A, Maimoni-Rodella R et al (1999) Phytochemical evidence for the plant origin of Brazilian propolis from Sao Paulo state. Z Naturforsch C 54:401–405PubMed
12.
go back to reference Dobrowolski JW, Vohora SB, Sharma K, Shah SA, Naqvi SA, Dandiya PC (1991) Antibacterial, antifungal, antiamoebic, antiinflammatory and antipyretic studies on propolis bee products. J Ethnopharmacol 35:77–82PubMedCrossRef Dobrowolski JW, Vohora SB, Sharma K, Shah SA, Naqvi SA, Dandiya PC (1991) Antibacterial, antifungal, antiamoebic, antiinflammatory and antipyretic studies on propolis bee products. J Ethnopharmacol 35:77–82PubMedCrossRef
13.
go back to reference Cheung KW, Sze DM, Chan WK, Deng RX, Tu W, Chan GC (2011) Brazilian green propolis and its constituent, artepillin C inhibits allogeneic activated human CD4 T cells expansion and activation. J Ethnopharmacol 138:463–471PubMedCrossRef Cheung KW, Sze DM, Chan WK, Deng RX, Tu W, Chan GC (2011) Brazilian green propolis and its constituent, artepillin C inhibits allogeneic activated human CD4 T cells expansion and activation. J Ethnopharmacol 138:463–471PubMedCrossRef
14.
go back to reference Park YK, Alencar SM, Aguiar CL (2002) Botanical origin and chemical composition of Brazilian propolis. J Agric Food Chem 50:2502–2506PubMedCrossRef Park YK, Alencar SM, Aguiar CL (2002) Botanical origin and chemical composition of Brazilian propolis. J Agric Food Chem 50:2502–2506PubMedCrossRef
15.
go back to reference Ugur A, Arslan T (2004) An in vitro study on antimicrobial activity of propolis from Mugla province of Turkey. J Med Food 7:90–94PubMedCrossRef Ugur A, Arslan T (2004) An in vitro study on antimicrobial activity of propolis from Mugla province of Turkey. J Med Food 7:90–94PubMedCrossRef
16.
go back to reference Khalil ML (2006) Biological activity of bee propolis in health and disease. Asian Pac J Cancer Prev 7:22–31PubMed Khalil ML (2006) Biological activity of bee propolis in health and disease. Asian Pac J Cancer Prev 7:22–31PubMed
17.
go back to reference Orsolic N, Basic I (2003) Immunomodulation by water-soluble derivative of propolis: a factor of antitumor reactivity. J Ethnopharmacol 84:265–273PubMedCrossRef Orsolic N, Basic I (2003) Immunomodulation by water-soluble derivative of propolis: a factor of antitumor reactivity. J Ethnopharmacol 84:265–273PubMedCrossRef
18.
go back to reference Tani H, Hasumi K, Tatefuji T, Hashimoto K, Koshino H, Takahashi S (2010) Inhibitory activity of Brazilian green propolis components and their derivatives on the release of cys-leukotrienes. Bioorg Med Chem 18:151–157PubMedCrossRef Tani H, Hasumi K, Tatefuji T, Hashimoto K, Koshino H, Takahashi S (2010) Inhibitory activity of Brazilian green propolis components and their derivatives on the release of cys-leukotrienes. Bioorg Med Chem 18:151–157PubMedCrossRef
19.
go back to reference Moura SA, Negri G, Salatino A, Lima LD, Dourado LP, Mendes JB et al. Aqueous extract of Brazilian green propolis: primary components, evaluation of inflammation and wound healing by using subcutaneous implanted sponges. Evid Based Complement Alternat Med, 2009;in press. Moura SA, Negri G, Salatino A, Lima LD, Dourado LP, Mendes JB et al. Aqueous extract of Brazilian green propolis: primary components, evaluation of inflammation and wound healing by using subcutaneous implanted sponges. Evid Based Complement Alternat Med, 2009;in press.
20.
go back to reference Marcucci MC, Ferreres F, Custodio AR, Ferreira MM, Bankova VS, Garcia-Viguera C et al (2000) Evaluation of phenolic compounds in Brazilian propolis from different geographic regions. Z Naturforsch C 55:76–81PubMed Marcucci MC, Ferreres F, Custodio AR, Ferreira MM, Bankova VS, Garcia-Viguera C et al (2000) Evaluation of phenolic compounds in Brazilian propolis from different geographic regions. Z Naturforsch C 55:76–81PubMed
21.
go back to reference de Castro SL, Higashi KO (1995) Effect of different formulations of propolis on mice infected with Trypanosoma cruzi. J Ethnopharmacol 46:55–58PubMedCrossRef de Castro SL, Higashi KO (1995) Effect of different formulations of propolis on mice infected with Trypanosoma cruzi. J Ethnopharmacol 46:55–58PubMedCrossRef
22.
go back to reference Bankova V (2005) Recent trends and important developments in propolis research. Evid Based Complement Alternat Med 2:29–32PubMedCrossRef Bankova V (2005) Recent trends and important developments in propolis research. Evid Based Complement Alternat Med 2:29–32PubMedCrossRef
23.
go back to reference Sawaya AC, Tomazela DM, Cunha IB, Bankova VS, Marcucci MC, Custodio AR et al (2004) Electrospray ionization mass spectrometry fingerprinting of propolis. Analyst 129:739–744PubMedCrossRef Sawaya AC, Tomazela DM, Cunha IB, Bankova VS, Marcucci MC, Custodio AR et al (2004) Electrospray ionization mass spectrometry fingerprinting of propolis. Analyst 129:739–744PubMedCrossRef
24.
go back to reference Hashimoto T, Tori M, Asakawa Y, Wollenweber E (1988) Synthesis of two allergenic constituents of propolis and poplar bud excretion. Z Naturforsch C 43:470–472PubMed Hashimoto T, Tori M, Asakawa Y, Wollenweber E (1988) Synthesis of two allergenic constituents of propolis and poplar bud excretion. Z Naturforsch C 43:470–472PubMed
25.
go back to reference Lin WL, Liang WH, Lee YJ, Chuang SK, Tseng TH (2010) Antitumor progression potential of caffeic acid phenethyl ester involving p75(NTR) in C6 glioma cells. Chem Biol Interact 188:607–615PubMedCrossRef Lin WL, Liang WH, Lee YJ, Chuang SK, Tseng TH (2010) Antitumor progression potential of caffeic acid phenethyl ester involving p75(NTR) in C6 glioma cells. Chem Biol Interact 188:607–615PubMedCrossRef
26.
go back to reference Ang ES, Pavlos NJ, Chai LY, Qi M, Cheng TS, Steer JH et al (2009) Caffeic acid phenethyl ester, an active component of honeybee propolis attenuates osteoclastogenesis and bone resorption via the suppression of RANKL-induced NF-kappaB and NFAT activity. J Cell Physiol 221:642–649PubMedCrossRef Ang ES, Pavlos NJ, Chai LY, Qi M, Cheng TS, Steer JH et al (2009) Caffeic acid phenethyl ester, an active component of honeybee propolis attenuates osteoclastogenesis and bone resorption via the suppression of RANKL-induced NF-kappaB and NFAT activity. J Cell Physiol 221:642–649PubMedCrossRef
27.
go back to reference Park JH, Lee JK, Kim HS, Chung ST, Eom JH, Kim KA et al (2004) Immunomodulatory effect of caffeic acid phenethyl ester in Balb/c mice. Int Immunopharmacol 4:429–436PubMedCrossRef Park JH, Lee JK, Kim HS, Chung ST, Eom JH, Kim KA et al (2004) Immunomodulatory effect of caffeic acid phenethyl ester in Balb/c mice. Int Immunopharmacol 4:429–436PubMedCrossRef
28.
go back to reference Huang MT, Ma W, Yen P, Xie JG, Han J, Frenkel K et al (1996) Inhibitory effects of caffeic acid phenethyl ester (CAPE) on 12-O-tetradecanoylphorbol-13-acetate-induced tumor promotion in mouse skin and the synthesis of DNA, RNA and protein in HeLa cells. Carcinogenesis 17:761–765PubMedCrossRef Huang MT, Ma W, Yen P, Xie JG, Han J, Frenkel K et al (1996) Inhibitory effects of caffeic acid phenethyl ester (CAPE) on 12-O-tetradecanoylphorbol-13-acetate-induced tumor promotion in mouse skin and the synthesis of DNA, RNA and protein in HeLa cells. Carcinogenesis 17:761–765PubMedCrossRef
29.
go back to reference Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB (1996) Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci U S A 93:9090–9095PubMedCrossRef Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB (1996) Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci U S A 93:9090–9095PubMedCrossRef
30.
go back to reference Chen MJ, Chang WH, Lin CC, Liu CY, Wang TE, Chu CH et al (2008) Caffeic acid phenethyl ester induces apoptosis of human pancreatic cancer cells involving caspase and mitochondrial dysfunction. Pancreatology 8:566–576PubMedCrossRef Chen MJ, Chang WH, Lin CC, Liu CY, Wang TE, Chu CH et al (2008) Caffeic acid phenethyl ester induces apoptosis of human pancreatic cancer cells involving caspase and mitochondrial dysfunction. Pancreatology 8:566–576PubMedCrossRef
31.
go back to reference Roos TU, Heiss EH, Schwaiberger AV, Schachner D, Sroka IM, Oberan T et al (2011) Caffeic acid phenethyl ester inhibits PDGF-induced proliferation of vascular smooth muscle cells via activation of p38 MAPK, HIF-1alpha, and heme oxygenase-1. J Nat Prod 74:352–356PubMedCrossRef Roos TU, Heiss EH, Schwaiberger AV, Schachner D, Sroka IM, Oberan T et al (2011) Caffeic acid phenethyl ester inhibits PDGF-induced proliferation of vascular smooth muscle cells via activation of p38 MAPK, HIF-1alpha, and heme oxygenase-1. J Nat Prod 74:352–356PubMedCrossRef
32.
go back to reference Basini G, Baioni L, Bussolati S, Grasselli F, Daquino C, Spatafora C et al (2010) Antiangiogenic properties of an unusual benzo[k, l]xanthene lignan derived from CAPE (caffeic acid phenethyl ester). Invest New Drugs 30:186–190PubMedCrossRef Basini G, Baioni L, Bussolati S, Grasselli F, Daquino C, Spatafora C et al (2010) Antiangiogenic properties of an unusual benzo[k, l]xanthene lignan derived from CAPE (caffeic acid phenethyl ester). Invest New Drugs 30:186–190PubMedCrossRef
33.
go back to reference Marquez N, Sancho R, Macho A, Calzado MA, Fiebich BL, Munoz E (2004) Caffeic acid phenethyl ester inhibits T-cell activation by targeting both nuclear factor of activated T-cells and NF-kappaB transcription factors. J Pharmacol Exp Ther 308:993–1001PubMedCrossRef Marquez N, Sancho R, Macho A, Calzado MA, Fiebich BL, Munoz E (2004) Caffeic acid phenethyl ester inhibits T-cell activation by targeting both nuclear factor of activated T-cells and NF-kappaB transcription factors. J Pharmacol Exp Ther 308:993–1001PubMedCrossRef
34.
go back to reference Wang LC, Lin YL, Liang YC, Yang YH, Lee JH, Yu HH et al (2009) The effect of caffeic acid phenethyl ester on the functions of human monocyte-derived dendritic cells. BMC Immunol 10:39PubMedCrossRef Wang LC, Lin YL, Liang YC, Yang YH, Lee JH, Yu HH et al (2009) The effect of caffeic acid phenethyl ester on the functions of human monocyte-derived dendritic cells. BMC Immunol 10:39PubMedCrossRef
35.
go back to reference Wang LC, Chu KH, Liang YC, Lin YL, Chiang BL (2010) Caffeic acid phenethyl ester inhibits nuclear factor-kappaB and protein kinase B signalling pathways and induces caspase-3 expression in primary human CD4+ T cells. Clin Exp Immunol 160:223–232PubMedCrossRef Wang LC, Chu KH, Liang YC, Lin YL, Chiang BL (2010) Caffeic acid phenethyl ester inhibits nuclear factor-kappaB and protein kinase B signalling pathways and induces caspase-3 expression in primary human CD4+ T cells. Clin Exp Immunol 160:223–232PubMedCrossRef
36.
go back to reference Kimoto T, Arai S, Aga M, Hanaya T, Kohguchi M, Nomura Y et al (1996) Cell cycle and apoptosis in cancer induced by the artepillin C extracted from Brazilian propolis. Gan To Kagaku Ryoho 23:1855–1859PubMed Kimoto T, Arai S, Aga M, Hanaya T, Kohguchi M, Nomura Y et al (1996) Cell cycle and apoptosis in cancer induced by the artepillin C extracted from Brazilian propolis. Gan To Kagaku Ryoho 23:1855–1859PubMed
37.
go back to reference Kimoto T, Arai S, Kohguchi M, Aga M, Nomura Y, Micallef MJ et al (1998) Apoptosis and suppression of tumor growth by artepillin C extracted from Brazilian propolis. Cancer Detect Prev 22:506–515PubMedCrossRef Kimoto T, Arai S, Kohguchi M, Aga M, Nomura Y, Micallef MJ et al (1998) Apoptosis and suppression of tumor growth by artepillin C extracted from Brazilian propolis. Cancer Detect Prev 22:506–515PubMedCrossRef
38.
go back to reference Kimoto T, Aga M, Hino K, Koya-Miyata S, Yamamoto Y, Micallef MJ et al (2001) Apoptosis of human leukemia cells induced by Artepillin C, an active ingredient of Brazilian propolis. Anticancer Res 21:221–228PubMed Kimoto T, Aga M, Hino K, Koya-Miyata S, Yamamoto Y, Micallef MJ et al (2001) Apoptosis of human leukemia cells induced by Artepillin C, an active ingredient of Brazilian propolis. Anticancer Res 21:221–228PubMed
39.
go back to reference Shimizu K, Ashida H, Matsuura Y, Kanazawa K (2004) Antioxidative bioavailability of artepillin C in Brazilian propolis. Arch Biochem Biophys 424:181–188PubMedCrossRef Shimizu K, Ashida H, Matsuura Y, Kanazawa K (2004) Antioxidative bioavailability of artepillin C in Brazilian propolis. Arch Biochem Biophys 424:181–188PubMedCrossRef
40.
go back to reference Paulino N, Abreu SR, Uto Y, Koyama D, Nagasawa H, Hori H et al (2008) Anti-inflammatory effects of a bioavailable compound, artepillin C, in Brazilian propolis. Eur J Pharmacol 587:296–301PubMedCrossRef Paulino N, Abreu SR, Uto Y, Koyama D, Nagasawa H, Hori H et al (2008) Anti-inflammatory effects of a bioavailable compound, artepillin C, in Brazilian propolis. Eur J Pharmacol 587:296–301PubMedCrossRef
41.
go back to reference Shimizu K, Das SK, Hashimoto T, Sowa Y, Yoshida T, Sakai T et al (2005) Artepillin C in Brazilian propolis induces G(0)/G(1) arrest via stimulation of Cip1/p21 expression in human colon cancer cells. Mol Carcinog 44:293–299PubMedCrossRef Shimizu K, Das SK, Hashimoto T, Sowa Y, Yoshida T, Sakai T et al (2005) Artepillin C in Brazilian propolis induces G(0)/G(1) arrest via stimulation of Cip1/p21 expression in human colon cancer cells. Mol Carcinog 44:293–299PubMedCrossRef
42.
go back to reference Messerli SM, Ahn MR, Kunimasa K, Yanagihara M, Tatefuji T, Hashimoto K et al (2009) Artepillin C (ARC) in Brazilian green propolis selectively blocks oncogenic PAK1 signaling and suppresses the growth of NF tumors in mice. Phytother Res 23:423–427PubMedCrossRef Messerli SM, Ahn MR, Kunimasa K, Yanagihara M, Tatefuji T, Hashimoto K et al (2009) Artepillin C (ARC) in Brazilian green propolis selectively blocks oncogenic PAK1 signaling and suppresses the growth of NF tumors in mice. Phytother Res 23:423–427PubMedCrossRef
43.
go back to reference Kimoto T, Koya-Miyata S, Hino K, Micallef MJ, Hanaya T, Arai S et al (2001) Pulmonary carcinogenesis induced by ferric nitrilotriacetate in mice and protection from it by Brazilian propolis and artepillin C. Virchows Arch 438:259–270PubMedCrossRef Kimoto T, Koya-Miyata S, Hino K, Micallef MJ, Hanaya T, Arai S et al (2001) Pulmonary carcinogenesis induced by ferric nitrilotriacetate in mice and protection from it by Brazilian propolis and artepillin C. Virchows Arch 438:259–270PubMedCrossRef
44.
go back to reference Landmann R, Knopf HP, Link S, Sansano S, Schumann R, Zimmerli W (1996) Human monocyte CD14 is upregulated by lipopolysaccharide. Infect Immun 64:1762–1769PubMed Landmann R, Knopf HP, Link S, Sansano S, Schumann R, Zimmerli W (1996) Human monocyte CD14 is upregulated by lipopolysaccharide. Infect Immun 64:1762–1769PubMed
45.
go back to reference Blonska M, Bronikowska J, Pietsz G, Czuba ZP, Scheller S, Krol W (2004) Effects of ethanol extract of propolis (EEP) and its flavones on inducible gene expression in J774A.1 macrophages. J Ethnopharmacol 91:25–30PubMedCrossRef Blonska M, Bronikowska J, Pietsz G, Czuba ZP, Scheller S, Krol W (2004) Effects of ethanol extract of propolis (EEP) and its flavones on inducible gene expression in J774A.1 macrophages. J Ethnopharmacol 91:25–30PubMedCrossRef
46.
go back to reference Ansorge S, Reinhold D, Lendeckel U (2003) Propolis and some of its constituents down-regulate DNA synthesis and inflammatory cytokine production but induce TGF-beta1 production of human immune cells. Z Naturforsch C 58:580–589PubMed Ansorge S, Reinhold D, Lendeckel U (2003) Propolis and some of its constituents down-regulate DNA synthesis and inflammatory cytokine production but induce TGF-beta1 production of human immune cells. Z Naturforsch C 58:580–589PubMed
47.
go back to reference Pagliarone AC, Orsatti CL, Bufalo MC, Missima F, Bachiega TF, Junior JP et al (2009) Propolis effects on pro-inflammatory cytokine production and Toll-like receptor 2 and 4 expression in stressed mice. Int Immunopharmacol 9:1352–1356PubMedCrossRef Pagliarone AC, Orsatti CL, Bufalo MC, Missima F, Bachiega TF, Junior JP et al (2009) Propolis effects on pro-inflammatory cytokine production and Toll-like receptor 2 and 4 expression in stressed mice. Int Immunopharmacol 9:1352–1356PubMedCrossRef
48.
go back to reference De Castro SL. Propolis: biological and pharmacological activities. Therapeutic uses of bee product. Annual Review of Biomedical Science; 2001, p. 49-83. De Castro SL. Propolis: biological and pharmacological activities. Therapeutic uses of bee product. Annual Review of Biomedical Science; 2001, p. 49-83.
49.
go back to reference Marcucci MC (1995) Propolis: chemical composition, biological properties and therapeutic activity. Apidologie 26:83–89CrossRef Marcucci MC (1995) Propolis: chemical composition, biological properties and therapeutic activity. Apidologie 26:83–89CrossRef
50.
go back to reference Cole N, Sou PW, Ngo A, Tsang KH, Severino JA, Arun SJ et al (2010) Topical ‘Sydney’ propolis protects against UV-radiation-induced inflammation, lipid peroxidation and immune suppression in mouse skin. Int Arch Allergy Immunol 152:87–97PubMedCrossRef Cole N, Sou PW, Ngo A, Tsang KH, Severino JA, Arun SJ et al (2010) Topical ‘Sydney’ propolis protects against UV-radiation-induced inflammation, lipid peroxidation and immune suppression in mouse skin. Int Arch Allergy Immunol 152:87–97PubMedCrossRef
51.
go back to reference Said RA, Grassi TF, Scolastici C, de Lima RO Alves, Darros BR, Barbisan LF et al (2010) Absence of chemopreventive influence of propolis on the rat liver altered foci development. Exp Toxicol Pathol 62:405–412PubMedCrossRef Said RA, Grassi TF, Scolastici C, de Lima RO Alves, Darros BR, Barbisan LF et al (2010) Absence of chemopreventive influence of propolis on the rat liver altered foci development. Exp Toxicol Pathol 62:405–412PubMedCrossRef
52.
go back to reference Kawase A, Matsumoto Y, Hadano M, Ishii Y, Iwaki M (2009) Differential effects of chrysin on nitrofurantoin pharmacokinetics mediated by intestinal breast cancer resistance protein in rats and mice. J Pharm Pharm Sci 12:150–163PubMed Kawase A, Matsumoto Y, Hadano M, Ishii Y, Iwaki M (2009) Differential effects of chrysin on nitrofurantoin pharmacokinetics mediated by intestinal breast cancer resistance protein in rats and mice. J Pharm Pharm Sci 12:150–163PubMed
53.
go back to reference Khan MS, Halagowder D, Devaraj SN (2011) Methylated chrysin induces co-ordinated attenuation of the canonical Wnt and NF-kB signaling pathway and upregulates apoptotic gene expression in the early hepatocarcinogenesis rat model. Chem Biol Interact 193:12–21PubMedCrossRef Khan MS, Halagowder D, Devaraj SN (2011) Methylated chrysin induces co-ordinated attenuation of the canonical Wnt and NF-kB signaling pathway and upregulates apoptotic gene expression in the early hepatocarcinogenesis rat model. Chem Biol Interact 193:12–21PubMedCrossRef
54.
go back to reference Badr MO, Edrees NM, Abdallah AA, El-Deen NA, Neamat-Allah AN, Ismail HT (2011) Anti-tumour effects of Egyptian propolis on Ehrlich ascites carcinoma. Vet Ital 47:341–350PubMed Badr MO, Edrees NM, Abdallah AA, El-Deen NA, Neamat-Allah AN, Ismail HT (2011) Anti-tumour effects of Egyptian propolis on Ehrlich ascites carcinoma. Vet Ital 47:341–350PubMed
55.
go back to reference Omene CO, Wu J, Frenkel K. Caffeic Acid Phenethyl Ester (CAPE) derived from propolis, a honeybee product, inhibits growth of breast cancer stem cells. Invest New Drugs, 2011;in press. Omene CO, Wu J, Frenkel K. Caffeic Acid Phenethyl Ester (CAPE) derived from propolis, a honeybee product, inhibits growth of breast cancer stem cells. Invest New Drugs, 2011;in press.
56.
go back to reference Demestre M, Messerli SM, Celli N, Shahhossini M, Kluwe L, Mautner V et al (2009) CAPE (caffeic acid phenethyl ester)-based propolis extract (Bio 30) suppresses the growth of human neurofibromatosis (NF) tumor xenografts in mice. Phytother Res 23:226–230PubMedCrossRef Demestre M, Messerli SM, Celli N, Shahhossini M, Kluwe L, Mautner V et al (2009) CAPE (caffeic acid phenethyl ester)-based propolis extract (Bio 30) suppresses the growth of human neurofibromatosis (NF) tumor xenografts in mice. Phytother Res 23:226–230PubMedCrossRef
57.
go back to reference Jung BI, Kim MS, Kim HA, Kim D, Yang J, Her S et al (2010) Caffeic acid phenethyl ester, a component of beehive propolis, is a novel selective estrogen receptor modulator. Phytother Res 24:295–300PubMed Jung BI, Kim MS, Kim HA, Kim D, Yang J, Her S et al (2010) Caffeic acid phenethyl ester, a component of beehive propolis, is a novel selective estrogen receptor modulator. Phytother Res 24:295–300PubMed
58.
go back to reference Ahn MR, Kunimasa K, Ohta T, Kumazawa S, Kamihira M, Kaji K et al (2007) Suppression of tumor-induced angiogenesis by Brazilian propolis: major component artepillin C inhibits in vitro tube formation and endothelial cell proliferation. Cancer Lett 252:235–243PubMedCrossRef Ahn MR, Kunimasa K, Ohta T, Kumazawa S, Kamihira M, Kaji K et al (2007) Suppression of tumor-induced angiogenesis by Brazilian propolis: major component artepillin C inhibits in vitro tube formation and endothelial cell proliferation. Cancer Lett 252:235–243PubMedCrossRef
59.
go back to reference Kunimasa K, Ahn MR, Kobayashi T, Eguchi R, Kumazawa S, Fujimori Y et al. Brazilian propolis suppresses angiogenesis by inducing apoptosis in tube-forming endothelial cells through inactivation of survival signal ERK1/2. Evid Based Complement Alternat Med, 2009;in press. Kunimasa K, Ahn MR, Kobayashi T, Eguchi R, Kumazawa S, Fujimori Y et al. Brazilian propolis suppresses angiogenesis by inducing apoptosis in tube-forming endothelial cells through inactivation of survival signal ERK1/2. Evid Based Complement Alternat Med, 2009;in press.
60.
go back to reference Izuta H, Shimazawa M, Tsuruma K, Araki Y, Mishima S, Hara H (2009) Bee products prevent VEGF-induced angiogenesis in human umbilical vein endothelial cells. BMC Complement Altern Med 9:45PubMedCrossRef Izuta H, Shimazawa M, Tsuruma K, Araki Y, Mishima S, Hara H (2009) Bee products prevent VEGF-induced angiogenesis in human umbilical vein endothelial cells. BMC Complement Altern Med 9:45PubMedCrossRef
61.
go back to reference Chikaraishi Y, Izuta H, Shimazawa M, Mishima S, Hara H (2009) Angiostatic effects of Brazilian green propolis and its chemical constituents. Mol Nutr Food Res 54:566–575CrossRef Chikaraishi Y, Izuta H, Shimazawa M, Mishima S, Hara H (2009) Angiostatic effects of Brazilian green propolis and its chemical constituents. Mol Nutr Food Res 54:566–575CrossRef
62.
go back to reference Sze DM, Brown R, Yang S, Ho PJ, Gibson J, Joshua D (2006) The use of thalidomide in myeloma therapy as an effective anticancer drug. Curr Cancer Drug Targets 6:325–331PubMedCrossRef Sze DM, Brown R, Yang S, Ho PJ, Gibson J, Joshua D (2006) The use of thalidomide in myeloma therapy as an effective anticancer drug. Curr Cancer Drug Targets 6:325–331PubMedCrossRef
63.
go back to reference Fung KL, Liang RH, Chan GC (2009) Vincristine but not imatinib could suppress mesenchymal niche's support to lymphoid leukemic cells. Leuk Lymphoma 51:515–522CrossRef Fung KL, Liang RH, Chan GC (2009) Vincristine but not imatinib could suppress mesenchymal niche's support to lymphoid leukemic cells. Leuk Lymphoma 51:515–522CrossRef
64.
go back to reference Lee KW, Kang NJ, Kim JH, Lee KM, Lee DE, Hur HJ et al (2008) Caffeic acid phenethyl ester inhibits invasion and expression of matrix metalloproteinase in SK-Hep1 human hepatocellular carcinoma cells by targeting nuclear factor kappa B. Genes Nutr 2:319–322PubMedCrossRef Lee KW, Kang NJ, Kim JH, Lee KM, Lee DE, Hur HJ et al (2008) Caffeic acid phenethyl ester inhibits invasion and expression of matrix metalloproteinase in SK-Hep1 human hepatocellular carcinoma cells by targeting nuclear factor kappa B. Genes Nutr 2:319–322PubMedCrossRef
65.
go back to reference Hattori H, Okuda K, Murase T, Shigetsura Y, Narise K, Semenza GL et al (2011) Isolation, identification, and biological evaluation of HIF-1-modulating compounds from Brazilian green propolis. Bioorg Med Chem 19:5392–5401PubMedCrossRef Hattori H, Okuda K, Murase T, Shigetsura Y, Narise K, Semenza GL et al (2011) Isolation, identification, and biological evaluation of HIF-1-modulating compounds from Brazilian green propolis. Bioorg Med Chem 19:5392–5401PubMedCrossRef
66.
go back to reference Padmavathi R, Senthilnathan P, Chodon D, Sakthisekaran D (2006) Therapeutic effect of paclitaxel and propolis on lipid peroxidation and antioxidant system in 7,12 dimethyl benz(a)anthracene-induced breast cancer in female Sprague Dawley rats. Life Sci 78:2820–2825PubMedCrossRef Padmavathi R, Senthilnathan P, Chodon D, Sakthisekaran D (2006) Therapeutic effect of paclitaxel and propolis on lipid peroxidation and antioxidant system in 7,12 dimethyl benz(a)anthracene-induced breast cancer in female Sprague Dawley rats. Life Sci 78:2820–2825PubMedCrossRef
67.
go back to reference Orsolic N, Benkovic V, Lisicic D, Dikic D, Erhardt J, Knezevic AH (2009) Protective effects of propolis and related polyphenolic/flavonoid compounds against toxicity induced by irinotecan. Med Oncol 27:1346–1358PubMedCrossRef Orsolic N, Benkovic V, Lisicic D, Dikic D, Erhardt J, Knezevic AH (2009) Protective effects of propolis and related polyphenolic/flavonoid compounds against toxicity induced by irinotecan. Med Oncol 27:1346–1358PubMedCrossRef
68.
go back to reference Albukhari AA, Gashlan HM, El-Beshbishy HA, Nagy AA, Abdel-Naim AB (2009) Caffeic acid phenethyl ester protects against tamoxifen-induced hepatotoxicity in rats. Food Chem Toxicol 47:1689–1695PubMedCrossRef Albukhari AA, Gashlan HM, El-Beshbishy HA, Nagy AA, Abdel-Naim AB (2009) Caffeic acid phenethyl ester protects against tamoxifen-induced hepatotoxicity in rats. Food Chem Toxicol 47:1689–1695PubMedCrossRef
69.
go back to reference Orsolic N, Basic I (2005) Antitumor, hematostimulative and radioprotective action of water-soluble derivative of propolis (WSDP). Biomed Pharmacother 59:561–570PubMedCrossRef Orsolic N, Basic I (2005) Antitumor, hematostimulative and radioprotective action of water-soluble derivative of propolis (WSDP). Biomed Pharmacother 59:561–570PubMedCrossRef
70.
go back to reference Zedan H, Hofny ER, Ismail SA (2009) Propolis as an alternative treatment for cutaneous warts. Int J Dermatol 48:1246–1249PubMedCrossRef Zedan H, Hofny ER, Ismail SA (2009) Propolis as an alternative treatment for cutaneous warts. Int J Dermatol 48:1246–1249PubMedCrossRef
71.
go back to reference Iljazovic E, Ljuca D, Sahimpasic A, Avdic S (2006) Efficacy in treatment of cervical HRHPV infection by combination of beta interferon, and herbal therapy in woman with different cervical lesions. Bosn J Basic Med Sci 6:79–84PubMed Iljazovic E, Ljuca D, Sahimpasic A, Avdic S (2006) Efficacy in treatment of cervical HRHPV infection by combination of beta interferon, and herbal therapy in woman with different cervical lesions. Bosn J Basic Med Sci 6:79–84PubMed
72.
go back to reference Coelho LG, Bastos EM, Resende CC, Silva CM Paula e, Sanches BS, de Castro FJ et al (2007) Brazilian green propolis on Helicobacter pylori infection. a pilot clinical study. Helicobacter 12:572–574PubMedCrossRef Coelho LG, Bastos EM, Resende CC, Silva CM Paula e, Sanches BS, de Castro FJ et al (2007) Brazilian green propolis on Helicobacter pylori infection. a pilot clinical study. Helicobacter 12:572–574PubMedCrossRef
73.
go back to reference Chirumbolo S (2011) Propolis as anti-inflammatory and anti-allergic compounds: which role for flavonoids? Int Immunopharmacol 11:1386–1387PubMedCrossRef Chirumbolo S (2011) Propolis as anti-inflammatory and anti-allergic compounds: which role for flavonoids? Int Immunopharmacol 11:1386–1387PubMedCrossRef
74.
go back to reference de Castro PA, Savoldi M, Bonatto D, Barros MH, Goldman MH, Berretta AA et al (2011) Molecular characterization of propolis-induced cell death in Saccharomyces cerevisiae. Eukaryot Cell 10:398–411PubMedCrossRef de Castro PA, Savoldi M, Bonatto D, Barros MH, Goldman MH, Berretta AA et al (2011) Molecular characterization of propolis-induced cell death in Saccharomyces cerevisiae. Eukaryot Cell 10:398–411PubMedCrossRef
75.
go back to reference Freitas JA, Vanat N, Pinheiro JW, Balarin MR, Sforcin JM, Venancio EJ (2011) The effects of propolis on antibody production by laying hens. Poult Sci 90:1227–1233PubMedCrossRef Freitas JA, Vanat N, Pinheiro JW, Balarin MR, Sforcin JM, Venancio EJ (2011) The effects of propolis on antibody production by laying hens. Poult Sci 90:1227–1233PubMedCrossRef
76.
go back to reference Zhu W, Chen M, Shou Q, Li Y, Hu F (2011) Biological activities of Chinese propolis and Brazilian propolis on streptozotocin-induced type 1 diabetes mellitus in rats. Evid Based Complement Alternat Med 2011:468529PubMed Zhu W, Chen M, Shou Q, Li Y, Hu F (2011) Biological activities of Chinese propolis and Brazilian propolis on streptozotocin-induced type 1 diabetes mellitus in rats. Evid Based Complement Alternat Med 2011:468529PubMed
77.
go back to reference Venkatesha SH, Berman BM, Moudgil KD (2011) Herbal medicinal products target defined biochemical and molecular mediators of inflammatory autoimmune arthritis. Bioorg Med Chem 19:21–29PubMedCrossRef Venkatesha SH, Berman BM, Moudgil KD (2011) Herbal medicinal products target defined biochemical and molecular mediators of inflammatory autoimmune arthritis. Bioorg Med Chem 19:21–29PubMedCrossRef
78.
go back to reference Hsieh CC, Lin BF (2011) Dietary factors regulate cytokines in murine models of systemic lupus erythematosus. Autoimmun Rev 11:22–27PubMedCrossRef Hsieh CC, Lin BF (2011) Dietary factors regulate cytokines in murine models of systemic lupus erythematosus. Autoimmun Rev 11:22–27PubMedCrossRef
79.
go back to reference Pagliarone AC, Missima F, Orsatti CL, Bachiega TF, Sforcin JM (2009) Propolis effect on Th1/Th2 cytokines production by acutely stressed mice. J Ethnopharmacol 125:230–233PubMedCrossRef Pagliarone AC, Missima F, Orsatti CL, Bachiega TF, Sforcin JM (2009) Propolis effect on Th1/Th2 cytokines production by acutely stressed mice. J Ethnopharmacol 125:230–233PubMedCrossRef
80.
go back to reference Sa-Nunes A, Faccioli LH, Sforcin JM (2003) Propolis: lymphocyte proliferation and IFN-gamma production. J Ethnopharmacol 87:93–97PubMedCrossRef Sa-Nunes A, Faccioli LH, Sforcin JM (2003) Propolis: lymphocyte proliferation and IFN-gamma production. J Ethnopharmacol 87:93–97PubMedCrossRef
81.
go back to reference Hu F, Hepburn HR, Li Y, Chen M, Radloff SE, Daya S (2005) Effects of ethanol and water extracts of propolis (bee glue) on acute inflammatory animal models. J Ethnopharmacol 100:276–283PubMedCrossRef Hu F, Hepburn HR, Li Y, Chen M, Radloff SE, Daya S (2005) Effects of ethanol and water extracts of propolis (bee glue) on acute inflammatory animal models. J Ethnopharmacol 100:276–283PubMedCrossRef
82.
go back to reference Girgin G, Baydar T, Ledochowski M, Schennach H, Bolukbasi DN, Sorkun K et al (2009) Immunomodulatory effects of Turkish propolis: changes in neopterin release and tryptophan degradation. Immunobiology 214:129–134PubMedCrossRef Girgin G, Baydar T, Ledochowski M, Schennach H, Bolukbasi DN, Sorkun K et al (2009) Immunomodulatory effects of Turkish propolis: changes in neopterin release and tryptophan degradation. Immunobiology 214:129–134PubMedCrossRef
83.
go back to reference Orsi RO, Sforcin JM, Funari SR, Bankova V (2005) Effects of Brazilian and Bulgarian propolis on bactericidal activity of macrophages against Salmonella typhimurium. Int Immunopharmacol 5:359–368PubMedCrossRef Orsi RO, Sforcin JM, Funari SR, Bankova V (2005) Effects of Brazilian and Bulgarian propolis on bactericidal activity of macrophages against Salmonella typhimurium. Int Immunopharmacol 5:359–368PubMedCrossRef
84.
go back to reference Song YS, Park EH, Hur GM, Ryu YS, Kim YM, Jin C (2002) Ethanol extract of propolis inhibits nitric oxide synthase gene expression and enzyme activity. J Ethnopharmacol 80:155–161PubMedCrossRef Song YS, Park EH, Hur GM, Ryu YS, Kim YM, Jin C (2002) Ethanol extract of propolis inhibits nitric oxide synthase gene expression and enzyme activity. J Ethnopharmacol 80:155–161PubMedCrossRef
85.
go back to reference Sforcin JM, Orsi RO, Bankova V (2005) Effect of propolis, some isolated compounds and its source plant on antibody production. J Ethnopharmacol 98:301–305PubMedCrossRef Sforcin JM, Orsi RO, Bankova V (2005) Effect of propolis, some isolated compounds and its source plant on antibody production. J Ethnopharmacol 98:301–305PubMedCrossRef
86.
go back to reference Orsatti CL, Missima F, Pagliarone AC, Bachiega TF, Bufalo MC, Araujo JP Jr et al (2010) Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice. Phytother Res 24:1141–1146PubMed Orsatti CL, Missima F, Pagliarone AC, Bachiega TF, Bufalo MC, Araujo JP Jr et al (2010) Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice. Phytother Res 24:1141–1146PubMed
87.
go back to reference Claus R, Kinscherf R, Gehrke C, Bonaterra G, Basnet P, Metz J et al (2000) Antiapoptotic effects of propolis extract and propol on human macrophages exposed to minimally modified low density lipoprotein. Arzneimittelforschung 50:373–379PubMed Claus R, Kinscherf R, Gehrke C, Bonaterra G, Basnet P, Metz J et al (2000) Antiapoptotic effects of propolis extract and propol on human macrophages exposed to minimally modified low density lipoprotein. Arzneimittelforschung 50:373–379PubMed
88.
go back to reference Murad JM, Calvi SA, Soares AM, Bankova V, Sforcin JM (2002) Effects of propolis from Brazil and Bulgaria on fungicidal activity of macrophages against Paracoccidioides brasiliensis. J Ethnopharmacol 79:331–334PubMedCrossRef Murad JM, Calvi SA, Soares AM, Bankova V, Sforcin JM (2002) Effects of propolis from Brazil and Bulgaria on fungicidal activity of macrophages against Paracoccidioides brasiliensis. J Ethnopharmacol 79:331–334PubMedCrossRef
Metadata
Title
The Immunomodulatory and Anticancer Properties of Propolis
Authors
Godfrey Chi-Fung Chan
Ka-Wai Cheung
Daniel Man-Yuen Sze
Publication date
01-06-2013
Publisher
Humana Press Inc
Published in
Clinical Reviews in Allergy & Immunology / Issue 3/2013
Print ISSN: 1080-0549
Electronic ISSN: 1559-0267
DOI
https://doi.org/10.1007/s12016-012-8322-2

Other articles of this Issue 3/2013

Clinical Reviews in Allergy & Immunology 3/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.