The immunomodulatory and anticancer properties of propolis

Clinical Reviews in Allergy and Immunology

Volumn 44, Issue 3, 2013, Pages 262-273

  Chan, Godfrey Chi Fung ^a   Cheung, Ka Wai ^b   Sze, Daniel Man Yuen ^c  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

Author keywords

Anticancer; Immune; Propolis

Indexed keywords

ALDEHYDE DERIVATIVE; AROMATIC COMPOUND; ARTEPILLIN C; CAFFEIC ACID PHENETHYL ESTER; CALCIUM; CYTOKINE; ESSENTIAL OIL; FLAVONOID; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOMODULATING AGENT; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; IRON; KETONE DERIVATIVE; MAGNESIUM; NICKEL; PHENOL; POLYPHENOL DERIVATIVE; PROPOLIS; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; UNINDEXED DRUG; VITAMIN; WAX; ZINC;

ANTIANGIOGENIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BRAZIL; CANCER CELL; CANCER STEM CELL; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CELL SURVIVAL; CHEMICAL COMPOSITION; COLORIMETRY; CYTOKINE PRODUCTION; DRUG BIOAVAILABILITY; DRUG DETERMINATION; DRUG EFFICACY; DRUG SAFETY; DRUG SYNTHESIS; HUMAN; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MACROPHAGE ACTIVATION; NONHUMAN; ONCOGENE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TUMOR MICROENVIRONMENT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CAFFEIC ACIDS; CELL LINE, TUMOR; HUMANS; IMMUNOLOGIC FACTORS; NEOPLASMS; NEOPLASTIC STEM CELLS; ONCOGENE PROTEINS; PHENYLETHYL ALCOHOL; PHENYLPROPIONATES; PROPOLIS; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TUMOR MICROENVIRONMENT;

EID: 84877876080     PISSN: 10800549     EISSN: 15590267     Source Type: Journal    
DOI: 10.1007/s12016-012-8322-2     Document Type: Review

References (88)

1. Burdock GA (1998) Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol 36:347-363 (Pubitemid 28255348)
2. 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 74:105-112 (Pubitemid 32141092)
3. Salatino A, Teixeira EW, Negri G, Message D (2005) Origin and chemical variation of Brazilian propolis. Evid Based Complement Alternat Med 2:33-38 (Pubitemid 41399512)
4. Castaldo S, Capasso F (2002) Propolis, an old remedy used in modern medicine. Fitoterapia 73(Suppl 1):S1-S6 (Pubitemid 35472198)
5. 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 72:239-246
6. 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-S63 (Pubitemid 35472204)
7. 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 48:5226-5230
8. Pileggi R, Antony K, Johnson K, Zuo J, Shannon Holliday L (2009) Propolis inhibits osteoclast maturation. Dent Traumatol 25:584-588
9. van Ketel WG, Bruynzeel DP (1992) Occupational dermatitis in an accordion repairer. Contact Dermatitis 27:186
10. Han SK, Yamauchi K, Park HK (2001) Effect of nitrite and propolis preservative on volatile basic nitrogen changes in meat products. Microbios 105:71-75 (Pubitemid 33689326)
11. 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 54:401-405 (Pubitemid 29337459)
12. 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 35:77-82
13. 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 138:463-471
14. Park YK, Alencar SM, Aguiar CL (2002) Botanical origin and chemical composition of Brazilian propolis. J Agric Food Chem 50:2502-2506 (Pubitemid 34437358)
15. Ugur A, Arslan T (2004) An in vitro study on antimicrobial activity of propolis from Mugla province of Turkey. J Med Food 7:90-94 (Pubitemid 38445928)
16. Khalil ML (2006) Biological activity of bee propolis in health and disease. Asian Pac J Cancer Prev 7:22-31
17. Orsolic N, Basic I (2003) Immunomodulation by water-soluble derivative of propolis: a factor of antitumor reactivity. J Ethnopharmacol 84:265-273 (Pubitemid 36324266)
18. 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 18:151-157
19. 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. 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 55:76-81 (Pubitemid 30152868)
21. de Castro SL, Higashi KO (1995) Effect of different formulations of propolis on mice infected with Trypanosoma cruzi. J Ethnopharmacol 46:55-58
22. Bankova V (2005) Recent trends and important developments in propolis research. Evid Based Complement Alternat Med 2:29-32 (Pubitemid 41399511)
23. Sawaya AC, Tomazela DM, Cunha IB, Bankova VS, Marcucci MC, Custodio AR et al (2004) Electrospray ionization mass spectrometry fingerprinting of propolis. Analyst 129:739-744 (Pubitemid 39120520)
24. Hashimoto T, Tori M, Asakawa Y, Wollenweber E (1988) Synthesis of two allergenic constituents of propolis and poplar bud excretion. Z Naturforsch C 43:470-472
25. 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 188:607-615
26. 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 221:642-649
27. 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 4:429-436 (Pubitemid 38375975)
28. 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 17:761-765 (Pubitemid 26129690)
29. 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 93:9090-9095 (Pubitemid 26282023)
30. 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 8:566-576
31. 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 74:352-356
32. 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 30:186-190
33. 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 308:993-1001 (Pubitemid 38263975)
34. 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 10:39
35. 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 160:223-232
36. 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 23:1855-1859 (Pubitemid 26398843)
37. 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 22:506-515 (Pubitemid 28537432)
38. 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 21:221-228 (Pubitemid 32267646)
39. Shimizu K, Ashida H, Matsuura Y, Kanazawa K (2004) Antioxidative bioavailability of artepillin C in Brazilian propolis. Arch Biochem Biophys 424:181-188 (Pubitemid 38401951)
40. 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 587:296-301
41. 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 44:293-299 (Pubitemid 41780753)
42. 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 23:423-427
43. 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 438:259-270 (Pubitemid 32247167)
44. Landmann R, Knopf HP, Link S, Sansano S, Schumann R, Zimmerli W (1996) Human monocyte CD14 is upregulated by lipopolysaccharide. Infect Immun 64:1762-1769 (Pubitemid 26129837)
45. 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 91:25-30 (Pubitemid 38270223)
46. 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 58:580-589 (Pubitemid 36971463)
47. 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 9:1352-1356
48. De Castro SL. Propolis: biological and pharmacological activities. Therapeutic uses of bee product. Annual Review of Biomedical Science; 2001, p. 49-83.
49. Marcucci MC (1995) Propolis: chemical composition, biological properties and therapeutic activity. Apidologie 26:83-89
50. 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 152:87-97
51. 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 62:405-412
52. 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 12:150-163
53. 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 193:12-21
54. 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 47:341-350
55. 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. 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 23:226-230
57. 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 24:295-300
58. 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 252:235-243 (Pubitemid 46809795)
59. 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. 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 9:45
61. 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 54:566-575
62. 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 6:325-331 (Pubitemid 43961867)
63. Fung KL, Liang RH, Chan GC (2009) Vincristine but not imatinib could suppress mesenchymal niche's support to lymphoid leukemic cells. Leuk Lymphoma 51:515-522
64. 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 2:319-322 (Pubitemid 351447705)
65. 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 19:5392-5401
66. 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 78:2820-2825
67. 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 27:1346-1358
68. 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 47:1689-1695
69. Orsolic N, Basic I (2005) Antitumor, hematostimulative and radioprotective action of water-soluble derivative of propolis (WSDP). Biomed Pharmacother 59:561-570 (Pubitemid 41820386)
70. Zedan H, Hofny ER, Ismail SA (2009) Propolis as an alternative treatment for cutaneous warts. Int J Dermatol 48:1246-1249
71. 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 6:79-84
72. 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 12:572-574 (Pubitemid 47312389)
73. Chirumbolo S (2011) Propolis as anti-inflammatory and anti-allergic compounds: which role for flavonoids? Int Immunopharmacol 11:1386-1387
74. 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 10:398-411
75. 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 90:1227-1233
76. 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 2011:468529
77. Venkatesha SH, Berman BM, Moudgil KD (2011) Herbal medicinal products target defined biochemical and molecular mediators of inflammatory autoimmune arthritis. Bioorg Med Chem 19:21-29
78. Hsieh CC, Lin BF (2011) Dietary factors regulate cytokines in murine models of systemic lupus erythematosus. Autoimmun Rev 11:22-27
79. Pagliarone AC, Missima F, Orsatti CL, Bachiega TF, Sforcin JM (2009) Propolis effect on Th1/Th2 cytokines production by acutely stressed mice. J Ethnopharmacol 125:230-233
80. Sa-Nunes A, Faccioli LH, Sforcin JM (2003) Propolis: lymphocyte proliferation and IFN-gamma production. J Ethnopharmacol 87:93-97 (Pubitemid 36644979)
81. 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 100:276-283 (Pubitemid 41213289)
82. 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 214:129-134
83. 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 5:359-368 (Pubitemid 40126359)
84. 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 80:155-161 (Pubitemid 34462202)
85. Sforcin JM, Orsi RO, Bankova V (2005) Effect of propolis, some isolated compounds and its source plant on antibody production. J Ethnopharmacol 98:301-305 (Pubitemid 40461985)
86. 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 24:1141-1146
87. 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 50:373-379 (Pubitemid 30217129)
88. 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 79:331-334 (Pubitemid 34155352)