2,748
Views
106
CrossRef citations to date
0
Altmetric
REVIEW

Emerging Adjuvant Therapy for Cancer: Propolis and its Constituents

REFERENCES

  • Abdulrhman M, Elbarbary NS, Ahmed Amin D, Saeid Ebrahim R. Honey and a mixture of honey, beeswax, and olive oil-propolis extract in treatment of chemotherapy-induced oral mucositis: a randomized controlled pilot study. Pediatr Hematol Oncol. 2012;29(3):285–92.
  • Ahn J-C, Biswas R, Chung P-S. Synergistic effect of radachlorin mediated photodynamic therapy on propolis induced apoptosis in AMC-HN-4 cell lines via caspase dependent pathway. Photodiagnosis Photodyn Ther. 2013;10(3):236–43.
  • Al-Hariri MT. Propolis and its direct and indirect hypoglycemic effect. J Family Community Med. 2011;18(3):152–4.
  • Alvarez-Suarez JM, Giampieri F, Battino M. Honey as a source of dietary antioxidants: structures, bioavailability and evidence of protective effects against human chronic diseases. Curr Med Chem. 2013;20(5):621–38.
  • Avcı CB, Gündüz C, Baran Y, Sahin F, Yılmaz S, Dogan ZO, Saydam G. Caffeic acid phenethyl ester triggers apoptosis through induction of loss of mitochondrial membrane potential in CCRF-CEM cells. J Cancer Res Clin Oncol. 2011;137(1):41–7.
  • Badr MOT, Edrees NMM, Abdallah AAM, El-Deen NAMN, Neamat-Allah ANF, Ismail HTH. Anti-tumour effects of Egyptian propolis on Ehrlich ascites carcinoma. Vet Ital. 2014;47(3):341–50.
  • Barlak Y, Değer O, Colak M, Karataylı SC, Bozdayı AM, Yücesan F. Effect of Turkish propolis extracts on proteome of prostate cancer cell line. Proteome Sci. 2011;9(1):74.
  • Basini G, Baioni L, Bussolati S, Grasselli F, Daquino C, Spatafora C, Tringali C. Antiangiogenic properties of an unusual benzo[k,l]xanthene lignan derived from CAPE (caffeic acid phenethyl ester). Invest New Drugs. 2012;30(1):186–90.
  • Biscaia D, Ferreira SRS. Propolis extracts obtained by low pressure methods and supercritical fluid extraction. J Supercrit Fluids. 2009;51(1):17–23.
  • Camargo MS, Prieto AM, Resende FA, Boldrin PK, Cardoso CRP, Fernández MF, Molina-Molina JM, Olea N, Vilegas W, Cuesta-Rubio O, Veranda EA. Evaluation of estrogenic, antiestrogenic and genotoxic activity of nemorosone, the major compound found in brown Cuban propolis. BMC Complement Altern Med. 2013;13(1):201.
  • Cavalcante DRR, Oliveira PS de, Góis SM, Soares AF, Cardoso JC, Padilha FF, de Alburquerque Junior RLC. Effect of green propolis on oral epithelial dysplasia in rats. Braz J Otorhinolaryngol. Associação Brasileira de Otorrinolaringologia e Cirurgia Cérvico Facial; 2014;77(3):278–84.
  • Chan GC-F, Cheung K-W, Sze DM-Y. The immunomodulatory and anticancer properties of propolis. Clin Rev Allergy Immunol. 2013;44(3):262–73.
  • Chen C-N, Hsiao C-J, Lee S-S, Guh J-H, Chiang P-C, Huang C-C, Huang WJ. Chemical modification and anticancer effect of prenylated flavanones from Taiwanese propolis. Nat Prod Res. 2012;26(2):116–24.
  • Chen C-R, Shen C-T, Wu J-J, Yang H-L, Hsu S-L, Chang C-MJ. Precipitation of sub-micron particles of 3,5-diprenyl-4-hydroxycinnamic acid in Brazilian propolis from supercritical carbon dioxide anti-solvent solutions. J Supercrit Fluids. 2009;50(2):176–82.
  • Chen M-J, Shih S-C, Wang H-Y, Lin C-C, Liu C-Y, Wang T-E, Chu C-H, Chen Y-J. Caffeic Acid phenethyl ester inhibits epithelial-mesenchymal transition of human pancreatic cancer cells. Evid Based Complement Alternat Med. 2013;2013:270906.
  • Choudhari MK, Haghniaz R, Rajwade JM, Paknikar KM. Anticancer activity of Indian stingless bee propolis: an in vitro study. Evid Based Complement Alternat Med. 2013;2013:928280.
  • Chuu C-P, Lin H-P, Ciaccio MF, Kokontis JM, Hause RJ, Hiipakka RA, Liao S, Jones RB. Caffeic acid phenethyl ester suppresses the proliferation of human prostate cancer cells through inhibition of p70S6K and Akt signaling networks. Cancer Prev Res (Phila). 2012;5(5):788–97.
  • Cogulu O, Biray C, Gunduz C, Karaca E, Aksoylar S, Sorkun K, Salih B, Ozkinay F. Effects of Manisa propolis on telomerase activity in leukemia cells obtained from the bone marrow of leukemia patients. Int J Food Sci Nutr. 2009;60(7):601–5.
  • De Oliveira PF, de Souza Lima IM, Munari CC, Bastos JK, da Silva Filho AA, Tavares DC. Comparative evaluation of antiproliferative effects of Brazilian green propolis, its main source Baccharis dracunculifolia, and their major constituents artepillin C and baccharin. Planta Med. 2014;80(6):490–2.
  • Díaz-Carballo D, Gustmann S, Acikelli AH, Bardenheuer W, Buehler H, Jastrow H, Ergun S, Strumberg D. 7-epi-nemorosone from Clusia rosea induces apoptosis, androgen receptor down-regulation and dysregulation of PSA levels in LNCaP prostate carcinoma cells. Phytomedicine. 2012;19(14):1298–306.
  • Dornelas CA, Fechine-Jamacaru FV, Albuquerque IL, Magalhães HIF, Dias TA, Faria MHG, Alves MK, Rabenhorst SH, de Almeida PR, Lemos TL, Castro JD, Moraes ME, Moraes MO. Angiogenesis inhibition by green propolis and the angiogenic effect of L-lysine on bladder cancer in rats. Acta Cir Bras. 2012;27(8):529–36.
  • Dornelas CA, Fechine-Jamacaru FV, Albuquerque IL, Magalhães HIF, Souza AJS, de Alves LA.Chemoprevention with green propolis green propolis extracted in L-lysine versus carcinogenesis promotion with L-lysine in N-Butyl-N-[4-hydroxybutyl] nitrosamine (BBN) induced rat bladder cancer. Acta Cir Bras. 2012;27(2):185–92.
  • Endo S, Matsunaga T, Kanamori A, Otsuji Y, Nagai H, Sundaram K, El-Kabbani O, Toyooka N, Ohta S, Hara A. Selective inhibition of human type-5 17β-hydroxysteroid dehydrogenase (AKR1C3) by baccharin, a component of Brazilian propolis. J Nat Prod. 2012;75(4):716–21.
  • Ernst E, Cassileth BR. The prevalence of complementary/alternative medicine in cancer: a systematic review. Cancer. 1998;83(4):777–82.
  • Fan Y, Ma L, Zhang W, Xu Y, Suolangzhaxi, Zhi X, Cui E, Song X. Microemulsion can improve the immune-enhancing activity of propolis flavonoid on immunosuppression and immune response. Int J Biol Macromol. 2014;63:126–32.
  • Franchi GC, Moraes CS, Toreti VC, Daugsch A, Nowill AE, Park YK. Comparison of effects of the ethanolic extracts of brazilian propolis on human leukemic cells as assessed with the MTT assay. Evid Based Complement Alternat Med. 2012;2012:918956.
  • Hattori H, Okuda K, Murase T, Shigetsura Y, Narise K, Semenza GL, Nagasawa H. Isolation, identification, and biological evaluation of HIF-1-modulating compounds from Brazilian green propolis. Bioorg Med Chem. 2011;19(18):5392–401.
  • Hehlgans S, Lange I, Eke I, Kammerer B, Cordes N. Human head and neck squamous cell carcinoma cell lines are differentially radiosensitised by the honeybee product Propolis. Int J Radiat Biol. 2011;87(3):243–53.
  • Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer. 2013;13(10):714–26.
  • Hsu T-H, Chu C-C, Hung M-W, Lee H-J, Hsu H-J, Chang T-C. Caffeic acid phenethyl ester induces E2F-1-mediated growth inhibition and cell-cycle arrest in human cervical cancer cells. FEBS J. 2013;280(11):2581–93.
  • Huang W-J, Liang Y-C, Chuang S-E, Chi L-L, Lee C-Y, Lin C-W, Chen A-L, Huang J-S, Chiu C-J, Lee C-F, Huang C-Y, Chen C-N. NBM-HD-1: a novel histone deacetylase inhibitor with anticancer activity. Evid Based Complement Alternat Med. 2012;2012:781417.
  • Huang W-J, Lin C-W, Lee C-Y, Chi L-L, Chao Y-C, Wang H-N, Chiou BL, Chen TJ, Huang CY, Chen CN. NBM-HD-3, a novel histone deacetylase inhibitor with anticancer activity through modulation of PTEN and AKT in brain cancer cells. J Ethnopharmacol. 2011;136(1):156–67.
  • Ishihara M, Naoi K, Hashita M, Itoh Y, Suzui M. Growth inhibitory activity of ethanol extracts of Chinese and Brazilian propolis in four human colon carcinoma cell lines. Oncol Rep. 2009;22(2):349–54.
  • Izuta H, Shimazawa M, Tsuruma K, Araki Y, Mishima S, Hara H. Bee products prevent VEGF-induced angiogenesis in human umbilical vein endothelial cells. BMC Complement Altern Med. 2009;9:45.
  • Kamiya T, Nishihara H, Hara H, Adachi T. Ethanol extract of Brazilian red propolis induces apoptosis in human breast cancer MCF-7 cells through endoplasmic reticulum stress. J Agric Food Chem. American Chemical Society; 2012;60(44):11065–70.
  • Khacha-ananda S, Tragoolpua K, Chantawannakul P, Tragoolpua Y. Antioxidant and anti-cancer cell proliferation activity of propolis extracts from two extraction methods. Asian Pac J Cancer Prev. 2013;14(11):6991–5.
  • Khan MS, Devaraj H, Devaraj N. Chrysin abrogates early hepatocarcinogenesis and induces apoptosis in N-nitrosodiethylamine-induced preneoplastic nodules in rats. Toxicol Appl Pharmacol. 2011;251(1):85–94.
  • Kouidhi B, Zmantar T, Bakhrouf A. Anti-cariogenic and anti-biofilms activity of Tunisian propolis extract and its potential protective effect against cancer cells proliferation. Anaerobe. 2010;16(6):566–71.
  • Kumazaki M, Shinohara H, Taniguchi K, Yamada N, Ohta S, Ichihara K, Akao Y. 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.
  • Kuo Y-Y, Lin H-P, Huo C, Su L-C, Yang J, Hsiao P-H, Chiang H-C, Chung C-J, Wang H-D, Chang J-Y, Chen Y-W, Chuu C-P. Caffeic acid phenethyl ester suppresses proliferation and survival of TW2.6 human oral cancer cells via inhibition of Akt signaling. Int J Mol Sci. Multidisciplinary Digital Publishing Institute; 2013;14(5):8801–17.
  • Kurek-Górecka AM, Sobczakb A, Rzepecka-Stojkod A, Górecki MT, Wardas M, Pawłowska-Góral K. Antioxidant activity of ethanolic fractions of Polish propolis. Z Naturforsch C. 2014;67(11–12):545–50.
  • Li F, Awale S, Tezuka Y, Kadota S. Cytotoxicity of constituents from Mexican propolis against a panel of six different cancer cell lines. Nat Prod Commun. 2010;5(10):1601–6.
  • Li F, He Y-M, Awale S, Kadota S, Tezuka Y. Two new cytotoxic phenylallylflavanones from Mexican propolis. Chem Pharm Bull (Tokyo). 2011;59(9):1194–6.
  • Lin W-L, Liang W-H, Lee Y-J, Chuang S-K, Tseng T-H. Antitumor progression potential of caffeic acid phenethyl ester involving p75(NTR) in C6 glioma cells. Chem Biol Interact. 2010;188(3):607–15.
  • Lirdprapamongkol K, Sakurai H, Abdelhamed S, Yokoyama S, Athikomkulchai S, Viriyaroj A, Awale S, Ruchirawat S, Svasti J, Saiki I. Chrysin overcomes TRAIL resistance of cancer cells through Mcl-1 downregulation by inhibiting STAT3 phosphorylation. Int J Oncol. 2013;43(1):329–37.
  • Li X, Wang J-N, Huang J-M, Xiong X-K, Chen M-F, Ong C-N, Shen HM, Yang XF. Chrysin promotes tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL) induced apoptosis in human cancer cell lines. Toxicol In Vitro. 2011;25(3):630–5.
  • Markiewicz-Żukowska R, Borawska MH, Fiedorowicz A, Naliwajko SK, Sawicka D, Car H. Propolis changes the anticancer activity of temozolomide in U87MG human glioblastoma cell line. BMC Complement Altern Med. 2013;13(1):50.
  • Meneghelli C, Joaquim LSD, Félix GLQ, Somensi A, Tomazzoli M, da Silva DA, Berti FV, Veleirinho MB, Recouvreux Dde O, de Mattos Zeri AC, Dias PF, Maraschin M. Southern Brazilian autumnal propolis shows anti-angiogenic activity: an in vitro and in vivo study. Microvasc Res. 2013;88:1–11.
  • Mesbah L, Samia A. Bioavailability and pharmacokinetic of the Algerian propolis constituent naringenin in rats after oral administration. Planta Med. 2011;77(12):PA11.
  • Missima F, Pagliarone AC, Orsatti CL, Araújo JP, Sforcin JM. The Effect of propolis on Th1/Th2 cytokine expression and production by melanoma-bearing mice submitted to stress. Phytother Res. 2010;24(10):1501–7.
  • Murtaza G, Sajjad A, Mehmood Z, Shah SH, Siddiqi AR. Possible molecular targets for therapeutic applications of caffeic acid phenethyl ester in inflammation and cancer. J Food Drug Anal. 2014
  • Novak EM, Silva MS e C, Marcucci MC, Sawaya ACHF, Giménez-Cassina López B, Fortes MAHZ, Giorgi RR, Marumo KT, Rodrigues RF, Maria DA. Antitumoural activity of Brazilian red propolis fraction enriched with xanthochymol and formononetin: An in vitro and in vivo study. J Funct Foods. 2014;11:91–102.
  • 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. 2012;30(4):1279–88.
  • Oršolić N, Car N, Lisičić D, Benković V, Knežević AH, Dikić D, Petrik J. Synergism between propolis and hyperthermal intraperitoneal chemotherapy with cisplatin on ehrlich ascites tumor in mice. J Pharm Sci. 2013;102(12):4395–405.
  • Pellati F, Prencipe FP, Benvenuti S. Headspace solid-phase microextraction-gas chroma- tography-mass spectrometry characterization of propolis volatile compounds. J Pharm Biomed Anal. 2013;84:103–11.
  • Pichichero E, Cicconi R, Mattei M, Canini A. Chrysin-induced apoptosis is mediated through p38 and Bax activation in B16-F1 and A375 melanoma cells. Int J Oncol. 2011;38(2):473–83.
  • Popolo A, Piccinelli LA, Morello S, Cuesta-Rubio O, Sorrentino R, Rastrelli L, Pinto A. Antiproliferative activity of brown Cuban propolis extract on human breast cancer cells. Nat Prod Commun. 2009;4(12):1711–6.
  • Popolo A, Piccinelli AL, Morello S, Sorrentino R, Osmany CR, Rastrelli L, Pinto A. Cytotoxic activity of nemorosone in human MCF-7 breast cancer cells. Can J Physiol Pharmacol. 2011;89(1):50–7.
  • Pratsinis H, Kletsas D, Melliou E, Chinou I. Antiproliferative activity of Greek propolis. J Med Food. 2010;13(2):286–90.
  • Rizk SM, Zaki HF, Mina MAM. Propolis attenuates doxorubicin-induced testicular toxicity in rats. Food Chem Toxicol. 2014;67:176–86.
  • Sawicka D, Car H, Borawska MH, Nikliński J. The anticancer activity of propolis. Folia Histochem Cytobiol. 2012;50(1):25–37.
  • Seda Vatansever H, Sorkun K, Ismet Deliloğlu Gurhan S, Ozdal-Kurt F, Turkoz E, Gencay O, Salih B. Propolis from Turkey induces apoptosis through activating caspases in human breast carcinoma cell lines. Acta Histochem. 2010;112(6):546–56.
  • Silva-Carvalho R, Miranda-Gonçalves V, Ferreira AM, Cardoso SM, Sobral AJFN, Almeida-Aguiar C, Baltazar F. Antitumoural and antiangiogenic activity of Portuguese propolis in in vitro and in vivo models. J Funct Foods. 2014;11:160–71.
  • Sobočanec S, Balog T, Šariċ A, Mačak-Šafranko Ž, Štroser M, Žarković K, Žarković N, Stojković. R, Ivanković. S, Marotti T. Antitumor effect of Croatian propolis as a consequence of diverse sex-related dihydropyrimidine dehydrogenase (DPD) protein expression. Phytomedicine. 2011;18(10):852–8.
  • Soda M, Hu D, Endo S, Takemura M, Li J, Wada R, Ifuku S, Zhao HT, El-Kabbani O, Ohta S, Yamamura K, Toyooka N, Hara A, Matsunaga T. Design, synthesis and evaluation of caffeic acid phenethyl ester-based inhibitors targeting a selectivity pocket in the active site of human aldo-keto reductase 1B10. Eur J Med Chem. 2012;48:321–9.
  • Sulaiman GM, Ad'hiah AH, Al-Sammarrae KW, Bagnati R, Frapolli R, Bello E, Uboldi S, Romano M, Panini N, Scanziani E, Pezzolato M, Erba E, D'Incalci M. Assessing the anti-tumour properties of Iraqi propolis in vitro and in vivo. Food Chem Toxicol. 2012;50(5):1632–41.
  • Sung B, Pandey MK, Ahn KS, Yi T, Chaturvedi MM, Liu M, Aggarwal BB. Anacardic acid (6-nonadecyl salicylic acid), an inhibitor of histone acetyltransferase, suppresses expression of nuclear factor-kappaB-regulated gene products involved in cell survival, proliferation, invasion, and inflammation through inhibition of the i. Blood. 2008;111(10):4880–91.
  • Szliszka E, Czuba ZP, Bronikowska J, Mertas A, Paradysz A, Krol W. Ethanolic Extract of Propolis Augments TRAIL-Induced Apoptotic Death in Prostate Cancer Cells. Evid Based Complement Alternat Med. 2011;2011:535172.
  • Szliszka E, Krol W. Polyphenols Isolated from Propolis Augment TRAIL-Induced Apoptosis in Cancer Cells. Evid Based Complement Alternat Med. 2013;2013:731940.
  • Szliszka E, Zydowicz G, Janoszka B, Dobosz C, Kowalczyk-Ziomek G, Krol W. Ethanolic extract of Brazilian green propolis sensitizes prostate cancer cells to TRAIL-induced apoptosis. Int J Oncol. 2011;38(4):941–53.
  • Szliszka E, Zydowicz G, Mizgala E, Krol W. Artepillin C (3,5-diprenyl-4-hydroxycinnamic acid) sensitizes LNCaP prostate cancer cells to TRAIL-induced apoptosis. Int J Oncol. 2012;41(3):818–28.
  • Teerasripreecha D, Phuwapraisirisan P, Puthong S, Kimura K, Okuyama M, Mori H, Kimura A, Chanchao C. In vitro antiproliferative/cytotoxic activity on cancer cell lines of a cardanol and a cardol enriched from Thai Apis mellifera propolis. BMC Complement Altern Med. 2012;12:27.
  • Tolba MF, Esmat A, Al-Abd AM, Azab SS, Khalifa AE, Mosli HA, Abdel-Rahman SZ, Abdel-Naim. Caffeic acid phenethyl ester synergistically enhances docetaxel and paclitaxel cytotoxicity in prostate cancer cells. IUBMB Life. 2013;65(8):716–29.
  • Toreti VC, Sato HH, Pastore GM, Park YK. Recent progress of propolis for its biological and chemical compositions and its botanical origin. Evid Based Complement Alternat Med. 2013;2013:697390.
  • Trusheva B, Trunkova D, Bankova V. Different extraction methods of biologically active components from propolis: a preliminary study. Chem Cent J. 2007;1:13.
  • Türkez H, Geyikoğlu F, Yousef MI, Toğar B, Vançelik S. Propolis alleviates 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced histological changes, oxidative stress and DNA damage in rat liver. Toxicol Ind Health. 2013;29(8):677–85.
  • Umthong S, Phuwapraisirisan P, Puthong S, Chanchao C. In vitro antiproliferative activity of partially purified Trigona laeviceps propolis from Thailand on human cancer cell lines. BMC Complement Altern Med. 2011;11(1):37.
  • Valente MJ, Baltazar AF, Henrique R, Estevinho L, Carvalho M. Biological activities of Portuguese propolis: protection against free radical-induced erythrocyte damage and inhibition of human renal cancer cell growth in vitro. Food Chem Toxicol. 2011;49(1):86–92.
  • Valença I, Morais-Santos F, Miranda-Gonçalves V, Ferreira AM, Almeida-Aguiar C, Baltazar F. Portuguese propolis disturbs glycolytic metabolism of human colorectal cancer in vitro. BMC Complement Altern Med. 2013;13(1):184.
  • Watanabe MAE, Amarante MK, Conti BJ, Sforcin JM. Cytotoxic constituents of propolis inducing anticancer effects: a review. J Pharm Pharmacol. 2011;63(11):1378–86.
  • Wolf RJ, Hilger RA, Hoheisel JD, Werner J, Holtrup F. In vivo activity and pharmacokinetics of nemorosone on pancreatic cancer xenografts. Ahmad A, editor. PLoS One. Public Library of Science; 2013;8(9):e74555.
  • Wu J, Omene C, Karkoszka J, Bosland M, Eckard J, Klein CB, Frenkel, K. Caffeic acid phenethyl ester (CAPE), derived from a honeybee product propolis, exhibits a diversity of anti-tumor effects in pre-clinical models of human breast cancer. Cancer Lett. 2011;308(1):43–53.
  • Yang H, Huang Z, Huang Y, Dong W, Pan Z, Wang L. Characterization of Chinese crude propolis by pyrolysis–gas chromatography/mass spectrometry. J Anal Appl Pyrolysis. 2014
  • Zhang W, Lan Y, Huang Q, Hua Z. Galangin induces B16F10 melanoma cell apoptosis via mitochondrial pathway and sustained activation of p38 MAPK. Cytotechnology. 2013;65(3):447–55.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.