Biological activities of Portuguese propolis: Protection against free radical-induced erythrocyte damage and inhibition of human renal cancer cell growth in vitro

Food and Chemical Toxicology

Volumn 49, Issue 1, 2011, Pages 86-92

  Valente, Maria J ^a   Baltazar, Ana F ^b   Henrique, Rui ^a,c   Estevinho, Letícia ^d   Carvalho, Márcia ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSIDADE FERNANDO PESSOA   (Portugal)

^c PORTUGUESE ONCOLOGY INSTITUTE   (Portugal)

^d INSTITUTO POLITÉCNICO DE BRAGANÇA   (Portugal)

Author keywords

Antioxidant activity; Antiproliferative activity; Cancer chemoprevention; Erythrocyte; Portuguese propolis; Renal cell carcinoma

Indexed keywords

2,2' AZOBIS(2 AMIDINOPROPANE); 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; MALONALDEHYDE; PROPOLIS;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CANCER CELL; CELL GROWTH; CHEMOPROPHYLAXIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; ERYTHROCYTE MEMBRANE; GROWTH INHIBITION; HEMOLYSIS; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; KIDNEY CARCINOMA; LIPID PEROXIDATION; PORTUGAL;

ADULT; CARCINOMA, RENAL CELL; CELL PROLIFERATION; DRUG SCREENING ASSAYS, ANTITUMOR; ERYTHROCYTES; FREE RADICALS; HUMANS; KIDNEY NEOPLASMS; PROPOLIS; TUMOR CELLS, CULTURED;

EID: 78650285093     PISSN: 02786915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fct.2010.10.001     Document Type: Article

References (57)

1. Asgary S., Naderi G., Askari N. Protective effect of flavonoids against red blood cell hemolysis by free radicals. Exp. Clin. Cardiol. 2005, 10:88-90.
2. Awale S., Li F., Onozuka H., Esumi H., Tezuka Y., Kadota S. Constituents of Brazilian red propolis and their preferential cytotoxic activity against human pancreatic PANC-1 cancer cell line in nutrient-deprived condition. Bioorg. Med. Chem. 2008, 16:181-189.
3. Bankova V. Chemical diversity of propolis and the problem of standardization. J. Ethnopharmacol. 2005, 100:114-117.
4. Banskota A.H., Nagaoka T., Sumioka L.Y., Tezuka Y., Awale S., Midorikawa K., Matsushige K., Kadota S. Antiproliferative activity of the Netherlands propolis and its active principles in cancer cell lines. J. Ethnopharmacol. 2002, 80:67-73.
5. Banskota A.H., Tezuka Y., Adnyana I.K., Ishii E., Midorikawa K., Matsushige K., Kadota S. Hepatoprotective and anti-Helicobacter pylori activities of constituents from Brazilian propolis. Phytomedicine 2001, 8:16-23.
6. Banskota A.H., Tezuka Y., Adnyana I.K., Midorikawa K., Matsushige K., Message D., Huertas A.A., Kadota S. Cytotoxic, hepatoprotective and free radical scavenging effects of propolis from Brazil, Peru, the Netherlands and China. J. Ethnopharmacol. 2000, 72:239-246.
7. Banskota A.H., Tezuka Y., Kadota S. Recent progress in pharmacological research of propolis. Phytother. Res. 2001, 15:561-571.
8. Biswas S., Bhattacharyya J., Dutta A.G. Oxidant induced injury of erythrocyte-role of green tea leaf and ascorbic acid. Mol. Cell. Biochem. 2005, 276:205-210.
9. Bufalo M.C., Candeias J.M., Sousa J.P., Bastos J.K., Sforcin J.M. In vitro cytotoxic activity of Baccharis dracunculifolia and propolis against HEp-2 cells. Nat. Prod. Res. 2010.
10. Burdock G.A. Review of the biological properties and toxicity of bee propolis (propolis). Food Chem. Toxicol. 1998, 36:347-363.
11. Cao G., Sofic E., Prior R.L. Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships. Free Radic. Biol. Med. 1997, 22:749-760.
12. Carvalho M., Hawksworth G., Milhazes N., Borges F., Monks T.J., Fernandes E., Carvalho F., Bastos M.L. Role of metabolites in MDMA (ecstasy)-induced nephrotoxicity: an in vitro study using rat and human renal proximal tubular cells. Arch. Toxicol. 2002, 76:581-588.
13. Carvalho M., Ferreira P.J., Mendes V.S., Silva R., Pereira J.A., Jerónimo C., Silva B.M. Human cancer cell antiproliferative and antioxidant activities of Juglans regia L. Food Chem. Toxicol. 2010, 48:441-447.
14. Chen C., Weng M., Wu C., Lin J. Comparison of radical scavenging activity, cytotoxic effects and apoptosis induction in human melanoma cells by taiwanese propolis from different sources. Evid. Based Complement. Alternat. Med. 2004, 1:175-185.
15. Chiao C., Carothers A.M., Grunberger D., Solomon G., Preston G.A., Barrett J.C. Apoptosis and altered redox state induced by caffeic acid phenethyl ester (CAPE) in transformed rat fibroblast cells. Cancer Res. 1995, 55:3576-3583.
16. Costa R.M., Magalhães A.S., Pereira J.A., Andrade P.B., Valentão P., Carvalho M., Silva B.M. Evaluation of free radical scavenging and antihemolytic activities of quince (Cydonia oblonga) leaf: a comparative study with green tea (Camellia sinensis). Food Chem. Toxicol. 2009, 47:860-865.
17. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Rad. Biol. Med. 1991, 11:81-128.
18. Falcão S.I., Vilas-Boas M., Estevinho L.M., Barros C., Domingues M.R., Cardoso S.M. Phenolic characterization of Northeast Portuguese propolis: usual and unusual compounds. Anal. Bioanal. Chem. 2010, 396:887-897.
19. Frenkel K., Wei H., Bhimani R., Ye J., Zadunaisky J.A., Huang M.T., Ferraro T., Conney A.H., Grunberger D. Inhibition of tumor promoter-mediated processes in mouse skin and bovine lens by caffeic acid phenethyl ester. Cancer Res. 1993, 53:1255-1261.
20. Fresco P., Borges F., Diniz C., Marques M.P. New insights on the anticancer properties of dietary polyphenols. Med. Res. Rev. 2006, 26:747-766.
21. Gardana C., Scaglianti M., Pietta P., Simonetti P. Analysis of the polyphenolic fraction of propolis from different sources by liquid chromatography-tandem mass spectrometry. J. Pharm. Biomed. Anal. 2007, 45:390-399.
22. Hwang H.J., Park H.J., Chung H., Min H., Park E., Hong J., Lee S.K. Inhibitory effects of caffeic acid phenethyl ester on cancer cell metastasis mediated by the down-regulation of matrix metalloproteinase expression in human HT1080 fibrosarcoma cells. J. Nutr. Biochem. 2006, 17:356-362.
23. 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, 22:349-354.
24. Izuta H., Narahara Y., Shimazawa M., Mishima S., Kondo S., Hara H. 1,1-Diphenyl-2-picrylhydrazyl radical scavenging activity of bee products and their constituents determined by ESR. Biol. Pharm. Bull. 2009, 32:1947-1951.
25. Jin U., Chung T., Kang S., Suh S., Kim J., Chung K., Gu Y., Suzuki I., Kim C. Caffeic acid phenyl ester in propolis is a strong inhibitor of matrix metalloproteinase-9 and invasion inhibitor: isolation and identification. Clin. Chim. Acta 2005, 362:57-64.
26. Kaviarasan S., Vijayalakshmi K., Anuradha C. Polyphenol-rich extract of fenugreek seeds protect erythrocytes from oxidative damage. Plant Foods Hum. Nutr. 2004, 59:143-147.
27. Kawaii S., Tomono Y., Katase E., Ogawa K., Yano M. Antiproliferative activity of flavonoids on several cancer cell lines. Biosci. Biotechnol. Biochem. 1999, 63:896-899.
28. Ko F.N., Hsiao G., Kuo Y.H. Protection of oxidative hemolysis by demethyldiisoeugenol in normal and beta-thalassemic red blood cells. Free Rad. Biol. Med. 1997, 22:215-222.
29. Kumazawa S., Hamasaka T., Nakayama T. Antioxidant activity of propolis of various geographic origins. Food Chem. 2004, 84:329-339.
30. Kunimasa, K., Ahn, M.R., Kobayashi, T., Eguchi, R., Kumazawa, S., Fujimori, Y., Nakano, T., Nakayama, T., Kaji, K., Ohta, T., 2009. Brazilian Propolis Suppresses Angiogenesis by Inducing Apoptosis in Tube-forming Endothelial Cells through Inactivation of Survival Signal ERK1/2. Evid. Based Complement. Alternat. Med. 1-7.
31. Lee K.W., Kang N.J., Kim J.H., Lee K.M., Lee D.E., Hur H.J., Lee H.J. 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. 2008, 2:319-322.
32. Li F., Awale S., Tezuka Y., Esumi H., Kadota S. Study on the constituents of Mexican propolis and their cytotoxic activity against PANC-1 human pancreatic cancer cells. J. Nat. Prod. 2010, 73:623-627.
33. Li F., Awale S., Tezuka Y., Kadota S. Cytotoxic constituents from Brazilian red propolis and their structure-activity relationship. Bioorg. Med. Chem. 2008, 16:5434-5440.
34. Libério S.A., Pereira A.L., Araújo M.J., Dutra R.P., Nascimento F.R., Monteiro-Neto V., Ribeiro M.N., Gonçalves A.G., Guerra R.N. The potential use of propolis as a cariostatic agent and its actions on mutans group streptococci. J. Ethnopharmacol. 2009, 125:1-9.
35. Marcucci M.C. Propolis: chemical composition, biological properties and therapeutic activity. Apidologie 1995, 26:83-99.
36. Marshak D.R., Greenwalt D.E. Differentiating primary human cells in rapid-throughput discovery applications. High Content Screening: A Powerful Approach to Systems Cell Biology and Drug Discovery 2006, 121-128. Humana Press, New Jersey. D. Taylor, J. Haskins, A. Giuliano (Eds.).
37. Moreira L., Dias L.G., Pereira J.A., Estevinho L. Antioxidant properties, total phenols and pollen analysis of propolis samples from Portugal. Food Chem. Toxicol. 2008, 46:3482-3485.
38. Moreno M. Comparison of the free radical-scavenging activity of propolis from several regions of Argentina. J. Ethnopharmacol. 2000, 71:109-114.
39. Motzer R.J., Mazumdar M., Bacik J., Russo P., Berg W.J., Metz E.M. Effect of cytokine therapy on survival for patients with advanced renal cell carcinoma. J. Clin. Oncol. 2000, 18:1928-1935.
40. Orsolić N., Saranović A.B., Basić I. Direct and indirect mechanism(s) of antitumour activity of propolis and its polyphenolic compounds. Planta Med. 2006, 72:20-27.
41. Orsolić N., Terzić S., Mihaljević Z., Sver L., Basić I. Effects of local administration of propolis and its polyphenolic compounds on tumor formation and growth. Biol. Pharm. Bull. 2005, 28:1928-1933.
42. Patel D., Shukla S., Gupta S. Apigenin and cancer chemoprevention: progress, potential and promise. Int. J. Oncol. 2007, 30:233-245.
43. Perron N.R., Brumaghim J.L. A review of the antioxidant mechanisms of polyphenol compounds related to iron binding. Cell Biochem. Biophys. 2009, 53:75-100.
44. Pratsinis H., Kletsas D., Melliou E., Chinou I. Antiproliferative activity of Greek propolis. J. Med. Food 2010, 13:286-290.
45. Rice-Evans C. Flavonoid antioxidants. Curr. Med. Chem. 2001, 8:797-807.
46. Rice-Evans C., Miller N., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Rad. Biol. Med. 1996, 20:933-956.
47. Russo A., Cardile V., Sanchez F., Troncoso N., Vanella A., Garbarino J.A. Chilean propolis: antioxidant activity and antiproliferative action in human tumor cell lines. Life Sci. 2004, 76:545-558.
48. Scazzocchio F., D'Auria F.D., Alessandrini D., Pantanella F. Multifactorial aspects of antimicrobial activity of propolis. Microbiol. Res. 2006, 161:327-333.
49. Schnitzler P., Neuner A., Nolkemper S., Zundel C., Nowack H., Sensch K.H., Reichling J. Antiviral activity and mode of action of propolis extracts and selected compounds. Phytother. Res. 2010, 24:S20-28.
50. Sforcin J.M. Propolis and the immune system: a review. J. Ethnopharmacol. 2007, 113:1-14.
51. Sha N., Guan S., Lu Z., Chen G., Huang H., Xie F., Yue Q., Liu X., Guo D. Cytotoxic constituents of Chinese propolis. J. Nat. Prod. 2009, 72:799-801.
52. Silici S., Koç N.A., Ayangil D., Çankaya S. Antifungal activities of propolis collected by different races of honeybees against yeasts isolated from patients with superficial mycoses. J. Pharmacol. Sci. 2005, 99:39-44.
53. Soares M.E., Carvalho M., Remião F., Carvalho F., Bastos M. Implementation of HPLC methodology for the quantification of malondialdehyde in cell suspensions and liver. J. Liq. Chromatogr. Relat. Technol. 2004, 27:2357-2369.
54. Tan-No K., Nakajima T., Shoji T., Nakagawasai O., Niijima F., Ishikawa M., Endo Y., Sato T., Satoh S., Tadano T. Anti-inflammatory effect of propolis through inhibition of nitric oxide production on carrageenin-induced mouse paw edema. Biol. Pharm. Bull. 2006, 29:96-99.
55. Usia T., Banskota A.H., Tezuka Y., Midorikawa K., Matsushige K., Kadota S. Constituents of Chinese propolis and their antiproliferative activities. J. Nat. Prod. 2002, 65:673-676.
56. Weng M., Liao C., Chen C., Wu C., Lin J. Propolin H from Taiwanese propolis induces G1 arrest in human lung carcinoma cells. J. Agric. Food Chem. 2007, 55:5289-5298.
57. Zou C.G., Agar N.S., Jones G.L. Oxidative insult to human red blood cells induced by free radical initiator AAPH and its inhibition by a commercial antioxidant mixture. Life Sci. 2001, 69:75-86.