Assessing the anti-tumour properties of Iraqi propolis in vitro and in vivo

Food and Chemical Toxicology

Volumn 50, Issue 5, 2012, Pages 1632-1641

  Sulaiman, Ghassan M ^a   Ad'hiah, Ali H ^b   Al Sammarrae, Khulood W ^c   Bagnati, Renzo ^d   Frapolli, Roberta ^d   Bello, Ezia ^d   Uboldi, Sarah ^d   Romano, Michela ^d   Panini, Nicolò ^d   Scanziani, Eugenio ^e   Pezzolato, Marzia ^f   Erba, Eugenio ^d   D'Incalci, Maurizio ^d  

^a UNIVERSITY OF TECHNOLOGY   (Iraq)

^b UNIVERSITY OF BAGHDAD   (Iraq)

^c AL NAHRAIN UNIVERSITY   (Iraq)

^d MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

^f Istituto Zooprofilattico Sperimentale Piemonte   (Italy)

Author keywords

BrdU DNA cell cycle; Cytotoxicity; Iraqi propolis

Indexed keywords

HISTONE H2AX; KI 67 ANTIGEN; PROPOLIS; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL STRAIN HCT116; CELL STRAIN HL 60; CELL SWELLING; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG DOSE COMPARISON; ENDOREDUPLICATION; FEMALE; GROWTH INHIBITION; IN VITRO STUDY; IN VIVO STUDY; IRAQ; MEMBRANE DAMAGE; MITOSIS INHIBITION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR; TUMOR REGRESSION; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; IRAQ; MICE; MICE, NUDE; MICROSCOPY, FLUORESCENCE; NEOPLASMS; PROPOLIS;

MUS;

EID: 84858257785     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.01.022     Document Type: Article

References (58)

1. Ad'hiah A.H., Sulaiman G.M., Jaber M.S. Some Immunological evaluations of Iraqi propolis extract in albino male mice. J. Fac. Med. Baghdad 2007, 49:121-125.
2. Alencar S.M., Oldoni T.L.C., Castro M.L., Cabral I.S.R., Costa-Neto C.M., Cury J.A., Rosalen P.L., Ikegaki M. Chemical composition and biological activity of a new type of Brazilian propolis: Red propolis. J. Ethnopharmacol. 2007, 113:278-283.
3. Benkovic V.H., Knezevic A.H., Brozovic, Knezevic G., Dikic D., Bevanda M., Basic I., Orsolic N. Enhanced antitumor activity of irinotecan combined with propolis and its polyphenolic compounds on Ehrlich ascites tumor in mice. Biomed. Pharmacother. 2007, 61:292-297.
4. Bestwick C.S., Milne L., Duthie S.J. Kaempferol induced inhibition of HL-60 cell growth results from a heterogeneous response, dominated by cell cycle alterations. Chem. Biol. Interact. 2007, 170:76-85.
5. Bufalo, M. C., Candeias, J. M. G., Sforcin, J. M. 2007. In vitro Cytotoxic effect of Brazilian green propolis on human laryngeal epidermoid carcinoma (HEp-2) cells. eCAM. 1-5.
6. Burdock G.A. Review of the biological properties and toxicity of propolis. Food Chem. Toxicol. 1998, 36:341-363.
7. Bredesen D.E., Rao R.V., Mehlen P. Cell death in the nervous system. Nature 2006, 443:796-802.
8. Brusselmans K., Vrolix R., Verhoeven G., Swinnen J.V. Induction of cancer cell apoptosis by flavonoids is associated with their ability to inhibit fatty acid synthase activity. J. Biol. Chem. 2005, 280:5636-5645.
9. Cantero G., Campanella C., Mateos S., Cortes F. Topoisomerase II inhibition and high yield of endoreduplication induced by the flavonoids luteolin and quercetin. Mutagenesis 2006, 21:321-325.
10. Chang J.S., Hsu Y., Kuo P.L., Kuo Y.C., Chiang L.C., Lin C.C. Increase of Bax/Bcl-XL ratio and arrest of cell cycle by luteolin in immortalized human hepatoma cell line. Life Sci. 2005, 76:1883-1893.
11. Cheang M.C.U., Chia S.K., Voduc D., Gao D., Leung S., Snider J., Watson M., Davies S., Bernard P.S., Parker J.S., Perou C.M., Ellis M.J., Nielsen T.O. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. JNCI J. Natl. Cancer Inst. 2009, 101:736-750.
12. Chen, C. N., Weng, M. S., Wu, C. L., Lin, J. K. 2004. Comparison of radical scavenging activity, cytotoxic effects and apoptosis induction in human melanoma cells by Taiwanese propolis from different sources. eCAM. 1, 175-185.
13. Chen C.N., WuC L., LinJ K. Propolin C from propolis induces apoptosis through activating caspases, Bid andcytochrome c release inhuman melanoma cells. Biochem. Pharmacol. 2004, 67:53-66.
14. Chen D., Daniel K.G., Chen M.S., Kuhn D.J., Landis-Piwowar K.R., Dou Q.P. Dietary flavonoids as proteasome inhibitors and apoptosis inducers in human leukemia cells. Biochem. Pharmacol. 2005, 69:1421-1432.
15. Chen Y.J., Shiao M.S., Wang S.Y. The antioxidant caffeic acid phenethyl ester induces apoptosis associated with selective scavenging of hydrogen peroxide in human leukemic HL-60 cells. Anticancer Drugs 2001, 12:143-149.
16. Danial N.N., Korsmeyer S.J. Cell death: critical control points. Cell 2004, 116:205-219.
17. Erba E., Bergamaschi D., Bassano L., Damia G., Ronzoni S., Faircloth G.T., D'Incalci M. Ecteinascidin-743 (ET-743), a natural marine compound, with a unique mechanism of action. Eur. J. Cancer 2001, 37:97-105.
18. Eom H.S., Lee E.J., Yoon B.S., Yoo B.S. Propolis inhibits the proliferation of human leukaemia HL-60 cells by inducing apoptosis through the mitochondrial pathway. Nat. Prod. Res. 2010, 24:375-386.
19. Ganguly C., Saha P., Panda C.K., Das S. Inhibition of growth, induction of apoptosis and alteration of gene expression by tea polyphenols in the highly metastatic human lung cancer cell line NCI-H460. Asian. Pac. J. Cancer. Prev. 2005, 6:326-331.
20. Gekker G., Hu S., Spivak M., Lokensgard J.R., Peterson P.K. Anti-HIV-1 activity of propolis in CD4+ lymphocyte and microglial cell cultures. J. Ethnopharmacol. 2005, 102:158-163.
21. Green D.R. Apoptotic pathways: the roads to ruin. Cell 1998, 94:695-698.
22. Gupta S.C., Kim J.H., Prasad S., Aggarwal B.B. Regulation of survival, proliferation, invasion, angiogenesis, and metastasis of tumor cells through modulation of inflammatory pathways by nutraceuticals. Cancer Metastasis Rev. 2010, 29:405-434.
23. Haddad, A. Q. 2008. The Cellular and molecular properties of flavonoid in prostate cancer chemoprevention. Ph.D. Thesis, University Toronto, Canada, pp. 1-244.
24. Haddad A.Q., Venkateswaran V., Viswanathan L., Teahan S.J., Fleshner N.E., Klotz L.H. Novel antiproliferative flavonoids induce cell cycle arrest in human prostate cancer cell lines. Prostate. Cancer. Prostatic. Dis. 2006, 9:68-76.
25. Huang X., Darzynkiewicz Z. Cytometric Assessment of Histone H2AX Phosphorylation: A Reporter of DNA Damage. Methods Mol. Biol. 2006, 314:73-80.
26. Inoue K., Saito M., Kanai T., Kawata T., Shigematsu N., Uno T., Isobe K., Liu C., Ito H. Anti-tumor effects of water-soluble propolis on a mouse sarcoma cell line in vivo and in vitro. Am. J. Chin. Med. 2008, 36:623-632.
27. 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.
28. Koc A.N., Silici S., Ayangil D., Ferahbas A., Cankaya S. Comparison of in vitro activities of antifungal drugs and ethanolic extract of propolis against Trichophyton rubrum and T. mentagrophytes by using a micro-dilution assay. Mycosis 2005, 48:205-210.
29. Koelbl O., Rosenwald A., Haber M., Muller J., Reuther J., Flentje M. P53 and Ki-67 as predictive markers for radiosensitivity in squamous cell carcinoma of the oral cavity? An immunohistochemical and clinicopathologic study. Int. J. Rad. Oncol. Biol. Phys. 2001, 49:147-154.
30. Kowaltowski A.J., Castilho R.F., Vercesi A.E. Mitochondrial permeability transition and oxidative stress. FEBS Lett. 2001, 495:12-15.
31. Kumar N., Mueen A.K.K., Dang R., Husain A. Antioxidant and antimicrobial activity of propolis from Tamil Nadu zone. J. Med. Plant Res. 2008, 2:361-364.
32. Lee S.H., Kim D.C., Lee J.Y., Cho M., Hwang W.I. A study on the anticancer activity of propolis. J. Food Sci. Nutr. 2000, 5:54-57.
33. Li F., Awale S., Tezuka Y., Kadota S. Cytotoxic constituents of propolis from Myanmar and their structure-activity relationship. Biol. Pharm. Bull. 2009, 32:2075-2078.
34. Lotfy M. Biological activity of bee propolis in health and disease. Asian Pac. J. Cancer Prev. 2006, 7:22-31.
35. MacPhail S.H., Banath J.P., Yu Y., Chu E., Olive P.L. Cell cycle-dependent expression of phosphorylated histone H2AX: reduced expression in un irradiated but not X-irradiated G1 phase cells. Radiat. Res. 2003, 159:759-767.
36. Mani F., Damasceno H.C.R., Novelli E.L.B., Martins E.A.M., Sforcin J.M. Propolis: effect of different concentrations, extracts and intake period on seric biochemical variables. J. Ethnopharmacol. 2006, 105:95-98.
37. Motomura M., Kwon K.M., Suh S.J., Lee Y.C., Kim Y.K., Lee I.S., Kim M.S., Kwon D.Y., Suzuki I., Kim C.H. Propolis induces cell cycle arrest and apoptosis in human leukemic U937 cells through Bcl-2/Bax regulation. Environ. Toxicol. Pharmacol. 2008, 26:61-67.
38. Naik D.G., Vaidya H.S., Behera B.C. Antioxidant properties of Indian propolis. J. Api. Pro. Api Med. Sci. 2009, 1:110-120.
39. Najafi M.F., Vahedy F., Seyyedin M., Jomehzadeh H.R., Bozary K. Effect of the water extracts of propolis on stimulation and inhibition of different cells. Cytotechnology 2007, 54:49-56.
40. Nikolov, N., Marekov, N., Bankova, V., Popov, S., Ignatova, R., Vladimirova, I., 1987. Method for the preparation of water-soluble derivative of propolis. Bulgarian Patent Application N, 79903/28.05.1987.
41. Onori P., De Morrow S., Gaudio E., Franchitto A., Mancinelli R., Venter J., Kopriva S., Ueno Y., Alvaro D., Savage J., Alpini G., Francis H. Caffeic acid phenethyl ester decreases cholangiocarcinoma growth by inhibition of NF-kB and induction of apoptosis. Int. J. Cancer. 2009, 125:565-576.
42. Orsolic N., Terzic S., Mihaljevic Z., Sver L., Basic I. Effects of local administration of propolis and its polyphenolic compounds on tumor formation and growth. Biol. Pharm. Bull. 2005, 28:1928-1933.
43. Padmavathi R., Senthilnathan P., Chodon D., Sakthisekaran D. 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. 2006, 78:2820-2825.
44. Pastor N., Cantero G., Campanella C., Cortes F. Endoreduplication induced in cultured Chinese hamster cells by different anti-topoisomerase II chemicals: Evidence for the essential contribution of the enzyme to chromosome segregation. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2005, 582:11-19.
45. Plochmann K., Korte G., Koutsilieri E., Richling E., Riederer P., Rethwilm A., Schreier P., Scheller C. Structure-activity relationships of flavonoid induced cytotoxicity on human leukemia cells. Arch. Biochem. Biophys. 2007, 460:1-9.
46. Powolny A., Xu J., Loo G. Deoxycholate induces DNA damage and apoptosis in human colon epithelial cells expressing either mutant or wild-type p53. Internat. J. Biochem. Cell Biol. 2001, 33:193-203.
47. Reed J.C. Apoptosis-based therapies. Nat.Rev.Drug Discov. 2002, 1:111-121.
48. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
49. Singh R.P., Agarwal R. Natural flavonoids targeting deregulated cell cycle progression in cancer cells. Curr. Drug. Targets 2006, 7:345-354.
50. Sulaiman, G. M., Al Sammarrae, K. W., Ad'hiah, A. H., Zucchetti, M., Frapolli, R., Bello, E., Erba, E., D'Incalci M., Bagnati, R. 2011. Chemical characterization of Iraqi propolis samples and assessing their antioxidant potentials. Food Chem. oxicol. 49, 2415-2421.
51. Syamsudin Dewi., Kusmardi R.M. Immunomodulatory and in vivo antiplasmodial activities of propolis extracts. Am. J. Pharmacol. Toxicol. 2009, 4:75-79.
52. Szliszka E., Czuba Z.P., Domino M., Mazur B., Zydowicz G., Krol W. Ethanolic extract of propolis (EEP) enhances the apoptosis- inducing potential of TRAIL in cancer cells. Molecules 2009, 14:738-754.
53. Tavecchio M., Simone M., Erba E., Chiolo I., Liberi G., Foiani M., D'Incalci M., Damia G. Role of homologous recombination in trabectedin-induced DNA damage. Eur. J. Cancer 2008, 44:609-618.
54. Trusheva B., Trunkova D., Bankova V. Different extraction methods of biologically active components from propolis: a preliminary study. Chem. Central J. 2007, 1:13.
55. Wang D., Xiang D.B., He Y.J., Li Z.P., Wu X.H., Mou J.H., Xiao H.L., Zhang Q.H. Effect of caffeic acid phenethyl ester on proliferation and apoptosis of colorectal cancer cells in vitro.World J. Gastroenterology 2005, 11:4008-4012.
56. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 2001, 15:2922-2933.
57. Yamaguchi H., Chen J., Bhalla K., Wang H.G. Regulation of Bax activation and apoptotic response to microtubule-damaging agents by p53 transcription-dependent and -independent pathways. J. Biol. Chem. 2004, 279:39431-39437.
58. Yoon G., Kang B.Y., Cheon S.H. Topoisomerase I inhibition and cytotoxicity of licochalcones A and E from Glycyrrhiza inflata. Arch. Pharm. Res. 2007, 30:313-316.