Cell cycle and apoptosis pathway modulation by Tualang honey in ER-dependent and -independent breast cancer cell lines;Modulación del ciclo celular y de la vía de apoptosis por la miel tualang en líneas celulares de cáncer de mama dependientes e independientes de RE

Journal of Apicultural Research

Volumn 55, Issue 5, 2016, Pages 366-374

  Fauzi, Agustine Nengsih ^a   Yaacob, Nik Soriani ^a  

^a SCHOOL OF MEDICAL SCIENCES   (Malaysia)

Author keywords

apoptosis; cell cycle; death receptor; MCF 7; MDA MB 231; p21; p53; Tualang honey

Indexed keywords

EID: 85008975665     PISSN: 00218839     EISSN: 20786913     Source Type: Journal    
DOI: 10.1080/00218839.2016.1249149     Document Type: Article

References (49)

1. Abraham, R.T., (2001). Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes and Development, 15, 2177–2196. doi:10.1101/gad.914401
2. Adrain, C., Creagh, E.M., & Martin, S.J., (2001). Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. The EMBO Journal, 20, 6627–6636. doi:10.1093/emboj/20.23.6627
3. Aggarwal, B.B., (2003). Signalling pathways of the TNF superfamily:A double-edged sword. Nature Reviews Immunology, 3, 745–756. doi:10.1038/nri1184
4. Aliyu, M., Odunola, O.A., Farooq, A.D., Mesaik, A.M., Choudhary, M.I., Beenish, F., … Ochuko, L.E., (2012). Acacia honey modulates cell cycle progression, pro-inflammatory cytokines and calcium ions secretion in PC-3 cell line. Journal of Cancer Science and Therapy, 4, 401–407. doi:10.4172/1948-5956.1000174
5. Amundson, S.A., Myers, T.G., & Fornace, Jr., A.J., (1998). Roles for p53 in growth arrest and apoptosis:Putting on the brakes after genotoxic stress. Oncogene, 17, 3287–3299. doi:10.1038/sj.onc.1202576
6. Bender, L.M., Morgan, M.J., Thomas, L.R., Liu, Z.G., & Thorburn, A., (2005). The adaptor protein TRADD activates distinct mechanisms of apoptosis from the nucleus and the cytoplasm. Cell and Death Differentiation, 12, 473–481. doi:10.1038/sj.cdd.4401578
7. Chahar, M.K., Sharma, N., Dobhal, M.P., & Joshi, Y.C., (2011). Flavonoids:A versatile source of anticancer drugs. Pharmacognosy Reviews, 5, 1–12. doi:10.4103/0973-7847.79093
8. Cooper, R., (2011). Editorial. Journal of ApiProduct and ApiMedical Science, 3(1), 1–3. doi:10.3896/IBRA.4.03.1.01
9. Erejuwa, O.O., Sulaiman, S.A., & Wahab, M.S.A., (2014). Effects of honey and its mechanisms of action on the development and progression of cancer. Molecules, 19, 2497–2522. doi:10.3390/molecules19022497
10. Fauzi, A.N., Norazmi, M.N., & Yaacob, N.S., (2011). Tualang honey induces apoptosis and disrupts the mitochondrial membrane potential of human breast and cervical cancer cell lines. Food and Chemical Toxicology, 49, 871–878. doi:10.1016/j.fct.2010.12.010
11. Fernandez-Cabezudo, M., El-Kharrag, R., Torab, F., Bashir, G., George, J.A., El-Taji, H., & al-Ramadi, B.K., (2013). Intravenous administration of Manuka honey inhibits tumor growth and improves host survival when used in combination with chemotherapy in a melanoma mouse model. PLoS ONE, 8, e55993. doi:10.1371/journal.pone.0055993
12. Ford, C.H.J., Al-Bader, M., Al-Ayadhi, B., & Francis, I., (2011). Reassessment of estrogen receptor expression in human breast cancer cell lines. Anticancer Research, 31, 521–527. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/21378333
13. Fukazawa, T., Walter, B., & Owen-Schaub, L.B., (2003). Adenoviral bid overexpression induces caspase-dependent cleavage of truncated bid and p53-independent apoptosis in human non-small cell Lung cancers. Journal of Biological Chemistry, 278, 25428–25434. doi:10.1074/jbc.M302058200
14. Ghashm, A.A., Othman, N.H., Khattak, M.N., Ismail, N.M., & Saini, R., (2010). Antiproliferative effect of Tualang honey on oral squamous cell carcinoma and osteosarcoma cell lines. BMC Complementary and Alternative Medicine, 10, 49. doi:10.1186/1472-6882-10-49
15. Gottifredi, V., McKinney, K., Poyurovsky, M.V., & Prives, C., (2004). Decreased p21 levels are required for efficient restart of DNA synthesis after S phase block. Journal of Biological Chemistry, 279, 5802–5810. doi:10.1074/jbc.M310373200
16. Hartwell, L.H., & Weinert, T.A., (1989). Checkpoints:Controls that ensure the order of cell cycle events. Science, 246, 629–634. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/2683079 10.1126/science.2683079
17. Hsu, H., Shu, H.B., Pan, M.G., & Goeddel, D.V., (1996). TRADD–TRAF2 and TRADD–FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell, 84, 299–308. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/856507510.1016/S0092-8674(00)80984-8
18. Hung, D.T., Jamison, T.F., & Schreiber, S.L., (1996). Understanding and controlling the cell cycle with natural products. Chemistry & Biology, 3, 623–639. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/880789510.1016/S1074-5521(96)90129-5
19. Ismail, N.I., Abdul Kadir, M.R., Mahmood, N.H., Singh, O.P., Iqbal, N., & Zulkifli, R.M., (2016). Apini and Meliponini foraging activities influence the phenolic content of different types of Malaysian honey. Journal of Apicultural Research, 55(2), 137–150. doi:10.1080/00218839.2016.1207388
20. Jaganathan, S.K., Mandal, S.M., Jana, S.K., Das, S., & Mandal, M., (2010). Studies on the phenolic profiling, anti-oxidant and cytotoxic activity of Indian honey:In vitro evaluation. Natural Product Research, 24, 1295–1306. doi:10.1080/14786410903184408
21. Jensen, E.V., & Jordan, V.C., (2003). The estrogen receptor:A model for molecular medicine. Clinical Cancer Research, 9, 1980–1989. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12796359
22. Kannan, T.P., Ali, A.Q., Abdullah, S.F., & Ahmad, A., (2009). Evaluation of Tualang honey as a supplement to fetal bovine serum in cell culture. Food and Chemical Toxicology, 47, 1696–1702. doi:10.1016/j.fct.2009.04.020
23. Kasibhatla, S., & Tseng, B., (2003). Why target apoptosis in cancer treatment? Molecular Cancer Therapeutics, 2, 573–580. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12813137
24. Khalil, M.I., Alam, N., Moniruzzaman, M., Sulaiman, S.A., & Gan, S.H., (2011). Phenolic acid composition and antioxidant properties of Malaysian honeys. Journal of Food Science, 76, C921–C928. doi:10.1111/j.1750-3841.2011.02282.x
25. Kiechle, F.L., & Zhang, X., (2002). Apoptosis:Biochemical aspects and clinical implications. Clinica Chimica Acta, 326, 27–45. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1241709510.1016/S0009-8981(02)00297-8
26. Kim, B., Fatayer, H., Hanby, A.M., Horgan, K., Perry, S.L., Valleley, E.M., … Hughes, T.A., (2013). Neoadjuvant chemotherapy induces expression levels of breast cancer resistance protein that predict disease-free survival in breast cancer. PLoS ONE, 8(5), e62766. doi:10.1371/journal.pone.0062766
27. Kishore, R.K., Halim, A.S., Syazana, M.S., & Sirajudeen, K.N., (2011). Tualang honey has higher phenolic content and greater radical scavenging activity compared with other honey sources. Nutrition Research, 31, 322–325. doi:10.1016/j.nutres.2011.03.001
28. Kyselova, Z., (2011). Toxicological aspects of the use of phenolic compounds in disease prevention. Interdisciplinary Toxicology, 4, 173–183. doi:10.2478/v10102-011-0027-5
29. Mohamed, M., Sirajudeen, K., Swamy, M., Yaacob, N.S., & Sulaiman, S.A., (2010). Studies on the antioxidant properties of Tualang honey of Malaysia. African Journal of Traditional Complementary and Alternative Medicines, 7, 59–63. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3005388/
30. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T., & Yasuhiko, Y., (2002). An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. Journal of Biological Chemistry, 277, 34287–34294. doi:10.1074/jbc.M204973200
31. Nasir, N.A., Halim, A.S., Singh, K.K., Dorai, A.A., & Haneef, M.N., (2010). Antibacterial properties of Tualang honey and its effect in burn wound management:A comparative study. BMC Complementary and Alternative Medicine, 10, 1–7. doi:10.1186/1472-6882-10-31
32. Newman, D.J., Cragg, G.M., & Snader, K.M., (2003). Natural products as sources of new drugs over the period 1981−2002. Journal of Natural Products, 66, 1022–1037. doi:10.1021/np030096l
33. Paruthiyil, S., Cvoro, A., Tagliaferri, M., Cohen, I., Shtivelman, E., & Leitman, D.C., (2011). Estrogen receptor beta causes a G2 cell cycle arrest by inhibiting CDK1 activity through the regulation of cyclin B1, GADD45A, and BTG2. Breast Cancer Research and Treatment, 129, 777–784. doi:10.1007/s10549-010-1273-5
34. Patisaul, H.B., & Jefferson, W., (2010). The pros and cons of phytoestrogens. Frontiers in Neuroendocrinology, 31, 400–419. doi:10.1016/j.yfrne.2010.03.003
35. Pichichero, E., Cicconi, R., Mattei, M., Muzi, M.G., & Canini, A., (2010). Acacia honey and chrysin reduce proliferation of melanoma cells through alterations in cell cycle progression. International Journal of Oncology, 37, 973–981. doi:10.3892/ijo_00000748
36. Pietenpol, J.A., & Stewart, Z.A., (2002). Cell cycle checkpoint signaling:Cell cycle arrest versus apoptosis. Toxicology, 181–182, 475–481. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1250535610.1016/S0300-483X(02)00460-2
37. Pucci, B., Kasten, M., & Giordano, A., (2000). Cell cycle and apoptosis. Neoplasia, 2, 291–299. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1100556310.1038/sj.neo.7900101
38. Sancar, A., Lindsey-Boltz, L.A., Ünsal-Kaçmaz, K., & Linn, S., (2004). Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annual Review of Biochemistry, 73, 39–85. doi:10.1146/annurev.biochem.73.011303.073723
39. Song, W., Dang, Q., Xu, D., Chen, Y., Zhu, G., Wu, K., … Li, L., (2014). Kaempferol induces cell cycle arrest and apoptosis in renal cell carcinoma through EGFR/p38 signaling. Oncology Reports, 31, 1350–1356. doi:10.3892/or.2014.2965
40. Swift, L.H., & Golsteyn, R.M., (2014). Genotoxic anti-cancer agents and their relationship to DNA damage, mitosis, and checkpoint adaptation in proliferating cancer cells. International Journal of Molecular Sciences, 15, 3403–3431. doi:10.3390/ijms15033403
41. Tan, H.T., Rahman, R.A., Gan, S.H., Halim, A.S., Hassan, S.A., Sulaiman, S.A., & Kirnpal-Kaur, B.S., (2009). The antibacterial properties of Malaysian tualang honey against wound and enteric microorganisms in comparison to manuka honey. BMC Complementary and Alternative Medicine, 9, 34. doi:10.1186/1472-6882-9-34
42. Torres, M.P., Rachagani, S., Purohit, V., Pandey, P., Joshi, S., Moore, E.D., … Batra, S.K., (2012). Graviola:A novel promising natural-derived drug that inhibits tumorigenicity and metastasis of pancreatic cancer cells in vitro and in vivo through altering cell metabolism. Cancer Letters, 323, 29–40. doi:10.1016/j.canlet.2012.03.031
43. Tourneur, L., & Chiocchia, G., (2010). FADD:A regulator of life and death. Trends in Immunology, 31, 260–269. doi:10.1016/j.it.2010.05.005
44. Tsiapara, A.V., Jaakkola, M., Chinou, I., Graikou, K., Tolonen, T., Virtanen, V., & Moutsatsou, P., (2009). Bioactivity of Greek honey extracts on breast cancer (MCF-7), prostate cancer (PC-3) and endometrial cancer (Ishikawa) cells:Profile analysis of extracts. Food Chemistry, 116, 702–708. doi:10.1016/j.foodchem.2009.03.024
45. Vladusic, E.A., Hornby, A.E., Guerra-Vladusic, F.K., Lakins, J., & Lupu, R., (2000). Expression and regulation of estrogen receptor beta in human breast tumors and cell lines. Oncology Reports, 7, 157–167. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10601611
46. Yaacob, N.S., Hamzah, N., Nik Mohamed Kamal, N.N., Zainal Abidin, S.A., Lai, C.S., Navaratnam, V., & Norazmi, M.N., (2010). Anticancer activity of a sub-fraction of dichloromethane extract of Strobilanthes crispus on human breast and prostate cancer cells in vitro. BMC Complementary and Alternative Medicine, 10, 42. doi:10.1186/1472-6882-10-42
47. Yaacob, N., Fauzi, A., & Norazmi, M., (2013). Tualang honey promotes apoptotic cell death induced by tamoxifen in human breast cancer cell lines. Evidance-Based Complementary and Alternative Medicine, 2013, 989841. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/23476711
48. Yaacob, N., & Ismail, N., (2014). Comparison of cytotoxicity and genotoxicity of 4-hydroxytamoxifen in combination with Tualang honey in MCF-7 and MCF-10A cells. BMC Complementary and Alternative Medicine, 14, 106. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/2464637510.1186/1472-6882-14-106
49. Zaid, S.S., Sulaiman, S.A., Sirajudeen, K.N., & Othman, N.H., (2010). The effects of tualang honey on female reproductive organs, tibia bone and hormonal profile in ovariectomised rats—Animal model for menopause. BMC Complementary and Alternative Medicine, 10, 82. doi:10.1186/1472-6882-10-82