The inhibitory effect of Manuka honey on human colon cancer HCT-116 and LoVo cell growth. Part 1: The suppression of cell proliferation, promotion of apoptosis and arrest of the cell cycle

Food and Function

Volumn 9, Issue 4, 2018, Pages 2145-2157

  Afrin, Sadia ^a   Giampieri, Francesca ^a   Gasparrini, Massimiliano ^a   Forbes Hernández, Tamara Y ^a   Cianciosi, Danila ^a   Reboredo Rodriguez, Patricia ^a,b   Amici, Adolfo ^a   Quiles, Josè L ^c   Battino, Maurizio ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF VIGO   (Spain)

^c UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; DISEASES; FLAVONOIDS; FOOD PRODUCTS; GENE EXPRESSION; PHENOLS;

APOPTOSIS INDUCTION; APOPTOTIC PATHWAYS; CELL CYCLE REGULATORS; CHEMOPREVENTIVE EFFECTS; DOSE-DEPENDENT MANNER; HUMAN COLON CANCER; PHENOLIC COMPOUNDS; PROTEIN EXPRESSIONS;

CELL DEATH;

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CELL CYCLE PROTEIN; TUMOR PROTEIN;

ADENOCARCINOMA; ANALYSIS; APOPTOSIS; CARCINOMA; CELL CYCLE S PHASE; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; COLON TUMOR; COMPARATIVE STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; FUNCTIONAL FOOD; GENE EXPRESSION REGULATION; GENETICS; HONEY; HUMAN; ISOLATION AND PURIFICATION; LEPTOSPERMUM; METABOLISM; NECTAR; PATHOLOGY; TUMOR CELL LINE;

ADENOCARCINOMA; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BIOMARKERS; CARCINOMA; CELL CYCLE PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; FUNCTIONAL FOOD; GENE EXPRESSION REGULATION, NEOPLASTIC; HONEY; HUMANS; LEPTOSPERMUM; NEOPLASM PROTEINS; PLANT NECTAR; S PHASE;

EID: 85051008208     PISSN: 20426496     EISSN: 2042650X     Source Type: Journal    
DOI: 10.1039/c8fo00164b     Document Type: Article

References (43)

1. J. Ferlay, I. Soerjomataram, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D. M. Parkin, D. Forman and F. Bray, Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012, Int. J. Cancer, 2015, 136, E359-E386.
2. A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu and M. J. Thun, Cancer statistics, 2009, Ca-Cancer J. Clin., 2009, 59, 225-249.
3. A. B. Mariotto, K. Robin Yabroff, Y. Shao, E. J. Feuer and M. L. Brown, Projections of the cost of cancer care in the United States: 2010-2020, J. Natl. Cancer Inst., 2011, 103, 117-128.
4. S. Elmore, Apoptosis: a review of programmed cell death, Toxicol. Pathol., 2007, 35, 495-516.
5. C.-W. Phang, S. A. Karsani, G. Sethi and S. N. A. Malek, Flavokawain C inhibits cell cycle and promotes apoptosis, associated with endoplasmic reticulum stress and regulation of MAPKs and Akt signaling pathways in HCT 116 human colon carcinoma cells, PLoS One, 2016, 11, e0148775.
6. G. I. Evan and K. H. Vousden, Proliferation, cell cycle and apoptosis in cancer, Nature, 2001, 411, 342-348.
7. A. Custodio and J. Feliu, Prognostic and predictive biomarkers for epidermal growth factor receptor-targeted therapy in colorectal cancer: beyond KRAS mutations, Crit. Rev. Oncol. Hematol., 2013, 85, 45-81.
8. X.-F. Huang and J.-Z. Chen, Obesity, the PI3K/Akt signal pathway and colon cancer, Obes. Rev., 2009, 10, 610-616.
9. W. Zhang and H. T. Liu, MAPK signal pathways in the regulation of cell proliferation in mammalian cells, Cell Res., 2002, 12, 9-18.
10. R. Sano and J. C. Reed, ER stress-induced cell death mechanisms, Biochim. Biophys. Acta, 2013, 1833, 3460-3470.
11. K. W. Lee, A. M. Bode and Z. Dong, Molecular targets of phytochemicals for cancer prevention, Nat. Rev. Cancer, 2011, 11, 211-218.
12. F. M. F. Roleira, E. J. Tavares-da-Silva, C. L. Varela, S. C. Costa, T. Silva, J. Garrido and F. Borges, Plant derived and dietary phenolic antioxidants: anticancer properties, Food Chem., 2015, 183, 235-258.
13. J. M. Alvarez-Suarez, M. Gasparrini, T. Y. Forbes-Hernández, L. Mazzoni and F. Giampieri, The composition and biological activity of honey: a focus on Manuka honey, Foods, 2014, 3, 420-432.
14. J. M. Alvarez-Suarez, F. Giampieri, M. Cordero, M. Gasparrini, T. Y. Forbes-Hernández, L. Mazzoni, S. Afrin, P. Beltrán-Ayala, A. M. González-Paramás and C. Santos-Buelga, Activation of AMPK/Nrf2 signalling by Manuka honey protects human dermal fibroblasts against oxidative damage by improving antioxidant response and mitochondrial function promoting wound healing, J. Funct. Foods, 2016, 25, 38-49.
15. M. Badolato, G. Carullo, E. Cione, F. Aiello and M. C. Caroleo, From the hive: Honey, a novel weapon against cancer, Eur. J. Med. Chem., 2017, 142, 290-299.
16. S. Afrin, T. Y. Forbes-Hernandez, M. Gasparrini, S. Bompadre, J. L. Quiles, G. Sanna, N. Spano, F. Giampieri and M. Battino, Strawberry-Tree Honey Induces Growth Inhibition of Human Colon Cancer Cells and Increases ROS Generation: A Comparison with Manuka Honey, Int. J. Mol. Sci., 2017, 18, 613.
17. M. J. Fernandez-Cabezudo, R. El-Kharrag, F. Torab, G. Bashir, J. A. George, H. El-Taji and B. K. Al-Ramadi, 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, 2013, 8, e55993.
18. B. Dimitrova, R. Gevrenova and E. Anklam, Analysis of phenolic acids in honeys of different floral origin by solidpase extraction and high-performance liquid chromatography, Phytochem. Anal., 2007, 18, 24-32.
19. C. Sun, H. Tan, Y. Zhang and H. Zhang, Phenolics and abscisic acid identified in acacia honey comparing different SPE cartridges coupled with HPLC-PDA, J. Food Compos. Anal., 2016, 53, 91-101.
20. N. Yamada, S. Noguchi, T. Mori, T. Naoe, K. Maruo and Y. Akao, Tumor-suppressive microRNA-145 targets catenin d-1 to regulate Wnt/-catenin signaling in human colon cancer cells, Cancer Lett., 2013, 335, 332-342.
21. A. Y. B. H. Ahmed, S. M. Wabaidur, M. R. Siddiqui, Z. A. Alothman, M. S. Obeid, M. R. Khan and S. A. Altamrah, Simultaneous determination of twenty-five polyphenols in multifloral and cactus honeys using solid-phase extraction and high-performance liquid chromatography with photodiode array detection, Eur. Food Res. Technol., 2016, 242, 943-952.
22. S. M. Marshall, K. R. Schneider, K. V. Cisneros and L. Gu, Determination of antioxidant capacities, a-dicarbonyls, and phenolic phytochemicals in Florida varietal honeys using HPLC-DAD-ESI-MSn, J. Agric. Food Chem., 2014, 62, 8623-8631.
23. R. J. Weston, K. R. Mitchell and K. L. Allen, Antibacterial phenolic components of New Zealand manuka honey, Food Chem., 1999, 64, 295-301.
24. C. T. P. Wen, S. Z. Hussein, S. Abdullah, N. A. Karim, S. Makpol and Y. A. M. Yusof, Gelam and nenas honeys inhibit proliferation of HT 29 colon cancer cells by inducing DNA damage and apoptosis while suppressing inflammation, Asian Pac. J. Cancer Prev., 2012, 13, 1605-1610.
25. A. A. Tahir, N. F. A. Sani, N. A. Murad, S. Makpol, W. Z. W. Ngah and Y. A. M. Yusof, Combined ginger extract & Gelam honey modulate Ras/ERK and PI3K/AKT pathway genes in colon cancer HT29 cells, Nutr. J., 2015, 14, 31.
26. S. K. Jaganathan and M. Mandal, Involvement of nonprotein thiols, mitochondrial dysfunction, reactive oxygen species and p53 in honey-induced apoptosis, Invest. New Drugs, 2010, 28, 624-633.
27. J.-Y. Kee, Y.-H. Han, D.-S. Kim, J.-G. Mun, J. Park, M.-Y. Jeong, J.-Y. Um and S.-H. Hong, Inhibitory effect of quercetin on colorectal lung metastasis through inducing apoptosis, and suppression of metastatic ability, Phytomedicine, 2016, 23, 1680-1690.
28. F. Giampieri, J. L. Quiles, F. J. Orantes-Bermejo, M. Gasparrini, T. Y. Forbes-Hernandez, C. Sánchez-González, J. Llopis, L. Rivas-García, S. Afrin, A. Varela-López, D. Cianciosi, P. Reboredo-Rodriguez, C. T. Fernández-Piñar, C. Iglesias Ruben, R. Ruiz, S. Aparicio, J. Crespo, D. L. Lopez, J. Xiao and M. Battino, Are by-products from beeswax recycling process a new promising source of bioactive compounds with biomedical properties?, Food Chem. Toxicol., 2018, 112, 126-133.
29. B. Yuan, N. Ma, L. Zhao, E. Zhao, Z. Gao, W. Wang, M. Song, G. Zhang, Q. Hu and H. Xiao, In vitro and in vivo inhibitory effects of a Pleurotuseryngiiprotein on colon cancer cells, Food Funct., 2017, 8, 3553-3562.
30. L. Song, J. Chang and Z. Li, A serine protease extracted from Trichosantheskirilowiiinduces apoptosis via the PI3K/AKT-mediated mitochondrial pathway in human colorectal adenocarcinoma cells, Food Funct., 2016, 7, 843-854.
31. K. B. Arun, A. Madhavan, T. R. Reshmitha, S. Thomas and P. Nisha, Musa paradisiaca inflorescence induces human colon cancer cell death by modulating cascades of transcriptional events, Food Funct., 2018, 9, 511-524.
32. M. Bhardwaj, N.-H. Kim, S. Paul, R. Jakhar, J. Han and S. C. Kang, 5-Hydroxy-7-methoxyflavone triggers mitochondrial-associated cell death via reactive oxygen species signaling in human colon carcinoma cells, PLoS One, 2016, 11, e0154525.
33. H. Teng, Q. Huang and L. Chen, Inhibition of cell proliferation and triggering of apoptosis by agrimonolide through MAP kinase (ERK and p38) pathways in human gastric cancer AGS cells, Food Funct., 2016, 7, 4605-4613.
34. G. Huang, J. Mao, Z. Ji and A. Ailati, Stachyose-induced apoptosis of Caco-2 cells via the caspase-dependent mitochondrial pathway, Food Funct., 2016, 6, 765-771.
35. H. Cho, H. Jung, H. Lee, H. C. Yi, H.-k. Kwak and K. T. Hwang, Chemopreventive activity of ellagitannins and their derivatives from black raspberry seeds on HT-29 colon cancer cells, Food Funct., 2015, 6, 1675-1683.
36. A. L. Rodd, K. Ververis, D. Sayakkarage, A. W. Khan, H. Rafehi, M. Ziemann, S. J. Loveridge, R. Lazarus, C. Kerr and T. Lockett, RNA sequencing supports distinct reactive oxygen species-mediated pathways of apoptosis by high and low size mass fractions of Bay leaf (Laurisnobilis) in HT-29 cells, Food Funct., 2015, 6, 2507-2524.
37. K. Vermeulen, D. R. Van Bockstaele and Z. N. Berneman, The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer, Cell Proliferation, 2003, 36, 131-149.
38. Y. Sun, X. Wu, X. Cai, M. Song, J. Zheng, C. Pan, P. Qiu, L. Zhang, S. Zhou and Z. Tang, Identification of pinostilbene as a major colonic metabolite of pterostilbene and its inhibitory effects on colon cancer cells, Mol. Nutr. Food Res., 2016, 60, 1924-1932.
39. S. Gómez-Alonso, V. J. Collins, D. Vauzour, A. Rodríguez-Mateos, G. Corona and J. P. E. Spencer, Inhibition of colon adenocarcinoma cell proliferation by flavonols is linked to a G2/M cell cycle block and reduction in cyclin D1 expression, Food Chem., 2012, 130, 493-500.
40. J. Wu, C. Omene, J. Karkoszka, M. Bosland, J. Eckard, C. B. Klein and K. Frenkel, 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, 43-53.
41. J. J. Johnson and H. Mukhtar, Curcumin for chemoprevention of colon cancer, Cancer Lett., 2007, 255, 170-181.
42. I. Khan, S. Paul, R. Jakhar, M. Bhardwaj, J. Han and S. C. Kang, Novel quercetin derivative TEF induces ER stress and mitochondria-mediated apoptosis in human colon cancer HCT-116 cells, Biomed. Pharmacother., 2016, 84, 789-799.
43. R. Zhang, Y. Chung, H. S. Kim, D. H. Kim, H. S. Kim, W. Y. Chang and J. W. Hyun, 20-O-(-D-glucopyranosyl)-20 (S)-protopanaxadiol induces apoptosis via induction of endoplasmic reticulum stress in human colon cancer cells, Oncol. Rep., 2013, 29, 1365-1370.