Citrus flavonoid naringenin reduces mammary tumor cell viability, adipose mass, and adipose inflammation in obese ovariectomized mice

Molecular Nutrition and Food Research

Volumn 61, Issue 9, 2017, Pages

  Ke, Jia Yu ^a   Banh, Taylor ^a   Hsiao, Yung Hsuan ^a   Cole, Rachel M ^a   Straka, Shana R ^b   Yee, Lisa D ^b   Belury, Martha A ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Adipose inflammation; Breast cancer; Naringenin; Obesity; Ovariectomy

Indexed keywords

FLAVANONE DERIVATIVE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; NARINGENIN;

ADIPOSE TISSUE; ANIMAL; BLOOD; BODY WEIGHT; C57BL MOUSE; CELL SURVIVAL; COMPLICATION; DRUG EFFECT; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; INFLAMMATION; METABOLISM; MOUSE; OBESITY; OVARIECTOMY; PATHOLOGY; TUMOR CELL LINE;

ADIPOSE TISSUE; ADIPOSITY; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BODY WEIGHT; CELL LINE, TUMOR; CELL SURVIVAL; FEMALE; FLAVANONES; INFLAMMATION; INSULIN; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, INBRED C57BL; OBESITY; OVARIECTOMY;

EID: 85018293374     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201600934     Document Type: Article

References (48)

1. La Vecchia, C., Giordano, S. H., Hortobagyi, G. N., Chabner, B., Overweight, obesity, diabetes, and risk of breast cancer: interlocking pieces of the puzzle. Oncologist 2011, 16, 726–729.
2. Eliassen, A. H., Colditz, G. A., Rosner, B., Willett, W. C., Hankinson, S. E., Adult weight change and risk of postmenopausal breast cancer. JAMA 2006, 296, 193–201.
3. Iyengar, N. M., Hudis, C. A., Dannenberg, A. J., Obesity and inflammation: new insights into breast cancer development and progression. Am. Soc. Clin. Oncol. Educ. Book 2013, 33, 46–51.
4. Ligibel, J. A., Strickler, H. D., Obesity and its impact on breast cancer: tumor incidence, recurrence, survival, and possible interventions. Am. Soc. Clin. Oncol. Educ. Book 2013, 52–59.
5. Bodmer, M., Meier, C., Krahenbuhl, S., Jick, S. S., Meier, C. R., Long-term metformin use is associated with decreased risk of breast cancer. Diabetes Care 2010, 33, 1304–1308.
6. Decensi, A., Puntoni, M., Goodwin, P., Cazzaniga, M. et al., Metformin and cancer risk in diabetic patients: a systematic review and meta-analysis. Cancer Prev. Res. (Phila) 2010, 3, 1451–1461.
7. Foretz, M., Guigas, B., Bertrand, L., Pollak, M., Viollet, B., Metformin: from mechanisms of action to therapies. Cell Metab. 2014, 20, 953–966.
8. de Jager, J., Kooy, A., Lehert, P., Wulffele, M. G. et al., Long term treatment with metformin in patients with type 2 diabetes and risk of vitamin B-12 deficiency: randomised placebo controlled trial. BMJ 2010, 340, c2181.
9. Alam, M. A., Subhan, N., Rahman, M. M., Uddin, S. J. et al., Effect of citrus flavonoids, naringin and naringenin, on metabolic syndrome and their mechanisms of action. Adv. Nutr. 2014, 5, 404–417.
10. Mulvihill, E. E., Allister, E. M., Sutherland, B. G., Telford, D. E. et al., Naringenin prevents dyslipidemia, apolipoprotein B overproduction, and hyperinsulinemia in LDL receptor-null mice with diet-induced insulin resistance. Diabetes 2009, 58, 2198–2210.
11. Ke, J.-Y., Kliewer, K. L., Hamad, E. M., Cole, R. M. et al., The flavonoid, naringenin, decreases adipose tissue mass and attenuates ovariectomy-associated metabolic disturbances in mice. Nutr. Metabol. 2015, 12, 1.
12. Ke, J. Y., Cole, R. M., Hamad, E. M., Hsiao, Y. H. et al., Citrus flavonoid, naringenin, increases locomotor activity and reduces diacylglycerol accumulation in skeletal muscle of obese ovariectomized mice. Mol. Nutr. Food Res. 2016, 60, 313–324.
13. Kanno, S., Tomizawa, A., Hiura, T., Osanai, Y. et al., Inhibitory effects of naringenin on tumor growth in human cancer cell lines and sarcoma S-180-implanted mice. Biol. Pharm. Bull. 2005, 28, 527–530.
14. Mir, I. A., Tiku, A. B., Chemopreventive and therapeutic potential of "naringenin," a flavanone present in citrus fruits. Nutr. Cancer 2015, 67, 27–42.
15. Bulzomi, P., Bolli, A., Galluzzo, P., Leone, S. et al., Naringenin and 17beta-estradiol coadministration prevents hormone-induced human cancer cell growth. IUBMB Life 2010, 62, 51–60.
16. Leonardi, T., Vanamala, J., Taddeo, S. S., Davidson, L. A. et al., Apigenin and naringenin suppress colon carcinogenesis through the aberrant crypt stage in azoxymethane-treated rats. Exp. Biol. Med. (Maywood) 2010, 235, 710–717.
17. So, F. V., Guthrie, N., Chambers, A. F., Moussa, M. et al., Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutr. Cancer 1996, 26, 167–181.
18. Totta, P., Acconcia, F., Leone, S., Cardillo, I. et al., Mechanisms of naringenin-induced apoptotic cascade in cancer cells: involvement of estrogen receptor alpha and beta signalling. IUBMB Life 2004, 56, 491–499.
19. Harmon, A. W., Patel, Y. M., Naringenin inhibits glucose uptake in MCF-7 breast cancer cells: a mechanism for impaired cellular proliferation. Breast Cancer Res. Treat. 2004, 85, 103–110.
20. Gu, J. W., Young, E., Patterson, S. G., Makey, K. L. et al., Postmenopausal obesity promotes tumor angiogenesis and breast cancer progression in mice. Cancer Biol. Ther. 2011, 11, 910–917.
21. Chitchumroonchokchai, C., Thomas-Ahner, J. M., Li, J., Riedl, K. M. et al., Anti-tumorigenicity of dietary alpha-mangostin in an HT-29 colon cell xenograft model and the tissue distribution of xanthones and their phase II metabolites. Mol. Nutr. Food Res. 2013, 57, 203–211.
22. Teegarden, M. D., Riedl, K. M., Schwartz, S. J., Chromatographic separation of PTAD-derivatized 25-hydroxyvitamin D3 and its C-3 epimer from human serum and murine skin. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2015, 991, 118–121.
23. Livak, K. J., Schmittgen, T. D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25, 402-408.
24. Seo, B. R., Bhardwaj, P., Choi, S., Gonzalez, J. et al., Obesity-dependent changes in interstitial ECM mechanics promote breast tumorigenesis. Sci. Transl. Med. 2015, 7, 301ra130.
25. Maccio, A., Madeddu, C., Obesity, inflammation, and postmenopausal breast cancer: therapeutic implications. Scientific World J. 2011, 11, 2020–2036.
26. Meric-Bernstam, F., Gonzalez-Angulo, A. M., Targeting the mTOR signaling network for cancer therapy. J. Clin. Oncol. 2009, 27, 2278–2287.
27. Pullen, N., Thomas, G., The modular phosphorylation and activation of p70s6k. FEBS Lett. 1997, 410, 78–82.
28. Ogden, C. L., Carroll, M. D., Kit, B. K., Flegal, K. M., Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014, 311, 806–814.
29. Chan, D. S., Vieira, A. R., Aune, D., Bandera, E. V. et al., Body mass index and survival in women with breast cancer-systematic literature review and meta-analysis of 82 follow-up studies. Ann. Oncol. 2014, 25, 1901–1914.
30. Rohan, T. E., Heo, M., Choi, L., Datta, M. et al., Body fat and breast cancer risk in postmenopausal women: a longitudinal study. J. Cancer Epidemiol. 2013, 2013, 754815.
31. Simpson, E. R., Brown, K. A., Minireview: obesity and breast cancer: a tale of inflammation and dysregulated metabolism. Mol. Endocrinol. 2013, 27, 715–725.
32. Hatkevich, T., Ramos, J., Santos-Sanchez, I., Patel, Y. M., A naringenin-tamoxifen combination impairs cell proliferation and survival of MCF-7 breast cancer cells. Exp. Cell Res. 2014, 327, 331–339.
33. Filho, J. C., Sarria, A. L., Becceneri, A. B., Fuzer, A. M. et al., Copper (II) and 2,2'-bipyridine complexation improves chemopreventive effects of naringenin against breast tumor cells. PloS One 2014, 9, e107058.
34. Salah I Abaza, M., Orabi, K. Y., Al-Quattan, E., Al-Attiyah, R. J., Growth inhibitory and chemo-sensitization effects of naringenin, a natural flavanone purified from Thymus vulgaris, on human breast and colorectal cancer. Cancer Cell Int. 2015, 15, 46.
35. de Boer, V. C., Dihal, A. A., van der Woude, H., Arts, I. C. et al., Tissue distribution of quercetin in rats and pigs. J. Nutr. 2005, 135, 1718–1725.
36. Azorin-Ortuno, M., Yanez-Gascon, M. J., Vallejo, F., Pallares, F. J. et al., Metabolites and tissue distribution of resveratrol in the pig. Mol. Nutr. Food Res. 2011, 55, 1154-1168.
37. Felgines, C., Texier, O., Garcin, P., Besson, C. et al., Tissue distribution of anthocyanins in rats fed a blackberry anthocyanin-enriched diet. Mol. Nutr. Food Res. 2009, 53, 1098–1103.
38. Elsheikh, S., Green, A. R., Aleskandarany, M. A., Grainge, M. et al., CCND1 amplification and cyclin D1 expression in breast cancer and their relation with proteomic subgroups and patient outcome. Breast Cancer Res. Treat. 2008, 109, 325–335.
39. Stendahl, M., Kronblad, A., Ryden, L., Emdin, S. et al., Cyclin D1 overexpression is a negative predictive factor for tamoxifen response in postmenopausal breast cancer patients. Br. J. Cancer 2004, 90, 1942–1948.
40. Ma, C. X., Reinert, T., Chmielewska, I., Ellis, M. J., Mechanisms of aromatase inhibitor resistance. Nat. Rev. Cancer 2015, 15, 261–275.
41. Osborne, C. K., Schiff, R., Mechanisms of endocrine resistance in breast cancer. Annu. Rev. Med. 2011, 62, 233–247.
42. Paplomata, E., O'Regan, R., The PI3K/AKT/mTOR pathway in breast cancer: targets, trials and biomarkers. Ther. Adv. Med. Oncol. 2014, 6, 154–166.
43. Garcia-Becerra, R., Santos, N., Diaz, L., Camacho, J., Mechanisms of resistance to endocrine therapy in breast cancer: focus on signaling pathways, miRNAs and genetically based resistance. Int. J. Mol. Sci. 2012, 14, 108–145.
44. Fujisaki, K., Fujimoto, H., Sangai, T., Nagashima, T. et al., Cancer-mediated adipose reversion promotes cancer cell migration via IL-6 and MCP-1. Breast Cancer Res. Treat. 2015, 150, 255–263.
45. Purushotham, A., Tian, M., Belury, M. A., The citrus fruit flavonoid naringenin suppresses hepatic glucose production from Fao hepatoma cells. Mol. Nutr. Food Res. 2009, 53, 300–307.
46. Jalving, M., Gietema, J. A., Lefrandt, J. D., de Jong, S. et al., Metformin: taking away the candy for cancer? Eur. J. Cancer 2010, 46, 2369–2380.
47. Dowling, R. J., Zakikhani, M., Fantus, I. G., Pollak, M. et al., Metformin inhibits mammalian target of rapamycin-dependent translation initiation in breast cancer cells. Cancer Res. 2007, 67, 10804–10812.
48. Zhuang, Y., Miskimins, W. K., Cell cycle arrest in Metformin treated breast cancer cells involves activation of AMPK, downregulation of cyclin D1, and requires p27Kip1 or p21Cip1. J. Mol. Signal. 2008, 3, 18.