Hesperetin impairs glucose uptake and inhibits proliferation of breast cancer cells

Cell Biochemistry and Function

Volumn 31, Issue 5, 2013, Pages 374-379

  Yang, Yong ^a   Wolfram, Joy ^a   Boom, Kathryn ^a   Fang, Xiaohong ^b   Shen, Haifa ^a,c   Ferrari, Mauro ^a,c  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b INSTITUTE OF CHEMISTRY   (China)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Breast cancer cells; Glucose uptake; GLUT1; GLUT4; Hesperetin

Indexed keywords

ANTINEOPLASTIC AGENT; GLUCOSE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; HESPERETIN; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CANCER INHIBITION; CELL DIVISION; CELL MEMBRANE; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

BREAST CANCER CELLS; GLUCOSE UPTAKE; GLUT1; GLUT4; HESPERETIN;

ANTIGENS, CD; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; FLAVONES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 4; HESPERIDIN; HUMANS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84879836724     PISSN: 02636484     EISSN: 10990844     Source Type: Journal    
DOI: 10.1002/cbf.2905     Document Type: Article

References (50)

1. Macheda ML, Rogers S, Best JD. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 2005; 202: 654-662.
2. Medina RA, Owen GI. Glucose transporters: expression, regulation and cancer. Biol Res 2002; 35: 9-26.
3. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-1033.
4. Alo PL, Visca P, Botti C, et al. Immunohistochemical expression of human erythrocyte glucose transporter and fatty acid synthase in infiltrating breast carcinomas and adjacent typical/atypical hyperplastic or normal breast tissue. Am J Clin Pathol 2001; 116: 129-134.
5. Zimmerman RL, Goonewardene S, Fogt F. Glucose transporter Glut-1 is of limited value for detecting breast carcinoma in serous effusions. Mod Pathol 2001; 14: 748-751.
6. Hao LS, Ni Q, Jia GQ, et al. Expression of glucose transporter 1 in human breast carcinoma and its clinical significance. Sichuan Da Xue Xue Bao Yi Xue Ban 2009; 40: 44-47.
7. Kang SS, Chun YK, Hur MH, et al. Clinical significance of glucose transporter 1 (GLUT1) expression in human breast carcinoma. Jpn J Cancer Res 2002; 93: 1123-1128.
8. Younes M, Brown RW, Mody DR, Fernandez L, Laucirica R. GLUT1 expression in human breast carcinoma: correlation with known prognostic markers. Anticancer Res 1995; 15: 2895-2898.
9. Binder C, Binder L, Marx D, Schauer A, Hiddemann W. Deregulated simultaneous expression of multiple glucose transporter isoforms in malignant cells and tissues. Anticancer Res 1997; 17: 4299-4304.
10. Grover-McKay M, Walsh SA, Seftor EA, Thomas PA, Hendrix MJ. Role for glucose transporter 1 protein in human breast cancer. Pathol Oncol Res 1998; 4: 115-120.
11. Godoy A, Ulloa V, Rodriguez F, et al. Differential subcellular distribution of glucose transporters GLUT1-6 and GLUT9 in human cancer: ultrastructural localization of GLUT1 and GLUT5 in breast tumour tissues. J Cell Physiol 2006; 207: 614-627.
12. Rogers S, Docherty SE, Slavin JL, Henderson MA, Best JD. Differential expression of GLUT12 in breast cancer and normal breast tissue. Cancer Lett 2003; 193: 225-233.
13. Rivenzon-Segal D, Rushkin E, Polak-Charcon S, Degani H. Glucose transporters and transport kinetics in retinoic acid-differentiated T47D human breast cancer cells. Am J Physiol Endocrinol Metab 2000; 279: E508-519.
14. Zamora-Leon SP, Golde DW, Concha II, et al. Expression of the fructose transporter GLUT5 in human breast cancer. Proc Natl Acad Sci U S A 1996; 93: 1847-1852.
15. Sweeney G, Somwar R, Foster L, et al. Intracellular delivery of phosphatidylinositol(3, 4, 5)trisphosphate and phosphatidylinositol(3, 4)bisphosphate cause translocation and incorporation of GLUT4 to the plasma membrane without increasing glucose transport in muscle and fat cells. Diabetes 2001; 50: A19-A19.
16. Pessin JE, Thurmond DC, Elmendorf JS, Coker KJ, Okada S. Molecular basis of insulin-stimulated GLUT4 vesicle trafficking. J Biol Chem 1999; 274: 2593-2596.
17. Resh MD. Development of insulin responsiveness of the glucose transporter and the (Na+, K+)-adenosine triphosphatase during in vitro adipocyte differentiation. J Biol Chem 1982; 257: 6978-6986.
18. Muretta JM, Mastick CC. How insulin regulates glucose transport in adipocytes. Vitam Horm 2009; 80: 245-286.
19. Wang YF, Litzenburger B, Kuiatse I, et al. Expression and Activity of Both IGF and Insulin Signaling Pathways in a Large Panel of Breast Cancer Cell Lines. Cancer Res 2009; 69: 762s-762s.
20. Noguchi Y, Sato S, Marat D, et al. Glucose uptake in the human gastric cancer cell line, MKN28, is increased by insulin stimulation. Cancer Lett 1999; 140: 69-74.
21. Cheatham B, Vlahos CJ, Cheatham L, Wang L, Blenis J, Kahn CR. Phosphatidylinositol 3-Kinase Activation Is Required for Insulin Stimulation of Pp70 S6 Kinase, DNA-Synthesis, and Glucose-Transporter Translocation. Mol Cell Biol 1994; 14: 4902-4911.
22. Tanti JF, Gremeaux T, Grillo S, et al. Overexpression of a constitutively active form of phosphatidylinositol 3-kinase is sufficient to promote glut 4 translocation in adipocytes. J Biol Chem 1996; 271: 25227-25232.
23. Sweeney G, Garg RR, Ceddia RB, et al. Intracellular delivery of phosphatidylinositol (3, 4, 5)-trisphosphate causes incorporation of glucose transporter 4 into the plasma membrane of muscle and fat cells without increasing glucose uptake. J Biol Chem 2004; 279: 32233-32242.
24. Singh A, Purohit A, Hejaz HA, Potter BV, Reed MJ. Inhibition of deoxyglucose uptake in MCF-7 breast cancer cells by 2-methoxyestrone and 2-methoxyestrone-3-O-sulfamate. Mol Cell Endocrinol 2000; 160: 61-66.
25. Okumura M, Yamamoto M, Sakuma H, et al. Leptin and high glucose stimulate cell proliferation in MCF-7 human breast cancer cells: reciprocal involvement of PKC-alpha and PPAR expression. Biochim Biophys Acta 2002; 1592: 107-116.
26. Yamamoto M, Patel NA, Taggart J, Sridhar R, Cooper DR. A shift from normal to high glucose levels stimulates cell proliferation in drug sensitive MCF-7 human breast cancer cells but not in multidrug resistant MCF-7/ADR cells which overproduce PKC-beta II. Int J Cancer 1999; 83: 98-106.
27. Tomas-Barberan FA, Clifford MN. Flavanones, chalcones and dihydrochalcones - nature, occurrence and dietary burden. J Sci Food Agric 2000; 80: 1073-1080.
28. Walle T. Absorption and metabolism of flavonoids. Free Radic Biol Med 2004; 36: 829-837.
29. Park JB. Flavonoids are potential inhibitors of glucose uptake in U937 cells. Biochem Biophys Res Comm 1999; 260: 568-574.
30. Erlund I, Meririnne E, Alfthan G, Aro A. Plasma kinetics and urinary excretion of the flavanones naringenin and hesperetin in humans after ingestion of orange juice and grapefruit juice. J Nutr 2001; 131: 235-241.
31. Brett GM, Hollands W, Needs PW, et al. Absorption, metabolism and excretion of flavanone from single portions of orange fruit and juice and effects of anthropometric variables and contraceptive pill use on flavanone excretion. Br J Nutr 2009; 101: 664-675.
32. Mullen W, Archeveque MA, Edwards CA, Matsumoto H, Crozier A. Bioavailability and metabolism of orange juice flavanones in humans: impact of a full-fat yogurt. J Agric Food Chem 2008; 56: 11157-11164.
33. Chung FY, Huang MY, Yeh CS, et al. GLUT1 gene is a potential hypoxic marker in colorectal cancer patients. BMC Cancer 2009; 9: 241.
34. Brown RS, Goodman TM, Zasadny KR, Greenson JK, Wahl RL. Expression of hexokinase II and Glut-1 in untreated human breast cancer. Nucl Med Biol 2002; 29: 443-453.
35. Verhagen JN, Vanderheijden MCM, Rijksen G, Derkinderen PJ, Vanunnik JAM, Staal GEJ. Determination and Characterization of Hexokinase in Thyroid-Cancer and Benign Neoplasms. Cancer 1985; 55: 1519-1524.
36. Yasuda S, Arii S, Mori A, et al. Hexokinase II and VEGF expression in liver tumors: correlation with hypoxia-inducible factor-1 alpha and its significance. J Hepatol 2004; 40: 117-123.
37. Cao XH, Fang LY, Gibbs S, et al. Glucose uptake inhibitor sensitizes cancer cells to daunorubicin and overcomes drug resistance in hypoxia. Cancer Chemoth Pharm 2007; 59: 495-505.
38. Maschek G, Savaraj N, Priebe W, et al. 2-deoxy-D-glucose increases the efficacy of adriamycin and paclitaxel in human osteosarcoma and non-small cell lung cancers in vivo. Cancer Res 2004; 64: 31-34.
39. Sandulache VC, Skinner HD, Wang Y, et al. Glycolytic inhibition alters anaplastic thyroid carcinoma tumor metabolism and improves response to conventional chemotherapy and radiation. Mol Cancer Ther 2012; 11: 1373-1380.
40. Brown RS, Wahl RL. Overexpression of Glut-1 Glucose-Transporter in Human Breast-Cancer - an Immunohistochemical Study. Cancer 1993; 72: 2979-2985.
41. Wojtaszewski JFP, Hansen BF, Urso B, Richter EA. Wortmannin inhibits both insulin- and contraction-stimulated glucose uptake and transport in rat skeletal muscle. J Appl Physiol 1996; 81: 1501-1509.
42. Purcell SH, Chi MM, Moley KH. Insulin-Stimulated Glucose Uptake Occurs in Specialized Cells within the Cumulus Oocyte Complex. Endocrinology 2012; 153: 2444-2454.
43. Zhou SH, Fan J, Chen XM, Cheng KJ, Wang SQ. Inhibition of Cell Proliferation and Glucose Uptake in Human Laryngeal Carcinoma Cells by Antisense Oligonucleotides against Glucose Transporter-1. Head Neck-J Sci Spec 2009; 31: 1624-1633.
44. Yanez JA, Remsberg CM, Miranda ND, Vega-Villa KR, Andrew PK, Davies NM. Pharmacokinetics of selected chiral flavonoids: hesperetin, narigenin and eriodictyol in rats and their content in fruit juice. Biopharm Drug Dispos 2008; 29: 63-82.
45. Brand W, Shao J, Hoek-van den Hil EF, et al. Stereoselective conjugation, transport and bioactivity of s- and R-hesperetin enantiomers in vitro. J Agric Food Chem 2010; 58: 6119-6125.
46. Nalini N, Aranganathan S, Kabalimurthy J. Chemopreventive efficacy of hesperetin (citrus flavonone) against 1, 2-dimethylhydrazine-induced rat colon carcinogenesis. Toxicol Mech Methods 2012; 22(5): 397-408.
47. Patil JR, Chidambara Murthy KN, Jayaprakasha GK, Chetti MB, Patil BS. Bioactive compounds from Mexican lime ( Citrus aurantifolia ) juice induce apoptosis in human pancreatic cells. J Agric Food Chem 2009; 57: 10933-10942.
48. Sivagami G, Vinothkumar R, Preethy CP, et al. Role of hesperetin (a natural flavonoid) and its analogue on apoptosis in HT-29 human colon adenocarcinoma cell line--a comparative study. Food Chem Toxicol 2012; 50: 660-671.
49. Choi EJ, Kim GD, Chee KM, Kim GH. Effects of hesperetin on vessel structure formation in mouse embryonic stem (mES) cells. Nutrition 2006; 22: 947-951.
50. Brand W, Oosterhuis B, Krajcsi P, et al. Interaction of hesperetin glucuronide conjugates with human BCRP, MRP2 and MRP3 as detected in membrane vesicles of overexpressing baculovirus-infected Sf9 cells. Biopharm Drug Dispos 2011; 32: 530-535.