Epithelial-mesenchymal transition induces similar metabolic alterations in two independent breast cancer cell lines

Cancer Letters

Volumn 364, Issue 1, 2015, Pages 44-58

  Kondaveeti, Yuvabharath ^a   Guttilla Reed, Irene K ^b   White, Bruce A ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF SAINT JOSEPH   (United States)

Author keywords

Aerobic glycolysis; Breast cancer; Epithelial mesenchymal transition; Metabolic reprogramming; Warburg effect

Indexed keywords

GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 12; GLUCOSE TRANSPORTER 3; LACTATE DEHYDROGENASE; MESSENGER RNA; PENTOSE PHOSPHATE; STAT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; GLYCOGEN PHOSPHORYLASE; LACTIC ACID DERIVATIVE;

ARTICLE; BREAST CANCER; CANCER CELL; CELL GROWTH; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GLUCONEOGENESIS; GLUCOSE TRANSPORT; GLYCOGEN METABOLISM; GLYCOLYSIS; HUMAN; HUMAN CELL; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; UPREGULATION; BREAST TUMOR; FEMALE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GLUCONEOGENESIS; GLYCOGEN PHOSPHORYLASE; GLYCOLYSIS; HUMANS; L-LACTATE DEHYDROGENASE; LACTATES;

EID: 84930008414     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.04.025     Document Type: Article

References (50)

1. Konecny G., Pauletti G., Pegram M., Untch M., Dandekar S., Aguilar Z., et al. Quantitative association between HER-2/neu and steroid hormone receptors in hormone receptor-positive primary breast cancer. J. Natl. Cancer Inst 2003, 95(2):142-153.
2. Cleator S., Heller W., Coombes R.C. Triple-negative breast cancer: therapeutic options. Lancet Oncol 2007, 8(3):235-244.
3. Weigelt B., Peterse J.L., van 't Veer L.J. Breast cancer metastasis: markers and models. Nat. Rev. Cancer 2005, 5(8):591-602.
4. Valastyan S., Weinberg R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147(2):275-292.
5. De Craene B., Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer 2013, 13(2):97-110.
6. Lamouille S., Xu J., Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol 2014, 15(3):178-196.
7. Koppenol W.H., Bounds P.L., Dang C.V. Otto Warburg's contributions to current concepts of cancer metabolism. Nat. Rev. Cancer 2011, 11(5):325-337.
8. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008, 7(1):11-20.
9. Deberardinis R.J., Sayed N., Ditsworth D., Thompson C.B. Brick by brick: metabolism and tumor cell growth. Curr. Opin. Genet. Dev 2008, 18(1):54-61.
10. Ward P.S., Thompson C.B. Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate. Cancer Cell 2012, 21(3):297-308.
11. Guttilla I.K., Phoenix K.N., Hong X., Tirnauer J.S., Claffey K.P., White B.A. Prolonged mammosphere culture of MCF-7 cells induces an EMT and repression of the estrogen receptor by microRNAs. Breast Cancer Res. Treat 2012, 132(1):75-85.
12. Sullivan N.J., Sasser A.K., Axel A.E., Vesuna F., Raman V., Ramirez N., et al. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 2009, 28(33):2940-2947.
13. Xie G., Yao Q., Liu Y., Du S., Liu A., Guo Z., et al. IL-6-induced epithelial-mesenchymal transition promotes the generation of breast cancer stem-like cells analogous to mammosphere cultures. Int. J. Oncol 2012, 40(4):1171-1179.
14. + breast cancer by expanding the cancer stem cell population. Mol. Cell 2012, 47(4):570-584.
15. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133(4):704-715.
16. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139(5):871-890.
17. Visvader J.E. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 2009, 23(22):2563-2577.
18. Ciavardelli D., Rossi C., Barcaroli D., Volpe S., Consalvo A., Zucchelli M., et al. Breast cancer stem cells rely on fermentative glycolysis and are sensitive to 2-deoxyglucose treatment. Cell Death Dis 2014, 5:e1336.
19. Yamamoto T., Seino Y., Fukumoto H., Koh G., Yano H., Inagaki N., et al. Over-expression of facilitative glucose transporter genes in human cancer. Biochem. Biophys. Res. Commun 1990, 170(1):223-230.
20. Augustin R. The protein family of glucose transport facilitators: it's not only about glucose after all. IUBMB Life 2010, 62(5):315-333.
21. Flavahan W.A., Wu Q., Hitomi M., Rahim N., Kim Y., Sloan A.E., et al. Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake. Nat. Neurosci 2013, 16(10):1373-1382.
22. Masin M., Vazquez J., Rossi S., Groeneveld S., Samson N., Schwalie P.C., et al. GLUT3 is induced during epithelial-mesenchymal transition and promotes tumor cell proliferation in non-small cell lung cancer. Cancer Metab 2014, 2:11.
23. Rogers S., Macheda M.L., Docherty S.E., Carty M.D., Henderson M.A., Soeller W.C., et al. Identification of a novel glucose transporter-like protein-GLUT-12. Am. J. Physiol. Endocrinol. Metab 2002, 282(3):E733-E738.
24. Stuart C.A., Howell M.E., Zhang Y., Yin D. Insulin-stimulated translocation of glucose transporter (GLUT) 12 parallels that of GLUT4 in normal muscle. J. Clin. Endocrinol. Metab 2009, 94(9):3535-3542.
25. Pujol-Gimenez J., Barrenetxe J., Gonzalez-Muniesa P., Lostao M.P. The facilitative glucose transporter GLUT12: what do we know and what would we like to know?. J. Physiol. Biochem 2013, 69(2):325-333.
26. Macheda M.L., Rogers S., Best J.D. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J. Cell. Physiol 2005, 202(3):654-662.
27. Favaro E., Bensaad K., Chong M.G., Tennant D.A., Ferguson D.J., Snell C., et al. Glucose utilization via glycogen phosphorylase sustains proliferation and prevents premature senescence in cancer cells. Cell Metab 2012, 16(6):751-764.
28. Hirschhaeuser F., Sattler U.G., Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res 2011, 71(22):6921-6925.
29. Doherty J.R., Cleveland J.L. Targeting lactate metabolism for cancer therapeutics. J. Clin. Invest 2013, 123(9):3685-3692.
30. Fantin V.R., St-Pierre J., Leder P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006, 9(6):425-434.
31. Wang Z.Y., Loo T.Y., Shen J.G., Wang N., Wang D.M., Yang D.P., et al. LDH-A silencing suppresses breast cancer tumorigenicity through induction of oxidative stress mediated mitochondrial pathway apoptosis. Breast Cancer Res. Treat 2012, 131(3):791-800.
32. Leiblich A., Cross S.S., Catto J.W., Phillips J.T., Leung H.Y., Hamdy F.C., et al. Lactate dehydrogenase-B is silenced by promoter hypermethylation in human prostate cancer. Oncogene 2006, 25(20):2953-2960.
33. Brown N.J., Higham S.E., Perunovic B., Arafa M., Balasubramanian S., Rehman I. Lactate dehydrogenase-B is silenced by promoter methylation in a high frequency of human breast cancers. PLoS ONE 2013, 8(2):e57697.
34. McCleland M.L., Adler A.S., Shang Y., Hunsaker T., Truong T., Peterson D., et al. An integrated genomic screen identifies LDHB as an essential gene for triple-negative breast cancer. Cancer Res 2012, 72(22):5812-5823.
35. Dennison J.B., Molina J.R., Mitra S., Gonzalez-Angulo A.M., Balko J.M., Kuba M.G., et al. Lactate dehydrogenase B: a metabolic marker of response to neoadjuvant chemotherapy in breast cancer. Clin. Cancer Res 2013, 19(13):3703-3713.
36. Lee I., Lee S.J., Kang W.K., Park C. Inhibition of monocarboxylate transporter 2 induces senescence-associated mitochondrial dysfunction and suppresses progression of colorectal malignancies in vivo. Mol. Cancer Ther 2012, 11(11):2342-2351.
37. Halestrap A.P., Wilson M.C. The monocarboxylate transporter family - role and regulation. IUBMB Life 2012, 64(2):109-119.
38. Halestrap A.P. The monocarboxylate transporter family - structure and functional characterization. IUBMB Life 2012, 64(1):1-9.
39. Doyen J., Trastour C., Ettore F., Peyrottes I., Toussant N., Gal J., et al. Expression of the hypoxia-inducible monocarboxylate transporter MCT4 is increased in triple negative breast cancer and correlates independently with clinical outcome. Biochem. Biophys. Res. Commun 2014, 451(1):54-61.
40. Jiang P., Du W., Wang X., Mancuso A., Gao X., Wu M., et al. p53 regulates biosynthesis through direct inactivation of glucose-6-phosphate dehydrogenase. Nat. Cell Biol 2011, 13(3):310-316.
41. Possemato R., Marks K.M., Shaul Y.D., Pacold M.E., Kim D., Birsoy K., et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 2011, 476(7360):346-350.
42. Locasale J.W., Grassian A.R., Melman T., Lyssiotis C.A., Mattaini K.R., Bass A.J., et al. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet 2011, 43(9):869-874.
43. Wellen K.E., Thompson C.B. A two-way street: reciprocal regulation of metabolism and signalling. Nat. Rev. Mol. Cell Biol 2012, 13(4):270-276.
44. Ruan H.B., Singh J.P., Li M.D., Wu J., Yang X. Cracking the O-GlcNAc code in metabolism. Trends Endocrinol. Metab 2013, 24(6):301-309.
45. Dong C., Yuan T., Wu Y., Wang Y., Fan T.W., Miriyala S., et al. Loss of FBP1 by Snail-mediated repression provides metabolic advantages in basal-like breast cancer. Cancer Cell 2013, 23(3):316-331.
46. Li B., Qiu B., Lee D.S., Walton Z.E., Ochocki J.D., Mathew L.K., et al. Fructose-1,6-bisphosphatase opposes renal carcinoma progression. Nature 2014, 513(7517):251-255.
47. Park J.W., Kim S.C., Kim W.K., Hong J.P., Kim K.H., Yeo H.Y., et al. Expression of phosphoenolpyruvate carboxykinase linked to chemoradiation susceptibility of human colon cancer cells. BMC Cancer 2014, 14:160.
48. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324(5930):1029-1033.
49. Kamran M.Z., Patil P., Gude R.P. Role of STAT3 in cancer metastasis and translational advances. Biomed Res. Int 2013, 2013:421821.
50. Guo L., Chen C., Shi M., Wang F., Chen X., Diao D., et al. Stat3-coordinated Lin-28-let-7-HMGA2 and miR-200-ZEB1 circuits initiate and maintain oncostatin M-driven epithelial-mesenchymal transition. Oncogene 2013, 32(45):5272-5282.