Twist promotes reprogramming of glucose metabolism in breast cancer cells through PI3K/AKT and p53 signaling pathways

Oncotarget

Volumn 6, Issue 28, 2015, Pages 25755-25769

  Yang, Li ^a   Hou, Yixuan ^a   Yuan, Jie ^b   Tang, Shifu ^a   Zhang, Hailong ^a   Zhu, Qing ^b   Du, Yan e ^a   Zhou, Mingli ^a   Wen, Siyang ^a   Xu, Liyun ^a   Tang, Xi ^a   Cui, Xiaojiang ^c   Liu, Manran ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^c CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Glucose metabolism; p53; PI3K AKT; Twist

Indexed keywords

BETA1 INTEGRIN; FOCAL ADHESION KINASE 1; GLUCOSE; LACTIC ACID; PROTEIN KINASE; PROTEIN P53; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR TWIST; ANTINEOPLASTIC AGENT; MTOR PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR; PTK2 PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TP53 PROTEIN, HUMAN; TWIST RELATED PROTEIN 1; TWIST1 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER CELL LINE; BREAST EPITHELIUM CELL; CANCER CELL; CARCINOGENICITY; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENERGY METABOLISM; EPITHELIAL MESENCHYMAL TRANSITION; G6PD GENE; GENE; GENE EXPRESSION; GLUCOSE INTAKE; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HYPOXIA; LDHA GENE; MITOCHONDRION; PHENOTYPE; PKM2 GENE; UPREGULATION; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL MOTION; DRUG EFFECTS; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR CELL LINE;

ANTIGENS, CD29; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; ENERGY METABOLISM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; HUMANS; LACTIC ACID; MITOCHONDRIA; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TOR SERINE-THREONINE KINASES; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53; TWIST-RELATED PROTEIN 1;

EID: 84944463194     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4697     Document Type: Article

References (54)

1. Warburg O. On the origin of cancer cells. Science. 1956; 123:309-314.
2. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer cell. 2008; 13:472-482.
3. Mayevsky A. Mitochondrial function and energy metabolism in cancer cells: past overview and future perspectives. Mitochondrion. 2009; 9:165-179.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
5. Ferreira LM. Cancer metabolism: the Warburg effect today. Experimental and molecular pathology. 2010; 89:372-380.
6. Bensinger SJ, Christofk HR. New aspects of the Warburg effect in cancer cell biology. Seminars in cell & developmental biology. 2012; 23:352-361.
7. Dang CV. Links between metabolism and cancer. Genes & development. 2012; 26:877-890.
8. Roberts DJ, Miyamoto S. Hexokinase II integrates energy metabolism and cellular protection: Akting on mitochondria and TORCing to autophagy. Cell death and differentiation. 2015; 22:248-257.
9. Yu Z, Zhao X, Huang L, Zhang T, Yang F, Xie L, Song S, Miao P, Zhao L, Sun X, Liu J, Huang G. Proviral insertion in murine lymphomas 2 (PIM2) oncogene phosphorylates pyruvate kinase M2 (PKM2) and promotes glycolysis in cancer cells. The Journal of biological chemistry. 2013; 288:35406-35416.
10. Allison SJ, Knight JR, Granchi C, Rani R, Minutolo F, Milner J, Phillips RM. Identification of LDH-A as a therapeutic target for cancer cell killing via (i) p53/NAD(H)- dependent and (ii) p53-independent pathways. Oncogenesis. 2014; 3:e102.
11. Xie H, Hanai J, Ren JG, Kats L, Burgess K, Bhargava P, Signoretti S, Billiard J, Duffy KJ, Grant A, Wang X, Lorkiewicz PK, Schatzman S, Bousamra M 2nd, Lane AN, Higashi RM, et al. Targeting lactate dehydrogenase-a inhibits tumorigenesis and tumor progression in mouse models of lung cancer and impacts tumor-initiating cells. Cell metabolism. 2014; 19:795-809.
12. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis?. Nature reviews Cancer. 2004; 4:891-899.
13. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annual review of cell and developmental biology. 2011; 27:441-464.
14. Porporato PE, Payen VL, Perez-Escuredo J, De Saedeleer CJ, Danhier P, Copetti T, Dhup S, Tardy M, Vazeille T, Bouzin C, Feron O, Michiels C, Gallez B, Sonveaux P. A mitochondrial switch promotes tumor metastasis. Cell reports. 2014; 8:754-766.
15. Tang S, Yang L, Tang X, Liu M. The role of oxidized ATM in the regulation of oxidative stress-induced energy metabolism reprogramming of CAFs. Cancer letters. 2014; 353:133-144.
16. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004; 117:927-939.
17. Eckert MA, Lwin TM, Chang AT, Kim J, Danis E, Ohno-Machado L, Yang J. Twist1-induced invadopodia formation promotes tumor metastasis. Cancer cell. 2011; 19:372-386.
18. Karreth F, Tuveson DA. Twist induces an epithelialmesenchymal transition to facilitate tumor metastasis. Cancer biology & therapy. 2004; 3:1058-1059.
19. Hu P, Yang J, Hou Y, Zhang H, Zeng Z, Zhao L, Yu T, Tang X, Tu G, Cui X, Liu M. LncRNA expression signatures of twist-induced epithelial-to-mesenchymal transition in MCF10A cells. Cellular signalling. 2014; 26:83-93.
20. Robey RB, Hay N. Is Akt the "Warburg kinase"?-Aktenergy metabolism interactions and oncogenesis. Seminars in cancer biology. 2009; 19:25-31.
21. Gottlieb E, Vousden KH. p53 regulation of metabolic pathways. Cold Spring Harb Perspect Biol. 2010; 2:a001040.
22. Sun Q, Chen X, Ma J, Peng H, Wang F, Zha X, Wang Y, Jing Y, Yang H, Chen R, Chang L, Zhang Y, Goto J, Onda H, Chen T, Wang MR, et al. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108:4129-4134.
23. Carraway H, Hidalgo M. New targets for therapy in breast cancer: mammalian target of rapamycin (mTOR) antagonists. Breast cancer research. 2004; 6:219-224.
24. Sarbassov DD, Ali SM, Sabatini DM. Growing roles for the mTOR pathway. Current opinion in cell biology. 2005; 17:596-603.
25. Jiang P, Du W, Wang X, Mancuso A, Gao X, Wu M, Yang X. p53 regulates biosynthesis through direct inactivation of glucose-6-phosphate dehydrogenase. Nature Cell Biology. 2011; 13:310-316.
26. Merlo GR, Basolo F, Fiore L, Duboc L, Hynes NE. p53-dependent and p53-independent activation of apoptosis in mammary epithelial cells reveals a survival function of EGF and insulin. The Journal of cell biology. 1995; 128:1185-1196.
27. Nieves-Neira W, Pommier Y. Apoptotic response to camptothecin and 7-hydroxystaurosporine (UCN-01) in the human breast cancer cell lines of the NCI Anticancer Drug Screen: multifactorial relationships with topoisomerase I, protein kinase C, Bcl-2, p53, MDM-2 and caspase pathways. International journal of cancer Journal international du cancer. 1999; 82:396-404.
28. Bartek J, Iggo R, Gannon J, Lane DP. Genetic and immunochemical analysis of mutant p53 in human breast cancer cell lines. Oncogene. 1990; 5:893-899.
29. Olovnikov IA, Kravchenko JE, Chumakov PM. Homeostatic functions of the p53 tumor suppressor: regulation of energy metabolism and antioxidant defense. Seminars in cancer biology. 2009; 19:32-41.
30. Korotchkina LG, Leontieva OV, Bukreeva EI, Demidenko ZN, Gudkov AV, Blagosklonny MV. The choice between p53-induced senescence and quiescence is determined in part by the mTOR pathway. Aging (Albany, NY). 2010; 2:344-352.
31. Lim ST, Mikolon D, Stupack DG, Schlaepfer DD. FERM control of FAK function: implications for cancer therapy. Cell cycle. 2008; 7:2306-2314.
32. Wu N, Luo J, Jiang B, Wang L, Wang S, Wang C, Fu C, Li J, Shi D. Marine bromophenol bis (2, 3-dibromo-4, 5-dihydroxy-phenyl)-methane inhibits the proliferation, migration, and invasion of hepatocellular carcinoma cells via modulating beta1-integrin/FAK signaling. Marine drugs. 2015; 13:1010-1025.
33. Chang TM, Hung WC. The homeobox transcription factor Prox1 inhibits proliferation of hepatocellular carcinoma cells by inducing p53-dependent senescence-like phenotype. Cancer biology & therapy. 2013; 14:222-229.
34. Mazurek S. Pyruvate kinase type M2: a key regulator of the metabolic budget system in tumor cells. The international journal of biochemistry & cell biology. 2011; 43:969-980.
35. Mazurek S, Boschek CB, Hugo F, Eigenbrodt E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Seminars in cancer biology. 2005; 15:300-308.
36. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, Cantley LC. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature. 2008; 452:230-233.
37. Christofk HR, Vander Heiden MG, Wu N, Asara JM, Cantley LC. Pyruvate kinase M2 is a phosphotyrosinebinding protein. Nature. 2008; 452:181-186.
38. Ferguson EC, Rathmell JC. New roles for pyruvate kinase M2: working out the Warburg effect. Trends in biochemical sciences. 2008; 33:359-362.
39. Xie H, Valera VA, Merino MJ, Amato AM, Signoretti S, Linehan WM, Sukhatme VP, Seth P. LDH-A inhibition, a therapeutic strategy for treatment of hereditary leiomyomatosis and renal cell cancer. Molecular cancer therapeutics. 2009; 8:626-635.
40. Le A, Cooper CR, Gouw AM, Dinavahi R, Maitra A, Deck LM, Royer RE, Vander Jagt DL, Semenza GL, Dang CV. Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107:2037-2042.
41. Sheng SL, Liu JJ, Dai YH, Sun XG, Xiong XP, Huang G. Knockdown of lactate dehydrogenase A suppresses tumor growth and metastasis of human hepatocellular carcinoma. The FEBS journal. 2012; 279:3898-3910.
42. Zhao YH, Zhou M, Liu H, Ding Y, Khong HT, Yu D, Fodstad O, Tan M. Upregulation of lactate dehydrogenase A by ErbB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene. 2009; 28:3689-3701.
43. Yang W, Zheng Y, Xia Y, Ji H, Chen X, Guo F, Lyssiotis CA, Aldape K, Cantley LC, Lu Z. ERK1/2- dependent phosphorylation and nuclear translocation of PKM2 promotes the Warburg effect. Nat Cell Biol. 2012; 14:1295-1304.
44. Wood T. Physiological functions of the pentose phosphate pathway. Cell biochemistry and function. 1986; 4:241-247.
45. Furuta E, Okuda H, Kobayashi A, Watabe K. Metabolic genes in cancer: their roles in tumor progression and clinical implications. Biochimica et biophysica acta. 2010; 1805:141-152.
46. Kuo W, Lin J, Tang TK. Human glucose-6-phosphate dehydrogenase (G6PD) gene transforms NIH 3T3 cells and induces tumors in nude mice. International journal of cancer Journal international du cancer. 2000; 85:857-864.
47. Li C, Li Y, He L, Agarwal AR, Zeng N, Cadenas E, Stiles BL. PI3K/AKT signaling regulates bioenergetics in immortalized hepatocytes. Free Radical Biology and Medicine. 2013; 60:29-40.
48. Schwartzenberg-Bar-Yoseph F, Armoni M, Karnieli E. The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression. Cancer research. 2004; 64:2627-2633.
49. Kawauchi K, Araki K, Tobiume K, Tanaka N. p53 regulates glucose metabolism through an IKK-NF-kappaB pathway and inhibits cell transformation. Nat Cell Biol. 2008; 10:611-618.
50. Maestro R, Tos APD, Hamamori Y, Krasnokutsky S, Sartorelli V, Kedes L, Doglioni C, Beach DH, Hannon GJ. twist is a potential oncogene that inhibits apoptosis. Genes & development. 1999; 13:2207-2217.
51. Piccinin S, Tonin E, Sessa S, Demontis S, Rossi S, Pecciarini L, Zanatta L, Pivetta F, Grizzo A, Sonego M, Rosano C, Dei Tos AP, Doglioni C, Maestro R. A "twist box" code of p53 inactivation: twist box: p53 interaction promotes p53 degradation. Cancer cell. 2012; 22:404-415.
52. Wang L, Hou Y, Sun Y, Zhao L, Tang X, Hu P, Yang J, Zeng Z, Yang G, Cui X, Liu M. c-Ski activates cancerassociated fibroblasts to regulate breast cancer cell invasion. Molecular oncology. 2013; 7:1116-1128.
53. Yang L, Liu X, Wu D, Zhang M, Ran G, Bi Y, Huang H. Growth inhibition and induction of apoptosis in SGC7901 human gastric cancer cells by evodiamine. Molecular medicine reports. 2014; 9:1147-1152.
54. Edmond V, Merdzhanova G, Gout S, Brambilla E, Gazzeri S, Eymin B. A new function of the splicing factor SRSF2 in the control of E2F1-mediated cell cycle progression in neuroendocrine lung tumors. Cell cycle. 2013; 12:1267-1278.