In vitro and in vivo study of epigallocatechin-3-gallate-induced apoptosis in aerobic glycolytic hepatocellular carcinoma cells involving inhibition of phosphofructokinase activity

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Li, Sainan ^a   Wu, Liwei ^a   Feng, Jiao ^a   Li, Jingjing ^a   Liu, Tong ^a,b   Zhang, Rong ^a,b   Xu, Shizan ^a,c   Cheng, Keran ^a,c   Zhou, Yuqing ^a,c   Zhou, Shunfeng ^a,c   Kong, Rui ^a,c   Chen, Kan ^a   Wang, Fan ^a   Xia, Yujing ^a   Lu, Jie ^a   Zhou, Yingqun ^a   Dai, Weiqi ^a   Guo, Chuanyong ^a  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

^c MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; CATECHIN; EPIGALLOCATECHIN GALLATE; TUMOR PROTEIN;

AEROBIC METABOLISM; ANALOGS AND DERIVATIVES; APOPTOSIS; DRUG EFFECTS; ENZYMOLOGY; GLYCOLYSIS; HEP-G2 CELL LINE; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PATHOLOGY;

AEROBIOSIS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CATECHIN; GLYCOLYSIS; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; NEOPLASM PROTEINS; PHOSPHOFRUCTOKINASES;

EID: 84976574811     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28479     Document Type: Article

References (85)

1. Vander Heiden, M. G., Cantley, L. C. & Thompson, C. B. Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science (New York, N.Y.) 324, 1029-1033, doi: 10.1126/science.1160809 (2009).
2. Brahimi-Horn, M. C., Chiche, J. & Pouyssegur, J. Hypoxia signalling controls metabolic demand. Current opinion in cell biology 19, 223-229, doi: 10.1016/j.ceb.2007.02.003 (2007).
3. Warburg, O. On the origin of cancer cells. Science (New York, N.Y.) 123, 309-314 (1956).
4. Pouyssegur, J., Dayan, F. & Mazure, N. M. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441, 437-443, doi: 10.1038/nature04871 (2006).
5. Fischer, K. et al. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 109, 3812-3819, doi: 10.1182/blood-2006-07-035972 (2007).
6. Koukourakis, M. I., Giatromanolaki, A., Harris, A. L. & Sivridis, E. Comparison of metabolic pathways between cancer cells and stromal cells in colorectal carcinomas: A metabolic survival role for tumor-Associated stroma. Cancer research 66, 632-637, doi: 10.1158/0008-5472.can-05-3260 (2006).
7. Swietach, P., Vaughan-Jones, R. D. & Harris, A. L. Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer metastasis reviews 26, 299-310, doi: 10.1007/s10555-007-9064-0 (2007).
8. Al Hasawi, N., Alkandari, M. F. & Luqmani, Y. A. Phosphofructokinase: A mediator of glycolytic flux in cancer progression. Critical reviews in oncology/hematology 92, 312-321, doi: 10.1016/j.critrevonc.2014.05.007 (2014).
9. Sola-Penna, M., Da Silva, D., Coelho, W. S., Marinho-Carvalho, M. M. & Zancan, P. Regulation of mammalian muscle type 6-phosphofructo-1-kinase and its implication for the control of the metabolism. IUBMB life 62, 791-796, doi: 10.1002/iub.393 (2010).
10. Granchi, C. & Minutolo, F. Anticancer agents that counteract tumor glycolysis. ChemMedChem 7, 1318-1350, doi: 10.1002/cmdc.201200176 (2012).
11. Rathmell, J. C. et al. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factorindependent survival. Molecular and cellular biology 23, 7315-7328 (2003).
12. Moreno-Sanchez, R. et al. Phosphofructokinase type 1 kinetics, isoform expression, and gene polymorphisms in cancer cells. Journal of cellular biochemistry 113, 1692-1703, doi: 10.1002/jcb.24039 (2012).
13. Deng, H. et al. Phosphorylation of Bad at Thr-201 by JNK1 promotes glycolysis through activation of phosphofructokinase-1. The Journal of biological chemistry 283, 20754-20760, doi: 10.1074/jbc.M800024200 (2008).
14. Siddiqui, I. A. et al. Green tea polyphenol EGCG blunts androgen receptor function in prostate cancer. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 25, 1198-1207, doi: 10.1096/fj.10-167924 (2011).
15. Singh, T. & Katiyar, S. K. Green tea polyphenol, (-)-epigallocatechin-3-gallate, induces toxicity in human skin cancer cells by targeting beta-catenin signaling. Toxicology and applied pharmacology 273, 418-424, doi: 10.1016/j.taap.2013.09.021 (2013).
16. Zhou, D. H., Wang, X. & Feng, Q. EGCG enhances the efficacy of cisplatin by downregulating hsa-miR-98-5p in NSCLC A549 cells. Nutrition and cancer 66, 636-644, doi: 10.1080/01635581.2014.894101 (2014).
17. Jankun, J., Selman, S. H., Swiercz, R. & Skrzypczak-Jankun, E. Why drinking green tea could prevent cancer. Nature 387, 561, doi: 10.1038/42381 (1997).
18. Shimizu, M. et al. (-)-Epigallocatechin gallate and polyphenon E inhibit growth and activation of the epidermal growth factor receptor and human epidermal growth factor receptor-2 signaling pathways in human colon cancer cells. Clinical cancer research: An official journal of the American Association for Cancer Research 11, 2735-2746, doi: 10.1158/1078-0432.ccr-04-2014 (2005).
19. Shimizu, M. et al. EGCG inhibits activation of the insulin-like growth factor (IGF)/IGF-1 receptor axis in human hepatocellular carcinoma cells. Cancer letters 262, 10-18, doi: 10.1016/j.canlet.2007.11.026 (2008).
20. Garcia, V. et al. Galiellalactone induces cell cycle arrest and apoptosis through the ATM/ATR pathway in prostate cancer cells. Oncotarget, doi: 10.18632/oncotarget.6606 (2015).
21. Mukhtar, H. & Ahmad, N. Tea polyphenols: prevention of cancer and optimizing health. The American journal of clinical nutrition 71, 1698S-1702S; discussion 1703S-1694S (2000).
22. Yang, C. S., Maliakal, P. & Meng, X. Inhibition of carcinogenesis by tea. Annual review of pharmacology and toxicology 42, 25-54, doi: 10.1146/annurev.pharmtox.42.082101.154309 (2002).
23. Ahmad, N., Feyes, D. K., Nieminen, A. L., Agarwal, R. & Mukhtar, H. Green tea constituent epigallocatechin-3-gallate and induction of apoptosis and cell cycle arrest in human carcinoma cells. Journal of the National Cancer Institute 89, 1881-1886 (1997).
24. Khan, N., Afaq, F., Saleem, M., Ahmad, N. & Mukhtar, H. Targeting multiple signaling pathways by green tea polyphenol (-)-epigallocatechin-3-gallate. Cancer research 66, 2500-2505, doi: 10.1158/0008-5472.can-05-3636 (2006).
25. Singh, B. N., Shankar, S. & Srivastava, R. K. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochemical pharmacology 82, 1807-1821, doi: 10.1016/j.bcp.2011.07.093 (2011).
26. Zhou, Y. et al. Improving the Anticancer Efficacy of Laminin Receptor-Specific Therapeutic Ruthenium Nanoparticles (RuBBLoaded EGCG-RuNPs) via ROS-Dependent Apoptosis in SMMC-7721 Cells. ACS applied materials & interfaces, doi: 10.1021/acsami.5b02261 (2015).
27. Kuo, P. L. & Lin, C. C. Green tea constituent (-)-epigallocatechin-3-gallate inhibits Hep G2 cell proliferation and induces apoptosis through p53-dependent and Fas-mediated pathways. Journal of biomedical science 10, 219-227, doi: 68711 (2003).
28. Gupta, S., Hastak, K., Afaq, F., Ahmad, N. & Mukhtar, H. Essential role of caspases in epigallocatechin-3-gallate-mediated inhibition of nuclear factor kappa B and induction of apoptosis. Oncogene 23, 2507-2522, doi: 10.1038/sj.onc.1207353 (2004).
29. Givant-Horwitz, V., Davidson, B. & Reich, R. Laminin-induced signaling in tumor cells: The role of the M(r) 67, 000 laminin receptor. Cancer research 64, 3572-3579, doi: 10.1158/0008-5472.can-03-3424 (2004).
30. Adhami, V. M., Siddiqui, I. A., Ahmad, N., Gupta, S. & Mukhtar, H. Oral consumption of green tea polyphenols inhibits insulin-like growth factor-I-induced signaling in an autochthonous mouse model of prostate cancer. Cancer research 64, 8715-8722, doi: 10.1158/0008-5472.can-04-2840 (2004).
31. Lee, Y. K. et al. VEGF receptors on chronic lymphocytic leukemia (CLL) B cells interact with STAT 1 and 3: implication for apoptosis resistance. Leukemia 19, 513-523, doi: 10.1038/sj.leu.2403667 (2005).
32. Li, S. et al. Epigallocatechin-3-gallate attenuates apoptosis and autophagy in concanavalin A-induced hepatitis by inhibiting BNIP3. Drug design, development and therapy 10, 631-647, doi: 10.2147/dddt.s99420 (2016).
33. Zhang, X. F. et al. Overexpression of WWP1 promotes tumorigenesis and predicts unfavorable prognosis in patients with hepatocellular carcinoma. Oncotarget 6, 40920-40933, doi: 10.18632/oncotarget.5712 (2015).
34. Lu, Q. Y., Zhang, L., Yee, J. K., Go, V. W. & Lee, W. N. Metabolic Consequences of LDHA inhibition by Epigallocatechin Gallate and Oxamate in MIA PaCa-2 Pancreatic Cancer Cells. Metabolomics: Official journal of the Metabolomic Society 11, 71-80, doi: 10.1007/s11306-014-0672-8 (2015).
35. Gao, F. et al. Epigallocatechin gallate inhibits human tongue carcinoma cells via HK2mediated glycolysis. Oncology reports 33, 1533-1539, doi: 10.3892/or.2015.3727 (2015).
36. Costa Leite, T., Da Silva, D., Guimaraes Coelho, R., Zancan, P. & Sola-Penna, M. Lactate favours the dissociation of skeletal muscle 6-phosphofructo-1-kinase tetramers down-regulating the enzyme and muscle glycolysis. The Biochemical journal 408, 123-130, doi: 10.1042/bj20070687 (2007).
37. Spitz, G. A., Furtado, C. M., Sola-Penna, M. & Zancan, P. Acetylsalicylic acid and salicylic acid decrease tumor cell viability and glucose metabolism modulating 6-phosphofructo-1-kinase structure and activity. Biochemical pharmacology 77, 46-53, doi: 10.1016/j.bcp.2008.09.020 (2009).
38. Zancan, P., Marinho-Carvalho, M. M., Faber-Barata, J., Dellias, J. M. & Sola-Penna, M. ATP and fructose-2, 6-bisphosphate regulate skeletal muscle 6-phosphofructo-1-kinase by altering its quaternary structure. IUBMB life 60, 526-533, doi: 10.1002/iub.58 (2008).
39. Zancan, P., Rosas, A. O., Marcondes, M. C., Marinho-Carvalho, M. M. & Sola-Penna, M. Clotrimazole inhibits and modulates heterologous association of the key glycolytic enzyme 6-phosphofructo-1-kinase. Biochemical pharmacology 73, 1520-1527, doi: 10.1016/j.bcp.2007.01.018 (2007).
40. Zancan, P., Almeida, F. V., Faber-Barata, J., Dellias, J. M. & Sola-Penna, M. Fructose-2, 6-bisphosphate counteracts guanidinium chloride-, thermal-, and ATP-induced dissociation of skeletal muscle key glycolytic enzyme 6-phosphofructo-1-kinase: A structural mechanism for PFK allosteric regulation. Archives of biochemistry and biophysics 467, 275-282, doi: 10.1016/j.abb.2007.08.032 (2007).
41. Ahmad, N., Cheng, P. & Mukhtar, H. Cell cycle dysregulation by green tea polyphenol epigallocatechin-3-gallate. Biochemical and biophysical research communications 275, 328-334, doi: 10.1006/bbrc.2000.3297 (2000).
42. Pan, Y. et al. CUL4A facilitates hepatocarcinogenesis by promoting cell cycle progression and epithelial-mesenchymal transition. Scientific reports 5, 17006, doi: 10.1038/srep17006 (2015).
43. Staal, G. E., Kalff, A., Heesbeen, E. C., van Veelen, C. W. & Rijksen, G. Subunit composition, regulatory properties, and phosphorylation of phosphofructokinase from human gliomas. Cancer research 47, 5047-5051 (1987).
44. Yang, K. C. et al. Involvement of proapoptotic Bcl-2 family members in terbinafine-induced mitochondrial dysfunction and apoptosis in HL60 cells. Food and chemical toxicology: An international journal published for the British Industrial Biological Research Association 44, 214-226, doi: 10.1016/j.fct.2005.07.008 (2006).
45. Feldenberg, L. R., Thevananther, S., del Rio, M., de Leon, M. & Devarajan, P. Partial ATP depletion induces Fas-And caspasemediated apoptosis in MDCK cells. The American journal of physiology 276, F837-846 (1999).
46. Wu, C. H. et al. In vitro and in vivo study of phloretin-induced apoptosis in human liver cancer cells involving inhibition of type II glucose transporter. International journal of cancer 124, 2210-2219, doi: 10.1002/ijc.24189 (2009).
47. Kang, M. H. & Reynolds, C. P. Bcl-2 inhibitors: Targeting mitochondrial apoptotic pathways in cancer therapy. Clinical cancer research: An official journal of the American Association for Cancer Research 15, 1126-1132, doi: 10.1158/1078-0432.ccr-08-0144 (2009).
48. Youle, R. J. & Strasser, A. The BCL-2 protein family: opposing activities that mediate cell death. Nature reviews. Molecular cell biology 9, 47-59, doi: 10.1038/nrm2308 (2008).
49. Zha, J., Harada, H., Yang, E., Jockel, J. & Korsmeyer, S. J. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87, 619-628 (1996).
50. Shen, Y. C. et al. Activating oxidative phosphorylation by a pyruvate dehydrogenase kinase inhibitor overcomes sorafenib resistance of hepatocellular carcinoma. British journal of cancer 108, 72-81, doi: 10.1038/bjc.2012.559 (2013).
51. Dai, W. et al. By reducing hexokinase 2, resveratrol induces apoptosis in HCC cells addicted to aerobic glycolysis and inhibits tumor growth in mice. Oncotarget 6, 13703-13717, doi: 10.18632/oncotarget.3800 (2015).
52. Zhai, B. et al. Inhibition of Akt reverses the acquired resistance to sorafenib by switching protective autophagy to autophagic cell death in hepatocellular carcinoma. Molecular cancer therapeutics 13, 1589-1598, doi: 10.1158/1535-7163.mct-13-1043 (2014).
53. Yang, E. J. et al. EGCG attenuates autoimmune arthritis by inhibition of STAT3 and HIF-1alpha with Th17/Treg control. PloS one 9, e86062, doi: 10.1371/journal.pone.0086062 (2014).
54. Macheda, M. L., Rogers, S. & Best, J. D. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. Journal of cellular physiology 202, 654-662, doi: 10.1002/jcp.20166 (2005).
55. Board, M., Humm, S. & Newsholme, E. A. Maximum activities of key enzymes of glycolysis, glutaminolysis, pentose phosphate pathway and tricarboxylic acid cycle in normal, neoplastic and suppressed cells. The Biochemical journal 265, 503-509 (1990).
56. Shim, H. et al. c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proceedings of the National Academy of Sciences of the United States of America 94, 6658-6663 (1997).
57. Loiseau, A. M., Rousseau, G. G. & Hue, L. Fructose 2, 6-bisphosphate and the control of glycolysis by glucocorticoids and by other agents in rat hepatoma cells. Cancer research 45, 4263-4269 (1985).
58. Coelho, W. S., Costa, K. C. & Sola-Penna, M. Serotonin stimulates mouse skeletal muscle 6-phosphofructo-1-kinase through tyrosine-phosphorylation of the enzyme altering its intracellular localization. Molecular genetics and metabolism 92, 364-370, doi: 10.1016/j.ymgme.2007.07.010 (2007).
59. Mouton, V. et al. Heart 6-phosphofructo-2-kinase activation by insulin requires PKB (protein kinase B), but not SGK3 (serum-And glucocorticoid-induced protein kinase 3). The Biochemical journal 431, 267-275, doi: 10.1042/bj20101089 (2010).
60. Chesney, J. et al. Fructose-2, 6-bisphosphate synthesis by 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphatase 4 (PFKFB4) is required for the glycolytic response to hypoxia and tumor growth. Oncotarget 5, 6670-6686, doi: 10.18632/oncotarget.2213 (2014).
61. Domenech, E. et al. AMPK and PFKFB3 mediate glycolysis and survival in response to mitophagy during mitotic arrest. Nature cell biology 17, 1304-1316, doi: 10.1038/ncb3231 (2015).
62. Pan, Q. Z. et al. A nomogram for predicting the benefit of adjuvant cytokine-induced killer cell immunotherapy in patients with hepatocellular carcinoma. Scientific reports 5, 9202, doi: 10.1038/srep09202 (2015).
63. Zhou, D. et al. A monocyte/granulocyte to lymphocyte ratio predicts survival in patients with hepatocellular carcinoma. Scientific reports 5, 15263, doi: 10.1038/srep15263 (2015).
64. Jiang, H. et al. Genetic variants in de novo lipogenic pathway genes predict the prognosis of surgically-Treated hepatocellular carcinoma. Scientific reports 5, 9536, doi: 10.1038/srep09536 (2015).
65. Yu, D. et al. Suppression of CYP2C9 by microRNA hsa-miR-128-3p in human liver cells and association with hepatocellular carcinoma. Scientific reports 5, 8534, doi: 10.1038/srep08534 (2015).
66. Zeng, J. et al. Metabolomics Identifies Biomarker Pattern for Early Diagnosis of Hepatocellular Carcinoma: from Diethylnitrosamine Treated Rats to Patients. Scientific reports 5, 16101, doi: 10.1038/srep16101 (2015).
67. Zhang, W. et al. A weighted relative difference accumulation algorithm for dynamic metabolomics data: long-Term elevated bile acids are risk factors for hepatocellular carcinoma. Scientific reports 5, 8984, doi: 10.1038/srep08984 (2015).
68. Dai, W. et al. Anti-miR-197 inhibits migration in HCC cells by targeting KAI 1/CD82. Biochemical and biophysical research communications 446, 541-548, doi: 10.1016/j.bbrc.2014.03.006 (2014).
69. Cheng, P. et al. Ethyl pyruvate inhibits proliferation and induces apoptosis of hepatocellular carcinoma via regulation of the HMGB1-RAGE and AKT pathways. Biochemical and biophysical research communications 443, 1162-1168, doi: 10.1016/j. bbrc.2013.12.064 (2014).
70. Dai, W. et al. Genistein inhibits hepatocellular carcinoma cell migration by reversing the epithelial-mesenchymal transition: partial mediation by the transcription factor NFAT1. Molecular carcinogenesis 54, 301-311, doi: 10.1002/mc.22100 (2015).
71. Wang, F. et al. The synergistic in vitro and in vivo antitumor effect of combination therapy with salinomycin and 5-fluorouracil against hepatocellular carcinoma. PloS one 9, e97414, doi: 10.1371/journal.pone.0097414 (2014).
72. Zhu, R. et al. Diagnostic Performance of Des-gamma-carboxy Prothrombin for Hepatocellular Carcinoma: A Meta-Analysis. Gastroenterology research and practice 2014, 529314, doi: 10.1155/2014/529314 (2014).
73. Chen, K. et al. Inhibitive effects of 15-deoxy-Delta(12), (14)-prostaglandin J2 on hepatoma-cell proliferation through reactive oxygen species-mediated apoptosis. OncoTargets and therapy 8, 3585-3593, doi: 10.2147/ott.s92832 (2015).
74. Li, J. et al. Astaxanthin Inhibits Proliferation and Induces Apoptosis of Human Hepatocellular Carcinoma Cells via Inhibition of Nf-Kappab P65 and Wnt/Beta-Catenin in Vitro. Marine drugs 13, 6064-6081, doi: 10.3390/md13106064 (2015).
75. Morimoto, M. et al. Higher discontinuation and lower survival rates are likely in elderly Japanese patients with advanced hepatocellular carcinoma receiving sorafenib. Hepatology research: The official journal of the Japan Society of Hepatology 41, 296-302, doi: 10.1111/j.1872-034X.2011.00778.x (2011).
76. Roh, J. L., Park, J. Y., Kim, E. H., Jang, H. J. & Kwon, M. Activation of mitochondrial oxidation by PDK2 inhibition reverses cisplatin resistance in head and neck cancer. Cancer letters 371, 20-29, doi: 10.1016/j.canlet.2015.11.023 (2016).
77. Zhao, Y., Butler, E. B. & Tan, M. Targeting cellular metabolism to improve cancer therapeutics. Cell death & disease 4, e532, doi: 10.1038/cddis.2013.60 (2013).
78. Fiorini, R. N. et al. Short-Term administration of (-)-epigallocatechin gallate reduces hepatic steatosis and protects against warm hepatic ischemia/reperfusion injury in steatotic mice. Liver transplantation: official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society 11, 298-308, doi: 10.1002/lt.20348 (2005).
79. Lecumberri, E., Dupertuis, Y. M., Miralbell, R. & Pichard, C. Green tea polyphenol epigallocatechin-3-gallate (EGCG) as adjuvant in cancer therapy. Clinical nutrition (Edinburgh, Scotland) 32, 894-903, doi: 10.1016/j.clnu.2013.03.008 (2013).
80. Kemp, R. G. Phosphofructokinase from rabbit skeletal muscle. Methods in enzymology 42, 71-77 (1975).
81. Kuo, H. J., Malencik, D. A., Liou, R. S. & Anderson, S. R. Factors affecting the activation of rabbit muscle phosphofructokinase by actin. Biochemistry 25, 1278-1286 (1986).
82. Alves, G. G. et al. p-Nitrophenylphosphatase activity catalyzed by plasma membrane (Ca(2+) + Mg(2+)ATPase: correlation with structural changes modulated by glycerol and Ca(2+). Bioscience reports 21, 25-32 (2001).
83. Sola-Penna, M. et al. A radioassay for phosphofructokinase-1 activity in cell extracts and purified enzyme. Journal of biochemical and biophysical methods 50, 129-140 (2002).
84. Zancan, P. & Sola-Penna, M. Calcium influx: A possible role for insulin modulation of intracellular distribution and activity of 6-phosphofructo-1-kinase in human erythrocytes. Molecular genetics and metabolism 86, 392-400, doi: 10.1016/j.ymgme.2005.07.005 (2005).
85. Marinho-Carvalho, M. M., Zancan, P. & Sola-Penna, M. Modulation of 6-phosphofructo-1-kinase oligomeric equilibrium by calmodulin: formation of active dimers. Molecular genetics and metabolism 87, 253-261, doi: 10.1016/j.ymgme.2005.11.002 (2006).