Frequent alteration of the protein synthesis of enzymes for glucose metabolism in hepatocellular carcinomas

Journal of Gastroenterology

Volumn 49, Issue 9, 2014, Pages 1324-1332

  Shimizu, Takayuki ^a   Inoue, Ken ichi ^a   Hachiya, Hiroyuki ^a   Shibuya, Norisuke ^a   Shimoda, Mitsugi ^a   Kubota, Keiichi ^a  

^a DOKKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Aerobic glycolysis; HIF 1 ; NRF2; Pentose phosphate pathway; Succinate dehydrogenase

Indexed keywords

ALDOA PROTEIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOENZYME; MESSENGER RNA; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE A; SUCCINATE DEHYDROGENASE B; TRANSKETOLASE; UNCLASSIFIED DRUG; GLUCOSE; NFE2L2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CANCER PATIENT; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME SYNTHESIS; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HYPOXIA; LIVER CELL CARCINOMA; LYSIS; OXIDATIVE PHOSPHORYLATION; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STABILITY; RNA TRANSCRIPTION; WHOLE CELL; GENE EXPRESSION REGULATION; GENETICS; GLYCOLYSIS; LIVER TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CARCINOMA, HEPATOCELLULAR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; GLYCOLYSIS; HUMANS; LIVER NEOPLASMS; NF-E2-RELATED FACTOR 2; OXIDATIVE PHOSPHORYLATION; PENTOSE PHOSPHATE PATHWAY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84926617046     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-013-0895-x     Document Type: Article

References (46)

1. Warburg O. On the origin of cancer cells. Science. 1956;123: 309-14.
2. Weinhouse S. The warburg hypothesis fifty years later. Zeitschrift Fü r Krebsforschung Und Klinische Onkologie. 1976;87:115-26.
3. Fantin VR, St-Pierre J, Leder P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell. 2006;9:425-34.
4. Moreno-Sańchez R, Rodríguez-Enríquez S, Marıń-Hernańdez A, Saavedra E. Energy metabolism in tumor cells. FEBS J. 2007;274:1393-418.
5. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the warburg effect: The metabolic requirements of cell proliferation. Science 2009;324:1029-33.
6. Levine AJ, Puzio-Kuter AM. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science. 2010;330:1340-4.
7. Semela D, Dufour J. Angiogenesis and hepatocellular carcinoma. J Hepatol. 2004;41:864-80.
8. Khan MA, Combs CS, Brunt EM, Lowe VJ, Wolverson MK, Solomon H, et al. Positron emission tomography scanning in the evaluation of hepatocellular carcinoma. J Hepatol. 2000;32: 792-7.
9. Shiomi S, Nishiguchi S, Ishizu H, Iwata Y, Sasaki N, Tamori A, et al. Usefulness of positron emission tomography with fluorine- 18-fluorodeoxyglucose for predicting outcome in patients with hepatocellular carcinoma. Am J Gastroenterol. 2001;96:1877-80.
10. Hamaguchi T, Iizuka N, Tsunedomi R, Hamamoto Y, Miyamoto T, Iida M, et al. Glycolysis module activated by hypoxia-inducible factor 1a is related to the aggressive phenotype of hepatocellular carcinoma. Int J Oncol. 2008;33:725.
11. Daskalow K, Pfander D, Weichert W, Rohwer N, Thelen A, Neuhaus P, et al. Distinct temporospatial expression patterns of glycolysis-related proteins in human hepatocellular carcinoma. Histochem Cell Biol. 2009;132:21-31.
12. Kitamura K, Hatano E, Higashi T, Narita M, Seo S, Nakamoto Y, et al. Proliferative activity in hepatocellular carcinoma is closely correlated with glucose metabolism but not angiogenesis. J Hepatol. 2011;55:846-57.
13. Arocho A, Chen B, Ladanyi M, Pan Q. Validation of the 2-DeltaDeltaCt calculation as an alternate method of data analysis for quantitative PCR of BCR-ABL P210 transcripts. Diagn Mol Pathol. 2006;15:56-61.
14. Riganti C, Gazzano E, Polimeni M, Aldieri E, Ghigo D. The pentose phosphate pathway: an antioxidant defense and a crossroad in tumor cell fate. Free Radical Biol Med. 2012;53:421-36.
15. Gottlieb E, Tomlinson IP. Mitochondrial tumour suppressors: a genetic and biochemical update. Nat Rev Cancer. 2005;5:857-66.
16. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell. 2008;13:472-82.
17. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-a prolyl hydroxylase. Cancer Cell. 2005;7:77-85.
18. Fukuda R, Zhang H, Kim J, Shimoda L, Dang CV, Semenza GL. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell. 2007;129:111-22.
19. Bayley J, Devilee P. The warburg effect in 2012. Curr Opin Oncol. 2012;24:62-7.
20. Nath B, Szabo G. Hypoxia and hypoxia inducible factors: diverse roles in liver diseases. Hepatology. 2012;55:622-33.
21. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, et al. The expression and distribution of the hypoxiainducible factors HIF-1a and HIF-2a in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol. 2000;157:411-21.
22. Huang G, Yang L, Lu W. Expression of hypoxia-inducible factor 1a and vascular endothelial growth factor in hepatocellular carcinoma: impact on neovascularization and survival. World J Gastroenterol. 2005;11:1705-8.
23. Xie H, Song J, Liu K, Ji H, Shen H, Hu S, et al. The expression of hypoxia-inducible factor-1a in hepatitis B virus-related hepatocellular carcinoma: correlation with patients' prognosis and hepatitis B virus X protein. Dig Dis Sci. 2008;53:3225-33.
24. Bangoura G, Liu Z, Qian Q, Jiang C, Yang G, Jing S. Prognostic significance of HIF-2alpha/EPAS1 expression in hepatocellular carcinoma. World J Gastroenterol. 2007;13:3176.
25. Guichard C, Amaddeo G, Imbeaud S, Ladeiro Y, Pelletier L, Maad IB, et al. Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nat Genet. 2012;44:694-8.
26. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, et al. An Nrf2/small maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236:313-22.
27. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, et al. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet. 2003;35:238-45.
28. Kobayashi A, Kang M, Okawa H, Ohtsuji M, Zenke Y, Chiba T, et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell. 2004;24:7130-9.
29. Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell. 2012;22:66-79.
30. Singh A, Misra V, Thimmulappa RK, Lee H, Ames S, Hoque MO, et al. Dysfunctional KEAP1-NRF2 interaction in non-smallcell lung cancer. PLoS Medicine. 2006;3:e420.
31. Shibata T, Kokubu A, Gotoh M, Ojima H, Ohta T, Yamamoto M, et al. Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer. Gastroenterology. 2008;135: 1358-1368. e4.
32. Jiang T, Chen N, Zhao F, Wang X, Kong B, Zheng W, et al. High levels of Nrf2 determine chemoresistance in type II endometrial cancer. Cancer Res. 2010;70:5486-96.
33. Padmanabhan B, Tong KI, Ohta T, Nakamura Y, Scharlock M, Ohtsuji M, et al. Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol Cell. 2006;21:689-700.
34. Shibata T, Ohta T, Tong KI, Kokubu A, Odogawa R, Tsuta K, et al. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc Natl Acad Sci. 2008;105:13568-73.
35. Chen W, Sun Z, Wang X, Jiang T, Huang Z, Fang D, et al. Direct interaction between Nrf2 and p21 Cip1/WAF1 upregulates the Nrf2-mediated antioxidant response. Mol Cell. 2009;34:663-73.
36. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol. 2010;12:213-23.
37. Lau A, Wang X, Zhao F, Villeneuve NF, Wu T, Jiang T, et al. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol Cell. 2010;30:3275-85.
38. Wang R, An J, Ji F, Jiao H, Sun H, Zhou D. Hypermethylation of the Keap1 gene in human lung cancer cell lines and lung cancer tissues. Biochem Biophys Res Commun. 2008;373:151-4.
39. Zhang P, Singh A, Yegnasubramanian S, Esopi D, Kombairaju P, Bodas M, et al. Loss of kelch-like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol Cancer Ther. 2010;9:336-46.
40. Adam J, Hatipoglu E, O'Flaherty L, Ternette N, Sahgal N, Lockstone H, et al. Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: roles for fumarate in KEAP1 succination and Nrf2 signaling. Cancer Cell. 2011;20:524-37.
41. Yoo NJ, Kim HR, Kim YR, An CH, Lee SH. Somatic mutations of the KEAP1 gene in common solid cancers. Histopathology. 2012;60:943-52.
42. Inami Y, Waguri S, Sakamoto A, Kouno T, Nakada K, Hino O, et al. Persistent activation of Nrf2 through p62 in hepatocellular carcinoma cells. J Cell Biol. 2011;193:275-84.
43. Kinoshita M, Miyata M. Underexpression of mRNA in human hepatocellular carcinoma focusing on eight loci. Hepatology. 2002;36:433-8.
44. Castaldo G, Calcagno G, Sibillo R, Cuomo R, Nardone G, Castellano L, et al. Quantitative analysis of aldolase A mRNA in liver discriminates between hepatocellular carcinoma and cirrhosis. Clin Chem. 2000;46:901-6.
45. Ying H, Kimmelman AC, Lyssiotis CA, Hua S, Chu GC, Fletcher-Sananikone E, et al. Oncogenic kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell. 2012;149:656-70.
46. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646-74