Repressing malic enzyme 1 redirects glucose metabolism, unbalances the redox state, and attenuates migratory and invasive abilities in nasopharyngeal carcinoma cell lines

Chinese Journal of Cancer

Volumn 31, Issue 11, 2012, Pages 519-531

  Zheng, Fang Jing ^a   Ye, Hao Bin ^a,b   Wu, Man Si ^a   Lian, Yi Fan ^a   Qian, Chao Nan ^a   Zeng, Yi Xin ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Low glucose; Malic enzyme 1; NADPH; Nasopharyngeal carcinoma

Indexed keywords

CASPASE 3; FATTY ACID; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; LACTIC ACID; MALATE DEHYDROGENASE (DECARBOXYLATING); MALATE DEHYDROGENASE (DECARBOXYLATING) 1; PENTOSE PHOSPHATE; PHOSPHOGLUCONATE DEHYDROGENASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CELL INVASION; CELL PROTECTION; CELL STIMULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; ENZYME INHIBITION; FATTY ACID SYNTHESIS; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; MIGRATION INHIBITION; MITOCHONDRIAL MEMBRANE POTENTIAL; NASOPHARYNX CARCINOMA; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PENTOSE PHOSPHATE CYCLE; PHYSICAL TOLERANCE; WILD TYPE;

CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; GLUCOSE; GLYCOLYSIS; HUMANS; MALATE DEHYDROGENASE; NADP; NASOPHARYNGEAL NEOPLASMS; NEOPLASM INVASIVENESS; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; PENTOSE PHOSPHATE PATHWAY; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84870286932     PISSN: 1000467X     EISSN: 1944446X     Source Type: Journal    
DOI: 10.5732/cjc.012.10088     Document Type: Article

References (44)

1. Yu MC, Ho JH, Henderson BE, et al. Epidemiology of nasopharyngeal carcinoma in Malaysia and Hong Kong. Natl Cancer Inst Monogr, 1985,69: 203-207.
2. Yuan JM, Wang XL, Xiang YB, et al. Preserved foods in relation to risk of nasopharyngeal carcinoma in Shanghai, China. Int J Cancer, 2000,85: 358-363.
3. Hildesheim A, Levine PH. Etiology of nasopharyngeal carcinoma: a review. Epidemiol Rev, 1993,15: 466-485.
4. Bei JX, Li Y, Jia WH, et al. A genome-wide association study of nasopharyngeal carcinoma identifies three new susceptibility loci. Nat Genet, 2010,42: 599-603.
5. Feng BJ, Huang W, Shugart YY, et al. Genome-w ide scan for familial nasopharyngeal carcinoma reveals evidence of linkage to chromosome 4. Nat Genet, 2002,31: 395-399.
6. Jiang RC, Qin HD, Zeng MS, et al. A functional variant in the transcriptional regulatory region of gene LOC344967 cosegre- gates with disease phenotype in familial nasopharyngeal carcinoma. Cancer Res, 2006,66: 693-700.
7. Warburg O. Iron, the oxygen-ca rrier of respiration-fe rment. Science, 1925,61: 575-582.
8. Mashima T, Seimiya H, Tsuruo T. De novo fatty-ac id synthesis and related pathways as molecular targets for cancer therapy. Br J Cancer, 2009,100: 1369-1372.
9. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, et al. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab, 2008,7: 11-20.
10. Tomes L, Emberley E, Niu Y, et al. Necrosis and hypoxia in invasive breast carcinoma. Breast Cancer Res Treat, 2003,81: 61-69.
11. Deberardinis RJ, Sayed N, Ditsworth D, et al. Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev, 2008,18: 54-61.
12. Chang GG, Wang JK, Huang TM, et al. Purification and characterization of the cytosolic NADP (+)-de pendent malic enzyme from human breast cancer cell line. Eur J Biochem, 1991,202: 681-688.
13. Kam PL, Lin CC, Li JC, et al. High malic enzyme activity in tumor cells and its cross-re action with anti-pi geon liver malic enzyme serum. Mol Cell Biochem, 1988,79: 171-179.
14. DeBerardinis RJ, Mancuso A, Daikhin E, et al. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci U S A, 2007,104: 19345-19350.
15. Huo Y, Qiu WY, Pan Q, et al. Reactive oxygen species (ROS) are essential mediators in epidermal growth factor (EGF)- stimulated corneal epithelial cell proliferation, adhesion, migration, and wound healing. Exp Eye Res, 2009,89: 876-886.
16. Cheng M, Zaman G, Rawlinson SC, et al. Mechanical strain stimulates ROS cell proliferation through IGF-II and estrogen through IGF-I. J Bone Miner Res, 1999,14: 1742-1750.
17. Jallali N, Ridha H, Thrasivoulou C, et al. Vulnerability to ROS- induced cell death in ageing articular cartilage: the role of antioxidant enzyme activity. Osteoarthritis Cartilage, 2005,13: 614-622.
18. Kim JY, Park JH. ROS-de pendent caspase-9 activation in hypoxic cell death. FEBS Lett, 2003,549: 94-98.
19. Ward PS, Patel J, Wise DR, et al. The common feature of leukemia-as sociated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ke toglutarate to 2-hy droxy- glutarate. Cancer Cell, 2010,17: 225-234.
20. Miyashita N, Laurie-Ahlberg CC, Wilton AN, et al. Quantitative analysis of X chromosome effects on the activities of the glucose 6-ph osphate and 6-ph osphogluconate dehydrogenases of Drosophila melanogaster. Genetics, 1986,113: 321-335.
21. Dozin B, Rall JE, Nikodem VM. Tissue-specific control of rat malic enzyme activity and messenger RNA levels by a high carbohydrate diet. Proc Natl Acad Sci U S A, 1986,83: 4705-4709.
22. Giandomenico AR, Cerniglia GE, Biaglow JE, et al. The importance of sodium pyruvate in assessing damage produced by hydrogen peroxide. Free Radic Biol Med, 1997,23: 426-434.
23. Jones DP. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol, 2002,348: 93-112.
24. Krycer JR, Sharpe LJ, Luu W, et al. The Akt-SR EBP nexus: cell signaling meets lipid metabolism. Trends Endocrinol Metab, 2010,21: 268-276.
25. Robey RB, Hay N. Is Akt the Warburg kinase?-Akt-energy metabolism interactions and oncogenesis. Semin Cancer Biol, 2009,19: 25-31.
26. Rathmell JC, Fox CJ, Plas DR, et al. Akt-directed glucose metabolism can prevent Bax conformation change and promote growth factor-in dependent survival. Mol Cell Biol, 2003,23: 7315-7328.
27. Wang HQ, Altomare DA, Skele KL, et al. Positive feedback regulation between AKT activation and fatty acid synthase expression in ovarian carcinoma cells. Oncogene, 2005,24: 3574-3582.
28. Porstmann T, Griffiths B, Chung YL, et al. PKB/Akt induces transcription of enzymes involved in cholesterol and fatty acid biosynthesis via activation of SREBP. Oncogene, 2005,24: 6465-6481.
29. Batlle E, Sancho E, Franci C, et al. The transcription factor snail is a repressor of E-ca dherin gene expression in epithelial tumour cells. Nat Cell Biol, 2000,2: 84-89.
30. Zhou BP, Deng J, Xia W, et al. Dual regulation of Snail by GSK-3b eta-m ediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol, 2004,6: 931-940.
31. Hatzivassiliou G, Zhao F, Bauer DE, et al. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell, 2005,8: 311-321.
32. Elstrom RL, Bauer DE, Buzzai M, et al. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res, 2004,64: 3892-3899.
33. Brown LJ, Longacre MJ, Hasan NM, et al. Chronic reduction of the cytosolic or mitochondrial NAD(P)-malic enzyme does not affect insulin secretion in a rat insulinoma cell line. J Biol Chem, 2009,284: 35359-35367.
34. Martin R, Ibeas E, Carvalho-Tavares J, et al. Natural triterpenic diols promote apoptosis in astrocytoma cells through ROS-mediated mitochondrial depolarization and JNK activation. PLoS One, 2009,4: e5975.
35. Guan L, Han B, Li Z, et al. Sodium selenite induces apoptosis by ROS-m ediated endoplasmic reticulum stress and mito-chondrial dysfunction in human acute promyelocytic leukemia NB4 cells. Apoptosis, 2009,14: 218-225.
36. Rogalska A, Koceva-Chyla A, Jozwiak Z. Aclarubicin-in duced ROS generation and collapse of mitochondrial membrane potential in human cancer cell lines. Chem Biol Interact, 2008,176: 58-70.
37. Trachootham D, Zhou Y, Zhang H, et al. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell, 2006,10: 241-252.
38. Lin VC, Chou CH, Lin YC, et al. Osthole suppresses fatty acid synthase expression in HER2-overexpressing breast cancer cells through modulating Akt/mTOR pathway. J Agric Food Chem, 2010,58: 4786-4793.
39. Van de Sande T, Roskams T, Lerut E, et al. High-level expression of fatty acid synthase in human prostate cancer tissues is linked to activation and nuclear localization of Akt/ PKB. J Pathol, 2005,206: 214-219.
40. Van de Sande T, De Schrijver E, Heyns W, et al. Role of the phosphatidylinositol 3'-kinase/PTEN/Akt kinase pathway in the overexpression of fatty acid synthase in LNCaP prostate cancer cells. Cancer Res, 2002,62: 642-646.
41. Walenta S, Salameh A, Lyng H, et al. Correlation of high lactate levels in head and neck tumors with incidence of metastasis. Am J Pathol, 1997,150: 409-415.
42. Schwickert G, Walenta S, Sundfor K, et al. Correlation of high lactate levels in human cervical cancer with incidence of metastasis. Cancer Res, 1995,55: 4757-4759.
43. Martinez-Outschoorn UE, Prisco M, Ertel A, et al. Ketones and lactate increase cancer cell stemness, driving recurrence, metastasis and poor clinical outcome in breast cancer: achieving personalized medicine via Metabolo-Genomics. Cell Cycle, 2011,10: 1271-1286.
44. Naruse K, Yamada Y, Aoki S, et al. Lactate dehydrogenase is a prognostic indicator for prostate cancer patients with bone metastasis. Hinyokika Kiyo, 2007,53: 287-292.