Warburg effect increases steady-state ROS condition in cancer cells through decreasing their antioxidant capacities (Anticancer effects of 3-bromopyruvate through antagonizing Warburg effect)

Medical Hypotheses

Volumn 81, Issue 5, 2013, Pages 866-870

  El Sayed, Salah Mohamed ^a   Mahmoud, Ahmed Alamir ^a   El Sawy, Samer Ahmed ^a   Abdelaal, Esam Abdelrahim ^a   Fouad, Amira Murad ^a   Yousif, Reda Salah ^a   Hashim, Marwa Shaban ^a   Hemdan, Shima Badawy ^a   Kadry, Zainab Mahmoud ^a   Abdelmoaty, Mohamed Ahmed ^a   Gabr, Adel Gomaa ^b   Omran, Faten M ^a   Nabo, Manal Mohamed Helmy ^c,d   Ahmed, Nagwa Sayed ^a  

^a SOHAG UNIVERSITY   (Egypt)

^b ASSIUT UNIVERSITY   (Egypt)

^c Sohag University   (Egypt)

^d King Abdullah Medical City ^*  (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; BROMOPYRUVIC ACID; CITRIC ACID; GLUCOSE 6 PHOSPHATE ISOMERASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; HEXOKINASE; HEXOKINASE 11; HYALURONIC ACID; LACTIC ACID; MALIC ACID; MONOCARBOXYLATE TRANSPORTER; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; OXALOACETIC ACID; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; URONIC ACID;

ANTIOXIDANT ACTIVITY; ARTICLE; CANCER CELL; CITRIC ACID CYCLE; CYTOTOXICITY; DNA SYNTHESIS; GLUCOSE METABOLISM; GLYCOLYSIS; HEXOSE MONOPHOSPHATE SHUNT; HUMAN; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; STEADY STATE; TUMOR MICROENVIRONMENT; WARBURG EFFECT;

CITRIC ACID CYCLE; GLUCOSE-6-PHOSPHATASE; GLYCOLYSIS; HUMANS; LACTIC ACID; MODELS, BIOLOGICAL; NEOPLASMS; PYRUVATES; REACTIVE OXYGEN SPECIES;

EID: 84886802319     PISSN: 03069877     EISSN: 15322777     Source Type: Journal    
DOI: 10.1016/j.mehy.2013.08.024     Document Type: Article

References (45)

1. Warburg O. On the origin of cancer cells. Science 1956, 123(3191):309-314.
2. Xu R.H., Pelicano H., Zhou Y., Carew J.S., Feng L., Bhalla K.N., et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res 2005, 65(2):613-621.
3. Marín-Hernández A., Rodríguez-Enríquez S., Vital-González P.A., Flores-Rodríguez F.L., Macías-Silva M., Sosa-Garrocho M., et al. Determining and understanding the control of glycolysis in fast-growth tumor cells. Flux control by an over-expressed but strongly product-inhibited hexokinase. FEBS J 2006, 273(9):1975-1988.
4. Hirschhaeuser F., Sattler U.G., Mueller-Klieser W. Lactate: a metabolic key player in cancer. Cancer Res 2011, 71(22):6921-6925.
5. Gatenby R.A., Gillies R.J. Why do cancers have high aerobic glycolysis?. Nat Rev Cancer 2004, 4(11):891-899.
6. Shime H., Yabu M., Akazawa T., Kodama K., Matsumoto M., Seya T., et al. Tumorsecreted lactic acid promotes IL-23/IL-17 proinflammatory pathway. J Immunol 2008, 180(11):7175-7183.
7. Végran F., Boidot R., Michiels C., Sonveaux P., Feron O. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-κB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 2011, 71(7):2550-2560.
8. 2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem J 2009, 418(1):29-37.
9. Desagher S., Glowinski J., Prémont J. Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J Neurosci 1997, 17(23):9060-9067.
10. Shim H., Dolde C., Lewis B.C., Wu C.S., Dang G., Jungmann R.A., et al. c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proc Natl Acad Sci USA 1997, 94(13):6658-6663.
11. Colen C.B., Shen Y., Ghoddoussi F., Yu P., Francis T.B., Koch B.J., et al. Metabolic targeting of lactate efflux by malignant glioma inhibits invasiveness and induces necrosis: an in vivo study. Neoplasia 2011, 13(7):620-632.
12. El Sayed S.M. 3-Bromopyruvate antagonizes effects of lactate and pyruvate, synergizes with citrate and exerts novel anti-glioma effects. J Bioenerg Biomembr 2012, 44(1):61-79.
13. Garcia C.K., Goldstein J.L., Pathak R.K., Anderson R.G., Brown M.S. Molecular characterization of a membrane transporter for lactate, pyruvate, and other monocarboxylates: implications for the Cori cycle. Cell 1994, 76(5):865-873.
14. Behrend L., Henderson G., Zwacka R.M. Reactive oxygen species in oncogenic transformation. Biochem Soc Trans 2003, 31:1441-1444.
15. Vafa O., Wade M., Kern S., Beeche M., Pandita T.K., Hampton G.M., et al. C-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 2002, 9(5):1031-1044.
16. Semenza G.L. Tumor metabolism: cancer cells give and take lactate. J Clin Invest 2008, 118(12):3835-3837.
17. Puntel R.L., Roos D.H., Grotto D., Garcia S.C., Nogueira C.W., Rocha J.B. Antioxidant properties of Krebs cycle intermediates against malonate pro oxidant activity in vitro: a comparative study using the colorimetric method and HPLC analysis to determine malondialdehyde in rat brain homogenates. Life Sci 2007, 81(1):51-62.
18. Ashrafian H., Czibik G., Bellahcene M., Aksentijević D., Smith A.C., Mitchell S.J., et al. Fumarate is cardioprotective via activation of the Nrf2 antioxidant pathway. Cell Metab 2012, 15(3):361-371.
19. Yamaguchi M., Hatefi Y. Mitochondrial nicotinamide nucleotide transhydrogenase: NADPH binding increases and NADP binding decreases the acidity and susceptibility to modification of cysteine-893. Biochemistry 1989, 28(14):6050-6056.
20. Müller J.G., Bücheler U.S., Kayser K., Schirmer R.H., Werner D., Krauth Siegel R.L. Glutathione reductase in human and murine lung tumors: high levels of mRNA and enzymatic activity. Cell Mol Biol (Noisy-le-grand) 1993, 39(4):389-396.
21. El Sayed S.M., Abou El-Magd R.M., Shishido Y., Chung S.P., Sakai T., Watanabe H., et al. D-amino acid oxidase gene therapy sensitizes glioma cells to the antiglycolytic effect of 3-bromopyruvate. Cancer Gene Ther 2012, 19(1):1-18.
22. Gatenby R.A., Gawlinski E.T. The glycolytic phenotype in carcinogenesis and tumor invasion: insights through mathematical models. Cancer Res 2003, 63(14):3847-3854.
23. Gatenby R.A., Gawlinski E.T., Gmitro A.F., Kaylor B., Gillies R.J. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 2006, 66(10):5216-5223.
24. Stern R., Shuster S., Neudecker B.A., Formby B. Lactate stimulates fibroblast expression of hyaluronan and CD44: the Warburg effect revisited. Exp Cell Res 2002, 276(1):24-31.
25. Szatrowski T.P., Nathan C.F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 1991, 51(3):794-798.
26. Kawanishi S., Hiraku Y., Pinlaor S., Ma N. Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol Chem 2006, 387(4):365-372.
27. Toyokuni S., Okamoto K., Yodoi J., Hiai H. Persistent oxidative stress in cancer. FEBS Lett 1995, 358(1):1-3.
28. Lebedeva M.A., Eaton J.S., Shadel G.S. Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis. Biochim Biophys Acta 2009, 1787(5):328-334.
29. Cardone R.A., Casavola V., Reshkin S.J. The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat Rev Cancer 2005, 5(10):786-795.
30. Pani G., Galeotti T., Chiarugi P. Metastasis: cancer cell's escape from oxidative stress. Cancer Metastasis Rev 2010, 29(2):351-378. Review.
31. Robert K Murray, Daryl K Granner, Peter A, Mayes, Victor W Rodwell. Harper's illustrated biochemistry. 2003; (26th ed.), Overview of Metabolism (pp. 122-237). Lange Medical Books/McGraw-Hill Medical Publishing Division.
32. Mathupala S.P., Ko Y.H., Pedersen P.L. Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 2006, 25(34):4777-4786.
33. Slomiany M.G., Grass G.D., Robertson A.D., Yang X.Y., Maria B.L., Beeson C., et al. Hyaluronan, CD44, and emmprin regulate lactate efflux and membrane localization of monocarboxylate transporters in human breast carcinoma cells. Cancer Res 2009, 69(4):1293-1301.
34. Kakizaki I., Kojima K., Takagaki K., Endo M., Kannagi R., Ito M., et al. A novel mechanism for the inhibition of hyaluronan biosynthesis by 4-methylumbelliferone. J Biol Chem 2004, 279(32):33281-33329.
35. Richter U., Wicklein D., Geleff S., Schumacher U. The interaction between CD44 on tumour cells and hyaluronan under physiologic flow conditions: implications for metastasis formation. Histochem Cell Biol 2012, 137(5):687-695.
36. Ween M.P., Oehler M.K., Ricciardelli C. Role of Versican, Hyaluronan and CD44 in Ovarian Cancer Metastasis. Int J Mol Sci 2011, 12(2):1009-1029.
37. Hubbard C., McNamara J.T., Azumaya C., Patel M.S., Zimmer J. The hyaluronan synthase catalyzes the synthesis and membrane translocation of hyaluronan. J Mol Biol 2012, 418(1-2):21-31.
38. Watanabe H., Takehana K., Date M., Shinozaki T., Raz A. Tumor cell autocrine motility factor is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res 1996, 56(13):2960-2963.
39. Yasasever V., Dinçer M., Camlica H., Duranyildiz D., Dalay N. Evaluation of phosphohexose isomerase as a metastasis marker in breast cancer patients. Eur J Gynaecol Oncol 1997, 18(5):397-399.
40. Stubbs M., McSheehy P.M., Griffiths J.R., Bashford C.L. Causes and consequences of tumour acidity and implications for treatment. Mol Med Today 2000, 6(1):15-19. Review.
41. Ko Y.H., Pedersen P.L., Geschwind J.F. Glucose catabolism in the rabbit VX2 tumor model for liver cancer: characterization and targeting hexokinase. Cancer Lett 2001, 173(1):83-91.
42. Ganapathy-Kanniappan S., Geschwind J.F., Kunjithapatham R., Buijs M., Vossen J.A., Tchernyshyov I., et al. Glyceraldehyde-3- phosphate dehydrogenase (GAPDH) is pyruvylated during 3-bromopyruvate mediated cancer cell death. Anticancer Res 2009, 29(12):4909-4918.
43. Mulet C., Lederer F. Bromopyruvate as an affinity label for baker's yeast. flavocytochrome b2. Kinetic study of the inactivation reaction. Eur J Biochem 1977, 73(2):443-447.
44. El Sayed S.M., El-Magd R.M., Shishido Y., Yorita K., Chung S.P., Tran D.H., et al. D-Amino acid oxidase-induced oxidative stress, 3- bromopyruvate and citrate inhibit angiogenesis, exhibiting potent anticancer effects. J Bioenerg Biomembr 2012, 44(5):513-523.
45. Nakano A., Tsuji D., Miki H., Cui Q., El Sayed S.M., Ikegame A., et al. Glycolysis inhibition inactivates ABC transporters to restore drug sensitivity in malignant cells. PLoS One 2011, 6(11):e27222.