The multikinase inhibitor Sorafenib enhances glycolysis and synergizes with glycolysis blockade for cancer cell killing

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Tesori, Valentina ^a   Piscaglia, Anna Chiara ^a   Samengo, Daniela ^a   Barba, Marta ^a   Bernardini, Camilla ^a   Scatena, Roberto ^a   Pontoglio, Alessandro ^a   Castellini, Laura ^b   Spelbrink, Johannes N ^c,d   Maulucci, Giuseppe ^a   Puglisi, Maria Ausiliatrice ^a   Pani, Giovambattista ^a   Gasbarrini, Antonio ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; DEOXYGLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NICOTINAMIDE; PROTEIN KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; SORAFENIB; TARGET OF RAPAMYCIN KINASE;

ANALOGS AND DERIVATIVES; ANIMAL; AUTOPHAGY; CELL RESPIRATION; CELL SURVIVAL; DRUG EFFECTS; ENERGY METABOLISM; GLYCOLYSIS; METABOLISM; MITOCHONDRION; RAT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CELL LINE, TUMOR; CELL RESPIRATION; CELL SURVIVAL; DEOXYGLUCOSE; ENERGY METABOLISM; GLYCOLYSIS; MITOCHONDRIA; NIACINAMIDE; PHENYLUREA COMPOUNDS; PROTEIN KINASE INHIBITORS; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84924943656     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09149     Document Type: Article

References (41)

1. Bonuccelli, G. et al. Ketones and lactate "fuel" tumor growth and metastasis: Evidence that epithelial cancer cells use oxidative mitochondrial metabolism. Cell Cycle 9, 3506-3514 (2010).
2. DeBerardinis, R. J., Lum, J. J., Hatzivassiliou, G.& Thompson, C. B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 7, 11-20 (2008).
3. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
4. WARBURG, O. On respiratory impairment in cancer cells. Science 124, 269-270 (1956).
5. Pani, G., Giannoni, E., Galeotti, T. & Chiarugi, P. Redox-based escape mechanism from death: the cancer lesson. Antioxid. Redox. Signal. 11, 2791-2806 (2009).
6. Diehn,M. et al.Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458, 780-783 (2009).
7. Liu, H., Savaraj, N., Priebe, W. & Lampidis, T. J. Hypoxia increases tumor cell sensitivity to glycolytic inhibitors: a strategy for solid tumor therapy (Model C). Biochem. Pharmacol. 64, 1745-1751 (2002).
8. Lin, Z. Y. & Chuang, W. L. Genes responsible for the characteristics of primary cultured invasive phenotype hepatocellular carcinoma cells. Biomed. Pharmacother. 66, 454-458 (2012).
9. Piscaglia, A. C. et al. Establishment of cancer cell lines from rat hepatocholangiocarcinoma and assessment of the role of granulocyte-colony stimulating factor and hepatocyte growth factor in their growth, motility and survival. J. Hepatol. 51, 77-92 (2009).
10. Roberts, L. R. Sorafenib in liver cancer - just the beginning. N. Engl. J. Med. 359, 420-422 (2008).
11. Hatzivassiliou, G. et al. RAF inhibitors prime wild-type RAF to activate theMAPK pathway and enhance growth. Nature 464, 431-435 (2010).
12. Wilhelm, S.M. et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res. 64, 7099-7109 (2004).
13. Nazarian, R. et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468, 973-977 (2010).
14. Will, Y. et al. Effect of the multitargeted tyrosine kinase inhibitors imatinib, dasatinib, sunitinib, and sorafenib on mitochondrial function in isolated rat heart mitochondria and H9c2 cells. Toxicol. Sci. 106, 153-161 (2008).
15. Chiou, J. F. et al. Sorafenib induces preferential apoptotic killing of a drug-and radio-resistant Hep G2 cells through a mitochondria-dependent oxidative stress mechanism. Cancer Biol. Ther. 8, 1904-1913 (2009).
16. Coriat, R. et al. Sorafenib-induced hepatocellular carcinoma cell death depends on reactive oxygen species production in vitro and in vivo. Mol. Cancer Ther. 11, 2284-2293 (2012).
17. Ulivi, P. et al. Role of RAF/MEK/ERK pathway, p-STAT-3 and Mcl-1 in sorafenib activity in human pancreatic cancer cell lines. J. Cell Physiol 220, 214-221 (2009).
18. Solit, D. B. et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 439, 358-362 (2006).
19. Zmijewski, J. W. et al. Exposure to hydrogen peroxide induces oxidation and activation of AMP-activated protein kinase. J. Biol. Chem. 285, 33154-33164 (2010).
20. Bull, V. H., Rajalingam, K. & Thiede, B. Sorafenib-induced mitochondrial complex I inactivation and cell death in human neuroblastoma cells. J. Proteome. Res. 11, 1609-1620 (2012).
21. Wanrooij, S., Goffart, S., Pohjoismaki, J. L., Yasukawa, T. & Spelbrink, J. N. Expression of catalytic mutants of the mtDNA helicase Twinkle and polymerase POLG causes distinct replication stalling phenotypes. Nucleic Acids Res. 35, 3238-3251 (2007).
22. Inoki, K., Zhu, T. & Guan, K. L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590 (2003).
23. Mizushima, N. & Komatsu, M. Autophagy: renovation of cells and tissues. Cell 147, 728-741 (2011).
24. Kimura, S., Noda, T. & Yoshimori, T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 3, 452-460 (2007).
25. Dang, C. V. Links between metabolism and cancer. Genes Dev. 26, 877-890 (2012).
26. Yagoda, N. et al. RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447, 864-868 (2007).
27. Mueckler, M. et al. Sequence and structure of a human glucose transporter. Science 229, 941-945 (1985).
28. Eto, K. et al. Cloning of a complete protein-coding sequence of human platelettype phosphofructokinase isozyme from pancreatic islet. Biochem. Biophys. Res. Commun. 198, 990-998 (1994).
29. Oliva, D., Cali, L., Feo, S. & Giallongo, A. Complete structure of the human gene encoding neuron-specific enolase. Genomics 10, 157-165 (1991).
30. Kurata, T., Oguri, T., Isobe, T., Ishioka, S. & Yamakido, M. Differential expression of facilitative glucose transporter (GLUT) genes in primary lung cancers and their liver metastases. Jpn. J. Cancer Res. 90, 1238-1243 (1999).
31. Moon, J. S. et al. Kruppel-like factor 4 (KLF4) activates the transcription of the gene for the platelet isoform of phosphofructokinase (PFKP) in breast cancer. J. Biol. Chem. 286, 23808-23816 (2011).
32. Selga, E.,Morales, C.,Noe, V., Peinado, M. A. &Ciudad, C. J. Role of caveolin 1, Ecadherin, Enolase 2 and PKCalpha on resistance to methotrexate in human HT29 colon cancer cells. BMC. Med. Genomics 1, 35 (2008).
33. Kaplon, J. et al. A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence. Nature 498, 109-112 (2013).
34. Schafer, Z. T. et al. Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 461, 109-113 (2009).
35. Choo, A. Y. et al.Glucose addiction of TSC null cells is caused by failed mTORC1-dependent balancing of metabolic demand with supply. Mol. Cell 38, 487-499 (2010).
36. Shackelford, D. B. et al. LKB1 inactivation dictates therapeutic response of nonsmall cell lung cancer to the metabolism drug phenformin. Cancer Cell 23, 143-158 (2013).
37. Birsoy, K. et al. Metabolic determinants of cancer cell sensitivity to glucose limitation and biguanides. Nature 508, 108-112 (2014).
38. Fumarola, C. et al. Effects of sorafenib on energy metabolism in breast cancer cells: role of AMPK-mTORC1 signaling. Breast Cancer Res. Treat. 141, 67-78 (2013).
39. McElroy, W. D. & DeLuca, M. A. Firefly and bacterial luminescence: basic science and applications. J. Appl. Biochem. 5, 197-209 (1983).
40. Pesta, D. & Gnaiger, E. High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol. Biol. 810, 25-58 (2012).
41. Reers, M., Smith, T.W. & Chen, L. B. J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480-4486 (1991).