Reduced methylation of PFKFB3 in cancer cells shunts glucose towards the pentose phosphate pathway

Nature Communications

Volumn 5, Issue , 2014, Pages

  Yamamoto, Takehiro ^a   Takano, Naoharu ^a,b   Ishiwata, Kyoko ^a,b   Ohmura, Mitsuyo ^a   Nagahata, Yoshiko ^a,b   Matsuura, Tomomi ^a,b   Kamata, Aki ^a   Sakamoto, Kyoko ^a   Nakanishi, Tsuyoshi ^a,c   Kubo, Akiko ^a,b   Hishiki, Takako ^a,b   Suematsu, Makoto ^a,b  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c SHIMADZU CORPORATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ARGININE; CARBON MONOXIDE; GLUCOSE; HAEM CONTAINING CYSTATHIONINE BETA SYNTHASE; PFKFB3 PROTEIN; PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 1; SYNTHETASE; UNCLASSIFIED DRUG;

BIOCHEMISTRY; CANCER; CARBON MONOXIDE; CYTOLOGY; ENVIRONMENTAL STRESS; FUNCTIONAL ROLE; GLUCOSE; INHIBITION; METABOLISM; METHYLATION; PHOSPHATE (ORGANIC); PHYSIOLOGY; PROTEIN; REACTION RATE; SIGNALING; TOLERANCE;

ALLOSTERISM; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CAPILLARY ELECTROPHORESIS; CELL PROLIFERATION ASSAY; CELL VIABILITY ASSAY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MODIFICATION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; GLYCOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MALE; MASS SPECTROMETRY; METABOLOMICS; NONHUMAN; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PROTEIN METHYLATION; SITE DIRECTED MUTAGENESIS; TUMOR XENOGRAFT; UBIQUITINATION; WESTERN BLOTTING;

CELL LINE, TUMOR; DOWN-REGULATION; GLUCOSE; GLYCOLYSIS; HEME OXYGENASE (DECYCLIZING); HUMANS; METHYLATION; NEOPLASMS; OXIDATIVE STRESS; PENTOSE PHOSPHATE PATHWAY; PHOSPHOFRUCTOKINASE-2;

EID: 84896509301     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4480     Document Type: Article

References (58)

1. Verma, A., Hirsch, D. J., Glatt, C. E., Ronnett, G. V. & Snyder, S. H. Carbon monoxide: a putative neural messenger. Science 259, 381-384 (1993). (Pubitemid 23055683)
2. Suematsu, M. et al. Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. J. Clin. Invest. 96, 2431-2437 (1995).
3. Ryter, S. W., Alam, J. & Choi, A. M. Haem oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86, 583-650 (2006).
4. Kajimura, M., Fukuda, R., Bateman, R. M., Yamamoto, T. & Suematsu, M. Interactions of multiple gas-transducing systems: hallmarks and uncertainties of CO, NO, and H2S gas biology. Antioxid. Redox Signal. 13, 157-192 (2010).
5. Hishiki, T. et al. Carbon monoxide: impact on remethylation/ transsulfuration metabolism and its pathophysiologic implications. J. Mol. Med. (Berl) 90, 245-254 (2012).
6. Nuhn, P. et al. Heme oxygenase-1 and its metabolites affect pancreatic tumor growth in vivo. Mol. Cancer 8, 37 (2009).
7. Frezza, C. et al. Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase. Nature 477, 225-228 (2011).
8. Tsai, J. R. et al. High expression of heme oxygenase-1 is associated with tumor invasiveness and poor clinical outcome in non-small cell lung cancer patients. Cell Oncol. (Dordr) 35, 461-471 (2012).
9. Lee, S. E. et al. Induction of heme oxygenase-1 inhibits cell death in crotonaldehyde-stimulated HepG2 cells via the PKC-d-p38-Nrf2 pathway. PLoS One 7, e41676 (2012).
10. Banerjee, P. et al. Haem oxygenase-1 promotes survival of renal cancer cells through modulation of apoptosis- and autophagy-regulating molecules. J. Biol. Chem. 287, 32113-32123 (2012).
11. Al-Owais, M. M. et al. Carbon monoxide mediates the anti-apoptotic effects of haem oxygenase-1 in medulloblastoma DAOY cells via K+ channel inhibition. J. Biol. Chem. 287, 24754-24764 (2012).
12. Shintani, T. et al. Cystathionine b-synthase as a carbon monoxide- sensitive regulator of bile excretion. Hepatology 49, 141-150 (2009).
13. Kabil, O. et al. Reversible heme-dependent regulation of human cystathionine b-synthase by a flavoprotein oxidoreductase. Biochemistry 50, 8261-8263 (2011).
14. Morikawa, T. et al. Hypoxic regulation of the cerebral microcirculation is mediated by a carbon monoxide-sensitive hydrogen sulfide pathway. Proc. Natl Acad. Sci. USA 109, 1293-1298 (2012).
15. Yamamoto, T., Takano, N., Ishiwata, K. & Suematsu, M. Carbon monoxide stimulates global protein methylation via its inhibitory action on cystathionine b-synthase. J. Clin. Biochem. Nutr. 48, 96-100 (2011).
16. Ge, Y., Jensen, T. L., Matherly, L. H. & Taub, J. W. Transcriptional regulation of the cystathionine-beta -synthase gene in Down syndrome and non-Down syndrome megakaryocytic leukaemia cell lines. Blood 101, 1551-1557 (2003). (Pubitemid 36182533)
17. Galbiatti, A. L. et al. Association between 11 genetic polymorphisms in folate-metabolising genes and head and neck cancer risk. Eur. J. Cancer 48, 1525-1531 (2012).
18. Semmler, A., Simon, M., Moskau, S. & Linnebank, M. Polymorphisms of methionine metabolism and susceptibility to meningioma formation: laboratory investigation. J. Neurosurg. 108, 999-1004 (2008). (Pubitemid 351656849)
19. Pufulete, M. et al. Folate status, genomic DNA hypomethylation, and risk of colorectal adenoma and cancer: a case control study. Gastroenterology 124, 1240-1248 (2003). (Pubitemid 36531800)
20. Warburg, O., Wind, F. & Negelein, E. The metabolism of tumours in the body. J. Gen. Physiol. 8, 519-530 (1927).
21. Riganti, C., Gazzano, E., Polimeni, M., Aldieri, E. & Ghigo, D. The pentose phosphate pathway: an antioxidant defence and a crossroad in tumour cell fate. Free Radic. Biol. Med. 53, 421-436 (2012).
22. Vaughn, A. E. & Deshmukh, M. Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat. Cell Biol. 10, 1477-1483 (2008).
23. Mor, I., Cheung, E. C. & Vousden, K. H. Control of glycolysis through regulation of PFK1: old friends and recent additions. Cold Spring Harb. Symp. Quant. Biol. 76, 211-216 (2011).
24. Yang, Y. & Bedford, M. T. Protein arginine methyltransferases and cancer. Nat. Rev. Cancer 13, 37-50 (2013).
25. Hori, R. et al. Gene transfection of H25A mutant heme oxygenase-1 protects cells against hydroperoxide-induced cytotoxicity. J. Biol. Chem. 277, 10712-10718 (2002). (Pubitemid 34968199)
26. Herrero-Mendez, A. et al. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/CCdh1. Nat. Cell Biol. 11, 747-752 (2009).
27. Conklin, K. A. Chemotherapy-associated oxidative stress: impact on chemotherapeutic effectiveness. Integr. Cancer Ther. 3, 294-300 (2004). (Pubitemid 39552423)
28. Bao, Y. et al. Energy management by enhanced glycolysis in G1 phase in human colon cancer cells in vivo and in vitro. Mol. Cancer Res. 11, 973-985 (2013).
29. Handa, K. et al. Phosphorescence-assisted microvascular O2 measurements reveal alterations of oxygen demand in human metastatic colon cancer in the liver of superimmunodeficient NOG mice. Adv. Exp. Med. Biol. 662, 423-429 (2010).
30. Kubo, A. et al. Semi-quantitative analyses of metabolic systems of human colon cancer metastatic xenografts in livers of superimmunodeficient NOG mice. Anal. Bioanal. Chem. 400, 1895-1904 (2011).
31. Wu, Y. C. et al. Hydrogen sulphide lowers proliferation and induces protective autophagy in colon epithelial cells. PLoS One 7, e37572 (2012).
32. Pei, Y., Wu, B., Cao, Q., Wu, L. & Yang, G. Hydrogen sulfide mediates the antisurvival effect of sulforaphane on human prostate cancer cells. Toxicol. Appl. Pharmacol. 257, 420-428 (2011).
33. Szabo, C. et al. Tumor-derived hydrogen sulfide, produced by cystathionine-bsynthase, stimulates bioenergetics, cell proliferation, and angiogenesis in colon cancer. Proc. Natl Acad. Sci. USA 110, 12474-12479 (2013).
34. Deutsch, J. C., Santhosh-Kumar, C. R. & Kolhouse, J. F. Glutathione oxidation in real time by thermospray liquid chromatography-mass spectrometry. J. Chromatogr. A. 862, 161-168 (1999). (Pubitemid 29497808)
35. Francoleon, N. E., Carrington, S. J. & Fukuto, J. M. The reaction of H2S with oxidized thiols: generation of persulfides and implications to H2S biology. Arch. Biochem. Biophys. 516, 146-153 (2011).
36. Okar, D. A. et al. PFK-2/FBPase-2: maker and breaker of the essential biofactor fructose-2,6-bisphosphate. Trends Biochem. Sci. 26, 30-35 (2001). (Pubitemid 32124707)
37. Chesney, J. et al. An inducible gene product for 6-phosphofructo-2-kinase with an AU-rich instability element: role in tumour cell glycolysis and the Warburg effect. Proc. Natl Acad. Sci. USA 96, 3047-3052 (1999). (Pubitemid 29148841)
38. Atsumi, T. et al. High expression of inducible 6-phosphofructo-2-kinase/ fructose-2,6-bis- phosphatase (iPFK-2; PFKFB3) in human cancers. Cancer Res. 62, 5881-5887 (2002). (Pubitemid 35204749)
39. Yalcin, A., Telang, S., Clem, B. & Chesney, J. Regulation of glucose metabolism by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatases in cancer. Exp. Mol. Pathol. 86, 174-179 (2009).
40. Bensaad, K. et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126, 107-120 (2006). (Pubitemid 44040989)
41. Yin, L., Kosugi, M. & Kufe, D. Inhibition of the MUC1-C oncoprotein induces multiple myeloma cell death by down-regulating TIGAR expression and depleting NADPH. Blood 119, 810-816 (2012).
42. Wanka, C., Steinbach, J. P. & Rieger, J. Tp53-induced glycolysis and apoptosis regulator (TIGAR) protects glioma cells from starvation-induced cell death by up-regulating respiration and improving cellular redox homeostasis. J. Biol. Chem. 287, 33436-33446 (2012).
43. Almeida, A., Moncada, S. & Bolaños, J. P. Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat. Cell Biol. 6, 45-51 (2004). (Pubitemid 38425729)
44. Sakakibara, R. et al. Characterization of a human placental fructose-6- phosphate, 2-kinase/fructose-2,6-bisphosphatase. J. Biochem. 122, 122-128 (1997). (Pubitemid 27346231)
45. Kim, S. G., Cavalier, M., El-Maghrabi, M. R. & Lee, Y. H. A direct substratesubstrate interaction found in the kinase domain of the bifunctional enzyme, 6- phosphofructo-2-kinase/fructose-2,6-bisphosphatase. J. Mol. Biol. 370, 14-26 (2007). (Pubitemid 46817564)
46. Seo, M., Kim, J. D., Neau, D., Sehgal, I. & Lee, Y. H. Structure-based development of small molecule PFKFB3 inhibitors: a framework for potential cancer therapeutic agents targeting the Warburg effect. PLoS One 6, e24179 (2011).
47. Clem, B. F. et al. Targeting 6-phosphofructo-2-kinase (PFKFB3) as a therapeutic strategy against cancer. Mol. Cancer Ther. 12, 1461-1470 (2013).
48. Suematsu, M. et al. Early midzonal oxidative stress preceding cell death in hypoperfused rat liver. Gastroenterology 103, 994-1001 (1992).
49. Sosa, V. et al. Oxidative stress and cancer: an overview. Ageing Res. Rev. 12, 376-390 (2013).
50. Trachootham, D., Alexandre, J. & Huang, P. Targeting cancer cells by ROSmediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov. 8, 579-591 (2009).
51. Nagano, O., Okazaki, S. & Saya, H. Redox regulation in stem-like cancer cells by CD44 variant isoforms. Oncogene 32, 5191-5198 (2013).
52. Tamada, M. et al. Modulation of glucose metabolism by CD44 contributes to antioxidant status and drug resistance in cancer cells. Cancer Res. 72, 1438-1448 (2012).
53. Ishimoto, T. et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumour growth. Cancer Cell 19, 387-400 (2011).
54. Nishida, M. et al. Hydrogen sulphide anion regulates redox signaling via electrophile sulfhydration. Nat. Chem. Biol. 8, 714-724 (2012).
55. Van Schaftingen, E., Lederer, B., Bartrons, R. & Hers, H. G. A kinetic study of pyrophosphate: fructose-6-phosphate phosphotransferase from potato tubers. Application to a microassay of fructose 2,6-bisphosphate. Eur. J. Biochem. 129, 191-195 (1982).
56. Kinoshita, A. et al. Roles of hemoglobin allostery in hypoxia-induced metabolic alterations in erythrocytes: simulation and its verification by metabolome analysis. J. Biol. Chem. 282, 10731-10741 (2007). (Pubitemid 47093422)
57. Ishii, I. et al. Cystathionine gamma-lyase-deficient mice require dietary cysteine to protect against acute lethal myopathy and oxidative injury. J. Biol. Chem. 285, 26358-26368 (2010).
58. Hattori, K. et al. Paradoxical ATP elevation in ischemic penumbra revealed by quantitative imaging mass spectrometry. Antioxid. Redox Signal. 13, 1157-1167 (2010).