Phosphofructokinase: A mediator of glycolytic flux in cancer progression

Critical Reviews in Oncology/Hematology

Volumn 92, Issue 3, 2014, Pages 312-321

  Hasawi, Nada Al ^a   Alkandari, Mariam F ^a   Luqmani, Yunus A ^a  

^a KUWAIT UNIVERSITY   (Kuwait)

Author keywords

Aerobic glycolysis; Cancer; Fructose 1,6 bisphosphate; PFK

Indexed keywords

6 AMINONICOTINAMIDE; 6 PHOSPHOFRUCTOKINASE; ACETYLSALICYLIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM; CALMODULIN; CLOTRIMAZOLE; DEOXYGLUCOSE; ETOPOSIDE; HYPOXIA INDUCIBLE FACTOR; LACTIC ACID; LOCAL ANESTHETIC AGENT; LONIDAMINE; METFORMIN; NONSTEROID ANTIINFLAMMATORY AGENT; OXALIPLATIN; PACLITAXEL; PYRUVATE KINASE; PYRUVATE KINASE TYPE M2; RESVERATROL; SALICYLIC ACID; UNCLASSIFIED DRUG; CARRIER PROTEIN; ENZYME INHIBITOR; GLUCOSE; MEMBRANE PROTEIN; THYROID HORMONE; THYROID HORMONE-BINDING PROTEINS;

BLOOD BRAIN BARRIER; BREAST CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CITRIC ACID CYCLE; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; GLYCOLYSIS; HORMONAL REGULATION; HUMAN; HYPOXIA; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; LIVER DISEASE; LUNG CANCER; METASTASIS; NEUROTOXICITY; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PROSTATE CANCER; PROSTATE HYPERTROPHY; REVIEW; STOMACH CANCER; TRANSCRIPTION REGULATION; TUMOR INVASION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE COURSE; DRUG EFFECTS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY;

ANIMALS; CARRIER PROTEINS; DISEASE PROGRESSION; ENZYME ACTIVATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; GLYCOLYSIS; HUMANS; MEMBRANE PROTEINS; NEOPLASMS; PHOSPHOFRUCTOKINASES; THYROID HORMONES;

EID: 84912122526     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2014.05.007     Document Type: Review

References (96)

1. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
2. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
3. Laking G., Price P. 18-Fluorodeoxyglucose positron emission tomography (FDG-PET) and the staging of early lung cancer. Thorax 2001, 56 Suppl. 2:ii38-ii44.
4. Gambhir S.S. Molecular imaging of cancer with positron emission tomography. Nat Rev Cancer 2002, 2:683-693.
5. Mochiki E., Kuwano H., Katoh H., Asao T., Oriuchi N., Endo K. Evaluation of 18F-2-deoxy-2-fluoro-d-glucose positron emission tomography for gastric cancer. World J Surg 2004, 28:247-253.
6. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008, 30:393-402.
7. Shaw R.J. Glucose metabolism and cancer. Curr Opin Cell Bio 2006, 18:598-608.
8. Gatenby R.A., Gillies R.J. Why do cancers have high aerobic glycolysis?. Nat Rev Cancer 2004, 4:891-899.
9. Sonveaux P., Vegran F., Schroeder T., et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Investig 2008, 118:3930-3942.
10. Jose C., Bellance N., Rossignol R. Choosing between glycolysis and oxidative phosphorylation: a tumor's dilemma?. Biochim Biophys Acta 2011, 1807:552-561.
11. Moreno-Sanchez R., Rodriguez-Enriquez S., Marin-Hernandez A., Saavedra E. Energy metabolism in tumor cells. FEBS J 2007, 274:1393-1418.
12. Dang C.V., Hamaker M., Sun P., Le A., Gao P. Therapeutic targeting of cancer cell metabolism. J Mol Med (Berlin) 2011, 89:205-212.
13. Ramanathan A., Wang C., Schreiber S.L. Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements. Proc Natl Acad Sci USA 2005, 102:5992-5997.
14. Gordan J.D., Thompson C.B., Simon M.C. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 2007, 12:108-113.
15. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
16. Elstrom R.L., Bauer D.E., Buzzai M., et al. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 2004, 64:3892-3899.
17. Bensaad K., Tsuruta A., Selak M.A., et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006, 126:107-120.
18. Matoba S., Kang J.G., Patino W.D., et al. p53 regulates mitochondrial respiration. Science 2006, 312:1650-1653.
19. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003, 3:721-732.
20. Huang L.E. Carrot and stick: HIF-alpha engages c-Myc in hypoxic adaptation. Cell Death Differ 2008, 15:672-677.
21. Jiang B.H., Jiang G., Zheng J.Z., Lu Z., Hunter T., Vogt P.K. Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ 2001, 12:363-369.
22. Lopez-Lazaro M. HIF-1: hypoxia-inducible factor or dysoxia-inducible factor?. FASEB J 2006, 20:828-832.
23. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metabol 2008, 7:11-20.
24. Kim S.G., Manes N.P., El-Maghrabi M.R., Lee Y.H. Crystal structure of the hypoxia-inducible form of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (PFKFB3): a possible new target for cancer therapy. J Biol Chem 2006, 281:2939-2944.
25. Dang C.V., Kim J.W., Gao P., Yustein J. The interplay between MYC and HIF in cancer. Nat Rev Cancer 2008, 8:51-56.
26. McLean L.A., Roscoe J., Jorgensen N.K., Gorin F.A., Cala P.M. Malignant gliomas display altered pH regulation by NHE1 compared with nontransformed astrocytes. Am J Physiol Cell Physiol 2000, 278:C676-C688.
27. Williams A.C., Collard T.J., Paraskeva C. An acidic environment leads to p53 dependent induction of apoptosis in human adenoma and carcinoma cell lines: implications for clonal selection during colorectal carcinogenesis. Oncogene 1999, 18:3199-3204.
28. Gatenby R.A., Gawlinski E.T. A reaction-diffusion model of cancer invasion. Cancer Res 1996, 56:5745-5753.
29. Brizel D.M., Schroeder T., Scher R.L., et al. Elevated tumor lactate concentrations predict for an increased risk of metastases in head-and-neck cancer. Int J Radiat Oncol Biol Phys 2001, 51:349-353.
30. Boros L.G., Torday J.S., Lim S., Bassilian S., Cascante M., Lee W.N. Transforming growth factor beta2 promotes glucose carbon incorporation into nucleic acid ribose through the nonoxidative pentose cycle in lung epithelial carcinoma cells. Cancer Res 2000, 60:1183-1185.
31. Boren J., Cascante M., Marin S., et al. Gleevec (STI571) influences metabolic enzyme activities and glucose carbon flow toward nucleic acid and fatty acid synthesis in myeloid tumor cells. J Biol Chem 2001, 276:37747-37753.
32. Boros L.G., Bassilian S., Lim S., Lee W.N. Genistein inhibits nonoxidative ribose synthesis in MIA pancreatic adenocarcinoma cells: a new mechanism of controlling tumor growth. Pancreas 2001, 22:1-7.
33. Szeliga M., Obara-Michlewska M. Glutamine in neoplastic cells: focus on the expression and roles of glutaminases. Neurochem Int 2009, 55:71-75.
34. Lobo C., Ruiz-Bellido M.A., Aledo J.C., Marquez J., Nunez De Castro I., Alonso F.J. Inhibition of glutaminase expression by antisense mRNA decreases growth and tumourigenicity of tumour cells. Biochem J 2000, 348 Pt 2:257-261.
35. Zheng J. Energy metabolism of cancer: glycolysis versus oxidative phosphorylation (Review). Oncol Lett 2012, 4:1151-1157.
36. Macheda M.L., Rogers S., Best J.D. Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 2005, 202:654-662.
37. Semenza G.L. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J 2007, 405:1-9.
38. Tennant D.A., Duran R.V., Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010, 10:267-277.
39. Pelicano H., Martin D.S., Xu R.H., Huang P. Glycolysis inhibition for anticancer treatment. Oncogene 2006, 25:4633-4646.
40. Ganapathy-Kanniappan S., Vali M., Kunjithapatham R., et al. 3-bromopyruvate: a new targeted antiglycolytic agent and a promise for cancer therapy. Curr Pharm Biotechnol 2010, 11:510-517.
41. Di Cosimo S., Ferretti G., Papaldo P., Carlini P., Fabi A., Cognetti F. Lonidamine: efficacy and safety in clinical trials for the treatment of solid tumors. Drugs Today (Barc) 2003, 39:157-174.
42. Varshney R., Dwarakanath B., Jain V. Radiosensitization by 6-aminonicotinamide and 2-deoxy-d-glucose in human cancer cells. Int J Radiat Biol 2005, 81:397-408.
43. Ben Sahra I., Laurent K., Giuliano S., et al. Targeting cancer cell metabolism: the combination of metformin and 2-deoxyglucose induces p53-dependent apoptosis in prostate cancer cells. Cancer Res 2010, 70:2465-2475.
44. 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 2009, 86:174-179.
45. Jenkins C.M., Yang J., Sims H.F., Gross R.W. Reversible high affinity inhibition of phosphofructokinase-1 by acyl-CoA: a mechanism integrating glycolytic flux with lipid metabolism. J Biol Chem 2011, 286:11937-11950.
46. Zancan P., Almeida F.V., Faber-Barata J., Dellias J.M., Sola-Penna M. Fructose-2,6-bisphosphate counteracts guanidinium chloride-, thermal-, and ATP-induced dissociation of skeletal muscle key glycolytic enzyme 6-phosphofructo-1-kinase: a structural mechanism for PFK allosteric regulation. Arch Biochem Biophys 2007, 467:275-282.
47. Sola-Penna M., Da Silva D., Coelho W.S., Marinho-Carvalho M.M., Zancan P. Regulation of mammalian muscle type 6-phosphofructo-1-kinase and its implication for the control of the metabolism. Int Union Biochem Mol Biol Life 2010, 62:791-796.
48. Costa Leite T., Da Silva D., Guimaraes Coelho R., Zancan P., Sola-Penna M. Lactate favours the dissociation of skeletal muscle 6-phosphofructo-1-kinase tetramers down-regulating the enzyme and muscle glycolysis. Biochem J 2007, 408:123-130.
49. Zancan P., Marinho-Carvalho M.M., Faber-Barata J., Dellias J.M., Sola-Penna M. ATP and fructose-2,6-bisphosphate regulate skeletal muscle 6-phosphofructo-1-kinase by altering its quaternary structure. Int Union Biochem Mol Biol Life 2008, 60:526-533.
50. Marcondes M.C., Sola-Penna M., Zancan P. Clotrimazole potentiates the inhibitory effects of ATP on the key glycolytic enzyme 6-phosphofructo-1-kinase. Arch Biochem Biophys 2010, 497:62-67.
51. Marinho-Carvalho M.M., Costa-Mattos P.V., Spitz G.A., Zancan P., Sola-Penna M. Calmodulin upregulates skeletal muscle 6-phosphofructo-1-kinase reversing the inhibitory effects of allosteric modulators. Biochim Biophys Acta Mol Cell Biol Lipids 2009, 1794:1175-1180.
52. Coelho W.S., Costa K.C., Sola-Penna M. Serotonin stimulates mouse skeletal muscle 6-phosphofructo-1-kinase through tyrosine-phosphorylation of the enzyme altering its intracellular localization. Mol Genet Metab 2007, 92:364-370.
53. Gomes Alves G., Sola-Penna M. Epinephrine modulates cellular distribution of muscle phosphofructokinase. Mol Genet Metab 2003, 78:302-306.
54. Da Silva D., Zancan P., Coelho W.S., Gomez L.S., Sola-Penna M. Metformin reverses hexokinase and 6-phosphofructo-1-kinase inhibition in skeletal muscle, liver and adipose tissues from streptozotocin-induced diabetic mouse. Arch Biochem Biophy 2012, 496:53-60.
55. Real-Hohn A., Zancan P., Da Silva D., et al. Filamentous actin and its associated binding proteins are the stimulatory site for 6-phosphofructo-1-kinase association within the membrane of human erythrocytes. Biochimie 2010, 92:538-544.
56. Zancan P., Sola-Penna M. Calcium influx: a possible role for insulin modulation of intracellular distribution and activity of 6-phosphofructo-1-kinase in human erythrocytes. Mol Genet Metab 2005, 86:392-400.
57. Zancan P., Sola-Penna M. Regulation of human erythrocyte metabolism by insulin: cellular distribution of 6-phosphofructo-1-kinase and its implication for red blood cell function. Mol Genet Metab 2005, 86:401-411.
58. Silva A.P., Alves G.G., Araujo A.H., Sola-Penna M. Effects of insulin and actin on phosphofructokinase activity and cellular distribution in skeletal muscle. Anais da Academia Brasileira de Ciências 2004, 76:541-548.
59. Marinho-Carvalho M.M., Zancan P., Sola-Penna M. Modulation of 6-phosphofructo-1-kinase oligomeric equilibrium by calmodulin: formation of active dimers. Mol Genet Metab 2006, 87:253-261.
60. Okar D.A., Manzano A., Navarro-Sabate A., Riera L., Bartrons R., Lange A.J. PFK-2/FBPase-2: maker and breaker of the essential biofactor fructose-2,6-bisphosphate. Trends Biochem Sci 2001, 26:30-35.
61. Rider M.H., Bertrand L., Vertommen D., Michels P.A., Rousseau G.G., Hue L. 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem J 2004, 381:561-579.
62. Moon J.S., Kim H.E., Koh E., 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 2011, 286:23808-23816.
63. Zhao L.F., Iwasaki Y., Nishiyama M., et al. Liver X receptor alpha is involved in the transcriptional regulation of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase gene. Diabetes 2012, 61:1062-1071.
64. Novellasdemunt L., Tato I., Navarro-Sabate A., et al. Akt-dependent activation of the heart 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (PFKFB2) isoenzyme by amino acids. J Biol Chem 2013, 288:10640-10651.
65. Coelho R.G., Calaca Ide C., Celestrini Dde M., Correia A.H., Costa M.A., Sola-Penna M. Clotrimazole disrupts glycolysis in human breast cancer without affecting non-tumoral tissues. Mol Genet Metab 2012, 103:394-398.
66. Zancan P., Rosas A.O., Marcondes M.C., Marinho-Carvalho M.M., Sola-Penna M. Clotrimazole inhibits and modulates heterologous association of the key glycolytic enzyme 6-phosphofructo-1-kinase. Biochem Pharmacol 2007, 73:1520-1527.
67. Spitz G.A., Furtado C.M., Sola-Penna M., Zancan P. Acetylsalicylic acid and salicylic acid decrease tumor cell viability and glucose metabolism modulating 6-phosphofructo-1-kinase structure and activity. Biochem Pharmacol 2009, 77:46-53.
68. Kirsh V.A., Kreiger N., Cotterchio M., Sloan M., Theis B. Nonsteroidal antiinflammatory drug use and breast cancer risk: subgroup findings. Am J Epidemiol 2007, 166:709-716.
69. Brasky T.M., Bonner M.R., Moysich K.B., et al. Non-steroidal anti-inflammatory drugs (NSAIDs) and breast cancer risk: differences by molecular subtype. Cancer Causes Contr 2010, 22:965-975.
70. Zhao Y.S., Zhu S., Li X.W., et al. Association between NSAIDs use and breast cancer risk: a systematic review and meta-analysis. Breast Cancer Res Treat 2009, 117:141-150.
71. Kundu J.K., Surh Y.J. Cancer chemopreventive and therapeutic potential of resveratrol: mechanistic perspectives. Cancer Lett 2008, 269:243-261.
72. Fulda S., Debatin K.M. Sensitization for anticancer drug-induced apoptosis by the chemopreventive agent resveratrol. Oncogene 2004, 23:6702-6711.
73. Kueck A., Opipari A.W., Griffith K.A., et al. Resveratrol inhibits glucose metabolism in human ovarian cancer cells. Gynecol Oncol 2007, 107:450-457.
74. Deng H., Yu F., Chen J., Zhao Y., Xiang J., Lin A. Phosphorylation of Bad at Thr-201 by JNK1 promotes glycolysis through activation of phosphofructokinase-1. J Biol Chem 2008, 283:20754-20760.
75. Gomez L.S., Zancan P., Marcondes M.C., et al. Resveratrol decreases breast cancer cell viability and glucose metabolism by inhibiting 6-phosphofructo-1-kinase. Biochimie 2013, 95:1336-1343.
76. Schwartz D., Beitner R. Detachment of the glycolytic enzymes, phosphofructokinase and aldolase, from cytoskeleton of melanoma cells, induced by local anesthetics. Mol Genet Metab 2000, 69:159-164.
77. Glass-Marmor L., Beitner R. Taxol (paclitaxel) induces a detachment of phosphofructokinase from cytoskeleton of melanoma cells and decreases the levels of glucose 1,6-bisphosphate, fructose 1,6-bisphosphate and ATP. Eur J Pharmacol 1999, 370:195-199.
78. Wu C., Khan S.A., Peng L.J., Lange A.J. Roles for fructose-2,6-bisphosphate in the control of fuel metabolism: beyond its allosteric effects on glycolytic and gluconeogenic enzymes. Adv Enzyme Regul 2006, 46:72-88.
79. Okar D.A., Wu C., Lange A.J. Regulation of the regulatory enzyme, 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase. Adv Enzyme Regul 2004, 44:123-154.
80. Hue L., Beauloye C., Marsin A.S., Bertrand L., Horman S., Rider M.H. Insulin and ischemia stimulate glycolysis by acting on the same targets through different and opposing signaling pathways. J Mol Cell Cardiol 2002, 34:1091-1097.
81. Wang Q., Donthi R.V., Wang J., et al. Cardiac phosphatase-deficient 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase increases glycolysis, hypertrophy, and myocyte resistance to hypoxia. Am J Physiol Heart Circul Physiol 2008, 294:H2889-H2897.
82. Atsumi T., Chesney J., Metz C., et al. High expression of inducible 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (iPFK-2; PFKFB3) in human cancers. Cancer Res 2002, 62:5881-5887.
83. Marsin A.S., Bouzin C., Bertrand L., Hue L. The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. J Biol Chem 2002, 277:30778-30783.
84. Minchenko A., Leshchinsky I., Opentanova I., et al. Hypoxia-inducible factor-1-mediated expression of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) gene. Its possible role in the Warburg effect. J Biol Chem 2002, 277:6183-6187.
85. Telang S., Yalcin A., Clem A.L., et al. Ras transformation requires metabolic control by 6-phosphofructo-2-kinase. Oncogene 2006, 25:7225-7234.
86. Calvo M.N., Bartrons R., Castano E., Perales J.C., Navarro-Sabate A., Manzano A. PFKFB3 gene silencing decreases glycolysis, induces cell-cycle delay and inhibits anchorage-independent growth in HeLa cells. FEBS Lett 2006, 580:3308-3314.
87. Minchenko O., Opentanova I., Caro J. Hypoxic regulation of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase gene family (PFKFB-1-4) expression in vivo. FEBS Lett 2003, 554:264-270.
88. Clem B., Telang S., Clem A., et al. Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth. Mol Cancer Therapeut 2008, 7:110-120.
89. Mazurek S., Boschek C.B., Hugo F., Eigenbrodt E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Semin Cancer Biol 2005, 15:300-308.
90. Christofk H.R., Vander Heiden M.G., Harris M.H., et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230-233.
91. Bluemlein K., Gruning N.M., Feichtinger R.G., Lehrach H., Kofler B., Ralser M. No evidence for a shift in pyruvate kinase PKM1 to PKM2 expression during tumorigenesis. Oncotarget 2010, 2:393-400.
92. Lencioni R. Loco-regional treatment of hepatocellular carcinoma. Hepatology 2010, 52:762-773.
93. Vali M., Vossen J.A., Buijs M., et al. Targeting of VX2 rabbit liver tumor by selective delivery of 3-bromopyruvate: a biodistribution and survival study. J Pharmacol Exp Therapeut 2008, 327:32-37.
94. Pedersen P.L. 3-Bromopyruvate (3BP) a fast acting, promising, powerful, specific, and effective "small molecule" anti-cancer agent taken from labside to bedside: introduction to a special issue. J Bioenerg Biomembr 2012, 44:1-6.
95. Birsoy K., Wang T., Possemato R., et al. MCT1-mediated transport of a toxic molecule is an effective strategy for targeting glycolytic tumors. Nat Genet 2013, 45:104-108.
96. Beneteau M., Zunino B., Jacquin M.A., et al. Combination of glycolysis inhibition with chemotherapy results in an antitumor immune response. Proc Natl Acad Sci USA 2012, 109:20071-20076.