PFKFB3 activation in cancer cells by the p38/MK2 pathway in response to stress stimuli

Biochemical Journal

Volumn 452, Issue 3, 2013, Pages 531-543

  Novellasdemunt, Laura ^a   Bultot, Laurent ^b   Manzano, Anna ^a   Ventura, Francesc ^a   Rosa, Jose Luis ^a   Vertommen, Didier ^b   Rider, Mark H ^b   Navarro Sabate, Aurea ^a   Bartrons, Ramon ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

6 phosphofructo 2 kinase fructose 2, 6 biphosphatase 3 (PFKFB3); Gene regulation; Glycolysis; Metabolism; Mitogen activated protein kinase activated protein kinase 2 (MK2); P38; Stress stimulus

Indexed keywords

6 PHOSPHOFRUCTO 2 KINASE; 6 PHOSPHOFRUCTOKINASE; ANISOMYCIN; HYDROGEN PEROXIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE ACTIVATED PROTEIN KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PFKFB3 PROTEIN; SERUM RESPONSE FACTOR; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL PROLIFERATION; CELL STRESS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE DELETION; GENETIC TRANSFECTION; GLYCOLYSIS; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SERUM RESPONSIVE ELEMENT; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; ENZYME ACTIVATION; GLYCOLYSIS; HELA CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; NEOPLASMS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOFRUCTOKINASE-2; PHOSPHORYLATION; PROTEIN BINDING;

EID: 84878404837     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121886     Document Type: Article

References (42)

1. Warburg, O. (1956) On the origin of cancer cells. Science 123, 309-314
2. Van Schaftingen, E. (1987) Fructose 2,6-bisphosphate. Adv. Enzymol. Relat. Areas Mol. Biol. 59, 315-395
3. Rider, M. H., Bertrand, L., Vertommen, D., Michels, P. A., Rousseau, G. G. and Hue, L. (2004) 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem. J. 381, 561-579 (Pubitemid 39120464)
4. Chesney, J., Mitchell, R., Benigni, F., Bacher, M., Spiegel, L., Al-Abed, Y., Han, J. H., Metz, C. and Bucala, R. (1999) An inducible gene product for 6-phosphofructo-2-kinase with an AU-rich instability element: role in tumor cell glycolysis and the Warburg effect. Proc. Natl. Acad. Sci. U.S.A. 96, 3047-3052 (Pubitemid 29148841)
5. Riera, L., Manzano, A., Navarro-Sabate, A., Perales, J. C. and Bartrons, R. (2002) Insulin induces PFKFB3 gene expression in HT29 human colon adenocarcinoma cells. Biochim. Biophys. Acta 1589, 89-92 (Pubitemid 34463076)
6. Bando, H., Atsumi, T., Nishio, T., Niwa, H., Mishima, S., Shimizu, C., Yoshioka, N., Bucala, R. and Koike, T. (2005) Phosphorylation of the 6-phosphofructo-2-kinase/fructose 2,6-bisphosphatase/PFKFB3 family of glycolytic regulators in human cancer. Clin. Cancer Res. 11, 5784-5792 (Pubitemid 41170304)
7. Obach, M., Navarro-Sabate, A., Caro, J., Kong, X., Duran, J., Gomez, M., Perales, J. C., Ventura, F., Rosa, J. L. and Bartrons, R. (2004) 6-Phosphofructo-2-kinase (pfkfb3) gene promoter contains hypoxia-inducible factor-1 binding sites necessary for transactivation in response to hypoxia. J. Biol. Chem. 279, 53562-53570 (Pubitemid 40051863)
8. Minchenko, O. H., Ochiai, A., Opentanova, I. L., Ogura, T., Minchenko, D. O., Caro, J., Komisarenko, S. V. and Esumi, H. (2005) Overexpression of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-4 in the human breast and colon malignant tumors. Biochimie 87, 1005-1010 (Pubitemid 41377160)
9. Moon, J. S., Jin, W. J., Kwak, J. H., Kim, H. J., Yun, M. J., Kim, J. W., Park, S. W. and Kim, K. S. (2011) Androgen stimulates glycolysis for de novo lipid synthesis by increasing the activities of hexokinase 2 and 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 2 in prostate cancer cells. Biochem. J. 433, 225-233
10. Sakakibara, R., Uemura, M., Hirata, T., Okamura, N. and Kato, M. (1997) Human placental fructose-6-phosphate,2-kinase/fructose-2,6-bisphosphatase: its isozymic form, expression and characterization. Biosci. Biotechnol. Biochem. 61, 1949-1952 (Pubitemid 127471802)
11. Manzano, A., Rosa, J. L., Ventura, F., Perez, J. X., Nadal, M., Estivill, X., Ambrosio, S., Gil, J. and Bartrons, R. (1998) Molecular cloning, expression, and chromosomal localization of a ubiquitously expressed human 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphatase gene (PFKFB3) . Cytogenet. Cell Genet. 83, 214-217 (Pubitemid 29112740)
12. Duran, J., Obach, M., Navarro-Sabate, A., Manzano, A., Gomez, M., Rosa, J. L., Ventura, F., Perales, J. C. and Bartrons, R. (2009) Pfkfb3 is transcriptionally upregulated in diabetic mouse liver through proliferative signals. FEBS J. 276, 4555-4568
13. Yalcin, A., Telang, S., Clem, B. and Chesney, J. (2009) Regulation of glucose metabolism by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatases in cancer. Exp. Mol. Pathol. 86, 174-179
14. Calvo, M. N., Bartrons, R., Castano, E., Perales, J. C., Navarro-Sabate, A. and Manzano, A. (2006) PFKFB3 gene silencing decreases glycolysis, induces cell-cycle delay and inhibits anchorage-independent growth in HeLa cells. FEBS Lett. 580, 3308-3314 (Pubitemid 44251000)
15. Kessler, R., Bleichert, F., Warnke, J. P. and Eschrich, K. (2008) 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase (PFKFB3) is up-regulated in high-grade astrocytomas. J. Neuro-Oncol. 86, 257-264
16. Novellasdemunt, L., Obach, M., Millan-Arino, L., Manzano, A., Ventura, F., Rosa, J. L., Jordan, A., Navarro-Sabate, A. and Bartrons, R. (2012) Progestins activate 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 3 (PFKFB3) in breast cancer cells. Biochem. J. 442, 345-356
17. Ando, M., Uehara, I., Kogure, K., Asano, Y., Nakajima, W., Abe, Y., Kawauchi, K. and Tanaka, N. (2010) Interleukin 6 enhances glycolysis through expression of the glycolytic enzymes hexokinase 2 and 6-phosphofructo-2-kinase/ fructose-2,6-bisphosphatase-3. J. Nippon Med. Sch. 77, 97-105
18. Ruiz-Garcia, A., Monsalve, E., Novellasdemunt, L., Navarro-Sabate, A., Manzano, A., Rivero, S., Castrillo, A., Casado, M., Laborda, J., Bartrons, R. and Diaz-Guerra, M. J. (2011) Cooperation of adenosine with macrophage Toll-4 receptor agonists leads to increased glycolytic flux through the enhanced expression of PFKFB3 gene. J. Biol. Chem. 286, 19247-19258
19. Marsin, A. S., Bouzin, C., Bertrand, L. and Hue, L. (2002) 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. 277, 30778-30783 (Pubitemid 34970775)
20. Marsin, A. S., Bertrand, L., Rider, M. H., Deprez, J., Beauloye, C., Vincent, M. F., Van den Berghe, G., Carling, D. and Hue, L. (2000) Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 10, 1247-1255
21. Deprez, J., Vertommen, D., Alessi, D. R., Hue, L. and Rider, M. H. (1997) Phosphorylation and activation of heart 6-phosphofructo-2-kinase by protein kinase B and other protein kinases of the insulin signaling cascades. J. Biol. Chem. 272, 17269-17275 (Pubitemid 27311150)
22. Mouton, V., Toussaint, L., Vertommen, D., Gueuning, M. A., Maisin, L., Havaux, X., Sanchez-Canedo, C., Bertrand, L., Dequiedt, F., Hemmings, B. A. et al. (2010) Heart 6-phosphofructo-2-kinase activation by insulin requires PKB (protein kinase B), but not SGK3 (serum- and glucocorticoid-induced protein kinase 3). Biochem. J. 431, 267-275
23. Cargnello, M. and Roux, P. P. (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75, 50-83
24. Cuadrado, A. and Nebreda, A. R. (2010) Mechanisms and functions of p38 MAPK signalling. Biochem. J. 429, 403-417
25. Gaestel, M. (2006) MAPKAP kinases: MKs - two's company, three's a crowd. Nat. Rev. Mol. Cell Biol. 7, 120-130
26. Heidenreich, O., Neininger, A., Schratt, G., Zinck, R., Cahill, M. A., Engel, K., Kotlyarov, A., Kraft, R., Kostka, S., Gaestel, M. and Nordheim, A. (1999) MAPKAP kinase 2 phosphorylates serum response factor in vitro and in vivo. J. Biol. Chem. 274, 14434-14443
27. Messenguy, F. and Dubois, E. (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316, 1-21 (Pubitemid 37249349)
28. Pellegrini, L., Tan, S. and Richmond, T. J. (1995) Structure of serum response factor core bound to DNA. Nature 376, 490-498
29. Miano, J. M. (2003) Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 35, 577-593
30. Van Schaftingen, E., Lederer, B., Bartrons, R. and Hers, H. G. (1982) 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
31. Gutmann, I. and Wahlefeld, A. W. (1974) L (+) -lactate determination with lactate dehydrogenase and NAD. In Methods of Enzymatic Analysis (Bergmeyer, H. U., ed.), pp. 1464-1468, Academic Press, New York
32. Horman, S., Morel, N., Vertommen, D., Hussain, N., Neumann, D., Beauloye, C., El Najjar, N., Forcet, D., Viollet, B., Walsh, M. P. et al. (2008) AMP-activated protein kinase phosphorylates and desensitizes smooth muscle myosin light chain kinase. J. Biol. Chem. 283, 18505-18512
33. Vertommen, D., Rider, M., Ni, Y., Waelkens, E., Merlevede, W., Vandenheede, J. R. and Van Lint, J. (2000) Regulation of protein kinase D by multisite phosphorylation. Identification of phosphorylation sites by mass spectrometry and characterization by site-directed mutagenesis. J. Biol. Chem. 275, 19567-19576 (Pubitemid 30441550)
34. Karin, M. (1994) Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr. Opin. Cell Biol. 6, 415-424
35. Treisman, R. (1996) Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8, 205-215
36. Roux, P. P. and Blenis, J. (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344 (Pubitemid 38756868)
37. Ronkina, N., Menon, M. B., Schwermann, J., Arthur, J. S., Legault, H., Telliez, J. B., Kayyali, U. S., Nebreda, A. R., Kotlyarov, A. and Gaestel, M. (2010) Stress induced gene expression: a direct role for MAPKAP kinases in transcriptional activation of immediate early genes. Nucleic Acids Res. 39, 2503-2518
38. Posern, G. and Treisman, R. (2006) Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 16, 588-596 (Pubitemid 44636222)
39. Yalcin, A., Clem, B. F., Simmons, A., Lane, A., Nelson, K., Clem, A. L., Brock, E., Siow, D., Wattenberg, B., Telang, S. and Chesney, J. (2009) Nuclear targeting of 6-phosphofructo-2-kinase (PFKFB3) increases proliferation via cyclin-dependent kinases. J. Biol. Chem. 284, 24223-24232
40. Riera, L., Obach, M., Navarro-Sabate, A., Duran, J., Perales, J. C., Vinals, F., Rosa, J. L., Ventura, F. and Bartrons, R. (2003) Regulation of ubiquitous 6-phosphofructo-2-kinase by the ubiquitin-proteasome proteolytic pathway during myogenic C2C12 cell differentiation. FEBS Lett. 550, 23-29 (Pubitemid 37281351)
41. Herrero-Mendez, A., Almeida, A., Fernandez, E., Maestre, C., Moncada, S. and Bolanos, J. P. (2009) The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat. Cell Biol. 11, 747-752
42. Garcia-Cao, I., Song, M. S., Hobbs, R. M., Laurent, G., Giorgi, C., de Boer, V. C., Anastasiou, D., Ito, K., Sasaki, A. T., Rameh, L. et al. (2012) Systemic elevation of PTEN induces a tumor-suppressive metabolic state. Cell 149, 49-62