The energy blockers bromopyruvate and lonidamine lead GL15 glioblastoma cells to death by different p53-dependent routes

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Davidescu, Magdalena ^a   Macchioni, Lara ^a   Scaramozzino, Gaetano ^a   Cristina Marchetti, Maria ^a   Migliorati, Graziella ^a   Vitale, Rita ^b   Corcelli, Angela ^c   Roberti, Rita ^a   Castigli, Emilia ^a   Corazzi, Lanfranco ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF BARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BROMOPYRUVATE; ENZYME INHIBITOR; INDAZOLE DERIVATIVE; LONIDAMINE; PROTEIN P53; PYRUVIC ACID DERIVATIVE;

APOPTOSIS; AUTOPHAGY; DRUG EFFECTS; ENERGY METABOLISM; GLIOBLASTOMA; HUMAN; METABOLISM; MITOCHONDRION; TUMOR CELL LINE;

APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; ENERGY METABOLISM; ENZYME INHIBITORS; GLIOBLASTOMA; HUMANS; INDAZOLES; MITOCHONDRIA; PYRUVATES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84942155644     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14343     Document Type: Article

References (46)

1. Krakstad, C. and Chekenya, M. Survival signalling and apoptosis resistance in glioblastomas: opportunities for targeted therapeutics. Molecular Cancer 9, 135-148 (2010).
2. Holland, E. C. Gliomagenesis: genetic alterations and mouse models. Nat. Rev. Genet. 2, 120-129 (2001).
3. Wolf, A., Agnihotri, S. and Guha, A. Targeting metabolic remodeling in glioblastoma multiforme. Oncotarget 1, 552-562 (2010).
4. Wolf, A., Agnihotri, S., Munoz, D. and Guha, A. Developmental profile and regulation of the glycolytic enzyme hexokinase 2 in normal brain and glioblastoma multiforme. Neurobiol. Dis. 44, 84-91 (2011).
5. Pastorino, J. G., Hoek, J. B. and Shulga, N. Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res. 65, 10545-10554 (2005).
6. Pedersen, P. L. Warburg, me and Hexokinase 2: Multiple discoveries of key molecular events underlying one of cancers most common phenotypes, the Warburg Effect i.e., elevated glycolysis in the presence of oxygen. J. Bioenerg. Biomembr. 39, 211-222 (2007).
7. Xu, R-H. et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res. 65, 613-621 (2005).
8. Kim, J. S. et al. Role of reactive oxygen species-mediated mitochondrial dysregulation in 3-bromopyruvate induced cell death in hepatoma cells: ROS-mediated cell death by 3-BrPA. J. Bioenerg. Biomembr. 40, 607-618 (2008).
9. Pereira da Silva, A. P. et al. A. Inhibition of energy-producing pathways of HepG2 cells by 3-bromopyruvate. Biochem. J. 417, 717-726 (2009).
10. Yun, J. et al. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science 325, 1555-1559 (2009).
11. Qin, J. Z., Xin, H. and Nickoloff, B. J. 3-Bromopyruvate induces necrotic cell death in sensitive melanoma cell lines. Biochem. Biophys. Res. Commun. 396, 495-500 (2010).
12. Ko, Y. H. et al. Advanced cancers: eradication in all cases using 3-bromopyruvate therapy to deplete ATP. Biochem. Biophys. Res. Commun. 324, 269-275 (2004).
13. Corsi, G. and Palazzo, G. 1-Halobenzyl-1H-indazole-3-carboxylic acids. A new class of antispermatogenic agents. J. Med. Chem. 19, 778-783 (1976).
14. Ravagnan, L. et al. Lonidamine triggers apoptosis via a direct, Bcl-2-inhibited effect on the mitochondrial permeability transition pore. Oncogene 18, 2537-2546 (1999).
15. Ben-Yoseph, O., Lyons, J. C., Song, C. W. and Ross, B. D. Mechanism of action of lonidamine in the 9L brain tumor model involves inhibition of lactate efflux and intracellular acidification. J. Neurooncol. 36, 149-157 (1998).
16. Lena, A. et al. Drugs targeting the mitochondrial pore act as cytotoxic and cytostatic agents in temozolomide-resistant glioma cells. J. Transl. Med. doi: 10.1186/1479-5876-7-13 (2009).
17. Guillamo, J. S. et al. Migration pathways of human glioblastoma cells xenografted into the immunosuppressed rat brain. J. Neurooncol. 52, 205-215 (2001).
18. Castigli, E. et al. Interleukin-1beta induces apoptosis in GL15 glioblastoma-derived human cell line. Am. J. Physiol. Cell Physiol. 279, C2043-C2049 (2000).
19. Buratta, M. et al. Loss of cardiolipin in palmitate-treated GL15 glioblastoma cells favors cytochrome c release from mitochondria leading to apoptosis. J. Neurochem. 105, 1019-1031 (2008).
20. Sciaccaluga, M. et al. CXCL12-induced glioblastoma cell migration requires intermediate conductance Ca2+-activated K+cannel activity. Am. J. Physiol. Cell Physiol. 299, C175-184 (2010).
21. Sciaccaluga, M. et al. Functional cross talk between CXCR4 and PDGFR on glioblastoma cells is essential for migration. PLoS ONE 8, e73426. doi: 10.1371/journal.pone.0073426 (2013).
22. Davidescu, M. et al. Bromopyruvate mediates autophagy and cardiolipin degradation to monolyso-cardiolipin in GL15 glioblastoma cells. J. Bioenerg. Biomembr. 44, 51-60 (2012).
23. Tasdemir, E. et al. Regulation of autophagy by cytoplasmic p53. Nat. Cell Biol. 10, 676-687 (2008).
24. Caspari, T. How to activate p53. Current Biology 10, R315-R317 (2000).
25. Aslan, J. E. and Thomas, G. Death by committee: organellar trafficking and communication in apoptosis. Traffic 10, 1390-1404 (2009).
26. Zhang, Y.-B. et al. Autophagy protein p62/SQSTM1 is involved in HAMLET-induced cell death by modulating apoptosis in U87MG cells. Cell Death and Disease 4, e550, doi: 10.1038/cddis.2013.77 (2013).
27. Yang, X., Fraser, M., Moll, U. M., Basak, A. and Tsang, B. K. Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway. Cancer Res. 15, 3126-3136 (2006).
28. Meloche, H. P., Luczak, M. A. and Wurster, J. M. The substrate analog bromopyruvate, as both a substrate and alkylating agent for 2-keto-3-deoxy-6-phosphogluconic aldolase. Kinetic and stereochemical studies. J. Biol. Chem. 247, 4186-4191 (1972).
29. Ko, Y. H., Pedersen, P. L. and Geschwind, J. F. Glucose catabolism in the rabbit VX2 tumor model for liver cancer: characterization and targeting hexokinase. Cancer Lett. 173, 83-91 (2001).
30. El Sayed, S. M. et al. 3-Bromopyruvate antagonizes effects of lactate and pyruvate, synergizes with citrate and exerts novel antiglioma effects. J. Bioenerg. Biomembr. 44, 61-79 (2012).
31. Shoshan, M. C. 3-Bromopyruvate: targets and outcomes. J. Bioenerg. Biomembr. 44, 7-15 (2012).
32. Mizushima, N. Yoshimori, T. and Levine, B. Methods in mammalian autophagy research. Cell 140, 313-326 (2010).
33. Zalckvar, E. et al. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep. 10, 285-292 (2009).
34. Kang, R., Zeh, H. J., Lotze, M. T. and Tang, D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18, 571-580 (2011).
35. Pastorino, J. G. and Hoeck, J. B. Regulation of hexokinase binding to VDAC. J. Bioenerg. Biomembr. 40, 171-182 (2008).
36. Macchioni, L. et al. Mitochondrial dysfunction and effect of antiglycolytic bromopyruvic acid in GL15 glioblastoma cells. J. Bioenerg. Biomembr. 43, 507-518 (2011).
37. Mathupala, S. P., Ko, Y. H. and Pedersen, P. L. Hexokinase II: cancers double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 25, 4777-4786 (2006).
38. Chen, Z., Zhang, H., Lu, W. and Huang, P. Role of mitochondria-associated hexokinase II in cancer cell death induced by 3-bromopyruvate. Biochim. Biophys. Acta 1787, 553-560 (2009).
39. Moll, U. M. and Petrenko, O. The MDM2-p53 intercation. Mol. Cancer Res. 1, 1001-1008 (2003).
40. Maclaine, N. J. and Hupp, T. R. The regulation of p53 by phosphorylation: a model for how distinct signals integrate into the p53 pathway. Aging 1, 490-502 (2009).
41. Li, C. H., Cheng, Y. W., Liao, P. L. and Kang, J. J. Translocation of p53 to mitochondria is regulated by its lipid binding property to anionic phospholipids and it participates in cell death control. Neoplasia 12, 150-160 (2010).
42. Shankar, S. and Srivastava, R. K. Involvement of Bcl-2 family members, phosphatidylinositol 3-kinase/AKT and mitochondrial p53 in curcumin (diferulolylmethane)-induced apoptosis in prostate cancer. Int. J. Oncol. 4, 905-918 (2007).
43. Susin, S. A. et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441-446 (1999).
44. Castigli, E. et al. GL15 and U251 glioblastoma-derived human cell lines are peculiarly susceptible to induction of mitotic death by very low concentrations of okadaic acid. Oncol. Rep. 15, 463-470 (2006).
45. Floridi, A. et al. Effect of lonidamine on the energy metabolism of Erlich ascites tumor cells. Cancer Res. 41, 4661-4666 (1981).
46. Sun, G. et al. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis of cellular glycerophospholipids enabled by multiplexed solvent dependent analyte-matrix interactions. Anal. Chem. 80, 7576-7585 (2008).