Mechanisms underlying 3-bromopyruvate-induced cell death in colon cancer

Journal of Bioenergetics and Biomembranes

Volumn 47, Issue 4, 2015, Pages 319-329

  Sun, Yiming ^a   Liu, Zhe ^a   Zou, Xue ^a   Lan, Yadong ^a   Sun, Xiaojin ^a   Wang, Xiu ^a   Zhao, Surong ^a   Jiang, Chenchen ^b   Liu, Hao ^a  

^a BENGBU MEDICAL COLLEGE   (China)

^b UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

3 Bromopyruvate; Apoptosis; ATP; Autophagy; Necroptosis

Indexed keywords

3 BROMOPYRUVATE; 3 METHYLADENINE; ANTINEOPLASTIC AGENT; UNCLASSIFIED DRUG; BROMOPYRUVATE; PYRUVIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL CULTURE; CELL DEATH; CELL ENERGY; CELL STRUCTURE; CHROMATIN CONDENSATION; COLON CANCER; COLONY FORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GROWTH; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MTT ASSAY; NECROPTOSIS; NONHUMAN; ROOM TEMPERATURE; TUMOR GROWTH; WESTERN BLOTTING; ANIMAL; AUTOPHAGY; BAGG ALBINO MOUSE; COLONIC NEOPLASMS; DRUG EFFECTS; DRUG SCREENING; ENERGY METABOLISM; FEMALE; METABOLISM; MORTALITY; NUDE MOUSE; TUMOR CELL LINE;

ANIMALS; AUTOPHAGY; CELL LINE, TUMOR; COLONIC NEOPLASMS; ENERGY METABOLISM; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; PYRUVATES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84940436219     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-015-9612-1     Document Type: Article

References (50)

1. Bellairs R (1961) Cell death in chick embryos as studied by electron microscopy. J Anat 95(54–60):53
2. Cardaci S, Desideri E, Ciriolo MR (2012) Targeting aerobic glycolysis: 3-bromopyruvate as a promising anticancer drug. J Bioenerg Biomembr 44:17–29. doi:10.1007/s10863-012-9422-7
3. Chen Z, Zhang H, Lu W, Huang P (2009) Role of mitochondria-associated hexokinase II in cancer cell death induced by 3-bromopyruvate. Biochim Biophys Acta 1787:553–560. doi:10.1016/j.bbabio.2009.03.003
4. Chesney J et al (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
5. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK (2009) Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137:1112–1123. doi:10.1016/j.cell.2009.05.037
6. Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195–213
7. da-Silva WS et al (2004) Mitochondrial bound hexokinase activity as a preventive antioxidant defense: steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria. J Biol Chem 279:39846–39855. doi:10.1074/jbc.M403835200
8. Degterev A et al (2005) Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1:112–119. doi:10.1038/nchembio711
9. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102:33–42
10. Ferraro E et al (2008) Apoptosome-deficient cells lose cytochrome c through proteasomal degradation but survive by autophagy-dependent glycolysis. Mol Biol Cell 19:3576–3588. doi:10.1091/mbc.E07-09-0858
11. Festjens N, Vanden Berghe T, Vandenabeele P (2006) Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757:1371–1387. doi:10.1016/j.bbabio.2006.06.014
12. Galluzzi L et al (2012) Molecular definitions of cell death subroutines: recommendations of the nomenclature committee on cell death 2012. Cell Death Differ 19:107–120. doi:10.1038/cdd.2011.96
13. Ganapathy-Kanniappan S et al (2010) 3-bromopyruvate: a new targeted antiglycolytic agent and a promise for cancer therapy. Curr Pharm Biotechnol 11:510–517
14. Geschwind JF, Ko YH, Torbenson MS, Magee C, Pedersen PL (2002) Novel therapy for liver cancer: direct intraarterial injection of a potent inhibitor of ATP production. Cancer Res 62:3909–3913
15. He S, Wang L, Miao L, Wang T, Du F, Zhao L, Wang X (2009) Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137:1100–1111. doi:10.1016/j.cell.2009.05.021
16. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90. doi:10.3322/caac.20107
17. Jin S, White E (2008) Tumor suppression by autophagy through the management of metabolic stress. Autophagy 4:563–566
18. Kabeya Y et al (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720–5728. doi:10.1093/emboj/19.21.5720
19. Komatsu M et al (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880–884. doi:10.1038/nature04723
20. Kuma A et al (2004) The role of autophagy during the early neonatal starvation period. Nature 432:1032–1036. doi:10.1038/nature03029
21. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185:1481–1486
22. Levy AG et al (2012) The combination of the novel glycolysis inhibitor 3-BrOP and rapamycin is effective against neuroblastoma. Invest New Drugs 30:191–199. doi:10.1007/s10637-010-9551-y
23. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489
24. Liu XH, Zheng XF, Wang YL (2009) Inhibitive effect of 3-bromopyruvic acid on human breast cancer MCF-7 cells involves cell cycle arrest and apoptotic induction. Chin Med J (Engl) 122:1681–1685
25. Liu Z et al (2014) 3-Bromopyruvate induces apoptosis in breast cancer cells by downregulating Mcl-1 through the PI3K/Akt signaling pathway. Anticancer Drugs 25:447–455. doi:10.1097/CAD.0000000000000081
26. Lockshin RA, Zakeri Z (2007) Cell death in health and disease. J Cell Mol Med 11:1214–1224. doi:10.1111/j.1582-4934.2007.00150.x
27. Lukens JR, Vogel P, Johnson GR, Kelliher MA, Iwakura Y, Lamkanfi M, Kanneganti TD (2013) RIP1-driven autoinflammation targets IL-1alpha independently of inflammasomes and RIP3. Nature 498:224–227. doi:10.1038/nature12174
28. Mathew R, White E (2011) Autophagy in tumorigenesis and energy metabolism: friend by day, foe by night. Curr Opin Genet Dev 21:113–119. doi:10.1016/j.gde.2010.12.008
29. Mathiasen IS, Jaattela M (2002) Triggering caspase-independent cell death to combat cancer. Trends Mol Med 8:212–220
30. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728–741. doi:10.1016/j.cell.2011.10.026
31. Mortensen M et al (2011) The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med 208:455–467. doi:10.1084/jem.20101145
32. Narendra D, Tanaka A, Suen DF, Youle RJ (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183:795–803. doi:10.1083/jcb.200809125
33. Ota S, Geschwind JF, Buijs M, Wijlemans JW, Kwak BK, Ganapathy-Kanniappan S (2013) Ultrasound-guided direct delivery of 3-bromopyruvate blocks tumor progression in an orthotopic mouse model of human pancreatic cancer. Target Oncol 8:145–151. doi:10.1007/s11523-013-0273-x
34. Parks SK, Mazure NM, Counillon L, Pouyssegur J (2013) Hypoxia promotes tumor cell survival in acidic conditions by preserving ATP levels. J Cell Physiol 228:1854–1862. doi:10.1002/jcp.24346
35. Peter ME, Krammer PH (2003) The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 10:26–35. doi:10.1038/sj.cdd.4401186
36. Schweichel JU, Merker HJ (1973) The morphology of various types of cell death in prenatal tissues. Teratology 7:253–266. doi:10.1002/tera.1420070306
37. Shoshan MC (2012) 3-Bromopyruvate: targets and outcomes. J Bioenerg Biomembr 44:7–15. doi:10.1007/s10863-012-9419-2
38. Simonnet H et al (2002) Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma. Carcinogenesis 23:759–768
39. Takahashi A et al (2012) Autophagy guards against cisplatin-induced acute kidney injury. Am J Pathol 180:517–525. doi:10.1016/j.ajpath.2011.11.001
40. Tanida I, Ueno T, Kominami E (2004) LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 36:2503–2518. doi:10.1016/j.biocel.2004.05.009
41. Thapa RJ et al (2013) Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc Natl Acad Sci U S A 110:E3109–3118. doi:10.1073/pnas.1301218110
42. Verhagen AM et al (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43–53
43. Warburg O (1928) The chemical constitution of respiration ferment. Science 68:437–443. doi:10.1126/science.68.1767.437
44. Warburg O (1956) On the origin of cancer cells. Science 123:309–314
45. Xu RH et al (2005) 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
46. Yuan J, Kroemer G (2010) Alternative cell death mechanisms in development and beyond. Genes Dev 24:2592–2602. doi:10.1101/gad.1984410
47. Zhang DW et al (2009a) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325:332–336. doi:10.1126/science.1172308
48. Zhang Q et al (2014) Hexokinase II inhibitor, 3-BrPA induced autophagy by stimulating ROS formation in human breast cancer cells. Genes Cancer 5:100–112
49. Zhang X et al (2009b) Novel therapy for malignant pleural mesothelioma based on anti-energetic effect: an experimental study using 3-Bromopyruvate on nude mice. Anticancer Res 29:1443–1448
50. Zuo X, Djordjevic JT, Bijosono Oei J, Desmarini D, Schibeci SD, Jolliffe KA, Sorrell TC (2011) Miltefosine induces apoptosis-like cell death in yeast via Cox9p in cytochrome c oxidase. Mol Pharmacol 80:476–485. doi:10.1124/mol.111.072322