Targeting mitochondria with avocatin B induces selective leukemia cell death

Cancer Research

Volumn 75, Issue 12, 2015, Pages 2478-2488

  Lee, Eric A ^a   Angka, Leonard ^a   Rota, Sarah Grace ^a   Hanlon, Thomas ^a   Mitchell, Andrew ^a   Hurren, Rose ^b   Wang, Xiao Ming ^b   Gronda, Marcela ^b   Boyaci, Ezel ^a   Bojko, Barbara ^a   Minden, Mark ^b   Sriskanthadevan, Shrivani ^b   Datti, Alessandro ^c,d   Wrana, Jeffery L ^c   Edginton, Andrea ^a   Pawliszyn, Janusz ^a   Joseph, Jamie W ^a   Quadrilatero, Joe ^a   Schimmer, Aaron D ^b   Spagnuolo, Paul A ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF PERUGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; AVOCATIN B; CARNITINE PALMITOYLTRANSFERASE I; CYTOCHROME C; ETOMOXIR; LIPID; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; PLANT EXTRACT; VEGETABLE OIL;

ACUTE MYELOBLASTIC LEUKEMIA; ARTICLE; AVOCADO; CELL ASSAY; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; FATTY ACID OXIDATION; HEMATOPOIETIC STEM CELL; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; LEUKEMIA CELL; LIPID TRANSPORT; MITOCHONDRION; OUTCOME ASSESSMENT; PERIPHERAL BLOOD STEM CELL; PRIORITY JOURNAL; ANIMAL; APOPTOSIS; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; FRUIT; LEUKEMIA, MYELOID, ACUTE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION; PATHOLOGY; PERSEA; PROCEDURES;

ANIMALS; APOPTOSIS; CELL DEATH; CHROMATOGRAPHY, LIQUID; FRUIT; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MASS SPECTROMETRY; MICE; MITOCHONDRIA; OXIDATION-REDUCTION; PERSEA; PLANT EXTRACTS; PLANT OILS; REACTIVE OXYGEN SPECIES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84941735924     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2676     Document Type: Article

References (49)

1. Skrtic M, Sriskanthadevan S, Jhas B, Gebbia M, Wang X, Wang Z, et al. Inhibition of mitochondrial translation as a therapeutic strategy for human acute myeloid leukemia. Cancer Cell 2011; 20: 674-88.
2. Samudio I, Harmancey R, Fiegl M, Kantarjian H, Konopleva M, Korchin B, et al. Pharmacologic inhibition of fatty acid oxidation sensitizes human leukemia cells to apoptosis induction. J Clin Invest 2010; 120: 142-56.
3. Shipley JL, Butera JN. Acute myelogenous leukemia. Exp Hematol 2009; 37: 649-58.
4. Lowenberg B, Downing JR, Burnett A. Acute myeloid leukemia. N Engl J Med 1999; 341: 1051-62.
5. McDermott SP, Eppert K, Notta F, Isaac M, Datti A, Al-Awar R, et al. A small molecule screening strategy with validationon human leukemia stem cells uncovers the therapeutic efficacy of kinetin riboside. Blood 2012; 119: 1200-7.
6. Spagnuolo PA, Hurren R, Gronda M, MacLean N, Datti A, Basheer A, et al. Inhibition of intracellular dipeptidyl peptidases 8 and 9 enhances parthenolide's anti-leukemic activity. Leukemia 2013; 27: 1236-44.
7. Spagnuolo PA, Hu J, Hurren R, Wang X, Gronda M, Sukhai MA, et al. The antihelmintic flubendazole inhibits microtubule function through a mechanism distinct from Vinca alkaloids and displays preclinical activity in leukemia and myeloma. Blood 2010; 115: 4824-33.
8. Sukhai MA, Prabha S, Hurren R, Rutledge AC, Lee AY, Sriskanthadevan S, et al. Lysosomal disruption preferentially targets acute myeloid leukemia cells and progenitors. J Clin Invest 2013; 123: 315-28.
9. Sachlos E, Risueno RM, Laronde S, Shapovalova Z, Lee JH, Russell J, et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell 2012; 149: 1284-97.
10. Angka L, Lee EA, Rota SG, Hanlon T, Sukhai M, Minden M, et al. Glucopsychosine increases cytosolic calcium to induce calpain-mediated apoptosis of acute myeloid leukemia cells. Cancer Lett 2014; 348: 29-37.
11. Abe Y, Sakairi T, Beeson C, Kopp JB. TGF-beta1 stimulates mitochondrial oxidative phosphorylation and generation of reactive oxygen species in cultured mouse podocytes, mediated in part by the mTOR pathway. Am J Physiol Renal Physiol 2013; 305: F1477-90.
12. Dam AD, Mitchell AS, Rush JW, Quadrilatero J. Elevated skeletal muscle apoptotic signaling following glutathione depletion. Apoptosis 2012; 17: 48-60.
13. Owusu-Ansah E, Yavari A, Banerjee U. A protocol for in vivo detection of reactive oxygen species. 2008; doi: 10.1038/nprot.2008.23.
14. Boyaci E, Sparham C, Pawliszyn J. Thin-film microextraction coupled to LC-ESI-MS/MS for determination of quaternary ammonium compounds in water samples. Anal Bioanal Chem 2014; 406: 409-20.
15. Boyaci E, Gorynski K, Rodriguez-Lafuente A, Bojko B, Pawliszyn J. Introduction of solid-phase microextraction as a high-throughput sample preparation tool in laboratory analysis of prohibited substances. Anal Chim Acta 2014; 809: 69-81.
16. McMillan EM, Graham DA, Rush JW, Quadrilatero J. Decreased DNA fragmentation and apoptotic signaling in soleus muscle of hypertensive rats following 6 weeks of treadmill training. J Appl Physiol 2012; 113: 1048-57.
17. Christensen ME, Jansen ES, Sanchez W, Waterhouse NJ. Flow cytometry based assays for the measurement of apoptosis-associated mitochondrial membrane depolarisation and cytochrome c release. Methods 2013; 61: 138-45.
18. Waterhouse NJ, Trapani JA. A new quantitative assay for cytochrome c release in apoptotic cells. Cell Death Differ 2003; 10: 853-5.
19. Warner JK, Wang JC, Takenaka K, Doulatov S, McKenzie JL, Harrington L, et al. Direct evidence for cooperating genetic events in the leukemic transformation of normal human hematopoietic cells. Leukemia 2005; 19: 1794-805.
20. Alves HM, Coxon DT, Falshaw CP, Godtfredsen WO, Ollis WD. The Avocatins - a new class of natural products. Ann Braz Acad Sci 1970; 42: 4.
21. ChemBank. 2014; Cited Sept 2014. http://chembank.broadinstitute.org/chemistry/viewMolecule.htm;jsessionid=9CC037B2065BFDE714299282-DD50A255?cbid=3198534.
22. Konopleva M, Watt J, Contractor R, et al. Mechanisms of antileukemic activity of the novel Bcl-2 homology domain-3 mimetic GX15-070 (obatoclax). Cancer Res 2008; 68: 3413-20.
23. Carracedo A, Cantley LC, Pandolfi PP. Cancer metabolism: fatty acid oxidation in the limelight. Nat Rev Cancer 2013; 13: 227-32.
24. Heiden MGV, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-33.
25. Kirsch M, De Groot H. NAD(P)H, a directly operating antioxidant? FASEB J 2001; 15: 1569-74.
26. Pike LS, Smift AL, Croteau NJ, Ferrick DA, Wu M. Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Biochim Biophys Acta 2011; 1807: 726-34.
27. Godbout JP, Berg BM, Kelley KW, Johnson RW. alpha-Tocopherol reduces lipopolysaccharide-induced peroxide radical formation and interleukin-6 secretion in primary murine microglia and in brain. J Neuroimmunol 2004; 149: 101-9.
28. 1 and cycling peripheral blood lymphocytes and induce massive deletion of mature T and B cells. Cancer Res 2000; 60: 1901-7.
29. Vejpongsa P, Yeh ETH Topoisomerase 2beta: a promising molecular target for primary prevention of anthracycline-induced cardiotoxicity. Clin Pharmacol Ther 2014; 95: 45-52.
30. Desjardins P, Frost E, Morais R. Ethidium bromide-induced loss of mitochondrial DNA from primary chicken embryo fibroblasts. Mol Cell Biol 1985; 5: 1163-9.
31. Hashiguchi K, Zhang-Akiyama QM. Establishment of human cell lines lacking mitochondrial DNA. Methods Mol Biol 2009; 554: 383-91.
32. Reddy JK, Hashimoto T. Peroxisomal beta-oxidation and peroxisome proliferator-activated receptor alpha: an adaptive metabolic system. Annu Rev Nutr 2001; 21: 193-230.
33. Sriskanthadevan S, Jeyaraju DV, Chung TE, Prabha S, Xu W, Skrtic M, et al. AML cells have low spare reserve capacity in their respiratory chain that renders them susceptible to oxidative metabolic stress. Blood 2015; 125: 2120-30.
34. Tomasello F, Messina A, Lartigue L, Schembri L, Medina C, Reina S, et al. Outer membrane VDAC1 controls permeability transition of the inner mitochondrial membrane in cellulo during stress-induced apoptosis. Cell Res 2009; 19: 1363-76.
35. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99-163.
36. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-33.
37. Campbell RG, Hashim SA. Deposition in adipose tissue and transport of odd-numbered fatty acids. Am J Physiol 1969; 217: 1614-8.
38. Wolk A, Furuheim M, Vessby B. Fatty acid composition of adipose tissue and serum lipids are valid biological markers of dairy fat intake in men. J Nutr 2001; 131: 828-33.
39. Gotoh N, Moroda K, Watanabe H, Yoshinaga K, Tanaka M, Mizobe H, et al. Metabolism of odd-numbered fatty acids and even-numbered fatty acids in mouse. J Oleo Sci 2008; 57: 293-9.
40. Pi-Sunyer FX. Rats enriched with odd-carbon fatty acids. Effect of prolonged starvation on liver glycogen and serum lipids, glucose and insulin. Diabetes 1971; 20: 200-5.
41. VanItallie TB, Khachadurian AK. Rats enriched with odd-carbon fatty acids: maintenance of liver glycogen during starvation. Science 1969; 165: 811-3.
42. Klein RA, Halliday D, Pittet PG. The use of 13-methyltetradecanoic acid as an indicator of adipose tissue turnover. Lipids 1980; 15: 572-9.
43. Berg JM, Tymoczko JL, Stryer L. Biochemistry. Certain fatty acids require additional steps for degradation. 5th ed. New York: W H Freeman; 2002. Available from: http://www.ncbi.nlm.nih.gov/books/NBK22387/.
44. Schrauwen P, Hesselink MK. Oxidative capacity, lipotoxicity, and mito-chondrial damage in type 2 diabetes. Diabetes 2004; 53: 1412-7.
45. Schrauwen P, Schrauwen-Hinderling V, Hoeks J, Hesselink MK. Mitochondrial dysfunction and lipotoxicity. Biochim Biophys Acta 2010; 1801: 266-71.
46. Holubarsch CJ, Rohrbach M, Karrasch M, Boehm E, Polonski L, Ponikowski P, et al. A double-blind randomized multicentre clinical trial to evaluate the efficacy and safety oftwo doses of etomoxir in comparison with placebo in patients with moderate congestive heart failure: the ERGO (etomoxir for the recovery of glucose oxidation) study. Clin Sci 2007; 113: 205-12.
47. Ashrafian H, Horowitz JD, Frenneaux MP. Perhexiline. Cardiovasc Drug Rev 2007; 25: 76-97.
48. Passeron J. [Effectiveness of trimetazidine in stable effort angina due to chronic coronary insufficiency. A double-blind versus placebo study]. Presse Med 1986; 15: 1775-8.
49. Aldakkak M, Stowe DF, Camara AK. Safety and efficacy of ranolazine for the treatment of chronic angina pectoris. Clin Med Insights Ther 2013; 2013: 1-14.