Drug redeployment to kill leukemia and lymphoma cells by disrupting SCD1-mediated synthesis of monounsaturated fatty acids

Cancer Research

Volumn 75, Issue 12, 2015, Pages 2530-2540

  Southam, Andrew D ^a   Khanim, Farhat L ^a   Hayden, Rachel E ^a   Constantinou, Julia K ^a   Koczula, Katarzyna M ^a   Michell, Robert H ^a   Viant, Mark R ^a   Drayson, Mark T ^a   Bunce, Chris M ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACYL COENZYME A DESATURASE; BEZAFIBRATE; CARBON 13; FATTY ACID SYNTHASE; GLUCOSE; MEDROXYPROGESTERONE ACETATE; MONOUNSATURATED FATTY ACID; OLEIC ACID; PALMITIC ACID; PHOSPHOLIPID; STEAROYL COA DESATURASE 1; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; SCD1 PROTEIN, HUMAN;

ACUTE MYELOBLASTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; ARTICLE; BURKITT LYMPHOMA; CELL KILLING; CONTROLLED STUDY; DRUG MECHANISM; DRUG REDEPLOYMENT; DRUG TARGETING; FATTY ACID SYNTHESIS; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKEMIA CELL; LIPID METABOLISM; LIPIDOMICS; LIPOGENESIS; LYMPHOMA CELL; MASS SPECTROMETRY; PHARMACODYNAMICS; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; HL 60 CELL LINE; K562 CELL LINE; LEUKEMIA; LYMPHOMA; METABOLISM; PROGNOSIS; TUMOR CELL LINE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BEZAFIBRATE; CELL LINE, TUMOR; FATTY ACIDS, MONOUNSATURATED; HL-60 CELLS; HUMANS; K562 CELLS; LEUKEMIA; LIPID METABOLISM; LYMPHOMA; MEDROXYPROGESTERONE ACETATE; PROGNOSIS; STEAROYL-COA DESATURASE;

EID: 84941734485     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0202     Document Type: Article

References (50)

1. Buechner T, Berdel WE, Haferlach C, Haferlach T, Schnittger S, Mueller-Tidow C, et al. Age-related risk profile and chemotherapy dose response in acute myeloid leukemia: a study by the German Acute Myeloid Leukemia Cooperative Group. J Clin Oncol 2009; 27: 61-9.
2. Burnett AK, Hills RK, Milligan DW, Goldstone AH, Prentice AG, McMullin M-F, et al. Attempts to optimize induction and consolidation treatment in acute myeloid leukemia: results of the MRC AML12 trial. J Clin Oncol 2010; 28: 586-95.
3. Molyneux EM, Rochford R, Griffin B, Newton R, Jackson G, Menon G, et al. Burkitt's lymphoma. Lancet 2012; 379: 1234-44.
4. Ashburn TT, Thor KB. Drug repositioning: identifying and developing new uses for existing drugs. Nat Rev Drug Discov 2004; 3: 673-83.
5. Palumbo A, Facon T, Sonneveld P, Blade J, Offidani M, Gay F, et al. Thalidomide for treatment of multiple myeloma: 10 years later. Blood 2008; 111: 3968-77.
6. Wang ZY, Chen Z. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood 2008; 111: 2505-15.
7. Fenton SL, Luong QT, Sarafeim A, Mustard KJW, Pound J, Desmond JC, et al. Fibrates and medroxyprogesterone acetate induce apoptosis of primary Burkitt's lymphoma cells and cell lines: potential for applying old drugs to a new disease. Leukemia 2003; 17: 568-75.
8. Hayden RE, Pratt G, Davies NJ, Khanim FL, Birtwistle J, Delgado J, et al. Treatment ofprimary CLL cells with bezafibrate and medroxyprogesterone acetate induces apoptosis and represses the pro-proliferative signal of CD40-ligand, in part through increased 15d Delta(12,14,)PGJ(2). Leukemia 2009; 23: 292-304.
9. Khanim FL, Hayden RE, Birtwistle J, Lodi A, Tiziani S, Davies NJ, et al. Combined bezafibrate and medroxyprogesterone acetate: potential novel therapy for acute myeloid leukaemia. PLoS ONE 2009; 4: 14.
10. Hayden RE, Kussaibati R, Cronin LM, Pratt G, Roberts C, Drayson MT, et al. Bezafibrate and medroxyprogesterone acetate target resting and CD40L-stimulated primary marginal zone lymphoma and show promise in indolent B-cell non-Hodgkin lymphomas. Leuk Lymphoma 2015; 56: 1079-87.
11. Murray JA, Khanim FL, Hayden RE, Craddock CF, Holyoake TL, Jackson N, et al. Combined bezafibrate and medroxyprogesterone acetate have efficacy without haematological toxicity in elderly and relapsed acute myeloid leukaemia (AML). Br J Haematol 2010; 149: 65-9.
12. Molyneux E, Merrick B, Khanim FL, Banda K, Dunn JA, Iqbal G, et al. Bezafibrate and medroxyprogesterone acetate in resistant and relapsed endemic Burkitt lymphoma in Malawi; an open-label, single-arm, phase 2 study (ISRCTN34303497). Br J Haematol 2014; 164: 888-90.
13. Willson TM, Brown PJ, Sternbach DD, Henke BR. The PPARs: from orphan receptors to drug discovery. J Med Chem 2000; 43: 527-50.
14. Yadav BK, Gupta RK, Gyawali P, Shrestha R, Poudel B, Sigdel M, et al. Effects of long-term use of depo-medroxyprogesterone acetate on lipid metabolism in Nepalese women. Korean J Lab Med 2011; 31: 95-7.
15. Menendez JA, Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer 2007; 7: 763-77.
16. Swinnen JV, Brusselmans K, Verhoeven G. Increased lipogenesis in cancer cells: new players, novel targets. Curr Opin Clin Nutr Metab Care 2006; 9: 358-65.
17. Igal RA Stearoyl-CoA desaturase-1: anovel key player in the mechanisms of cell proliferation, programmed cell death and transformation to cancer. Carcinogenesis 2010; 31: 1509-15.
18. Noto A, Raffa S, De Vitis C, Roscilli G, Malpicci D, Coluccia P, et al. Stearoyl-CoA desaturase-1 is a key factor for lung cancer-initiating cells. Cell Death Dis 2013; 4: e947.
19. Bhatt AP, Jacobs SR, Freemerman AJ, Makowski L, Rathmell JC, Dittmer DP, et al. Dysregulation of fatty acid synthesis and glycolysis in non-Hodgkin lymphoma. Proc Natl Acad Sci U S A 2012; 109: 11818-23.
20. Pizer ES, Wood FD, Pasternack GR, Kuhajda FP. Fatty acid synthase (FAS): a target for cytotoxic antimetabolites in HL60 promyelocytic leukemia cells. Cancer Res 1996; 56: 745-51.
21. Beckers A, Organe S, Tinunermans L, Scheys K, Peeters A, Brusselmans K, et al. Chemical inhibition of Acetyl-CoA carboxylase induces growth arrest and cytotoxicity selectively in cancer cells. Cancer Res 2007; 67: 8180-7.
22. Fritz V, Benfodda Z, Rodier G, Henriquet C, Iborra F, Avances C, et al. Abrogation of de novo lipogenesis by stearoyl-CoA desaturase 1 inhibition interferes with oncogenic signaling and blocks prostate cancer progression in mice. Mol Cancer Ther 2010; 9: 1740-54.
23. Kant S, Kumar A, Singh SM. Fatty acid synthase inhibitor orlistat induces apoptosis in T cell lymphoma: role of cell survival regulatory molecules. Biochim Biophys Acta 2012; 1820: 1764-73.
24. Wang C, Xu CX, Sun MW, Luo DX, Liao DF, Cao DL. Acetyl-CoA carboxylase-alpha inhibitor TOFA induces human cancer cell apoptosis. Biochem Biophys Res Commun 2009; 385: 302-6.
25. Listenberger LL, Han XL, Lewis SE, Cases S, Farese RV, Ory DS, et al. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci U S A 2003; 100: 3077-82.
26. Nolan CJ, Larter CZ. Lipotoxicity: why do saturated fatty acids cause and monounsaturates protect against it? J Gastroenterol Hepatol 2009; 24: 703-6.
27. Sellick CA, Hansen R, Maqsood AR, Dunn WB, Stephens GM, Goodacre R, et al. Effective quenching processes for physiologically valid metabolite profiling of suspension cultured mammalian cells. Anal Chem 2009; 81: 174-83.
28. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37: 911-7.
29. Wu H, Southam AD, Hines A, Viant MR. High-throughput tissue extraction protocol for NMR- and MS-based metabolomics. Anal Biochem 2008; 372: 204-12.
30. Southam AD, Payne TG, Cooper HJ, Arvanitis TN, Viant MR. Dynamic range and mass accuracy of wide-scan direct infusion nanoelectrospray Fourier transform ion cyclotron resonance mass spectrometry-based meta-bolomics increased by the spectral stitching method. Anal Chem 2007; 79: 4595-602.
31. Payne TG, Southam AD, Arvanitis TN, Viant MR. A signal filtering method for improved quantification and noise discrimination in fourier transform ion cyclotron resonance mass spectrometry-based metabolomics data. J Am Soc Mass Spectrom 2009; 20: 1087-95.
32. Dieterle F, Ross A, Schlotterbeck G, Senn H. Probabilistic quotient nor-malizationas robust method to account for dilution of complex biological mixtures. Application in H-1 NMR metabonomics. Anal Chem 2006; 78: 4281-90.
33. Parsons HM, Ludwig C, Gunther UL, Viant MR. Improved classification accuracy in 1-and 2-dimensional NMR metabolomics data using the variance stabilising generalised logarithm transformation. BMC Bioinform 2007; 8: 16.
34. Weber RJM, Viant MR. MI-Pack: increased confidence of metabolite identification in mass spectra by integrating accurate masses and metabolic pathways. Chemometrics Intell Lab Syst 2010; 104: 75-82.
35. Briaud I, Harmon JS, Kelpe CL, Segu VBG, Poitout V. Lipotoxicity of the pancreatic beta-cell is associated with glucose-dependent esterification of fatty acids into neutral lipids. Diabetes 2001; 50: 315-21.
36. Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 1995; 57: 289-300.
37. Lozzio CB, Lozzio BB. Human chronic myelogenous leukemia cell-line with positive philadelphia chromosome. Blood 1975; 45: 321-34.
38. Collins SJ, Gallo RC, Gallagher RE. Continuous growth and differentiation of human myeloid leukemic-cellsinsuspension culture. Nature 1977; 270: 347-9.
39. Mason P, Liang B, Li L, Fremgen T, Murphy E, Quinn A, et al. SCD1 inhibition causes cancer cell death by depleting mono-unsaturated fatty acids. PLoS ONE 2012; 7: e33823.
40. Roongta UV, Pabalan JG, Wang X, Ryseck R-P, Fargnoli J, Henley BJ, et al. Cancer cell dependence on unsaturated fatty acids implicates stearoyl-CoA desaturase as a target for cancer therapy. Mol Cancer Res 2011; 9: 1551-61.
41. Wei Y, Wang D, Topczewski F, Pagliassotti MJ. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol Endocrinol Metab 2006; 291: E275-E81.
42. Matsui H, Yokoyama T, Sekiguchi K, Iijima D, Sunaga H, Maniwa M, et al. Stearoyl-CoA desaturase-1 (SCD1) augments saturated fatty acid-induced lipid accumulation and inhibits apoptosis in cardiac myocytes. PLoS ONE 2012; 7: 13.
43. Cunnane SC The conditional nature of the dietary need for polyunsaturates: a proposal to reclassify èssential fatty acids' as 'conditionally-indispensable' or conditionally-dispensable' fatty acids. Br J Nutr 2000; 84: 803-12.
44. Rysman E, Brusselmans K, Scheys K, Timmermans L, Derua R, Munck S, et al. De novo lipogenesis protects cancer cells from free radicals and chemotherapeutics by promoting membrane lipid saturation. Cancer Res 2010; 70: 8117-26.
45. Hess D, Chisholm JW, Igal RA. Inhibition of stearoylCoA desaturase activity blocks cell cycle progression and induces programmed cell death in lung cancer cells. PLoS ONE 2010; 5: 8.
46. Scaglia N, Chisholm JW, Igal RA. Inhibition of stearoylCoA desaturase-1 inactivates acetyl-CoA carboxylase and impairs proliferation in cancer cells: role of AMPK. PLoS ONE 2009; 4: e6812.
47. von Roemeling CA, Marlow LA, Wei JJ, Cooper SJ, Caulfield TR, Wu K, et al. Stearoyl-CoA desaturase 1 is a novel molecular therapeutic target for clear cell renal cell carcinoma. Clin Cancer Res 2013; 19: 2368-80.
48. Williams KJ, Argus JP, Zhu Y, Wilks MQ, Marbois BN, York AG, et al. An essential requirement for the SCAP/SREBP signaling axis to protect cancer cells from lipotoxicity. Cancer Res 2013; 73: 2850-62.
49. Listenberger LL, Ory DS, Schaffer JE. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J Biol Chem 2001; 276: 14890-5.
50. Malhotra JD, Miao H, Zhang K, Wolfson A, Pennathur S, Pipe SW, et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc Natl Acad Sci U S A 2008; 105: 18525-30.