Influence of cancer metabolism on the therapy of childhood leukaemia

1. Stary J, Zimmermann M, Campbell M, et al. Intensive chemotherapy for childhood acute lymphoblastic leukemia: Results of the randomized intercontinental trial ALL IC-BFM 2002. J Clin Oncol 2014;32(3):174–184.

2. Pession A, Valsecchi MG, Masera G, et al. Long-term results of a randomized trial on extended use of high dose L-asparaginase for standard risk childhood acute lymphoblastic leukemia. J Clin Oncol 2005;23(28):7161–7167.

3. Silverman LB, Gelber RD, Dalton VK, et al. Improved outcome for children with acute lymphoblastic leukemia: results of Dana-Farber Consortium Protocol 91-01. Blood 2001;97(5):1211–1219.

4. Kaspers GJ, Pieters R, Van Zantwijk CH, et al. Prednisolone resistance in childhood acute lymphoblastic leukemia: vitro-vivo correlations and cross-resistance to other drugs. Blood 1998;92(1):259–266.

5. Appel IM, Kazemier KM, Boos J, et al. Pharmacokinetic, pharmacodynamic and intracellular effects of PEG-asparaginase in newly diagnosed childhood acute lymphoblastic leukemia: results from a single agent window study. Leuk Off. J Leuk Soc Am Leuk Res Fund, 2008;22(9):1665–1679.

6. Krasotkina J, Borisova A, Gervaziev YV, Sokolov NN. One-step purification and kinetic properties of the recombinant L-asparaginase from Erwinia carotovora. Enzyme 2004;221:215–221.

7. Offman MN, Krol M, Patel N, et al. Rational engineering of L-asparaginase reveals importance of dual activity for cancer cell toxicity Rational engineering of L-asparaginase reveals importance of dual activity for cancer cell toxicity. Protein Eng 2012;117(5):1614–1621.

8. Chan WK, Lorenzi PL, Anishkin A, et al. The glutaminase activity of L- Asparaginase is not required for anticancer activity against ASNS-negative cells. Blood 2014;123(23):3596–3606.

9. Ohnuma T, Holland JF, Freeman A, Sinks LF. Biochemical and pharmacological studies with asparaginase in man biochemical in man and pharmacological studies with asparaginase. Cancer Res 1970;30:2297–2305.

10. Holleman A, Cheok MH, den Boer ML, et al. Gene-expression patterns in drug-resistant acute lymphoblastic leukemia cells and response to treatment. N Engl J Med 2004;351(6):533–542.

11. Ramakers-van Woerden NL, Pieters R, Loonen AH, et al. TEL/AML1 gene fusion is related to in vitro drug sensitivity for L-asparaginase in childhood acute lymphoblastic leukemia. Blood 2000;96(3):1094–1099.

12. Krejci O, Starkova J, Otova B, et al. Upregulation of asparagine synthetase fails to avert cell cycle arrest induced by L-asparaginase in TEL/AML1-positive leukaemic cells. Leukemia 2004;18(3):434–441.

13. Stams WAG, den Boer ML, Beverloo HB, et al. Sensitivity to L-asparaginase is not associated with expression levels of asparagine synthetase in t(12;21)+ pediatric ALL. Blood 2003;101(7):2743–2747.

14. Fine BM, Kaspers GJL, Ho M, Loonen AH, Boxer LM. A genome-wide view of the in vitro response to L-asparaginase in acute lymphoblastic leukemia. Cancer Res 2005;65(1):291–299.

15. Tanfous M Ben, Sharif-Askari B, Ceppi F, et al. Polymorphisms of asparaginase pathway and asparaginase-related complications in children with acute lymphoblastic leukemia. Clin Cancer Res 2015;21(2):329–334.

16. Bunpo P, Dudley A, Cundiff JK, et al. GCN2 protein kinase is required to activate amino acid deprivation responses in mice treated with the anti-cancer agent L-asparaginase. J Biol Chem 2009;284(47):32742–32749.

17. Wilson GJ, Bunpo P, Cundiff JK, Wek RC, Anthony TG. The eukaryotic initiation factor 2 kinase GCN2 protects against hepatotoxicity during asparaginase treatment. Am J Physiol Endocrinol Metab 2013;305(9):E1124–1133.

18. Patel N, Krishnan S, Offman MN, et al. A dyad of lymphoblastic lysosomal cysteine proteases degrades the antileukemic drug L-asparaginase. J Clin Invest 2009;119(7):1964–1973.

19. van der Meer LT, Waanders E, Levers M, et al. A germ line mutation in cathepsin B points toward a role in asparaginase pharmacokinetics. Blood 2014;124(19):3027–3029.

20. Iwamoto S, Mihara K. Mesenchymal cells regulate the response of acute lymphoblastic leukemia cells to asparaginase. J Clin Invest 2007;117(4):1049–1057.

21. Tong WH, Pieters R, Hop WCJ, et al. No evidence of increased asparagine levels in the bone marrow of patients with acute lymphoblastic leukemia during asparaginase therapy. Pediatr Blood Cancer 2013;60(2):258–261.

22. Ehsanipour EA, Sheng X, Behan JW, et al. Adipocytes cause leukemia cell resistance to L-asparaginase via release of glutamine. Cancer Res 2013;73(10):2998–3006.

23. Willems L, Jacque N, Jacquel A, et al. Inhibiting glutamine uptake represents an attractive new strategy for treating acute myeloid leukemia Inhibiting glutamine uptake represents an attractive new strategy for treating acute myeloid leukemia. Blood 2013;122(20):3521–3532.

24. McCredie KB, Ho DH, Freireich EJ. L-asparaginase for the treatment of cancer. CA Cancer J Clin 1973;23(4):220–227.

25. Lorenzi PL, Llamas J, Gunsior M, et al. Asparagine synthetase is a predictive biomarker of L-asparaginase activity in ovarian cancer cell lines. Mol Cancer Ther 2008;7(10):3123–3128.

26. Lorenzi PL, Reinhold WC, Rudelius M, et al. Asparagine synthetase as a causal, predictive biomarker for L-asparaginase activity in ovarian cancer cells. Mol Cancer Ther 2006;5(11):2613–2623.

27. Hays JL, Kim G, Walker A, et al. A phase II clinical trial of polyethylene glycol-conjugated L-asparaginase in patients with advanced ovarian cancer: Early closure for safety. Mol Clin Oncol 2013;1(3):565–569.

28. Panosyan EH, Wang Y, Xia P, et al. Asparagine depletion potentiates the cytotoxic effect of chemotherapy against brain tumors. Mol Cancer Res 2014;12(5):694–702.

29. Tardito S, Chiu M, Uggeri J, et al. L-Asparaginase and inhibitors of glutamine synthetase disclose glutamine addiction of β-catenin-mutated human hepatocellular carcinoma cells. Curr Cancer Drug Targets 2011;11(8):929–943.

30. Sircar K, Huang H, Hu L, et al. Integrative molecular profiling reveals asparagine synthetase is a target in castration-resistant prostate cancer. Am J Pathol 2012;180(3):895–903.

31. Dufour E, Gay F, Aguera K, et al. Pancreatic tumor sensitivity to plasma L-asparagine starvation. Pancreas 2012;41(6):940–948.

32. Hanahan D, Weinberg RAA. Hallmarks of cancer: The next generation. Cell 2011;144(5):646–674.

33. Lum JJ, Bui T, Gruber M, et al. The transcription factor HIF-1 plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes Dev 2007;21(9):1037–1049.

34. Rathmell JC, Vander Heiden MG, Harris MH, Frauwirth KA, Thompson CB. In the absence of extrinsic signals, nutrient utilization by lymphocytes is insufficient to maintain either cell size or viability found to result in a large accumulation of small atrophic. Mol Cell 2000;6:683–692.

35. Palomero T, Sulis ML, Cortina M, et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat Med 2007;13(10):1203–1210.

36. Gutierrez A, Sanda T, Grebliunaite R, et al. High frequency of PTEN, PI3K, and AKT abnormalities in T-cell acute lymphoblastic leukemia. Blood 2009;114(3):647–650.

37. Liu YL, Yan Y, Webster C, et al. Timing of the loss of Pten protein determines disease severity in a mouse model of myeloid malignancy. Blood 2016;127(15):1912–1922.

38. Mavrakis KJ, Wolfe AL, Oricchio E, et al. Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol 2010;12(4):372–379.

39. Haberl S, Haferlach T, Stengel A, et al. MYC rearranged B-cell neoplasms: Impact of genetics on classification. Cancer Genet 2016;209(10):431–439.

40. Deng C, Lipstein MR, Scotto L, et al. Silencing c-Myc translation as a therapeutic strategy through targeting PI3K delta and CK1 epsilon in hematological malignancies. Blood 2017;129(1):88–99.

41. Chiang MY, Wang Q, Gormley AC, et al. High selective pressure for Notch1 mutations that induce Myc in T-cell acute lymphoblastic leukemia. Blood 2016;128(18):2229–2240.

42. Shim H, Dolde C, Lewis BC, et al. c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proc Natl Acad Sci U. S. A. 1997;94(13):6658–6663.

43. Shim H, Chun YS, Lewis BC, Dang C V. A unique glucose-dependent apoptotic pathway induced by c-Myc. Proc Natl Acad Sci 1998;95(4):1511–1516.

44. Li F, Wang Y, Zeller KI, et al. Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Mol Cell Biol 2005;25(14):6225–6234.

45. Xiang Y, Stine ZE, Xia J, et al. Targeted inhibition of tumor-specific glutaminase diminishes cell-autonomous tumorigenesis. J Clin Invest 2015;125(6):2293–2306.

46. Zenz T, Eichhorst B, Busch R, et al. TP53 mutation and survival in chronic lymphocytic leukemia. J Clin Oncol 2010;28(29):4473–4479.

47. Zenz T, Habe S, Denzel T, et al. Detailed analysis of p53 pathway defects in fludarabine-refractory chronic lymphocytic leukemia (CLL): dissecting the contribution of 17p deletion, TP53 mutation, p53-p21 dysfunction, and miR34a in a prospective clinical trial. Blood 2009;114(13):2589–2597.

48. Green DR, Galluzzi L, Kroemer G. Metabolic control of cell death. Science 2014;345(6203):1250256–1250256.

49. Bensaad K, Tsuruta A, Selak MA, et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006;126(1):107–120.

50. Warburg O. On respiratory impairment in cancer cells. Science 1956;124(3215):269–270.

51. Warburg O. On the origin of cancer cells. Science 1956;123(3191):309–314.

52. Moreno-Sánchez R, Rodríguez-Enríquez S, Marín-Hernández A, Saavedra E. Energy metabolism in tumor cells. FEBS J 2007;274(6):1393–1418.

53. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Ann Rev Cell Dev Biol 2011;27(1):441–464.

54. Larrue C, Saland E, Vergez F, et al. Antileukemic activity of 2-deoxy-D-glucose through inhibition of N-linked glycosylation in acute myeloid leukemia with FLT3-ITD or c-KIT mutations. Mol Cancer Ther 2015;14(10):2364–2373.

55. Lobo C, Ruiz-Bellido MA, Aledo JC, et al. Inhibition of glutaminase expression by antisense mRNA decreases growth and tumourigenicity of tumour cells. Biochem J 2000;348 Pt 2:257–261.

56. Gao P, Tchernyshyov I, Chang T-C, et al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 2009;458(7239):762–765.

57. Wang J, Erickson JW, Fuji R, et al. Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. 2010;18(3):207–219.

58. Ricciardi MR, Mirabilii S, Allegretti M, et al. No title. Blood 2015;126(16):1925–1929.

59. Kiriyama Y, Kubota M, Takimoto T, et al. Biochemical characterization of U937 cells resistant to L-asparaginase: the role of asparagine synthetase. Leukemia 1989;3(4):294–297.

60. Zhang J, Fan J, Venneti S, et al. Asparagine plays a critical role in regulating cellular adaptation to glutamine depletion. Mol Cell 2014;56(2):205–218.

61. Saunders EF. The effect of L-asparaginase on the nucleic acid metabolism and cell cycle of human leukemia cells. Blood 1972;39(4):575–580.

62. Whitecar JP, Bodey GP, Hill CS, Samaan NA. Effect of L-asparaginase on carbohydrate metabolism. Metabolism 1970;19(8):581–586.

63. Kessel D, Bosmann HB. Effects of L-asparaginase on protein and glycoprotein synthesis. FEBS Lett 1970;10(2):85–88.

64. Yu M, Henning R, Walker A, et al. L-asparaginase inhibits invasive and angiogenic activity and induces autophagy in ovarian cancer. J Cell Mol Med 2012;16(10):2369–2378.

65. Iiboshi Y, Papst PJ, Hunger SP, Terada N. l-Asparaginase inhibits the rapamycin-targeted signaling pathway. Biochem Biophys Res Commun 1999;260(2):534–539.

66. Hermanova I, Arruabarrena-Aristorena A, Valis K, et al. Pharmacological inhibition of fatty-acid oxidation synergistically enhances the effect of l-asparaginase in childhood ALL cells. Leukemia 2016;30(1):209–218.

67. Estañ MC, Calviño E, Calvo S, et al. Apoptotic efficacy of etomoxir in human acute myeloid leukemia cells. Cooperation with arsenic trioxide and glycolytic inhibitors, and regulation by oxidative stress and protein kinase activities. PLoS One 2014;9(12):e115250.

68. Carracedo A, Cantley LC, Pandolfi PP. Cancer metabolism: fatty acid oxidation in the limelight. Nat Rev Cancer 2013;13:227–232.

69. Tirado-Vélez JM, Joumady I, Sáez-Benito A, Cózar-Castellano I, Perdomo G. Inhibition of fatty acid metabolism reduces human myeloma cells proliferation. PLoS One 2012;7(9):e46484.

70. 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(6):726–734.

71. Huang J, Das SK, Jha P, et al. The PPAR agonist fenofibrate suppresses B-cell lymphoma in mice by modulating lipid metabolism. Biochim Biophys Acta - Mol Cell Biol Lipids 2013;1831(10):1555–1565.

72. Li J, Zhao S, Zhou X, et al. Inhibition of lipolysis by mercaptoacetate and etomoxir specifically sensitize drug-resistant lung adenocarcinoma cell to paclitaxel. PLoS One 2013;8(9):e74623.

73. Samudio I, Harmancey R, Fiegl M, et al. Pharmacologic inhibition of fatty acid oxidation sensitizes human leukemia cells to apoptosis induction. J Clin Invest 2010;120(1):142–156.

74. Takahashi H, Inoue J, Sakaguchi K, et al. Autophagy is required for cell survival under L-asparaginase-induced metabolic stress in acute lymphoblastic leukemia cells. Oncogene 2017;36(30):4267–4276.

75. Shinohara H, Kumazaki M, Minami Y, et al. Perturbation of energy metabolism by fatty-acid derivative AIC-47 and imatinib in BCR-ABL-harboring leukemic cells. Cancer Lett 2016;371(1):1–11.

76. Tung S, Shi Y, Wong K, et al. PPARα and fatty acid oxidation mediate glucocorticoid resistance in chronic lymphocytic leukemia. Blood 2013;122(6):969–980.

77. Zaal EA, Wu W, Jansen G, et al. Bortezomib resistance in multiple myeloma is associated with increased serine synthesis. Cancer Metab 2017;5(1):7.