Resistance to Dasatinib in primary chronic lymphocytic leukemia lymphocytes involves AMPK-mediated energetic reprogramming

Oncotarget

Volumn 4, Issue 12, 2013, Pages 2550-2566

  Marignac, Veronica Martinez ^a   Smith, Sarah ^a   Toban, Nader ^a   Bazile, Miguel ^a   Aloyz, Raquel ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

AMPK; CLL; Dasatinib; eIF4E; Glycolysis; Kinase inhibitor; Metabolism; Metformin; OXPHOS; Signaling

Indexed keywords

ADENOSINE TRIPHOSPHATE; DASATINIB; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; CANCER PROGNOSIS; CHRONIC LYMPHATIC LEUKEMIA; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL (TOPIC); DIABETES MELLITUS; GLUCOSE METABOLISM; GLYCOLYSIS; HUMAN; IN VITRO STUDY; LYMPHOCYTE; MITOCHONDRIAL RESPIRATION; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; SURVIVAL RATE;

AMP-ACTIVATED PROTEIN KINASES; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; COCULTURE TECHNIQUES; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LACTIC ACID; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTES; OXIDATIVE PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84891904194     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: None     Document Type: Article

References (83)

1. Calissano C, Damle RN, Marsilio S, Yan XJ, Yancopoulos S, Hayes G, Emson C, Murphy EJ, Hellerstein MK, Sison C, Kaufman MS, Kolitz JE, Allen SL, et al. Intraclonal complexity in chronic lymphocytic leukemia: fractions enriched in recently born/divided and older/quiescent cells. Mol Med. 2011; 17:1374-1382.
2. Cheson BD, Byrd JC, Rai KR, Kay NE, O'Brien SM, Flinn IW, Wiestner A,Kipps TJ. Novel targeted agents and the need to refine clinical end points in chronic lymphocytic leukemia. Journal of Clinical Oncology. 2012; 30:2820-2822.
3. Lu K,Wang X. Therapeutic advancement of chronic lymphocytic leukemia. J Hematol Oncol. 2012; 5:55.
4. Woyach JA, Johnson AJ,Byrd JC. The B-cell receptor signaling pathway as a therapeutic target in CLL. Blood. 2012; 120:1175-1184.
5. Wierda WG. Current and investigational therapies for patients with CLL. Hematology Am Soc Hematol Educ Program. 2006:285-294.
6. Shanafelt TD. Predicting clinical outcome in CLL: how and why. Hematology Am Soc Hematol Educ Program. 2009:421-429.
7. Eisele L, Haddad T, Sellmann L, Duhrsen U,Durig J. Expression levels of CD38 on leukemic B cells but not on non-leukemic T cells are comparably stable over time and predict the course of disease in patients with chronic lymphocytic leukemia. Leuk Res. 2009; 33:775-778.
8. Cardaci S,Ciriolo MR. TCA Cycle Defects and Cancer: When Metabolism Tunes Redox State. Int J Cell Biol. 2012; 2012:161837.
9. Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov. 2011; 10:671-684.
10. Feron O. Pyruvate into lactate and back: from the Warburg effect to symbiotic energy fuel exchange in cancer cells. Radiother Oncol. 2009; 92:329-333.
11. Del Barco S, Vazquez-Martin A, Cufi S, Oliveras-Ferraros C, Bosch-Barrera J, Joven J, Martin-Castillo B,Menendez JA. Metformin: multi-faceted protection against cancer. Oncotarget. 2011; 2:896-917.
12. van't Veer MB, Brooijmans AM, Langerak AW, Verhaaf B, Goudswaard CS, Graveland WJ, van Lom K,Valk PJ. The predictive value of lipoprotein lipase for survival in chronic lymphocytic leukemia. Haematologica. 2006; 91:56-63.
13. Pallasch CP, Schwamb J, Konigs S, Schulz A, Debey S, Kofler D, Schultze JL, Hallek M, Ultsch A,Wendtner CM. Targeting lipid metabolism by the lipoprotein lipase inhibitor orlistat results in apoptosis of B-cell chronic lymphocytic leukemia cells. Leukemia. 2008; 22:585-592.
14. Spaner DE, Lee E, Shi Y, Wen F, Li Y, Tung S, McCaw L, Wong K, Gary-Gouy H, Dalloul A, Ceddia R,Gorzcynski R. PPAR-alpha is a therapeutic target for chronic lymphocytic leukemia. Leukemia. 2013; 27:1090-1099.
15. Tili E, Michaille JJ, Luo Z, Volinia S, Rassenti LZ, Kipps TJ,Croce CM. The down-regulation of miR-125b in chronic lymphocytic leukemias leads to metabolic adaptation of cells to a transformed state. Blood. 2012; 120:2631-2638.
16. Lemons JM, Feng XJ, Bennett BD, Legesse-Miller A, Johnson EL, Raitman I, Pollina EA, Rabitz HA, Rabinowitz JD,Coller HA. Quiescent fibroblasts exhibit high metabolic activity. PLoS Biol. 2010; 8:e1000514.
17. Ono K, Suzushima H, Watanabe Y, Kikukawa Y, Shimomura T, Furukawa N, Kawaguchi T,Araki E. Rapid amelioration of hyperglycemia facilitated by dasatinib in a chronic myeloid leukemia patient with type 2 diabetes mellitus. Intern Med. 2012; 51:2763-2766.
18. Agostino NM, Chinchilli VM, Lynch CJ, Koszyk-Szewczyk A, Gingrich R, Sivik J,Drabick JJ. Effect of the tyrosine kinase inhibitors (sunitinib, sorafenib, dasatinib, and imatinib) on blood glucose levels in diabetic and nondiabetic patients in general clinical practice. J Oncol Pharm Pract. 2011; 17:197-202.
19. Veneri D, Franchini M,Bonora E. Imatinib and regression of type 2 diabetes. N Engl J Med. 2005; 352:1049-1050.
20. Bohm S, Hess D, Gillessen S,Brandle M. Improved glycemic control with the multi-receptor tyrosine kinase inhibitor pazopanib. Diabetes Care. 2010; 33:e82.
21. Amrein L, Soulieres D, Johnston JB,Aloyz R. p53 and autophagy contribute to dasatinib resistance in primary CLL lymphocytes. Leuk Res. 2011; 35:99-102.
22. Wang X, Eno CO, Altman BJ, Zhu Y, Zhao G, Olberding KE, Rathmell JC,Li C. ER stress modulates cellular metabolism. Biochem J. 2011; 435:285-296.
23. Santos CX, Tanaka LY, Wosniak J,Laurindo FR. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal. 2009; 11:2409-2427.
24. Bellodi C, Lidonnici MR, Hamilton A, Helgason GV, Soliera AR, Ronchetti M, Galavotti S, Young KW, Selmi T,Yacobi R. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. The Journal of clinical investigation. 2009; 119:1109.
25. Hao W, Chang CP, Tsao CC,Xu J. Oligomycin-induced bioenergetic adaptation in cancer cells with heterogeneous bioenergetic organization. J Biol Chem. 2010; 285:12647-12654.
26. Li N, Ragheb K, Lawler G, Sturgis J, Rajwa B, Melendez JA,Robinson JP. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem. 2003; 278:8516-8525.
27. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S,Thompson CB. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proceedings of the National Academy of Sciences. 2007; 104:19345-19350.
28. Reitzer LJ, Wice BM,Kennell D. Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. Journal of Biological Chemistry. 1979; 254:2669-2676.
29. Gupta V,Bamezai RN. Human pyruvate kinase M2: a multifunctional protein. Protein Sci. 2010; 19:2031-2044.
30. Mihaylova MM,Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol. 2011; 13:1016-1023.
31. Wang R,Green DR. Metabolic checkpoints in activated T cells. Nat Immunol. 2012; 13:907-915.
32. Semenza GL. Involvement of hypoxia-inducible factor 1 in human cancer. Intern Med. 2002; 41:79-83.
33. Semenza GL. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE. 2007; 2007:cm8.
34. Semenza GL. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J. 2007; 405:1-9.
35. Dando I, Fiorini C, Pozza ED, Padroni C, Costanzo C, Palmieri M,Donadelli M. UCP2 inhibition triggers ROS-dependent nuclear translocation of GAPDH and autophagic cell death in pancreatic adenocarcinoma cells. Biochim Biophys Acta. 2013; 1833:672-679.
36. Mehta SL,Li PA. Neuroprotective role of mitochondrial uncoupling protein 2 in cerebral stroke. J Cereb Blood Flow Metab. 2009; 29:1069-1078.
37. Plander M, Ugocsai P, Seegers S, Orso E, Reichle A, Schmitz G, Hofstadter F,Brockhoff G. Chronic lymphocytic leukemia cells induce anti-apoptotic effects of bone marrow stroma. Ann Hematol. 90:1381-1390.
38. McNamara CR,Degterev A. Small-molecule inhibitors of the PI3K signaling network. Future Med Chem. 2011; 3:549-565.
39. Bensaad K, Cheung EC,Vousden KH. Modulation of intracellular ROS levels by TIGAR controls autophagy. EMBO J. 2009; 28:3015-3026.
40. Owen MR, Doran E,Halestrap AP. Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J. 2000; 348 Pt 3:607-614.
41. Zhang M, Fu W, Prabhu S, Moore JC, Ko J, Kim JW, Druker BJ, Trapp V, Fruehauf J, Gram H, Fan HY,Ong ST. Inhibition of polysome assembly enhances imatinib activity against chronic myelogenous leukemia and overcomes imatinib resistance. Mol Cell Biol. 2008; 28:6496-6509.
42. Fan S, Li Y, Yue P, Khuri FR,Sun SY. The eIF4E/eIF4G interaction inhibitor 4EGI-1 augments TRAIL-mediated apoptosis through c-FLIP Down-regulation and DR5 induction independent of inhibition of cap-dependent protein translation. Neoplasia. 2010; 12:346-356.
43. Ben Sahra I, Regazzetti C, Robert G, Laurent K, Le Marchand-Brustel Y, Auberger P, Tanti JF, Giorgetti-Peraldi S,Bost F. Metformin, independent of AMPK, induces mTOR inhibition and cell-cycle arrest through REDD1. Cancer Res. 2011; 71:4366-4372.
44. Ben Sahra I, Laurent K, Loubat A, Giorgetti-Peraldi S, Colosetti P, Auberger P, Tanti JF, Le Marchand-Brustel Y,Bost F. The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level. Oncogene. 2008; 27:3576-3586.
45. Kalender A, Selvaraj A, Kim SY, Gulati P, Brule S, Viollet B, Kemp BE, Bardeesy N, Dennis P, Schlager JJ, Marette A, Kozma SC,Thomas G. Metformin, independent of AMPK, inhibits mTORC1 in a rag GTPase-dependent manner. Cell Metab. 2010; 11:390-401.
46. Krejci A. Metabolic sensors and their interplay with cell signalling and transcription. Biochem Soc Trans. 2012; 40:311-323.
47. Zheng J. Energy metabolism of cancer: Glycolysis versus oxidative phosphorylation (Review). Oncol Lett. 2012; 4:1151-1157.
48. Hall A, Meyle KD, Lange MK, Klima M, Sanderhoff M, Dahl C, Abildgaard C, Thorup K, Moghimi SM, Jensen PB, Bartek J, Guldberg P,Christensen C. Dysfunctional oxidative phosphorylation makes malignant melanoma cells addicted to glycolysis driven by the (V600E)BRAF oncogene. Oncotarget. 2013; 4:584-599.
49. Guido C, Whitaker-Menezes D, Lin Z, Pestell RG, Howell A, Zimmers TA, Casimiro MC, Aquila S, Ando S, Martinez-Outschoorn UE, Sotgia F,Lisanti MP. Mitochondrial fission induces glycolytic reprogramming in cancer-associated myofibroblasts, driving stromal lactate production, and early tumor growth. Oncotarget. 2012; 3:798-810.
50. Salem AF, Whitaker-Menezes D, Lin Z, Martinez-Outschoorn UE, Tanowitz HB, Al-Zoubi MS, Howell A, Pestell RG, Sotgia F,Lisanti MP. Two-compartment tumor metabolism: autophagy in the tumor microenvironment and oxidative mitochondrial metabolism (OXPHOS) in cancer cells. Cell Cycle. 2012; 11:2545-2556.
51. Brody JI,Merlie K. Metabolic and biosynthetic features of lymphocytes from patients with diabetes mellitus: similarities to lymphocytes in chronic lymphocytic leukaemia. Br J Haematol. 1970; 19:193-201.
52. Brody JI, Oski FA,Singer DE. Impaired pentose phosphate shunt and decreased glycolytic activity in lymphocytes of chronic lymphocytic leukemia. Metabolic pathway. Blood. 1969; 34:421-429.
53. Galili U, Leizerowitz R, Moreb J, Gamliel H, Gurfel D,Polliack A. Metabolic and ultrastructural aspects of the in vitro lysis of chronic lymphocytic leukemia cells by glucocorticoids. Cancer Res. 1982; 42:1433-1440.
54. Caro P, Kishan AU, Norberg E, Stanley IA, Chapuy B, Ficarro SB, Polak K, Tondera D, Gounarides J, Yin H, Zhou F, Green MR, Chen L, et al. Metabolic signatures uncover distinct targets in molecular subsets of diffuse large B cell lymphoma. Cancer Cell. 2012; 22:547-560.
55. Rousset S, Alves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F,Ricquier D. The biology of mitochondrial uncoupling proteins. Diabetes. 2004; 53 Suppl 1:S130-135.
56. Song Z, Lu P, Furman RR, Leonard JP, Martin P, Tyrell L, Lee FY, Knowles DM, Coleman M,Wang YL. Activities of SYK and PLCgamma2 predict apoptotic response of CLL cells to SRC tyrosine kinase inhibitor dasatinib. Clin Cancer Res. 16:587-599.
57. Will Y, Dykens JA, Nadanaciva S, Hirakawa B, Jamieson J, Marroquin LD, Hynes J, Patyna S,Jessen BA. Effect of the multitargeted tyrosine kinase inhibitors imatinib, dasatinib, sunitinib, and sorafenib on mitochondrial function in isolated rat heart mitochondria and H9c2 cells. Toxicol Sci. 2008; 106:153-161.
58. Mulukutla BC, Khan S, Lange A,Hu WS. Glucose metabolism in mammalian cell culture: new insights for tweaking vintage pathways. Trends Biotechnol. 2010; 28:476-484.
59. Yaktapour N, Ubelhart R, Schuler J, Aumann K, Dierks C, Burger M, Pfeifer D, Jumaa H, Veelken H, Brummer T,Zirlik K. Insulin-like growth factor-1 receptor (IGF1R) as a novel target in chronic lymphocytic leukemia. Blood. 2013; 122:1621-1633.
60. Buentke E, Nordstrom A, Lin H, Bjorklund AC, Laane E, Harada M, Lu L, Tegnebratt T, Stone-Elander S, Heyman M, Soderhall S, Porwit A, Ostenson CG, et al. Glucocorticoid-induced cell death is mediated through reduced glucose metabolism in lymphoid leukemia cells. Blood Cancer J. 2011; 1:e31.
61. Spaner DE. Oral high-dose glucocorticoids and ofatumumab in fludarabine-resistant chronic lymphocytic leukemia. Leukemia. 2012; 26:1144-1145.
62. Tung S, Shi Y, Wong K, Zhu F, Gorczynski R, Laister RC, Minden M, Blechert AK, Genzel Y, Reichl U,Spaner DE. PPARalpha and fatty acid oxidation mediate glucocorticoid resistance in chronic lymphocytic leukemia. Blood. 2013; 122:969-980.
63. O'Neill HM. AMPK and Exercise: Glucose Uptake and Insulin Sensitivity. Diabetes Metab J. 2013; 37:1-21.
64. O'Neill HM, Holloway GP,Steinberg GR. AMPK regulation of fatty acid metabolism and mitochondrial biogenesis: implications for obesity. Mol Cell Endocrinol. 2013; 366:135-151.
65. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA, Bruncko M, Deckwerth TL, Dinges J, Hajduk PJ, Joseph MK, Kitada S, Korsmeyer SJ, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature. 2005; 435:677-681.
66. Giordano A, Calvani M, Petillo O, Grippo P, Tuccillo F, Melone MA, Bonelli P, Calarco A,Peluso G. tBid induces alterations of mitochondrial fatty acid oxidation flux by malonyl-CoA-independent inhibition of carnitine palmitoyltransferase-1. Cell Death Differ. 2005; 12:603-613.
67. Paumen MB, Ishida Y, Han H, Muramatsu M, Eguchi Y, Tsujimoto Y,Honjo T. Direct interaction of the mitochondrial membrane protein carnitine palmitoyltransferase I with Bcl-2. Biochem Biophys Res Commun. 1997; 231:523-525.
68. Amrein PC. The potential for dasatinib in treating chronic lymphocytic leukemia, acute myeloid leukemia, and myeloproliferative neoplasms. Leuk Lymphoma. 2011; 52:754-763.
69. Madan E, Gogna R, Bhatt M, Pati U, Kuppusamy P,Mahdi AA. Regulation of glucose metabolism by p53: emerging new roles for the tumor suppressor. Oncotarget. 2011; 2:948-957.
70. Cosentino C, Grieco D,Costanzo V. ATM activates the pentose phosphate pathway promoting anti-oxidant defence and DNA repair. EMBO J. 2011; 30:546-555.
71. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nature reviews Cancer. 2012; 12:401-410.
72. Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M, Kondo S, Dumont DJ, Gutterman JU, Walker CL, Slingerland JM,Mills GB. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nature Cell Biology. 2007; 9:218-224.
73. Liang JY, Shao SH, Xu ZX, Hennessy B, Ding ZY, Larrea M, Kondo S, Dumont DJ, Gutterman JU, Walker CL, Slingerland JM,Mills GB. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nature Cell Biology. 2007; 9:218-U125.
74. DeBerardinis RJ. Is cancer a disease of abnormal cellular metabolism? New angles on an old idea. Genet Med. 2008; 10:767-777.
75. DeBerardinis RJ, Lum JJ, Hatzivassiliou G,Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008; 7:11-20.
76. Hetz C, Chevet E,Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov. 2013; 12:703-719.
77. Amrein L, Shawi M, Grenier J, Aloyz R,Panasci L. The phosphatidylinositol-3 kinase I inhibitor BKM120 induces cell death in B-chronic lymphocytic leukemia cells in vitro. Int J Cancer. 2013; 133:247-252.
78. Blake DA,McLean NV. A colorimetric assay for the measurement of D-glucose consumption by cultured cells. Anal Biochem. 1989; 177:156-160.
79. Christodoulopoulos G, Muller C, Salles B, Kazmi R,Panasci L. Potentiation of chlorambucil cytotoxicity in B-cell chronic lymphocytic leukemia by inhibition of DNA-dependent protein kinase activity using wortmannin. Cancer Res. 1998; 58:1789-1792.
80. Christodoulopoulos G, Malapetsa A, Schipper H, Golub E, Radding C,Panasci LC. Chlorambucil induction of HsRad51 in B-cell chronic lymphocytic leukemia. Clin Cancer Res. 1999; 5:2178-2184.
81. Bello VE, Aloyz RS, Christodoulopoulos G,Panasci LC. Homologous recombinational repair vis-a-vis chlorambucil resistance in chronic lymphocytic leukemia. Biochem Pharmacol. 2002; 63:1585-1588.
82. Amrein L, Hernandez TA, Ferrario C, Johnston J, Gibson SB, Panasci L,Aloyz R. Dasatinib sensitizes primary chronic lymphocytic leukaemia lymphocytes to chlorambucil and fludarabine in vitro. Br J Haematol. 2008; 143:698-706.
83. Pietrangeli CE, Hayashi S,Kincade PW. Stromal cell lines which support lymphocyte growth: characterization, sensitivity to radiation and responsiveness to growth factors. Eur J Immunol. 1988; 18:863-872.