Tyrosine kinase inhibition in leukemia induces an altered metabolic state sensitive to mitochondrial perturbations

Clinical Cancer Research

Volumn 21, Issue 6, 2015, Pages 1360-1372

  Alvarez Calderon, Francesca ^a,b   Gregory, Mark A ^a,b   Pham Danis, Catherine ^a,b   DeRyckere, Deborah ^b,c   Stevens, Brett M ^b   Zaberezhnyy, Vadym ^a,b   Hill, Amanda A ^b,c   Gemta, Lelisa ^a,d   Kumar, Amit ^a   Kumar, Vijay ^a   Wempe, Michael F ^a   Pollyea, Daniel A ^b   Jordan, Craig T ^a,b   Serkova, Natalie J ^b   Graham, Douglas K ^a,b,c   DeGregori, James ^a,b,c  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c Children's Hospital Colorado   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD135 ANTIGEN; COPPER ZINC SUPEROXIDE DISMUTASE; CYTARABINE; DASATINIB; DEOXYGLUCOSE; DIHYDROLIPOAMIDE ACETYLTRANSFERASE; DOXORUBICIN; IMATINIB; LESTAURTINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OLIGOMYCIN; PROTEIN TYROSINE KINASE; PYRUVATE DEHYDROGENASE; QUIZARTINIB; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; STAT5 PROTEIN; ANTINEOPLASTIC AGENT; BCR ABL PROTEIN; DLAT PROTEIN, MOUSE; FLT3 PROTEIN, MOUSE; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; PROTEIN KINASE INHIBITOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE DEHYDROGENASE (NADP+); SMALL INTERFERING RNA; SUPEROXIDE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BLAST CELL CRISIS; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CELL SURVIVAL; CELL VIABILITY; CHRONIC MYELOID LEUKEMIA; CITRIC ACID CYCLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFICACY; DRUG POTENTIATION; DRUG SENSITIZATION; DRUG TARGETING; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; GENE SILENCING; GLUCOSE UTILIZATION; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA; LEUKEMIA CELL LINE; LOW DRUG DOSE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MONOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SURVIVAL TIME; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; METABOLISM; MITOCHONDRION; NONOBESE DIABETIC MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL LINE, TUMOR; DIHYDROLIPOYLLYSINE-RESIDUE ACETYLTRANSFERASE; DISEASE MODELS, ANIMAL; FEMALE; FMS-LIKE TYROSINE KINASE 3; FUSION PROTEINS, BCR-ABL; HUMANS; IMATINIB MESYLATE; KETONE OXIDOREDUCTASES; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; OLIGOMYCINS; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SUPEROXIDES;

EID: 84927583872     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-2146     Document Type: Article

References (49)

1. Deininger MW, Goldman JM, Melo JV. The molecular biology of chronic myeloid leukemia. Blood 2000;96:3343-56.
2. Faderl S, O'Brien S, Pui C-H, Stock W, Wetzler M, Hoelzer D, et al. Adult acute lymphoblastic leukemia: concepts and strategies. Cancer 2010;116:1165-76.
3. Foa R, Vitale A, Vignetti M, Meloni G, Guarini A, De Propris MS, et al. Dasatinib as first-line treatment for adult patients with Philadelphia chromosome-positive acute lymphoblastic leukemia. Blood 2011;118:6521-8.
4. Smith A, Howell D, Patmore R, Jack A, Roman E. Incidence of haematological malignancy by sub-type: a report from the Haematological Malignancy Research Network. Br J Cancer 2011;105:1684-92.
5. Santos FP, Jones D, Qiao W, Cortes JE, Ravandi F, Estey EE, et al. Prognostic value of FLT3 mutations among different cytogenetic subgroups in acute myeloid leukemia. Cancer 2011;117:2145-55.
6. Patel JP, Gönen M, Figueroa ME, Fernandez H, Sun Z, Racevskis J, et al. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N Engl J Med 2012;366:1079-89.
7. Cortes JE, Kantarjian H, Foran JM, Ghirdaladze D, Zodelava M, Borthakur G, et al. Phase I study of quizartinib administered daily to patients with relapsed or refractory acute myeloid leukemia irrespective of FMS-like tyrosine kinase 3-internal tandem duplication status. J Clin Oncol 2013;31:3681-7.
8. Smith BD, Levis M, Beran M, Giles F, Kantarjian H, Berg K, et al. Single-agent CEP-701, a novel FLT3 inhibitor, shows biologic and clinical activity in patients with relapsed or refractory acute myeloid leukemia. Blood 2004;103:3669-76.
9. Knapper S, Burnett AK, Littlewood T, Kell WJ, Agrawal S, Chopra R, et al. A phase 2 trial of the FLT3 inhibitor lestaurtinib (CEP701) as first-line treatment for older patients with acute myeloid leukemia not considered fit for intensive chemotherapy. Blood 2006;108:3262-70.
10. Tennant DA, Durán RV, Boulahbel H, Gottlieb E. Metabolic transformation in cancer. Carcinogenesis 2009;30:1269-80.
11. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029-33.
12. Elstrom RL, Bauer DE, Buzzai M, Karnauskas R, Harris MH, Plas DR, et al. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res 2004;64:3892-9.
13. Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB, Hay N. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev 2001;15:1406-18.
14. Gottschalk S, Anderson N, Hainz C, Eckhardt SG, Serkova NJ. Imatinib (STI571)-mediated changes in glucose metabolism in human leukemia BCR-ABL-positive cells. Clin Cancer Res 2004;10:6661-8.
15. Barnes K, McIntosh E, Whetton AD, Daley GQ, Bentley J, Baldwin SA. Chronic myeloid leukaemia: an investigation into the role of Bcr-Abl-induced abnormalities in glucose transport regulation. Oncogene 2005;24:3257-67.
16. Kominsky DJ, Klawitter J, Brown JL, Boros LG, Melo JV, Eckhardt SG, et al. Abnormalities in glucose uptake and metabolism in imatinib-resistant human BCR-ABL-positive cells. Clin Cancer Res 2009;15:3442-50.
17. Zhao F, Mancuso A, Bui TV, Tong X, Gruber JJ, Swider CR, et al. Imatinib resistance associated with BCR-ABL upregulation is dependent on HIF-1alpha-induced metabolic reprograming. Oncogene 2010;29:2962-72.
18. Kluza J, Jendoubi M, Ballot C, Dammak A, Jonneaux A, Idziorek T, et al. Exploiting mitochondrial dysfunction for effective elimination of imatinib-resistant leukemic cells. PLoS One 2011;6:e21924.
19. Samudio I, Fiegl M, Andreeff M. Mitochondrial uncoupling and the Warburg effect: molecular basis for the reprogramming of cancer cell metabolism. Cancer Res 2009;69:2163-6.
20. 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.
21. Gregory MA, Phang TL, Neviani P, Alvarez-Calderon F, Eide CA, O'Hare T, et al. Wnt/Ca2+/NFAT signaling maintains survival of Ph+ leukemia cells upon inhibition of Bcr-Abl. Cancer Cell 2010;18:74-87.
22. Williams RT, den Besten W, Sherr CJ. Cytokine-dependent imatinib resistance in mouse BCR-ABL+, Arf-null lymphoblastic leukemia. Genes Dev 2007;21:2283-7.
23. Williams RT, Sherr CJ. The INK4-ARF (CDKN2A/B) locus in hematopoiesis and BCR-ABL-induced leukemias. Cold Spring Harb Symp Quant Biol 2008;73:461-7.
24. Roberton AM, Holloway CT, Knight IG, Beechey RB. A comparison of the effects of NN′-dicyclohexylcarbodi-imide, oligomycin A and aurovertin on energy-linked reactions in mitochondria and submitochondrial particles. Biochem J 1968;108:445-56.
25. Symersky J, Pagadala V, Osowski D, Krah A, Meier T, Faraldo-Gomez JD, et al. Structure of the c(10) ring of the yeast mitochondrial ATP synthase in the open conformation. Nat Struct Mol Biol 2012;19:485-91, S1.
26. Daley GQ, Baltimore D. Transformation of an interleukin 3-dependent hematopoietic cell line by the chronic myelogenous leukemia-specific P210bcr/abl protein. Proc Natl Acad Sci U S A 1988;85:9312-6.
27. Brandts CH, Sargin B, Rode M, Biermann C, Lindtner B, Schwable J, et al. Constitutive activation of Akt by Flt3 internal tandem duplications is necessary for increased survival, proliferation, and myeloid transformation. Cancer Res 2005;65:9643-50.
28. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, Parslow D, et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 2007;292:C125-36.
29. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, Capaldi RA. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 2004;64:985-93.
30. de Souza-Pinto NC, Eide L, Hogue BA, Thybo T, Stevnsner T, Seeberg E, et al. Repair of 8-oxodeoxyguanosine lesions in mitochondrial dna depends on the oxoguanine dna glycosylase (OGG1) gene and 8-oxoguanine accumulates in the mitochondrial dna of OGG1-defective mice. Cancer Res 2001;61:5378-81.
31. Gao N, Rahmani M, Dent P, Grant S. 2-Methoxyestradiol-induced apoptosis in human leukemia cells proceeds through a reactive oxygen species and Akt-dependent process. Oncogene 2005;24:3797-809.
32. Chao Q, Sprankle KG, Grotzfeld RM, Lai AG, Carter TA, Velasco AM, et al. Identification of N-(5-tert-butyl-isoxazol-3-yl)-N′-{4-[7-(2-morpholin-4-yl-ethoxy)imidazo[2,1-b][1,3]benzothiazol-2-yl]phenyl}urea dihydrochloride (AC220), a uniquely potent, selective, and efficacious FMS-like tyrosine kinase-3 (FLT3) inhibitor. JMed Chem 2009;52:7808-16.
33. Jobe SM, Wilson KM, Leo L, Raimondi A, Molkentin JD, Lentz SR, et al. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood 2008;111:1257-65.
34. Bonnet S, Archer SL, Allalunis-Turner J, Haromy A, Beaulieu C, Thompson R, et al. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 2007;11:37-51.
35. Anastasiou D, Yu Y, Israelsen WJ, Jiang JK, Boxer MB, Hong BS, et al. Pyruvate kinase M2 activators promote tetramer formation and suppress tumorigenesis. Nat Chem Biol 2012;8:839-47.
36. Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 2002;192:1-15.
37. Barzilai A, Yamamoto K-I. DNA damage responses to oxidative stress. DNA Repair 2004;3:1109-15.
38. Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M, et al. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc Natl Acad Sci U S A 2013;110:5887-92.
39. Bonora M, Bononi A, DeMarchi E, Giorgi C, Lebiedzinska M, Marchi S, et al. Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle 2013;12:674-83.
40. Kinnally KW, Antonsson B. A tale of two mitochondrial channels, MAC and PTP, in apoptosis. Apoptosis 2007;12:857-68.
41. Rasola A, Bernardi P. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 2007;12:815-33.
42. Symersky J, Osowski D, Walters DE, Mueller DM. Oligomycin frames a common drug-binding site in the ATP synthase. Proc Natl Acad Sci U S A 2012;109:13961-5.
43. Wolvetang EJ, Johnson KL, Krauer K, Ralph SJ, Linnane AW. Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett 1994;339:40-4.
44. Santamaria G, Martinez-Diez M, Fabregat I, Cuezva JM. Efficient execution of cell death in non-glycolytic cells requires the generation of ROS controlled by the activity of mitochondrial H+-ATP synthase. Carcinogenesis 2006;27:925-35.
45. Formentini L, Sanchez-Arago M, Sanchez-Cenizo L, Cuezva JM. The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Mol Cell 2012;45:731-42.
46. Johnson KM, Chen X, Boitano A, Swenson L, Opipari AW Jr, Glick GD. Identification and validation of the mitochondrial F1F0-ATPase as the molecular target of the immunomodulatory benzodiazepine Bz-423. Chem Biol 2005;12:485-96.
47. Roesch A, Vultur A, Bogeski I, Wang H, Zimmermann Katharina M, Speicher D, et al. Overcoming intrinsic multidrug resistance in melanoma by blocking the mitochondrial respiratory chain of slow-cycling JARID1B high cells. Cancer Cell 2013;23:811-25.
48. Tennant DA, Durán RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010;10:267-77.
49. 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.