Investigating and targeting chronic lymphocytic leukemia metabolism with the human immunodeficiency virus protease inhibitor ritonavir and metformin

References

• Riches JC, Ramsay AG, Gribben JG. Chronic lymphocytic leukemia: an update on biology and treatment. Curr Oncol Rep 2011;13:379–385.
   PubMedGoogle Scholar
• Jaglowski S, Jones JA. Choosing first-line therapy for chronic lymphocytic leukemia. Expert Rev Anticancer Ther 2011;11: 1379–1390.
   PubMed Web of Science ®Google Scholar
• Brown JR. Final results of a phase I study of idelalisib (GS-1101) a selective inhibitor of PI3Kδ, in patients with relapsed or refractory CLL. J Clin Oncol 2013;31(Suppl.): Abstract 7003.
   Web of Science ®Google Scholar
• O’Brien SM. A phase II study of the selective phosphatidylinositol 3-kinase delta (PI3Kδ) inhibitor idelalisib (GS-1101) in combination with rituximab (R) in treatment-naive patients (pts) ≥ 65 years with chronic lymphocytic leukemia (CLL) or small lymphocytic lymphoma (SLL). J Clin Oncol 2013;31(Suppl.): Abstract 7005.
   Web of Science ®Google Scholar
• Quiroga MP, Balakrishnan K, Kurtova AV, et al. B-cell antigen receptor signaling enhances chronic lymphocytic leukemia cell migration and survival: specific targeting with a novel spleen tyrosine kinase inhibitor, R406. Blood 2009;114:1029–1037.
   PubMed Web of Science ®Google Scholar
• Niedermeier M, Hennessy BT, Knight ZA, et al. Isoform-selective phosphoinositide 3’-kinase inhibitors inhibit CXCR4 signaling and overcome stromal cell-mediated drug resistance in chronic lymphocytic leukemia: a novel therapeutic approach. Blood 2009;113:5549–5557.
   PubMed Web of Science ®Google Scholar
• Byrd JC, Furman RR, Coutre SE, et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N Engl J Med 2013;369:32–42.
   PubMed Web of Science ®Google Scholar
• Brown JR. The treatment of relapsed refractory chronic lymphocytic leukemia. Hematology Am Soc Hematol Educ Program 2011:110–118.
   Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646–674.
   PubMed Web of Science ®Google Scholar
• Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov 2011;10:671–684.
   PubMed Web of Science ®Google Scholar
• Warburg O. On the origin of cancer cells. Science 1956;123: 309–314.
   PubMed Web of Science ®Google Scholar
• Kaida H, Ishibashi M, Yuzuriha M, et al. Glucose transporter expression of an esophageal gastrointestinal tumor detected by F-18 FDG PET/CT. Clin Nucl Med 2010;35:505–509.
   PubMed Web of Science ®Google Scholar
• Chan DA, Sutphin PD, Nguyen P, et al. Targeting GLUT1 and the Warburg effect in renal cell carcinoma by chemical synthetic lethality. Sci Transl Med 2011;3: 94ra70.
   Web of Science ®Google Scholar
• Vera JC, Reyes AM, Carcamo JG, et al. Genistein is a natural inhibitor of hexose and dehydroascorbic acid transport through the glucose transporter, GLUT1. J Biol Chem 1996;271: 8719–8724.
   PubMed Web of Science ®Google Scholar
• Wood TE, Dalili S, Simpson CD, et al. A novel inhibitor of glucose uptake sensitizes cells to FAS-induced cell death. Mol Cancer Ther 2008;7:3546–3555.
   PubMed Web of Science ®Google Scholar
• Pelicano H, Martin DS, Xu RH, et al. Glycolysis inhibition for anticancer treatment. Oncogene 2006;25:4633–4646.
   PubMed Web of Science ®Google Scholar
• Ko YH, Smith BL, Wang Y, et al. Advanced cancers: eradication in all cases using 3-bromopyruvate therapy to deplete ATP. Biochem Biophys Res Commun 2004;324:269–275.
   PubMed Web of Science ®Google Scholar
• McBrayer SK, Cheng JC, Singhal S, et al. Multiple myeloma exhibits novel dependence on GLUT4, GLUT8, and GLUT11: implications for glucose transporter-directed therapy. Blood 2012;119:4686–4697.
   PubMed Web of Science ®Google Scholar
• Murata H, Hruz PW, Mueckler M. The mechanism of insulin resistance caused by HIV protease inhibitor therapy. J Biol Chem 2000;275:20251–20254.
   PubMed Web of Science ®Google Scholar
• Valceckiene V, Kontenyte R, Jakubauskas A, et al. Selection of reference genes for quantitative polymerase chain reaction studies in purified B cells from B cell chronic lymphocytic leukaemia patients. Br J Haematol 2010;151:232–238.
   PubMed Web of Science ®Google Scholar
• Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3: RESEARCH0034.
   PubMed Web of Science ®Google Scholar
• Lee JO, Lee SK, Jung JH, et al. Metformin induces Rab4 through AMPK and modulates GLUT4 translocation in skeletal muscle cells. J Cell Physiol 2011;226:974–981.
   PubMed Web of Science ®Google Scholar
• Liu J, Chen G, Feng L, et al. Loss of p53 and altered miR15-a/16-1short right arrowMCL-1 pathway in CLL: insights from TCL1-Tg:p53 mouse model and primary human leukemia cells. Leukemia 2014;28:118–128.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Altman BJ, Coloff JL, et al. Glycogen synthase kinase 3alpha and 3beta mediate a glucose-sensitive antiapoptotic signaling pathway to stabilize Mcl-1. Mol Cell Biol 2007;27: 4328–4339.
   PubMed Web of Science ®Google Scholar
• Jones RG, Thompson CB. Tumor suppressors and cell metabolism: a recipe for cancer growth. Genes Dev 2009;23:537–548.
   PubMed Web of Science ®Google Scholar
• Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029–1033.
   PubMed Web of Science ®Google Scholar
• Shanmugam M, McBrayer SK, Qian J, et al. Targeting glucose consumption and autophagy in myeloma with the novel nucleoside analogue 8-aminoadenosine. J Biol Chem 2009;284:26816–26830.
   PubMed Web of Science ®Google Scholar
• Xu RH, Pelicano H, Zhou Y, et al. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res 2005;65: 613–621.
   PubMed Web of Science ®Google Scholar
• Bartel TB, Haessler J, Brown TL, et al. F18-fluorodeoxyglucose positron emission tomography in the context of other imaging techniques and prognostic factors in multiple myeloma. Blood 2009;114:2068–2076.
   PubMed Web of Science ®Google Scholar
• Zamagni E, Patriarca F, Nanni C, et al. Prognostic relevance of 18-F FDG PET/CT in newly diagnosed multiple myeloma patients treated with up-front autologous transplantation. Blood 2011;118:5989–5995.
   PubMed Web of Science ®Google Scholar
• Reitzer LJ, Wice BM, Kennell D. The pentose cycle. Control and essential function in HeLa cell nucleic acid synthesis. J Biol Chem 1980;255:5616–5626.
   PubMed Web of Science ®Google Scholar
• Ikezoe T, Hisatake Y, Takeuchi T, et al. HIV-1 protease inhibitor, ritonavir: a potent inhibitor of CYP3A4, enhanced the anticancer effects of docetaxel in androgen-independent prostate cancer cells in vitro and in vivo. Cancer Res 2004;64:7426–7431.
   PubMed Web of Science ®Google Scholar
• Srirangam A, Mitra R, Wang M, et al. Effects of HIV protease inhibitor ritonavir on Akt-regulated cell proliferation in breast cancer. Clin Cancer Res 2006;12:1883–1896.
   PubMed Web of Science ®Google Scholar
• Sato A, Asano T, Ito K. Ritonavir interacts with bortezomib to enhance protein ubiquitination and histone acetylation synergistically in renal cancer cells. Urology 2012;79:966.e913–e921.
   Google Scholar
• Podar K, Gouill SL, Zhang J, et al. A pivotal role for Mcl-1 in bortezomib-induced apoptosis. Oncogene 2008;27:721–731.
   PubMed Web of Science ®Google Scholar
• Mills JR, Hippo Y, Robert F, et al. mTORC1 promotes survival through translational control of Mcl-1. Proc Natl Acad Sci USA 2008;105:10853–10858.
   PubMed Web of Science ®Google Scholar
• Eguchi T, Itadani H, Shimomura T, et al. Expression levels of p18INK4C modify the cellular efficacy of cyclin-dependent kinase inhibitors via regulation of Mcl-1 expression in tumor cell lines. Mol Cancer Ther 2009;8:1460–1472.
   PubMed Web of Science ®Google Scholar
• Nguyen M, Marcellus RC, Roulston A, et al. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc Natl Acad Sci USA 2007;104:19512–19517.
   PubMed Web of Science ®Google Scholar
• Pradelli LA, Beneteau M, Chauvin C, et al. Glycolysis inhibition sensitizes tumor cells to death receptors-induced apoptosis by AMP kinase activation leading to Mcl-1 block in translation. Oncogene 2010;29:1641–1652.
   PubMed Web of Science ®Google Scholar
• Shanmugam M, McBrayer SK, Rosen ST. Targeting the Warburg effect in hematological malignancies: from PET to therapy. Curr Opin Oncol 2009;21:531–536.
   PubMed Web of Science ®Google Scholar
• Altenberg B, Greulich KO. Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes. Genomics 2004;84:1014–1020.
   PubMed Web of Science ®Google Scholar
• Dowling RJ, Niraula S, Stambolic V, et al. Metformin in cancer: translational challenges. J Mol Endocrinol 2012;48:R31–R43.
   PubMed Web of Science ®Google Scholar
• Pollak MN. Investigating metformin for cancer prevention and treatment: the end of the beginning. Cancer Discov 2012;2:778–790.
   PubMed Web of Science ®Google Scholar
• Guigas B, Detaille D, Chauvin C, et al. Metformin inhibits mitochondrial permeability transition and cell death: a pharmacological in vitro study. Biochem J 2004;382:877–884.
   PubMed Web of Science ®Google Scholar
• Phoenix KN, Vumbaca F, Claffey KP. Therapeutic metformin/AMPK activation promotes the angiogenic phenotype in the ERalpha negative MDA-MB-435 breast cancer model. Breast Cancer Res Treat 2009;113:101–111.
   PubMed Web of Science ®Google Scholar
• Liu T, Weinberg JB, Davis ED, et al. The metabolic signature of CLL: enhanced glucose metabolism in a subset of high-risk CLL patients. Blood 2012;120(Suppl. 1): Abstract 1785.
   Google Scholar
• Gardner JR, Devlin S, Knapp K, et al. Aerobic glycolysis predicts outcome in early chronic lymphocytic leukemia. Blood 2012;120(Suppl. 1): Abstract 2482.
   Google Scholar