Regulation of HIF-1α signaling and chemoresistance in acute lymphocytic leukemia under hypoxic conditions of the bone marrow microenvironment

References

• Kantarjian HM, O’Brien S, Smith TL, Cortes J, Giles FJ, Beran M, et al. Results of treatment with hyper-CVAD, a dose-intensive regimen, in adult acute lymphocytic leukemia. J Clin Oncol 2000; 18:547 - 61; PMID: 10653870
   PubMed Web of Science ®Google Scholar
• Bassan R, Spinelli O, Oldani E, Intermesoli T, Tosi M, Peruta B, et al. Improved risk classification for risk-specific therapy based on the molecular study of minimal residual disease (MRD) in adult acute lymphoblastic leukemia (ALL). Blood 2009; 113:4153 - 62; http://dx.doi.org/10.1182/blood-2008-11-185132; PMID: 19141862
   PubMed Web of Science ®Google Scholar
• Konopleva M, Konoplev S, Hu W, Zaritskey AY, Afanasiev BV, Andreeff M. Stromal cells prevent apoptosis of AML cells by up-regulation of anti-apoptotic proteins. Leukemia 2002; 16:1713 - 24; http://dx.doi.org/10.1038/sj.leu.2402608; PMID: 12200686
   PubMed Web of Science ®Google Scholar
• Tabe Y, Konopleva M, Munsell MF, Marini FC, Zompetta C, McQueen T, et al. PML-RARalpha is associated with leptin-receptor induction: the role of mesenchymal stem cell-derived adipocytes in APL cell survival. Blood 2004; 103:1815 - 22; http://dx.doi.org/10.1182/blood-2003-03-0802; PMID: 14630813
   PubMed Web of Science ®Google Scholar
• Iwamoto S, Mihara K, Downing JR, Pui CH, Campana D. Mesenchymal cells regulate the response of acute lymphoblastic leukemia cells to asparaginase. Clin Cancer Res 2008; •••:14; PMID: 18172247
   PubMed Web of Science ®Google Scholar
• Manabe A, Coustan-Smith E, Behm FG, Raimondi SC, Campana D. Bone marrow-derived stromal cells prevent apoptotic cell death in B-lineage acute lymphoblastic leukemia. Blood 1992; 79:2370 - 7; PMID: 1373973
   PubMed Web of Science ®Google Scholar
• Kumagai MA, Manabe A, Pui CH, Behm FG, Raimondi SC, Hancock ML, et al. Stroma-supported culture in childhood B-lineage acute lymphoblastic leukemia cells predicts treatment outcome. J Clin Invest 1996; 97:755 - 60; http://dx.doi.org/10.1172/JCI118474; PMID: 8609232
   PubMed Web of Science ®Google Scholar
• Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 2007; 104:5431 - 6; http://dx.doi.org/10.1073/pnas.0701152104; PMID: 17374716
   PubMed Web of Science ®Google Scholar
• Mortensen BT, Jensen PO, Helledie N, Iversen PO, Ralfkiaer E, Larsen JK, et al. Changing bone marrow micro-environment during development of acute myeloid leukaemia in rats. Br J Haematol 1998; 102:458 - 64; http://dx.doi.org/10.1046/j.1365-2141.1998.00801.x; PMID: 9695960
   PubMed Web of Science ®Google Scholar
• Benito J, Shi YX, Szymanska B, Carol H, Boehm I, Lu HB, et al. Pronounced hypoxia in models of murine and human leukemia: high efficacy of hypoxia-activated prodrug PR-104. PLoS One 2011; 6:e23108; http://dx.doi.org/10.1371/journal.pone.0023108; PMID: 21853076
   PubMed Web of Science ®Google Scholar
• Wellmann S, Guschmann M, Griethe W, Eckert C, von Stackelberg A, Lottaz C, et al. Activation of the HIF pathway in childhood ALL, prognostic implications of VEGF. Leukemia 2004; 18:926 - 33; http://dx.doi.org/10.1038/sj.leu.2403332; PMID: 15014526
   PubMed Web of Science ®Google Scholar
• Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 1995; 92:5510 - 4; http://dx.doi.org/10.1073/pnas.92.12.5510; PMID: 7539918
   PubMed Web of Science ®Google Scholar
• Jiang BH, Semenza GL, Bauer C, Marti HH. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am J Physiol 1996; 271:C1172 - 80; PMID: 8897823
   PubMed Web of Science ®Google Scholar
• Gottlieb E, Armour SM, Thompson CB. Mitochondrial respiratory control is lost during growth factor deprivation. Proc Natl Acad Sci U S A 2002; 99:12801 - 6; http://dx.doi.org/10.1073/pnas.202477599; PMID: 12228733
   PubMed Web of Science ®Google Scholar
• 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. Mol Cell 2000; 6:683 - 92; http://dx.doi.org/10.1016/S1097-2765(00)00066-6; PMID: 11030347
   PubMed Web of Science ®Google Scholar
• Vander Heiden MG, Plas DR, Rathmell JC, Fox CJ, Harris MH, Thompson CB. Growth factors can influence cell growth and survival through effects on glucose metabolism. Mol Cell Biol 2001; 21:5899 - 912; http://dx.doi.org/10.1128/MCB.21.17.5899-5912.2001; PMID: 11486029
   PubMed Web of Science ®Google Scholar
• Lugthart S, Cheok MH, den Boer ML, Yang W, Holleman A, Cheng C, et al. Identification of genes associated with chemotherapy crossresistance and treatment response in childhood acute lymphoblastic leukemia. Cancer Cell 2005; 7:375 - 86; http://dx.doi.org/10.1016/j.ccr.2005.03.002; PMID: 15837626
   PubMed Web of Science ®Google Scholar
• Pouysségur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006; 441:437 - 43; http://dx.doi.org/10.1038/nature04871; PMID: 16724055
   PubMed Web of Science ®Google Scholar
• Kallio PJ, Wilson WJ, O’Brien S, Makino Y, Poellinger L. Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J Biol Chem 1999; 274:6519 - 25; http://dx.doi.org/10.1074/jbc.274.10.6519; PMID: 10037745
   PubMed Web of Science ®Google Scholar
• Das F, Ghosh-Choudhury N, Dey N, Mandal CC, Mahimainathan L, Kasinath BS, et al. Unrestrained mammalian target of rapamycin complexes 1 and 2 increase expression of phosphatase and tensin homolog deleted on chromosome 10 to regulate phosphorylation of Akt kinase. J Biol Chem 2012; 287:3808 - 22; http://dx.doi.org/10.1074/jbc.M111.246397; PMID: 22184110
   PubMed Web of Science ®Google Scholar
• Mottet D, Dumont V, Deccache Y, Demazy C, Ninane N, Raes M, et al. Regulation of hypoxia-inducible factor-1alpha protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta pathway in HepG2 cells. J Biol Chem 2003; 278:31277 - 85; http://dx.doi.org/10.1074/jbc.M300763200; PMID: 12764143
   PubMed Web of Science ®Google Scholar
• Stiehl DP, Jelkmann W, Wenger RH, Hellwig-Bürgel T. Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett 2002; 512:157 - 62; http://dx.doi.org/10.1016/S0014-5793(02)02247-0; PMID: 11852072
   PubMed Web of Science ®Google Scholar
• Majumder PK, Febbo PG, Bikoff R, Berger R, Xue Q, McMahon LM, et al. mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways. Nat Med 2004; 10:594 - 601; http://dx.doi.org/10.1038/nm1052; PMID: 15156201
   PubMed Web of Science ®Google Scholar
• Brugarolas J, Kaelin WG Jr.. Dysregulation of HIF and VEGF is a unifying feature of the familial hamartoma syndromes. Cancer Cell 2004; 6:7 - 10; http://dx.doi.org/10.1016/j.ccr.2004.06.020; PMID: 15261137
   PubMed Web of Science ®Google Scholar
• Dekanty A, Lavista-Llanos S, Irisarri M, Oldham S, Wappner P. The insulin-PI3K/TOR pathway induces a HIF-dependent transcriptional response in Drosophila by promoting nuclear localization of HIF-alpha/Sima. J Cell Sci 2005; 118:5431 - 41; http://dx.doi.org/10.1242/jcs.02648; PMID: 16278294
   PubMed Web of Science ®Google Scholar
• Xu R-H, Pelicano H, Zhang H, Giles FJ, Keating MJ, Huang P. Synergistic effect of targeting mTOR by rapamycin and depleting ATP by inhibition of glycolysis in lymphoma and leukemia cells. Leukemia 2005; 19:2153 - 8; http://dx.doi.org/10.1038/sj.leu.2403968; PMID: 16193082
   PubMed Web of Science ®Google Scholar
• Teachey DT, Obzut DA, Cooperman J, Fang J, Carroll M, Choi JK, et al. The mTOR inhibitor CCI-779 induces apoptosis and inhibits growth in preclinical models of primary adult human ALL. Blood 2006; 107:1149 - 55; http://dx.doi.org/10.1182/blood-2005-05-1935; PMID: 16195324
   PubMed Web of Science ®Google Scholar
• Lock RB, Liem N, Farnsworth ML, Milross CG, Xue C, Tajbakhsh M, et al. The nonobese diabetic/severe combined immunodeficient (NOD/SCID) mouse model of childhood acute lymphoblastic leukemia reveals intrinsic differences in biologic characteristics at diagnosis and relapse. Blood 2002; 99:4100 - 8; http://dx.doi.org/10.1182/blood.V99.11.4100; PMID: 12010813
   PubMed Web of Science ®Google Scholar
• Zeng Z, Sarbassov D, Samudio IJ, Yee KW, Munsell MF, Ellen Jackson C, et al. Rapamycin derivatives reduce mTORC2 signaling and inhibit AKT activation in AML. Blood 2007; 109:3509 - 12; http://dx.doi.org/10.1182/blood-2006-06-030833; PMID: 17179228
   PubMed Web of Science ®Google Scholar
• Tibes R, Qiu Y, Lu Y, Hennessy B, Andreeff M, Mills GB, et al. Reverse phase protein array: validation of a novel proteomic technology and utility for analysis of primary leukemia specimens and hematopoietic stem cells. Mol Cancer Ther 2006; 5:2512 - 21; http://dx.doi.org/10.1158/1535-7163.MCT-06-0334; PMID: 17041095
   PubMed Web of Science ®Google Scholar
• Noonan KE, Beck C, Holzmayer TA, Chin JE, Wunder JS, Andrulis IL, et al. Quantitative analysis of MDR1 (multidrug resistance) gene expression in human tumors by polymerase chain reaction. Proc Natl Acad Sci U S A 1990; 87:7160 - 4; http://dx.doi.org/10.1073/pnas.87.18.7160; PMID: 1976252
   PubMed Web of Science ®Google Scholar
• Kornblau SM, Tibes R, Qiu YH, Chen W, Kantarjian HM, Andreeff M, et al. Functional proteomic profiling of AML predicts response and survival. Blood 2009; 113:154 - 64; http://dx.doi.org/10.1182/blood-2007-10-119438; PMID: 18840713
   PubMed Web of Science ®Google Scholar
• Lee K, Qian DZ, Rey S, Wei H, Liu JO, Semenza GL. Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells. Proc Natl Acad Sci U S A 2009; 106:2353 - 8; http://dx.doi.org/10.1073/pnas.0812801106; PMID: 19168635
   PubMed Web of Science ®Google Scholar
• Greenberger LM, Horak ID, Filpula D, Sapra P, Westergaard M, Frydenlund HF, et al. A RNA antagonist of hypoxia-inducible factor-1alpha, EZN-2968, inhibits tumor cell growth. Mol Cancer Ther 2008; 7:3598 - 608; http://dx.doi.org/10.1158/1535-7163.MCT-08-0510; PMID: 18974394
   PubMed Web of Science ®Google Scholar
• Rey S, Lee K, Wang CJ, Gupta K, Chen SP, McMillan A, et al. Synergistic effect of HIF-1alpha gene therapy and HIF-1-activated bone marrow-derived angiogenic cells in a mouse model of limb ischemia. Proc Natl Acad Sci U S A 2009; 106:20399 - 404; http://dx.doi.org/10.1073/pnas.0911921106; PMID: 19948968
   PubMed Web of Science ®Google Scholar
• Manabe A, Coustan-Smith E, Behm FG, Raimondi SC, Campana D. Bone marrow-derived stromal cells prevent apoptotic cell death in B-lineage acute lymphoblastic leukemia. Blood 1992; 79:2370 - 7; PMID: 1373973
   PubMed Web of Science ®Google Scholar
• Land SC, Tee AR. Hypoxia-inducible factor 1alpha is regulated by the mammalian target of rapamycin (mTOR) via an mTOR signaling motif. J Biol Chem 2007; 282:20534 - 43; http://dx.doi.org/10.1074/jbc.M611782200; PMID: 17502379
   PubMed Web of Science ®Google Scholar
• Görlach A, Camenisch G, Kvietikova I, Vogt L, Wenger RH, Gassmann M. Efficient translation of mouse hypoxia-inducible factor-1alpha under normoxic and hypoxic conditions. Biochim Biophys Acta 2000; 1493:125 - 34; PMID: 10978514
   PubMed Web of Science ®Google Scholar
• Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, et al. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006; 22:159 - 68; http://dx.doi.org/10.1016/j.molcel.2006.03.029; PMID: 16603397
   PubMed Web of Science ®Google Scholar
• Fiegl M, Samudio I, Clise-Dwyer K, Burks JK, Mnjoyan Z, Andreeff M. CXCR4 expression and biologic activity in acute myeloid leukemia are dependent on oxygen partial pressure. Blood 2009; 113:1504 - 12; http://dx.doi.org/10.1182/blood-2008-06-161539; PMID: 18957686
   PubMed Web of Science ®Google Scholar
• Azab AK, Hu J, Quang P, Azab F, Pitsillides C, Awwad R, et al. Hypoxia promotes dissemination of multiple myeloma through acquisition of endothelial to mesenchymal transition-like features. Blood 2012; http://dx.doi.org/10.1182/blood-2011-09-380410; PMID: 22394600
   PubMed Web of Science ®Google Scholar
• Eliasson P, Rehn M, Hammar P, Larsson P, Sirenko O, Flippin LA, et al. Hypoxia mediates low cell-cycle activity and increases the proportion of long-term-reconstituting hematopoietic stem cells during in vitro culture. Exp Hematol 2010; 38:301 - 10, e2; http://dx.doi.org/10.1016/j.exphem.2010.01.005; PMID: 20138114
   PubMed Web of Science ®Google Scholar
• Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, et al. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 2010; 7:391 - 402; http://dx.doi.org/10.1016/j.stem.2010.06.020; PMID: 20804974
   PubMed Web of Science ®Google Scholar
• Wang Y, Liu Y, Malek SN, Zheng P, Liu Y. Targeting HIF1α eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 2011; 8:399 - 411; http://dx.doi.org/10.1016/j.stem.2011.02.006; PMID: 21474104
   PubMed Web of Science ®Google Scholar
• Gutierrez A, Sanda T, Grebliunaite R, Carracedo A, Salmena L, Ahn Y, et al. High frequency of PTEN, PI3K, and AKT abnormalities in T-cell acute lymphoblastic leukemia. Blood 2009; 114:647 - 50; http://dx.doi.org/10.1182/blood-2009-02-206722; PMID: 19458356
   PubMed Web of Science ®Google Scholar
• Remke M, Pfister S, Kox C, Toedt G, Becker N, Benner A, et al. High-resolution genomic profiling of childhood T-ALL reveals frequent copy-number alterations affecting the TGF-beta and PI3K-AKT pathways and deletions at 6q15-16.1 as a genomic marker for unfavorable early treatment response. Blood 2009; 114:1053 - 62; http://dx.doi.org/10.1182/blood-2008-10-186536; PMID: 19406988
   PubMed Web of Science ®Google Scholar
• Tabe Y, Jin L, Tsutsumi-Ishii Y, Xu Y, McQueen T, Priebe W, et al. Activation of integrin-linked kinase is a critical prosurvival pathway induced in leukemic cells by bone marrow-derived stromal cells. Cancer Res 2007; 67:684 - 94; http://dx.doi.org/10.1158/0008-5472.CAN-06-3166; PMID: 17234779
   PubMed Web of Science ®Google Scholar
• Mathupala SP, Ko YH, Pedersen PL. Hexokinase II: cancer’s double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 2006; 25:4777 - 86; http://dx.doi.org/10.1038/sj.onc.1209603; PMID: 16892090
   PubMed Web of Science ®Google Scholar
• Yee KW, Zeng Z, Konopleva M, Verstovsek S, Ravandi F, Ferrajoli A, et al. Phase I/II study of the mammalian target of rapamycin inhibitor everolimus (RAD001) in patients with relapsed or refractory hematologic malignancies. Clin Cancer Res 2006; 12:5165 - 73; http://dx.doi.org/10.1158/1078-0432.CCR-06-0764; PMID: 16951235
   PubMed Web of Science ®Google Scholar
• Semenza GL. Evaluation of HIF-1 inhibitors as anticancer agents. Drug Discov Today 2007; 12:853 - 9; http://dx.doi.org/10.1016/j.drudis.2007.08.006; PMID: 17933687
   PubMed Web of Science ®Google Scholar
• Maher JC, Krishan A, Lampidis TJ. Greater cell cycle inhibition and cytotoxicity induced by 2-deoxy-D-glucose in tumor cells treated under hypoxic vs aerobic conditions. Cancer Chemother Pharmacol 2004; 53:116 - 22; http://dx.doi.org/10.1007/s00280-003-0724-7; PMID: 14605866
   PubMed Web of Science ®Google Scholar