The PERK-eIF2α phosphorylation arm is a pro-survival pathway of BCR-ABL signaling and confers resistance to imatinib treatment in chronic myeloid leukemia cells

References

• Tassone P, Tagliaferri P, Fulciniti MT, Di Martino MT, Venuta S. Novel therapeutic approaches based on the targeting of microenvironment-derived survival pathways in human cancer: experimental models and translational issues. Curr Pharm Des 2007; 13:487 - 96; http://dx.doi.org/10.2174/138161207780162872; PMID: 17348845
   PubMed Web of Science ®Google Scholar
• Ellgaard L, Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 2003; 4:181 - 91; http://dx.doi.org/10.1038/nrm1052; PMID: 12612637
   PubMed Web of Science ®Google Scholar
• Schröder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74:739 - 89; http://dx.doi.org/10.1146/annurev.biochem.73.011303.074134; PMID: 15952902
   PubMed Web of Science ®Google Scholar
• Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8:519 - 29; http://dx.doi.org/10.1038/nrm2199; PMID: 17565364
   PubMed Web of Science ®Google Scholar
• Ron D. Translational control in the endoplasmic reticulum stress response. J Clin Invest 2002; 110:1383 - 8; PMID: 12438433
   PubMed Web of Science ®Google Scholar
• Wek RC, Jiang HY, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 2006; 34:7 - 11; http://dx.doi.org/10.1042/BST0340007; PMID: 16246168
   PubMed Web of Science ®Google Scholar
• Deng J, Lu PD, Zhang Y, Scheuner D, Kaufman RJ, Sonenberg N, et al. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 2004; 24:10161 - 8; http://dx.doi.org/10.1128/MCB.24.23.10161-10168.2004; PMID: 15542827
   PubMed Web of Science ®Google Scholar
• Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, et al. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol 2003; 23:5651 - 63; http://dx.doi.org/10.1128/MCB.23.16.5651-5663.2003; PMID: 12897138
   PubMed Web of Science ®Google Scholar
• Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, et al. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 2007; 14:230 - 9; http://dx.doi.org/10.1038/sj.cdd.4401984; PMID: 16794605
   PubMed Web of Science ®Google Scholar
• Schönthal AH. Endoplasmic reticulum stress and autophagy as targets for cancer therapy. Cancer Lett 2009; 275:163 - 9; http://dx.doi.org/10.1016/j.canlet.2008.07.005; PMID: 18692955
   PubMed Web of Science ®Google Scholar
• Kurzrock R, Gutterman JU, Talpaz M. The molecular genetics of Philadelphia chromosome-positive leukemias. N Engl J Med 1988; 319:990 - 8; http://dx.doi.org/10.1056/NEJM198810133191506; PMID: 3047582
   PubMed Web of Science ®Google Scholar
• Ren R. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat Rev Cancer 2005; 5:172 - 83; http://dx.doi.org/10.1038/nrc1567; PMID: 15719031
   PubMed Web of Science ®Google Scholar
• Savona M, Talpaz M. Getting to the stem of chronic myeloid leukaemia. Nat Rev Cancer 2008; 8:341 - 50; http://dx.doi.org/10.1038/nrc2368; PMID: 18385684
   PubMed Web of Science ®Google Scholar
• Schiffer CA. BCR-ABL tyrosine kinase inhibitors for chronic myelogenous leukemia. N Engl J Med 2007; 357:258 - 65; http://dx.doi.org/10.1056/NEJMct071828; PMID: 17634461
   PubMed Web of Science ®Google Scholar
• Quintás-Cardama A, Kantarjian H, Cortes J. Flying under the radar: the new wave of BCR-ABL inhibitors. Nat Rev Drug Discov 2007; 6:834 - 48; http://dx.doi.org/10.1038/nrd2324; PMID: 17853901
   PubMed Web of Science ®Google Scholar
• Weisberg E, Manley PW, Cowan-Jacob SW, Hochhaus A, Griffin JD. Second generation inhibitors of BCR-ABL for the treatment of imatinib-resistant chronic myeloid leukaemia. Nat Rev Cancer 2007; 7:345 - 56; http://dx.doi.org/10.1038/nrc2126; PMID: 17457302
   PubMed Web of Science ®Google Scholar
• Verfaillie T, Salazar M, Velasco G, Agostinis P.. Linking ER Stress to Autophagy: Potential Implications for Cancer Therapy. Int J Cell Biol 2010; 2010:930509
   PubMedGoogle Scholar
• Wang G, Yang ZQ, Zhang K. Endoplasmic reticulum stress response in cancer: molecular mechanism and therapeutic potential. Am J Transl Res 2010; 2:65 - 74; PMID: 20182583
   PubMed Web of Science ®Google Scholar
• Piwocka K, Vejda S, Cotter TG, O’Sullivan GC, McKenna SL. Bcr-Abl reduces endoplasmic reticulum releasable calcium levels by a Bcl-2-independent mechanism and inhibits calcium-dependent apoptotic signaling. Blood 2006; 107:4003 - 10; http://dx.doi.org/10.1182/blood-2005-04-1523; PMID: 16469868
   PubMed Web of Science ®Google Scholar
• Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999; 397:271 - 4; http://dx.doi.org/10.1038/16729; PMID: 9930704
   PubMed Web of Science ®Google Scholar
• Su Q, Wang S, Gao HQ, Kazemi S, Harding HP, Ron D, et al. Modulation of the eukaryotic initiation factor 2 alpha-subunit kinase PERK by tyrosine phosphorylation. J Biol Chem 2008; 283:469 - 75; http://dx.doi.org/10.1074/jbc.M704612200; PMID: 17998206
   PubMed Web of Science ®Google Scholar
• Hantschel O, Warsch W, Eckelhart E, Kaupe I, Grebien F, Wagner KU, et al. BCR-ABL uncouples canonical JAK2-STAT5 signaling in chronic myeloid leukemia. Nat Chem Biol 2012; 8:285 - 93; http://dx.doi.org/10.1038/nchembio.775; PMID: 22286129
   PubMed Web of Science ®Google Scholar
• Donzé O, Jagus R, Koromilas AE, Hershey JW, Sonenberg N. Abrogation of translation initiation factor eIF-2 phosphorylation causes malignant transformation of NIH 3T3 cells. EMBO J 1995; 14:3828 - 34; PMID: 7641700
   PubMed Web of Science ®Google Scholar
• Calabretta B, Perrotti D. The biology of CML blast crisis. Blood 2004; 103:4010 - 22; http://dx.doi.org/10.1182/blood-2003-12-4111; PMID: 14982876
   PubMed Web of Science ®Google Scholar
• Donato NJ, Wu JY, Stapley J, Lin H, Arlinghaus R, Aggarwal BB, et al. Imatinib mesylate resistance through BCR-ABL independence in chronic myelogenous leukemia. Cancer Res 2004; 64:672 - 7; http://dx.doi.org/10.1158/0008-5472.CAN-03-1484; PMID: 14744784
   PubMed Web of Science ®Google Scholar
• Nambu T, Araki N, Nakagawa A, Kuniyasu A, Kawaguchi T, Hamada A, et al. Contribution of BCR-ABL-independent activation of ERK1/2 to acquired imatinib resistance in K562 chronic myeloid leukemia cells. Cancer Sci 2010; 101:137 - 42; http://dx.doi.org/10.1111/j.1349-7006.2009.01365.x; PMID: 19843070
   PubMed Web of Science ®Google Scholar
• Jagani Z, Dorsch M, Warmuth M. Hedgehog pathway activation in chronic myeloid leukemia. Cell Cycle 2010; 9:3449 - 56; http://dx.doi.org/10.4161/cc.9.17.12945; PMID: 20928937
   PubMed Web of Science ®Google Scholar
• Vakana E, Platanias LC. AMPK in BCR-ABL expressing leukemias. Regulatory effects and therapeutic implications. Oncotarget 2011; 2:1322 - 8; PMID: 22249159
   PubMed Web of Science ®Google Scholar
• Dufies M, Jacquel A, Belhacene N, Robert G, Cluzeau T, Luciano F, et al. Mechanisms of AXL overexpression and function in Imatinib-resistant chronic myeloid leukemia cells. Oncotarget 2011; 2:874 - 85; PMID: 22141136
   PubMed Web of Science ®Google Scholar
• Chomel JC, Turhan AG. Chronic myeloid leukemia stem cells in the era of targeted therapies: resistance, persistence and long-term dormancy. Oncotarget 2011; 2:713 - 27; PMID: 21946665
   PubMed Web of Science ®Google Scholar
• Graham SM, Jørgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L, et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 2002; 99:319 - 25; http://dx.doi.org/10.1182/blood.V99.1.319; PMID: 11756187
   PubMed Web of Science ®Google Scholar
• Chen Y, Peng C, Sullivan C, Li D, Li S. Critical molecular pathways in cancer stem cells of chronic myeloid leukemia. Leukemia 2010; 24:1545 - 54; http://dx.doi.org/10.1038/leu.2010.143; PMID: 20574455
   PubMed Web of Science ®Google Scholar
• Bobrovnikova-Marjon E, Grigoriadou C, Pytel D, Zhang F, Ye J, Koumenis C, et al. PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage. Oncogene 2010; 29:3881 - 95; http://dx.doi.org/10.1038/onc.2010.153; PMID: 20453876
   PubMed Web of Science ®Google Scholar
• Hamanaka RB, Bobrovnikova-Marjon E, Ji X, Liebhaber SA, Diehl JA. PERK-dependent regulation of IAP translation during ER stress. Oncogene 2009; 28:910 - 20; http://dx.doi.org/10.1038/onc.2008.428; PMID: 19029953
   PubMed Web of Science ®Google Scholar
• Liu Y, László C, Liu Y, Liu W, Chen X, Evans SC, et al. Regulation of G(1) arrest and apoptosis in hypoxia by PERK and GCN2-mediated eIF2alpha phosphorylation. Neoplasia 2010; 12:61 - 8; PMID: 20072654
   PubMed Web of Science ®Google Scholar
• Papadakis AI, Paraskeva E, Peidis P, Muaddi H, Li S, Raptis L, et al. eIF2alpha Kinase PKR modulates the hypoxic response by Stat3-dependent transcriptional suppression of HIF-1alpha. Cancer Res 2010; 70:7820 - 9; http://dx.doi.org/10.1158/0008-5472.CAN-10-0215; PMID: 20924113
   PubMed Web of Science ®Google Scholar
• Mounir Z, Krishnamoorthy JL, Wang S, Papadopoulou B, Campbell S, Muller WJ, et al. Akt determines cell fate through inhibition of the PERK-eIF2α phosphorylation pathway. Sci Signal 2011; 4:ra62; http://dx.doi.org/10.1126/scisignal.2001630; PMID: 21954288
   PubMed Web of Science ®Google Scholar
• Peidis P, Papadakis AI, Muaddi H, Richard S, Koromilas AE. Doxorubicin bypasses the cytoprotective effects of eIF2α phosphorylation and promotes PKR-mediated cell death. Cell Death Differ 2011; 18:145 - 54; http://dx.doi.org/10.1038/cdd.2010.76; PMID: 20559319
   PubMed Web of Science ®Google Scholar
• Peidis P, Papadakis AI, Rajesh K, Koromilas AE. HDAC pharmacological inhibition promotes cell death through the eIF2α kinases PKR and GCN2. Aging (Albany NY) 2010; 2:669 - 77; PMID: 21076179
   PubMedGoogle Scholar
• Muaddi H, Majumder M, Peidis P, Papadakis AI, Holcik M, Scheuner D, et al. Phosphorylation of eIF2α at serine 51 is an important determinant of cell survival and adaptation to glucose deficiency. Mol Biol Cell 2010; 21:3220 - 31; http://dx.doi.org/10.1091/mbc.E10-01-0023; PMID: 20660158
   PubMed Web of Science ®Google Scholar
• Bellodi C, Lidonnici MR, Hamilton A, Helgason GV, Soliera AR, Ronchetti M, et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest 2009; 119:1109 - 23; http://dx.doi.org/10.1172/JCI35660; PMID: 19363292
   PubMed Web of Science ®Google Scholar
• Altman BJ, Jacobs SR, Mason EF, Michalek RD, MacIntyre AN, Coloff JL, et al. Autophagy is essential to suppress cell stress and to allow BCR-Abl-mediated leukemogenesis. Oncogene 2011; 30:1855 - 67; http://dx.doi.org/10.1038/onc.2010.561; PMID: 21151168
   PubMed Web of Science ®Google Scholar
• He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67 - 93; http://dx.doi.org/10.1146/annurev-genet-102808-114910; PMID: 19653858
   PubMed Web of Science ®Google Scholar
• Tanimura A, Yujiri T, Tanaka Y, Hatanaka M, Mitani N, Nakamura Y, et al. The anti-apoptotic role of the unfolded protein response in Bcr-Abl-positive leukemia cells. Leuk Res 2009; 33:924 - 8; http://dx.doi.org/10.1016/j.leukres.2009.01.027; PMID: 19237191
   PubMed Web of Science ®Google Scholar
• Oehler VG, Yeung KY, Choi YE, Bumgarner RE, Raftery AE, Radich JP. The derivation of diagnostic markers of chronic myeloid leukemia progression from microarray data. Blood 2009; 114:3292 - 8; http://dx.doi.org/10.1182/blood-2009-03-212969; PMID: 19654405
   PubMed Web of Science ®Google Scholar
• Zheng C, Li L, Haak M, Brors B, Frank O, Giehl M, et al. Gene expression profiling of CD34+ cells identifies a molecular signature of chronic myeloid leukemia blast crisis. Leukemia 2006; 20:1028 - 34; http://dx.doi.org/10.1038/sj.leu.2404227; PMID: 16617318
   PubMed Web of Science ®Google Scholar
• Keeshan K, Mills KI, Cotter TG, McKenna SL. Elevated Bcr-Abl expression levels are sufficient for a haematopoietic cell line to acquire a drug-resistant phenotype. Leukemia 2001; 15:1823 - 33; http://dx.doi.org/10.1038/sj.leu.2402309; PMID: 11753601
   PubMed Web of Science ®Google Scholar
• Cramer K, Nieborowska-Skorska M, Koptyra M, Slupianek A, Penserga ET, Eaves CJ, et al. BCR/ABL and other kinases from chronic myeloproliferative disorders stimulate single-strand annealing, an unfaithful DNA double-strand break repair. Cancer Res 2008; 68:6884 - 8; http://dx.doi.org/10.1158/0008-5472.CAN-08-1101; PMID: 18757400
   PubMed Web of Science ®Google Scholar