Genetic alterations in glucocorticoid signaling pathway components are associated with adverse prognosis in children with relapsed ETV6/RUNX1-positive acute lymphoblastic leukemia

References

• Pui CH, Carroll WL, Meshinchi S, et al. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J Clin Oncol 2011; 29: 551–565.
   PubMed Web of Science ®Google Scholar
• Seeger K, Buchwald D, Peter A, et al. TEL-AML1 fusion in relapsed childhood acute lymphoblastic leukemia. Blood 1999; 94: 374–376.
   PubMed Web of Science ®Google Scholar
• Kuster L, Grausenburger R, Fuka G, et al. ETV6/RUNX1-positive relapses evolve from an ancestral clone and frequently acquire deletions of genes implicated in glucocorticoid signaling. Blood 2011; 117: 2658–2667.
   PubMed Web of Science ®Google Scholar
• Inaba H, Pui CH. Glucocorticoid use in acute lymphoblastic leukaemia. Lancet Oncol 2010; 11: 1096–1106.
   PubMed Web of Science ®Google Scholar
• Schrappe M, Reiter A, Ludwig WD, et al. Improved outcome in childhood acute lymphoblastic leukemia despite reduced use of anthracyclines and cranial radiotherapy: results of trial ALL-BFM 90. German-Austrian-Swiss ALL-BFM Study Group. Blood 2000; 95: 3310–3322.
   PubMed Web of Science ®Google Scholar
• Conter V, Bartram CR, Valsecchi MG, et al. Molecular response to treatment redefines all prognostic factors in children and adolescents with B-cell precursor acute lymphoblastic leukemia: results in 3184 patients of the AIEOP-BFM ALL 2000 study. Blood 2010; 115: 3206–3214.
   PubMed Web of Science ®Google Scholar
• von Stackelberg A, Seeger K, Henze G, et al. Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia after first relapse. Leukemia 2004; 18: 1727–1728 ;author reply 1728–1729.
   PubMed Web of Science ®Google Scholar
• Eckert C, Biondi A, Seeger K, et al. Prognostic value of minimal residual disease in relapsed childhood acute lymphoblastic leukaemia. Lancet 2001; 358: 1239–1241.
   PubMed Web of Science ®Google Scholar
• Schmidt S, Rainer J, Ploner C, et al. Glucocorticoid-induced apoptosis and glucocorticoid resistance: molecular mechanisms and clinical relevance. Cell Death Differ 2004; 11(Suppl. 1): S45–55.
   PubMed Web of Science ®Google Scholar
• Mullighan CG, Goorha S, Radtke I, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 2007; 446: 758–776.
   PubMed Web of Science ®Google Scholar
• van Galen JC, Kuiper RP, van Emst L, et al. BTG1 regulates glucocorticoid receptor autoinduction in acute lymphoblastic leukemia. Blood 2010; 115: 4810–4819.
   PubMed Web of Science ®Google Scholar
• Lilljebjorn H, Heidenblad M, Nilsson B, et al. Combined high-resolution array-based comparative genomic hybridization and expression profiling of ETV6/RUNX1-positive acute lymphoblastic leukemias reveal a high incidence of cryptic Xq duplications and identify several putative target genes within the commonly gained region. Leukemia 2007; 21: 2137–2144.
   PubMed Web of Science ®Google Scholar
• van Delft FW, Horsley S, Colman S, et al. Clonal origins of relapse in ETV6-RUNX1 acute lymphoblastic leukemia. Blood 2011; 117: 6247–6254.
   PubMed Web of Science ®Google Scholar
• Mullighan CG, Phillips LA, Su X, et al. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 2008; 322: 1377–1380.
   PubMed Web of Science ®Google Scholar
• Eckert C, Henze G, Seeger K, et al. Use of allogeneic hematopoietic stem-cell transplantation based on minimal residual disease response improves outcomes for children with relapsed acute lymphoblastic leukemia in the intermediate-risk group. J Clin Oncol 2013; 31: 2736–2742.
   PubMed Web of Science ®Google Scholar
• Eckert C, von Stackelberg A, Seeger K, et al. Minimal residual disease after induction is the strongest predictor of prognosis in intermediate risk relapsed acute lymphoblastic leukaemia – long-term results of trial ALL-REZ BFM P95/96. Eur J Cancer 2013; 49: 1346–1355.
   PubMed Web of Science ®Google Scholar
• Inthal A, Zeitlhofer P, Zeginigg M, et al. CREBBP HAT domain mutations prevail in relapse cases of high hyperdiploid childhood acute lymphoblastic leukemia. Leukemia 2012; 26: 1797–1803.
   PubMed Web of Science ®Google Scholar
• Morak M, Attarbaschi A, Fischer S, et al. Small sizes and indolent evolutionary dynamics challenge the potential role of P2RY8-CRLF2-harboring clones as main relapse-driving force in childhood ALL. Blood 2012; 120: 5134–5142.
   PubMed Web of Science ®Google Scholar
• Riml S, Schmidt S, Ausserlechner MJ, et al. Glucocorticoid receptor heterozygosity combined with lack of receptor auto-induction causes glucocorticoid resistance in Jurkat acute lymphoblastic leukemia cells. Cell Death Differ 2004; 11(Suppl. 1): S65–S72.
   PubMedGoogle Scholar
• Fuka G, Kantner HP, Grausenburger R, et al. Silencing of ETV6/RUNX1 abrogates PI3K/AKT/mTOR signaling and impairs reconstitution of leukemia in xenografts. Leukemia 2012; 26: 927–933.
   PubMed Web of Science ®Google Scholar
• Patel N, Goff LK, Clark T, et al. Expression profile of wild-type ETV6 in childhood acute leukaemia. Br J Haematol 2003; 122: 94–98.
   PubMed Web of Science ®Google Scholar
• Stams WA, den Boer ML, Beverloo HB, et al. Expression levels of TEL, AML1, and the fusion products TEL-AML1 and AML1-TEL versus drug sensitivity and clinical outcome in t(12;21)-positive pediatric acute lymphoblastic leukemia. Clin Cancer Res 2005; 11: 2974–2980.
   PubMed Web of Science ®Google Scholar
• Liu X, Pan Z, Zhang L, et al. JAB1 accelerates mitochondrial apoptosis by interaction with proapoptotic BclGs. Cell Signal 2008; 20: 230–240.
   PubMed Web of Science ®Google Scholar
• Glinskii AB, Glinsky GV, Lin HY, et al. Modification of survival pathway gene expression in human breast cancer cells by tetraiodothyroacetic acid (tetrac). Cell Cycle 2009; 8: 3554–3562.
   Web of Science ®Google Scholar
• Kullmann MK, Grubbauer C, Goetsch K, et al. The p27-Skp2 axis mediates glucocorticoid-induced cell cycle arrest in T-lymphoma cells. Cell Cycle 2013; 12: 2625–2635.
   PubMed Web of Science ®Google Scholar
• Meissner B, Bartram T, Eckert C, et al. Frequent and sex-biased deletion of SLX4IP by illegitimate V(D)J-mediated recombination in childhood acute lymphoblastic leukemia. Hum Mol Genet 2014; 23: 590–601.
   PubMed Web of Science ®Google Scholar
• Girardi C, De Pitta C, Casara S, et al. Analysis of miRNA and mRNA expression profiles highlights alterations in ionizing radiation response of human lymphocytes under modeled microgravity. PLoS One 2012; 7: e31293.
   PubMed Web of Science ®Google Scholar
• Mraz M, Dolezalova D, Plevova K, et al. MicroRNA-650 expression is influenced by immunoglobulin gene rearrangement and affects the biology of chronic lymphocytic leukemia. Blood 2012; 119: 2110–2113.
   PubMed Web of Science ®Google Scholar
• Sulong S, Moorman AV, Irving JA, et al. A comprehensive analysis of the CDKN2A gene in childhood acute lymphoblastic leukemia reveals genomic deletion, copy number neutral loss of heterozygosity, and association with specific cytogenetic subgroups. Blood 2009; 113: 100–107.
   PubMed Web of Science ®Google Scholar
• Mirebeau D, Acquaviva C, Suciu S, et al. The prognostic significance of CDKN2A, CDKN2B and MTAP inactivation in B-lineage acute lymphoblastic leukemia of childhood. Results of the EORTC studies 58881 and 58951. Haematologica 2006; 91: 881–885.
   PubMed Web of Science ®Google Scholar
• Graf Einsiedel H, Taube T, Hartmann R, et al. Deletion analysis of p16(INKa) and p15(INKb) in relapsed childhood acute lymphoblastic leukemia. Blood 2002; 99: 4629–4631.
   PubMed Web of Science ®Google Scholar
• Ploner C, Rainer J, Niederegger H, et al. The BCL2 rheostat in glucocorticoid-induced apoptosis of acute lymphoblastic leukemia. Leukemia 2008; 22: 370–377.
   PubMed Web of Science ®Google Scholar
• Bachmann PS, Gorman R, Papa RA, et al. Divergent mechanisms of glucocorticoid resistance in experimental models of pediatric acute lymphoblastic leukemia. Cancer Res 2007; 67: 4482–4490.
   PubMed Web of Science ®Google Scholar
• Tissing WJ, Lauten M, Meijerink JP, et al. Expression of the glucocorticoid receptor and its isoforms in relation to glucocorticoid resistance in childhood acute lymphocytic leukemia. Haematologica 2005; 90: 1279–1281.
   PubMed Web of Science ®Google Scholar
• Haarman EG, Kaspers GJ, Pieters R, et al. Glucocorticoid receptor alpha, beta and gamma expression vs in vitro glucocorticod resistance in childhood leukemia. Leukemia 2004; 18: 530–537.
   PubMed Web of Science ®Google Scholar
• Kofler R, Schmidt S, Kofler A, et al. Resistance to glucocorticoid-induced apoptosis in lymphoblastic leukemia. J Endocrinol 2003; 178: 19–27.
   PubMed Web of Science ®Google Scholar
• Kotani A, Ha D, Schotte D, et al. A novel mutation in the miR-128b gene reduces miRNA processing and leads to glucocorticoid resistance of MLL-AF4 acute lymphocytic leukemia cells. Cell Cycle 2010; 9: 1037–1042.
   PubMed Web of Science ®Google Scholar
• Kuiper RP, Schoenmakers EF, van Reijmersdal SV, et al. High-resolution genomic profiling of childhood ALL reveals novel recurrent genetic lesions affecting pathways involved in lymphocyte differentiation and cell cycle progression. Leukemia 2007; 21: 1258–1266.
   PubMed Web of Science ®Google Scholar
• Hogan LE, Meyer JA, Yang J, et al. Integrated genomic analysis of relapsed childhood acute lymphoblastic leukemia reveals therapeutic strategies. Blood 2011; 118: 5218–5226.
   PubMed Web of Science ®Google Scholar
• Bokemeyer A, Eckert C, Meyr F, et al. Copy number genome alterations are associated with treatment response and outcome in relapsed childhood ETV6/RUNX1-positive acute lymphoblastic leukemia. Haematologica 2014; 99: 706–714.
   PubMed Web of Science ®Google Scholar
• Schmidt S, Irving JA, Minto L, et al. Glucocorticoid resistance in two key models of acute lymphoblastic leukemia occurs at the level of the glucocorticoid receptor. FASEB J 2006; 20: 2600–2602.
   PubMed Web of Science ®Google Scholar
• Irving JA, Minto L, Bailey S, et al. Loss of heterozygosity and somatic mutations of the glucocorticoid receptor gene are rarely found at relapse in pediatric acute lymphoblastic leukemia but may occur in a subpopulation early in the disease course. Cancer Res 2005; 65: 9712–9718.
   PubMed Web of Science ®Google Scholar
• Bonapace L, Bornhauser BC, Schmitz M, et al. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J Clin Invest 2010; 120: 1310–1323.
   PubMed Web of Science ®Google Scholar
• Attarbaschi A, Mann G, Konig M, et al. Incidence and relevance of secondary chromosome abnormalities in childhood TEL/AML1 + acute lymphoblastic leukemia: an interphase FISH analysis. Leukemia 2004; 18: 1611–1616.
   PubMed Web of Science ®Google Scholar
• McLean TW, Ringold S, Neuberg D, et al. TEL/AML-1 dimerizes and is associated with a favorable outcome in childhood acute lymphoblastic leukemia. Blood 1996; 88: 4252–4258.
   PubMed Web of Science ®Google Scholar
• Lilljebjorn H, Soneson C, Andersson A, et al. The correlation pattern of acquired copy number changes in 164 ETV6/RUNX1-positive childhood acute lymphoblastic leukemias. Hum Mol Genet 2010; 19: 3150–3158.
   PubMed Web of Science ®Google Scholar
• Montpetit A, Larose J, Boily G, et al. Mutational and expression analysis of the chromosome 12p candidate tumor suppressor genes in pre-B acute lymphoblastic leukemia. Leukemia 2004; 18: 1499–1504.
   PubMed Web of Science ®Google Scholar
• Ausserlechner MJ, Obexer P, Wiegers GJ, et al. The cell cycle inhibitor p16(INK4A) sensitizes lymphoblastic leukemia cells to apoptosis by physiologic glucocorticoid levels. J Biol Chem 2001; 276: 10984–10989.
   Web of Science ®Google Scholar
• Waanders E, Scheijen B, van der Meer LT, et al. The origin and nature of tightly clustered BTG1 deletions in precursor B-cell acute lymphoblastic leukemia support a model of multiclonal evolution. PLoS Genet 2012; 8: e1002533.
   PubMed Web of Science ®Google Scholar
• Flohr T, Schrauder A, Cazzaniga G, et al. Minimal residual disease-directed risk stratification using real-time quantitative PCR analysis of immunoglobulin and T-cell receptor gene rearrangements in the international multicenter trial AIEOP-BFM ALL 2000 for childhood acute lymphoblastic leukemia. Leukemia 2008; 22: 771–782.
   PubMed Web of Science ®Google Scholar