In-vitro modeling of TKI resistance in the high-risk B-cell acute lymphoblastic leukemia fusion gene RANBP2-ABL1 - implications for targeted therapy

References

• Pui CH, Pei D, Campana D, et al. A revised definition for cure of childhood acute lymphoblastic leukemia. Leukemia. 2014;28(12):2336–2343.
   PubMed Web of Science ®Google Scholar
• Pulte D, Jansen L, Gondos A, et al. Survival of adults with acute lymphoblastic leukemia in Germany and the United States. PLoS One. 2014;9(1):e85554.
   PubMed Web of Science ®Google Scholar
• Cortes J, Rea D, Lipton JH. Treatment-free remission with first- and second-generation tyrosine kinase inhibitors. Am J Hematol. 2019;94(3):346–357.
   PubMed Web of Science ®Google Scholar
• Hunger SP, Raetz EA, Loh ML, et al. Improving outcomes for high-risk ALL: translating new discoveries into clinical care. Pediatr Blood Cancer. 2011;56(6):984–993.
   PubMed Web of Science ®Google Scholar
• Den Boer ML, van Slegtenhorst M, De Menezes RX, et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol. 2009;10(2):125–134.
   PubMed Web of Science ®Google Scholar
• Mullighan CG, Su X, Zhang J, et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med. 2009;360(5):470–480.
   PubMed Web of Science ®Google Scholar
• Roberts KG, Li Y, Payne-Turner D, et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N Engl J Med. 2014;371(11):1005–1015. 11
   PubMed Web of Science ®Google Scholar
• Roberts KG, Gu Z, Payne-Turner D, et al. High frequency and poor outcome of philadelphia chromosome-like acute lymphoblastic leukemia in adults. J Clin Oncol. 2017;35(4):394–401.
   PubMed Web of Science ®Google Scholar
• Tasian SK, Loh ML, Hunger SP. Philadelphia chromosome-like acute lymphoblastic leukemia. Blood. 2017;130(19):2064–2072.
   PubMed Web of Science ®Google Scholar
• Roberts KG, Morin RD, Zhang J, et al. Genetic alterations activating kinase and cytokine receptor signaling in high-risk acute lymphoblastic leukemia. Cancer Cell. 2012;22(2):153–166.
   PubMed Web of Science ®Google Scholar
• Lengline E, Beldjord K, Dombret H, et al. Successful tyrosine kinase inhibitor therapy in a refractory B-cell precursor acute lymphoblastic leukemia with EBF1-PDGFRB fusion. Haematologica. 2013;98(11):e146–e148.
   PubMed Web of Science ®Google Scholar
• Weston BW, Hayden MA, Roberts KG, et al. Tyrosine kinase inhibitor therapy induces remission in a patient with refractory EBF1-PDGFRB-positive acute lymphoblastic leukemia. J Clin Oncol. 2013;31(25):e413–e416.
   PubMed Web of Science ®Google Scholar
• Yeung DT, Moulton DJ, Heatley SL, et al. Relapse of BCR-ABL1-like ALL mediated by the ABL1 kinase domain mutation T315I following initial response to dasatinib treatment. Leukemia. 2015;29(1):230–232.
   PubMed Web of Science ®Google Scholar
• Loh ML, Tasian SK, Rabin KR, et al. A phase 1 dosing study of ruxolitinib in children with relapsed or refractory solid tumors, leukemias, or myeloproliferative neoplasms: a Children's Oncology Group phase 1 consortium study (ADVL1011). Pediatr Blood Cancer. 2015;62(10):1717–1724.
   PubMed Web of Science ®Google Scholar
• Moorman AV, Schwab C, Winterman E, et al. Adjuvant tyrosine kinase inhibitor therapy improves outcome for children and adolescents with acute lymphoblastic leukaemia who have an ABL-class fusion. Br J Haematol. 2020;191(5):844–851.
   PubMed Web of Science ®Google Scholar
• Tanasi I, Ba I, Sirvent N, et al. Efficacy of tyrosine kinase inhibitors in Ph-like acute lymphoblastic leukemia harboring ABL-class rearrangements. Blood. 2019;134(16):1351–1355.
   PubMed Web of Science ®Google Scholar
• Gorre ME, Mohammed M, Ellwood K, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science. 2001;293(5531):876–880.
   PubMed Web of Science ®Google Scholar
• Soverini S, De Benedittis C, Papayannidis C, et al. Drug resistance and BCR-ABL kinase domain mutations in Philadelphia chromosome-positive acute lymphoblastic leukemia from the imatinib to the second-generation tyrosine kinase inhibitor era: the main changes are in the type of mutations, but not in the frequency of mutation involvement. Cancer. 2014;120(7):1002–1009.
   PubMed Web of Science ®Google Scholar
• Wylie AA, Schoepfer J, Jahnke W, et al. The allosteric inhibitor ABL001 enables dual targeting of BCR-ABL1. Nature. 2017;543(7647):733–737.
   PubMed Web of Science ®Google Scholar
• Hughes TP, Mauro MJ, Cortes JE, et al. Asciminib in chronic myeloid leukemia after ABL kinase inhibitor failure. N Engl J Med. 2019;381(24):2315–2326.
   PubMed Web of Science ®Google Scholar
• Branford S, Rudzki Z, Walsh S, et al. High frequency of point mutations clustered within the adenosine triphosphate-binding region of BCR/ABL in patients with chronic myeloid leukemia or Ph-positive acute lymphoblastic leukemia who develop imatinib (STI571) resistance. Blood. 2002;99(9):3472–3475.
   PubMed Web of Science ®Google Scholar
• Tang C, Schafranek L, Watkins DB, et al. Tyrosine kinase inhibitor resistance in chronic myeloid leukemia cell lines: investigating resistance pathways. Leuk Lymphoma. 2011;52(11):2139–2147.
   PubMed Web of Science ®Google Scholar
• Cortes JE, Kantarjian H, Shah NP, et al. Ponatinib in refractory Philadelphia chromosome-positive leukemias. N Engl J Med. 2012;367(22):2075–2088.
   PubMed Web of Science ®Google Scholar
• Shah NP, Kasap C, Weier C, et al. Transient potent BCR-ABL inhibition is sufficient to commit chronic myeloid leukemia cells irreversibly to apoptosis. Cancer Cell. 2008;14(6):485–493.
   PubMed Web of Science ®Google Scholar
• Peng B, Lloyd P, Schran H. Clinical pharmacokinetics of imatinib. Clin Pharmacokinet. 2005;44(9):879–894.
   PubMed Web of Science ®Google Scholar
• White D, Saunders V, Lyons AB, et al. In vitro sensitivity to imatinib-induced inhibition of ABL kinase activity is predictive of molecular response in patients with de novo CML. Blood. 2005;106(7):2520–2526.
   PubMed Web of Science ®Google Scholar
• Cortes JE, Kim DW, Pinilla-Ibarz J, et al. A phase 2 trial of ponatinib in Philadelphia chromosome-positive leukemias. N Engl J Med. 2013;369(19):1783–1796.
   PubMed Web of Science ®Google Scholar
• Eide CA, Zabriskie MS, Savage Stevens SL, et al. Combining the allosteric inhibitor asciminib with ponatinib suppresses emergence of and restores efficacy against highly resistant BCR-ABL1 mutants. Cancer Cell. 2019;36(4):431.e5–443.e5.
   Web of Science ®Google Scholar
• Loh ML, Zhang J, Harvey RC, et al. Tyrosine kinome sequencing of pediatric acute lymphoblastic leukemia: a report from the Children's Oncology Group TARGET Project. Blood. 2013;121(3):485–488.
   PubMed Web of Science ®Google Scholar
• Roberts KG, Mullighan CG. Genomics in acute lymphoblastic leukaemia: insights and treatment implications. Nat Rev Clin Oncol. 2015;12(6):344–357.
   PubMed Web of Science ®Google Scholar
• Lilljebjorn H, Fioretos T. New oncogenic subtypes in pediatric B-cell precursor acute lymphoblastic leukemia. Blood. 2017;130(12):1395–1401.
   PubMed Web of Science ®Google Scholar
• Maude SL, Tasian SK, Vincent T, et al. Targeting JAK1/2 and mTOR in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood. 2012;120(17):3510–3518.
   PubMed Web of Science ®Google Scholar
• Tasian SK, Teachey DT, Li Y, et al. Potent efficacy of combined PI3K/mTOR and JAK or ABL inhibition in murine xenograft models of Ph-like acute lymphoblastic leukemia. Blood. 2017;129(2):177–187.
   PubMed Web of Science ®Google Scholar
• Chang BH, Willis SG, Stork L, et al. Imatinib resistant BCR-ABL1 mutations at relapse in children with Ph + ALL: a Children's Oncology Group (COG) study. Br J Haematol. 2012;157(4):507–510.
   PubMed Web of Science ®Google Scholar
• Kayser S, Levis MJ. FLT3 tyrosine kinase inhibitors in acute myeloid leukemia: clinical implications and limitations. Leuk Lymphoma. 2014;55(2):243–255.
   PubMed Web of Science ®Google Scholar
• Soverini S, Mancini M, Bavaro L, et al. Chronic myeloid leukemia: the paradigm of targeting oncogenic tyrosine kinase signaling and counteracting resistance for successful cancer therapy. Mol Cancer. 2018;17(1):49.
   PubMedGoogle Scholar
• Zhang Y, Gao Y, Zhang H, et al. PDGFRB mutation and tyrosine kinase inhibitor resistance in Ph-like acute lymphoblastic leukemia. Blood. 2018;131(20):2256–2261.
   PubMed Web of Science ®Google Scholar
• Gibbons DL, Pricl S, Kantarjian H, et al. The rise and fall of gatekeeper mutations? The BCR-ABL1 T315I paradigm. Cancer. 2012;118(2):293–299.
   PubMed Web of Science ®Google Scholar
• Greaves M, Maley CC. Clonal evolution in cancer. Nature. 2012;481(7381):306–313.
   PubMed Web of Science ®Google Scholar
• Shah NP. Ponatinib: targeting the T315I mutation in chronic myelogenous leukemia. Clin Adv Hematol Oncol. 2011;9(12):925–926.
   PubMedGoogle Scholar
• Zabriskie MS, Eide CA, Tantravahi SK, et al. BCR-ABL1 compound mutations combining key kinase domain positions confer clinical resistance to ponatinib in Ph chromosome-positive leukemia. Cancer Cell. 2014;26(3):428–442.
   PubMed Web of Science ®Google Scholar
• Eadie LN, Saunders VA, Branford S, et al. The new allosteric inhibitor asciminib is susceptible to resistance mediated by ABCB1 and ABCG2 overexpression in vitro. Oncotarget. 2018;9(17):13423–13437.
   PubMedGoogle Scholar
• Roberts KG. The biology of Philadelphia chromosome-like ALL. Best Pract Res Clin Haematol. 2017;30(3):212–221.
   PubMed Web of Science ®Google Scholar
• Hunger SP, Mullighan CG. Redefining ALL classification: toward detecting high-risk ALL and implementing precision medicine. Blood. 2015;125(26):3977–3987.
   PubMed Web of Science ®Google Scholar