Seminars in Hematology
Volume 46 , Pages S22-S26 , April 2009

Understanding the Role of Mutations in Therapeutic Decision Making for Chronic Myeloid Leukemia

  • Elias Jabbour

      Affiliations

    • Department of Leukemia, University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Unit 428, Houston, TX
    • Corresponding Author InformationAddress correspondence to Elias Jabbour, MD, Assistant Professor of Medicine, Department of Leukemia, University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Unit 428, Houston, TX 77030
  • ,
  • Simona Soverini

      Affiliations

    • Molecular Biology Unit, Department of Hematology and Medical Oncology “L. e A. Seràgnoli,” University of Bologna, Bologna, Italy

References 

  1. Rowley JD. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature. 1973;243:290–293
  2. Bartram CR, de Klein A, Hagemeijer A, van Agthoven T, Geurts van Kessel A, Bootsma D, et al. Translocation of c-ab1 oncogene correlates with the presence of a Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1983;306:277–280
  3. Nardi V, Azam M, Daley GQ. Mechanisms and implications of imatinib resistance mutations in BCR-ABL. Curr Opin Hematol. 2004;11:35–43
  4. Jabbour E, Kantarjian H, Jones D, Talpaz M, Bekele N, O'Brien S, et al. Frequency and clinical significance of BCR-ABL mutations in patients with chronic myeloid leukemia treated with imatinib mesylate. Leukemia. 2006;20:1767–1773
  5. Soverini S, Martinelli G, Colarossi S, Gnani A, Castagnetti F, Rosti G, et al. Presence or the emergence of a F317L BCR-ABL mutation may be associated with resistance to dasatinib in Philadelphia chromosome-positive leukemia. J Clin Oncol. 2006;24:e51–e52
  6. Apperley JF. Part I: mechanisms of resistance to imatinib in chronic myeloid leukaemia. Lancet Oncol. 2007;8:1018–1029
  7. Corbin AS, La Rosee P, Stoffregen EP, Druker BJ, Deininger MW. Several Bcr-Abl kinase domain mutants associated with imatinib mesylate resistance remain sensitive to imatinib. Blood. 2003;101:4611–4614
  8. Branford S, Rudzki Z, Walsh S, Parkinson I, Grigg A, Szer J, et al. Detection of BCR-ABL mutations in patients with CML treated with imatinib is virtually always accompanied by clinical resistance, and mutations in the ATP phosphate-binding loop (P-loop) are associated with a poor prognosis. Blood. 2003;102:276–283
  9. Kantarjian H, Schiffer C, Jones D, Cortes J. Monitoring the response and course of chronic myeloid leukemia in the modern era of BCR-ABL tyrosine kinase inhibitors: practical advice on the use and interpretation of monitoring methods. Blood. 2008;111:1774–1780
  10. Hughes T, Deininger M, Hochhaus A, Branford S, Radich J, Kaeda J, et al. Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood. 2006;108:28–37
  11. Baccarani M, Saglio G, Goldman J, Hochhaus A, Simonsson B, Appelbaum F, et al. Evolving concepts in the management of chronic myeloid leukemia: recommendations from an expert panel on behalf of the European LeukemiaNet. Blood. 2006;108:1809–1820
  12. Soverini S, Colarossi S, Gnani A, Rosti G, Castagnetti F, Poerio A, et al. Contribution of ABL kinase domain mutations to imatinib resistance in different subsets of Philadelphia-positive patients: by the GIMEMA Working Party on Chronic Myeloid Leukemia. Clin Cancer Res. 2006;12:7374–7379
  13. Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, Kuriyan J, et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell. 2002;2:117–125
  14. Azam M, Latek RR, Daley GQ. Mechanisms of autoinhibition and STI-571/imatinib resistance revealed by mutagenesis of BCR-ABL. Cell. 2003;112:831–843
  15. Cortes J, Jabbour E, Kantarjian H, Yin CC, Shan J, O'Brien S, et al. Dynamics of BCR-ABL kinase domain mutations in chronic myeloid leukemia after sequential treatment with multiple tyrosine kinase inhibitors. Blood. 2007;110:4005–4011
  16. Jabbour E, Kantarjian HM, Jones D, Reddy N, O'Brien S, Garcia-Manero G, et al. Characteristics and outcome of chronic myeloid leukemia patients with F317L BCR-ABL kinase domain mutation after therapy with tyrosine kinase inhibitors. Blood. 2008;112:4839–4842
  17. Nicolini FE, Hayette S, Corm S, Bachy E, Bories D, Tulliez M, et al. Clinical outcome of 27 imatinib mesylate-resistant chronic myelogenous leukemia patients harboring a T315I BCR-ABL mutation. Haematologica. 2007;92:1238–1241
  18. Jabbour E, Kantarjian H, Jones D, Breeden M, Garcia-Manero G, O'Brien S, et al. Characteristics and outcomes of patients with chronic myeloid leukemia and T315I mutation following failure of imatinib mesylate therapy. Blood. 2008;112:53–55
  19. Jabbour E, Kantarjian H, Atallah E, Borthakur G, Wierda W, Faderl S, et al. Impact of imatinib mesylate dose escalation on resistance and sub-optimal responses to standard-dose therapy in patients (pts) with chronic myeloid leukemia (CML). Blood. 2007;110:313a–314a
  20. Jabbour E, Kantarjian HM, Jones D, Shan J, O'Brien S, Reddy N, et al. Imatinib mesylate dose escalation is associated with durable responses in patients with chronic myeloid leukemia post cytogenetic failure on standard-dose imatinib therapy. Blood. 2008;Dec 5. [Epub ahead of print]
  21. Lombardo LJ, Lee FY, Chen P, Norris D, Barrish JC, Behnia K, et al. Discovery of N-(2-chloro-6-methyl-phenyl)-2-(6-(4-(2-hydroxyethyl)-piperazin-1-yl)-2-methylpyrimidin-4-ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem. 2004;47:6658–6661
  22. Weisberg E, Manley PW, Breitenstein W, Bruggen J, Cowan-Jacob SW, Ray A, et al. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell. 2005;7:129–141
  23. Golemovic M, Verstovsek S, Giles F, Cortes J, Manshouri T, Manley PW, et al. AMN107, a novel aminopyrimidine inhibitor of Bcr-Abl, has in vitro activity against imatinib-resistant chronic myeloid leukemia. Clin Cancer Res. 2005;11:4941–4947
  24. Shah NP, Tran C, Lee FY, Chen P, Norris D, Sawyers CL. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science. 2004;305:399–401
  25. O'Hare T, Walters DK, Stoffregen EP, Jia T, Manley PW, Mestan J, et al. In vitro activity of Bcr-Abl inhibitors AMN107 and BMS-354825 against clinically relevant imatinib-resistant Abl kinase domain mutants. Cancer Res. 2005;65:4500–4505
  26. Radich J, Kim D, Martinelli G, Branford S, Mueller M, Haque A, et al. Response to nilotinib in chronic myelogenous leukemia patients in chronic phase (CML-CP) according to BCR-ABL mutations at baseline. Haematologica. 2008;93:21
  27. Saglio G, Radich J, Kim D, Martinelli G, Branford S, Mueller M, et al. Response to nilotinib in chronic myelogenous leukemia patients in chronic phase (CML-CP) according to BCR-ABL mutations at baseline. J Clin Oncol. 2008;26:387s
  28. Hochhaus A, Mueller M, Cortes JE, Kim D, Matloub Y, Ploughman L, et al. Dasatinib efficacy by dosing schedule across individual baseline BCR-ABL mutations in chronic phase chronic myelogenous leukemia (CML-CP) after imatinib failure. J Clin Oncol. 2008;26(May 20 suppl):375s
  29. Hochhaus A, Müller MC, Cortes JE, Kim DW, Matloub Y, Ploughman L, et al. Dasatinib efficacy after imatinib failure by dosing schedule and baseline BCR-ABL mutation status in patients with chronic myeloid leukemia in chronic phase (CML-CP). Haematologica. 2008;93(Suppl 1):371–372
  30. Deguchi Y, Kimura S, Ashihara E, Niwa T, Hodohara K, Fujiyama Y, et al. Comparison of imatinib, dasatinib, nilotinib and INNO-406 in imatinib-resistant cell lines. Leuk Res. 2008;32:980–983
  31. Burgess MR, Skaggs BJ, Shah NP, Lee FY, Sawyers CL. Comparative analysis of two clinically active BCR-ABL kinase inhibitors reveals the role of conformation-specific binding in resistance. Proc Natl Acad Sci U S A. 2005;102:3395–3400
  32. Puttini M, Coluccia AM, Boschelli F, Cleris L, Marchesi E, Donella-Deana A, et al. In vitro and in vivo activity of SKI-606, a novel Src-Abl inhibitor, against imatinib-resistant Bcr-Abl+ neoplastic cells. Cancer Res. 2006;66:11314–11322
  33. Kimura S, Naito H, Segawa H, Kuroda J, Yuasa T, Sato K, et al. NS-187, a potent and selective dual Bcr-Abl/Lyn tyrosine kinase inhibitor, is a novel agent for imatinib-resistant leukemia. Blood. 2005;106:3948–3954
  34. O'Hare T, Pollock R, Stoffregen EP, Keats JA, Abdullah OM, Moseson EM, et al. Inhibition of wild-type and mutant Bcr-Abl by AP23464, a potent ATP-based oncogenic protein kinase inhibitor: implications for CML. Blood. 2004;104:2532–2539
  35. Warmuth M, Simon N, Mitina O, Mathes R, Fabbro D, Manley PW, et al. Dual-specific Src and Abl kinase inhibitors, PP1 and CGP76030, inhibit growth and survival of cells expressing imatinib mesylate-resistant Bcr-Abl kinases. Blood. 2003;101:664–672
  36. Marin D, Maloisel F, Legros L, Nicolini FE, Roy L, Rousselot P. Efficacy of subcutaneous homoharringtonine in chronic myeloid leukemia patients resistant to tyrosine kinase inhibitors and harboring a BCR-ABL mutation. Haematologica. 2008;93(s1):56
  37. Cortes JC, Khoury J, Corm S, Nicolini FE, Benichou AC, Craig AR, et al. Data from a multicenter open label study of subcutaneous omacetaxine mepesuccinate in imatinib-resistant chronic myeloid leukemia patients with T315I mutation. Haematologica. 2008;93(Suppl 1):48–49
  38. Giles FJ, Cortes J, Jones D, Bergstrom D, Kantarjian H, Freedman SJ. MK-0457, a novel kinase inhibitor, is active in patients with chronic myeloid leukemia or acute lymphocytic leukemia with the T315I BCR-ABL mutation. Blood. 2007;109:500–502
  39. Carter TA, Wodicka LM, Shah NP, Velasco AM, Fabian MA, Treiber DK, et al. Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc Natl Acad Sci U S A. 2005;102:11011–11016
  40. National Comprehensive Cancer Network. NCCN: Clinical practice guidelines in oncology (Chronic myelogenous leukemia). 2009;© 2006 National Comprehensive Cancer Network, Inc. Version 2. Jenkintown, PA
  41. Willis SG, Lange T, Demehri S, Otto S, Crossman L, Niederwieser D, et al. High-sensitivity detection of BCR-ABL kinase domain mutations in imatinib-naive patients: correlation with clonal cytogenetic evolution but not response to therapy. Blood. 2005;106:2128–2137
  42. Khorashad JS, Anand M, Marin D, Saunders S, Al-Jabary T, Iqbal A, et al. The presence of a BCR-ABL mutant allele in CML does not always explain clinical resistance to imatinib. Leukemia. 2006;20:658–663
  43. Sherbenou DW, Wong MJ, Humayun A, McGreevey LS, Harrell P, Yang R, et al. Mutations of the BCR-ABL-kinase domain occur in a minority of patients with stable complete cytogenetic response to imatinib. Leukemia. 2007;21:489–493

 Editorial support was provided by Daniel Hutta, PhD, and Michael Mandola, PhD (Health Interactions) on behalf of Novartis Oncology.

 STATEMENT OF CONFLICT OF INTEREST: Dr Jabbour is on the Speakers Bureau for Novartis Pharmaceuticals Corp. Dr Soverini has no relationships with the supplement sponsor to disclose.

PII: S0037-1963(09)00020-1

doi: 10.1053/j.seminhematol.2009.01.009

Seminars in Hematology
Volume 46 , Pages S22-S26 , April 2009