High imatinib dose overcomes insufficient response associated with ABCG2 haplotype in chronic myelogenous leukemia patients

Oncotarget

Volumn 4, Issue 10, 2013, Pages 1582-1591

  Delord, Marc ^a   Philippe Rousselot, ^b   Jean Michel Cayuela, ^c,d   Francois Sigaux ^a,c   Joelle Guilhot ^e   Claude Preudhomme, ^f   Francois Guilhot ^e   Pascale Loiseau, ^g   Emmanuel Raffoux, ^g   Daniela Geromin, ^g   Emmanuelle Genin ^h   Fabien Calvo, ^d,g   Bruzzoni Giovanelli, Heriberto ^d,g  

^a UNIVERSITÉ PARIS DIDEROT   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^c Laboratoire Central d'Hematologie   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e POITIERS UNIVERSITY HOSPITAL   (France)

^f UNIV LILLE   (France)

^g SAINT LOUIS HOSPITAL   (France)

^h UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

Author keywords

ABCG2; BCR ABL; CML; Imatinib; Molecular response; Pharmacogenetic; SNPs

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; IMATINIB;

ABCG2 GENE; ADULT; ALLELE; ARTICLE; CHRONIC MYELOID LEUKEMIA; COHORT ANALYSIS; CUMULATIVE INCIDENCE OF MAJOR MOLECULAR RESPONSE; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG DOSE INCREASE; DRUG TRANSPORT; FEMALE; GENE; GENE FREQUENCY; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MYELOID LEUKEMIA; SINGLE NUCLEOTIDE POLYMORPHISM;

ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BENZAMIDES; COHORT STUDIES; DNA, NEOPLASM; FEMALE; GENOTYPE; HAPLOTYPES; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MALE; MIDDLE AGED; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHARMACOGENETICS; PIPERAZINES; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSPECTIVE STUDIES; PYRIMIDINES; RETROSPECTIVE STUDIES; TREATMENT OUTCOME;

EID: 84886739824     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1050     Document Type: Article

References (49)

1. Hochhaus A, O'Brien SG, Guilhot F, Druker BJ, Branford S, Foroni L, Goldman JM, Müller MC, Radich JP, Rudoltz M, Mone M, Gathmann I, Hughes TP, Larson RA. Sixyear follow-up of patients receiving imatinib for the fi rstline treatment of chronic myeloid leukemia. Macmillan Publishers Limited; 2009:1054-1061. Available at: http:// www.ncbi.nlm.nih.gov/pubmed/19282833.
2. Kantarjian H, Shah NP, Hochhaus A, Cortes J, Shah S, Ayala M, Moiraghi B, Shen Z, Mayer J, Pasquini R, Nakamae H, Huguet F, Boqué C, Chuah C, Bleickardt E, Bradley-Garelik MB, Zhu C, Szatrowski T, Shapiro D, Baccarani M. Dasatinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukemia. The New England Journal of Medicine. 2010;362(24):2260-2270.
3. Saglio G, Kim D-W, Issaragrisil S, Le Coutre P, Etienne G, Lobo C, Pasquini R, Clark RE, Hochhaus A, Hughes TP, Gallagher N, Hoenekopp A, Dong M, Haque A, Larson RA, Kantarjian HM. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. The New England Journal of Medicine. 2010;362(24):2251-2259.
4. Aichberger KJ, Herndlhofer S, Schernthaner G-H, Schillinger M, Mitterbauer-Hohendanner G, Sillaber C, Valent P. Progressive peripheral arterial occlusive disease and other vascular events during nilotinib therapy in CML. American Journal of Hematology. 2011;86(7):1-7.
5. Montani D, Bergot E, Gunther S, Savale L, Bergeron A, Bourdin A, Bouvaist H, Canuet M, Pison C, Macro M, Poubeau P, Girerd B, Natali D, Guignabert C, Perros F, O'Callaghan DS, Jais X, Tubert-Bitter P, Zalcman G, Sitbon O, Simonneau G, Humbert M. Pulmonary Arterial Hypertension in Patients Treated by Dasatinib. Circulation. 2012;125(17):2128-37.
6. Kantarjian HM, O'Brien S, Cortes J, Giles FJ, Rios MB, Shan J, Faderl S, Garcia-Manero G, Ferrajoli A, Verstovsek S, Wierda W, Keating M, Talpaz M. Imatinib Mesylate Therapy Improves Survival in Patients with Newly Diagnosed Philadelphia Chromosome-Positive Chronic Myelogenous Leukemia in the Chronic Phase. Cancer. 2003;98:2636-2642.
7. Kantarjian HM, Hochhaus A, Saglio G, Souza C De, Flinn IW, Stenke L, Goh Y-T, Rosti G, Nakamae H, Gallagher NJ, Hoenekopp A, Blakesley RE, Larson RA, Hughes TP. Nilotinib versus imatinib for the treatment of patients with newly diagnosed chronic phase, Philadelphia chromosomepositive, chronic myeloid leukaemia: 24-month minimum follow-up of the phase 3 randomised ENESTnd trial. The lancet oncology. 2011;12(9):841-851.
8. Kantarjian HM, Shah NP, Cortes JE, Baccarani M, Agarwal MB, Undurraga MS, Wang J, Kassack Ipiña JJ, Kim D-W, Ogura M, Pavlovsky C, Junghanss C, Milone JH, Nicolini FE, Robak T, Van Droogenbroeck J, Vellenga E, Bradley-Garelik MB, Zhu C, Hochhaus A. Dasatinib or imatinib in newly diagnosed chronic-phase chronic myeloid leukemia: 2-year follow-up from a randomized phase 3 trial (DASISION). Blood. 2012;119(5):1123-9.
9. Chomel J, Turhan AG. Chronic myeloid leukemia stem cells in the era of targeted therapies: resistance, persistence and long-term dormancy. Oncotarget. 2011;2(9):713-27.
10. Larson RA, Druker BJ, Guilhot F, O'Brien SG, Riviere GJ, Krahnke T, Gathmann I, Wang Y. Imatinib pharmacokinetics and its correlation with response and safety in chronic-phase chronic myeloid leukemia: a subanalysis of the IRIS study. Blood. 2008;111(8):4022-4028.
11. Marin D, Bazeos A, Mahon F-X, Eliasson L, Milojkovic D, Bua M, Apperley JF, Szydlo R, Desai R, Kozlowski K, Paliompeis C, Latham V, Foroni L, Molimard M, Reid A, Rezvani K, de Lavallade H, Guallar C, Goldman J, Khorashad JS. Adherence is the critical factor for achieving molecular responses in patients with chronic myeloid leukemia who achieve complete cytogenetic responses on imatinib. Journal of clinical oncology. 2010;28(14):2381-2388.
12. Picard S, Titier K, Etienne G, Teilhet E, Ducint D, Bernard M-A, Lassalle R, Marit G, Reiffers J, Begaud B, Moore N, Molimard M, Mahon F-X. Trough imatinib plasma levels are associated with both cytogenetic and molecular responses to standard-dose imatinib in chronic myeloid leukemia. Blood. 2007;109(8):3496-3499.
13. Chen H-C, Hu W-X, Liu Q-X, Li W-K, Chen F-Z, Rao Z-Z, Liu X-F, Luo Y-P, Cao Y-F. Genetic polymorphisms of metabolic enzymes CYP1A1, CYP2D6, GSTM1 and GSTT1 and leukemia susceptibility. European journal of cancer prevention. 2008;17(3):251-258.
14. Kim DHD, Xu W, Ma C, Liu X, Siminovitch K, Messner HA, Lipton JH. Genetic variants in the candidate genes of the apoptosis pathway and susceptibility to chronic myeloid leukemia. Blood. 2009;113(11):2517-2525.
15. Taspinar M, Aydos SE, Comez O, Elhan AH, Karabulut HG, Sunguroglu A. CYP1A1, GST gene polymorphisms and risk of chronic myeloid leukemia. Swiss medical weekly. 2008;138(1-2):12-17.
16. Zhang Y, Wang B, Ye S, Liu S, Liu M, Shen C, Teng Y, Qi J. Killer cell immunoglobulin-like receptor gene polymorphisms in patients with leukemia: possible association with susceptibility to the disease. Leukemia research. 2010;34(1):55-58.
17. Boultwood J, Perry J, Zaman R, Fernandez-Santamaria C, Littlewood T, Kusec R, Pellagatti A, Wang L, Clark RE, Wainscoat JS. High-density single nucleotide polymorphism array analysis and ASXL1 gene mutation screening in chronic myeloid leukemia during disease progression. Leukemia. 2010;24(6):1139-1145.
18. Zhang S-J, Shi J-Y, Li J-Y. GATA-2 L359 V mutation is exclusively associated with CML progression but not other hematological malignancies and GATA-2 P250A is a novel single nucleotide polymorphism. Leukemia research. 2009;33(8):1141-1143.
19. Nambu T, Hamada A, Nakashima R, Yuki M, Kawaguchi T, Mitsuya H, Saito H. Association of SLCO1B3 polymorphism with intracellular accumulation of imatinib in leukocytes in patients with chronic myeloid leukemia. Biological & pharmaceutical bulletin. 2011;34(1):114-119.
20. Angelini S, Soverini S, Ravegnini G, Barnett M, Turrini E, Thornquist M, Pane F, Hughes TP, White DL, Radich J, Kim D-W, Saglio G, Cilloni D, Iacobucci I, Perini G, Woodman R, Cantelli-Forti G, Baccarani M, Hrelia P, Martinelli G. Association between imatinib transporters and metabolizing enzymes genotype and response in newly diagnosed chronic myeloid leukemia patients receiving imatinib therapy. Haematologica. 2013;98(2):193-200.
21. Crossman LC, O'Hare T, Lange T, Willis SG, Stoffregen EP, Corbin AS, O'Brien SG, Heinrich MC, Druker BJ, Middleton PG, Deininger MWN. A single nucleotide polymorphism in the coding region of ABL and its effects on sensitivity to imatinib. Leukemia. 2005;19(11):1859-1862.
22. Dulucq S, Bouchet S, Turcq B, Lippert E, Etienne G, Reiffers J, Molimard M, Krajinovic M, Mahon F-X. Multidrug resistance gene (MDR1) polymorphisms are associated with major molecular responses to standarddose imatinib in chronic myeloid leukemia. Blood. 2008;112(5):2024-2027.
23. Guillem VM, Cervantes F, Martínez J, Alvarez-Larrán A, Collado M, Camós M, Sureda A, Maffioli M, Marugán I, Hernández-Boluda J-C. XPC genetic polymorphisms correlate with the response to imatinib treatment in patients with chronic phase chronic myeloid leukemia. American journal of hematology. 2010;85(7):482-486.
24. Kim DH, Xu W, Kamel-Reid S, Liu X, Jung CW, Kim S, Lipton JH. Clinical relevance of vascular endothelial growth factor (VEGFA) and VEGF receptor (VEGFR2) gene polymorphism on the treatment outcome following imatinib therapy. Annals of oncology. 2010;21(6):1179-1188.
25. Kim DHD, Kong JH, Byeun JY, Jung CW, Xu W, Liu X, Kamel-Reid S, Kim Y-K, Kim H-J, Lipton JH. The IFNG (IFN-gamma) genotype predicts cytogenetic and molecular response to imatinib therapy in chronic myeloid leukemia. Clinical cancer research. 2010;16(21):5339-5350.
26. Kim DHD, Sriharsha L, Xu W, Kamel-Reid S, Liu X, Siminovitch K, Messner HA, Lipton JH. Clinical relevance of a pharmacogenetic approach using multiple candidate genes to predict response and resistance to imatinib therapy in chronic myeloid leukemia. Clinical cancer research. 2009;15(14):4750-4758.
27. Maffioli M, Camós M, Gaya A, Hernández-Boluda J-C, Alvarez-Larrán A, Domingo A, Granell M, Guillem V, Vallansot R, Costa D, Bellosillo B, Colomer D, Cervantes F. Correlation between genetic polymorphisms of the hOCT1 and MDR1 genes and the response to imatinib in patients newly diagnosed with chronic-phase chronic myeloid leukemia. Leukemia Research. 2011;35(8):1014-1019.
28. Ni L-N, Li J-Y, Miao K-R, Qiao C, Zhang S-J, Qiu H-R, Qian S-X. Multidrug resistance gene (MDR1) polymorphisms correlate with imatinib response in chronic myeloid leukemia. Medical oncology. 2011;28(1):265-269.
29. Deenik W, van der Holt B, Janssen JJWM, Chu IWT, Valk PJM, Ossenkoppele GJ, van der Heiden IP, Sonneveld P, van Schaik RHN, Cornelissen JJ. Polymorphisms in the multidrug resistance gene MDR1 (ABCB1) predict for molecular resistance in patients with newly diagnosed chronic myeloid leukemia receiving high-dose imatinib. Blood. 2010;116(26):6144-6146. .
30. Dulucq S, Preudhomme C, Guilhot F, Mahon F-X. Response: is there really a relationship between Multidrug Resistance Gene (MDR1) polymorphisms and major molecular response to imatinib in chronic myeloid leukemia? Blood. 2010;116(26):6145-6146.
31. Giles FJ, Rosti G, Beris P, Clark RE, Le Coutre P, Mahon F-X, Steegmann J-L, Valent P, Saglio G. Nilotinib is superior to imatinib as fi rst-line therapy of chronic myeloid leukemia: the ENESTnd study. Expert review of hematology. 2010;3(6):665-673.
32. Baccarani M, Cortes J, Pane F, Niederwieser D, Saglio G, Apperley J, Cervantes F, Deininger M, Gratwohl A, Guilhot F, Hochhaus A, Horowitz M, Hughes T, Kantarjian H, Larson R, Radich J, Simonsson B, Silver RT, Goldman J, Hehlmann R. Chronic myeloid leukemia: an update of concepts and management recommendations of European LeukemiaNet. Journal of clinical oncology offi cial journal of the American Society of Clinical Oncology. 2009;27(35):6041-6051.
33. Simon RM, Paik S, Hayes DF. Use of archived specimens in evaluation of prognostic and predictive biomarkers. Journal of the National Cancer Institute. 2009;101(21):1446-52.
34. Ahmed I, Tamouza R, Delord M, Krishnamoorthy R, Tzourio C, Mulot C, Nacfer M, Lambert J-C, Beaune P, Laurent-Puig P, Loriot M-A, Charron D, Elbaz A. Association between Parkinson's disease and the HLADRB1 locus. Movement disorders. 2012;27(9):1104-10. .
35. Hehlmann R, Lauseker M, Jung-Munkwitz S, Leitner A, Müller MC, Pletsch N, Proetel U, Haferlach C, Schlegelberger B, Balleisen L, Hänel M, Pfirrmann M, Krause SW, Nerl C, Pralle H, Gratwohl A, Hossfeld DK, Hasford J, Hochhaus A, Saussele S. Tolerability-adapted imatinib 800 mg/d versus 400 mg/d versus 400 mg/d plus interferon-a in newly diagnosed chronic myeloid leukemia. Journal of clinical oncology. 2011;29(12):1634-1642.
36. Preudhomme C, Guilhot J, Nicolini FE, Guerci-Bresler A, Rigal-Huguet F, Maloisel F, Coiteux V, Gardembas M, Berthou C, Vekhoff A, Rea D, Jourdan E, Allard C, Delmer A, Rousselot P, Legros L, Berger M, Corm S, Etienne G, Roche-Lestienne C, Eclache V, Mahon F-X, Guilhot F. Imatinib plus peginterferon alfa-2a in chronic myeloid leukemia. The New England journal of medicine. 2010;363(26):2511-2521.
37. Ieiri I. Functional signifi cance of genetic polymorphisms in P-glycoprotein (MDR1, ABCB1) and breast cancer resistance protein (BCRP, ABCG2). Drug metabolism and pharmacokinetics. Int J Biochem Mol Biol. 2012;27(1):85-105.
38. Mo W, Zhang J-T. Human ABCG2: structure, function, and its role in multidrug resistance. International journal of biochemistry and molecular biology. 2012;3(1):1-27.
39. White DL, Dang P, Engler J, Frede A, Zrim S, Osborn M, Saunders VA, Manley PW, Hughes TP. Functional activity of the OCT-1 protein is predictive of long-term outcome in patients with chronic-phase chronic myeloid leukemia treated with imatinib. J Clin Oncol. 2010; 28:2761-2767.
40. White, D.L. Saunders, V.A. Dang, P. Engler, J. Hughes TP. OCT-1 activity measurement provides a superior imatinib response predictor than screening for single-nucleotide polymorphisms of OCT-1. Leukemia. 2010;24(11):1962-1965.
41. Hughes T, Deininger M, Hochhaus A, Branford S, Radich J, Kaeda J, Baccarani M, Cortes J, Cross NCP, Druker BJ, Gabert J, Grimwade D, Hehlmann R, Kamel-Reid S, Lipton JH, Longtine J, Martinelli G, Saglio G, Soverini S, Stock W, Goldman JM. 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(1):28-37.
42. Site 1000 Genomes Project ftp. Ftp://ftp.1000genomes.ebi. ac.uk/. Available at: ftp://ftp.1000genomes.ebi.ac.uk/.
43. http://www.1000genomes.org/.
44. Latouche A, Porcher R, Chevret S. Sample size formula for proportional hazards modelling of competing risks. Statistics in Medicine. 2004;23(21):3263-3274.
45. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B Methodological. 1995;57(1):289-300.
46. Schaid DJ, Rowland CM, Tines DE, Jacobson RM, Poland GA. Score Tests for Association between Traits and Haplotypes when Linkage Phase Is Ambiguous. American journal of human genetics. 2002;70(2):425-434.
47. Sinnwell JP SD. Haplo.stats: Statistical Analysis of Haplotypes with Traits and Covariates when Linkage Phase is Ambiguous. R package version 1.4.4.
48. Site SG and GEMC. http://mayoresearch.mayo.edu/mayo/ research/schaid_lab/. Available at: http://mayoresearch. mayo.edu/mayo/research/schaid_lab/software.cfm).
49. González, Juan R; Armengol, Lluís; Guinó, Elisabet; Solé, Xavier; Moreno V. http://cran.r-project.org/web/packages/ SNPassoc/index.html.