Instability of mRNA expression signatures of drug transporters in chronic myeloid leukemia patients resistant to imatinib

Oncology Reports

Volumn 29, Issue 2, 2013, Pages 741-750

  Gromicho, Marta ^a   Magalhães, Marta ^a   Torres, Fátima ^b   Dinis, Joana ^a   Fernandes, Alexandra R ^c,d,e   Rendeiro, Paula ^b   Tavares, Purificação ^b   Laires, António ^a   Rueff, José ^a   Rodrigues, António Sebastião ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b CGC GENETICS   (Portugal)

^c UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^d UNIVERSIDADE LUSÓFONA DE HUMANIDADES E TECNOLOGIAS   (Portugal)

^e INSTITUTO SUPERIOR TÉCNICO   (Portugal)

Author keywords

ABCB1; ABCC1; ABCG2; BCR ABL1; Chronic myeloid leukemia; Drug resistance; Drug transporters; Imatinib; MVP; SLC22A1; Tyrosine kinase inhibitors

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; DASATINIB; IMATINIB; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; ORGANIC CATION TRANSPORTER; PROTEIN SLCA22A12; UNCLASSIFIED DRUG;

ABCB1 GENE; ABCC1 GENE; ABCG2 GENE; ADULT; AGED; ARTICLE; CANCER PATIENT; CHRONIC MYELOID LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; DNA POLYMORPHISM; DOSE RESPONSE; FEMALE; GENE EXPRESSION; GENE MUTATION; GENOTYPE; HUMAN; MVP GENE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; SLC22A12 GENE; TREATMENT RESPONSE; TUMOR GENE;

ADULT; AGED; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BENZAMIDES; DNA MUTATIONAL ANALYSIS; DRUG RESISTANCE, NEOPLASM; FEMALE; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOTYPE; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MALE; MIDDLE AGED; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; ORGANIC ANION TRANSPORTERS; ORGANIC CATION TRANSPORT PROTEINS; P-GLYCOPROTEIN; PIPERAZINES; POLYMORPHISM, GENETIC; PYRIMIDINES; RNA, MESSENGER; STATISTICS, NONPARAMETRIC; VAULT RIBONUCLEOPROTEIN PARTICLES; YOUNG ADULT;

EID: 84872768729     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2012.2153     Document Type: Article

References (57)

1. Druker BJ: Translation of the Philadelphia chromosome into therapy for CML. Blood 112: 4808-4817, 2008.
2. Jabbour E, Cortes J and Kantarjian H: Long-term outcomes in the second-line treatment of chronic myeloid leukemia: a review of tyrosine kinase inhibitors. Cancer 117: 897-906, 2011.
3. Hochhaus A, O'Brien SG, Guilhot F, et al: Six-year follow-up of patients receiving imatinib for the first-line treatment of chronic myeloid leukemia. Leukemia 23: 1054-1061, 2009.
4. de Lavallade H, Apperley J F, Khorashad JS, et al: Imatinib for newly diagnosed patients with chronic myeloid leukemia: incidence of sustained responses in an intention-to-treat analysis. J Clin Oncol 26: 3358-3363, 2008.
5. Marin D, Milojkovic D, Olavarria E, et al: European LeukemiaNet criteria for failure or suboptimal response reliably identify patients with CML in early chronic phase treated with imatinib whose eventual outcome is poor. Blood 112: 4437-4444, 2008.
6. Baccarani M, Castagnetti F, Gugliotta G, Palandri F and Soverini S: Response definitions and European Leukemianet Management recommendations. Best Pract Res Clin Haematol 22: 331-341, 2009.
7. Soverini S, Colarossi S, Gnani 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 12: 7374-7379, 2006. (Pubitemid 46095411)
8. Larson RA, Druker BJ, Guilhot F, et al: Imatinib pharmacokinetics and its correlation with response and safety in chronic-phase chronic myeloid leukemia: a subanalysis of the IRIS study. Blood 111: 4022-4028, 2008.
9. Picard S, Titier K, Etienne G, et al: Trough imatinib plasma levels are associated with both cytogenetic and molecular responses to standard-dose imatinib in chronic myeloid leukemia. Blood 109: 3496-3499, 2007. (Pubitemid 46572540)
10. Thomas J, Wang L, Clark RE and Pirmohamed M: Active transport of imatinib into and out of cells: implications for drug resistance. Blood 104: 3739-3745, 2004. (Pubitemid 39564452)
11. White DL, Saunders VA, Dang P, et al: Most CML patients who have a suboptimal response to imatinib have low OCT-1 activity: higher doses of imatinib may overcome the negative impact of low OCT-1 activity. Blood 110: 4064-4072, 2007. (Pubitemid 350248463)
12. Clark RE, Davies A, Pirmohamed M and Giannoudis A: Pharmacologic markers and predictors of responses to imatinib therapy in patients with chronic myeloid leukemia. Leuk Lymphoma 49: 639-642, 2008. (Pubitemid 351517203)
13. Wang L, Giannoudis A, Lane S, Williamson P, Pirmohamed M and Clark R: Expression of the uptake drug transporter hOCT1 is an important clinical determinant of the response to imatinib in chronic myeloid leukemia. Clin Pharmacol Ther 83: 258-264, 2008.
14. Rodrigues AS, Dinis J, Gromicho M, Martins C, Laires A and Rueff J: Genomics and cancer drug resistance. Curr Pharm Biotechnol 13: 651-673, 2012.
15. Cortez MAA, Scrideli CA, Yunes JA, et al: mRNA expression profile of multidrug resistance genes in childhood acute lymphoblastic leukemia. Low expression levels associated with a higher risk of toxic death. Pediatr Blood Cancer 53: 996-1004, 2009.
16. Raaijmakers MHGP: ATP-binding-cassette transporters in hematopoietic stem cells and their utility as therapeutical targets in acute and chronic myeloid leukemia. Leukemia 21: 2094-2102, 2007. (Pubitemid 47430452)
17. Steiner E, Holzmann K, Elbling L, Micksche M and Berger W: Cellular functions of vaults and their involvement in multidrug resistance. Curr Drug Targets 7: 923-934, 2006.
18. Vasconcelos FC, Silva KL, Souza PSD, et al: Variation of MDR protein expression and activity levels according to clinical status and evolution of CML patients. Cytometry B Clin Cytom 80: 158-166, 2010.
19. Stromskaya T, Rybalkina EY, Kruglov S, et al: Role of p-glycoprotein in evolution of populations of chronic myeloid leukemia cells treated with imatinib. Biochemistry (Mosc) 73: 29-37, 2008. (Pubitemid 351653320)
20. Gromicho M, Dinis J, Magalhães M, et al: Development of imatinib and dasatinib resistance: dynamics of expression of drug transporters ABCB1, ABCC1, ABCG2, MVP, and SLC22A1. Leuk Lymphoma 52: 1980-1990, 2011.
21. Nijmeijer BA, Szuhai K, Goselink HM, et al: Long-term culture of primary human lymphoblastic leukemia cells in the absence of serum or hematopoietic growth factors. Exp Hematol 37: 376-385, 2009.
22. van Dongen JJ, Macintyre EA, Gabert JA, et al: Standardized RT-PCR analysis of fusion gene transcripts from chromosome aberrations in acute leukemia for detection of minimal residual disease. Report of the BIOMED-1 Concerted Action: investigation of minimal residual disease in acute leukemia. Leukemia 13: 1901-1928, 1999.
23. Gabert J, Beillard E, van der Velden VHJ, et al: Standardization and quality control studies of 'real-time' quantitative reverse transcriptase polymerase chain reaction of fusion gene transcripts for residual disease detection in leukemia - a Europe Against Cancer program. Leukemia 17: 2318-2357, 2003. (Pubitemid 38072573)
24. Schefe JH, Lehmann KE, Buschmann IR, Unger T and FunkeKaiser H: Quantitative real-time RT-PCR data analysis: current concepts and the novel 'gene expression's CT difference' formula. J Mol Med 84: 901-910, 2006. (Pubitemid 44655868)
25. Crossman LC, Druker BJ, Deininger MWN, Pirmohamed M, Wang L and Clark RE: hOCT 1 and resistance to imatinib. Blood 106: 1133-1134, 2005.
26. Burger H, van Tol H, Brok M, et al: Chronic imatinib mesylate exposure leads to reduced intracellular drug accumulation by induction of the ABCG2 (BCRP) and ABCB1 (MDR1) drug transport pumps. Cancer Biol Therapy 4: 747-752, 2005. (Pubitemid 41351174)
27. Gardner ER, Sparreboom A, Verweij J and Figg WD: Lack of ABC transporter autoinduction in mice following long-term exposure to imatinib. Cancer Biol Therapy 7: 412-415, 2008. (Pubitemid 351847058)
28. Gurney H, Wong M, Balleine RL, et al: Imatinib disposition and ABCB1 (MDR1, P-glycoprotein) genotype. Clin Pharm Ther 82: 33 - 40, 2007. (Pubitemid 46944197)
29. Xu C, Li CY-T and Kong A-NT: Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28: 249-268, 2005. (Pubitemid 44698742)
30. Eechoute K, Sparreboom A, Burger H, et al: Drug transporters and imatinib treatment: implications for clinical practice. Clin Cancer Res 17: 406-415, 2011.
31. White DL, Saunders VA, Dang P, et al: OCT-1-mediated influx is a key determinant of the intracellular uptake of imatinib but not nilotinib (AMN107): reduced OCT-1 activity is the cause of low in vitro sensitivity to imatinib. Blood 108: 697-704, 2006. (Pubitemid 44061372)
32. - cells. Leukemia 20: 750-754, 2006.
33. de Lavallade H, Finetti P, Carbuccia N, et al: A gene expression signature of primary resistance to imatinib in chronic myeloid leukemia. Leukemia Res 34: 254-257, 2010.
34. Villuendas R, Steegmann JL, Pollán M, et al: Identification of genes involved in imatinib resistance in CML: a gene-expression profiling approach. Leukemia 20: 1047-1054, 2006. (Pubitemid 43797296)
35. Lange T, Günther C, Köhler T, et al: High levels of BAX, low levels of MRP-1, and high platelets are independent predictors of response to imatinib in myeloid blast crisis of CML. Blood 101: 2152-2155, 2003. (Pubitemid 36302051)
36. Czyzewski K and Styczynski J: Imatinib is a substrate for various multidrug resistance proteins. Neoplasma 56: 202-207, 2009.
37. Shukla S, Sauna ZE and Ambudkar SV: Evidence for the interaction of imatinib at the transport-substrate site(s) of the multidrug-resistance-linked ABC drug transporters ABCB1 (P-glycoprotein) and ABCG2. Leukemia 22: 445-447, 2008. (Pubitemid 351250557)
38. Scheffer GL, Schroeijers AB, Izquierdo MA, Wiemer EA and Scheper RJ: Lung resistance-related protein/major vault protein and vaults in multidrug-resistant cancer. Curr Opin Oncol 12: 550-556, 2000. (Pubitemid 32039654)
39. White DL, Dang P, Engler J, et al: 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 28: 2761-2767, 2010.
40. + cells have reduced uptake of imatinib due to low OCT-1 activity. Leukemia 24: 765-770, 2010.
41. Hu S, Franke RM, Filipski KK, et al: Interaction of imatinib with human organic ion carriers. Clin Cancer Res 14: 3141-3148, 2008.
42. O'Hare T, Eide CA and Deininger MWN: Bcr-Abl kinase domain mutations, drug resistance, and the road to a cure for chronic myeloid leukemia. Blood 110: 2242-2249, 2007. (Pubitemid 47523141)
43. Redaelli S, Piazza R, Rostagno R, et al: Activity of bosutinib, dasatinib, and nilotinib against 18 imatinib-resistant BCR/ABL mutants. J Clin Oncol 27: 469-471, 2008.
44. Wang L, Knight K, Lucas C and Clark RE: The role of serial BCR-ABL transcript monitoring in predicting the emergence of BCR-ABL kinase mutations in imatinib-treated patients with chronic myeloid leukemia. Haematologica 91: 235-239, 2006.
45. Gruber FX, Lundán T, Goll R, et al: BCR-ABL isoforms associated with intrinsic or acquired resistance to imatinib: more heterogeneous than just ABL kinase domain point mutations? Med Oncol 29: 219-226, 2012.
46. Guilhot F, Apperley J, Kim D-W, et al: Dasatinib induces significant hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in accelerated phase. Blood 109: 4143-4150, 2007. (Pubitemid 46743375)
47. Ernst T, Hoffmann J, Erben P, et al: ABL single nucleotide polymorphisms may masquerade as BCR-ABL mutations associated with resistance to tyrosine kinase inhibitors in patients with chronic myeloid leukemia. Haematologica 93: 1389-1393, 2008.
48. Willis SG, Lange T, Demehri S, 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 106: 2128-2137, 2005. (Pubitemid 41291730)
49. + acute lymphoblastic leukemia show high rates of regression, suggesting weak selective effects. Blood 115: 5428-5429, 2010.
50. Soverini S, Hochhaus A, Nicolini FE, et al: Bcr-Abl kinase domain mutation analysis in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors: recommendations from an expert panel on behalf of European LeukemiaNet. Blood 118: 1208-1215, 2011.
51. Sharma P, Kumar L, Mohanty S and Kochupillai V: Response to imatinib mesylate in chronic myeloid leukemia patients with variant BCR-ABL fusion transcripts. Ann Hematol 89: 241-247, 2010.
52. Polampalli S, Choughule A, Negi N, et al: Analysis and comparison of clinicohematological parameters and molecular and cytogenetic response of two Bcr/Abl fusion transcripts. Genetics Mol Res 7: 1138-1149, 2008.
53. Lucas CM, Harris RJ, Giannoudis A, et al: Chronic myeloid leukemia patients with the e13a2 BCR-ABL fusion transcript have inferior responses to imatinib compared to patients with the e14a2 transcript. Haematologica 94: 1362-1367, 2009.
54. Verma D, Kantarjian HM, Jones D, et al: Chronic myeloid leukemia (CML) with P190 BCR-ABL: analysis of characteristics, outcomes, and prognostic significance. Blood 114: 2232-2235, 2009.
55. Dulucq S, Bouchet S, Turcq B, et al: Multidrug resistance gene (MDR1) polymorphisms are associated with major molecular responses to standard-dose imatinib in chronic myeloid leukemia. Blood 112: 2024-2027, 2008.
56. Ni L-N, Li J-Y, Miao K-R, et al: Multidrug resistance gene (MDR1) polymorphisms correlate with imatinib response in chronic myeloid leukemia. Med Oncol 28: 265-269, 2011.
57. Kim DHD, Sriharsha L, Xu W, et al: Clinical relevance of a pharmacogenetic approach using multiple candidate genes to predict response and resistance to imatinib therapy in chronic myeloid leukemia. Clin Cancer Res 15: 4750-4758, 2009.