Lyn kinase-dependent regulation of miR181 and myeloid cell leukemia-1 expression: Implications for drug resistance in myelogenous leukemia

Molecular Pharmacology

Volumn 78, Issue 5, 2010, Pages 811-817

  Zimmerman, Eric I ^a   Dollins, Claudia M ^b   Crawford, Melissa ^c   Grant, Steven ^d   Nana Sinkam, Serge P ^c   Richards, Kristy L ^b   Hammond, Scott M ^b   Graves, Lee M ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; IMATINIB; LUCIFERASE; MICRORNA; MICRORNA 181B; MICRORNA 181D; PROTEIN KINASE LYN; PROTEIN MCL 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CANCER RESISTANCE; CELL STRAIN HL 60; CELL STRAIN K 562; ENZYME INHIBITION; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; MYELOID LEUKEMIA; PRIORITY JOURNAL; REPORTER GENE; SEQUENCE ANALYSIS;

ANTINEOPLASTIC AGENTS; CALCITRIOL; CELL LINE, TUMOR; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; LEUKEMIA, MYELOID; MICRORNAS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIMIDINES; SRC-FAMILY KINASES;

EID: 77958134349     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.066258     Document Type: Article

References (42)

1. Ambros V (2001) microRNAs: tiny regulators with great potential. Cell 107:823-826.
2. Bagrintseva K, Geisenhof S, Kern R, Eichenlaub S, Reindl C, Ellwart JW, Hiddemann W, and Spiekermann K (2005) FLT3-ITD-TKD dual mutants associated with AML confer resistance to FLT3 PTK inhibitors and cytotoxic agents by overexpression of Bcl-x(L). Blood 105:3679-3685. (Pubitemid 40628216)
3. Breitenbuecher F, Markova B, Kasper S, Carius B, Stauder T, Böhmer FD, Masson K, Rönnstrand L, Huber C, Kindler T, et al. (2009) A novel molecular mechanism of primary resistance to FLT3-kinase inhibitors in AML. Blood 113:4063-4073.
4. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, et al. (2005) A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353:1793-1801. (Pubitemid 41549891)
5. Chen CZ, Li L, Lodish HF, and Bartel DP (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303:83-86. (Pubitemid 38055775)
6. Chen G, Zhu W, Shi D, Lv L, Zhang C, Liu P, and Hu W (2010) MicroRNA-181a sensitizes human malignant glioma U87MG cells to radiation by targeting Bcl-2. Oncol Rep 23:997-1003.
7. Chen L, Yan HX, Yang W, Hu L, Yu LX, Liu Q, Li L, Huang DD, Ding J, Shen F, et al. (2009) The role of microRNA expression pattern in human intrahepatic cholangiocarcinoma. J Hepatol 50:358-369.
8. Crawford M, Batte K, Yu L, Wu X, Nuovo GJ, Marsh CB, Otterson GA, and Nana-Sinkam SP (2009) MicroRNA 133B targets pro-survival molecules MCL-1 and BCL2L2 in lung cancer. Biochem Biophys Res Commun 388:483-489.
9. Dai Y, Rahmani M, Corey SJ, Dent P, and Grant S (2004) A Bcr/Abl-independent, Lyn-dependent form of imatinib mesylate (STI-571) resistance is associated with altered expression of Bcl-2. J Biol Chem 279:34227-34239. (Pubitemid 39318046)
10. Debernardi S, Skoulakis S, Molloy G, Chaplin T, Dixon-McIver A, and Young BD (2007) MicroRNA miR-181a correlates with morphological sub-class of acute myeloid leukaemia and the expression of its target genes in global genome-wide analysis. Leukemia 21:912-916. (Pubitemid 46672066)
11. Dixon-McIver A, East P, Mein CA, Cazier JB, Molloy G, Chaplin T, Andrew Lister T, Young BD, and Debernardi S (2008) Distinctive patterns of microRNA expression associated with karyotype in acute myeloid leukaemia. PLoS One 3:e2141. (Pubitemid 352025167)
12. Donato NJ, Wu JY, Stapley J, Gallick G, Lin H, Arlinghaus R, and Talpaz M (2003) BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood 101:690-698. (Pubitemid 36077594)
13. Eiring AM, Harb JG, Neviani P, Garton C, Oaks JJ, Spizzo R, Liu S, Schwind S, Santhanam R, Hickey CJ, et al. (2010) miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 140:652-665.
14. Hammond SM (2006) MicroRNAs as oncogenes. Curr Opin Genet Dev 16:4-9.
15. Hochhaus A, Kreil S, Corbin AS, La Rosée P, Müller MC, Lahaye T, Hanfstein B, Schoch C, Cross NC, Berger U, et al. (2002) Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia 16:2190-2196. (Pubitemid 35331833)
16. Hummel R, Hussey DJ, and Haier J (2010) MicroRNAs: predictors and modifiers of chemo- and radiotherapy in different tumour types. Eur J Cancer 46:298-311.
17. Illmer T, Schaich M, Platzbecker U, Freiberg-Richter J, Oelschlägel U, von Bonin M, Pursche S, Bergemann T, Ehninger G, and Schleyer E (2004) P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate. Leukemia 18:401-408. (Pubitemid 38425851)
18. Ito T, Tanaka H, and Kimura A (2007) Establishment and characterization of a novel imatinib-sensitive chronic myeloid leukemia cell line MYL, and an imatinib-resistant subline MYL-R showing overexpression of Lyn. Eur J Haematol 78:417-431. (Pubitemid 46558198)
19. Kaufmann SH, Karp JE, Svingen PA, Krajewski S, Burke PJ, Gore SD, and Reed JC (1998) Elevated expression of the apoptotic regulator Mcl-1 at the time of leukemic relapse. Blood 91:991-1000. (Pubitemid 28078303)
20. Khusial PR, Vadla B and Goldberg GS (2009) Src regulates the expression of Lin28: implications for cell growth, adhesion, and communication. Cell Commun Adhes 15:407-409.
21. Li S (2008) Src-family kinases in the development and therapy of Philadelphia chromosome-positive chronic myeloid leukemia and acute lymphoblastic leukemia. Leuk Lymphoma 49:19-26. (Pubitemid 351146878)
22. Liu S, Wu LC, Pang J, Santhanam R, Schwind S, Wu YZ, Hickey CJ, Yu J, Becker H, Maharry K, et al. (2010) Sp1/NFkappaB/HDAC/miR-29b regulatory network in KIT-driven myeloid leukemia. Cancer Cell 17:333-347.
23. Marcucci G, Radmacher MD, Maharry K, Mrózek K, Ruppert AS, Paschka P, Vukosavljevic T, Whitman SP, Baldus CD, Langer C, et al. (2008) MicroRNA expression in cytogenetically normal acute myeloid leukemia. N Engl J Med 358:1919-1928. (Pubitemid 351620112)
24. Mott JL, Kobayashi S, Bronk SF, and Gores GJ (2007) mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26:6133-6140. (Pubitemid 47414372)
25. Nam S, Williams A, Vultur A, List A, Bhalla K, Smith D, Lee FY, and Jove R (2007) Dasatinib (BMS-354825) inhibits Stat5 signaling associated with apoptosis in chronic myelogenous leukemia cells. Mol Cancer Ther 6:1400-1405. (Pubitemid 46712003)
26. Neilson JR, Zheng GX, Burge CB, and Sharp PA (2007) Dynamic regulation of miRNA expression in ordered stages of cellular development. Genes Dev 21:578-589.
27. Newman MA, Thomson JM, and Hammond SM (2008) Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14:1539-1549.
28. Okamoto M, Hayakawa F, Miyata Y, Watamoto K, Emi N, Abe A, Kiyoi H, Towatari M, and Naoe T (2007) Lyn is an important component of the signal transduction pathway specific to FLT3/ITD and can be a therapeutic target in the treatment of AML with FLT3/ITD. Leukemia 21:403-410.
29. San José-Enériz E, Román-Gómez J, Jiménez-Velasco A, Garate L, Martin V, Cordeu L, Vilas-Zornoza A, Rodríguez-Otero P, Calasanz MJ, Prósper F, et al. (2009) MicroRNA expression profiling in imatinib-resistant chronic myeloid leukemia patients without clinically significant ABL1-mutations. Mol Cancer 8:69.
30. Schwind SGM, Maharry K, Radmacher MD, Whitman SP, Paschka P, Mrózek K, Kolitz JE, Larson RE, and Bloomfield CD (2009) MicroRNA 181a (miR-181a) expression as a prognosticator in cytogenetically normal acute myeloid leukemia (CN AML) (Abstract). J Clin Oncol 27:7001.
31. Shangary S and Johnson DE (2003) Recent advances in the development of anticancer agents targeting cell death inhibitors in the Bcl-2 protein family. Leukemia 17:1470-1481. (Pubitemid 36986949)
32. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Muckenthaler MU, Ganser A, Eder M, and Scherr M (2007) Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Blood 109:4399-4405. (Pubitemid 46743409)
33. Wang Q, Zimmerman EI, Toutchkine A, Martin TD, Graves LM and Lawrence D (2010a) Multicolor monitoring of dysregulated protein kinases in chronic myelogenous leukemia. ACS Chem Biol doi: 10.1021/cb100099h.
34. Wang QM, Studzinski GP, Chen F, Coffman FD, and Harrison LE (2000) p53/56(lyn) antisense shifts the 1,25-dihydroxyvitamin D3-induced G1/S block in HL60 cells to S phase. J Cell Physiol 183:238-246. (Pubitemid 30185942)
35. Wang WX, Wilfred BR, Xie K, Jennings MH, Hu Y, Stromberg AJ, and Nelson PT (2010b) Individual microRNAs (miRNAs) display distinct mRNA targeting "rules". RNA Biol 7:373-380.
36. Wang X, Gocek E, Liu CG, and Studzinski GP (2009) MicroRNAs181 regulate the expression of p27Kip1 in human myeloid leukemia cells induced to differentiate by 1,25-dihydroxyvitamin D3. Cell Cycle 8:736-741.
37. Wang X and Studzinski GP (1997) Antiapoptotic action of 1,25-dihydroxyvitamin D3 is associated with increased mitochondrial MCL-1 and RAF-1 proteins and reduced release of cytochrome c. Exp Cell Res 235:210-217. (Pubitemid 27381699)
38. Warr MR and Shore GC (2008) Unique biology of Mcl-1: therapeutic opportunities in cancer. Curr Mol Med 8:138-147.
39. Wu J, Meng F, Kong LY, Peng Z, Ying Y, Bornmann WG, Darnay BG, Lamothe B, Sun H, Talpaz M, et al. (2008) Association between imatinib-resistant BCR-ABL mutation-negative leukemia and persistent activation of LYN kinase. J Natl Cancer Inst 100:926-939. (Pubitemid 351957515)
40. Xu HM, Tepper CG, Jones JB, Fernandez CE, and Studzinski GP (1993) 1,25-Dihydroxyvitamin D3 protects HL60 cells against apoptosis but down-regulates the expression of the bcl-2 gene. Exp Cell Res 209:367-374.
41. Yamamoto M, Kurosu T, Kakihana K, Mizuchi D, and Miura O (2004) The two major imatinib resistance mutations E255K and T315I enhance the activity of BCR/ABL fusion kinase. Biochem Biophys Res Commun 319:1272-1275. (Pubitemid 38759547)
42. Zhong Q, Gao W, Du F, and Wang X (2005) Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121:1085-1095. (Pubitemid 40884398)