MiR-638 regulates differentiation and proliferation in leukemic cells by targeting cyclin-dependent kinase

Journal of Biological Chemistry

Volumn 290, Issue 3, 2015, Pages 1818-1828

  Lin, Yi ^a   Li, Dengju ^b   Liang, Qing ^c   Liu, Shangqing ^c   Zuo, Xuelan ^c   Li, Lin ^d   Sun, Xuemei ^d   Li, Wenxin ^a   Guo, Mingxiong ^a   Huang, Zan ^a  

^a WUHAN UNIVERSITY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c ZHONGNAN HOSPITAL OF WUHAN UNIVERSITY   (China)

^d NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CYTOLOGY; DISEASES; ENZYMES;

ACUTE MYELOID LEUKEMIA; CYCLIN-DEPENDENT KINASE; DIAGNOSIS AND PROGNOSIS; DIFFERENTIATION AND PROLIFERATIONS; ECTOPIC EXPRESSIONS; LEUKEMIA THERAPIES; MYELOID DIFFERENTIATION; PHORBOL 12 MYRISTATE 13 ACETATES;

CELLS;

CYCLIN DEPENDENT KINASE 2; MICRORNA; MICRORNA 638; UNCLASSIFIED DRUG; CDK2 PROTEIN, HUMAN; MIRN638 MICRORNA, HUMAN; OLIGONUCLEOTIDE; PHORBOL 13 ACETATE 12 MYRISTATE; TUMOR MARKER;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CANCER PROGNOSIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMOGENESIS; PHENOTYPE; PRIMARY TUMOR; PROTEIN TARGETING; RNA PROCESSING; UPREGULATION; ACUTE MYELOBLASTIC LEUKEMIA; GENETICS; HEK293 CELL LINE; HEMATOPOIESIS; HL 60 CELL LINE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY; TUMOR CELL LINE;

BASE SEQUENCE; BIOMARKERS, TUMOR; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 2; GENE EXPRESSION REGULATION, LEUKEMIC; HEK293 CELLS; HEMATOPOIESIS; HL-60 CELLS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICRORNAS; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES; PHENOTYPE; SEQUENCE HOMOLOGY, NUCLEIC ACID; TETRADECANOYLPHORBOL ACETATE; UP-REGULATION;

EID: 84922190602     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.599191     Document Type: Article

References (57)

1. Palma, C. A., Tonna, E. J., Ma, D. F., and Lutherborrow, M. A. (2012) MicroRNA control of myelopoiesis and the differentiation block in acute myeloid leukaemia. J. Cell Mol. Med. 16, 978-987
2. Mrózek, K., Heerema, N. A., and Bloomfield, C. D. (2004) Cytogenetics in acute leukemia. Blood Rev. 18, 115-136
3. Hackanson, B., Bennett, K. L., Brena, R. M., Jiang, J., Claus, R., Chen, S. S., Blagitko-Dorfs, N., Maharry, K., Whitman, S. P., Schmittgen, T. D., Lübbert, M., Marcucci, G., Bloomfield, C. D., and Plass, C. (2008) Epigenetic modification of CCAAT/enhancer binding protein alpha expression in acute myeloid leukemia. Cancer Res. 68, 3142-3151
4. Garzon, R., Liu, S., Fabbri, M., Liu, Z., Heaphy, C. E., Callegari, E., Schwind, S., Pang, J., Yu, J., Muthusamy, N., Havelange, V., Volinia, S., Blum, W., Rush, L. J., Perrotti, D., Andreeff, M., Bloomfield, C. D., Byrd, J. C., Chan, K., Wu, L. C., Croce, C. M., and Marcucci, G. (2009) MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directlyDNMT3Aand 3B and indirectly DNMT1. Blood 113, 6411-6418
5. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
6. Mineno, J., Okamoto, S., Ando, T., Sato, M., Chono, H., Izu, H., Takayama, M., Asada, K., Mirochnitchenko, O., Inouye, M., and Kato, I. (2006) The expression profile of microRNAs in mouse embryos. Nucleic Acids Res. 34, 1765-1771
7. Wang, X. S., Gong, J. N., Yu, J., Wang, F., Zhang, X. H., Yin, X. L., Tan, Z. Q., Luo, Z. M., Yang, G. H., Shen, C., and Zhang, J. W. (2012) MicroRNA-29a and microRNA-142-3p are regulators of myeloid differentiation and acute myeloid leukemia. Blood 119, 4992-5004
8. Tsukamoto, Y., Nakada, C., Noguchi, T., Tanigawa, M., Nguyen, L. T., Uchida, T., Hijiya, N., Matsuura, K., Fujioka, T., Seto, M., and Moriyama, M. (2010) MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res. 70, 2339-2349
9. Garzon, R., Pichiorri, F., Palumbo, T., Iuliano, R., Cimmino, A., Aqeilan, R., Volinia, S., Bhatt, D., Alder, H., Marcucci, G., Calin, G. A., Liu, C. G., Bloomfield, C. D., Andreeff, M., and Croce, C. M. (2006) MicroRNA fingerprints during human megakaryocytopoiesis. Proc. Natl. Acad. Sci. U.S.A. 103, 5078-5083
10. Mukai, H. Y., Motohashi, H., Ohneda, O., Suzuki, N., Nagano, M., and Yamamoto, M. (2006) Transgene insertion in proximity to the c-myb gene disrupts erythroid-megakaryocytic lineage bifurcation. Mol. Cell. Biol. 26, 7953-7965
11. Fukao, T., Fukuda, Y., Kiga, K., Sharif, J., Hino, K., Enomoto, Y., Kawamura, A., Nakamura, K., Takeuchi, T., and Tanabe, M. (2007) An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell 129, 617-631
12. Calin, G. A., Dumitru, C. D., Shimizu, M., Bichi, R., Zupo, S., Noch, E., Aldler, H., Rattan, S., Keating, M., Rai, K., Rassenti, L., Kipps, T., Negrini, M., Bullrich, F., and Croce, C. M. (2002) Frequent deletions and downregulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. U.S.A. 99, 15524-15529
13. Pulikkan, J. A., Dengler, V., Peramangalam, P. S., Peer Zada, A. A., Müller-Tidow, C., Bohlander, S. K., Tenen, D. G., and Behre, G. (2010) Cell-cycle regulator E2F1 and microRNA-223 comprise an autoregulatory negative feedback loop in acute myeloid leukemia. Blood 115, 1768-1778
14. Salvatori, B., Iosue, I., Djodji Damas, N., Mangiavacchi, A., Chiaretti, S., Messina, M., Padula, F., Guarini, A., Bozzoni, I., Fazi, F., and Fatica, A. (2011) Critical Role of c-Myc in Acute Myeloid Leukemia Involving Direct Regulation of miR-26a and Histone Methyltransferase EZH2. Genes Cancer 2, 585-592
15. Favreau, A. J., Cross, E. L., and Sathyanarayana, P. (2012) miR-199b-5p directly targets PODXL and DDR1 and decreased levels of miR-199b-5p correlate with elevated expressions ofPODXLand DDR1 in acute myeloid leukemia. Am. J. Hematol. 87, 442-446
16. Lin, Y., Zeng, Y., Zhang, F., Xue, L., Huang, Z., Li, W., and Guo, M. (2013) Characterization of MicroRNA Expression Profiles and the Discovery of Novel MicroRNAs Involved in Cancer during Human Embryonic Development. PLoS One 8, e69230
17. Li, P., Liu, Y., Yi, B., Wang, G., You, X., Zhao, X., Summer, R., Qin, Y., and Sun, J. (2013) MicroRNA-638 is highly expressed in human vascular smooth muscle cells and inhibits PDGF-BB-induced cell proliferation and migration through targeting orphan nuclear receptor NOR1. Cardiovasc. Res. 99, 185-193
18. Li, D., Wang, Q., Liu, C., Duan, H., Zeng, X., Zhang, B., Li, X., Zhao, J., Tang, S., Li, Z., Xing, X., Yang, P., Chen, L., Zeng, J., Zhu, X., Zhang, S., Zhang, Z., Ma, L., He, Z., Wang, E., Xiao, Y., Zheng, Y., and Chen, W. (2012) Aberrant expression of miR-638 contributes to benzo(a)pyreneinduced human cell transformation. Toxicol. Sci. 125, 382-391
19. Tanaka, M., Oikawa, K., Takanashi, M., Kudo, M., Ohyashiki, J., Ohyashiki, K., and Kuroda, M. (2009) Down-regulation of miR-92 in human plasma is a novel marker for acute leukemia patients. PLoS One 4, e5532
20. Li, J., Liu, K., Liu, Y., Xu, Y., Zhang, F., Yang, H., Liu, J., Pan, T., Chen, J., Wu, M., Zhou, X., and Yuan, Z. (2013) Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity. Nat. Immunol. 14, 793-803
21. Jaiswal, R., Luk, F., Gong, J., Mathys, J. M., Grau, G. E., and Bebawy, M. (2012) Microparticle conferred microRNA profiles: implications in the transfer and dominance of cancer traits. Mol. Cancer 11, 37
22. Lal, A., Pan, Y., Navarro, F., Dykxhoorn, D. M., Moreau, L., Meire, E., Bentwich, Z., Lieberman, J., and Chowdhury, D. (2009) miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat. Struct. Mol. Biol. 16, 492-498
23. Wang, J., Xiang, G., Mitchelson, K., and Zhou, Y. (2011) Microarray profiling of monocytic differentiation reveals miRNA-mRNA intrinsic correlation. J. Cell. Biochem. 112, 2443-2453
24. Kharfan-Dabaja, M., Ayala, E., Lindner, I., Cejas, P. J., Bahlis, N. J., Kolonias, D., Carlson, L. M., and Lee, K. P. (2005) Differentiation of acute and chronic myeloid leukemic blasts into the dendritic cell lineage: analysis of various differentiation-inducing signals. Cancer Immunol. Immunother. 54, 25-36
25. Dubois, C., Schlageter, M. H., de Gentile, A., Guidez, F., Balitrand, N., Toubert, M. E., Krawice, I., Fenaux, P., Castaigne, S., and Najean, Y. (1994) Hematopoietic growth factor expression and ATRA sensitivity in acute promyelocytic blast cells. Blood 83, 3264-3270
26. Fazi, F., Rosa, A., Fatica, A., Gelmetti, V., De Marchis, M. L., Nervi, C., and Bozzoni, I. (2005) A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPα regulates human granulopoiesis. Cell 123, 819-831
27. Benedetti, L., Grignani, F., Scicchitano, B. M., Jetten, A. M., Diverio, D., Lo Coco, F., Avvisati, G., Gambacorti-Passerini, C., Adamo, S., Levin, A. A., Pelicci, P. G., and Nervi, C. (1996) Retinoid-induced differentiation of acute promyelocytic leukemia involves PML-RARα-mediated increase of type II transglutaminase. Blood 87, 1939-1950
28. Liu, L., Wen, Q., Gong, R., Gilles, L., Stankiewicz, M. J., Li, W., Guo, M., Li, L., Sun, X., Li, W., Crispino, J. D., and Huang, Z. (2014) PSTPIP2 dysregulation contributes to aberrant terminal differentiation in GATA-1-deficient megakaryocytes by activating LYN. Cell Death Dis. 5, e988
29. Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T., and Tada, K. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26, 171-176
30. Gallagher, R., Collins, S., Trujillo, J., McCredie, K., Ahearn, M., Tsai, S., Metzgar, R., Aulakh, G., Ting, R., Ruscetti, F., and Gallo, R. (1979) Characterization of the continuous, differentiating myeloid cell line (HL-60) from a patient with acute promyelocytic leukemia. Blood 54, 713-733
31. Duprez, E., Tong, J. H., Dérré, J., Chen, S. J., Berger, R., Chen, Z., and Lanotte, M. (1997) JEM-1, a novel gene encoding a leucine-zipper nuclear factor upregulated during retinoid-induced maturation of NB4 promyelocytic leukaemia. Oncogene 14, 1563-1570
32. Weil, S. C., Rosner, G. L., Reid, M. S., Chisholm, R. L., Farber, N. M., Spitznagel, J. K., and Swanson, M. S. (1987) cDNA cloning of human myeloperoxidase: decrease in myeloperoxidase mRNA upon induction of HL-60 cells. Proc. Natl. Acad. Sci. U.S.A. 84, 2057-2061
33. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
34. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20
35. Schmitz, N. M., Leibundgut, K., and Hirt, A. (2005) CDK2 catalytic activity and loss of nuclear tethering of retinoblastoma protein in childhood acute lymphoblastic leukemia. Leukemia 19, 1783-1787
36. Wang, K., Xu, L., Pan, L., Xu, K., and Li, G. (2014) The functional BRCA1 rs799917 genetic polymorphism is associated with gastric cancer risk in a Chinese Han population. Tumour Biol. 10.1007/s13277-014-2655-9
37. Ma, K., Pan, X., Fan, P., He, Y., Gu, J., Wang, W., Zhang, T., Li, Z., and Luo, X. (2014) Loss of miR-638 in vitro promotes cell invasion and a mesenchymal-like transition by influencing SOX2 expression in colorectal carcinoma cells. Mol. Cancer 13, 118
38. Zhao, L. Y., Yao, Y., Han, J., Yang, J., Wang, X. F., Tong, D. D., Song, T. S., Huang, C., and Shao, Y. (2014) miR-638 suppresses cell proliferation in gastric cancer by targeting Sp2. Dig. Dis. Sci. 59, 1743-1753
39. Jiang, X., Huang, H., Li, Z., He, C., Li, Y., Chen, P., Gurbuxani, S., Arnovitz, S., Hong, G. M., Price, C., Ren, H., Kunjamma, R. B., Neilly, M. B., Salat, J., Wunderlich, M., Slany, R. K., Zhang, Y., Larson, R. A., Le Beau, M. M., Mulloy, J. C., Rowley, J. D., and Chen, J. (2012) MiR-495 is a tumor-suppressor microRNA down-regulated in MLL-rearranged leukemia. Proc. Natl. Acad. Sci. U.S.A. 109, 19397-19402
40. Zhu, D. X., Zhu, W., Fang, C., Fan, L., Zou, Z. J., Wang, Y. H., Liu, P., Hong, M., Miao, K. R., Liu, P., Xu, W., and Li, J. Y. (2012) miR-181a/b significantly enhances drug sensitivity in chronic lymphocytic leukemia cells via targeting multiple anti-apoptosis genes. Carcinogenesis 33, 1294-1301
41. Johnnidis, J. B., Harris, M. H., Wheeler, R. T., Stehling-Sun, S., Lam, M. H., Kirak, O., Brummelkamp, T. R., Fleming, M. D., and Camargo, F. D. (2008) Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 451, 1125-1129
42. Eyholzer, M., Schmid, S., Wilkens, L., Mueller, B. U., and Pabst, T. (2010) The tumour-suppressive miR-29a/b1 cluster is regulated by CEBPA and blocked in human AML. Br. J. Cancer 103, 275-284
43. Seca, H., Almeida, G. M., Guimarães, J. E., and Vasconcelos, M. H. (2010) miR signatures and the role of miRs in acute myeloid leukaemia. Eur. J. Cancer 46, 1520-1527
44. Wang, X., Gocek, E., Liu, C. G., and Studzinski, G. P. (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
45. Chen, C. Z., Li, L., Lodish, H. F., and Bartel, D. P. (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303, 83-86
46. O'Connell, R. M., Rao, D. S., Chaudhuri, A. A., Boldin, M. P., Taganov, K. D., Nicoll, J., Paquette, R. L., and Baltimore, D. (2008) Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J. Exp. Med. 205, 585-594
47. Radomska, H. S., Huettner, C. S., Zhang, P., Cheng, T., Scadden, D. T., and Tenen, D. G. (1998) CCAAT/enhancer binding protein α is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Mol. Cell. Biol. 18, 4301-4314
48. Subramanian, S., Thayanithy, V., West, R. B., Lee, C. H., Beck, A. H., Zhu, S., Downs-Kelly, E., Montgomery, K., Goldblum, J. R., Hogendoorn, P. C., Corless, C. L., Oliveira, A. M., Dry, S. M., Nielsen, T. O., Rubin, B. P., Fletcher, J. A., Fletcher, C. D., and van de Rijn, M. (2010) Genome-wide transcriptome analyses reveal p53 inactivation-mediated loss of miR-34a expression in malignant peripheral nerve sheath tumours. J. Pathol. 220, 58-70
49. Tikoo, R., Casaccia-Bonnefil, P., Chao, M. V., and Koff, A. (1997) Changes in cyclin-dependent kinase 2 and p27kip1 accompany glial cell differentiation of central glia-4 cells. J. Biol. Chem. 272, 442-447
50. Martinez, L. A., Chen, Y., Fischer, S. M., and Conti, C. J. (1999) Coordinated changes in cell cycle machinery occur during keratinocyte terminal differentiation. Oncogene 18, 397-406
51. Klausen, P., Bjerregaard, M. D., Borregaard, N., and Cowland, J. B. (2004) End-stage differentiation of neutrophil granulocytes in vivo is accompanied by up-regulation of p27kip1 and down-regulation of CDK2, CDK4, and CDK6. J. Leukoc. Biol. 75, 569-578
52. Lim, S., and Kaldis, P. (2012) Loss of Cdk2 and Cdk4 induces a switch from proliferation to differentiation in neural stem cells. Stem Cells 30, 1509-1520
53. Dobashi, Y., Shoji, M., Kitagawa, M., Noguchi, T., and Kameya, T. (2000) Simultaneous suppression of cdc2 and cdk2 activities induces neuronal differentiation of PC12 cells. J. Biol. Chem. 275, 12572-12580
54. Aref, S., Mabed, M., El-Sherbiny, M., Selim, T., and Metwaly, A. (2006) Cyclin D1 expression in acute leukemia. Hematology 11, 31-34
55. Wessendorf, S., Schwaenen, C., Kohlhammer, H., Kienle, D., Wrobel, G., Barth, T. F., Nessling, M., Möller, P., Döhner, H., Lichter, P., and Bentz, M. (2003) Hidden gene amplifications in aggressive B-cell non-Hodgkin lymphomas detected by microarray-based comparative genomic hybridization. Oncogene 22, 1425-1429
56. Büschges, R., Weber, R. G., Actor, B., Lichter, P., Collins, V. P., and Reifenberger, G. (1999) Amplification and expression of cyclin D genes (CCND1, CCND2 and CCND3) in human malignant gliomas. Brain Pathol. 9, 435-442; discussion 432-433
57. Rehmsmeier, M., Steffen, P., Höchsmann, M., and Giegerich, R. (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10, 1507-1517