The microRNA miR-92 increases proliferation of myeloid cells and by targeting p63 modulates the abundance of its isoforms

FASEB Journal

Volumn 23, Issue 11, 2009, Pages 3957-3966

  Manni, Isabella ^a   Artuso, Simona ^a   Careccia, Silvia ^a   Rizzo, Maria Giulia ^a   Baserga, Renato ^b   Piaggio, Giulia ^a   Sacchi, Ada ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

3 UTR; Hematopoiesis; p53 family; Small noncoding RNAs

Indexed keywords

ANTAGOMIR; BROXURIDINE; GRANULOCYTE COLONY STIMULATING FACTOR; LUCIFERASE; MICRORNA; MICRORNA 92; OLIGONUCLEOTIDE; PROTEIN P63; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL CYCLE; CELL DEATH; CELL GROWTH; CELL LINE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL;

3' UNTRANSLATED REGIONS; ANTIGENS, CD; CELL PROLIFERATION; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; HCT116 CELLS; HUMANS; MICRORNAS; MYELOID CELLS; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN ISOFORMS;

EID: 70350560746     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-131847     Document Type: Article

References (50)

1. Ambros, V. (2004) The functions of animal microRNAs. Nature 431, 350-355
2. Zhang, B., Pan, X., Cobb, G. P., and Anderson, T. A. (2007) microRNAs as oncogenes and tumor suppressors. Dev. Biol. 302, 1-12 (review)
3. Griffiths-Jones, S., Grocock, R. J., van Dongen, S., Bateman, A., and Enright, A. J. (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, 140-144
4. Meister, G., and Tuschl, T. (2004) Mechanisms of gene silencing by doublestranded RNA. Nature 31, 343-349 (Pubitemid 39265674)
5. Yue, J., and Tigyi, G. (2006) MicroRNA trafficking and human cancer. Cancer Biol. Ther. 5, 573-578
6. Esquela-Kerscher, A., and Slack, F. J. (2006) Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259-269
7. Carleton, M., Cleary, M. A., and Linsley, P. S. (2007) MicroRNAs and cell cycle regulation. Cell Cycle 6, 2127-2132
8. Ma, L., and Weinberg, R. A. (2008) MicroRNAs in malignant progression. Cell Cycle 7, 570-572
9. Ota, A., Tagawa, H., Karnan, S., Tsuzuki, S., Karpas, A., Kira, S., Yoshida, Y., and Seto, M. (2004) Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res. 64, 3087-3095 (Pubitemid 38581408)
10. Hayashita, Y., Osada, H., Tatematsu, Y., Yamada, H., Yanagisawa, K., Tomida, S., Yatabe, Y., Kawahara, K., Sekido, Y., and Takahashi, T. (2005) A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res. 65, 9628-9633 (Pubitemid 41541436)
11. Chen, A,. Luo, M., Yuan, G., Yu, J., Deng, T., Zhang, L., Zhou, Y., Mitchelson, K., and Cheng, J. (2008) Complementary analysis of microRNA and mRNA expression during phorbol 12-myristate 13-acetate (TPA)-induced differentiation of HL-60 cells. Biotechnol. Lett. 30, 2045-2052
12. He, L., Thomson, J. M., Hemann, M. T., Hernando-Monge, E., Mu, D., Goodson, S., Powers, S., Cordon-Cardo, C., Lowe, S. W., Hannon, G. J., and Hammond, S. M. (2005) A microRNA polycistron as a potential human oncogene. Nature 435, 828-833 (Pubitemid 40839734)
13. Venturini, L., Battmer, K., Castoldi, M., Schultheis, B., Hochhaus, A., Muckenthaler, M. U., 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)
14. Xiao, C., Srinivasan, L., Calado, D. P., Patterson, H. C., Zhang, B., Wang, J., Henderson, J. M., Kutok, J. L., and Rajewsky, K. (2008) Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol. 9, 405-414
15. Ventura, A., Young, A. G., Winslow, M. M., Lintault, L., Meissner, A., Erkeland, S. J., Newman, J., Bronson, R. T., Crowley, D., Stone, J. R., Jaenisch, R., Sharp, P. A., and Jacks, T. (2008) Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132, 875-886 (Pubitemid 351312807)
16. Mills, A. A., Zheng, B., Wang, X. J., Vogel, H., Roop, D. R., and Bradley, A. (1999) p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708-713 (Pubitemid 29197649)
17. Yang, A., Schweitzer, R., Sun, D., Kaghad, M., Walker, N., Bronson, R. T., Tabin, C., Sharpe, A., Caput, D., Crum, C., and McKeon, F. (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398, 714-718 (Pubitemid 29197650)
18. Yang, A., Kaghad, M., Wang, Y., Gillett, E., Fleming, M. D., Dotsch, V., Andrews, N. C., Caput, D., and McKeon, F. (1998) p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell 2, 305-316 (Pubitemid 128379271)
19. Yi, R., Poy, M. N., Stoffel, M., and Fuchs, E. (2008) A skin microRNA promotes differentiation by repressing 'stemness.' Nature 452, 225-229
20. Lena, A. M., Shalom-Feuerstein, R., di Val Cervo, P. R., Aberdam, D., Knight, R. A., Melino, G., and Candi, E. (2008) miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ. 15, 1187-1195
21. Papagiannakopoulos, T., Shapiro, A., and Kosik, K. S. (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 68, 8164-8172
22. Valtieri, M., Tweardy, D. J., Caracciolo, D., Johnson, K., Mavilio, F., Altmann, S., Santoli, D., and Rovera, G. (1987) Cytokine-dependent granulocytic differentiation. Regulation of proliferative and differentiative responses in a murine progenitor cell line. J. Immunol. 138, 3829-3835 (Pubitemid 17078259)
23. Askew, D. S., Ashmun, R. A., Simmons, B. C., and Cleveland, J. L. (1991) Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6, 1915-1922
24. Zhou-Li, F., Xu, S. Q., Dews, M., and Baserga, R. (1997) Co-operation of simian virus 40 T antigen and insulin receptor substrate-1 in protection from apoptosis induced by interleukin-3 withdrawal. Oncogene 15, 961-970 (Pubitemid 27399557)
25. Shi, B., Prisco, M., Calin, G., Liu, C. G., Russo, G., Giordano, A., and Baserga, R. (2006) Expression profiles of microRNA in proliferating and differentiating 32D murine myeloid cells. J. Cell. Physiol. 207, 706-710 (Pubitemid 43668234)
26. Ando, K., and Griffin, J. D. (1995) Cdk4 integrates growth stimulatory and inhibitory signals during G1 phase of hematopoietic cells. Oncogene 10, 751-755
27. Cummins, J. M., He, Y., Leary, R. J., Pagliarini, R., Diaz, L. A. Jr., Sjoblom, T., Barad, O., Bentwich, Z., Szafranska, A. E., Labourier, E., Raymond, C. K., Roberts, B. S., Juhl, H., Kinzler, K. W., Vogelstein, B., and Velculescu, V. E. (2006) The colorectal microRNAome. Proc. Natl. Acad. Sci. U. S. A. 103, 3687-3692
28. Wu, G., Osada, M., Guo, Z., Fomenkov, A., Begum, S., Zhao, M., Upadhyay, S., Xing, M., Wu, F., Moon, C., Westra, W. H., Koch, W. M., Mantovani, R., Califano, J. A., Ratovitski, E., Sidransky, D., and Trink, B. (2005) ΔNp63α up-regulates the Hsp70 gene in human cancer. Cancer Res. 65, 758-766 (Pubitemid 40216433)
29. Brasier, A. R., Tate, J. E., and Habener, J. F. (1989) Optimized use of the firefly luciferase assay as a reporter gene in mammalian cell lines. BioTechniques 7, 1116-1122
30. Patterson, M. K., Jr. (1979) Measurement of growth and viability of cells in culture. In Cell culture. Methods in Enzymology, Vol.58 (Jakoby, W. B. and Pastan, I. H., eds) pp. 141-152, Academic Press, New York
31. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25, 402-408 (Pubitemid 34164012)
32. Gurtner, A., Manni, I., Fuschi, P., Mantovani, R., Guadagni, F., Sacchi, A., and Piaggio, G. (2003) Requirement for down regulatation of the CCAAT-binding activity of the NF-Y transcription factor during skeletal muscle differentiation. Mol. Biol. Cell 14, 2706-2715 (Pubitemid 36871515)
33. Lecellier, C. H., Dunoyer, P., Arar, K., Lehmann-Che, J., Eyquem, S., Himber, C., Saïb, A., and Voinnet, O. (2005) A cellular microRNA mediates antiviral defense in human cells. Science 308, 557-560 (Pubitemid 40570587)
34. Lu, Y., Thomson, J. M., Wong, H. Y., Hammond, S. M., and Hogan, B. L. (2007) Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev. Biol. 310, 442-453 (Pubitemid 47483685)
35. Matsubara, H., Takeuchi, T., Nishikawa, E., Yanagisawa, K., Hayashita, Y., Ebi, H., Yamada, H., Suzuki, M., Nagino, M., Nimura, Y., Osada, H., and Takahashi, T. (2007) Apoptosis induction by antisense oligonucleotides against miR-17-5p and miR-20a in lung cancers overexpressing miR-17-92. Oncogene 26, 6099-6105 (Pubitemid 47373805)
36. Mendell, J. T. (2008) miRiad roles for the miR-17-92 cluster in development and disease. Cell 133, 217-222
37. Pichiorri, F., Suh, S. S., Ladetto, M., Kuehl, M., Palumbo, T., Drandi, D., Taccioli, C., Zanesi, N., Alder, H., Hagan, J. P., Munker, R., Volinia, S., Boccadoro, M., Garzon, R., Palumbo, A., Aqeilan, R. I., and Croce, C. M. (2008) MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 105, 12885-12890
38. Cloonan, N., Brown, M. K., Steptoe, A. L., Wani, S., Chan, W. L., Forrest, A. R., Kolle, G., Gabrielli, B., Grimmond, S. M. (2008) The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol. 9, R127
39. Wang, L., Pal, S., and Sif, S. (2008) Protein arginine methyltransferase 5 suppresses the transcription of the RB family of tumor suppressors in leukemia and lymphoma cells. Mol. Cell. Biol. 28, 6262-6277
40. Nagel, S., Venturini, L., Przybylski, G. K., Grabarczyk, P., Schmidt, C. A., Meyer, C., Drexler, H. G., Macleod, R. A., and Scherr, M. (2009) Activation of miR-17-92 by NK-like homeodomain proteins suppresses apoptosis via reduction of E2F1 in T-cell acute lymphoblastic leukemia. Leuk. Lymphoma 15, 1-8
41. Koralov, S. B., Muljo, S. A., Galler, G. R., Krek, A., Chakraborty, T., Kanellopoulou, C., Jensen, K., Cobb, B. S., Merkenschlager, M., Rajewsky, N., and Rajewsky, K. (2008) Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell 132, 860-874 (Pubitemid 351312808)
42. Petrocca, F., Vecchione, A., and Croce, C. M. (2008) Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res. 68, 8191-8194
43. Yang, A., Zhu, Z., Kapranov, P., McKeon, F., Church, G. M., Gingeras, T. R., and Struhl, K. (2006) Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol. Cell. 24, 593-602 (Pubitemid 350284225)
44. Petitjean, A., Ruptier, C., Tribollet, V., Hautefeuille, A., Chardon, F., Cavard, C., Puisieux, A., Hainaut, P., and Caron de Fromentel, C. (2008) Properties of the six isoforms of p63: p53-like regulation in response to genotoxic stress and cross talk with DeltaNp73. Carcinogenesis 29, 273-281
45. Candi, E., Dinsdale, D., Rufini, A., Salomoni, P., Knight, R. A., Mueller, M., Krammer, and P. H., Melino, G. (2007) TAp63 and DeltaNp63 in cancer and epidermal development. Cell Cycle 6, 274-285 (Pubitemid 46271573)
46. Truong, A. B., and Khavari, P. A. (2007) Control of keratinocyte proliferation and differentiation by p63. Cell Cycle 6, 295-299 (Pubitemid 46271576)
47. Koster, M. I., Lu, S. L., White, L. D., Wang, X. J., and Roop, D. R. (2006) Reactivation of developmentally expressed p63 isoforms predisposes to tumor development and progression. Cancer Res. 66, 3981-3986
48. Barbieri, C. E., Tang, L. J., Brown, K. A., and Pietenpol, J. A. (2006) Loss of p63 leads to increased cell migration and up-regulation of genes involved in invasion and metastasis. Cancer Res. 66, 7589-7597
49. Dohn, M., Zhang, S., and Chen, X. (2001) p63alpha and DeltaNp63alpha can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene 20, 3193-3205 (Pubitemid 32553672)
50. Testoni, B., and Mantovani, R. (2006) Mechanisms of transcriptional repression of cell-cycle G2/M promoters by p63. Nucleic Acids Res. 34, 928-938 (Pubitemid 43380676)