The oncogenic MicroRNA miR-22 targets the TET2 tumor suppressor to promote hematopoietic stem cell self-renewal and transformation

Cell Stem Cell

Volumn 13, Issue 1, 2013, Pages 87-101

  Song, Su Jung ^a   Ito, Keisuke ^a,d   Ala, Ugo ^a   Kats, Lev ^a   Webster, Kaitlyn ^a   Sun, Su Ming ^b   Jongen Lavrencic, Mojca ^b   Manova Todorova, Katia ^c   Teruya Feldstein, Julie ^c   Avigan, David E ^a   Delwel, Ruud ^b   Pandolfi, Pier Paolo ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; MICRORNA 22; TEN ELEVEN TRANSLOCATION 2 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; LUCIFERASE; MESSENGER RNA; MICRORNA; MIRN22 MICRORNA, MOUSE; ONCOPROTEIN; TET2 PROTEIN, HUMAN;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL RENEWAL; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOLOGY; DOWN REGULATION; EPIGENETICS; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKEMIA CELL; MOUSE; MYELODYSPLASTIC SYNDROME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STEM CELL; ANIMAL; C57BL MOUSE; ENZYME IMMUNOASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; HEMATOLOGIC DISEASE; METABOLISM; MORTALITY; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEMATOLOGIC NEOPLASMS; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOENZYME TECHNIQUES; LUCIFERASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; MYELODYSPLASTIC SYNDROMES; PROTO-ONCOGENE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SURVIVAL RATE;

EID: 84880571480     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.06.003     Document Type: Article

References (47)

1. Abdel-Wahab, O., Mullally, A., Hedvat, C., Garcia-Manero, G., Patel, J., Wadleigh, M., Malinge, S., Yao, J., Kilpivaara, O., Bhat, R., et al. (2009). Genetic characterization of TET1, TET2, and TET3 alterations in myeloid malignancies. Blood 114, 144-147.
2. Abdel-Wahab, O., Manshouri, T., Patel, J., Harris, K., Yao, J., Hedvat, C., Heguy, A., Bueso-Ramos, C., Kantarjian, H., Levine, R.L., and Verstovsek, S. (2010). Genetic analysis of transforming events that convert chronic myeloproliferative neoplasms to leukemias. Cancer Res. 70, 447-452.
3. Arnold, C.P., Tan, R., Zhou, B., Yue, S.B., Schaffert, S., Biggs, J.R., Doyonnas, R., Lo, M.C., Perry, J.M., Renault, V.M., et al. (2011). MicroRNA programs in normal and aberrant stem and progenitor cells. Genome Res. 21, 798-810.
4. Bartel, D.P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
5. Berger, A.H., Knudson, A.G., and Pandolfi, P.P. (2011). A continuum model for tumour suppression. Nature 476, 163-169.
6. Betel, D., Wilson, M., Gabow, A., Marks, D.S., and Sander, C. (2008). The microRNA.org resource: targets and expression. Nucleic Acids Res. 36(Database issue), D149-D153.
7. Branco, M.R., Ficz, G., and Reik, W. (2012). Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 13, 7-13.
8. Calin, G.A., and Croce, C.M. (2006). MicroRNA signatures in human cancers. Nat. Rev. Cancer 6, 857-866.
9. Chen, C.Z., Li, L., Lodish, H.F., and Bartel, D.P. (2004). MicroRNAs modulate hematopoietic lineage differentiation. Science 303, 83-86.
10. Delhommeau, F., Dupont, S., Della Valle, V., James, C., Trannoy, S., Massé, A., Kosmider, O., Le Couedic, J.P., Robert, F., Alberdi, A., et al. (2009). Mutation in TET2 in myeloid cancers. N. Engl. J. Med. 360, 2289-2301.
11. Di Bernardo, M.C., Crowther-Swanepoel, D., Broderick, P., Webb, E., Sellick, G., Wild, R., Sullivan, K., Vijayakrishnan, J., Wang, Y., Pittman, A.M., et al. (2008). A genome-wide association study identifies six susceptibility loci for chronic lymphocytic leukemia. Nat. Genet. 40, 1204-1210.
12. Dostalova Merkerova, M., Krejcik, Z., Votavova, H., Belickova, M., Vasikova, A., and Cermak, J. (2011). Distinctive microRNA expression profiles in CD34+ bone marrow cells from patients with myelodysplastic syndrome. Eur. J. Hum. Genet. 19, 313-319.
13. Elmén, J., Lindow, M., Schütz, S., Lawrence, M., Petri, A., Obad, S., Lindholm, M., Hedtjärn, M., Hansen, H.F., Berger, U., et al. (2008). LNA-mediated microRNA silencing in non-human primates. Nature 452, 896-899.
14. Esteller, M. (2008). Epigenetics in cancer. N. Engl. J. Med. 358, 1148-1159.
15. Ficz, G., Branco, M.R., Seisenberger, S., Santos, F., Krueger, F., Hore, T.A., Marques, C.J., Andrews, S., and Reik, W. (2011). Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398-402.
16. Figueroa, M.E., Abdel-Wahab, O., Lu, C., Ward, P.S., Patel, J., Shih, A., Li, Y., Bhagwat, N., Vasanthakumar, A., Fernandez, H.F., et al. (2010). Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18, 553-567.
17. Gangaraju, V.K., and Lin, H. (2009). MicroRNAs: key regulators of stem cells. Nat. Rev. Mol. Cell Biol. 10, 116-125.
18. 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 (Database issue), D140-D144.
19. Ito, S., D'Alessio, A.C., Taranova, O.V., Hong, K., Sowers, L.C., and Zhang, Y. (2010). Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133.
20. Ito, S., Shen, L., Dai, Q., Wu, S.C., Collins, L.B., Swenberg, J.A., He, C., and Zhang, Y. (2011). Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303.
21. Jankowska, A.M., Szpurka, H., Tiu, R.V., Makishima, H., Afable, M., Huh, J., O'Keefe, C.L., Ganetzky, R., McDevitt, M.A., and Maciejewski, J.P. (2009). Loss of heterozygosity 4q24 and TET2 mutations associated with myelodysplastic/ myeloproliferative neoplasms. Blood 113, 6403-6410.
22. Jongen-Lavrencic, M., Sun, S.M., Dijkstra, M.K., Valk, P.J., and Löwenberg, B. (2008). MicroRNA expression profiling in relation to the genetic heterogeneity of acute myeloid leukemia. Blood 111, 5078-5085.
23. Kallin, E.M., Rodríguez-Ubreva, J., Christensen, J., Cimmino, L., Aifantis, I., Helin, K., Ballestar, E., and Graf, T. (2012). Tet2 facilitates the derepression of myeloid target genes during CEBPa-induced transdifferentiation of pre-B cells. Mol. Cell 48, 266-276.
24. Ko, M., Huang, Y., Jankowska, A.M., Pape, U.J., Tahiliani, M., Bandukwala, H.S., An, J., Lamperti, E.D., Koh, K.P., Ganetzky, R., et al. (2010). Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 468, 839-843.
25. Kosmider, O., Gelsi-Boyer, V., Cheok, M., Grabar, S., Della-Valle, V., Picard, F., Viguié, F., Quesnel, B., Beyne-Rauzy, O., Solary, E., et al.; Groupe Francophone des Myélodysplasies. (2009). TET2 mutation is an independent favorable prognostic factor in myelodysplastic syndromes (MDSs). Blood 114, 3285-3291.
26. Lanford, R.E., Hildebrandt-Eriksen, E.S., Petri, A., Persson, R., Lindow, M., Munk, M.E., Kauppinen, S., and Ørum, H. (2010). Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198-201.
27. 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.
28. Li, Z., Cai, X., Cai, C.L., Wang, J., Zhang, W., Petersen, B.E., Yang, F.C., and Xu, M. (2011). Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 118, 4509-4518.
29. Liu, T.C., Lin, P.M., Chang, J.G., Lee, J.P., Chen, T.P., and Lin, S.F. (2000). Mutation analysis of PTEN/MMAC1 in acute myeloid leukemia. Am. J. Hematol. 63, 170-175.
30. Moran-Crusio, K., Reavie, L., Shih, A., Abdel-Wahab, O., Ndiaye-Lobry, D., Lobry, C., Figueroa, M.E., Vasanthakumar, A., Patel, J., Zhao, X., et al. (2011). Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20, 11-24.
31. Patsos, G., Germann, A., Gebert, J., and Dihlmann, S. (2010). Restoration of absent in melanoma 2 (AIM2) induces G2/M cell cycle arrest and promotes invasion of colorectal cancer cells. Int. J. Cancer 126, 1838-1849.
32. Petersen, M., and Wengel, J. (2003). LNA: a versatile tool for therapeutics and genomics. Trends Biotechnol. 21, 74-81.
33. Poliseno, L., Salmena, L., Riccardi, L., Fornari, A., Song, M.S., Hobbs, R.M., Sportoletti, P., Varmeh, S., Egia, A., Fedele, G., et al. (2010). Identification of the miR-106b-25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci. Signal. 3, ra29.
34. Quivoron, C., Couronné, L., Della Valle, V., Lopez, C.K., Plo, I., Wagner-Ballon, O., Do Cruzeiro, M., Delhommeau, F., Arnulf, B., Stern, M.H., et al. (2011). TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20, 25-38.
35. Rodríguez-Paredes, M., and Esteller, M. (2011). Cancer epigenetics reaches mainstream oncology. Nat. Med. 17, 330-339.
36. Sasaki, M., Knobbe, C.B., Munger, J.C., Lind, E.F., Brenner, D., Brüstle, A., Harris, I.S., Holmes, R., Wakeham, A., Haight, J., et al. (2012). IDH1(R132H) mutation increases murine haematopoietic progenitors and alters epigenetics. Nature 488, 656-659.
37. Shen, L., Kantarjian, H., Guo, Y., Lin, E., Shan, J., Huang, X., Berry, D., Ahmed, S., Zhu, W., Pierce, S., et al. (2010). DNA methylation predicts survival and response to therapy in patients with myelodysplastic syndromes. J. Clin. Oncol. 28, 605-613.
38. Shih, A.H., Abdel-Wahab, O., Patel, J.P., and Levine, R.L. (2012). The role of mutations in epigenetic regulators in myeloid malignancies. Nat. Rev. Cancer 12, 599-612.
39. Smith, A.E., Mohamedali, A.M., Kulasekararaj, A., Lim, Z., Gäken, J., Lea, N.C., Przychodzen, B., Mian, S.A., Nasser, E.E., Shooter, C., et al. (2010). Nextgeneration sequencing of the TET2 gene in 355 MDS and CMML patients reveals low-abundance mutant clones with early origins, but indicates no definite prognostic value. Blood 116, 3923-3932.
40. Song, S.J., Poliseno, L., Song, M.S., Ala, U., Webster, K., Ng, C., Beringer, G., Brikbak, N.J., Yuan, X., Cantley, L.C., et al. (2013). microRNA-antagonism regulates breast cancer stemness and metastasis via TET family dependent chromatin remodelling. Cell 154, in press. http://dx.doi.org/ 10.1016/j.cell. 2013.06.026.
41. Stenvang, J., Silahtaroglu, A.N., Lindow, M., Elmen, J., and Kauppinen, S. (2008). The utility of LNA in microRNA-based cancer diagnostics and therapeutics. Semin. Cancer Biol. 18, 89-102.
42. Tefferi, A., Lim, K.H., Abdel-Wahab, O., Lasho, T.L., Patel, J., Patnaik, M.M., Hanson, C.A., Pardanani, A., Gilliland, D.G., and Levine, R.L. (2009). Detection of mutant TET2 in myeloid malignancies other than myeloproliferative neoplasms: CMML, MDS, MDS/MPN and AML. Leukemia 23, 1343-1345.
43. Wang, J., Xiang, G., Zhang, K., and Zhou, Y. (2012). Expression signatures of intragenic miRNAs and their corresponding host genes in myeloid leukemia cells. Biotechnol. Lett. 34, 2007-2015.
44. Yamazaki, J., Taby, R., Vasanthakumar, A., Macrae, T., Ostler, K.R., Shen, L., Kantarjian, H.M., Estecio, M.R., Jelinek, J., Godley, L.A., and Issa, J.P. (2012). Effects of TET2 mutations on DNA methylation in chronic myelomonocytic leukemia. Epigenetics 7, 201-207.
45. Yilmaz, O.H., Valdez, R., Theisen, B.K., Guo, W., Ferguson, D.O., Wu, H., and Morrison, S.J. (2006). Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441, 475-482.
46. Zhang, J., Grindley, J.C., Yin, T., Jayasinghe, S., He, X.C., Ross, J.T., Haug, J.S., Rupp, D., Porter-Westpfahl, K.S., Wiedemann, L.M., et al. (2006). PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441, 518-522.
47. Zhang, Y., Roccaro, A.M., Rombaoa, C., Flores, L., Obad, S., Fernandes, S.M., Sacco, A., Liu, Y., Ngo, H., Quang, P., et al. (2012). LNA-mediated anti-miR-155 silencing in low-grade B-cell lymphomas. Blood 120, 1678-1686.