Characterization of a set of tumor suppressor microRNAs in T cell acute lymphoblastic leukemia

Science Signaling

Volumn 7, Issue 352, 2014, Pages

  Sanghvi, Viraj R ^a   Mavrakis, Konstantinos J ^a   Van Der Meulen, Joni ^a,b   Boice, Michael ^a,c   Wolfe, Andrew L ^a,c   Carty, Mark ^a,c   Mohan, Prathibha ^a   Rondou, Pieter ^b   Socci, Nicholas D ^a   Benoit, Yves ^b   Taghon, Tom ^d   Van Vlierberghe, Pieter ^b   Leslie, Christina S ^a   Speleman, Frank ^b   Wendel, Hans Guido ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b GHENT UNIVERSITY HOSPITAL   (Belgium)

^c Weill Cornell Medical Center   (United States)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; TRANSCRIPTION FACTOR; HBP1 PROTEIN, MOUSE; HIGH MOBILITY GROUP PROTEIN; REPRESSOR PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER PATIENT; FUNCTIONAL ASSESSMENT; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; LEUKEMIA CELL; LYMPHOCYTE SUBPOPULATION; MACHINE LEARNING; MOUSE; NONHUMAN; ONCOGENE C MYC; ONCOGENE MYB; THYMOCYTE; TUMOR SUPPRESSOR GENE; ADOPTIVE TRANSFER; ANIMAL; ARTIFICIAL INTELLIGENCE; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION;

MUS;

ADOPTIVE TRANSFER; ANIMALS; ARTIFICIAL INTELLIGENCE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MYB; GENES, TUMOR SUPPRESSOR; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HIGH MOBILITY GROUP PROTEINS; HUMANS; MICE; MICRORNAS; MODELS, GENETIC; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTE SUBSETS;

EID: 84911952822     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005500     Document Type: Article

References (56)

1. A. P. Weng, A. A. Ferrando, W. Lee, J. P. t. Morris, L. B. Silverman, C. Sanchez-Irizarry, S. C. Blacklow, A. T. Look, J. C. Aster, Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306, 269-271 (2004).
2. J. Zhang, L. Ding, L. Holmfeldt, G.Wu, S. L. Heatley, D. Payne-Turner, J. Easton, X. Chen, J. Wang, M. Rusch, C. Lu, S. C. Chen, L. Wei, J. R. Collins-Underwood, J. Ma, K. G. Roberts, S. B. Pounds, A. Ulyanov, J. Becksfort, P. Gupta, R. Huether, R.W. Kriwacki, M. Parker, D. J. McGoldrick, D. Zhao, D. Alford, S. Espy, K. C. Bobba, G. Song, D. Pei, C. Cheng, S. Roberts, M. I. Barbato, D. Campana, E. Coustan-Smith, S. A. Shurtleff, S. C. Raimondi,M. Kleppe, J. Cools, K. A. Shimano, M. L. Hermiston, S. Doulatov, K. Eppert, E. Laurenti, F. Notta, J. E. Dick, G. Basso, S. P. Hunger, M. L. Loh, M. Devidas, B.Wood, S. Winter, K. P. Dunsmore, R. S. Fulton, L. L. Fulton, X. Hong, C. C. Harris, D. J. Dooling, K. Ochoa, K. J. Johnson, J. C. Obenauer,W. E. Evans, C. H. Pui, C.W. Naeve, T. J. Ley, E. R. Mardis, R. K. Wilson, J. R. Downing, C. G. Mullighan, The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163 (2012).
3. T. Palomero, M. L. Sulis, M. Cortina, P. J. Real, K. Barnes, M. Ciofani, E. Caparros, J. Buteau, K. Brown, S. L. Perkins, G. Bhagat, A. M. Agarwal, G. Basso, M. Castillo, S. Nagase, C. Cordon-Cardo, R. Parsons, J. C. Zúñiga-Pflücker, M. Dominguez, A. A. Ferrando, Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat. Med. 13, 1203-1210 (2007).
4. L. He, J. M. Thomson, M. T. Hemann, E. Hernando-Monge, D. Mu, S. Goodson, S. Powers, C. Cordon-Cardo, S. W. Lowe, G. J. Hannon, S. M. Hammond, A microRNA polycistron as a potential human oncogene. Nature 435, 828-833 (2005).
5. P. Mu, Y.C. Han, D. Betel, E. Yao, M. Squatrito, P. Ogrodowski, E. deStanchina, A. D'Andrea, C. Sander, A. Ventura, Genetic dissection of the miR-17∼92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev. 23, 2806-2811 (2009).
6. K. J. Mavrakis, A. L. Wolfe, E. Oricchio, T. Palomero, K. de Keersmaecker, K. McJunkin, J. Zuber, T. James, A. A. Khan, C. S. Leslie, J. S. Parker, P. J. Paddison, W. Tam, A. Ferrando, H. G. Wendel, Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat. Cell Biol. 12, 372-379 (2010).
7. K. J. Mavrakis, J. Van Der Meulen, A. L. Wolfe, X. Liu, E. Mets, T. Taghon, A. A. Khan, M. Setty, P. Rondou, P. Vandenberghe, E. Delabesse, Y. Benoit, N. B. Socci, C. S. Leslie, P. Van Vlierberghe, F. Speleman, H. G. Wendel, A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL). Nat. Genet. 43, 673-678 (2011).
8. P.W. Hsu, H. D. Huang, S. D. Hsu, L. Z. Lin, A. P. Tsou, C. P. Tseng, P. F. Stadler, S.Washietl, I. L. Hofacker, miRNAMap: Genomic maps of microRNA genes and their target genes in mammalian genomes. Nucleic Acids Res. 34, D135-D139 (2006).
9. K. Felekkis, K. Voskarides, H. Dweep, C. Sticht, N. Gretz, C. Deltas, Increased number of microRNA target sites in genes encoded in CNV regions. Evidence for an evolutionary genomic interaction. Mol. Biol. Evol. 28, 2421-2424 (2011).
10. E. A. Miska, E. Alvarez-Saavedra, A. L. Abbott, N. C. Lau, A. B. Hellman, S. M. McGonagle, D. P. Bartel, V. R. Ambros, H. R. Horvitz, Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLOS Genet. 3, e215 (2007).
11. C.Y.Park, L. T. Jeker, K. Carver-Moore, A. Oh, H. J. Liu, R. Cameron, H. Richards, Z. Li, D. Adler, Y. Yoshinaga, M. Martinez, M. Nefadov, A. K. Abbas, A. Weiss, L. L. Lanier, P. J. de Jong, J. A. Bluestone, D. Srivastava, M. T. McManus, A resource for the conditional ablation of microRNAs in the mouse. Cell Rep. 1, 385-391 (2012).
12. M. S. Ebert, P. A. Sharp, Roles for microRNAs in conferring robustness to biological processes. Cell 149, 515-524 (2012).
13. G. A. Calin, C. D. Dumitru, M. Shimizu, R. Bichi, S. Zupo, E. Noch, H. Aldler, S. Rattan, M. Keating, K. Rai, L. Rassenti, T. Kipps, M. Negrini, F. Bullrich, C. M. Croce, Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. U.S.A. 99, 15524-15529 (2002).
14. E. S. Raveche, E. Salerno, B. J. Scaglione, V. Manohar, F. Abbasi, Y. C. Lin, T. Fredrickson, P. Landgraf, S. Ramachandra, K. Huppi, J. R. Toro, V. E. Zenger, R. A. Metcalf, G. E. Marti, Abnormal microRNA-16 locus with synteny to human 13q14 linked to CLL in NZB mice. Blood 109, 5079-5086 (2007).
15. M. P. Boldin, K. D. Taganov, D. S. Rao, L. Yang, J. L. Zhao, M. Kalwani, Y. Garcia-Flores, M. Luong, A. Devrekanli, J. Xu, G. Sun, J. Tay, P. S. Linsley, D. Baltimore, miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J. Exp. Med. 208, 1189-1201 (2011).
16. P. Mestdagh, P. Van Vlierberghe, A. De Weer, D. Muth, F. Westermann, F. Speleman, J. Vandesompele, A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 10, R64 (2009).
17. W. S. Pear, J. C. Aster, M. L. Scott, R. P. Hasserjian, B. Soffer, J. Sklar, D. Baltimore, Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J. Exp. Med. 183, 2283-2291 (1996).
18. K. J. Mavrakis, H. G. Wendel, TargetScreen: An unbiased approach to identify functionally important microRNA targets. Cell Cycle 9, 2080-2084 (2010).
19. J. Kluiver, J. H. Gibcus, C. Hettinga, A. Adema, M. K. Richter, N. Halsema, I. Slezak-Prochazka, Y. Ding, B. J. Kroesen, A. van den Berg, Rapid generation of microRNA sponges for microRNA inhibition. PLOS One 7, e29275 (2012).
20. M. Scherr, L. Venturini, K. Battmer, M. Schaller-Schoenitz, D. Schaefer, I. Dallmann, A. Ganser, M. Eder, Lentivirus-mediated antagomir expression for specific inhibition of miRNA function. Nucleic Acids Res. 35, e149 (2007).
21. D. Betel, A. Koppal, P. Agius, C. Sander, C. Leslie, Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol. 11, R90 (2010).
22. P. Van Vlierberghe, A. Ambesi-Impiombato, A. Perez-Garcia, J. E. Haydu, I. Rigo, M. Hadler, V. Tosello, G. Della Gatta, E. Paietta, J. Racevskis, P. H. Wiernik, S. M. Luger, J. M. Rowe, M. Rue, A. A. Ferrando, ETV6 mutations in early immature human T cell leukemias. J. Exp. Med. 208, 2571-2579 (2011).
23. I. Homminga, R. Pieters, A.W. Langerak, J. J. de Rooi, A. Stubbs, M. Verstegen, M. Vuerhard, J. Buijs-Gladdines, C. Kooi, P. Klous, P. van Vlierberghe, A. A. Ferrando, J. M. Cayuela, B.Verhaaf,H.B. Beverloo, M.Horstmann, V. de Haas, A. S.Wiekmeijer,K.Pike-Overzet, F. J. Staal, W. de Laat, J. Soulier, F. Sigaux, J. P. Meijerink, Integrated transcript and genome analyses reveal NKX2-1 and MEF2C as potential oncogenes in T cell acute lymphoblastic leukemia. Cancer Cell 19, 484-497 (2011).
24. C. Xiao, D. P. Calado, G. Galler, T. H. Thai, H. C. Patterson, J. Wang, N. Rajewsky, T. P. Bender, K. Rajewsky, MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131, 146-159 (2007).
25. WAF1/CIP1 transcription by RB binding proteins. Oncogene 17, 3463-3469 (1998).
26. T. Zhuma, R. Tyrrell, B. Sekkali, G. Skavdis, A. Saveliev, M. Tolaini, K. Roderick, T. Norton, S. Smerdon, S. Sedgwick, R. Festenstein, D. Kioussis, Human HMG box transcription factor HBP1: A role in hCD2 LCR function. EMBO J. 18, 6396-6406 (1999).
27. B. Sekkali, E. Szabat, E. Ktistaki, M. Tolaini, K. Roderick, N. Harker, A. Patel, K.Williams, T. Norton, D. Kioussis, Human high mobility group box transcription factor 1 affects thymocyte development and transgene variegation. J. Immunol. 175, 5203-5212 (2005).
28. T. C. Chang, D. Yu, Y. S. Lee, E. A. Wentzel, D. E. Arking, K. M. West, C. V. Dang, A. Thomas-Tikhonenko, J. T. Mendell, Widespread microRNA repression by Myc contributes to tumorigenesis. Nat. Genet. 40, 43-50 (2008).
29. A. Klinakis, M. Szabolcs, K. Politi, H. Kiaris, S. Artavanis-Tsakonas, A. Efstratiadis, Myc is a Notch1 transcriptional target and a requisite for Notch1-induced mammary tumorigenesis in mice. Proc. Natl. Acad. Sci. U.S.A. 103, 9262-9267 (2006).
30. T. Palomero, W. K. Lim, D. T. Odom, M. L. Sulis, P. J. Real, A. Margolin, K. C. Barnes, J. O'Neil, D. Neuberg, A. P. Weng, J. C. Aster, F. Sigaux, J. Soulier, A. T. Look, R. A. Young, A. Califano, A. A. Ferrando, NOTCH1 directly regulates c-MYC and activates a feed-forwardloop transcriptional network promoting leukemic cell growth. Proc. Natl. Acad. Sci. U.S.A. 103, 18261-18266 (2006).
31. L.Soucek, J. Whitfield, C.P. Martins, A. J. Finch, D. J. Murphy, N. M.Sodir, A. N. Karnezis, L. B. Swigart, S. Nasi, G. I. Evan, Modelling Myc inhibition as a cancer therapy. Nature 455, 679-683 (2008).
32. L. Soucek, M. Helmer-Citterich, A. Sacco, R. Jucker, G. Cesareni, S. Nasi, Design and properties of a Myc derivative that efficiently homodimerizes. Oncogene 17, 2463-2472 (1998).
33. S. Costinean, N. Zanesi, Y. Pekarsky, E. Tili, S. Volinia, N. Heerema, C. M. Croce, Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in Eμ-miR155 transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 103, 7024-7029 (2006).
34. P. S. Eis, W. Tam, L. Sun, A. Chadburn, Z. Li, M. F. Gomez, E. Lund, J. E. Dahlberg, Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Natl. Acad. Sci. U.S.A. 102, 3627-3632 (2005).
35. Y. Pekarsky, U. Santanam, A. Cimmino, A. Palamarchuk, A. Efanov, V. Maximov, S. Volinia, H. Alder, C. G. Liu, L. Rassenti, G. A. Calin, J. P. Hagan, T. Kipps, C. M. Croce, Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res. 66, 11590-11593 (2006).
36. U. Santanam, N. Zanesi, A. Efanov, S. Costinean, A. Palamarchuk, J. P. Hagan, S. Volinia, H. Alder, L. Rassenti, T. Kipps, C. M. Croce, Y. Pekarsky, Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc. Natl. Acad. Sci. U.S.A. 107, 12210-12215 (2010).
37. W. Tam, J. E. Dahlberg, miR-155/BIC as an oncogenic microRNA. Genes Chromosomes Cancer 45, 211-212 (2006).
38. I. Lahortiga, K. De Keersmaecker, P. Van Vlierberghe, C. Graux, B. Cauwelier, F. Lambert, N. Mentens, H. B. Beverloo, R. Pieters, F. Speleman, M. D. Odero, M. Bauters, G. Froyen, P. Marynen, P. Vandenberghe, I. Wlodarska, J. P. Meijerink, J. Cools, Duplication of the MYB oncogene in T cell acute lymphoblastic leukemia. Nat. Genet. 39, 593-595 (2007).
39. E. Clappier,W. Cuccuini, A. Kalota, A. Crinquette, J.M. Cayuela,W. A. Dik, A.W. Langerak, B. Montpellier, B. Nadel, P. Walrafen, O. Delattre, A. Aurias, T. Leblanc, H. Dombret, A. M. Gewirtz, A. Baruchel, F. Sigaux, J. Soulier, The C-MYB locus is involved in chromosomal translocation and genomic duplications in human T-cell acute leukemia (T-ALL), the translocation defining a new T-ALL subtype in very young children. Blood 110, 1251-1261 (2007).
40. H. Biedenkapp, U. Borgmeyer, A. E. Sippel, K. H. Klempnauer, Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature 335, 835-837 (1988).
41. J. Zuber, A. R. Rappaport,W. Luo, E.Wang, C. Chen, A. V. Vaseva, J. Shi, S.Weissmueller, C. Fellmann, M. J. Taylor, M. Weissenboeck, T. G. Graeber, S. C. Kogan, C. R. Vakoc, S. W. Lowe, An integrated approach to dissecting oncogene addiction implicates a Mybcoordinated self-renewal program as essential for leukemia maintenance. Genes Dev. 25, 1628-1640 (2011).
42. FBW7 ubiquitin ligase complex as a tumor suppressor in T cell leukemia. J. Exp. Med. 204, 1825-1835 (2007).
43. J. O'Neil, J. Grim, P. Strack, S. Rao, D. Tibbitts, C. Winter, J. Hardwick, M. Welcker, J. P. Meijerink, R. Pieters, G. Draetta, R. Sears, B. E. Clurman, A. T. Look, FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to g-secretase inhibitors. J. Exp. Med. 204, 1813-1824 (2007).
44. M. R. Mansour, T. Sanda, L. N. Lawton, X. Li, T. Kreslavsky, C. D. Novina, M. Brand, A. Gutierrez, M. A. Kelliher, C. H. Jamieson, H. von Boehmer, R. A. Young, A. T. Look, The TAL1 complex targets the FBXW7 tumor suppressor by activating miR-223 in human T cell acute lymphoblastic leukemia. J. Exp. Med. 210, 1545-1557 (2013).
45. T. Sanda, L. N. Lawton, M. I. Barrasa, Z. P. Fan, H. Kohlhammer, A. Gutierrez, W. Ma, J. Tatarek, Y. Ahn, M. A. Kelliher, C. H. Jamieson, L. M. Staudt, R. A. Young, A. T. Look, Core transcriptional regulatory circuit controlled by the TAL1 complex in human T cell acute lymphoblastic leukemia. Cancer Cell 22, 209-221 (2012).
46. A. L. Wolfe, K. Singh, Y. Zhong, P. Drewe, V. K. Rajasekhar, V. R. Sanghvi, K. J. Mavrakis, M. Jiang, J. Van Der Meulen, J. H. Schatz, C. M. Rodrigo, C. Zhao, P. Rondue, E. deStanchina, J. Teruya-Feldstein, M. A. Kelliher, F. Speleman, J. A. Porco Jr., J. Pelletier, G. Rätsch, H. G. Wendel, RNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer. Nature 513, 65-70 (2014).
47. V.M. Richon, X. Zhou, J. P.Secrist, C. Cordon-Cardo,W. K.Kelly,M. Drobnjak, P. A.Marks, Histone deacetylase inhibitors: Assays to assess effectiveness in vitro and in vivo. Methods Enzymol. 376, 199-205 (2004).
48. E. Bernstein, S. Y. Kim, M. A. Carmell, E. P. Murchison, H. Alcorn, M. Z. Li, A. A. Mills, S. J. Elledge, K. V. Anderson, G. J. Hannon, Dicer is essential for mouse development. Nat. Genet. 35, 215-217 (2003).
49. M. S. Kumar, J. Lu, K. L. Mercer, T. R. Golub, T. Jacks, Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet. 39, 673-677 (2007).
50. I. Van de Walle, G. De Smet, M. De Smedt, B. Vandekerckhove, G. Leclercq, J. Plum, T. Taghon, An early decrease in Notch activation is required for human TCR-αβ lineage differentiation at the expense of TCR-γδ T cells. Blood 113, 2988-2998 (2009).
51. C. Chen, D. A. Ridzon, A. J. Broomer, Z. Zhou,D.H. Lee, J. T. Nguyen,M. Barbisin,N. L.Xu, V. R. Mahuvakar, M. R. Andersen, K. Q. Lao, K. J. Livak, K. J. Guegler, Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179 (2005).
52. P. Mestdagh, T. Feys, N. Bernard, S. Guenther, C. Chen, F. Speleman, J. Vandesompele, High-throughput stem-loop RT-qPCR miRNA expression profiling using minute amounts of input RNA. Nucleic Acids Res. 36, e143 (2008).
53. K. J. Mavrakis, H. Zhu, R. L. Silva, J. R. Mills, J. Teruya-Feldstein, S. W. Lowe, W. Tam, J. Pelletier, H. G. Wendel, Tumorigenic activity and therapeutic inhibition of Rheb GTPase. Genes Dev. 22, 2178-2188 (2008).
54. D. R. Plas, S. Talapatra, A. L. Edinger, J. C. Rathmell, C. B. Thompson, Akt and Bcl-xL promote growth factor-independent survival through distinct effects on mitochondrial physiology. J. Biol. Chem. 276, 12041-12048 (2001).
55. H. G.Wendel, E. De Stanchina, J. S. Fridman, A. Malina, S. Ray, S. Kogan, C. Cordon-Cardo, J. Pelletier, S. W. Lowe, Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428, 332-337 (2004).
56. C. Xiao, L. Srinivasan, D. P. Calado, H. C. Patterson, B. Zhang, J. Wang, J. M. Henderson, J. L. Kutok, K. Rajewsky, Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol. 9, 405-414 (2008).