A mouse model for inducible overexpression of Prdm14 results in rapid-onset and highly penetrant T-cell acute lymphoblastic leukemia (T-ALL)

DMM Disease Models and Mechanisms

Volumn 6, Issue 6, 2013, Pages 1494-1506

  Carofino, Brandi L ^a   Ayanga, Bernard ^a   Justice, Monica J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CRE RECOMBINASE; MYC PROTEIN; NOTCH1 RECEPTOR; PRDM14 PROTEIN; PROTEIN; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL INFILTRATION; CELL MATURATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE OVEREXPRESSION; HEMATOPOIETIC STEM CELL; LEUKEMIA CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; STEM CELL; T CELL ACUTE LYMPHOBLASTIC LEUKEMIA; T CELL LEUKEMIA; THYMOCYTE; WESTERN BLOTTING;

ANIMALS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; MICE; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; TRANSCRIPTION FACTORS;

EID: 84888869072     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.012575     Document Type: Article

References (64)

1. Adams, J. R., Xu, K., Liu, J. C., Agamez, N. M. R., Loch, A. J., Wong, R. G., Wang, W., Wright, K. L., Lane, T. F., Zacksenhaus, E. et al. (2011). Cooperation between Pik3ca and p53 mutations in mouse mammary tumor formation. Cancer Res. 71, 2706-2717.
2. Aifantis, I., Raetz, E. and Buonamici, S. (2008). Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat. Rev. Immunol. 8, 380-390.
3. Allman, D., Karnell, F. G., Punt, J. A., Bakkour, S., Xu, L., Myung, P., Koretzky, G. A., Pui, J. C., Aster, J. C. and Pear, W. S. (2001). Separation of Notch1 promoted lineage commitment and expansion/transformation in developing T cells. J. Exp. Med. 194, 99-106.
4. Becher, O. J. and Holland, E. C. (2006). Genetically engineered models have advantages over xenografts for preclinical studies. Cancer Res. 66, 3355-3358, discussion 3358-3359.
5. Berquam-Vrieze, K. E., Nannapaneni, K., Brett, B. T., Holmfeldt, L., Ma, J., Zagorodna, O., Jenkins, N. A., Copeland, N. G., Meyerholz, D. K., Knudson, C. M. et al. (2011). Cell of origin strongly influences genetic selection in a mouse model of T-ALL. Blood 118, 4646-4656.
6. Chan, Y.-S., Göke, J., Lu, X., Venkatesan, N., Feng, B., Su, I.-H. and Ng, H.-H. (2013). A PRC2-dependent repressive role of PRDM14 in human embryonic stem cells and induced pluripotent stem cell reprogramming. Stem Cells 31, 682-692.
7. Chervinsky, D. S., Zhao, X.-F., Lam, D. H., Ellsworth, M., Gross, K. W. and Aplan, P. D. (1999). Disordered T-cell development and T-cell malignancies in SCL LMO1 doubletransgenic mice: parallels with E2A-deficient mice. Mol. Cell. Biol. 19, 5025-5035.
8. Chew, V., Toh, H. C. and Abastado, J.-P. (2012). Immune microenvironment in tumor progression: characteristics and challenges for therapy. J. Oncol. 2012, 608406.
9. Chia, N.-Y., Chan, Y.-S., Feng, B., Lu, X., Orlov, Y. L., Moreau, D., Kumar, P., Yang, L., Jiang, J., Lau, M.-S. et al. (2010). A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature 468, 316-320.
10. Dail, M., Li, Q., McDaniel, A., Wong, J., Akagi, K., Huang, B., Kang, H. C., Kogan, S. C., Shokat, K., Wolff, L. et al. (2010). Mutant Ikzf1, KrasG12D, and Notch1 cooperate in T lineage leukemogenesis and modulate responses to targeted agents. Proc. Natl. Acad. Sci. USA 107, 5106-5111.
11. Dalerba, P., Cho, R. W. and Clarke, M. F. (2007). Cancer stem cells: models and concepts. Annu. Rev. Med. 58, 267-284.
12. Dettman, E. J., Simko, S. J., Ayanga, B., Carofino, B. L., Margolin, J. F., Morse, H. C., 3rd and Justice, M. J. (2011). Prdm14 initiates lymphoblastic leukemia after expanding a population of cells resembling common lymphoid progenitors. Oncogene 30, 2859-2873.
13. Forozan, F., Mahlamäki, E. H., Monni, O., Chen, Y., Veldman, R., Jiang, Y., Gooden, G. C., Ethier, S. P., Kallioniemi, A. and Kallioniemi, O.-P. (2000). Comparative genomic hybridization analysis of 38 breast cancer cell lines: a basis for interpreting complementary DNA microarray data. Cancer Res. 60, 4519-4525.
14. Fowlkes, B. J. and Robey, E. A. (2002). A reassessment of the effect of activated Notch1 on CD4 and CD8 T cell development. J. Immunol. 169, 1817-1821.
15. Frese, K. K. and Tuveson, D. A. (2007). Maximizing mouse cancer models. Nat. Rev. Cancer 7, 654-658.
16. George, A., Morse, H. C., 3rd and Justice, M. J. (2003). The homeobox gene Hex induces T-cell-derived lymphomas when overexpressed in hematopoietic precursor cells. Oncogene 22, 6764-6773.
17. Gillich, A., Bao, S., Grabole, N., Hayashi, K., Trotter, M. W. B., Pasque, V., Magnúsdóttir, E. and Surani, M. A. (2012). Epiblast stem cell-based system reveals reprogramming synergy of germline factors. Cell Stem Cell 10, 425-439.
18. Grabher, C., von Boehmer, H. and Look, A. T. (2006). Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat. Rev. Cancer 6, 347-359.
19. Grabole, N., Tischler, J., Hackett, J. A., Kim, S., Tang, F., Leitch, H. G., Magnúsdóttir, E. and Surani, M. A. (2013). Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep. 14, 629-637.
20. Hanahan, D. and Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
21. Hohenauer, T. and Moore, A. W. (2012). The Prdm family: expanding roles in stem cells and development. Development 139, 2267-2282.
22. Hohenstein, P., Slight, J., Ozdemir, D. D., Burn, S. F., Berry, R. and Hastie, N. D. (2008). High-efficiency Rosa26 knock-in vector construction for Cre-regulated overexpression and RNAi. PathoGenetics 1, 3.
23. Hu, M., Yao, J., Cai, L., Bachman, K. E., van den BrÛle, F., Velculescu, V. and Polyak, K. (2005). Distinct epigenetic changes in the stromal cells of breast cancers. Nat. Genet. 37, 899-905.
24. International Agency for Research on Cancer and World Health Organization (2008). World Cancer Report 2008. Lyon: International Agency for Research on Cancer.
25. Justice, M. J., Morse, H. C., 3rd, Jenkins, N. A. and Copeland, N. G. (1994). Identification of Evi-3, a novel common site of retroviral integration in mouse AKXD B-cell lymphomas. J. Virol. 68, 1293-1300.
26. Keating, A. K., Salzberg, D. B., Sather, S., Liang, X., Nickoloff, S., Anwar, A., Deryckere, D., Hill, K., Joung, D., Sawczyn, K. K. et al. (2006). Lymphoblastic leukemia/lymphoma in mice overexpressing the Mer (MerTK) receptor tyrosine kinase. Oncogene 25, 6092-6100.
27. King, A. G., Kondo, M., Scherer, D. C. and Weissman, I. L. (2002). Lineage infidelity in myeloid cells with TCR gene rearrangement: a latent developmental potential of proT cells revealed by ectopic cytokine receptor signaling. Proc. Natl. Acad. Sci. USA 99, 4508-4513.
28. Kühn, R. and Torres, R. M. (2002). Cre/loxP recombination system and gene targeting. Methods Mol. Biol. 180, 175-204.
29. Kühn, R., Schwenk, F., Aguet, M. and Rajewsky, K. (1995). Inducible gene targeting in mice. Science 269, 1427-1429.
30. Leitch, H. G., McEwen, K. R., Turp, A., Encheva, V., Carroll, T., Grabole, N., Mansfield, W., Nashun, B., Knezovich, J. G., Smith, A. et al. (2013). Naive pluripotency is associated with global DNA hypomethylation. Nat. Struct. Mol. Biol. 20, 311-316.
31. Liu, B., Zhang, S., Hui, L., Qiu, X. and Cui, Z. (2010). [Relationship between the expression of PRDM14 in non-small cell lung cancer and the clinicopathologic characteristics]. Chinese Journal of Lung Cancer 13, 867-872.
32. Loh, M. L. and Mullighan, C. G. (2012). Advances in the genetics of high-risk childhood B-progenitor acute lymphoblastic leukemia and juvenile myelomonocytic leukemia: implications for therapy. Clin. Cancer Res. 18, 2754-2767.
33. Ma, Z., Swigut, T., Valouev, A., Rada-Iglesias, A. and Wysocka, J. (2011). Sequencespecific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 18, 120-127.
34. Mack, D. L., Leibowitz, D. S., Cooper, S., Ramsey, H., Broxmeyer, H. E. and Hromas, R. (2002). Down-regulation of the myeloid homeobox protein Hex is essential for normal T-cell development. Immunology 107, 444-451.
35. McCormack, M. P., Young, L. F., Vasudevan, S., de Graaf, C. A., Codrington, R., Rabbitts, T. H., Jane, S. M. and Curtis, D. J. (2010). The Lmo2 oncogene initiates leukemia in mice by inducing thymocyte self-renewal. Science 327, 879-883.
36. Moelans, C. B., de Weger, R. A., Monsuur, H. N., Vijzelaar, R. and van Diest, P. J. (2010). Molecular profiling of invasive breast cancer by multiplex ligation-dependent probe amplification-based copy number analysis of tumor suppressor and oncogenes. Mod. Pathol. 23, 1029-1039.
37. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. and Melton, D. A. (2003). Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. USA 100, 14920-14925.
38. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global doublefluorescent Cre reporter mouse. Genesis 45, 593-605.
39. Nagy, A., Mar, L. and Watts, G. (2009). Creation and use of a cre recombinase transgenic database. Methods Mol. Biol. 530, 365-378.
40. Nishikawa, N., Toyota, M., Suzuki, H., Honma, T., Fujikane, T., Ohmura, T., Nishidate, T., Ohe-Toyota, M., Maruyama, R., Sonoda, T. et al. (2007). Gene amplification and overexpression of PRDM14 in breast cancers. Cancer Res. 67, 9649-9657.
41. Palomero, T. and Ferrando, A. (2008). Oncogenic NOTCH1 control of MYC and PI3K: challenges and opportunities for anti-NOTCH1 therapy in T-cell acute lymphoblastic leukemias and lymphomas. Clin. Cancer Res. 14, 5314-5317.
42. Pear, W. S., Aster, J. C., Scott, M. L., Hasserjian, R. P., Soffer, B., Sklar, J. and Baltimore, D. (1996). Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J. Exp. Med. 183, 2283-2291.
43. Pettitt, S. J., Liang, Q., Rairdan, X. Y., Moran, J. L., Prosser, H. M., Beier, D. R., Lloyd, K. C., Bradley, A. and Skarnes, W. C. (2009). Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat. Methods 6, 493-495.
44. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
45. Plaut, M. (1987). Lymphocyte hormone receptors. Annu. Rev. Immunol. 5, 621-669.
46. Pui, J. C., Allman, D., Xu, L., DeRocco, S., Karnell, F. G., Bakkour, S., Lee, J. Y., Kadesch, T., Hardy, R. R., Aster, J. C. et al. (1999). Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 11, 299-308.
47. Rakowski, L. A., Garagiola, D. D., Li, C. M., Decker, M., Caruso, S., Jones, M., Kuick, R., Cierpicki, T., Maillard, I. and Chiang, M. Y. (2013). Convergence of the ZMIZ1 and NOTCH1 pathways at C-MYC in acute T lymphoblastic leukemias. Cancer Res. 73, 930-941.
48. Robey, E., Chang, D., Itano, A., Cado, D., Alexander, H., Lans, D., Weinmaster, G. and Salmon, P. (1996). An activated form of Notch influences the choice between CD4 and CD8 T cell lineages. Cell 87, 483-492.
49. Robinson, G. W. and Hennighausen, L. (2011). MMTV-Cre transgenes can adversely affect lactation: considerations for conditional gene deletion in mammary tissue. Anal. Biochem. 412, 92-95.
50. Rosenbloom, K. R., Sloan, C. A., Malladi, V. S., Dreszer, T. R., Learned, K., Kirkup, V. M., Wong, M. C., Maddren, M., Fang, R., Heitner, S. G. et al. (2013). ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res. 41, D56-D63.
51. Ross, S. R. and Solter, D. (1985). Glucocorticoid regulation of mouse mammary tumor virus sequences in transgenic mice. Proc. Natl. Acad. Sci. USA 82, 5880-5884.
52. Simko, S. J., Voicu, H., Carofino, B. L. and Justice, M. J. (2012). Mouse Lymphoblastic Leukemias Induced by Aberrant Prdm14 Expression Demonstrate Widespread Copy Number Alterations Also Found in Human ALL. Cancers 4, 1050-1066.
53. Smith, D. P., Bath, M. L., Metcalf, D., Harris, A. W. and Cory, S. (2006). MYC levels govern hematopoietic tumor type and latency in transgenic mice. Blood 108, 653-661.
54. Stier, S., Cheng, T., Dombkowski, D., Carlesso, N. and Scadden, D. T. (2002). Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood 99, 2369-2378.
55. Tandon, P., Gallo, C. A., Khatri, S., Barger, J. F., Yepiskoposyan, H. and Plas, D. R. (2011). Requirement for ribosomal protein S6 kinase 1 to mediate glycolysis and apoptosis resistance induced by Pten deficiency. Proc. Natl. Acad. Sci. USA 108, 2361-2365.
56. Thoms, J. A. I., Birger, Y., Foster, S., Knezevic, K., Kirschenbaum, Y., Chandrakanthan, V., Jonquieres, G., Spensberger, D., Wong, J. W., Oram, S. H. et al. (2011). ERG promotes T-acute lymphoblastic leukemia and is transcriptionally regulated in leukemic cells by a stem cell enhancer. Blood 117, 7079-7089.
57. Tsuneyoshi, N., Sumi, T., Onda, H., Nojima, H., Nakatsuji, N. and Suemori, H. (2008). PRDM14 suppresses expression of differentiation marker genes in human embryonic stem cells. Biochem. Biophys. Res. Commun. 367, 899-905.
58. Wagner, K. U., Claudio, E., Rucker, E. B., 3rd, Riedlinger, G., Broussard, C., Schwartzberg, P. L., Siebenlist, U. and Hennighausen, L. (2000). Conditional deletion of the Bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development 127, 4949-4958.
59. Wagner, K. U., McAllister, K., Ward, T., Davis, B., Wiseman, R. and Hennighausen, L. (2001). Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res. 10, 545-553.
60. Wittschieben, J. P., Patil, V., Glushets, V., Robinson, L. J., Kusewitt, D. F. and Wood, R. D. (2010). Loss of DNA polymerase ζ enhances spontaneous tumorigenesis. Cancer Res. 70, 2770-2778.
61. Xiong, J., Armato, M. A. and Yankee, T. M. (2011). Immature single-positive CD8+ thymocytes represent the transition from Notch-dependent to Notch-independent T-cell development. Int. Immunol. 23, 55-64.
62. Yamaji, M., Seki, Y., Kurimoto, K., Yabuta, Y., Yuasa, M., Shigeta, M., Yamanaka, K., Ohinata, Y. and Saitou, M. (2008). Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40, 1016-1022.
63. Zambrowicz, B. P., Imamoto, A., Fiering, S., Herzenberg, L. A., Kerr, W. G. and Soriano, P. (1997). Disruption of overlapping transcripts in the ROSA β geo 26 gene trap strain leads to widespread expression of β-galactosidase in mouse embryos and hematopoietic cells. Proc. Natl. Acad. Sci. USA 94, 3789-3794.
64. Zhang, D. J., Wang, Q., Wei, J., Baimukanova, G., Buchholz, F., Stewart, A. F., Mao, X. and Killeen, N. (2005). Selective expression of the Cre recombinase in late-stage thymocytes using the distal promoter of the Lck gene. J. Immunol. 174, 6725-6731.