Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015 (2015), Article ID 165238, 9 pages
http://dx.doi.org/10.1155/2015/165238
Review Article

ZNF423 and ZNF521: EBF1 Antagonists of Potential Relevance in B-Lymphoid Malignancies

1Laboratory of Molecular Haematopoiesis and Stem Cell Biology, Department of Experimental and Clinical Medicine, Magna Græcia University, 88100 Catanzaro, Italy
2YCR Cancer Research Unit, Department of Biology, University of York, Heslington, York YO10 5DD, UK

Received 19 October 2015; Accepted 25 November 2015

Academic Editor: Mariateresa Fulciniti

Copyright © 2015 Maria Mesuraca et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. R. Hardy and K. Hayakawa, “B cell development pathways,” Annual Review of Immunology, vol. 19, pp. 595–621, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. R. R. Hardy, P. W. Kincade, and K. Dorshkind, “The protean nature of cells in the B lymphocyte lineage,” Immunity, vol. 26, no. 6, pp. 703–714, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. R. S. Welner, R. Pelayo, and P. W. Kincade, “Evolving views on the genealogy of B cells,” Nature Reviews Immunology, vol. 8, no. 2, pp. 95–106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. E. V. Rothenberg, “Stepwise specification of lymphocyte developmental lineages,” Current Opinion in Genetics and Development, vol. 10, no. 4, pp. 370–379, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Hagman and K. Lukin, “Transcription factors drive B cell development,” Current Opinion in Immunology, vol. 18, no. 2, pp. 127–134, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. C. V. Laiosa, M. Stadtfeld, and T. Graf, “Determinants of lymphoid-myeloid lineage diversification,” Annual Review of Immunology, vol. 24, pp. 705–738, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Schebesta, S. McManus, G. Salvagiotto, A. Delogu, G. A. Busslinger, and M. Busslinger, “Transcription factor Pax5 activates the chromatin of key genes involved in B cell signaling, adhesion, migration, and immune function,” Immunity, vol. 27, no. 1, pp. 49–63, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. S. L. Nutt and B. L. Kee, “The transcriptional regulation of B cell lineage commitment,” Immunity, vol. 26, no. 6, pp. 715–725, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Lin and R. Grosschedl, “Failure of B-cell differentiation in mice lacking the transcription factor EBF,” Nature, vol. 376, no. 6537, pp. 263–267, 1995. View at Publisher · View at Google Scholar · View at Scopus
  10. E. M. Mandel and R. Grosschedl, “Transcription control of early B cell differentiation,” Current Opinion in Immunology, vol. 22, no. 2, pp. 161–167, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Treiber, E. M. Mandel, S. Pott et al., “Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription- independent poising of chromatin,” Immunity, vol. 32, no. 5, pp. 714–725, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Yoshida, S. Y.-M. Ng, and K. Georgopoulos, “Awakening lineage potential by Ikaros-mediated transcriptional priming,” Current Opinion in Immunology, vol. 22, no. 2, pp. 154–160, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Yokota, T. Sudo, T. Ishibashi et al., “Complementary regulation of early B-lymphoid differentiation by genetic and epigenetic mechanisms,” International Journal of Hematology, vol. 98, no. 4, pp. 382–389, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Choukrallah and P. Matthias, “The interplay between chromatin and transcription factor networks during B cell development: who pulls the trigger first?” Frontiers in Immunology, vol. 5, article 156, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Dege and J. Hagman, “Mi-2/NuRD chromatin remodeling complexes regulate B and T-lymphocyte development and function,” Immunological Reviews, vol. 261, no. 1, pp. 126–140, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Grosschedl, “Establishment and maintenance of B cell identity,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 78, no. 1, pp. 23–30, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. E. V. Rothenberg, “Transcriptional control of early T and B cell developmental choices,” Annual Review of Immunology, vol. 32, pp. 283–321, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Boller and R. Grosschedl, “The regulatory network of B-cell differentiation: a focused view of early B-cell factor 1 function,” Immunological Reviews, vol. 261, no. 1, pp. 102–115, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Garel, F. Marín, R. Grosschedl, and P. Charnay, “Ebf1 controls early cell differentiation in the embryonic striatum,” Development, vol. 126, no. 23, pp. 5285–5294, 1999. View at Google Scholar · View at Scopus
  20. L. Dubois and A. Vincent, “The COE—Collier/Olf1/EBF—transcription factors: structural conservation and diversity of developmental functions,” Mechanisms of Development, vol. 108, no. 1-2, pp. 3–12, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Åkerblad, U. Lind, D. Liberg, K. Bamberg, and M. Sigvardsson, “Early B-cell factor (O/E-1) is a promoter of adipogenesis and involved in control of genes important for terminal adipocyte differentiation,” Molecular and Cellular Biology, vol. 22, no. 22, pp. 8015–8025, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Liberg, M. Sigvardsson, and P. Åkerblad, “The EBF/Olf/Collier family of transcription factors: regulators of differentiation in cells originating from all three embryonal germ layers,” Molecular and Cellular Biology, vol. 22, no. 24, pp. 8389–8397, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Garcia-Dominguez, C. Poquet, S. Garel, and P. Charnay, “Ebf gene function is required for coupling neuronal differentiation and cell cycle exit,” Development, vol. 130, no. 24, pp. 6013–6025, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. D. G. T. Hesslein, J. A. Fretz, Y. Xi et al., “Ebf1-dependent control of the osteoblast and adipocyte lineages,” Bone, vol. 44, no. 4, pp. 537–546, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Hagman, M. J. Gutch, H. Lin, and R. Grosschedl, “EBF contains a novel zinc coordination motif and multiple dimerization and transcriptional activation domains,” The EMBO Journal, vol. 14, no. 12, pp. 2907–2916, 1995. View at Google Scholar · View at Scopus
  26. A. Travis, J. Hagman, L. Hwang, and R. Grosschedl, “Purification of early-B-cell factor and characterization of its DNA-binding specificity,” Molecular and Cellular Biology, vol. 13, no. 6, pp. 3392–3400, 1993. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Fields, K. Ternyak, H. Gao, R. Ostraat, J. Akerlund, and J. Hagman, “The ‘zinc knuckle’ motif of early B cell factor is required for transcriptional activation of B cell-specific genes,” Molecular Immunology, vol. 45, no. 14, pp. 3786–3796, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. E. M. K. Smith, R. Gisler, and M. Sigvardsson, “Cloning and characterization of a promoter flanking the early B cell factor (EBF) gene indicates roles for E-proteins and autoregulation in the control of EBF expression,” Journal of Immunology, vol. 169, no. 1, pp. 261–270, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Roessler, I. Györy, S. Imhof et al., “Distinct promoters mediate the regulation of Ebf1 gene expression by interleukin-7 and Pax5,” Molecular and Cellular Biology, vol. 27, no. 2, pp. 579–594, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Fuxa, J. Skok, A. Souabni, G. Salvagiotto, E. Roldan, and M. Busslinger, “Pax5 induces V-to-DJ rearrangements and locus contraction of the immunoglobulin heavy-chain gene,” Genes and Development, vol. 18, no. 4, pp. 411–422, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Zandi, R. Mansson, P. Tsapogas, J. Zetterblad, D. Bryder, and M. Sigvardsson, “EBF1 is essential for B-lineage priming and establishment of a transcription factor network in common lymphoid progenitors,” Journal of Immunology, vol. 181, no. 5, pp. 3364–3372, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Vilagos, M. Hoffmann, A. Souabni et al., “Essential role of EBF1 in the generation and function of distinct mature B cell types,” Journal of Experimental Medicine, vol. 209, no. 4, pp. 775–792, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Nechanitzky, D. Akbas, S. Scherer et al., “Transcription factor EBF1 is essential for the maintenance of B cell identity and prevention of alternative fates in committed cells,” Nature Immunology, vol. 14, no. 8, pp. 867–875, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. Z. Zhang, C. V. Cotta, R. P. Stephan, C. G. de Guzman, and C. A. Klug, “Enforced expression of EBF in hematopoietic stem cells restricts lymphopoiesis to the B cell lineage,” The EMBO Journal, vol. 22, no. 18, pp. 4759–4769, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. J. M. R. Pongubala, D. L. Northrup, D. W. Lancki et al., “Transcription factor EBF restricts alternative lineage options and promotes B cell fate commitment independently of Pax5,” Nature Immunology, vol. 9, no. 2, pp. 203–215, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Lukin, S. Fields, L. Guerrettaz et al., “A dose-dependent role for EBF1 in repressing non-B-cell-specific genes,” European Journal of Immunology, vol. 41, no. 6, pp. 1787–1793, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Ungerback, J. Ahsberg, T. Strid, R. Somasundaram, and M. Sigvardsson, “Combined heterozygous loss of Ebf1 and Pax5 allows for T-lineage conversion of B cell progenitors,” Journal of Experimental Medicine, vol. 212, no. 7, pp. 1109–1123, 2015. View at Publisher · View at Google Scholar
  38. H. Kikuchi, M. Nakayama, Y. Takami, F. Kuribayashi, and T. Nakayama, “EBF1 acts as a powerful repressor of Blimp-1 gene expression in immature B cells,” Biochemical and Biophysical Research Communications, vol. 422, no. 4, pp. 780–785, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Maier, R. Ostraat, H. Gao et al., “Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription,” Nature Immunology, vol. 5, no. 10, pp. 1069–1077, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Hagman and K. Lukin, “Early B-cell factor ‘pioneers’ the way for B-cell development,” Trends in Immunology, vol. 26, no. 9, pp. 455–461, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Gao, K. Lukin, J. Ramírez, S. Fields, D. Lopez, and J. Hagman, “Opposing effects of SWI/SNF and Mi-2/NuRD chromatin remodeling complexes on epigenetic reprogramming by EBF and Pax5,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 27, pp. 11258–11263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Hagman, J. Ramírez, and K. Lukin, “B lymphocyte lineage specification, commitment and epigenetic control of transcription by early B cell factor 1,” Current Topics in Microbiology and Immunology, vol. 356, pp. 17–38, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Campos-Sanchez, A. Toboso-Navasa, I. Romero-Camarero, M. Barajas-Diego, I. Sanchez-Garcia, and C. Cobaleda, “Acute lymphoblastic leukemia and developmental biology: a crucial interrelationship,” Cell Cycle, vol. 10, no. 20, pp. 3473–3486, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. S. H. M. Pang, S. Carotta, and S. L. Nutt, “Transcriptional control of pre-B cell development and leukemia prevention,” Current Topics in Microbiology and Immunology, vol. 381, pp. 189–213, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Pérez-Vera, A. Reyes-León, and E. M. Fuentes-Pananá, “Signaling proteins and transcription factors in normal and malignant early B cell development,” Bone Marrow Research, vol. 2011, Article ID 502751, 10 pages, 2011. View at Publisher · View at Google Scholar
  46. R. Somasundaram, M. A. Prasad, J. Ungerback, and M. Sigvardsson, “Transcription factor networks in B-cell differentiation link development to acute lymphoid leukemia,” Blood, vol. 126, no. 2, pp. 144–152, 2015. View at Publisher · View at Google Scholar
  47. L. M. Heltemes-Harris, M. J. L. Willette, L. B. Ramsey et al., “Ebf1 or Pax5 haploinsufficiency synergizes with STAT5 activation to initiate acute lymphoblastic leukemia,” Journal of Experimental Medicine, vol. 208, no. 6, pp. 1135–1149, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. D. Heckl, A. Schwarzer, R. Haemmerle et al., “Lentiviral vector induced insertional haploinsufficiency of EBF1 causes murine leukemia,” Molecular Therapy, vol. 20, no. 6, pp. 1187–1195, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. M. A. Prasad, J. Ungerback, J. Ahsberg et al., “Ebf1 heterozygosity results in increased DNA damage in pro-B cells and their synergistic transformation by Pax5 haploinsufficiency,” Blood, vol. 125, no. 26, pp. 4052–4059, 2015. View at Publisher · View at Google Scholar
  50. R. P. Kuiper, E. F. P. M. Schoenmakers, S. V. van Reijmersdal et al., “High-resolution genomic profiling of childhood ALL reveals novel recurrent genetic lesions affecting pathways involved in lymphocyte differentiation and cell cycle progression,” Leukemia, vol. 21, no. 6, pp. 1258–1266, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. C. G. Mullighan, S. Goorha, I. Radtke et al., “Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia,” Nature, vol. 446, no. 7137, pp. 758–764, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. C. G. Mullighan, C. B. Miller, I. Radtke et al., “BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros,” Nature, vol. 453, no. 7191, pp. 110–114, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Shah, K. A. Schrader, E. Waanders et al., “A recurrent germline PAX5 mutation confers susceptibility to pre-B cell acute lymphoblastic leukemia,” Nature Genetics, vol. 45, no. 10, pp. 1226–1231, 2013. View at Google Scholar
  54. D. S. Mangum, J. Downie, C. C. Mason et al., “VPREB1 deletions occur independent of lambda light chain rearrangement in childhood acute lymphoblastic leukemia,” Leukemia, vol. 28, no. 1, pp. 216–220, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. A. K. Andersson, J. Ma, J. Wang et al., “The landscape of somatic mutations in infant MLL-rearranged acute lymphoblastic leukemias,” Nature Genetics, vol. 47, no. 4, pp. 330–337, 2015. View at Publisher · View at Google Scholar
  56. R. C. Harvey, C. G. Mullighan, X. Wang et al., “Identification of novel cluster groups in pediatric high-risk B-precursor acute lymphoblastic leukemia with gene expression profiling: correlation with genome-wide DNA copy number alterations, clinical characteristics, and outcome,” Blood, vol. 116, no. 23, pp. 4874–4884, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. J. J. Yang, D. Bhojwani, W. Yang et al., “Genome-wide copy number profiling reveals molecular evolution from diagnosis to relapse in childhood acute lymphoblastic leukemia,” Blood, vol. 112, no. 10, pp. 4178–4183, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Y. L. Tsai and R. R. Reed, “Cloning and functional characterization of Roaz, a zinc finger protein that interacts with O/E-1 to regulate gene expression: implications for olfactory neuronal development,” The Journal of Neuroscience, vol. 17, no. 11, pp. 4159–4169, 1997. View at Google Scholar · View at Scopus
  59. L. E. Cheng, J. Zhang, and R. R. Reed, “The transcription factor Zfp423/OAZ is required for cerebellar development and CNS midline patterning,” Developmental Biology, vol. 307, no. 1, pp. 43–52, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Y. L. Tsai and R. R. Reed, “Identification of DNA recognition sequences and protein interaction domains of the multiple-Zn-finger protein Roaz,” Molecular and Cellular Biology, vol. 18, no. 11, pp. 6447–6456, 1998. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Hata, J. Seoane, G. Lagna, E. Montalvo, A. Hemmati-Brivanlou, and J. Massagué, “OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways,” Cell, vol. 100, no. 2, pp. 229–240, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. M.-C. Ku, S. Stewart, and A. Hata, “Poly(ADP-ribose) polymerase 1 interacts with OAZ and regulates BMP-target genes,” Biochemical and Biophysical Research Communications, vol. 311, no. 3, pp. 702–707, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. G. Masserdotti, A. Badaloni, Y. S. Green et al., “ZFP423 coordinates Notch and bone morphogenetic protein signaling, selectively up-regulating Hes5 gene expression,” The Journal of Biological Chemistry, vol. 285, no. 40, pp. 30814–30824, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Huang, J. Laoukili, M. T. Epping et al., “ZNF423 is critically required for retinoic acid-induced differentiation and is a marker of neuroblastoma outcome,” Cancer Cell, vol. 15, no. 4, pp. 328–340, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. Y.-W. Cho, C.-J. Hong, A. Hou et al., “Zfp423 binds autoregulatory sites in p19 cell culture model,” PLoS ONE, vol. 8, no. 6, Article ID e66514, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. R. K. Gupta, Z. Arany, P. Seale et al., “Transcriptional control of preadipocyte determination by Zfp423,” Nature, vol. 464, no. 7288, pp. 619–623, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. R. K. Gupta, R. J. Mepani, S. Kleiner et al., “Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells,” Cell Metabolism, vol. 15, no. 2, pp. 230–239, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. U. J. Yun, N. Song, D. K. Yang et al., “miR-195a inhibits adipocyte differentiation by targeting the preadipogenic determinator Zfp423,” Journal of Cellular Biochemistry, vol. 116, no. 11, pp. 2589–2597, 2015. View at Publisher · View at Google Scholar
  69. A. Hammarstedt, S. Hedjazifar, L. Jenndahl et al., “WISP2 regulates preadipocyte commitment and PPARgamma activation by BMP4,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 7, pp. 2563–2568, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Kang, P. Akerblad, R. Kiviranta et al., “Regulation of early adipose commitment by Zfp521,” PLoS Biology, vol. 10, no. 11, Article ID e1001433, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Warming, P. Liu, T. Suzuki et al., “Evi3, a common retroviral integration site in murine B-cell lymphoma, encodes an EBFAZ-related Krüppel-like zinc finger protein,” Blood, vol. 101, no. 5, pp. 1934–1940, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. W. A. Alcaraz, D. A. Gold, E. Raponi, P. M. Gent, D. Concepcion, and B. A. Hamilton, “Zfp423 controls proliferation and differentiation of neural precursors in cerebellar vermis formation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 51, pp. 19424–19429, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Chaki, R. Airik, A. K. Ghosh et al., “Exome capture reveals ZNF423 and CEP164 mutations, linking renal ciliopathies to DNA damage response signaling,” Cell, vol. 150, no. 3, pp. 533–548, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. J. N. Ingle, M. Liu, D. L. Wickerham et al., “Selective estrogen receptor modulators and pharmacogenomic variation in ZNF423 regulation of BRCA1 expression: individualized breast cancer prevention,” Cancer Discovery, vol. 3, no. 7, pp. 812–825, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. H. M. Bond, M. Mesuraca, E. Carbone et al., “Early hematopoietic zinc finger protein (EHZF), the human homolog to mouse Evi3, is highly expressed in primitive human hematopoietic cells,” Blood, vol. 103, no. 6, pp. 2062–2070, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. H. M. Bond, M. Mesuraca, N. Amodio et al., “Early hematopoietic zinc finger protein-zinc finger protein 521: a candidate regulator of diverse immature cells,” International Journal of Biochemistry and Cell Biology, vol. 40, no. 5, pp. 848–854, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. F. Bernaudo, F. Monteleone, M. Mesuraca et al., “Validation of a novel shotgun proteomic workflow for the discovery of protein-protein interactions: focus on ZNF521,” Journal of Proteome Research, vol. 14, no. 4, pp. 1888–1899, 2015. View at Publisher · View at Google Scholar
  78. L. Harder, G. Eschenburg, A. Zech et al., “Aberrant ZNF423 impedes B cell differentiation and is linked to adverse outcome of ETV6-RUNX1 negative B precursor acute lymphoblastic leukemia,” Journal of Experimental Medicine, vol. 210, no. 11, pp. 2289–2304, 2013. View at Publisher · View at Google Scholar · View at Scopus
  79. S. M. Chambers, N. C. Boles, K.-Y. K. Lin et al., “Hematopoietic fingerprints: an expression database of stem cells and their progeny,” Cell Stem Cell, vol. 1, no. 5, pp. 578–591, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. R. Gazit, B. S. Garrison, T. N. Rao et al., “Transcriptome analysis identifies regulators of hematopoietic stem and progenitor cells,” Stem Cell Reports, vol. 1, no. 3, pp. 266–280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Riddell, R. Gazit, B. S. Garrison et al., “Reprogramming committed murine blood cells to induced hematopoietic stem cells with defined factors,” Cell, vol. 157, no. 3, pp. 549–564, 2014. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Mega, M. Lupia, N. Amodio et al., “Zinc finger protein 521 antagonizes early B-cell factor 1 and modulates the B-lymphoid differentiation of primary hematopoietic progenitors,” Cell Cycle, vol. 10, no. 13, pp. 2129–2139, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. E. Matsubara, I. Sakai, J. Yamanouchi et al., “The role of zinc finger protein 521/early hematopoietic zinc finger protein in erythroid cell differentiation,” The Journal of Biological Chemistry, vol. 284, no. 6, pp. 3480–3487, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. L. Salerno, C. Cosentino, G. Morrone, F. Amato, and B. D. MacArthur, “Computational modeling of a transcriptional switch underlying B-lymphocyte lineage commitment of hematopoietic multipotent cells,” PLoS ONE, vol. 10, no. 7, Article ID e0132208, 2015. View at Publisher · View at Google Scholar
  85. M. K. Lobo, C. Yeh, and X. W. Yang, “Pivotal role of early B-cell factor 1 in development of striatonigral medium spiny neurons in the matrix compartment,” Journal of Neuroscience Research, vol. 86, no. 10, pp. 2134–2146, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. W. N. Addison, M. M. Fu, H. X. Yang et al., “Direct transcriptional repression of Zfp423 by Zfp521 mediates a bone morphogenic protein-dependent osteoblast versus adipocyte lineage commitment switch,” Molecular and Cellular Biology, vol. 34, no. 16, pp. 3076–3085, 2014. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Wu, E. Hesse, F. Morvan et al., “Zfp521 antagonizes Runx2, delays osteoblast differentiation in vitro, and promotes bone formation in vivo,” Bone, vol. 44, no. 4, pp. 528–536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Hesse, H. Saito, R. Kiviranta et al., “Zfp521 controls bone mass by HDAC3-dependent attenuation of Runx2 activity,” The Journal of Cell Biology, vol. 191, no. 7, pp. 1271–1283, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. R. Kiviranta, K. Yamana, H. Saito et al., “Coordinated transcriptional regulation of bone homeostasis by Ebf1 and Zfp521 in both mesenchymal and hematopoietic lineages,” Journal of Experimental Medicine, vol. 210, no. 5, pp. 969–985, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Mesuraca, O. Galasso, L. Guido et al., “Expression profiling and functional implications of a set of zinc finger proteins, ZNF423, ZNF470, ZNF521, and ZNF780B, in primary osteoarthritic articular chondrocytes,” Mediators of Inflammation, vol. 2014, Article ID 318793, 11 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  91. R. La Rocca, M. Fulciniti, T. Lakshmikanth et al., “Early hematopoietic zinc finger protein prevents tumor cell recognition by natural killer cells,” The Journal of Immunology, vol. 182, no. 8, pp. 4529–4537, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Kamiya, S. Banno, N. Sasai et al., “Intrinsic transition of embryonic stem-cell differentiation into neural progenitors,” Nature, vol. 470, no. 7335, pp. 503–510, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. R. Spina, G. Filocamo, E. Iaccino et al., “Critical role of zinc finger protein 521 in the control of growth, clonogenicity and tumorigenic potential of medulloblastoma cells,” Oncotarget, vol. 4, no. 8, pp. 1280–1292, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. N. Ohkubo, E. Matsubara, J. Yamanouchi et al., “Abnormal behaviors and developmental disorder of hippocampus in zinc finger protein 521 (ZFP521) mutant mice,” PLoS ONE, vol. 9, no. 3, Article ID e92848, 2014. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Lou, X. Pan, T. Huang et al., “Incoherent feed-forward regulatory loops control segregation of C-mechanoreceptors, nociceptors, and pruriceptors,” Journal of Neuroscience, vol. 35, no. 13, pp. 5317–5329, 2015. View at Publisher · View at Google Scholar
  96. M. J. Justice, H. C. Morse III, N. A. Jenkins, and N. G. Copeland, “Identification of Evi-3, a novel common site of retroviral integration in mouse AKXD B-cell lymphomas,” Journal of Virology, vol. 68, no. 3, pp. 1293–1300, 1994. View at Google Scholar · View at Scopus
  97. S. Warming, T. Suzuki, T. P. Yamaguchi, N. A. Jenkins, and N. G. Copeland, “Early B-cell factor-associated zinc-finger gene is a frequent target of retroviral integration in murine B-cell lymphomas,” Oncogene, vol. 23, no. 15, pp. 2727–2731, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. T. Hiratsuka, Y. Takei, R. Ohmori et al., “ZFP521 contributes to pre-B-cell lymphomagenesis through modulation of the pre-B-cell receptor signaling pathway,” Oncogene, 2015. View at Publisher · View at Google Scholar
  99. K. E. Hentges, K. C. Weiser, T. Schountz, L. S. Woodward, H. C. Morse III, and M. J. Justice, “Evi3, a zinc-finger protein related to EBFAZ, regulates EBF activity in B-cell leukemia,” Oncogene, vol. 24, no. 7, pp. 1220–1230, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Hauer, A. Borkhardt, I. Sánchez-García, and C. Cobaleda, “Genetically engineered mouse models of human B-cell precursor leukemias,” Cell Cycle, vol. 13, no. 18, pp. 2836–2846, 2014. View at Publisher · View at Google Scholar · View at Scopus
  101. K. Miyazaki, N. Yamasaki, H. Oda et al., “Enhanced expression of p210BCR/ABL and aberrant expression of Zfp423/ZNF423 induce blast crisis of chronic myelogenous leukemia,” Blood, vol. 113, no. 19, pp. 4702–4710, 2009. View at Publisher · View at Google Scholar · View at Scopus
  102. L. van der Weyden, G. Giotopoulos, K. Wong et al., “Somatic drivers of B-ALL in a model of ETV6-RUNX1; Pax5+/− leukemia,” BMC Cancer, vol. 15, article 585, 2015. View at Publisher · View at Google Scholar
  103. N. Yamasaki, K. Miyazaki, A. Nagamachi et al., “Identification of Zfp521/ZNF521 as a cooperative gene for E2A-HLF to develop acute B-lineage leukemia,” Oncogene, vol. 29, no. 13, pp. 1963–1975, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. T. Haferlach, A. Kohlmann, L. Wieczorek et al., “Clinical utility of microarray-based gene expression profiling in the diagnosis and subclassification of leukemia: report from the international microarray innovations in leukemia study group,” Journal of Clinical Oncology, vol. 28, no. 15, pp. 2529–2537, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. S. Aibar, C. Fontanillo, C. Droste et al., “Analyse multiple disease subtypes and build associated gene networks using genome-wide expression profiles,” BMC Genomics, vol. 16, supplement 5, p. S3, 2015. View at Publisher · View at Google Scholar
  106. Y. Aoki, T. Watanabe, Y. Saito et al., “Identification of CD34+ and CD34- Leukemia-initiating cells in MLL-rearranged human acute lymphoblastic Leukemia,” Blood, vol. 125, no. 6, pp. 967–980, 2015. View at Publisher · View at Google Scholar · View at Scopus
  107. V. P. Lavallée, I. Baccelli, J. Krosl et al., “The transcriptomic landscape and directed chemical interrogation of MLL-rearranged acute myeloid leukemias,” Nature Genetics, vol. 47, no. 9, pp. 1030–1037, 2015. View at Publisher · View at Google Scholar
  108. K. K. Fleischmann, P. Pagel, I. Schmid, and A. A. Roscher, “RNAi-mediated silencing of MLL-AF9 reveals leukemia-associated downstream targets and processes,” Molecular Cancer, vol. 13, no. 1, article 27, 2014. View at Publisher · View at Google Scholar · View at Scopus
  109. Y. Qiao, X. Wang, R. Wang et al., “AF9 promotes hESC neural differentiation through recruiting TET2 to neurodevelopmental gene loci for methylcytosine hydroxylation,” Cell Discovery, vol. 1, article 15017, 2015. View at Publisher · View at Google Scholar
  110. F. Barabé, J. A. Kennedy, K. J. Hope, and J. E. Dick, “Modeling the initiation and progression of human acute leukemia in mice,” Science, vol. 316, no. 5824, pp. 600–604, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. J. Wei, M. Wunderlich, C. Fox et al., “Microenvironment determines lineage fate in a human model of MLL-AF9 leukemia,” Cancer Cell, vol. 13, no. 6, pp. 483–495, 2008. View at Publisher · View at Google Scholar · View at Scopus
  112. S. J. Horton, J. Jaques, C. Woolthuis et al., “MLL-AF9-mediated immortalization of human hematopoietic cells along different lineages changes during ontogeny,” Leukemia, vol. 27, no. 5, pp. 1116–1126, 2013. View at Publisher · View at Google Scholar · View at Scopus
  113. T. A. Schwickert, H. Tagoh, S. Gültekin et al., “Stage-specific control of early B cell development by the transcription factor Ikaros,” Nature Immunology, vol. 15, no. 3, pp. 283–293, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. E. Bolton-Gillespie, M. Schemionek, H.-U. Klein et al., “Genomic instability may originate from imatinib-refractory chronic myeloid leukemia stem cells,” Blood, vol. 121, no. 20, pp. 4175–4183, 2013. View at Publisher · View at Google Scholar · View at Scopus