Targeting tetramer-forming GABPβ isoforms impairs self-renewal of hematopoietic and leukemic stem cells

Cell Stem Cell

Volumn 11, Issue 2, 2012, Pages 207-219

  Yu, Shuyang ^a   Jing, Xuefang ^a   Colgan, John D ^a   Zhao, Dong Mei ^a   Xue, Hai Hui ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GA BINDING PROTEIN; GA BINDING PROTEIN ALPHA2BETA2; GA BINDING PROTEIN BETA; GA BINDING PROTEIN BETA1; GA BINDING PROTEIN BETA1L; GA BINDING PROTEIN BETA2; IMATINIB; ISOPROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLOOD CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL RENEWAL; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; COMPLEX FORMATION; CONTROLLED STUDY; GENE REGULATORY NETWORK; GENE TARGETING; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; LEUKEMIC STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN SUBUNIT; REGULATORY MECHANISM; STEM CELL; TRANSACTIVATION;

ANIMALS; CELL DIFFERENTIATION; GA-BINDING PROTEIN TRANSCRIPTION FACTOR; HEMATOPOIETIC STEM CELLS; LEUKEMIA; MICE; MICE, KNOCKOUT; NEOPLASTIC STEM CELLS; PROTEIN ISOFORMS;

EID: 84864625483     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.05.021     Document Type: Article

References (56)

1. A.H. Batchelor, D.E. Piper, F.C. de la Brousse, S.L. McKnight, and C. Wolberger The structure of GABPalpha/beta: an ETS domain- ankyrin repeat heterodimer bound to DNA Science 279 1998 1037 1041 (Pubitemid 28113306)
2. A. Briguet, and M.A. Ruegg The Ets transcription factor GABP is required for postsynaptic differentiation in vivo J. Neurosci. 20 2000 5989 5996 (Pubitemid 30658391)
3. T.S. Bush, M. St Coeur, K.K. Resendes, and A.G. Rosmarin GA-binding protein (GABP) and Sp1 are required, along with retinoid receptors, to mediate retinoic acid responsiveness of CD18 (beta 2 leukocyte integrin): a novel mechanism of transcriptional regulation in myeloid cells Blood 101 2003 311 317 (Pubitemid 36025924)
4. Y. Chen, Y. Hu, H. Zhang, C. Peng, and S. Li Loss of the Alox5 gene impairs leukemia stem cells and prevents chronic myeloid leukemia Nat. Genet. 41 2009 783 792
5. T. Cheng, N. Rodrigues, H. Shen, Y. Yang, D. Dombkowski, M. Sykes, and D.T. Scadden Hematopoietic stem cell quiescence maintained by p21cip1/waf1 Science 287 2000 1804 1808
6. Y. Chinenov, M. Henzl, and M.E. Martin The alpha and beta subunits of the GA-binding protein form a stable heterodimer in solution. Revised model of heterotetrameric complex assembly J. Biol. Chem. 275 2000 7749 7756 (Pubitemid 30159679)
7. K. Cui, C. Zang, T.Y. Roh, D.E. Schones, R.W. Childs, W. Peng, and K. Zhao Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation Cell Stem Cell 4 2009 80 93
8. A. Dakic, D. Metcalf, L. Di Rago, S. Mifsud, L. Wu, and S.L. Nutt PU.1 regulates the commitment of adult hematopoietic progenitors and restricts granulopoiesis J. Exp. Med. 201 2005 1487 1502 (Pubitemid 40664092)
9. F.C. de la Brousse, E.H. Birkenmeier, D.S. King, L.B. Rowe, and S.L. McKnight Molecular and genetic characterization of GABP beta Genes Dev. 8 1994 1853 1865
10. R.P. DeKoter, and H. Singh Regulation of B lymphocyte and macrophage development by graded expression of PU.1 Science 288 2000 1439 1441
11. J.M. Galan-Caridad, S. Harel, T.L. Arenzana, Z.E. Hou, F.K. Doetsch, L.A. Mirny, and B. Reizis Zfx controls the self-renewal of embryonic and hematopoietic stem cells Cell 129 2007 345 357 (Pubitemid 46574969)
12. F. Galvagni, S. Capo, and S. Oliviero Sp1 and Sp3 physically interact and co-operate with GABP for the activation of the utrophin promoter J. Mol. Biol. 306 2001 985 996 (Pubitemid 33030000)
13. B.J. Graves Inner workings of a transcription factor partnership Science 279 1998 1000 1002 (Pubitemid 28113293)
14. S. Gugneja, J.V. Virbasius, and R.C. Scarpulla Four structurally distinct, non-DNA-binding subunits of human nuclear respiratory factor 2 share a conserved transcriptional activation domain Mol. Cell. Biol. 15 1995 102 111 (Pubitemid 24379906)
15. H. Hock, M.J. Hamblen, H.M. Rooke, J.W. Schindler, S. Saleque, Y. Fujiwara, and S.H. Orkin Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells Nature 431 2004 1002 1007 (Pubitemid 39434423)
16. H. Hock, E. Meade, S. Medeiros, J.W. Schindler, P.J. Valk, Y. Fujiwara, and S.H. Orkin Tel/Etv6 is an essential and selective regulator of adult hematopoietic stem cell survival Genes Dev. 18 2004 2336 2341 (Pubitemid 39304679)
17. M. Holtz, S.J. Forman, and R. Bhatia Growth factor stimulation reduces residual quiescent chronic myelogenous leukemia progenitors remaining after imatinib treatment Cancer Res. 67 2007 1113 1120
18. B.J. Huntly, and D.G. Gilliland Leukaemia stem cells and the evolution of cancer-stem-cell research Nat. Rev. Cancer 5 2005 311 321 (Pubitemid 40488636)
19. K. Ito, R. Bernardi, A. Morotti, S. Matsuoka, G. Saglio, Y. Ikeda, J. Rosenblatt, D.E. Avigan, J. Teruya-Feldstein, and P.P. Pandolfi PML targeting eradicates quiescent leukaemia-initiating cells Nature 453 2008 1072 1078 (Pubitemid 351871736)
20. T. Ito, H.Y. Kwon, B. Zimdahl, K.L. Congdon, J. Blum, W.E. Lento, C. Zhao, A. Lagoo, G. Gerrard, and L. Foroni Regulation of myeloid leukaemia by the cell-fate determinant Musashi Nature 466 2010 765 768
21. H. Iwasaki, C. Somoza, H. Shigematsu, E.A. Duprez, J. Iwasaki-Arai, S. Mizuno, Y. Arinobu, K. Geary, P. Zhang, and T. Dayaram Distinctive and indispensable roles of PU.1 in maintenance of hematopoietic stem cells and their differentiation Blood 106 2005 1590 1600 (Pubitemid 41208570)
22. X. Jing, D.M. Zhao, T.J. Waldschmidt, and H.H. Xue GABPbeta2 is dispensible for normal lymphocyte development but moderately affects B cell responses J. Biol. Chem. 283 2008 24326 24333
23. H.S. Kang, M.L. Nelson, C.D. Mackereth, M. Schärpf, B.J. Graves, and L.P. McIntosh Identification and structural characterization of a CBP/p300-binding domain from the ETS family transcription factor GABP alpha J. Mol. Biol. 377 2008 636 646
24. K. LaMarco, C.C. Thompson, B.P. Byers, E.M. Walton, and S.L. McKnight Identification of Ets- and notch-related subunits in GA binding protein Science 253 1991 789 792 (Pubitemid 21917218)
25. E. Laurenti, B. Varnum-Finney, A. Wilson, I. Ferrero, W.E. Blanco-Bose, A. Ehninger, P.S. Knoepfler, P.F. Cheng, H.R. MacDonald, and R.N. Eisenman Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity Cell Stem Cell 3 2008 611 624
26. K. Miyamoto, K.Y. Araki, K. Naka, F. Arai, K. Takubo, S. Yamazaki, S. Matsuoka, T. Miyamoto, K. Ito, and M. Ohmura Foxo3a is essential for maintenance of the hematopoietic stem cell pool Cell Stem Cell 1 2007 101 112 (Pubitemid 46865800)
27. K. Naka, T. Hoshii, T. Muraguchi, Y. Tadokoro, T. Ooshio, Y. Kondo, S. Nakao, N. Motoyama, and A. Hirao TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia Nature 463 2010 676 680
28. N. Novershtern, A. Subramanian, L.N. Lawton, R.H. Mak, W.N. Haining, M.E. McConkey, N. Habib, N. Yosef, C.Y. Chang, and T. Shay Densely interconnected transcriptional circuits control cell states in human hematopoiesis Cell 144 2011 296 309
29. J.T. Opferman Life and death during hematopoietic differentiation Curr. Opin. Immunol. 19 2007 497 502 (Pubitemid 47464914)
30. S.H. Orkin, and L.I. Zon Hematopoiesis: an evolving paradigm for stem cell biology Cell 132 2008 631 644 (Pubitemid 351260057)
31. W.S. Pear, J.P. Miller, L. Xu, J.C. Pui, B. Soffer, R.C. Quackenbush, A.M. Pendergast, R. Bronson, J.C. Aster, M.L. Scott, and D. Baltimore Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow Blood 92 1998 3780 3792 (Pubitemid 28525205)
32. A. Ravel-Chapuis, M. Vandromme, J.L. Thomas, and L. Schaeffer Postsynaptic chromatin is under neural control at the neuromuscular junction EMBO J. 26 2007 1117 1128
33. S. Ristevski, D.A. O'Leary, A.P. Thornell, M.J. Owen, I. Kola, and P.J. Hertzog The ETS transcription factor GABPalpha is essential for early embryogenesis Mol. Cell. Biol. 24 2004 5844 5849 (Pubitemid 38787969)
34. A.G. Rosmarin, K.K. Resendes, Z. Yang, J.N. McMillan, and S.L. Fleming GA-binding protein transcription factor: a review of GABP as an integrator of intracellular signaling and protein-protein interactions Blood Cells Mol. Dis. 32 2004 143 154 (Pubitemid 38147712)
35. C. Sawa, M. Goto, F. Suzuki, H. Watanabe, J. Sawada, and H. Handa Functional domains of transcription factor hGABP beta1/E4TF1-53 required for nuclear localization and transcription activation Nucleic Acids Res. 24 1996 4954 4961 (Pubitemid 27007900)
36. C. Sawa, T. Yoshikawa, F. Matsuda-Suzuki, S. Deléhouzée, M. Goto, H. Watanabe, J. Sawada, K. Kataoka, and H. Handa YEAF1/RYBP and YAF-2 are functionally distinct members of a cofactor family for the YY1 and E4TF1/hGABP transcription factors J. Biol. Chem. 277 2002 22484 22490 (Pubitemid 34967221)
37. L. Schaeffer, N. Duclert, M. Huchet-Dymanus, and J.P. Changeux Implication of a multisubunit Ets-related transcription factor in synaptic expression of the nicotinic acetylcholine receptor EMBO J. 17 1998 3078 3090 (Pubitemid 28254380)
38. C.J. Spooner, J.X. Cheng, E. Pujadas, P. Laslo, and H. Singh A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates Immunity 31 2009 576 586
39. Z. Tothova, R. Kollipara, B.J. Huntly, B.H. Lee, D.H. Castrillon, D.E. Cullen, E.P. McDowell, S. Lazo-Kallanian, I.R. Williams, and C. Sears FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress Cell 128 2007 325 339 (Pubitemid 46137992)
40. J.L. Vogel, and T.M. Kristie The novel coactivator C1 (HCF) coordinates multiprotein enhancer formation and mediates transcription activation by GABP EMBO J. 19 2000 683 690 (Pubitemid 30093741)
41. C.R. Walkley, M.L. Fero, W.M. Chien, L.E. Purton, and G.A. McArthur Negative cell-cycle regulators cooperatively control self-renewal and differentiation of haematopoietic stem cells Nat. Cell Biol. 7 2005 172 178 (Pubitemid 40268132)
42. O. Wallerman, M. Motallebipour, S. Enroth, K. Patra, M.S. Bysani, J. Komorowski, and C. Wadelius Molecular interactions between HNF4a, FOXA2 and GABP identified at regulatory DNA elements through ChIP-sequencing Nucleic Acids Res. 37 2009 7498 7508
43. J.C. Wang, and J.E. Dick Cancer stem cells: lessons from leukemia Trends Cell Biol. 15 2005 494 501 (Pubitemid 41253469)
44. Y. Wang, A.V. Krivtsov, A.U. Sinha, T.E. North, W. Goessling, Z. Feng, L.I. Zon, and S.A. Armstrong The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML Science 327 2010 1650 1653
45. A. Wilson, M.J. Murphy, T. Oskarsson, K. Kaloulis, M.D. Bettess, G.M. Oser, A.C. Pasche, C. Knabenhans, H.R. Macdonald, and A. Trumpp c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation Genes Dev. 18 2004 2747 2763 (Pubitemid 39507768)
46. N.K. Wilson, S.D. Foster, X. Wang, K. Knezevic, J. Schütte, P. Kaimakis, P.M. Chilarska, S. Kinston, W.H. Ouwehand, and E. Dzierzak Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators Cell Stem Cell 7 2010 532 544
47. H.H. Xue, J. Bollenbacher, V. Rovella, R. Tripuraneni, Y.B. Du, C.Y. Liu, A. Williams, J.P. McCoy, and W.J. Leonard GA binding protein regulates interleukin 7 receptor alpha-chain gene expression in T cells Nat. Immunol. 5 2004 1036 1044 (Pubitemid 41057723)
48. H.H. Xue, J. Bollenbacher-Reilley, Z. Wu, R. Spolski, X. Jing, Y.C. Zhang, J.P. McCoy, and W.J. Leonard The transcription factor GABP is a critical regulator of B lymphocyte development Immunity 26 2007 421 431 (Pubitemid 46603002)
49. H.H. Xue, X. Jing, J. Bollenbacher-Reilley, D.M. Zhao, J.S. Haring, B. Yang, C. Liu, G.A. Bishop, J.T. Harty, and W.J. Leonard Targeting the GA binding protein beta1L isoform does not perturb lymphocyte development and function Mol. Cell. Biol. 28 2008 4300 4309 (Pubitemid 351904952)
50. Z.F. Yang, K. Drumea, J. Cormier, J. Wang, X. Zhu, and A.G. Rosmarin GABP transcription factor is required for myeloid differentiation, in part, through its control of Gfi-1 expression Blood 118 2011 2243 2253
51. O.H. Yilmaz, R. Valdez, B.K. Theisen, W. Guo, D.O. Ferguson, H. Wu, and S.J. Morrison Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells Nature 441 2006 475 482 (Pubitemid 44050144)
52. S. Yu, D.M. Zhao, R. Jothi, and H.H. Xue Critical requirement of GABPalpha for normal T cell development J. Biol. Chem. 285 2010 10179 10188
53. S. Yu, K. Cui, R. Jothi, D.M. Zhao, X. Jing, K. Zhao, and H.H. Xue GABP controls a critical transcription regulatory module that is essential for maintenance and differentiation of hematopoietic stem/progenitor cells Blood 117 2011 2166 2178
54. R. Yücel, H. Karsunky, L. Klein-Hitpass, and T. Möröy The transcriptional repressor Gfi1 affects development of early, uncommitted c-Kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus J. Exp. Med. 197 2003 831 844 (Pubitemid 36437861)
55. J. Zhang, J.C. Grindley, T. Yin, S. Jayasinghe, X.C. He, J.T. Ross, J.S. Haug, D. Rupp, K.S. Porter-Westpfahl, and L.M. Wiedemann PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention Nature 441 2006 518 522 (Pubitemid 44050154)
56. C. Zhao, J. Blum, A. Chen, H.Y. Kwon, S.H. Jung, J.M. Cook, A. Lagoo, and T. Reya Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo Cancer Cell 12 2007 528 541 (Pubitemid 350199070)