Myeloid translocation gene 16 is required for maintenance of haematopoietic stem cell quiescence

EMBO Journal

Volumn 31, Issue 6, 2012, Pages 1494-1505

  Fischer, Melissa A ^a   Moreno Miralles, Isabel ^a,b   Hunt, Aubrey ^a   Chyla, Brenda J ^a,d   Hiebert, Scott W ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d ABBOTT LABORATORIES   (United States)

Author keywords

CBFA2T3; haematopoietic stem cells; myeloid leukaemia; transcription

Indexed keywords

BROXURIDINE; TRANSCRIPTION FACTOR E2A; TRANSCRIPTION FACTOR E2F2;

ANIMAL CELL; ARTICLE; BINDING SITE; BONE MARROW; BONE MARROW TRANSPLANTATION; CELL CYCLE; CELL RENEWAL; CONTROLLED STUDY; FLOW CYTOMETRY; GENE; GENE EXPRESSION; GENE INACTIVATION; HEMATOPOIETIC STEM CELL; INTRON; MOUSE; MTG16 GENE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CELLS, CULTURED; E2F2 TRANSCRIPTION FACTOR; GENE EXPRESSION; HEMATOPOIETIC STEM CELLS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL; MICE, NUDE; NUCLEAR PROTEINS; S PHASE; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 84858794817     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.500     Document Type: Article

References (65)

1. Amann JM, Chyla BJ, Ellis TC, Martinez A, Moore AC, Franklin JL, McGhee L, Meyers S, Ohm JE, Luce KS, Ouelette AJ, Washington MK, Thompson MA, King D, Gautam S, Coffey RJ, Whitehead RH, Hiebert SW (2005) Mtgr1 is a transcriptional corepressor that is required for maintenance of the secretory cell lineage in the small intestine. Mol Cell Biol 25: 9576-9585 (Pubitemid 41507856)
2. Amann JM, Nip J, Strom DK, Lutterbach B, Harada H, Lenny N, Downing JR, Meyers S, Hiebert SW (2001) ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol Cell Biol 21: 6470-6483 (Pubitemid 32927415)
3. Bai X, Kim J, Yang Z, Jurynec MJ, Akie TE, Lee J, LeBlanc J, Sessa A, Jiang H, DiBiase A, Zhou Y, Grunwald DJ, Lin S, Cantor AB, Orkin SH, Zon LI (2010) TIF1gamma controls erythroid cell fate by regulating transcription elongation. Cell 142: 133-143
4. Boggs DR (1984) The total marrow mass of the mouse: a simplified method of measurement. Am J Hematol 16: 277-286 (Pubitemid 14127685)
5. Buitenhuis M, van Deutekom HW, Verhagen LP, Castor A, Jacobsen SE, Lammers JW, Koenderman L, Coffer PJ (2005) Differential regulation of granulopoiesis by the basic helix-loop-helix transcriptional inhibitors Id1 and Id2. Blood 105: 4272-4281 (Pubitemid 40720773)
6. Cai Y, Xu Z, Xie J, Ham AJ, Koury MJ, Hiebert SW, Brandt SJ (2009) Eto2/MTG16 and MTGR1 are heteromeric corepressors of the TAL1/SCL transcription factor in murine erythroid progenitors. Biochem Biophys Res Commun 390: 295-301
7. Calabi F, Pannell R, Pavloska G (2001) Gene targeting reveals a crucial role for MTG8 in the gut. Mol Cell Biol 21: 5658-5666 (Pubitemid 32702468)
8. Capron C, Lecluse Y, Kaushik AL, Foudi A, Lacout C, Sekkai D, Godin I, Albagli O, Poullion I, Svinartchouk F, Schanze E, Vainchenker W, Sablitzky F, Bennaceur-Griscelli A, Dumenil D (2006) The SCL relative LYL-1 is required for fetal and adult hematopoietic stem cell function and B-cell differentiation. Blood 107: 4678-4686 (Pubitemid 43882615)
9. Chevallier N, Corcoran CM, Lennon C, Hyjek E, Chadburn A, Bardwell VJ, Licht JD, Melnick A (2004) ETO protein of t(8;21) AML is a corepressor for Bcl-6 B-cell lymphoma oncoprotein. Blood 103: 1454-1463 (Pubitemid 38168662)
10. Chyla BJ, Moreno-Miralles I, Steapleton MA, Thompson MA, Bhaskara S, Engel M, Hiebert SW (2008) Deletion of Mtg16, a target of t(16;21), alters hematopoietic progenitor cell proliferation and lineage allocation. Mol Cell Biol 28: 6234-6247
11. Dalla-Favera R, Bregni M, Erikson J, Patterson D, Gallow RC, Croce CM (1982) Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci USA 79: 7824-7827 (Pubitemid 13182471)
12. Davis JN, Williams BJ, Herron JT, Galiano FJ, Meyers S (1999) ETO-2, a new member of the ETO-family of nuclear proteins. Oncogene 18: 1375-1383 (Pubitemid 29094890)
13. DeGregori J, Leone G, Miron A, Jakoi L, Nevins JR (1997) Distinct roles for E2F proteins in cell growth control and apoptosis. Proc Natl Acad Sci USA 94: 7245-7250 (Pubitemid 27345300)
14. Deneault E, Cellot S, Faubert A, Laverdure JP, Frechette M, Chagraoui J, Mayotte N, Sauvageau M, Ting SB, Sauvageau G (2009) A functional screen to identify novel effectors of hematopoietic stem cell activity. Cell 137: 369-379
15. Engel ME, Nguyen HN, Mariotti J, Hunt A, Hiebert SW (2010) Myeloid translocation gene 16 (MTG16) interacts with Notch transcription complex components to integrate Notch signaling in hematopoietic cell fate specification. Mol Cell Biol 30: 1852-1863
16. Erickson P, Gao J, Chang KS, Look T, Whisenant E, Raimondi S, Lasher R, Trujillo J, Rowley J, Drabkin H (1992) Identification of breakpoints in t(8;21) acute myelogenous leukemia and isolation of a fusion transcript, AML1/ETO, with similarity to Drosophila segmentation gene, runt. Blood 80: 1825-1831
17. Fujiwara T, Lee HY, Sanalkumar R, Bresnick EH (2010) Building multifunctionality into a complex containing master regulators of hematopoiesis. Proc Natl Acad Sci USA 107: 20429-20434
18. Gamou T, Kitamura E, Hosoda F, Shimizu K, Shinohara K, Hayashi Y, Nagase T, Yokoyama Y, Ohki M (1998) The partner gene of AML1 in t(16;21) myeloid malignancies is a novel member of the MTG8(ETO) family. Blood 91: 4028-4037 (Pubitemid 28261962)
19. Gelmetti V, Zhang J, Fanelli M, Minucci S, Pelicci PG, Lazar MA (1998) Aberrant recruitment of the nuclear receptor corepressorhistone deacetylase complex by the acute myeloid leukemia fusion partner ETO. Mol Cell Biol 18: 7185-7191 (Pubitemid 28533038)
20. Goardon N, Lambert JA, Rodriguez P, Nissaire P, Herblot S, Thibault P, Dumenil D, Strouboulis J, Romeo PH, Hoang T (2006) ETO2 coordinates cellular proliferation and differentiation during erythropoiesis. EMBO J 25: 357-366 (Pubitemid 43152856)
21. Graninger WB, Seto M, Boutain B, Goldman P, Korsmeyer SJ (1987) Expression of Bcl-2 and Bcl-2-Ig fusion transcripts in normal and neoplastic cells. J Clin Invest 80: 1512-1515 (Pubitemid 18027800)
22. Guo C, Hu Q, Yan C, Zhang J (2009) Multivalent binding of the ETO corepressor to E proteins facilitates dual repression controls targeting chromatin and the basal transcription machinery. Mol Cell Biol 29: 2644-2657
23. Hamlett I, Draper J, Strouboulis J, Iborra F, Porcher C, Vyas P (2008) Characterization of megakaryocyte GATA1-interacting proteins: the corepressor ETO2 and GATA1 interact to regulate terminal megakaryocyte maturation. Blood 112: 2738-2749
24. Hildebrand D, Tiefenbach J, Heinzel T, Grez M, Maurer AB (2001) Multiple regions of ETO cooperate in transcriptional repression. J Biol Chem 276: 9889-9895
25. Hock H, Hamblen MJ, Rooke HM, Schindler JW, Saleque S, Fujiwara Y, Orkin SH (2004) Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature 431: 1002-1007 (Pubitemid 39434423)
26. Hope KJ, Jin L, Dick JE (2003) Human acute myeloid leukemia stem cells. Arch Med Res 34: 507-514 (Pubitemid 38084704)
27. Hunt A, Fischer M, Engel ME, Hiebert SW (2011) Mtg16/Eto2 contributes to murine T-cell development. Mol Cell Biol 31: 2544-2551
28. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM, Yue P, Haverty PM, Bourgon R, Zheng J, Moorhead M, Chaudhuri S, Tomsho LP, Peters BA, Pujara K, Cordes S, Davis DP, Carlton VE, Yuan W, Li L et al (2010) Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466: 869-873
29. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121: 1109-1121 (Pubitemid 40884400)
30. Kitabayashi I, Ida K, Morohoshi F, Yokoyama A, Mitsuhashi N, Shimizu K, Nomura N, Hayashi Y, Ohki M (1998) The AML1-MTG8 leukemic fusion protein forms a complex with a novel member of the MTG8(ETO/CDR) family, MTGR1. Mol Cell Biol 18: 846-858 (Pubitemid 28063418)
31. Li QL, Ito K, Sakakura C, Fukamachi H, Inoue K, Chi XZ, Lee KY, Nomura S, Lee CW, Han SB, Kim HM, Kim WJ, Yamamoto H, Yamashita N, Yano T, Ikeda T, Itohara S, Inazawa J, Abe T, Hagiwara A et al (2002) Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109: 113-124 (Pubitemid 34327521)
32. Lin YC, Jhunjhunwala S, Benner C, Heinz S, Welinder E, Mansson R, Sigvardsson M, Hagman J, Espinoza CA, Dutkowski J, Ideker T, Glass CK, Murre C (2010) A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat Immunol 11: 635-643
33. Lindberg SR, Olsson A, Persson AM, Olsson I (2005) The Leukemiaassociated ETO homologues are differently expressed during hematopoietic differentiation. Exp Hematol 33: 189-198 (Pubitemid 40164901)
34. Linggi B, Muller-Tidow C, van de Locht L, Hu M, Nip J, Serve H, Berdel WE, van der Reijden B, Quelle DE, Rowley JD, Cleveland J, Jansen JH, Pandolfi PP, Hiebert SW (2002) The t(8;21) fusion protein, AML1 ETO, specifically represses the transcription of the p14(ARF) tumor suppressor in acute myeloid leukemia. Nat Med 8: 743-750 (Pubitemid 34778729)
35. Liu Y, Cheney MD, Gaudet JJ, Chruszcz M, Lukasik SM, Sugiyama D, Lary J, Cole J, Dauter Z, Minor W, Speck NA, Bushweller JH (2006) The tetramer structure of the Nervy homology two domain, NHR2, is critical for AML1/ETO's activity. Cancer Cell 9: 249-260
36. Lutterbach B, Westendorf JJ, Linggi B, Patten A, Moniwa M, Davie JR, Huynh KD, Bardwell VJ, Lavinsky RM, Rosenfeld MG, Glass C, Seto E, Hiebert SW (1998) ETO, a target of t(8;21) in acute leukemia, interacts with the N-CoR and mSin3 corepressors. Mol Cell Biol 18: 7176-7184 (Pubitemid 28533037)
37. Martinez JA, Williams CS, Amann JM, Ellis TC, Moreno-Miralles I, Washington MK, Gregoli P, Hiebert SW (2006) Deletion of Mtgr1 sensitizes the colonic epithelium to dextran sodium sulfateinduced colitis. Gastroenterology 131: 579-588 (Pubitemid 44142465)
38. McGhee L, Bryan J, Elliott L, Grimes HL, Kazanjian A, Davis JN, Meyers S (2003) Gfi-1 attaches to the nuclear matrix, associates with ETO (MTG8) and histone deacetylase proteins, and represses transcription using a TSA-sensitive mechanism. J Cell Biochem 89: 1005-1018 (Pubitemid 36927731)
39. Melnick AM, Westendorf JJ, Polinger A, Carlile GW, Arai S, Ball HJ, Lutterbach B, Hiebert SW, Licht JD (2000) The ETO protein disrupted in t(8;21)-associated acute myeloid leukemia is a corepressor for the promyelocytic leukemia zinc finger protein. Mol Cell Biol 20: 2075-2086 (Pubitemid 30123823)
40. Miller CL, Dykstra B, Eaves CJ (2008) Characterization of mouse hematopoietic stem and progenitor cells. Curr Protoc Immunol Chapter 22, Unit 22B 22
41. Miyoshi H, Kozu T, Shimizu K, Enomoto K, Maseki N, Kaneko Y, Kamada N, Ohki M (1993) The t(8;21) translocation in acute myeloid leukemia results in production of an AML1-MTG8 fusion transcript. EMBO J 12: 2715-2721 (Pubitemid 23218321)
42. Miyoshi H, Shimizu K, Kozu T, Maseki N, Kaneko Y, Ohki M (1991) t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc Natl Acad Sci USA 88: 10431-10434 (Pubitemid 21915849)
43. Moore AC, Amann JM, Williams CS, Tahinci E, Farmer TE, Martinez JA, Yang G, Luce KS, Lee E, Hiebert SW (2008) Myeloid translocation gene family members associate with T-cell factors (TCFs) and influence TCF-dependent transcription. Mol Cell Biol 28: 977-987 (Pubitemid 351160054)
44. Pabst T, Mueller BU, Harakawa N, Schoch C, Haferlach T, Behre G, Hiddemann W, Zhang DE, Tenen DG (2001) AML1-ETO downregulates the granulocytic differentiation factor C/EBPalpha in t(8;21) myeloid leukemia. Nat Med 7: 444-451 (Pubitemid 32298547)
45. Park S, ChenW, Cierpicki T, Tonelli M, Cai X, Speck NA, Bushweller JH (2009) Structure of the AML1-ETO eTAFH domain-HEB peptide complex and its contribution to AML1-ETO activity. Blood 113: 3558-3567
46. Peterson LF, Zhang DE (2004) The 8;21 translocation in leukemogenesis. Oncogene 23: 4255-4262 (Pubitemid 38758592)
47. Plevin MJ, Zhang J, Guo C, Roeder RG, Ikura M (2006) The acute myeloid leukemia fusion protein AML1-ETO targets E proteins via a paired amphipathic helix-like TBP-associated factor homology domain. Proc Natl Acad Sci USA 103: 10242-10247 (Pubitemid 44051151)
48. Salat D, Liefke R, Wiedenmann J, Borggrefe T, Oswald F (2008) ETO, but not leukemogenic fusion protein AML1/ETO, augments RBP-Jkappa/SHARP-mediated repression of notch target genes. Mol Cell Biol 28: 3502-3512 (Pubitemid 351657111)
49. Santaguida M, Schepers K, King B, Sabnis AJ, Forsberg EC, Attema JL, Braun BS, Passegue E (2009) JunB protects against myeloid malignancies by limiting hematopoietic stem cell proliferation and differentiation without affecting self-renewal. Cancer Cell 15: 341-352
50. Schuh AH, Tipping AJ, Clark AJ, Hamlett I, Guyot B, Iborra FJ, Rodriguez P, Strouboulis J, Enver T, Vyas P, Porcher C (2005) ETO-2 associates with SCL in erythroid cells and megakaryocytes and provides repressor functions in erythropoiesis. Mol Cell Biol 25: 10235-10250 (Pubitemid 41681951)
51. Semerad CL, Mercer EM, Inlay MA, Weissman IL, Murre C (2009) E2A proteins maintain the hematopoietic stem cell pool and promote the maturation of myelolymphoid and myeloerythroid progenitors. Proc Natl Acad Sci USA 106: 1930-1935
52. Shizuru JA, Negrin RS, Weissman IL (2005) Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu Rev Med 56: 509-538 (Pubitemid 40305275)
53. Silva FP, Morolli B, Storlazzi CT, Anelli L, Wessels H, Bezrookove V, Kluin-Nelemans HC, Giphart-Gassler M (2003) Identification of RUNX1/AML1 as a classical tumor suppressor gene. Oncogene 22: 538-547 (Pubitemid 36188611)
54. Soler E, Andrieu-Soler C, de Boer E, Bryne JC, Thongjuea S, Stadhouders R, Palstra RJ, Stevens M, Kockx C, van Ijcken W, Hou J, Steinhoff C, Rijkers E, Lenhard B, Grosveld F (2010) The genome-wide dynamics of the binding of Ldb1 complexes during erythroid differentiation. Genes Dev 24: 277-289
55. Song WJ, Sullivan MG, Legare RD, Hutchings S, Tan X, Kufrin D, Ratajczak J, Resende IC, Haworth C, Hock R, Loh M, Felix C, Roy DC, Busque L, Kurnit D, Willman C, Gewirtz AM, Speck NA, Bushweller JH, Li FP et al (1999) Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet 23: 166-175 (Pubitemid 29455388)
56. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13: 2129-2141 (Pubitemid 37161770)
57. Vangala RK, Heiss-Neumann MS, Rangatia JS, Singh SM, Schoch C, Tenen DG, Hiddemann W, Behre G (2003) The myeloid master regulator transcription factor PU.1 is inactivated by AML1-ETO in t(8;21) myeloid leukemia. Blood 101: 270-277 (Pubitemid 36025918)
58. Wang J, Hoshino T, Redner RL, Kajigaya S, Liu JM (1998) ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3/HDAC1 complex. Proc Natl Acad Sci USA 95: 10860-10865 (Pubitemid 28413159)
59. Wang X, Seed B (2003) A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 31: e154
60. Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z et al (2007) The genomic landscapes of human breast and colorectal cancers. Science 318: 1108-1113 (Pubitemid 350134889)
61. Yan M, Ahn EY, Hiebert SW, Zhang DE (2009) RUNX1/AML1 DNAbinding domain and ETO/MTG8 NHR2-dimerization domain are critical to AML1-ETO9a leukemogenesis. Blood 113: 883-886
62. Yan M, Burel SA, Peterson LF, Kanbe E, Iwasaki H, Boyapati A, Hines R, Akashi K, Zhang DE (2004) Deletion of an AML1-ETO C-terminal NcoR/SMRT-interacting region strongly induces leukemia development. Proc Natl Acad Sci USA 101: 17186-17191 (Pubitemid 39627795)
63. Yang G, Khalaf W, van de Locht L, Jansen JH, Gao M, Thompson MA, van der Reijden BA, Gutmann DH, Delwel R, Clapp DW, Hiebert SW (2005) Transcriptional repression of the neurofibromatosis-1 tumor suppressor by the t(8;21) fusion protein. Mol Cell Biol 25: 5869-5879 (Pubitemid 40946544)
64. Zeng H, Yucel R, Kosan C, Klein-Hitpass L, Moroy T (2004) Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells. EMBO J 23: 4116-4125 (Pubitemid 39472432)
65. Zhang J, Kalkum M, Yamamura S, Chait BT, Roeder RG (2004) E protein silencing by the leukemogenic AML1-ETO fusion protein. Science 305: 1286-1289 (Pubitemid 39129232)