A germline point mutation in Runx1 uncouples its role in definitive hematopoiesis from differentiation

Experimental Hematology

Volumn 41, Issue 11, 2013, Pages

  Dowdy, Christopher R ^b   Frederick, Dana ^b   Zaidi, Sayyed K ^a   Colby, Jennifer L ^b   Lian, Jane B ^a   Van Wijnen, Andre J ^c   Gerstein, Rachel M ^b   Stein, Janet L ^a   Stein, Gary S ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c MAYO CLINIC ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; HYBRID PROTEIN; MESSENGER RNA; SMAD PROTEIN; TRANSCRIPTION FACTOR RUNX1; TRANSFORMING GROWTH FACTOR BETA;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EMBRYO; ANIMAL TISSUE; ARTICLE; B LYMPHOBLAST; CELL LINEAGE; CELL MATURATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE FUNCTION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VIVO STUDY; LETHALITY; MISSENSE MUTATION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; RUNX1 GENE; T LYMPHOBLAST; TRANSACTIVATION;

MUS;

EID: 84887612674     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2013.06.006     Document Type: Article

References (57)

1. Okuda T., van Deursen J., Hiebert S.W., Grosveld G., Downing J.R. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 1996, 84:321-330.
2. North T.E., Stacy T., Matheny C.J., Speck N.A., de Bruijn M.F. Runx1 is expressed in adult mouse hematopoietic stem cells and differentiating myeloid and lymphoid cells, but not in maturing erythroid cells. Stem Cells 2004, 22:158-168.
3. Woolf E., Xiao C., Fainaru O., et al. Runx3 and Runx1 are required for CD8 T cell development during thymopoiesis. Proc Natl Acad Sci U S A 2003, 100:7731-7736.
4. Look A.T. Oncogenic transcription factors in the human acute leukemias. Science 1997, 278:1059-1064.
5. Harada H., Harada Y., Niimi H., Kyo T., Kimura A., Inaba T. High incidence of somatic mutations in the AML1/RUNX1 gene in myelodysplastic syndrome and low blast percentage myeloid leukemia with myelodysplasia. Blood 2004, 103:2316-2324.
6. Kuo M.C., Liang D.C., Huang C.F., et al. RUNX1 mutations are frequent in chronic myelomonocytic leukemia and mutations at the C-terminal region might predict acute myeloid leukemia transformation. Leukemia 2009, 23:1426-1431.
7. Dowdy C.R., Xie R., Frederick D., et al. Definitive hematopoiesis requires Runx1 C-terminal-mediated subnuclear targeting and transactivation. Hum Mol Genet 2010, 19:1048-1057.
8. North T., Gu T.L., Stacy T., et al. Cbfa2 is required for the formation ofintra-aortic hematopoietic clusters. Development 1999, 126:2563-2575.
9. Liakhovitskaia A., Lana-Elola E., Stamateris E., Rice D.P., van't Hof R.J., Medvinsky A. The essential requirement for Runx1 in the development of the sternum. Dev Biol 2010, 340:539-546.
10. Fukushima-Nakase Y., Naoe Y., Taniuchi I., Hosoi H., Sugimoto T., Okuda T. Shared and distinct roles mediated through C-terminal subdomains of acute myeloid leukemia/Runt-related transcription factor molecules in murine development. Blood 2005, 105:4298-4307.
11. Ichikawa M., Asai T., Saito T., et al. AML-1 is required for megakaryocytic maturation and lymphocytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat Med 2004, 10:299-304.
12. Barseguian K., Lutterbach B., Hiebert S.W., et al. Multiple subnuclear targeting signals of the leukemia-related AML1/ETO and ETO repressor proteins. Proc Natl Acad Sci U S A 2002, 99:15434-15439.
13. Durst K.L., Lutterbach B., Kummalue T., Friedman A.D., Hiebert S.W. The inv(16) fusion protein associates with corepressors via a smooth muscle myosin heavy-chain domain. Mol Cell Biol 2003, 23:607-619.
14. Kitabayashi I., Yokoyama A., Shimizu K., Ohki M. Interaction and functional cooperation of the leukemia-associated factors AML1 and p300 in myeloid cell differentiation. EMBO J 1998, 17:2994-3004.
15. McNeil S., Zeng C., Harrington K.S., et al. The t(8;21) chromosomal translocation in acute myelogenous leukemia modifies intranuclear targeting of the AML1/CBFalpha2 transcription factor. Proc Natl Acad Sci U S A 1999, 96:14882-14887.
16. Reed-Inderbitzin E., Moreno-Miralles I., Vanden-Eynden S.K., et al. RUNX1 associates with histone deacetylases and SUV39H1 to repress transcription. Oncogene 2006, 25:5777-5786.
17. Vradii D., Zaidi S.K., Lian J.B., van Wijnen A.J., Stein J.L., Stein G.S. Point mutation in AML1 disrupts subnuclear targeting, prevents myeloid differentiation, and effects a transformation-like phenotype. Proc Natl Acad Sci U S A 2005, 102:7174-7179.
18. Zeng C., van Wijnen A.J., Stein J.L., et al. Identification of a nuclear matrix targeting signal in the leukemia and bone-related AML/CBF-alpha transcription factors. Proc Natl Acad Sci U S A 1997, 94:6746-6751.
19. Zaidi S.K., Dowdy C.R., van Wijnen A.J., et al. Altered Runx1 subnuclear targeting enhances myeloid cell proliferation and blocks differentiation by activating a miR-24/MKP-7/MAPK network. Cancer Res 2009, 69:8249-8255.
20. Stein G.S., Lian J.B., Stein J.L., et al. Combinatorial organization of the transcriptional regulatory machinery in biological control and cancer. Adv Enzyme Regul 2005, 45:136-154.
21. Bakshi R., Zaidi S.K., Pande S., et al. The leukemogenic t(8;21) fusion protein AML1-ETO controls rRNA genes and associates with nucleolar-organizing regions at mitotic chromosomes. J Cell Sci 2008, 121:3981-3990.
22. Li X., Vradii D., Gutierrez S., et al. Subnuclear targeting of Runx1 is required for synergistic activation of the myeloid specific M-CSF receptor promoter by PU.1. J Cell Biochem 2005, 96:795-809.
23. Javed A., Afzal F., Bae J.S., et al. Specific residues of RUNX2 are obligatory for formation of BMP2-induced RUNX2-SMAD complex to promote osteoblast differentiation. Cells Tissues Organs 2009, 189:133-137.
24. Javed A., Bae J.S., Afzal F., et al. Structural coupling of Smad and Runx2 for execution of the BMP2 osteogenic signal. J Biol Chem 2008, 283:8412-8422.
25. Leboy P., Grasso-Knight G., D'Angelo M., et al. Smad-Runx interactions during chondrocyte maturation. J Bone Joint Surg Am 2001, 83-A(Suppl 1):S15-S22.
26. Afzal F., Pratap J., Ito K., et al. Smad function and intranuclear targeting share a Runx2 motif required for osteogenic lineage induction and BMP2 responsive transcription. J Cell Physiol 2005, 204:63-72.
27. Nickerson J.A., Krockmalnic G., Wan K.M., Penman S. The nuclear matrix revealed by eluting chromatin from a cross-linked nucleus. Proc Natl Acad Sci U S A 1997, 94:4446-4450.
28. Cai X., Gaudet J.J., Mangan J.K., et al. Runx1 loss minimally impacts long-term hematopoietic stem cells. PLoS One 2011, 6:e28430.
29. Tsuzuki S., Hong D., Gupta R., Matsuo K., Seto M., Enver T. Isoform-specific potentiation of stem and progenitor cell engraftment by AML1/RUNX1. PLoS Med 2007, 4:e172.
30. Ran D., Shia W.J., Lo M.C., et al. RUNX1a enhances hematopoietic lineage commitment from human embryonic stem cells and inducible pluripotent stem cells. Blood 2013, 121:2882-2890.
31. Fortunel N.O., Hatzfeld A., Hatzfeld J.A. Transforming growth factor-beta: pleiotropic role in the regulation of hematopoiesis. Blood 2000, 96:2022-2036.
32. Ruscetti F.W., Akel S., Bartelmez S.H. Autocrine transforming growth factor-beta regulation of hematopoiesis: many outcomes that depend on the context. Oncogene 2005, 24:5751-5763.
33. Kumar R., Fossati V., Israel M., Snoeck H.W. Lin-Sca1+kit- bone marrow cells contain early lymphoid-committed precursors that are distinct from common lymphoid progenitors. J Immunol 2008, 181:7507-7513.
34. Putz G., Rosner A., Nuesslein I., Schmitz N., Buchholz F. AML1 deletion in adult mice causes splenomegaly and lymphomas. Oncogene 2006, 25:929-939.
35. Growney J.D., Shigematsu H., Li Z., et al. Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. Blood 2005, 106:494-504.
36. Song W.J., Sullivan M.G., Legare R.D., et al. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet 1999, 23:166-175.
37. Liu Y., Pop R., Sadegh C., Brugnara C., Haase V.H., Socolovsky M. Suppression of Fas-FasL coexpression by erythropoietin mediates erythroblast expansion during the erythropoietic stress response invivo. Blood 2006, 108:123-133.
38. Koulnis M., Porpiglia E., Porpiglia P.A., et al. Contrasting dynamic responses invivo of the Bcl-xL and Bim erythropoietic survival pathways. Blood 2012, 119:1228-1239.
39. Lal A., Vichinsky E. The role of fetal hemoglobin-enhancing agents in thalassemia. Semin Hematol 2004, 41(4 Suppl 6):17-22.
40. Ichikawa M., Goyama S., Asai T., et al. AML1/Runx1 negatively regulates quiescent hematopoietic stem cells in adult hematopoiesis. J Immunol 2008, 180:4402-4408.
41. Kuo Y.H., Gerstein R.M., Castilla L.H. Cbfbeta-SMMHC impairs differentiation of common lymphoid progenitors and reveals an essential role for RUNX in early B-cell development. Blood 2008, 111:1543-1551.
42. Seo W., Ikawa T., Kawamoto H., Taniuchi I. Runx1-Cbfbeta facilitates early B lymphocyte development by regulating expression of Ebf1. J Exp Med 2012, 209:1255-1262.
43. Wong W.F., Nakazato M., Watanabe T., et al. Over-expression of Runx1 transcription factor impairs the development of thymocytes from the double-negative to double-positive stages. Immunology 2010, 130:243-253.
44. Nishimura M., Fukushima-Nakase Y., Fujita Y., et al. VWRPY motif-dependent and -independent roles of AML1/Runx1 transcription factor in murine hematopoietic development. Blood 2004, 103:562-570.
45. Blyth K., Slater N., Hanlon L., et al. Runx1 promotes B-cell survival and lymphoma development. Blood Cells Mol Dis 2009, 43:12-19.
46. Egawa T. Runx and ThPOK: A balancing act to regulate thymocyte lineage commitment. J Cell Biochem 2009, 107:1037-1045.
47. Grossmann V., Kern W., Harbich S., et al. Prognostic relevance of RUNX1 mutations in T-cell acute lymphoblastic leukemia. Haematologica 2011, 96:1874-1877.
48. Hashidate T., Murakami N., Nakagawa M., et al. AML1 enhances the expression of leukotriene B4 type-1 receptor in leukocytes. FASEB J 2010, 24:3500-3510.
49. Lukin K., Fields S., Lopez D., et al. Compound haploinsufficiencies of Ebf1 and Runx1 genes impede B cell lineage progression. Proc Natl Acad Sci U S A 2010, 107:7869-7874.
50. Spender L.C., Whiteman H.J., Karstegl C.E., Farrell P.J. Transcriptional cross-regulation of RUNX1 by RUNX3 in human B cells. Oncogene 2005, 24:1873-1881.
51. Swirski F.K., Nahrendorf M., Etzrodt M., et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009, 325:612-616.
52. Yokomizo T., Hasegawa K., Ishitobi H., et al. Runx1 is involved in primitive erythropoiesis in the mouse. Blood 2008, 111:4075-4080.
53. Choi Y., Elagib K.E., Delehanty L.L., Goldfarb A.N. Erythroid inhibition by the leukemic fusion AML1-ETO is associated with impaired acetylation of the major erythroid transcription factor GATA-1. Cancer Res 2006, 66:2990-2996.
54. Old J.M. Screening and genetic diagnosis of haemoglobin disorders. Blood Rev 2003, 17:43-53.
55. Lorsbach R.B., Moore J., Ang S.O., Sun W., Lenny N., Downing J.R. Role of RUNX1 in adult hematopoiesis: Analysis of RUNX1-IRES-GFP knock-in mice reveals differential lineage expression. Blood 2004, 103:2522-2529.
56. Sun W., Downing J.R. Haploinsufficiency of AML1 results in a decrease in the number of LTR-HSCs while simultaneously inducing an increase in more mature progenitors. Blood 2004, 104:3565-3572.
57. Zaidi S.K., Javed A., Pratap J., et al. Alterations in intranuclear localization of Runx2 affect biological activity. J Cell Physiol 2006, 209:935-942.