CoChat
Sign Up
Cited by 155Acute Myeloid Leukemia ResearchHematopoietic Stem Cell TransplantationChromatin Remodeling and Cancer

Expression of mutant Asxl1 perturbs hematopoiesis and promotes susceptibility to leukemic transformation

Open access
Nagase, Reina, Inoue, Daichi, Pastore, Alessandro, Fujino, Takeshi, Hou, Hsin-An, Yamasaki, Norimasa, Goyama, Susumu, Saika, Makoto +12 more·2018·Journal of Experimental Medicine
DOI 10.1084/jem.20171151PMC PMC5987913
Open this paper in CoChat — free accountOpen PDF

Abstract

Additional sex combs like 1 (ASXL1) is frequently mutated in myeloid malignancies and clonal hematopoiesis of indeterminate potential (CHIP). Although loss of ASXL1 promotes hematopoietic transformation, there is growing evidence that ASXL1 mutations might confer an alteration of function. In this study, we identify that physiological expression of a C-terminal truncated Asxl1 mutant in vivo using conditional knock-in (KI) results in myeloid skewing, age-dependent anemia, thrombocytosis, and morphological dysplasia. Although expression of mutant Asxl1 altered the functions of hematopoietic stem cells (HSCs), it maintained their survival in competitive transplantation assays and increased susceptibility to leukemic transformation by co-occurring RUNX1 mutation or viral insertional mutagenesis. KI mice displayed substantial reductions in H3K4me3 and H2AK119Ub without significant reductions in H3K27me3, distinct from the effects of Asxl1 loss. Chromatin immunoprecipitation followed by next-generation sequencing analysis demonstrated opposing effects of wild-type and mutant Asxl1 on H3K4me3. These findings reveal that ASXL1 mutations confer HSCs with an altered epigenome and increase susceptibility for leukemic transformation, presenting a novel model for CHIP.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1084/jem.20171151

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • C-terminally truncated ASXL1 binds to the Nr4a1 locus in murine marrow cells.

    “C-terminally truncated ASXL1 binds to the Nr4a1 locus in murine marrow cells, suggesting a possible direct mechanism of regulation (analysis of data in [51]).”

    From Clonal hematopoiesis and inflammation – the perpetual cycle (2023) · cites this paper as [51]

    The Results section reports mutant Asxl1 ChIP-seq binding data from mouse bone-marrow cells, and the Methods section identifies the deposited dataset. Our copy identifies Id3 as a bound locus but does not identify Nr4a1; the specific Nr4a1 finding is therefore not verifiable from the paper’s text, although the citing sentence labels it an analysis of the paper’s data. No page numbers were supplied for these passages. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 62

  1. Abdel-Wahab O., Adli M., LaFave L.M., Gao J., Hricik T., Shih A.H., Pandey S., Patel J.P., Chung Y.R., Koche R., 2012 ASXL1 mutations promote myeloid transformation through loss of PRC2-mediated gene repression. Cancer Cell. 22: 180– 193. 10.1016/j.ccr.2012.06.032 22897849 PMC3422511 · DOI
  2. Abdel-Wahab O., Gao J., Adli M., Dey A., Trimarchi T., Chung Y.R., Kuscu C., Hricik T., Ndiaye-Lobry D., Lafave L.M., 2013 Deletion of Asxl1 results in myelodysplasia and severe developmental defects in vivo. J. Exp. Med. 210: 2641– 2659. 10.1084/jem.20131141 24218140 PMC3832937 · DOI
  3. Addya S., Keller M.A., Delgrosso K., Ponte C.M., Vadigepalli R., Gonye G.E., and Surrey S. 2004 Erythroid-induced commitment of K562 cells results in clusters of differentially expressed genes enriched for specific transcription regulatory elements. Physiol. Genomics. 19: 117– 130. 10.1152/physiolgenomics.00028.2004 15252187 · DOI
  4. Balasubramani A., Larjo A., Bassein J.A., Chang X., Hastie R.B., Togher S.M., Lähdesmäki H., and Rao A. 2015 Cancer-associated ASXL1 mutations may act as gain-of-function mutations of the ASXL1-BAP1 complex. Nat. Commun. 6: 7307 10.1038/ncomms8307 26095772 PMC4557297 · DOI
  5. Behrens K., Maul K., Tekin N., Kriebitzsch N., Indenbirken D., Prassolov V., Müller U., Serve H., Cammenga J., and Stocking C. 2017 RUNX1 cooperates with FLT3-ITD to induce leukemia. J. Exp. Med. 214: 737– 752. 28213513 PMC5339673
  6. Bejar R., Stevenson K., Abdel-Wahab O., Galili N., Nilsson B., Garcia-Manero G., Kantarjian H., Raza A., Levine R.L., Neuberg D., and Ebert B.L. 2011 Clinical effect of point mutations in myelodysplastic syndromes. N. Engl. J. Med. 364: 2496– 2506. 10.1056/NEJMoa1013343 21714648 PMC3159042 · DOI · Paper page
  7. Blank U., and Karlsson S. 2015 TGF-β signaling in the control of hematopoietic stem cells. Blood. 125: 3542– 3550. 10.1182/blood-2014-12-618090 25833962 · DOI
  8. Cai Q., Jeannet R., Hua W.K., Cook G.J., Zhang B., Qi J., Liu H., Li L., Chen C.C., Marcucci G., and Kuo Y.H. 2016 CBFβ-SMMHC creates aberrant megakaryocyte-erythroid progenitors prone to leukemia initiation in mice. Blood. 128: 1503– 1515. 10.1182/blood-2016-01-693119 27443289 PMC5025900 · DOI
  9. Cantù C., Ierardi R., Alborelli I., Fugazza C., Cassinelli L., Piconese S., Bosè F., Ottolenghi S., Ferrari G., and Ronchi A. 2011 Sox6 enhances erythroid differentiation in human erythroid progenitors. Blood. 117: 3669– 3679. 10.1182/blood-2010-04-282350 21263153 · DOI
  10. Chen K., Liu J., Heck S., Chasis J.A., An X., and Mohandas N. 2009 Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc. Natl. Acad. Sci. USA. 106: 17413– 17418. 10.1073/pnas.0909296106 19805084 PMC2762680 · DOI
  11. Chen T.C., Hou H.A., Chou W.C., Tang J.L., Kuo Y.Y., Chen C.Y., Tseng M.H., Huang C.F., Lai Y.J., Chiang Y.C., 2014 Dynamics of ASXL1 mutation and other associated genetic alterations during disease progression in patients with primary myelodysplastic syndrome. Blood Cancer J. 4: e177 10.1038/bcj.2013.74 24442206 PMC3913943 · DOI
  12. Cook G.J., and Pardee T.S. 2013 Animal models of leukemia: any closer to the real thing? Cancer Metastasis Rev. 32: 63– 76. 10.1007/s10555-012-9405-5 23081702 PMC3568447 · DOI
  13. de Boer J., Williams A., Skavdis G., Harker N., Coles M., Tolaini M., Norton T., Williams K., Roderick K., Potocnik A.J., and Kioussis D. 2003 Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 33: 314– 325. 10.1002/immu.200310005 12548562 · DOI · Paper page
  14. Deed R.W., Jasiok M., and Norton J.D. 1998 Lymphoid-specific expression of the Id3 gene in hematopoietic cells. Selective antagonism of E2A basic helix-loop-helix protein associated with Id3-induced differentiation of erythroleukemia cells. J. Biol. Chem. 273: 8278– 8286. 10.1074/jbc.273.14.8278 9525934 · DOI
  15. Deplus R., Delatte B., Schwinn M.K., Defrance M., Méndez J., Murphy N., Dawson M.A., Volkmar M., Putmans P., Calonne E., 2013 TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J. 32: 645– 655. 10.1038/emboj.2012.357 23353889 PMC3590984 · DOI
  16. Dey A., Seshasayee D., Noubade R., French D.M., Liu J., Chaurushiya M.S., Kirkpatrick D.S., Pham V.C., Lill J.R., Bakalarski C.E., 2012 Loss of the tumor suppressor BAP1 causes myeloid transformation. Science. 337: 1541– 1546. 10.1126/science.1221711 22878500 PMC5201002 · DOI
  17. Döhner H., Estey E., Grimwade D., Amadori S., Appelbaum F.R., Büchner T., Dombret H., Ebert B.L., Fenaux P., Larson R.A., 2017 Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 129: 424– 447. 10.1182/blood-2016-08-733196 27895058 PMC5291965 · DOI
  18. Genovese G., Kähler A.K., Handsaker R.E., Lindberg J., Rose S.A., Bakhoum S.F., Chambert K., Mick E., Neale B.M., Fromer M., 2014 Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N. Engl. J. Med. 371: 2477– 2487. 10.1056/NEJMoa1409405 25426838 PMC4290021 · DOI · Paper page
  19. Goyama S., Schibler J., Cunningham L., Zhang Y., Rao Y., Nishimoto N., Nakagawa M., Olsson A., Wunderlich M., Link K.A., 2013 Transcription factor RUNX1 promotes survival of acute myeloid leukemia cells. J. Clin. Invest. 123: 3876– 3888. 10.1172/JCI68557 23979164 PMC3754260 · DOI
  20. Harada Y., and Harada H. 2009 Molecular pathways mediating MDS/AML with focus on AML1/RUNX1 point mutations. J. Cell. Physiol. 220: 16– 20. 10.1002/jcp.21769 19334039 · DOI
  21. Hess J.L., Bittner C.B., Zeisig D.T., Bach C., Fuchs U., Borkhardt A., Frampton J., and Slany R.K. 2006 c-Myb is an essential downstream target for homeobox-mediated transformation of hematopoietic cells. Blood. 108: 297– 304. 10.1182/blood-2005-12-5014 16507773 PMC1895838 · DOI
  22. Ikeda K., Ueda T., Yamasaki N., Nakata Y., Sera Y., Nagamachi A., Miyama T., Kobayashi H., Takubo K., Kanai A., 2016 Maintenance of the functional integrity of mouse hematopoiesis by EED and promotion of leukemogenesis by EED haploinsufficiency. Sci. Rep. 6: 29454 10.1038/srep29454 27432459 PMC4949429 · DOI
  23. Inoue D., Kitaura J., Togami K., Nishimura K., Enomoto Y., Uchida T., Kagiyama Y., Kawabata K.C., Nakahara F., Izawa K., 2013 Myelodysplastic syndromes are induced by histone methylation–altering ASXL1 mutations. J. Clin. Invest. 123: 4627– 4640. 10.1172/JCI70739 24216483 PMC3809801 · DOI
  24. Inoue D., Kitaura J., Matsui H., Hou H.A., Chou W.C., Nagamachi A., Kawabata K.C., Togami K., Nagase R., Horikawa S., 2015 SETBP1 mutations drive leukemic transformation in ASXL1-mutated MDS. Leukemia. 29: 847– 857. 10.1038/leu.2014.301 25306901 PMC4501574 · DOI
  25. Inoue D., Matsumoto M., Nagase R., Saika M., Fujino T., Nakayama K.I., and Kitamura T. 2016 Truncation mutants of ASXL1 observed in myeloid malignancies are expressed at detectable protein levels. Exp. Hematol. 44: 172– 176. 26700326
  26. Inoue D., Fujino T., Sheridan P., Zhang Y.Z., Nagase R., Horikawa S., Li Z., Matsui H., Kanai A., Saika M., 2018 A novel ASXL1-OGT axis plays roles in H3K4 methylation and tumor suppression in myeloid malignancies. Leukemia. 10.1038/s41375-018-0083-3 29556021 · DOI
  27. Kamminga L.M., Bystrykh L.V., de Boer A., Houwer S., Douma J., Weersing E., Dontje B., and de Haan G. 2006 The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood. 107: 2170– 2179. 10.1182/blood-2005-09-3585 16293602 PMC1895717 · DOI · Paper page
  28. Kimura H., Hayashi-Takanaka Y., Goto Y., Takizawa N., and Nozaki N. 2008 The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Struct. Funct. 33: 61– 73. 10.1247/csf.07035 18227620 · DOI
  29. Krivtsov A.V., Feng Z., Lemieux M.E., Faber J., Vempati S., Sinha A.U., Xia X., Jesneck J., Bracken A.P., Silverman L.B., 2008 H3K79 methylation profiles define murine and human MLL-AF4 leukemias. Cancer Cell. 14: 355– 368. 10.1016/j.ccr.2008.10.001 18977325 PMC2591932 · DOI
  30. Liu J., Zhang J., Ginzburg Y., Li H., Xue F., De Franceschi L., Chasis J.A., Mohandas N., and An X. 2013 Quantitative analysis of murine terminal erythroid differentiation in vivo: novel method to study normal and disordered erythropoiesis. Blood. 121: e43– e49. 10.1182/blood-2012-09-456079 23287863 PMC3578961 · DOI
  31. Mayle A., Luo M., Jeong M., and Goodell M.A. 2013 Flow cytometry analysis of murine hematopoietic stem cells. Cytometry A. 83: 27– 37. 10.1002/cyto.a.22093 22736515 PMC3638885 · DOI
  32. Micol J.B., Pastore A., Inoue D., Duployez N., Kim E., Lee S.C., Durham B.H., Chung Y.R., Cho H., Zhang X.J., 2017 ASXL2 is essential for haematopoiesis and acts as a haploinsufficient tumour suppressor in leukemia. Nat. Commun. 8: 15429 10.1038/ncomms15429 28516957 PMC5454368 · DOI
  33. Milne T.A., Sinclair D.A., and Brock H.W. 1999 The Additional sex combs gene of Drosophila is required for activation and repression of homeotic loci, and interacts specifically with Polycomb and super sex combs. Mol. Gen. Genet. 261: 753– 761. 10.1007/s004380050018 10394912 · DOI
  34. Murphy A.J., Bijl N., Yvan-Charvet L., Welch C.B., Bhagwat N., Reheman A., Wang Y., Shaw J.A., Levine R.L., Ni H., 2013 Cholesterol efflux in megakaryocyte progenitors suppresses platelet production and thrombocytosis. Nat. Med. 19: 586– 594. 10.1038/nm.3150 23584088 PMC3683965 · DOI
  35. Ng S.Y., Yoshida T., Zhang J., and Georgopoulos K. 2009 Genome-wide lineage-specific transcriptional networks underscore Ikaros-dependent lymphoid priming in hematopoietic stem cells. Immunity. 30: 493– 507. 10.1016/j.immuni.2009.01.014 19345118 PMC3012962 · DOI
  36. Papaemmanuil E., Gerstung M., Malcovati L., Tauro S., Gundem G., Van Loo P., Yoon C.J., Ellis P., Wedge D.C., Pellagatti A., Chronic Myeloid Disorders Working Group of the International Cancer Genome Consortium 2013 Clinical and biological implications of driver mutations in myelodysplastic syndromes. Blood. 122: 3616– 3627, quiz:3699. 10.1182/blood-2013-08-518886 24030381 PMC3837510 · DOI · Paper page
  37. Paschka P., Schlenk R.F., Gaidzik V.I., Herzig J.K., Aulitzky T., Bullinger L., Späth D., Teleanu V., Kündgen A., Köhne C.H., 2015 ASXL1 mutations in younger adult patients with acute myeloid leukemia: a study by the German-Austrian Acute Myeloid Leukemia Study Group. Haematologica. 100: 324– 330. 10.3324/haematol.2014.114157 25596267 PMC4349270 · DOI
  38. Paulson R.F. 2014 Targeting a new regulator of erythropoiesis to alleviate anemia. Nat. Med. 20: 334– 335. 10.1038/nm.3524 24710373 · DOI
  39. Pietras E.M., Reynaud D., Kang Y.A., Carlin D., Calero-Nieto F.J., Leavitt A.D., Stuart J.M., Göttgens B., and Passegué E. 2015 Functionally Distinct Subsets of Lineage-Biased Multipotent Progenitors Control Blood Production in Normal and Regenerative Conditions. Cell Stem Cell. 17: 35– 46. 10.1016/j.stem.2015.05.003 26095048 PMC4542150 · DOI · Paper page
  40. Quesada V., Conde L., Villamor N., Ordóñez G.R., Jares P., Bassaganyas L., Ramsay A.J., Beà S., Pinyol M., Martínez-Trillos A., 2011 Exome sequencing identifies recurrent mutations of the splicing factor SF3B1 gene in chronic lymphocytic leukemia. Nat. Genet. 44: 47– 52. 10.1038/ng.1032 22158541 · DOI
  41. Riz I., Akimov S.S., Eaker S.S., Baxter K.K., Lee H.J., Mariño-Ramírez L., Landsman D., Hawley T.S., and Hawley R.G. 2007 TLX1/HOX11-induced hematopoietic differentiation blockade. Oncogene. 26: 4115– 4123. 10.1038/sj.onc.1210185 17213805 PMC1955382 · DOI
  42. Sanchez-Pulido L., Kong L., and Ponting C.P. 2012 A common ancestry for BAP1 and Uch37 regulators. Bioinformatics. 28: 1953– 1956. 10.1093/bioinformatics/bts319 22645167 · DOI
  43. Scheuermann J.C., de Ayala Alonso A.G., Oktaba K., Ly-Hartig N., McGinty R.K., Fraterman S., Wilm M., Muir T.W., and Müller J. 2010 Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature. 465: 243– 247. 10.1038/nature08966 20436459 PMC3182123 · DOI
  44. Schuhmacher M., Kohlhuber F., Hölzel M., Kaiser C., Burtscher H., Jarsch M., Bornkamm G.W., Laux G., Polack A., Weidle U.H., and Eick D. 2001 The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res. 29: 397– 406. 10.1093/nar/29.2.397 11139609 PMC29676 · DOI
  45. Shi H., Yamamoto S., Sheng M., Bai J., Zhang P., Chen R., Chen S., Shi L., Abdel-Wahab O., Xu M., 2016 ASXL1 plays an important role in erythropoiesis. Sci. Rep. 6: 28789 10.1038/srep28789 27352931 PMC4926121 · DOI
  46. Shields B.J., Jackson J.T., Metcalf D., Shi W., Huang Q., Garnham A.L., Glaser S.P., Beck D., Pimanda J.E., Bogue C.W., 2016 Acute myeloid leukemia requires Hhex to enable PRC2-mediated epigenetic repression of Cdkn2a. Genes Dev. 30: 78– 91. 10.1101/gad.268425.115 26728554 PMC4701980 · DOI
  47. Sowa M.E., Bennett E.J., Gygi S.P., and Harper J.W. 2009 Defining the human deubiquitinating enzyme interaction landscape. Cell. 138: 389– 403. 10.1016/j.cell.2009.04.042 19615732 PMC2716422 · DOI
  48. Suzuki M., Moriguchi T., Ohneda K., and Yamamoto M. 2009 Differential contribution of the Gata1 gene hematopoietic enhancer to erythroid differentiation. Mol. Cell. Biol. 29: 1163– 1175. 10.1128/MCB.01572-08 19103751 PMC2643832 · DOI
  49. Suzuki M., Kobayashi-Osaki M., Tsutsumi S., Pan X., Ohmori S., Takai J., Moriguchi T., Ohneda O., Ohneda K., Shimizu R., 2013 GATA factor switching from GATA2 to GATA1 contributes to erythroid differentiation. Genes Cells. 18: 921– 933. 23911012
  50. Thol F., Friesen I., Damm F., Yun H., Weissinger E.M., Krauter J., Wagner K., Chaturvedi A., Sharma A., Wichmann M., 2011 Prognostic significance of ASXL1 mutations in patients with myelodysplastic syndromes. J. Clin. Oncol. 29: 2499– 2506. 10.1200/JCO.2010.33.4938 21576631 · DOI
  51. Tyagi S., Chabes A.L., Wysocka J., and Herr W. 2007 E2F activation of S phase promoters via association with HCF-1 and the MLL family of histone H3K4 methyltransferases. Mol. Cell. 27: 107– 119. 10.1016/j.molcel.2007.05.030 17612494 · DOI
  52. Ueda T., Nakata Y., Nagamachi A., Yamasaki N., Kanai A., Sera Y., Sasaki M., Matsui H., Honda Z., Oda H., 2016 Propagation of trimethylated H3K27 regulated by polycomb protein EED is required for embryogenesis, hematopoietic maintenance, and tumor suppression. Proc. Natl. Acad. Sci. USA. 113: 10370– 10375. 10.1073/pnas.1600070113 27578866 PMC5027452 · DOI
  53. Vardiman J.W., Thiele J., Arber D.A., Brunning R.D., Borowitz M.J., Porwit A., Harris N.L., Le Beau M.M., Hellström-Lindberg E., Tefferi A., and Bloomfield C.D. 2009 The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 114: 937– 951. 10.1182/blood-2009-03-209262 19357394 · DOI
  54. Wang J., Li Z., He Y., Pan F., Chen S., Rhodes S., Nguyen L., Yuan J., Jiang L., Yang X., 2014 Loss of Asxl1 leads to myelodysplastic syndrome-like disease in mice. Blood. 123: 541– 553. 10.1182/blood-2013-05-500272 24255920 PMC3901067 · DOI
  55. Watanabe-Okochi N., Kitaura J., Ono R., Harada H., Harada Y., Komeno Y., Nakajima H., Nosaka T., Inaba T., and Kitamura T. 2008 AML1 mutations induced MDS and MDS/AML in a mouse BMT model. Blood. 111: 4297– 4308. 10.1182/blood-2007-01-068346 18192504 · DOI
  56. Wolff L., Koller R., Hu X., and Anver M.R. 2003 A Moloney murine leukemia virus-based retrovirus with 4070A long terminal repeat sequences induces a high incidence of myeloid as well as lymphoid neoplasms. J. Virol. 77: 4965– 4971. 10.1128/JVI.77.8.4965-4971.2003 12663802 PMC152129 · DOI
  57. Xie M., Lu C., Wang J., McLellan M.D., Johnson K.J., Wendl M.C., McMichael J.F., Schmidt H.K., Yellapantula V., Miller C.A., 2014 Age-related mutations associated with clonal hematopoietic expansion and malignancies. Nat. Med. 20: 1472– 1478. 10.1038/nm.3733 25326804 PMC4313872 · DOI · Paper page
  58. Yamasaki N., Miyazaki K., Nagamachi A., Koller R., Oda H., Miyazaki M., Sasaki T., Honda Z.I., Wolff L., Inaba T., and Honda H. 2010 Identification of Zfp521/ZNF521 as a cooperative gene for E2A-HLF to develop acute B-lineage leukemia. Oncogene. 29: 1963– 1975. 20062079
  59. Yokomizo T., Hasegawa K., Ishitobi H., Osato M., Ema M., Ito Y., Yamamoto M., and Takahashi S. 2008 Runx1 is involved in primitive erythropoiesis in the mouse. Blood. 111: 4075– 4080. 10.1182/blood-2007-05-091637 18250229 · DOI · Paper page
  60. Yokoyama A., Wang Z., Wysocka J., Sanyal M., Aufiero D.J., Kitabayashi I., Herr W., and Cleary M.L. 2004 Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24: 5639– 5649. 10.1128/MCB.24.13.5639-5649.2004 15199122 PMC480881 · DOI
  61. Zhao Q., Chang C., Gonzalez J.P., Alzahrani K., Button J.L., and Fraidenraich D. 2016 Combined Id1 and Id3 Deletion Leads to Severe Erythropoietic Disturbances. PLoS One. 11: e0154480 10.1371/journal.pone.0154480 27128622 PMC4851361 · DOI
  62. Zhou P., Wang Z., Yuan X., Zhou C., Liu L., Wan X., Zhang F., Ding X., Wang C., Xiong S., 2013 Mixed lineage leukemia 5 (MLL5) protein regulates cell cycle progression and E2F1-responsive gene expression via association with host cell factor-1 (HCF-1). J. Biol. Chem. 288: 17532– 17543. 10.1074/jbc.M112.439729 23629655 PMC3682552 · DOI

Cited by

Sorted by citations

Authors
Nagase, R., Inoue, D., Pastore, A., Fujino, T., Hou, H.-A., Yamasaki, N., Goyama, S., Saika, M., Kanai, A., Sera, Y., Horikawa, S., Ota, Y., Asada, S., Hayashi, Y., Kawabata, K. C., Takeda, R., Tien, H.-F., Honda, H., Abdel-Wahab, O., & Kitamura, T.
Affiliations
  • Institute of Medical Science, The University of Tokyo (JP)
  • Memorial Sloan Kettering Cancer Center (US)
  • National Taiwan University Hospital (TW)
  • Hiroshima University (JP)
  • The University of Tokyo (JP)
Corresponding author
  • Inoue, Daichi
  • Kitamura, Toshio
ORCID
Venue
Journal of Experimental Medicine
Publisher
Rockefeller University Press
Published
2018-04-11
Volume
215
Issue
6
Pages
1729-1747
ISSN
  • 0022-1007 (ISSN-L)
  • 1540-9538
DOI
10.1084/jem.20171151
PMC
PMC5987913
OpenAlex
W2797367925
Cited by
155
References
4
Citations by year
2026: 7 · 2025: 14 · 2024: 18 · 2023: 15 · 2022: 22 · 2021: 27 · 2020: 28 · 2019: 15 · 2018: 9
FWCI
14.16
Type
journal article
Language
en
Open access
Licence
Locations
  • The Journal of Experimental Medicine (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • Japan Society for the Promotion of Science (26893051, B 15H04855)
  • Leukemia and Lymphoma Society
  • US Department of Defense (W81XWH-12-1-0041)
  • Edward P. Evans Foundation
  • Taub Foundation
  • Starr Foundation (I8-A8-075, I9-A9-059)
  • Friends of Leukemia Research Fund
  • Tokyo Biochemical Research Foundation
  • Uehara Memorial Foundation
Topics
  • Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
  • Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords
ASXL1, clonal hematopoiesis of indeterminate potential, myeloid neoplasms, hematopoietic stem cells, leukemic transformation, H3K4me3, H2AK119ub, H3K27me3, myeloid skewing, anemia, thrombocytosis, dysplasia, RUNX1 mutation, insertional mutagenesis, conditional knock-in mice
MeSH terms
Adult, Animals, Base Sequence, Cell Transformation, Neoplastic, Hematopoiesis, Hematopoietic Stem Cells, Histones, Humans, Leukemia, Mutation, Myelodysplastic Syndromes, Phenotype, Protein Binding, Repressor Proteins, Transcription, Genetic, Leukemia, Myeloid, Acute, Genome, Human, Gene Expression Regulation, Leukemic, Mutagenesis, Hematopoietic Stem Cell Transplantation, Epigenesis, Genetic, Mice, Gene Knock-In Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review