BRPF1 is essential for development of fetal hematopoietic stem cells

Journal of Clinical Investigation

Volumn 126, Issue 9, 2016, Pages 3247-3262

  You, Linya ^a,b   Li, Lin ^a,b   Zou, Jinfeng ^c   Yan, Kezhi ^a,b   Belle, Jad ^b   Nijnik, Anastasia ^b   Wang, Edwin ^c   Yang, Xiang Jiao ^a,b,d  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BROMODOMAIN AND PHD FINGER CONTAINING PROTEIN 1; HISTONE H3; NUCLEAR PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; BRPF1 PROTEIN, MOUSE; CARRIER PROTEIN; CHROMATIN; HISTONE; HISTONE ACETYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; APLASTIC ANEMIA; APOPTOSIS; ARTICLE; BLOOD CELL; BONE MARROW DEPRESSION; CELL AGING; CELL MATURATION; CHROMATIN; FETUS; FETUS LIVER; GENE DELETION; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HISTONE ACETYLATION; HOMEOSTASIS; LETHALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CYTOLOGY; EMBRYOLOGY; FEMALE; GENETIC EPIGENESIS; GENETICS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; LIVER; MALE; METABOLISM; PHYSIOLOGY; PROTEIN DOMAIN; SPLEEN; THYMUS;

ANIMALS; APOPTOSIS; BONE MARROW CELLS; CARRIER PROTEINS; CELL AGING; CHROMATIN; EPIGENESIS, GENETIC; FEMALE; GENE DELETION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HISTONE ACETYLTRANSFERASES; HISTONES; HOMEOSTASIS; LIVER; MALE; MICE; MICE, INBRED C57BL; PROTEIN DOMAINS; REACTIVE OXYGEN SPECIES; SPLEEN; THYMUS GLAND;

EID: 84987849615     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI80711     Document Type: Article

References (107)

1. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008;132(4):631-644
2. Doulatov S, Notta F, Laurenti E, Dick JE. Hematopoiesis: a human perspective. Cell Stem Cell. 2012;10(2):120-136
3. Copley MR, Beer PA, Eaves CJ. Hematopoietic stem cell heterogeneity takes center stage. Cell Stem Cell. 2012;10(6):690-697
4. Morrison SJ, Scadden DT. The bone marrow niche for haematopoietic stem cells. Nature. 2014;505(7483):327-334
5. Dzierzak E, Speck NA. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol. 2008;9(2):129-136
6. Medvinsky A, Rybtsov S, Taoudi S. Embryonic origin of the adult hematopoietic system: advances and questions. Development. 2011;138(6):1017-1031
7. Rossi DJ, Jamieson CH, Weissman IL. Stems cells and the pathways to aging and cancer. Cell. 2008;132(4):681-696
8. Biffi A, et al. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science. 2013;341(6148):1233158
9. Aiuti A, et al. Lentiviral hematopoietic stem cell gene therapy in patients with Wiskott-Aldrich syndrome. Science. 2013;341(6148):1233151
10. Naldini L. Ex vivo gene transfer and correction for cell-based therapies. Nat Rev Genet. 2011;12(5):301-315
11. Hütter G, et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med. 2009;360(7):692-698
12. Appel SH, et al. Hematopoietic stem cell transplantation in patients with sporadic amyotrophic lateral sclerosis. Neurology. 2008;71(17):1326-1334
13. Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med. 2006;354(17):1813-1826
14. McKinney-Freeman S, et al. The transcriptional landscape of hematopoietic stem cell ontogeny. Cell Stem Cell. 2012;11(5):701-714
15. Novershtern N, et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell. 2011;144(2):296-309
16. Rossi L, et al. Less is more: unveiling the functional core of hematopoietic stem cells through knockout mice. Cell Stem Cell. 2012;11(3):302-317
17. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128(4):707-719
18. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693-705
19. Ronan JL, Wu W, Crabtree GR. From neural development to cognition: unexpected roles for chromatin. Nat Rev Genet. 2013;14(5):347-359
20. Bonasio R, Tu S, Reinberg D. Molecular signals of epigenetic states. Science. 2010;330(6004):612-616
21. Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications. Annu Rev Biochem. 2011;80:473-499
22. Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature. 2013;502(7472):472-479
23. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol. 2007;14(11):1025-1040
24. Latham JA, Dent SY. Cross-regulation of histone modifications. Nat Struct Mol Biol. 2007;14(11):1017-1024
25. Musselman CA, Lalonde ME, Côté J, Kutateladze TG. Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol. 2012;19(12):1218-1227
26. Doyon Y, et al. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell. 2006;21(1):51-64
27. Ullah M, et al. Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes. Mol Cell Biol. 2008;28(22):6828-6843
28. Lalonde ME, et al. Exchange of associated factors directs a switch in HBO1 acetyltransferase histone tail specificity. Genes Dev. 2013;27(18):2009-2024
29. Qin S, et al. Recognition of unmodified histone H3 by the first PHD finger of bromodomain-PHD finger protein 2 provides insights into the regulation of histone acetyltransferases monocytic leukemic zinc-finger protein (MOZ) and MOZ-related factor (MORF). J Biol Chem. 2011;286(42):36944-36955
30. Klein BJ, et al. Bivalent interaction of the PZP domain of BRPF1 with the nucleosome impacts chromatin dynamics and acetylation. Nucleic Acids Res. 2016;44(1):472-484
31. Poplawski A, et al. Molecular insights into the recognition of N-terminal histone modifications by the BRPF1 bromodomain. J Mol Biol. 2014;426(8):1661-1676
32. Vezzoli A, et al. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol. 2010;17(5):617-619
33. Wu H, et al. Structural and histone binding ability characterizations of human PWWP domains. PLoS ONE. 2011;6(6):e18919
34. You L, Chen L, Penney J, Miao D, Yang XJ. Expression atlas of the multivalent epigenetic regulator Brpf1 and its requirement for survival of mouse embryos. Epigenetics. 2014;9(6):860-872
35. You L, et al. The lysine acetyltransferase activator Brpf1 governs dentate gyrus development through neural stem cells and progenitors. PLoS Genet. 2015;11(3):e1005034
36. You L, et al. The chromatin regulator Brpf1 regulates embryo development and cell proliferation. J Biol Chem. 2015;290(18):11349-11364
37. You L, et al. Deficiency of the chromatin regulator BRPF1 causes abnormal brain development. J Biol Chem. 2015;290(11):7114-7129
38. Borrow J, et al. The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nat Genet. 1996;14(1):33-41
39. Deguchi K, et al. MOZ-TIF2-induced acute myeloid leukemia requires the MOZ nucleosome binding motif and TIF2-mediated recruitment of CBP. Cancer Cell. 2003;3(3):259-271
40. Huntly BJ, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6(6):587-596
41. Chinen Y, et al. The leucine twenty homeobox (LEUTX) gene, which lacks a histone acetyltransferase domain, is fused to KAT6A in therapy-related acute myeloid leukemia with t(8;19)(p11;q13). Genes Chromosomes Cancer. 2014;53(4):299-308
42. Yang XJ, Ullah M. MOZ and MORF, two large MYSTic HATs in normal and cancer stem cells. Oncogene. 2007;26(37):5408-5419
43. Perfetto SP, Chattopadhyay PK, Roederer M. Seventeen-colour flow cytometry: unravelling the immune system. Nat Rev Immunol. 2004;4(8):648-655
44. Mayle A, Luo M, Jeong M, Goodell MA. Flow cytometry analysis of murine hematopoietic stem cells. Cytometry A. 2013;83(1):27-37
45. Oguro H, Ding L, Morrison SJ. SLAM family markers resolve functionally distinct subpopulations of hematopoietic stem cells and multipotent progenitors. Cell Stem Cell. 2013;13(1):102-116
46. de Boer J, et al. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur J Immunol. 2003;33(2):314-325
47. Vosshenrich CA, Cumano A, Müller W, Di Santo JP, Vieira P. Thymic stromal-derived lymphopoietin distinguishes fetal from adult B cell development. Nat Immunol. 2003;4(8):773-779
48. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109-1121
49. Kataoka K, et al. Evi1 is essential for hematopoietic stem cell self-renewal, and its expression marks hematopoietic cells with long-term multilineage repopulating activity. J Exp Med. 2011;208(12):2403-2416
50. Zhang Y, et al. PR-domain-containing Mds1-Evi1 is critical for long-term hematopoietic stem cell function. Blood. 2011;118(14):3853-3861
51. Kim I, Saunders TL, Morrison SJ. Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell. 2007;130(3):470-483
52. Hock H, et al. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature. 2004;431(7011):1002-1007
53. Zeng H, Yücel R, Kosan C, Klein-Hitpass L, Möröy T. Transcription factor Gfi1 regulates selfrenewal and engraftment of hematopoietic stem cells. EMBO J. 2004;23(20):4116-4125
54. Thorsteinsdottir U, et al. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood. 2002;99(1):121-129
55. Shen WF, Rozenfeld S, Kwong A, Köm ves LG, Lawrence HJ, Largman C. HOXA9 forms triple complexes with PBX2 and MEIS1 in myeloid cells. Mol Cell Biol. 1999;19(4):3051-3061
56. LaRonde-LeBlanc NA, Wolberger C. Structure of HoxA9 and Pbx1 bound to DNA: Hox hexapeptide and DNA recognition anterior to posterior. Genes Dev. 2003;17(16):2060-2072
57. Lawrence HJ, et al. Loss of expression of the Hoxa-9 homeobox gene impairs the proliferation and repopulating ability of hematopoietic stem cells. Blood. 2005;106(12):3988-3994
58. So CW, Karsunky H, Wong P, Weissman IL, Cleary ML. Leukemic transformation of hematopoietic progenitors by MLL-GAS7 in the absence of Hoxa7 or Hoxa9. Blood. 2004;103(8):3192-3199
59. Komorowska M, Mikkola HKA, Larsson J, Magnusson M. Hepatic leukemia factor is an important regulator of hematopoietic stem cell activity and identity. Blood. 2013;122:2410
60. Artinger EL, et al. An MLL-dependent network sustains hematopoiesis. Proc Natl Acad Sci U S A. 2013;110(29):12000-12005
61. Lalonde ME, Cheng X, Côté J. Histone target selection within chromatin: an exemplary case of teamwork. Genes Dev. 2014;28(10):1029-1041
62. Chen S, et al. The PZP domain of AF10 senses unmodified H3K27 to regulate DOT1Lmediated methylation of H3K79. Mol Cell. 2015;60(2):319-327
63. Zhou T, Chung YH, Chen J, Chen Y. Site-specific identification of lysine acetylation stoichiometries in mammalian cells. J Proteome Res. 2016;15(3):1103-1113
64. Tsai WW, et al. TRIM24 links a non-canonical histone signature to breast cancer. Nature. 2010;468(7326):927-932
65. Simó-Riudalbas L, et al. KAT6B is a tumor suppressor histone H3 lysine 23 acetyltransferase undergoing genomic loss in small cell lung cancer. Cancer Res. 2015;75(18):3936-3945
66. Huang F, et al. Histone acetyltransferase Enok regulates oocyte polarization by promoting expression of the actin nucleation factor spire. Genes Dev. 2014;28(24):2750-2763
67. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature. 2009;457(7231):887-891
68. Filippakopoulos P, Knapp S. Targeting bromodomains: epigenetic readers of lysine acetylation. Nat Rev Drug Discov. 2014;13(5):337-356
69. Challen GA, et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet. 2012;44(1):23-31
70. Moran-Crusio K, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell. 2011;20(1):11-24
71. Xie H, et al. Polycomb repressive complex 2 regulates normal hematopoietic stem cell function in a developmental-stage-specific manner. Cell Stem Cell. 2014;14(1):68-80
72. Hidalgo I, et al. Ezh1 is required for hematopoietic stem cell maintenance and prevents senescence-like cell cycle arrest. Cell Stem Cell. 2012;11(5):649-662
73. Jude CD, Climer L, Xu D, Artinger E, Fisher JK, Ernst P. Unique and independent roles for MLL in adult hematopoietic stem cells and progenitors. Cell Stem Cell. 2007;1(3):324-337
74. McMahon KA, et al. Mll has a critical role in fetal and adult hematopoietic stem cell self-renewal. Cell Stem Cell. 2007;1(3):338-345
75. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423(6937):255-260
76. Park IK, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003;423(6937):302-305
77. Katsumoto T, et al. MOZ is essential for maintenance of hematopoietic stem cells. Genes Dev. 2006;20(10):1321-1330
78. Thomas T, et al. Monocytic leukemia zinc finger protein is essential for the development of longterm reconstituting hematopoietic stem cells. Genes Dev. 2006;20(9):1175-1186
79. Summers AR, et al. HDAC3 is essential for DNA replication in hematopoietic progenitor cells. J Clin Invest. 2013;123(7):3112-3123
80. Cullen SM, Mayle A, Rossi L, Goodell MA. Hematopoietic stem cell development: an epigenetic journey. Curr Top Dev Biol. 2014;107:39-75
81. Mostoslavsky R, et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell. 2006;124(2):315-329
82. Ceccaldi R, et al. Bone marrow failure in Fanconi anemia is triggered by an exacerbated p53/p21 DNA damage response that impairs hematopoietic stem and progenitor cells. Cell Stem Cell. 2012;11(1):36-49
83. Abbas HA, et al. Mdm2 is required for survival of hematopoietic stem cells/progenitors via dampening of ROS-induced p53 activity. Cell Stem Cell. 2010;7(5):606-617
84. Simeonova I, et al. Mutant mice lacking the p53 C-terminal domain model telomere syndromes. Cell Rep. 2013;3(6):2046-2058
85. Hockemeyer D, Palm W, Wang RC, Couto SS, de Lange T. Engineered telomere degradation models dyskeratosis congenita. Genes Dev. 2008;22(13):1773-1785
86. Wang Y, Shen MF, Chang S. Essential roles for Pot1b in HSC self-renewal and survival. Blood. 2011;118(23):6068-6077
87. O'Meara MM, Zhang F, Hobert O. Maintenance of neuronal laterality in Caenorhabditis elegans through MYST histone acetyltransferase complex components LSY-12, LSY-13 and LIN-49. Genetics. 2010;186(4):1497-1502
88. Laue K, et al. The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development. 2008;135(11):1935-1946
89. Mishima Y, et al. The Hbo1-Brd1/Brpf2 complex is responsible for global acetylation of H3K14 and required for fetal liver erythropoiesis. Blood. 2011;118(9):2443-2453
90. Yan K, et al. The chromatin regulator BRPF3 preferentially activates the HBO1 acetyltransferase but is dispensable for mouse development and survival. J Biol Chem. 2016;291(6):2647-2663
91. Feng Y, et al. BRPF3-HBO1 regulates replication origin activation and histone H3K14 acetylation. EMBO J. 2016;35(2):176-192
92. Perez-Campo FM, Borrow J, Kouskoff V, Lacaud G. The histone acetyl transferase activity of monocytic leukemia zinc finger is critical for the proliferation of hematopoietic precursors. Blood. 2009;113(20):4866-4874
93. Kueh AJ, Dixon MP, Voss AK, Thomas T. HBO1 is required for H3K14 acetylation and normal transcriptional activity during embryonic development. Mol Cell Biol. 2011;31(4):845-860
94. Thomas T, Voss AK, Chowdhury K, Gruss P. Querkopf, a MYST family histone acetyltransferase, is required for normal cerebral cortex development. Development. 2000;127(12):2537-2548
95. Shima H, et al. Bromodomain-PHD finger protein 1 is critical for leukemogenesis associated with MOZ-TIF2 fusion. Int J Hematol. 2014;99(1):21-31
96. Moore SD, et al. Uterine leiomyomata with t(10;17) disrupt the histone acetyltransferase MORF. Cancer Res. 2004;64(16):5570-5577
97. Grasso CS, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature. 2012;487(7406):239-243
98. Lynch H, et al. Can unknown predisposition in familial breast cancer be family-specific? Breast J. 2013;19(5):520-528
99. Zack TI, et al. Pan-cancer patterns of somatic copy number alteration. Nat Genet. 2013;45(10):1134-1140
100. Kraft M, et al. Disruption of the histone acetyltransferase MYST4 leads to a Noonan syndromelike phenotype and hyperactivated MAPK signaling in humans and mice. J Clin Invest. 2011;121(9):3479-3491
101. Clayton-Smith J, et al. Whole-exome-sequencing identifies mutations in histone acetyltransferase gene KAT6B in individuals with the Say-Barber-Biesecker variant of Ohdo syndrome. Am J Hum Genet. 2011;89(5):675-681
102. Simpson MA, et al. De novo mutations of the gene encoding the histone acetyltransferase KAT6B cause Genitopatellar syndrome. Am J Hum Genet. 2012;90(2):290-294
103. Campeau PM, et al. Mutations in KAT6B, encoding a histone acetyltransferase, cause Genitopatellar syndrome. Am J Hum Genet. 2012;90(2):282-289
104. Yu HC, Geiger EA, Medne L, Zackai EH, Shaikh TH. An individual with blepharophimosis-ptosisepicanthus inversus syndrome (BPES) and additional features expands the phenotype associated with mutations in KAT6B. Am J Med Genet A. 2014;164(4):950-957
105. Arboleda VA, et al. De novo nonsense mutations in KAT6A, a lysine acetyl-transferase gene, cause a syndrome including microcephaly and global developmental delay. Am J Hum Genet. 2015;96(3):498-506
106. Tham E, et al. Dominant mutations in KAT6A cause intellectual disability with recognizable syndromic features. Am J Hum Genet. 2015;96(3):507-513
107. Yang XJ. MOZ and MORF acetyltransferases: Molecular interaction, animal development and human disease. Biochim Biophys Acta. 2015;1853(8):1818-1826