RUNX1 regulates the CD34 gene in haematopoietic stem cells by mediating interactions with a distal regulatory element

EMBO Journal

Volumn 30, Issue 19, 2011, Pages 4059-4070

  Levantini, Elena ^a,b   Lee, Sanghoon ^c   Radomska, Hanna S ^a,b,k   Hetherington, Christopher J ^a,b   Alberich Jorda, Meritxell ^a,b   Amabile, Giovanni ^a,b   Zhang, Pu ^a,b   Gonzalez, David A ^a,b   Zhang, Junyan ^a,b   Basseres, Daniela S ^d   Wilson, Nicola K ^e   Koschmieder, Steffen ^f   Huang, Gang ^g   Zhang, Dong Er ^h   Ebralidze, Alexander K ^a,b   Bonifer, Constanze ⁱ   Okuno, Yutaka ^j   Gottgens, Bertie ^e   Tenen, Daniel G ^b,c,l  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f UNIVERSITY OF MÜNSTER   (Germany)

^g CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^j KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

^k OHIO STATE UNIVERSITY   (United States)

^l Center for Life Science   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; TRANSCRIPTION FACTOR RUNX1;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CHROMOSOME; CONTROLLED STUDY; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; HEMATOPOIETIC STEM CELL; HUMAN; IN VIVO STUDY; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD34; BONE MARROW TRANSPLANTATION; CHROMATIN; CORE BINDING FACTOR ALPHA 2 SUBUNIT; FETAL BLOOD; GENE EXPRESSION REGULATION; GENOTYPE; HEMATOPOIETIC STEM CELLS; HL-60 CELLS; HUMANS; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; REGULATORY SEQUENCES, NUCLEIC ACID;

MUS; MUS MUSCULUS;

EID: 80053597496     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.285     Document Type: Article

References (74)

1. Barnett DH, Sheng S, Charn TH, Waheed A, Sly WS, Lin CY, Liu ET, Katzenellenbogen BS (2008) Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res 68: 3505-3515
2. Berezney R, Mortillaro M, Ma H, Meng C, Samarabandu J, Wei X, Somanathan S, Liou WS, Pan SJ, Cheng PC (1996) Connecting nuclear architecture and genomic function. J Cell Biochem 62: 223-226 (Pubitemid 26287206)
3. Boney-Montoya J, Ziegler YS, Curtis CD, Montoya JA, Nardulli AM (2010) Long-range transcriptional control of progesterone receptor gene expression. Mol Endocrinol 24: 346-358
4. Brown RC, Pattison S, van Ree J, Coghill E, Perkins A, Jane SM, Cunningham JM (2002) Distinct domains of erythroid Kruppel-like factor modulate chromatin remodeling and transactivation at the endogenous beta-globin gene promoter. Mol Cell Biol 22: 161-170 (Pubitemid 33144265)
5. 0 enhancer direct hematopoietic expression in tissue culture. Blood 80: 3051-3059 (Pubitemid 23004508)
6. Cai Z, de Bruijn M, Ma X, Dortland B, Luteijn T, Downing RJ, Dzierzak E (2000) Haploinsufficiency of AML1 affects the temporal and spatial generation of hematopoietic stem cells in the mouse embryo. Immunity 13: 423-431
7. Carter D, Chakalova L, Osborne CS, Dai YF, Fraser P (2002) Long-range chromatin regulatory interactions in vivo. Nat Genet 32: 623-626 (Pubitemid 35435174)
8. 0HS5 of the human beta-globin locus control region is dispensable for the formation of the beta-globin active chromatin hub. PLoS One 3: e2134.
9. Chavanas S, Adoue V, Mechin MC, Ying S, Dong S, Duplan H, Charveron M, Takahara H, Serre G, Simon M (2008) Long-range enhancer associated with chromatin looping allows AP-1 regulation of the peptidylarginine deiminase 3 gene in differentiated keratinocyte. PLoS One 3: e3408.
10. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA (2009) Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457: 887-891.
11. Chen X, Reitman M, Bieker JJ (1998) Chromatin structure and transcriptional control elements of the erythroid Kruppel-like factor (EKLF) gene. J Biol Chem 273: 25031-25040 (Pubitemid 28443259)
12. Collins A, Hewitt SL, Chaumeil J, Sellars M, Micsinai M, Allinne J, Parisi F, Nora EP, Bolland DJ, Corcoran AE, Kluger Y, Bosselut R, Ellmeier W, Chong MM, Littman DR, Skok JA (2011) RUNX transcription factor-mediated association of Cd4 and Cd8 enables coordinate gene regulation. Immunity 34: 303-314
13. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645 (Pubitemid 30412767)
14. Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295: 1306-1311 (Pubitemid 34157624)
15. Deshane J, Kim J, Bolisetty S, Hock TD, Hill-Kapturczak N, Agarwal A (2010) Sp1 regulates chromatin looping between an intronic enhancer and distal promoter of the human heme oxygenase-1 gene in renal cells. J Biol Chem 285: 16476-16486
16. Dunbar CE, Cottler-Fox M, O'Shaughnessy JA, Doren S, Carter C, Berenson R, Brown S, Moen RC, Greenblatt J, Stewart FM, Leitman SF, Wilson WH, Cowan K, Young NS, Nienhuis AW (1995) Retrovirally marked CD34-enriched peripheral blood and bone marrow cells contribute to long-term engraftment after autologous transplantation. Blood 85: 3048-3057
17. Ebralidze AK, Guibal FC, Steidl U, Zhang P, Lee S, Bartholdy B, Jorda MA, Petkova V, Rosenbauer F, Huang G, Dayaram T, Klupp J, O'Brien KB, Will B, Hoogenkamp M, Borden KL, Bonifer C, Tenen DG (2008) PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element. Genes Dev 22: 2085-2092
18. Galy A, Travis M, Cen D, Chen B (1995) Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity 3: 459-473
19. Gavrilov AA, Razin SV (2008) Spatial configuration of the chicken alpha-globin gene domain: immature and active chromatin hubs. Nucleic Acids Res 36: 4629-4640
20. Gottgens B, Nastos A, Kinston S, Piltz S, Delabesse EC, Stanley M, Sanchez MJ, Ciau-Uitz A, Patient R, Green AR (2002) Establishing the transcriptional programme for blood: the SCL stem cell enhancer is regulated by a multiprotein complex containing Ets and GATA factors. Embo J 21: 3039-3050 (Pubitemid 34670388)
21. Growney JD, Shigematsu H, Li Z, Lee BH, Adelsperger J, Rowan R, Curley DP, Kutok JL, Akashi K, Williams IR, Speck NA, Gilliland DG (2005) Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. Blood 106: 494-504 (Pubitemid 40981243)
22. Hagege H, Klous P, Braem C, Splinter E, Dekker J, Cathala G, de Laat W, Forne T (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2: 1722-1733
23. Hoogenkamp M, Lichtinger M, Krysinska H, Lancrin C, Clarke D, Williamson A, Mazzarella L, Ingram R, Jorgensen H, Fisher A, Tenen DG, Kouskoff V, Lacaud G, Bonifer C (2009) Early chro-matin unfolding by RUNX1: a molecular explanation for differential requirements during specification versus maintenance of the hematopoietic gene expression program. Blood 114: 299-309
24. Ichikawa M, Asai T, Chiba S, Kurokawa M, Ogawa S (2004a) Runx1/AML-1 ranks as a master regulator of adult hematopoi-esis. Cell Cycle 3: 722-724 (Pubitemid 40187898)
25. Ichikawa M, Asai T, Saito T, Seo S, Yamazaki I, Yamagata T, Mitani K, Chiba S, Ogawa S, Kurokawa M, Hirai H (2004b) AML-1 is required for megakaryocytic maturation and lympho-cytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat Med 10: 299-304 (Pubitemid 38667622)
26. Ichikawa M, Goyama S, Asai T, Kawazu M, Nakagawa M, Takeshita M, Chiba S, Ogawa S, Kurokawa M (2008) AML1/Runx1 negatively regulates quiescent hematopoietic stem cells in adult hematopoiesis. J Immunol 180: 4402-4408
27. Jackson DA (1997) Chromatin domains and nuclear compartments: establishing sites of gene expression in eukaryotic nuclei. Mol Biol Rep 24: 209-220 (Pubitemid 27358374)
28. Jackson DA, Hassan AB, Errington RJ, Cook PR (1993) Visualization of focal sites of transcription within human nuclei. EMBO J 12: 1059-1065 (Pubitemid 23095855)
29. Jacob B, Osato M (2009) Stem cell exhaustion and leukemogenesis. J Cell Biochem 107: 393-399
30. 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)
31. Kim SI, Bultman SJ, Jing H, Blobel GA, Bresnick EH (2007) Dissecting molecular steps in chromatin domain activation during hematopoietic differentiation. Mol Cell Biol 27: 4551-4565 (Pubitemid 46906576)
32. Kim SI, Bultman SJ, Kiefer CM, Dean A, Bresnick EH (2009) BRG1 requirement for long-range interaction of a locus control region with a downstream promoter. Proc Natl Acad Sci USA 106: 2259-2264
33. Krause DS, Fackler MJ, Civin CI, May WS (1996) CD34: structure, biology, and clinical utility. Blood 87: 1-13 (Pubitemid 26018389)
34. Kuhn R, Schwenk F, Aguet M, Rajewsky K (1995) Inducible gene targeting in mice. Science 269: 1427-1429
35. Li X, Vradii D, Gutierrez S, Lian JB, van Wijnen AJ, Stein JL, Stein GS, Javed A (2005) Subnuclear targeting of Runx1 is required for synergistic activation of the myeloid specific M-CSF receptor promoter by PU.1. J Cell Biochem 96: 795-809 (Pubitemid 41567550)
36. Ling JQ, Li T, Hu JF, Vu TH, Chen HL, Qiu XW, Cherry AM, Hoffman AR (2006) CTCF mediates interchromosomal colo-calization between Igf2/H19 and Wsb1/Nf1. Science 312: 269-272
37. Link H, Arseniev L, Bahre O, Kadar JG, Diedrich H, Poliwoda H (1996) Transplantation of allogeneic CD34+ blood cells. Blood 87: 4903-4909 (Pubitemid 26162395)
38. Liu Z, Ma Z, Terada LS, Garrard WT (2009) Divergent roles of RelA and c-Rel in establishing chromosomal loops upon activation of the Igkappa gene. J Immunol 183: 3819-3830
39. Marenduzzo D, Faro-Trindade I, Cook PR (2007) What are the molecular ties that maintain genomic loops? Trends Genet 23: 126-133
40. Melotti P, Calabretta B (1994) Ets-2 and c-Myb act independently in regulating expression of the hematopoietic stem cell antigen CD34. J Biol Chem 269: 25303-25309 (Pubitemid 24336208)
41. Michallet M, Philip T, Philip I, Godinot H, Sebban C, Salles G, Thiebaut A, Biron P, Lopez F, Mazars P, Roubi N, Leemhuis T, Hanania E, Reading C, Fine G, Atkinson K, Juttner C, Coiffier B, Fiere D, Archimbaud E (2000) Transplantation with selected autologous peripheral blood CD34+ Thy1+ hematopoietic stem cells (HSCs) in multiple myeloma: impact of HSC dose on engraftment, safety, and immune reconstitution. Exp Hematol 28: 858-870 (Pubitemid 30411992)
42. Morris JF, Rauscher III FJ, Davis B, Klemsz M, Xu D, Tenen D, Hromas R (1995) The myeloid zinc finger gene, MZF-1, regulates the CD34 promoter in vitro. Blood 86: 3640-3647
43. Okada H, Watanabe T, Niki M, Takano H, Chiba N, Yanai N, Tani K, Hibino H, Asano S, Mucenski ML, Ito Y, Noda T, Satake M (1998) AML1(-/-) embryos do not express certain hematopoiesis-re-lated gene transcripts including those of the PU.1 gene. Oncogene 17: 2287-2293 (Pubitemid 28515381)
44. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR (1996) AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoi-esis. Cell 84: 321-330 (Pubitemid 26042836)
45. Okuno Y, Huettner CS, Radomska HS, Petkova V, Iwasaki H, Akashi K, Tenen DG (2002a) Distal elements are critical for human CD34 expression in vivo. Blood 100: 4420-4426 (Pubitemid 35429680)
46. Okuno Y, Iwasaki H, Huettner CS, Radomska HS, Gonzalez DA, Tenen DG, Akashi K (2002b) Differential regulation of the human and murine CD34 genes in hematopoietic stem cells. Proc Natl Acad Sci USA 99: 6246-6251 (Pubitemid 34493297)
47. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P (2004) Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36: 1065-1071 (Pubitemid 41184467)
48. Patrinos GP, de Krom M, de Boer E, Langeveld A, Imam AM, Strouboulis J, de Laat W, Grosveld FG (2004) Multiple interactions between regulatory regions are required to stabilize an active chromatin hub. Genes Dev 18: 1495-1509 (Pubitemid 38780634)
49. Perrotti D, Melotti P, Skorski T, Casella I, Peschle C, Calabretta B (1995) Overexpression of the zinc finger protein MZF1 inhibits hematopoietic development from embryonic stem cells: correlation with negative regulation of CD34 and c-myb promoter activity. Mol Cell Biol 15: 6075-6087
50. Pilon AM, Nilson DG, Zhou D, Sangerman J, Townes TM, Bodine DM, Gallagher PG (2006) Alterations in expression and chromatin configuration of the alpha hemoglobin-stabilizing protein gene in erythroid Kruppel-like factor-deficient mice. Mol Cell Biol 26: 4368-4377 (Pubitemid 43788035)
51. Pimanda JE, Ottersbach K, Knezevic K, Kinston S, Chan WY, Wilson NK, Landry JR, Wood AD, Kolb-Kokocinski A, Green AR, Tannahill D, Lacaud G, Kouskoff V, Gottgens B (2007) Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc Natl Acad Sci USA 104: 17692-17697 (Pubitemid 350210896)
52. Putz G, Rosner A, Nuesslein I, Schmitz N, Buchholz F (2006) AML1 deletion in adult mice causes splenomegaly and lymphomas. Oncogene 25: 929-939 (Pubitemid 43237711)
53. Radomska HS, Gonzalez DA, Okuno Y, Iwasaki H, Nagy A, Akashi K, Tenen DG, Huettner CS (2002) Transgenic targeting with regulatory elements of the human CD34 gene. Blood 100: 4410-4419 (Pubitemid 35429679)
54. Radomska HS, Satterthwaite AB, Burn TC, Oliff IA, Huettner CS, Tenen DG (1998) Multiple control elements are required for expression of the human CD34 gene. Gene 222: 305-318 (Pubitemid 29003126)
55. Radomska HS, Satterthwaite AB, Taranenko N, Narravula S, Krause DS, Tenen DG (1999) A nuclear factor Y (NFY) site positively regulates the human CD34 stem cell gene. Blood 94: 3772-3780
56. Rathke C, Baarends WM, Jayaramaiah-Raja S, Bartkuhn M, Renkawitz R, Renkawitz-Pohl R (2007) Transition from a nucleo-some-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila. J Cell Sci 120: 1689-1700 (Pubitemid 46831799)
57. Roth TL, Sweatt JD (2009) Regulation of chromatin structure in memory formation. Curr Opin Neurobiol 19: 336-342
58. Sato T, Laver JH, Ogawa M (1999) Reversible expression of CD34 by murine hematopoietic stem cells. Blood 94: 2548-2554 (Pubitemid 29477281)
59. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, Eskiw CH, Luo Y, Wei CL, Ruan Y, Bieker JJ, Fraser P (2010) Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42: 53-61
60. Stein GS, van Wijnen AJ, Stein JL, Lian JB, Javed A, McNeil S, Pockwinse SM (1999) Insight into regulatory factor targeting to transcriptionally active subnuclear sites. Exp Cell Res 253: 110-116
61. Stein GS, van Wijnen AJ, Stein JL, Lian JB, Montecino M, Choi J, Zaidi K, Javed A (2000a) Intranuclear trafficking of transcription factors: implications for biological control. J Cell Sci 113(Part 14): 2527-2533 (Pubitemid 30599408)
62. Stein GS, van Wijnen AJ, Stein JL, Lian JB, Montecino M, Zaidi K, Javed A (2000b) Subnuclear organization and trafficking of regulatory proteins: implications for biological control and cancer. J Cell Biochem Suppl 79(Suppl 35): 84-92
63. Stella CC, Cazzola M, De Fabritiis P, De Vincentiis A, Gianni AM, Lanza F, Lauria F, Lemoli RM, Tarella C, Zanon P, Tura S (1995) CD34-positive cells: biology and clinical relevance. Haematologica 80: 367-387
64. Theo Sijtse Palstra RJ (2009) Close encounters of the 3C kind: long-range chromatin interactions and transcriptional regulation. Brief Funct Genomic Proteomic 8: 297-309
65. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W (2002) Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 10: 1453-1465 (Pubitemid 36050885)
66. Vernimmen D, De Gobbi M, Sloane-Stanley JA, Wood WG, Higgs DR (2007) Long-range chromosomal interactions regulate the timing of the transition between poised and active gene expression. EMBO J 26: 2041-2051 (Pubitemid 46625789)
67. Wadman IA, Osada H, Grutz GG, Agulnick AD, Westphal H, Forster A, Rabbitts TH (1997) The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J 16: 3145-3157 (Pubitemid 27234954)
68. Williams AO, Isaacs RJ, Stowell KM (2007) Down-regulation of human topoisomerase IIalpha expression correlates with relative amounts of specificity factors Sp1 and Sp3 bound at proximal and distal promoter regions. BMC Mol Biol 8: 36.
69. Zaidi SK, Sullivan AJ, van Wijnen AJ, Stein JL, Stein GS, Lian JB (2002) Integration of Runx and Smad regulatory signals at transcriptionally active subnuclear sites. Proc Natl Acad Sci USA 99: 8048-8053. (Pubitemid 34651003)
70. Zanjani ED, Almeida-Porada G, Livingston AG, Flake AW, Ogawa M (1998) Human bone marrow CD34-cells engraft in vivo and undergo multilineage expression that includes giving rise to CD34+ cells. Exp Hematol 26: 353-360 (Pubitemid 28177794)
71. Zanjani ED, Almeida-Porada G, Livingston AG, Porada CD, Ogawa M (1999) Engraftment and multilineage expression of human bone marrow CD34-cells in vivo. Ann NY Acad Sci 872: 220-231; discussion 231-232
72. Zanjani ED, Almeida-Porada G, Livingston AG, Zeng H, Ogawa M (2003) Reversible expression of CD34 by adult human bone marrow long-term engrafting hematopoietic stem cells. Exp Hematol 31: 406-412 (Pubitemid 36579366)
73. Zeng C, McNeil S, Pockwinse S, Nickerson J, Shopland L, Lawrence JB, Penman S, Hiebert S, Lian JB, van Wijnen AJ, Stein JL, Stein GS (1998) Intranuclear targeting of AML/CBFalpha regulatory factors to nuclear matrix-associated transcriptional domains. Proc Natl Acad Sci USA 95: 1585-1589 (Pubitemid 28103436)
74. Zeng C, van Wijnen AJ, Stein JL, Meyers S, Sun W, Shopland L, Lawrence JB, Penman S, Lian JB, Stein GS, Hiebert SW (1997) Identification of a nuclear matrix targeting signal in the leukemia and bone-related AML/CBF-alpha transcription factors. Proc Natl Acad Sci USA 94: 6746-6751 (Pubitemid 27281935)