Opposing roles of polycomb repressive complexes in hematopoietic stem and progenitor cells

Blood

Volumn 116, Issue 5, 2010, Pages 731-739

  Majewski, Ian J ^a   Ritchie, Matthew E ^b   Phipson, Belinda ^b   Corbin, Jason ^a   Pakusch, Miha ^a   Ebert, Anja ^c   Busslinger, Meinrad ^c   Koseki, Haruhiko ^d   Hu, Yifang ^b   Smyth, Gordon K ^b   Alexander, Warren S ^a,e   Hilton, Douglas J ^a,e   Blewitt, Marnie E ^a  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^d RIKEN Center for Integrative Medical Sciences   (Japan)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 1; POLYCOMB REPRESSIVE COMPLEX 2; UNCLASSIFIED DRUG; EED PROTEIN, MOUSE; EZH2 PROTEIN, MOUSE; HISTONE LYSINE METHYLTRANSFERASE; MULTIPROTEIN COMPLEX; REPRESSOR PROTEIN; SFMBT1 PROTEIN, MOUSE; SUZ12 PROTEIN, MOUSE; TRANSCRIPTION FACTOR YY1; YY1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CELL POPULATION; GENE FUNCTION; GENE IDENTIFICATION; HEMATOPOIETIC STEM CELL; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; COMPARATIVE STUDY; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; RADIATION CHIMERA; RNA INTERFERENCE; STEM CELL;

ANIMALS; BONE MARROW TRANSPLANTATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HEMATOPOIETIC STEM CELLS; HISTONE-LYSINE N-METHYLTRANSFERASE; MICE; MICE, INBRED C57BL; MULTIPROTEIN COMPLEXES; MUTATION; PHENOTYPE; RADIATION CHIMERA; REPRESSOR PROTEINS; RNA INTERFERENCE; STEM CELLS; TRANSCRIPTION, GENETIC; YY1 TRANSCRIPTION FACTOR;

EID: 77956282774     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-12-260760     Document Type: Article

References (52)

1. Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298(5595):1039-1043.
2. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell. 2002;111(2):185-196. (Pubitemid 35292439)
3. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 2002;16(22):2893-2905. (Pubitemid 35334738)
4. Muller J, Hart CM, Francis NJ, et al. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell. 2002;111(2):197-208.
5. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J. 2004;23(20):4061-4071. (Pubitemid 39472427)
6. Montgomery ND, Yee D, Chen A, et al. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol. 2005;15(10):942-947. (Pubitemid 40772064)
7. Sarma K, Margueron R, Ivanov A, Pirrotta V, Reinberg D. Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol Cell Biol. 2008;28(8):2718-2731.
8. Lee TI, Jenner RG, Boyer LA, et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell. 2006;125(2):301-313. (Pubitemid 44313811)
9. Boyer LA, Plath K, Zeitlinger J, et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature. 2006;441(7091):349-353.
10. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 2006;20(9):1123-1136.
11. Kirmizis A, Bartley SM, Kuzmichev A, et al. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev. 2004;18(13):1592-1605.
12. de Napoles M, Mermoud JE, Wakao R, et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell. 2004;7(5):663-676. (Pubitemid 39462687)
13. Wang H, Wang L, Erdjument-Bromage H, et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature. 2004;431(7010):873-878. (Pubitemid 39434086)
14. Cao R, Tsukada Y, Zhang Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell. 2005;20(6):845-854. (Pubitemid 41814874)
15. Kallin EM, Cao R, Jothi R, et al. Genome-wide uH2A localization analysis highlights Bmi1-dependent deposition of the mark at repressed genes. PLoS Genet. 2009;5(6):e1000506.
16. Wu S, Trievel RC, Rice JC. Human SFMBT is a transcriptional repressor protein that selectively binds the N-terminal tail of histone H3. FEBS Lett. 2007;581(17):3289-3296. (Pubitemid 46977378)
17. Atchison L, Ghias A, Wilkinson F, Bonini N, Atchison ML. Transcription factor YY1 functions as a PcG protein in vivo. EMBO J. 2003;22(6):1347-1358. (Pubitemid 36362698)
18. Wang L, Brown JL, Cao R, Zhang Y, Kassis JA, Jones RS. Hierarchical recruitment of polycomb group silencing complexes. Mol Cell. 2004;14(5):637-646.
19. Ku M, Koche RP, Rheinbay E, et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 2008;4(10):e1000242.
20. Rastelli L, Chan CS, Pirrotta V. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J. 1993;12(4):1513-1522. (Pubitemid 23112805)
21. Lee MG, Villa R, Trojer P, et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science. 2007;318(5849):447-450. (Pubitemid 47614529)
22. Francis NJ, Kingston RE, Woodcock CL. Chromatin compaction by a polycomb group protein complex. Science. 2004;306(5701):1574-1577.
23. Schoeftner S, Sengupta AK, Kubicek S, et al. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 2006;25(13):3110-3122. (Pubitemid 44121103)
24. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature. 1999;397(6715):164-168.
25. Oguro H, Iwama A, Morita Y, Kamijo T, van Lohuizen M, Nakauchi H. Differential impact of Ink4a and Arf on hematopoietic stem cells and their bone marrow microenvironment in Bmi1-deficient mice. J Exp Med. 2006;203(10):2247- 2253. (Pubitemid 44498359)
26. Majewski IJ, Blewitt ME, de Graaf CA, et al. Polycomb repressive complex 2 (PRC2) restricts hematopoietic stem cell activity. PLoS Biol. 2008;6(4):e93.
27. Lessard J, Schumacher A, Thorsteinsdottir U, van Lohuizen M, Magnuson T, Sauvageau G. Functional antagonism of the Polycomb-Group genes eed and Bmi1 in hemopoietic cell proliferation. Genes Dev. 1999;13(20):2691-2703. (Pubitemid 29508556)
28. Kimura S, Roberts AW, Metcalf D, Alexander WS. Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc Natl Acad Sci U S A. 1998;95(3):1195-1200. (Pubitemid 28124935)
29. Lok S, Kaushansky K, Holly RD, et al. Cloning and expression of murine thrombopoietin cDNA and stimulation of platelet production in vivo. Nature. 1994;369(6481):565-568.
30. Loughran SJ, Kruse EA, Hacking DF, et al. The transcription factor Erg is essential for definitive hematopoiesis and the function of adult hematopoietic stem cells. Nat Immunol. 2008;9(7):810-819.
31. Su IH, Basavaraj A, Krutchinsky AN, et al. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat Immunol. 2003;4(2):124-131. (Pubitemid 36193013)
32. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3(Article 3).
33. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545-15550. (Pubitemid 41528093)
34. Schumacher A, Faust C, Magnuson T. Positional cloning of a global regulator of anterior-posterior patterning in mice. Nature. 1996;384(6610):648.
35. van der Lugt NM, Domen J, Linders K, et al. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 1994;8(7):757-769. (Pubitemid 24985778)
36. Akasaka T, Kanno M, Balling R, Mieza MA, Taniguchi M, Koseki H. A role for mel-18, a Polycomb group-related vertebrate gene, during theanteroposterior specification of the axial skeleton. Development. 1996;122(5):1513-1522. (Pubitemid 26159640)
37. Isono K, Fujimura Y, Shinga J, et al. Mammalian polyhomeotic homologues Phc2 and Phc1 act in synergy to mediate polycomb repression of Hox genes. Mol Cell Biol. 2005;25(15):6694-6706. (Pubitemid 41023242)
38. Takihara Y, Tomotsune D, Shirai M, et al. Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development. 1997;124(19):3673-3682.
39. del Mar Lorente M, Marcos-Gutierrez C, Perez C, et al. Loss- and gain-of-function mutations show a polycomb group function for Ring1A in mice. Development. 2000;127(23):5093-5100. (Pubitemid 32000666)
40. Cales C, Roman-Trufero M, Pavon L, et al. Inactivation of the polycomb group protein Ring1B unveils an antiproliferative role in hematopoietic cell expansion and cooperation with tumorigenesis associated with Ink4a deletion. Mol Cell Biol. 2008;28(3):1018-1028.
41. Donohoe ME, Zhang X, McGinnis L, Biggers J, Li E, Shi Y. Targeted disruption of mouse Yin Yang 1 transcription factor results in peri-implantation lethality. Mol Cell Biol. 1999;19(10):7237-7244.
42. Stachura DL, Chou ST, Weiss MJ. Early block to erythromegakaryocytic development conferred by loss of transcription factor GATA-1. Blood. 2006;107(1):87-97.
43. Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer. 2006;6(11):846-856. (Pubitemid 44629896)
44. Kamminga LM, Bystrykh LV, de Boer A, et al. The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood. 2006;107(5):2170-2179.
45. Kim SY, Paylor SW, Magnuson T, Schumacher A. Juxtaposed Polycomb complexes co-regulate vertebral identity. Development. 2006;133(24):4957-4968. (Pubitemid 46085061)
46. Wilkinson FH, Park K, Atchison ML. Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proc Natl Acad Sci U S A. 2006;103(51):19296-19301. (Pubitemid 46026026)
47. Thorsteinsdottir U, Mamo A, Kroon E, et al. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood. 2002;99(1):121-129.
48. Lawrence HJ, Christensen J, Fong S, 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.
49. Zhang P, Iwasaki-Arai J, Iwasaki H, et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity. 2004;21(6):853-863.
50. Morin RD, Johnson NA, Severson TM, et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet. 42(2):181-185.
51. van Galen JC, Muris JJ, Oudejans JJ, et al. Expression of the polycomb-group gene BMI1 is related to an unfavourable prognosis in primary nodal DLBCL. J Clin Pathol. 2007;60(2):167-172. (Pubitemid 46245780)
52. Pietersen AM, Horlings HM, Hauptmann M, et al. EZH2 and BMI1 inversely correlate with prognosis and TP53 mutation in breast cancer. Breast Cancer Res. 2008;10(6):R109.