Polycomb repressive complex 2 (PRC2) restricts hematopoietic stem cell activity

PLoS Biology

Volumn 6, Issue 4, 2008, Pages 796-809

  Majewski, Ian J ^a,b   Blewitt, Marnie E ^a   De Graaf, Carolyn A ^a,b   McManus, Edward J ^a   Bahlo, Melanie ^a   Hilton, Adrienne A ^a   Hyland, Craig D ^a   Smyth, Gordon K ^a   Corbin, Jason E ^a   Metcalf, Donald ^a   Alexander, Warren S ^a,b   Hilton, Douglas J ^a,b  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLNITROSOUREA; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN DERIVATIVE; SUPPRESSOR OF ZESTE 12; THROMBOPOIETIN RECEPTOR; MESSENGER RNA; REPRESSOR PROTEIN; SUZ12 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; MOUSE; MUTATION; NONHUMAN; PROTEIN DEFICIENCY; PROTEIN FUNCTION; THROMBOCYTOPENIA; WILD TYPE; ALLELE; ANIMAL; FEMALE; GENETICS; MALE; METABOLISM; PHENOTYPE; TRANSGENIC MOUSE;

MUS;

ALLELES; ANIMALS; FEMALE; HEMATOPOIETIC STEM CELLS; MALE; MICE; MICE, TRANSGENIC; MUTATION; PHENOTYPE; POLYCOMB REPRESSIVE COMPLEX 2; POLYCOMB-GROUP PROTEINS; REPRESSOR PROTEINS; RNA, MESSENGER;

EID: 43249127096     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060093     Document Type: Article

References (68)

1. Birve A, Sengupta AK, Beuchle D, Larsson J, Kennison JA, et al. (2001) Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants. Development 128: 3371-3379.
2. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043.
3. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, et al. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196.
4. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905.
5. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208.
6. Cao R, Zhang Y (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14: 155-164.
7. Ringrose L, Ehret H, Paro R (2004) Distinct contributions of histone H3 lysine 9 and 27 methylation to locus-specific stability of polycomb complexes. Mol Cell 16: 641-653.
8. Kirmizis A, Bartley SM, Kuzmichev A, Margueron R, Reinberg D, et al. (2004) Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev 18: 1592-1605.
9. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
10. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
11. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123-1136.
12. Squazzo SL, O'Geen H, Komashko VM, Krig SR, Jin VX, et al. (2006) Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res 16: 890-900.
13. Tolhuis B, de Wit E, Muijrers I, Teunissen H, Talhout W, et al. (2006) Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38: 694-699.
14. Schwartz YB, Kahn TG, Nix DA, Li XY, Bourgon R, et al. (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38: 700-705.
15. Min J, Zhang Y, Xu RM (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17: 1823-1828.
16. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, et al. (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881.
17. Sparmann A, van Lohuizen M (2006) Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 6: 846-856.
18. Schoeftner S, Sengupta AK, Kubicek S, Mechtler K, Spahn L, et al. (2006) Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. Embo J 25: 3110-3122.
19. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
20. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, et al. (2005) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874.
21. Shumacher A, Faust C, Magnuson T (1996) Positional cloning of a global regulator of anterior-posterior patterning in mice. Nature 383: 250-253.
22. O'Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, et al. (2001) The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 21: 4330-4336.
23. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. Embo J 23: 4061-4071.
24. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, et al. (2003) EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. Embo J 22: 5323-5335.
25. Kirmizis A, Bartley SM, Farnham PJ (2003) Identification of the polycomb group protein SU(Z)12 as a potential molecular target for human cancer therapy. Mol Cancer Ther 2: 113-121.
26. Weinmann AS, Bartley SM, Zhang T, Zhang MQ, Farnham PJ (2001) Use of chromatin immunoprecipitation to clone novel E2F target promoters. Mol Cell Biol 21: 6820-6832.
27. Su IH, Basavaraj A, Krutchinsky AN, Hobert O, Ullrich A, et al. (2003) Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat Immunol 4: 124-131.
28. Iwama A, Oguro H, Negishi M, Kato Y, Morita Y, et al. (2004) Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 21: 843-851.
29. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, et al. (2003) Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423: 302-305.
30. Lessard J, Sauvageau G (2003) Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260.
31. Oguro H, Iwama A, Morita Y, Kamijo T, van Lohuizen M, et al. (2006) Differential impact of Ink4a and Arf on hematopoietic stem cells and their bone marrow microenvironment in Bmi1-deficient mice. J Exp Med 203: 2247-2253.
32. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397: 164-168.
33. Lessard J, Schumacher A, Thorsteinsdottir U, van Lohuizen M, Magnuson T, et al. (1999) Functional antagonism of the Polycomb-Group genes eed and Bmi1 in hemopoietic cell proliferation. Genes Dev 13: 2691-2703.
34. Richie ER, Schumacher A, Angel JM, Holloway M, Rinchik EM, et al. (2002) The Polycomb-group gene eed regulates thymocyte differentiation and suppresses the development of carcinogen-induced T-cell lymphomas. Oncogene 21: 299-306.
35. Su IH, Dobenecker MW, Dickinson E, Oser M, Basavaraj A, et al. (2005) Polycomb group protein ezh2 controls actin polymerization and cell signaling. Cell 121: 425-436.
36. Kamminga LM, Bystrykh LV, de Boer A, Houwer S, Douma J, et al. (2006) The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood 107: 2170-2179.
37. Lok S, Kaushansky K, Holly RD, Kuijper JL, Lofton-Day CE, et al. (1994) Cloning and expression of murine thrombopoietin cDNA and stimulation of platelet production in vivo. Nature 369: 565-568.
38. Kaushansky K, Lok S, Holly RD, Broudy VC, Lin N, et al. (1994) Promotion of megakaryocyte progenitor expansion and differentiation by the c-Mpl ligand thrombopoietin. Nature 369: 568-571.
39. Gurney AL, Carver-Moore K, de Sauvage FJ, Moore MW (1994) Thrombocytopenia in c-mpl-deficient mice. Science 265: 1445-1447.
40. de Sauvage FJ, Carver-Moore K, Luoh SM, Ryan A, Dowd M, et al. (1996) Physiological regulation of early and late stages of megakaryocytopoiesis by thrombopoietin. J Exp Med 183: 651-656.
41. Alexander WS, Roberts AW, Nicola NA, Li R, Metcalf D (1996) Deficiencies in progenitor cells of multiple hematopoietic lineages and defective megakaryocytopoiesis in mice lacking the thrombopoietic receptor c-Mpl. Blood 87: 2162-2170.
42. Ihara K, Ishii E, Eguchi M, Takada H, Suminoe A, et al. (1999) Identification of mutations in the c-mpl gene in congenital amegakaryocytic thrombocytopenia. Proc Natl Acad Sci U S A 96: 3132-3136.
43. Ballmaier M, Germeshausen M, Schulze H, Cherkaoui K, Lang S, et al. (2001) c-mpl mutations are the cause of congenital amegakaryocytic thrombocytopenia. Blood 97: 139-146.
44. Buza-Vidas N, Antonchuk J, Qian H, Mansson R, Luc S, et al. (2006) Cytokines regulate postnatal hematopoietic stem cell expansion: opposing roles of thrombopoietin and LNK. Genes Dev 20: 2018-2023.
45. Kimura S, Roberts AW, Metcalf D, Alexander WS (1998) Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc Natl Acad Sci U S A 95: 1195-1200.
46. Carver-Moore K, Broxmeyer HE, Luoh SM, Cooper S, Peng J, et al. (1996) Low levels of erythroid and myeloid progenitors in thrombopoietin-and cmpl-deficient mice. Blood 88: 803-808.
47. Ballmaier M, Germeshausen M, Krukemeier S, Welte K (2003) Thrombopoietin is essential for the maintenance of normal hematopoiesis in humans: development of aplastic anemia in patients with congenital amegakaryocytic thrombocytopenia. Ann N Y Acad Sci 996: 17-25.
48. Carpinelli MR, Hilton DJ, Metcalf D, Antonchuk JL, Hyland CD, et al. (2004) Suppressor screen in Mpl-/- mice: c-Myb mutation causes supraphysiological production of platelets in the absence of thrombopoietin signaling. Proc Natl Acad Sci U S A 101: 6553-6558.
49. Till JE, McCulloch E (1961) A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 14: 213-222.
50. Adolfsson J, Mansson R, Buza-Vidas N, Hultquist A, Liuba K, et al. (2005) Identification of Flt3p lympho-myeloid stem cells lacking erythro- megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121: 295-306.
51. Stachura DL, Chou ST, Weiss MJ (2006) Early block to erythromegakaryocytic development conferred by loss of transcription factor GATA-1. Blood 107: 87-97.
52. Pasini D, Bracken AP, Hansen JB, Capillo M, Helin K (2007) The polycomb group protein suz12 is required for embryonic stem cell differentiation. Mol Cell Biol 27: 3769-3779.
53. Montgomery ND, Yee D, Chen A, Kalantry S, Chamberlain SJ, et al. (2005) The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol 15: 942-947.
54. Kim SY, Levenson JM, Korsmeyer S, Sweatt JD, Schumacher A (2007) Developmental regulation of Eed complex composition governs a switch in global histone modification in brain. J Biol Chem 282: 9962-9972.
55. Kim SY, Paylor SW, Magnuson T, Schumacher A (2006) Juxtaposed Polycomb complexes co-regulate vertebral identity. Development 133: 4957-4968.
56. Kuzmichev A, Margueron R, Vaquero A, Preissner TS, Scher M, et al. (2005) Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci U S A 102: 1859-1864.
57. Chien J, Staub J, Avula R, Zhang H, Liu W, et al. (2005) Epigenetic silencing of TCEAL7 (Bex4) in ovarian cancer. Oncogene 24: 5089-5100.
58. Foltz G, Ryu GY, Yoon JG, Nelson T, Fahey J, et al. (2006) Genome-wide analysis of epigenetic silencing identifies BEX1 and BEX2 as candidate tumor suppressor genes in malignant glioma. Cancer Res 66: 6665-6674.
59. Pupa SM, Argraves WS, Forti S, Casalini P, Berno V, et al. (2004) Immunological and pathobiological roles of fibulin-1 in breast cancer. Oncogene 23: 2153-2160.
60. Wlazlinski A, Engers R, Hoffmann MJ, Hader C, Jung V, et al. (2007) Downregulation of several fibulin genes in prostate cancer. Prostate 67: 1770-1780.
61. Naderi A, Teschendorff AE, Beigel J, Cariati M, Ellis IO, et al. (2007) BEX2 is overexpressed in a subset of primary breast cancers and mediates nerve growth factor/nuclear factor-kappaB inhibition of apoptosis in breast cancer cell lines. Cancer Res 67: 6725-6736.
62. Quentmeier H, Tonelli R, Geffers R, Pession A, Uphoff CC, et al. (2005) Expression of BEX1 in acute myeloid leukemia with MLL rearrangements. Leukemia 19: 1488-1489.
63. Fischer C, Drexler HG, Reinhardt J, Zaborski M, Quentmeier H (2007) Epigenetic regulation of brain expressed X-linked-2, a marker for acute myeloid leukemia with mixed lineage leukemia rearrangements. Leukemia 21: 374-377.
64. Villa R, Pasini D, Gutierrez A, Morey L, Occhionorelli M, et al. (2007) Role of the polycomb repressive complex 2 in acute promyelocytic leukemia. Cancer Cell 11: 513-525.
65. Dickins RA, McJunkin K, Hernando E, Premsrirut PK, Krizhanovsky V, et al. (2007) Tissue-specific and reversible RNA interference in transgenic mice. Nat Genet 39: 914-921.
66. Dickins RA, Hemann MT, Zilfou JT, Simpson DR, Ibarra I, et al. (2005) Probing tumor phenotypes using stable and regulated synthetic microRNA precursors. Nat Genet 37: 1289-1295.
67. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
68. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.