A genome-wide RNA interference screen identifies a differential role of the mediator CDK8 module subunits for GATA/ RUNX-activated transcription in Drosophila

Molecular and Cellular Biology

Volumn 30, Issue 11, 2010, Pages 2837-2848

  Gobert, Vanessa ^a   Osman, Dani ^a   Bras, Stéphanie ^a   Augé, Benoit ^a   Boube, Muriel ^a   Bourbon, Henri Marc ^a   Horn, Thomas ^b   Boutros, Michael ^b   Haenlin, Marc ^a   Waltzer, Lucas ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 8; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR RUNX;

ANIMAL CELL; ARTICLE; BLOOD CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; DROSOPHILA; GENOME; IN VIVO STUDY; LOZENGE; MEDIATOR; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA INTERFERENCE; TRANSACTIVATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 8; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HEMATOPOIESIS; HIGH-THROUGHPUT SCREENING ASSAYS; MEDIATOR COMPLEX; PROTEIN INTERACTION MAPPING; PROTEIN SUBUNITS; RNA INTERFERENCE; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 77952602708     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01625-09     Document Type: Article

References (74)

1. Andrau, J. C., L. van de Pasch, P. Lijnzaad, T. Bijma, M. G. Koerkamp, J. van de Peppel, M. Werner, and F. C. Holstege. 2006. Genome-wide location of the coactivator mediator: binding without activation and transient Cdk8 interaction on DNA. Mol. Cell 22:179-192.
2. Arai, Y., F. Hosoda, H. Kobayashi, K. Arai, Y. Hayashi, N. Kamada, Y. Kaneko, and M. Ohki. 1997. The inv(11)(p15q22) chromosome translocation of de novo and therapy-related myeloid malignancies results in fusion of the nucleoporin gene, NUP98, with the putative RNA helicase gene, DDX10. Blood 89:3936-3944.
3. Arziman, Z., T. Horn, and M. Boutros. 2005. E-RNAi: a web application to design optimized RNAi constructs. Nucleic Acids Res. 33:W582-W588.
4. Bataille, L., B. Auge, G. Ferjoux, M. Haenlin, and L. Waltzer. 2005. Resolving embryonic blood cell fate choice in Drosophila: interplay of GCM and RUNX factors. Development 132:4635-4644. (Pubitemid 41632240)
5. Bjorklund, S., and C. M. Gustafsson. 2005. The yeast Mediator complex and its regulation. Trends Biochem. Sci. 30:240-244.
6. Boube, M., L. Joulia, D. L. Cribbs, and H. M. Bourbon. 2002. Evidence for a mediator of RNA polymerase II transcriptional regulation conserved from yeast to man. Cell 110:143-151. (Pubitemid 34876543)
7. Bourbon, H. M. 2008. Comparative genomics supports a deep evolutionary origin for the large, four-module transcriptional mediator complex. Nucleic Acids Res. 36:3993-4008.
8. Boutros, M., and J. Ahringer. 2008. The art and design of genetic screens: RNA interference. Nat. Rev. Genet. 9:554-566.
9. Boutros, M., A. A. Kiger, S. Armknecht, K. Kerr, M. Hild, B. Koch, S. A. Haas, R. Paro, N. Perrimon and the Heidelberg Fly Array Consortium. 2004. Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303:832-835.
10. Bresnick, E. H., M. L. Martowicz, S. Pal, and K. D. Johnson. 2005. Developmental control via GATA factor interplay at chromatin domains. J. Cell. Physiol. 205:1-9.
11. Cantor, A. B. 2005. GATA transcription factors in hematologic disease. Int. J. Hematol. 81:378-384.
12. Carrera, I., F. Janody, N. Leeds, F. Duveau, and J. E. Treisman. 2008. Pygopus activates Wingless target gene transcription through the mediator complex subunits Med12 and Med13. Proc. Natl. Acad. Sci. U. S. A. 105:6644-6649.
13. Carrera, I., and J. E. Treisman. 2008. Message in a nucleus: signaling to the transcriptional machinery. Curr. Opin. Genet. Dev. 18:397-403.
14. Chadick, J. Z., and F. J. Asturias. 2005. Structure of eukaryotic Mediator complexes. Trends Biochem. Sci. 30:264-271.
15. Clemens, J. C., C. A. Worby, N. Simonson-Leff, M. Muda, T. Maehama, B. A. Hemmings, and J. E. Dixon. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. U. S. A. 97:6499-6503.
16. Coffman, J. A. 2009. Is Runx a linchpin for developmental signaling in metazoans? J. Cell. Biochem. 107:194-202.
17. Collins, A., D. R. Littman, and I. Taniuchi. 2009. RUNX proteins in transcription factor networks that regulate T-cell lineage choice. Nat. Rev. Immunol. 9:106-115.
18. Conaway, R. C., S. Sato, C. Tomomori-Sato, T. Yao, and J. W. Conaway. 2005. The mammalian Mediator complex and its role in transcriptional regulation. Trends Biochem. Sci. 30:250-255.
19. de Bruijn, M. F., and N. A. Speck. 2004. Core-binding factors in hematopoiesis and immune function. Oncogene 23:4238-4248.
20. Deveaux, S., A. Filipe, V. Lemarchandel, J. Ghysdael, P. H. Romeo, and V. Mignotte. 1996. Analysis of the thrombopoietin receptor (MPL) promoter implicates GATA and Ets proteins in the coregulation of megakaryocyte-specific genes. Blood 87:4678-4685. (Pubitemid 26162367)
21. Dietzl, G., D. Chen, F. Schnorrer, K. C. Su, Y. Barinova, M. Fellner, B. Gasser, K. Kinsey, S. Oppel, S. Scheiblauer, A. Couto, V. Marra, K. Keleman, and B. J. Dickson. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448:151-156. (Pubitemid 47067374)
22. Donner, A. J., S. Szostek, J. M. Hoover, and J. M. Espinosa. 2007. CDK8 is a stimulus-specific positive coregulator of p53 target genes. Mol. Cell 27:121-133.
23. Elagib, K. E., and A. N. Goldfarb. 2007. Regulation of RUNX1 transcriptional function by GATA-1. Crit. Rev. Eukaryot. Gene Expr. 17:271-280.
24. Elagib, K. E., I. S. Mihaylov, L. L. Delehanty, G. C. Bullock, K. D. Ouma, J. F. Caronia, S. L. Gonias, and A. N. Goldfarb. 2008. Cross-talk of GATA-1 and P-TEFb in megakaryocyte differentiation. Blood 112:4884-4894.
25. Elagib, K. E., F. K. Racke, M. Mogass, R. Khetawat, L. L. Delehanty, and A. N. Goldfarb. 2003. RUNX1 and GATA-1 coexpression and cooperation in megakaryocytic differentiation. Blood 101:4333-4341.
26. Ferjoux, G., B. Auge, K. Boyer, M. Haenlin, and L. Waltzer. 2007. A GATA/ RUNX cis-regulatory module couples Drosophila blood cell commitment and differentiation into crystal cells. Dev. Biol. 305:726-734.
27. Firestein, R., A. J. Bass, S. Y. Kim, I. F. Dunn, S. J. Silver, I. Guney, E. Freed, A. H. Ligon, N. Vena, S. Ogino, M. G. Chheda, P. Tamayo, S. Finn, Y. Shrestha, J. S. Boehm, S. Jain, E. Bojarski, C. Mermel, J. Barretina, J. A. Chan, J. Baselga, J. Tabernero, D. E. Root, C. S. Fuchs, M. Loda, R. A. Shivdasani, M. Meyerson, and W. C. Hahn. 2008. CDK8 is a colorectal cancer oncogene that regulates beta-catenin activity. Nature 455:547-551.
28. Fossett, N., K. Hyman, K. Gajewski, S. H. Orkin, and R. A. Schulz. 2003. Combinatorial interactions of serpent, lozenge, and U-shaped regulate crystal cell lineage commitment during Drosophila hematopoiesis. Proc. Natl. Acad. Sci. U. S. A. 100:11451-11456.
29. Fossett, N., S. G. Tevosian, K. Gajewski, Q. Zhang, S. H. Orkin, and R. A. Schulz. 2001. The Friend of GATA proteins U-shaped, FOG-1, and FOG-2 function as negative regulators of blood, heart, and eye development in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 98:7342-7347.
30. Gajewski, K. M., R. P. Sorrentino, J. H. Lee, Q. Zhang, M. Russell, and R. A. Schulz. 2007. Identification of a crystal cell-specific enhancer of the black cells prophenoloxidase gene in Drosophila. Genesis 45:200-207.
31. Gao, H., X. Wu, and N. Fossett. 2009. Upregulation of the Drosophila friend of GATA gene u-shaped by JAK/STAT signaling maintains lymph gland prohemocyte potency. Mol. Cell. Biol. 29:6086-6096.
32. Gilsdorf, M., T. Horn, Z. Arziman, O. Pelz, E. Kiner, and M. Boutros. 2010. GenomeRNAi: a database for cell-based RNAi phenotypes. 2009 update. Nucleic Acids Res. 38:D448-D452.
33. Gordon, D. F., E. A. Tucker, K. Tundwal, H. Hall, W. M. Wood, and E. C. Ridgway. 2006. MED220/thyroid receptor-associated protein 220 functions as a transcriptional coactivator with Pit-1 and GATA-2 on the thyrotropinbeta promoter in thyrotropes. Mol. Endocrinol. 20:1073-1089.
34. Haenlin, M., and L. Waltzer. 2004. Roles of GATA factors in development. In S. Iuchi and N. Kuldell (ed.), Zinc finger proteins: from atomic contact to cellular function. Landes Bioscience, Austin, TX.
35. Ho, I. C., and S. Y. Pai. 2007. GATA-3 - not just for Th2 cells anymore. Cell Mol. Immunol. 4:15-29.
36. Holz, A., B. Bossinger, T. Strasser, W. Janning, and R. Klapper. 2003. The two origins of hemocytes in Drosophila. Development 130:4955-4962.
37. Huang, H., M. Yu, T. E. Akie, T. B. Moran, A. J. Woo, N. Tu, Z. Waldon, Y. Y. Lin, H. Steen, and A. B. Cantor. 2009. Differentiation-dependent interactions between RUNX-1 and FLI-1 during megakaryocyte development. Mol. Cell. Biol. 29:4103-4115.
38. Jensen, L. J., M. Kuhn, M. Stark, S. Chaffron, C. Creevey, J. Muller, T. Doerks, P. Julien, A. Roth, M. Simonovic, P. Bork, and C. von Mering. 2009. STRING 8 - a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37:D412-D416.
39. Jiang, H., F. Zhang, T. Kurosu, and B. M. Peterlin. 2005. Runx1 binds positive transcription elongation factor b and represses transcriptional elongation by RNA polymerase II: possible mechanism of CD4 silencing. Mol. Cell. Biol. 25:10675-10683.
40. Kim, S., X. Xu, A. Hecht, and T. G. Boyer. 2006. Mediator is a transducer of Wnt/beta-catenin signaling. J. Biol. Chem. 281:14066-14075.
41. Kim, W. Y., M. Sieweke, E. Ogawa, H. J. Wee, U. Englmeier, T. Graf, and Y. Ito. 1999. Mutual activation of Ets-1 and AML1 DNA binding by direct interaction of their autoinhibitory domains. EMBO J. 18:1609-1620.
42. Kim, Y. J., and J. T. Lis. 2005. Interactions between subunits of Drosophila Mediator and activator proteins. Trends Biochem. Sci. 30:245-249.
43. Kitabayashi, I., Y. Aikawa, L. A. Nguyen, A. Yokoyama, and M. Ohki. 2001. Activation of AML1-mediated transcription by MOZ and inhibition by the MOZ-CBP fusion protein. EMBO J. 20:7184-7196. (Pubitemid 34062310)
44. Knuesel, M. T., K. D. Meyer, C. Bernecky, and D. J. Taatjes. 2009. The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function. Genes Dev. 23:439-451.
45. Knuesel, M. T., K. D. Meyer, A. J. Donner, J. M. Espinosa, and D. J. Taatjes. 2009. The human CDK8 subcomplex is a histone kinase that requires Med12 for activity and can function independently of Mediator. Mol. Cell. Biol. 29:650-661.
46. Kornberg, R. D. 2005. Mediator and the mechanism of transcriptional activation. Trends Biochem. Sci. 30:235-239.
47. Lebestky, T., T. Chang, V. Hartenstein, and U. Banerjee. 2000. Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288:146-149. (Pubitemid 30203049)
48. Loncle, N., M. Boube, L. Joulia, C. Boschiero, M. Werner, D. L. Cribbs, and H. M. Bourbon. 2007. Distinct roles for Mediator Cdk8 module subunits in Drosophila development. EMBO J. 26:1045-1054. (Pubitemid 46303589)
49. Lowry, J. A., and J. P. Mackay. 2006. GATA-1: one protein, many partners. Int. J. Biochem. Cell Biol. 38:6-11.
50. Lutterbach, B., J. J. Westendorf, B. Linggi, A. Patten, M. Moniwa, J. R. Davie, K. D. Huynh, V. J. Bardwell, R. M. Lavinsky, M. G. Rosenfeld, C. Glass, E. Seto, and S. W. Hiebert. 1998. ETO, a target of t(8;21) in acute leukemia, interacts with the N-CoR and mSin3 corepressors. Mol. Cell. Biol. 18:7176-7184.
51. Malik, S., and R. G. Roeder. 2005. Dynamic regulation of pol II transcription by the mammalian Mediator complex. Trends Biochem. Sci. 30:256-263.
52. Mandal, L., U. Banerjee, and V. Hartenstein. 2004. Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat. Genet. 36:1019-1023.
53. Meister, M. 2004. Blood cells of Drosophila: cell lineages and role in host defence. Curr. Opin. Immunol. 16:10-15.
54. Milchanowski, A. B., A. L. Henkenius, M. Narayanan, V. Hartenstein, and U. Banerjee. 2004. Identification and characterization of genes involved in embryonic crystal cell formation during Drosophila hematopoiesis. Genetics 168:325-339.
55. Muller, P., D. Kuttenkeuler, V. Gesellchen, M. P. Zeidler, and M. Boutros. 2005. Identification of JAK/STAT signalling components by genome-wide RNA interference. Nature 436:871-875. (Pubitemid 41160648)
56. Muratoglu, S., B. Hough, S. T. Mon, and N. Fossett. 2007. The GATA factor Serpent cross-regulates lozenge and u-shaped expression during Drosophila blood cell development. Dev. Biol. 311:636-649.
57. Niebuhr, B., M. Fischer, M. Tager, J. Cammenga, and C. Stocking. 2008. Gatekeeper function of the RUNX1 transcription factor in acute leukemia. Blood Cells Mol. Dis. 40:211-218.
58. Nybakken, K., S. A. Vokes, T. Y. Lin, A. P. McMahon, and N. Perrimon. 2005. A genome-wide RNA interference screen in Drosophila melanogaster cells for new components of the Hh signaling pathway. Nat. Genet. 37:1323-1332.
59. Orkin, S. H., and L. I. Zon. 2008. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132:631-644. (Pubitemid 351260057)
60. Osman, D., V. Gobert, F. Ponthan, O. Heidenreich, M. Haenlin, and L. Waltzer. 2009. A Drosophila model identifies calpains as modulators of the human leukemogenic fusion protein AML1-ETO. Proc. Natl. Acad. Sci. U. S. A. 106:12043-12048.
61. Rehorn, K. P., H. Thelen, A. M. Michelson, and R. Reuter. 1996. A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila. Development 122:4023-4031.
62. Shimizu, R., and M. Yamamoto. 2005. Gene expression regulation and domain function of hematopoietic GATA factors. Semin. Cell Dev. Biol. 16:129-136.
63. Sinenko, S. A., L. Mandal, J. A. Martinez-Agosto, and U. Banerjee. 2009. Dual role of wingless signaling in stem-like hematopoietic precursor maintenance in Drosophila. Dev. Cell 16:756-763.
64. Sorrentino, R. P., T. Tokusumi, and R. A. Schulz. 2007. The Friend of GATA protein U-shaped functions as a hematopoietic tumor suppressor in Drosophila. Dev. Biol. 311:311-323.
65. Stumpf, M., C. Waskow, M. Krotschel, D. van Essen, P. Rodriguez, X. Zhang, B. Guyot, R. G. Roeder, and T. Borggrefe. 2006. The mediator complex functions as a coactivator for GATA-1 in erythropoiesis via subunit Med1/TRAP220. Proc. Natl. Acad. Sci. U. S. A. 103:18504-18509.
66. Takagi, Y., and R. D. Kornberg. 2006. Mediator as a general transcription factor. J. Biol. Chem. 281:80-89.
67. Treisman, J. 2001. Drosophila homologues of the transcriptional coactivation complex subunits TRAP240 and TRAP230 are required for identical processes in eye-antennal disc development. Development 128:603-615. (Pubitemid 32229602)
68. van de Peppel, J., N. Kettelarij, H. van Bakel, T. T. Kockelkorn, D. van Leenen, and F. C. Holstege. 2005. Mediator expression profiling epistasis reveals a signal transduction pathway with antagonistic submodules and highly specific downstream targets. Mol. Cell 19:511-522.
69. Waltzer, L., L. Bataille, S. Peyrefitte, and M. Haenlin. 2002. Two isoforms of Serpent containing either one or two GATA zinc fingers have different roles in Drosophila haematopoiesis. EMBO J. 21:5477-5486. (Pubitemid 35231027)
70. Waltzer, L., G. Ferjoux, L. Bataille, and M. Haenlin. 2003. Cooperation between the GATA and RUNX factors Serpent and Lozenge during Drosophila hematopoiesis. EMBO J. 22:6516-6525. (Pubitemid 38009599)
71. Woo, A. J., T. B. Moran, Y. L. Schindler, S. K. Choe, N. B. Langer, M. R. Sullivan, Y. Fujiwara, B. H. Paw, and A. B. Cantor. 2008. Identification of ZBP-89 as a novel GATA-1-associated transcription factor involved in megakaryocytic and erythroid development. Mol. Cell. Biol. 28:2675-2689.
72. Xu, G., R. Kanezaki, T. Toki, S. Watanabe, Y. Takahashi, K. Terui, I. Kitabayashi, and E. Ito. 2006. Physical association of the patient-specific GATA1 mutants with RUNX1 in acute megakaryoblastic leukemia accompanying Down syndrome. Leukemia 20:1002-1008. (Pubitemid 43797291)
73. Yoneda-Kato, N., A. T. Look, M. N. Kirstein, M. B. Valentine, S. C. Raimondi, K. J. Cohen, A. J. Carroll, and S. W. Morris. 1996. The t(3;5)(q25.1; q34) of myelodysplastic syndrome and acute myeloid leukemia produces a novel fusion gene, NPM-MLF1. Oncogene 12:265-275. (Pubitemid 26042564)
74. Zhou, H., S. Kim, S. Ishii, and T. G. Boyer. 2006. Mediator modulates Gli3-dependent Sonic hedgehog signaling. Mol. Cell. Biol. 26:8667-8682.