Transcriptional elongation factor ENL phosphorylated by ATM recruits polycomb and switches off transcription for DSB repair

Molecular Cell

Volumn 58, Issue 3, 2015, Pages 468-482

  Ui, Ayako ^a,b   Nagaura, Yuko ^a   Yasui, Akira ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b ST MARIANNA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; BMI1 PROTEIN; HISTONE H2A; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION ELONGATION FACTOR ENL; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; BMI1 PROTEIN, HUMAN; MLLT1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOTOPROTEIN; PROTEIN BINDING; RNF2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR PROTEIN;

ARTICLE; CHROMATIN; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DELETION MUTANT; DNA DOUBLE STRAND BREAK REPAIR; DNA REPAIR; DNA TRANSCRIPTION; GENE MUTATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; U2OS CELL LINE; UBIQUITINATION; WESTERN BLOTTING; AMINO ACID SEQUENCE; CONFOCAL MICROSCOPY; DOUBLE STRANDED DNA BREAK; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; RNA INTERFERENCE; SEQUENCE HOMOLOGY; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BLOTTING, WESTERN; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HEK293 CELLS; HUMANS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; POLYCOMB REPRESSIVE COMPLEX 1; PROTEIN BINDING; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84928907539     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.03.023     Document Type: Article

References (35)

1. Bittner C.B., Zeisig D.T., Zeisig B.B., Slany R.K. Direct physical and functional interaction of the NuA4 complex components Yaf9p and Swc4p. Eukaryot. Cell 2004, 3:976-983.
2. Buchwald G., van der Stoop P., Weichenrieder O., Perrakis A., van Lohuizen M., Sixma T.K. Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J. 2006, 25:2465-2474.
3. Cao R., Tsukada Y., Zhang Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell 2005, 20:845-854.
4. Chodosh L.A., Fire A., Samuels M., Sharp P.A. 5,6-Dichloro-1-beta-D-ribofuranosylbenzimidazole inhibits transcription elongation by RNA polymerase II invitro. J.Biol. Chem. 1989, 264:2250-2257.
5. de Napoles M., Mermoud J.E., Wakao R., Tang Y.A., Endoh M., Appanah R., Nesterova T.B., Silva J., Otte A.P., Vidal M., et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 2004, 7:663-676.
6. García-Cuéllar M.P., Zilles O., Schreiner S.A., Birke M., Winkler T.H., Slany R.K. The ENL moiety of the childhood leukemia-associated MLL-ENL oncoprotein recruits human Polycomb 3. Oncogene 2001, 20:411-419.
7. He N., Chan C.K., Sobhian B., Chou S., Xue Y., Liu M., Alber T., Benkirane M., Zhou Q. Human Polymerase-Associated Factor complex (PAFc) connects the Super Elongation Complex (SEC) to RNA polymerase II on chromatin. Proc. Natl. Acad. Sci. USA 2011, 108:E636-E645.
8. Hemenway C.S., de Erkenez A.C., Gould G.C. The polycomb protein MPc3 interacts with AF9, an MLL fusion partner in t(9;11)(p22;q23) acute leukemias. Oncogene 2001, 20:3798-3805.
9. Janicki S.M., Tsukamoto T., Salghetti S.E., Tansey W.P., Sachidanandam R., Prasanth K.V., Ried T., Shav-Tal Y., Bertrand E., Singer R.H., Spector D.L. From silencing to gene expression: real-time analysis in single cells. Cell 2004, 116:683-698.
10. Kakarougkas A., Ismail A., Chambers A.L., Riballo E., Herbert A.D., Künzel J., Löbrich M., Jeggo P.A., Downs J.A. Requirement for PBAF in transcriptional repression and repair at DNA breaks in actively transcribed regions of chromatin. Mol. Cell 2014, 55:723-732.
11. Kruhlak M., Crouch E.E., Orlov M., Montaño C., Gorski S.A., Nussenzweig A., Misteli T., Phair R.D., Casellas R. The ATM repair pathway inhibits RNA polymerase I transcription in response to chromosome breaks. Nature 2007, 447:730-734.
12. Lan L., Ui A., Nakajima S., Hatakeyama K., Hoshi M., Watanabe R., Janicki S.M., Ogiwara H., Kohno T., Kanno S., Yasui A. The ACF1 complex is required for DNA double-strand break repair in human cells. Mol. Cell 2010, 40:976-987.
13. Leach B.I., Kuntimaddi A., Schmidt C.R., Cierpicki T., Johnson S.A., Bushweller J.H. Leukemia fusion target AF9 is an intrinsically disordered transcriptional regulator that recruits multiple partners via coupled folding and binding. Structure 2013, 21:176-183.
14. Lin C., Garrett A.S., De Kumar B., Smith E.R., Gogol M., Seidel C., Krumlauf R., Shilatifard A. Dynamic transcriptional events in embryonic stem cells mediated by the super elongation complex (SEC). Genes Dev. 2011, 25:1486-1498.
15. Luo Z.J., Lin C.Q., Shilatifard A. The super elongation complex (SEC) family in transcriptional control. Nat. Rev. Mol. Cell Biol. 2012, 13:543-547.
16. Maethner E., Garcia-Cuellar M.P., Breitinger C., Takacova S., Divoky V., Hess J.L., Slany R.K. MLL-ENL inhibits polycomb repressive complex 1 to achieve efficient transformation of hematopoietic cells. Cell Rep. 2013, 3:1553-1566.
17. Mattiroli F., Vissers J.H., van Dijk W.J., Ikpa P., Citterio E., Vermeulen W., Marteijn J.A., Sixma T.K. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 2012, 150:1182-1195.
18. Mills A.A. Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat. Rev. Cancer 2010, 10:669-682.
19. Mueller D., Bach C., Zeisig D., Garcia-Cuellar M.P., Monroe S., Sreekumar A., Zhou R., Nesvizhskii A., Chinnaiyan A., Hess J.L., Slany R.K. A role for the MLL fusion partner ENL in transcriptional elongation and chromatin modification. Blood 2007, 110:4445-4454.
20. Rafalska-Metcalf I.U., Powers S.L., Joo L.M., LeRoy G., Janicki S.M. Single cell analysis of transcriptional activation dynamics. PLoS ONE 2010, 5:e10272.
21. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745.
22. Schulze J.M., Wang A.Y., Kobor M.S. YEATS domain proteins: a diverse family with many links to chromatin modification and transcription. Biochem. Cell Biol. 2009, 87:65-75.
23. Schwartz Y.B., Pirrotta V. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 2007, 8:9-22.
24. Shanbhag N.M., Rafalska-Metcalf I.U., Balane-Bolivar C., Janicki S.M., Greenberg R.A. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 2010, 141:970-981.
25. Shiloh Y., Ziv Y. The ATM protein kinase: regulating the cellularresponse to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 2013, 14:197-210.
26. Simon J.A., Kingston R.E. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 2009, 10:697-708.
27. Smith E., Lin C.Q., Shilatifard A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev. 2011, 25:661-672.
28. Sobhian B., Laguette N., Yatim A., Nakamura M., Levy Y., Kiernan R., Benkirane M. HIV-1 Tat assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP. Mol. Cell 2010, 38:439-451.
29. Steffen P.A., Ringrose L. What are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory. Nat. Rev. Mol. Cell Biol. 2014, 15:340-356.
30. Stock J.K., Giadrossi S., Casanova M., Brookes E., Vidal M., Koseki H., Brockdorff N., Fisher A.G., Pombo A. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 2007, 9:1428-1435.
31. Tan J., Jones M., Koseki H., Nakayama M., Muntean A.G., Maillard I., Hess J.L. CBX8, a polycomb group protein, is essential for MLL-AF9-induced leukemogenesis. Cancer Cell 2011, 20:563-575.
32. Wang H., Wang L., Erdjument-Bromage H., Vidal M., Tempst P., Jones R.S., Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004, 431:873-878.
33. Yokoyama A., Lin M., Naresh A., Kitabayashi I., Cleary M.L. A higher-order complex containing AF4 and ENL family proteins with P-TEFb facilitates oncogenic and physiologic MLL-dependent transcription. Cancer Cell 2010, 17:198-212.
34. Zeisig D.T., Bittner C.B., Zeisig B.B., García-Cuéllar M.P., Hess J.L., Slany R.K. The eleven-nineteen-leukemia protein ENL connects nuclear MLL fusion partners with chromatin. Oncogene 2005, 24:5525-5532.
35. Zhou Q., Li T.D., Price D.H. RNA polymerase II elongation control. Annu. Rev. Biochem. 2012, 81:119-143.