The PZP Domain of AF10 Senses Unmodified H3K27 to Regulate DOT1L-Mediated Methylation of H3K79

Molecular Cell

Volumn 60, Issue 2, 2015, Pages 319-327

  Chen, Shoudeng ^a   Yang, Ze ^b   Wilkinson, Alex W ^b   Deshpande, Aniruddha J ^a   Sidoli, Simone ^c   Krajewski, Krzysztof ^d   Strahl, Brian D ^d   Garcia, Benjamin A ^c   Armstrong, Scott A ^a   Patel, Dinshaw J ^a   Gozani, Or ^b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; HISTONE H3; PROTEIN AF10; PROTEIN DOT1L; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; CHROMATIN; DOT1L PROTEIN, HUMAN; HISTONE; LYSINE; METHYLTRANSFERASE; MLLT10 PROTEIN, HUMAN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENE EXPRESSION; GENE MUTATION; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; HYDROGEN BOND; IN VITRO STUDY; LEUKEMIA CELL; MOLECULAR RECOGNITION; NUCLEOSOME; PROTEIN BINDING; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; BINDING SITE; CARCINOGENESIS; CHEMISTRY; CHROMATIN; GENE EXPRESSION REGULATION; GENETICS; LEUKOCYTE; METABOLISM; METHYLATION; MOLECULAR MODEL; PATHOLOGY; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TUMOR CELL LINE; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CARCINOGENESIS; CELL LINE, TUMOR; CHROMATIN; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION REGULATION, LEUKEMIC; HISTONES; HUMANS; HYDROGEN BONDING; LEUKOCYTES; LYSINE; METHYLATION; METHYLTRANSFERASES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84944891723     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.08.019     Document Type: Article

References (40)

1. Bernt K.M., Zhu N., Sinha A.U., Vempati S., Faber J., Krivtsov A.V., Feng Z., Punt N., Daigle A., Bullinger L., et al. MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 2011, 20:66-78.
2. Bua D.J., Kuo A.J., Cheung P., Liu C.L., Migliori V., Espejo A., Casadio F., Bassi C., Amati B., Bedford M.T., et al. Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks. PLoS ONE 2009, 4:e6789.
3. Chen L., Deshpande A.J., Banka D., Bernt K.M., Dias S., Buske C., Olhava E.J., Daigle S.R., Richon V.M., Pollock R.M., Armstrong S.A. Abrogation of MLL-AF10 and CALM-AF10-mediated transformation through genetic inactivation or pharmacological inhibition of the H3K79 methyltransferase Dot1l. Leukemia 2013, 27:813-822.
4. Daigle S.R., Olhava E.J., Therkelsen C.A., Basavapathruni A., Jin L., Boriack-Sjodin P.A., Allain C.J., Klaus C.R., Raimondi A., Scott M.P., et al. Potent inhibition of DOT1L as treatment of MLL-fusion leukemia. Blood 2013, 122:1017-1025.
5. Deshpande A.J., Bradner J., Armstrong S.A. Chromatin modifications as therapeutic targets in MLL-rearranged leukemia. Trends Immunol. 2012, 33:563-570.
6. Deshpande A.J., Chen L., Fazio M., Sinha A.U., Bernt K.M., Banka D., Dias S., Chang J., Olhava E.J., Daigle S.R., et al. Leukemic transformation by the MLL-AF6 fusion oncogene requires the H3K79 methyltransferase Dot1l. Blood 2013, 121:2533-2541.
7. Deshpande A.J., Deshpande A., Sinha A.U., Chen L., Chang J., Cihan A., Fazio M., Chen C.W., Zhu N., Koche R., et al. AF10 regulates progressive H3K79 methylation and HOX gene expression in diverse AML subtypes. Cancer Cell 2014, 26:896-908.
8. Dik W.A., Brahim W., Braun C., Asnafi V., Dastugue N., Bernard O.A., van Dongen J.J., Langerak A.W., Macintyre E.A., Delabesse E. CALM-AF10+ T-ALL expression profiles are characterized by overexpression of HOXA and BMI1 oncogenes. Leukemia 2005, 19:1948-1957.
9. DiMartino J.F., Ayton P.M., Chen E.H., Naftzger C.C., Young B.D., Cleary M.L. The AF10 leucine zipper is required for leukemic transformation of myeloid progenitors by MLL-AF10. Blood 2002, 99:3780-3785.
10. Ferrari K.J., Scelfo A., Jammula S., Cuomo A., Barozzi I., Stützer A., Fischle W., Bonaldi T., Pasini D. Polycomb-dependent H3K27me1 and H3K27me2 regulate active transcription and enhancer fidelity. Mol. Cell 2014, 53:49-62.
11. Fuchs S.M., Krajewski K., Baker R.W., Miller V.L., Strahl B.D. Influence of combinatorial histone modifications on antibody and effector protein recognition. Curr. Biol. 2011, 21:53-58.
12. Klein B.J., Lalonde M.E., Côté J., Yang X.J., Kutateladze T.G. Crosstalk between epigenetic readers regulates the MOZ/MORF HAT complexes. Epigenetics 2014, 9:186-193.
13. Krivtsov A.V., Armstrong S.A. MLL translocations, histone modifications and leukaemia stem-cell development. Nat. Rev. Cancer 2007, 7:823-833.
14. Lalonde M.E., Avvakumov N., Glass K.C., Joncas F.H., Saksouk N., Holliday M., Paquet E., Yan K., Tong Q., Klein B.J., et al. Exchange of associated factors directs a switch in HBO1 acetyltransferase histone tail specificity. Genes Dev. 2013, 27:2009-2024.
15. Lan F., Collins R.E., De Cegli R., Alpatov R., Horton J.R., Shi X., Gozani O., Cheng X., Shi Y. Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 2007, 448:718-722.
16. Lee J.S., Shukla A., Schneider J., Swanson S.K., Washburn M.P., Florens L., Bhaumik S.R., Shilatifard A. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 2007, 131:1084-1096.
17. Lewis P.W., Müller M.M., Koletsky M.S., Cordero F., Lin S., Banaszynski L.A., Garcia B.A., Muir T.W., Becher O.J., Allis C.D. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 2013, 340:857-861.
18. Li H., Ilin S., Wang W., Duncan E.M., Wysocka J., Allis C.D., Patel D.J. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 2006, 442:91-95.
19. Li Y., Wen H., Xi Y., Tanaka K., Wang H., Peng D., Ren Y., Jin Q., Dent S.Y., Li W., et al. AF9 YEATS domain links histone acetylation to DOT1L-mediated H3K79 methylation. Cell 2014, 159:558-571.
20. Matthews A.G., Kuo A.J., Ramón-Maiques S., Han S., Champagne K.S., Ivanov D., Gallardo M., Carney D., Cheung P., Ciccone D.N., et al. RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 2007, 450:1106-1110.
21. McLean C.M., Karemaker I.D., van Leeuwen F. The emerging roles of DOT1L in leukemia and normal development. Leukemia 2014, 28:2131-2138.
22. Mohan M., Herz H.M., Takahashi Y.H., Lin C., Lai K.C., Zhang Y., Washburn M.P., Florens L., Shilatifard A. Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom). Genes Dev. 2010, 24:574-589.
23. Moore S.D., Strehl S., Dal Cin P. Acute myelocytic leukemia with t(11;17)(q23;q12-q21) involves a fusion of MLL and AF17. Cancer Genet. Cytogenet. 2005, 157:87-89.
24. Musselman C.A., Kutateladze T.G. Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res. 2011, 39:9061-9071.
25. Nguyen A.T., Zhang Y. The diverse functions of Dot1 and H3K79 methylation. Genes Dev. 2011, 25:1345-1358.
26. Okada Y., Jiang Q., Lemieux M., Jeannotte L., Su L., Zhang Y. Leukaemic transformation by CALM-AF10 involves upregulation of Hoxa5 by hDOT1L. Nat. Cell Biol. 2006, 8:1017-1024.
27. Onder T.T., Kara N., Cherry A., Sinha A.U., Zhu N., Bernt K.M., Cahan P., Marcarci B.O., Unternaehrer J., Gupta P.B., et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 2012, 483:598-602.
28. Peña P.V., Davrazou F., Shi X., Walter K.L., Verkhusha V.V., Gozani O., Zhao R., Kutateladze T.G. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 2006, 442:100-103.
29. Prasad R., Leshkowitz D., Gu Y., Alder H., Nakamura T., Saito H., Huebner K., Berger R., Croce C.M., Canaani E. Leucine-zipper dimerization motif encoded by the AF17 gene fused to ALL-1 (MLL) in acute leukemia. Proc. Natl. Acad. Sci. USA 1994, 91:8107-8111.
30. Saksouk N., Avvakumov N., Champagne K.S., Hung T., Doyon Y., Cayrou C., Paquet E., Ullah M., Landry A.J., Côté V., et al. HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol. Cell 2009, 33:257-265.
31. Shi X., Hong T., Walter K.L., Ewalt M., Michishita E., Hung T., Carney D., Peña P., Lan F., Kaadige M.R., et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 2006, 442:96-99.
32. Simon M.D., Chu F., Racki L.R., de la Cruz C.C., Burlingame A.L., Panning B., Narlikar G.J., Shokat K.M. The site-specific installation of methyl-lysine analogs into recombinant histones. Cell 2007, 128:1003-1012.
33. Steger D.J., Lefterova M.I., Ying L., Stonestrom A.J., Schupp M., Zhuo D., Vakoc A.L., Kim J.E., Chen J., Lazar M.A., et al. DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell. Biol. 2008, 28:2825-2839.
34. Stein E.M., Tallman M.S. Mixed lineage rearranged leukaemia: pathogenesis and targeting DOT1L. Curr. Opin. Hematol. 2015, 22:92-96.
35. Suzukawa K., Shimizu S., Nemoto N., Takei N., Taki T., Nagasawa T. Identification of a chromosomal breakpoint and detection of a novel form of an MLL-AF17 fusion transcript in acute monocytic leukemia with t(11;17)(q23;q21). Int. J. Hematol. 2005, 82:38-41.
36. Taverna S.D., Li H., Ruthenburg A.J., Allis C.D., Patel D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 2007, 14:1025-1040.
37. Vermeulen M., Mulder K.W., Denissov S., Pijnappel W.W., van Schaik F.M., Varier R.A., Baltissen M.P., Stunnenberg H.G., Mann M., Timmers H.T. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007, 131:58-69.
38. Vizán P., Beringer M., Ballaré C., Di Croce L. Role of PRC2-associated factors in stem cells and disease. FEBS J. 2015, 282:1723-1735.
39. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., Kauer M., Tackett A.J., Chait B.T., Badenhorst P., et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006, 442:86-90.
40. Yap K.L., Li S., Muñoz-Cabello A.M., Raguz S., Zeng L., Mujtaba S., Gil J., Walsh M.J., Zhou M.M. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by Polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 2010, 38:662-674.