Cellular functions of MLL/SET-family histone H3 lysine 4 methyltransferase components
Received date: 21 Jan 2016
Accepted date: 23 Feb 2016
Published date: 22 Mar 2016
Copyright
The MLL/SET family of histone H3 lysine 4 methyltransferases form enzyme complexes with core subunits ASH2L, WDR5, RbBP5, and DPY-30 (often abbreviated WRAD), and are responsible for global histone H3 lysine 4 methylation, a hallmark of actively transcribed chromatin in mammalian cells. Accordingly, the function of these proteins is required for a wide variety of processes including stem cell differentiation, cell growth and division, body segmentation, and hematopoiesis. While most work on MLL-WRAD has focused on the function this core complex in histone methylation, recent studies indicate that MLL-WRAD proteins interact with a variety of other proteins and lncRNAs and can localize to cellular organelles beyond the nucleus. In this review, we focus on the recently described activities and interacting partners of MLL-WRAD both inside and outside the nucleus.
Key words： H3K4MT; histone H3 lysine 4 methyltransferase; WDR5; RbBP5; ASH2L; DPY-30; SET; MLL; WRAD; Oct4; MYC; cell biology; protein lysine methylation
J. K. Bailey , Dzwokai Ma . Cellular functions of MLL/SET-family histone H3 lysine 4 methyltransferase components[J]. Frontiers in Biology, 2016 , 11(1) : 10 -18 . DOI: 10.1007/s11515-016-1390-6
| 1 |
Ali A, Veeranki S N, Tyagi S (2014). A SET-domain-independent role of WRAD complex in cell-cycle regulatory function of mixed lineage leukemia. Nucleic Acids Res, 42(12): 7611–7624
|
| 2 |
Allis C D, Berger S L, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y (2007). New nomenclature for chromatin-modifying enzymes. Cell, 131(4): 633–636
|
| 3 |
Ang Y S, Tsai S Y, Lee D F, Monk J, Su J, Ratnakumar K, Ding J, Ge Y, Darr H, Chang B, Wang J, Rendl M, Bernstein E, Schaniel C, Lemischka I R (2011). Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell, 145(2): 183–197
|
| 4 |
Bailey J K, Fields A T, Cheng K, Lee A, Wagenaar E, Lagrois R, Schmidt B, Xia B, Ma D (2015). WD repeat-containing protein 5 (WDR5) localizes to the midbody and regulates abscission. J Biol Chem, 290(14): 8987–9001
|
| 5 |
Bannister A J, Kouzarides T (2011). Regulation of chromatin by histone modifications. Cell Res, 21(3): 381–395
|
| 6 |
Bernstein B E, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey D K, Huebert D J, McMahon S, Karlsson E K, Kulbokas E J 3rd, Gingeras T R, Schreiber S L, Lander E S (2005). Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 120(2): 169–181
|
| 7 |
Bledau A S, Schmidt K, Neumann K, Hill U, Ciotta G, Gupta A, Torres D C, Fu J, Kranz A, Stewart A F, Anastassiadis K (2014). The H3K4 methyltransferase Setd1a is first required at the epiblast stage, whereas Setd1b becomes essential after gastrulation. Development, 141(5): 1022–1035
|
| 8 |
Cao F, Chen Y, Cierpicki T, Liu Y, Basrur V, Lei M, Dou Y (2010). An Ash2L/RbBP5 heterodimer stimulates the MLL1 methyltransferase activity through coordinated substrate interactions with the MLL1 SET domain. PLoS ONE, 5(11): e14102
|
| 9 |
Chen X, Xie W, Gu P, Cai Q, Wang B, Xie Y, Dong W, He W, Zhong G, Lin T, Huang J (2015). Upregulated WDR5 promotes proliferation, self-renewal and chemoresistance in bladder cancer via mediating H3K4 trimethylation. Sci Rep, 5: 8293
|
| 10 |
Cheng J, Blum R, Bowman C, Hu D, Shilatifard A, Shen S, Dynlacht B D (2014). A role for H3K4 monomethylation in gene repression and partitioning of chromatin readers. Mol Cell, 53(6): 979–992
|
| 11 |
Cheung P, Allis C D, Sassone-Corsi P (2000). Signaling to chromatin through histone modifications. Cell, 103(2): 263–271
|
| 12 |
Clausell J, Happel N, Hale T K, Doenecke D, Beato M (2009). Histone H1 subtypes differentially modulate chromatin condensation without preventing ATP-dependent remodeling by SWI/SNF or NURF. PLoS ONE, 4(10): e0007243
|
| 13 |
Couture J F, Skiniotis G (2013). Assembling a COMPASS. Epigenetics, 8: 349–354
|
| 14 |
Dai X, Guo W, Zhan C, Liu X, Bai Z, Yang Y (2015). WDR5 expression is prognostic of breast cancer outcome. PLoS ONE, 10(9): e0124964
|
| 15 |
Dias J, Van Nguyen N, Georgiev P, Gaub A, Brettschneider J, Cusack S, Kadlec J, Akhtar A (2014). Structural analysis of the KANSL1/WDR5/KANSL2 complex reveals that WDR5 is required for efficient assembly and chromatin targeting of the NSL complex. Genes Dev, 28(9): 929–942
|
| 16 |
Dou Y, Milne T A, Ruthenburg A J, Lee S, Lee J W, Verdine G L, Allis C D, Roeder R G (2006). Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol, 13(8): 713–719
|
| 17 |
Ernst J, Kheradpour P, Mikkelsen T S, Shoresh N, Ward L D, Epstein C B, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein B E (2011). Mapping and analysis of chromatin state dynamics in nine human cell types. Nature, 473(7345): 43–49
|
| 18 |
Ernst P, Vakoc C R (2012). WRAD: enabler of the SET1-family of H3K4 methyltransferases. Brief Funct Genomics, 11(3): 217–226
|
| 19 |
Fang L, Zhang J, Zhang H, Yang X, Jin X, Zhang L, Skalnik D G, Jin Y, Zhang Y, Huang X, Li J, Wong J (2016). H3K4 methyltransferase Set1a is a key Oct4 coactivactor essential for generation of Oct4 positive inner cell mass. Stem Cells, doi: 10.1002/stem.2250
|
| 20 |
Fischle W, Wang Y, Allis C D (2003). Histone and chromatin cross-talk. Curr Opin Cell Biol, 15(2): 172–183
|
| 21 |
Glaser S, Schaft J, Lubitz S, Vintersten K, van der Hoeven F, Tufteland K R, Aasland R, Anastassiadis K, Ang S L, Stewart A F (2006). Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development, 133(8): 1423–1432
|
| 22 |
Gomez J A, Wapinski O L, Yang Y W, Bureau J F, Gopinath S, Monack D M, Chang H Y, Brahic M, Kirkegaard K (2013). The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-g locus. Cell, 152(4): 743–754
|
| 23 |
Gori F, Friedman L G, Demay M B (2006). Wdr5, a WD-40 protein, regulates osteoblast differentiation during embryonic bone development. Dev Biol, 295(2): 498–506
|
| 24 |
Grebien F, Vedadi M, Getlik M, Giambruno R, Grover A, Avellino R, Skucha A, Vittori S, Kuznetsova E, Smil D, Barsyte-Lovejoy D, Li F, Poda G, Schapira M, Wu H, Dong A, Senisterra G, Stukalov A, Huber K V, Schönegger A, Marcellus R, Bilban M, Bock C, Brown P J, Zuber J, Bennett K L, Al-Awar R, Delwel R, Nerlov C, Arrowsmith C H, Superti-Furga G (2015). Pharmacological targeting of the Wdr5-MLL interaction in C/EBPα N-terminal leukemia. Nat Chem Biol, 11(8): 571–578
|
| 25 |
Harshman S W, Young N L, Parthun M R, Freitas M A (2013). H1 histones: current perspectives and challenges. Nucleic Acids Res, 41(21): 9593–9609
|
| 26 |
He X, Chen X, Zhang X, Duan X, Pan T, Hu Q, Zhang Y, Zhong F, Liu J, Zhang H, Luo J, Wu K, Peng G, Luo H, Zhang L, Li X, Zhang H (2015). An Lnc RNA (GAS5)/SnoRNA-derived piRNA induces activation of TRAIL gene by site-specifically recruiting MLL/COMPASS-like complexes. Nucleic Acids Res, 43(7): 3712–3725
|
| 27 |
Herz H M, Mohan M, Garruss A S, Liang K, Takahashi Y H, Mickey K, Voets O, Verrijzer C P, Shilatifard A (2012). Enhancer-associated H3K4 monomethylation by Trithorax-related, the Drosophila homolog of mammalian Mll3/Mll4. Genes Dev, 26(23): 2604–2620
|
| 28 |
Higa L A, Wu M, Ye T, Kobayashi R, Sun H, Zhang H (2006). CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol, 8(11): 1277–1283
|
| 29 |
Hu D, Gao X, Morgan M A, Herz H M, Smith E R, Shilatifard A (2013). The MLL3/MLL4 branches of the COMPASS family function as major histone H3K4 monomethylases at enhancers. Mol Cell Biol, 33(23): 4745–4754
|
| 30 |
Hu D, Gao X, Morgan M A, Herz H M, Smith E R, Shilatifard A (2013). The MLL3/MLL4 branches of the COMPASS family function as major histone H3K4 monomethylases at enhancers. Mol Cell Biol, 33(23): 4745–4754
|
| 31 |
Jenuwein T, Allis C D (2001). Translating the histone code. Science, 293(5532): 1074–1080
|
| 32 |
Jiang D, Gu X, He Y (2009). Establishment of the winter-annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell, 21(6): 1733–1746
|
| 33 |
Jiang D, Kong N C, Gu X, Li Z, He Y (2011). Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet, 7(3): e1001330
|
| 34 |
Jiang H, Shukla A, Wang X, Chen W Y, Bernstein B E, Roeder R G (2011). Role for Dpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains. Cell, 144(4): 513–525
|
| 35 |
Khare S P, Habib F, Sharma R, Gadewal N, Gupta S, Galande S (2012). HIstome—a relational knowledgebase of human histone proteins and histone modifying enzymes. Nucleic Acids Res, 40(Database issue): D337–D342
|
| 36 |
Kornberg R D (1977). Structure of chromatin. Annu Rev Biochem, 46(1): 931–954
|
| 37 |
Latham J A, Chosed R J, Wang S, Dent S Y (2011). Chromatin signaling to kinetochores: transregulation of Dam1 methylation by histone H2B ubiquitination. Cell, 146(5): 709–719
|
| 38 |
Lee J E, Wang C, Xu S, Cho Y W, Wang L, Feng X, Baldridge A, Sartorelli V, Zhuang L, Peng W, Ge K (2013). H3K4 mono- and di-methyltransferase MLL4 is required for enhancer activation during cell differentiation. eLife, 2: e01503
|
| 40 |
Lee J, Saha P K, Yang Q H, Lee S, Park J Y, Suh Y, Lee S K, Chan L, Roeder R G, Lee J W (2008). Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis. Proc Natl Acad Sci USA, 105(49): 19229–19234
|
| 39 |
Li Y, Han J, Zhang Y, Cao F, Liu Z, Li S, Wu J, Hu C, Wang Y, Shuai J, Chen J, Cao L, Li D, Shi P, Tian C, Zhang J, Dou Y, Li G, Chen Y, Lei M (2016). Structural basis for activity regulation of MLL family methyltransferases. Nature, 530: 447–452
|
| 41 |
Liu C, Zhang Y, Hou Y, Shen L, Li Y, Guo W, Xu D, Liu G, Zhao Z, Man K, Pan Y, Wang Z, Chen Y (2015). PAQR3 modulates H3K4 trimethylation by spatial modulation of the regulatory subunits of COMPASS-like complexes in mammalian cells. Biochem J, 467(3): 415–424
|
| 42 |
Luger K, Mäder A W, Richmond R K, Sargent D F, Richmond T J (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389(6648): 251–260
|
| 43 |
Marazzi I, Ho J S Y, Kim J, Manicassamy B, Dewell S, Albrecht R A, Seibert C W, Schaefer U, Jeffrey K L, Prinjha R K, Lee K, García-Sastre A, Roeder R G, Tarakhovsky A (2012). Suppression of the antiviral response by an influenza histone mimic. Nature, 483(7390): 428–433
|
| 44 |
Martin C, Zhang Y (2005). The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol, 6(11): 838–849
|
| 45 |
Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B, Gehrig P, Rutishauser D, Huang D, Caflisch A, Hottiger M O (2010). PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res, 38(19): 6350–6362
|
| 46 |
Miller T, Krogan N J, Dover J, Erdjument-Bromage H, Tempst P, Johnston M, Greenblatt J F, Shilatifard A (2001). COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci USA, 98(23): 12902–12907
|
| 47 |
Ng H H, Robert F, Young R A, Struhl K (2003). Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell, 11(3): 709–719
|
| 48 |
Nogales E, Ramey V H (2009). Structure-function insights into the yeast Dam1 kinetochore complex. J Cell Sci, 122(Pt 21): 3831–3836
|
| 49 |
Odho Z, Southall S M, Wilson J R (2010). Characterization of a novel WDR5-binding site that recruits RbBP5 through a conserved motif to enhance methylation of histone H3 lysine 4 by mixed lineage leukemia protein-1. J Biol Chem, 285(43): 32967–32976
|
| 50 |
Okamura K, Nakai K (2008). Retrotransposition as a source of new promoters. Mol Biol Evol, 25(6): 1231–1238
|
| 51 |
Pashkova N, Gakhar L, Winistorfer S C, Yu L, Ramaswamy S, Piper R C (2010). WD40 repeat propellers define a ubiquitin-binding domain that regulates turnover of F box proteins. Mol Cell, 40(3): 433–443
|
| 52 |
Patel A, Vought V E, Swatkoski S, Viggiano S, Howard B, Dharmarajan V, Monteith K E, Kupakuwana G, Namitz K E, Shinsky S A, Cotter R J, Cosgrove M S (2014). Automethylation activities within the mixed lineage leukemia-1 (MLL1) core complex reveal evidence supporting a “two-active site” model for multiple histone H3 lysine 4 methylation. J Biol Chem, 289(2): 868–884
|
| 53 |
Pokholok D K, Harbison C T, Levine S, Cole M, Hannett N M, Lee T I, Bell G W, Walker K, Rolfe P A, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford D K, Young R A (2005). Genome-wide map of nucleosome acetylation and methylation in yeast. Cell, 122(4): 517–527
|
| 54 |
Qin S, Liu Y, Tempel W, Eram M S, Bian C, Liu K, Senisterra G, Crombet L, Vedadi M, Min J (2014). Structural basis for histone mimicry and hijacking of host proteins by influenza virus protein NS1. Nat Commun, 5: 3952
|
| 55 |
Rea S, Eisenhaber F, O’Carroll D, Strahl B D, Sun Z W, Schmid M, Opravil S, Mechtler K, Ponting C P, Allis C D, Jenuwein T (2000). Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature, 406(6796): 593–599
|
| 56 |
Ruthenburg A J, Allis C D, Wysocka J (2007). Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell, 25(1): 15–30
|
| 57 |
Santos-Rosa H, Schneider R, Bannister A J, Sherriff J, Bernstein B E, Emre N C, Schreiber S L, Mellor J, Kouzarides T (2002). Active genes are tri-methylated at K4 of histone H3. Nature, 419(6905): 407–411
|
| 58 |
Schneider R, Bannister A J, Myers F A, Thorne A W, Crane-Robinson C, Kouzarides T (2004). Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol, 6(1): 73–77
|
| 59 |
Sebastian S, Sreenivas P, Sambasivan R, Cheedipudi S, Kandalla P, Pavlath G K, Dhawan J (2009). MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc Natl Acad Sci USA, 106(12): 4719–4724
|
| 60 |
Shilatifard A (2008). Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr Opin Cell Biol, 20(3): 341–348
|
| 61 |
Shinsky S A, Cosgrove M S (2015). Unique Role of the WD-40 Repeat Protein 5 (WDR5) Subunit within the Mixed Lineage Leukemia 3 (MLL3) Histone Methyltransferase Complex. J Biol Chem, 290(43): 25819–25833
|
| 62 |
Shinsky S A, Hu M, Vought V E, Ng S B, Bamshad M J, Shendure J, Cosgrove M S (2014). A non-active-site SET domain surface crucial for the interaction of MLL1 and the RbBP5/Ash2L heterodimer within MLL family core complexes. J Mol Biol, 426(12): 2283–2299
|
| 64 |
Skarnes W C, Rosen B, West A P, Koutsourakis M, Bushell W, Iyer V, Mujica A O, Thomas M, Harrow J, Cox T, Jackson D, Severin J, Biggs P, Fu J, Nefedov M, de Jong P J, Stewart A F, Bradley A (2011). A conditional knockout resource for the genome-wide study of mouse gene function. Nature, 474(7351): 337–342
|
| 65 |
Southall S M, Wong P S, Odho Z, Roe S M, Wilson J R (2009). Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol Cell, 33(2): 181–191
|
| 66 |
Stoller J Z, Huang L, Tan C C, Huang F, Zhou D D, Yang J, Gelb B D, Epstein J A (2010). Ash2l interacts with Tbx1 and is required during early embryogenesis. Exp Biol Med (Maywood), 235(5): 569–576
|
| 67 |
Takahashi Y H, Westfield G H, Oleskie A N, Trievel R C, Shilatifard A, Skiniotis G (2011). Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proc Natl Acad Sci USA, 108(51): 20526–20531
|
| 68 |
Terranova R, Agherbi H, Boned A, Meresse S, Djabali M (2006). Histone and DNA methylation defects at Hox genes in mice expressing a SET domain-truncated form of Mll. Proc Natl Acad Sci USA, 103(17): 6629–6634
|
| 69 |
Thakur J, Sanyal K (2011). The essentiality of the fungus-specific Dam1 complex is correlated with a one-kinetochore-one-microtubule interaction present throughout the cell cycle, independent of the nature of a centromere. Eukaryot Cell, 10(10): 1295–1305
|
| 70 |
Thoma F, Koller T (1977). Influence of histone H1 on chromatin structure. Cell, 12(1): 101–107
|
| 71 |
Thoma F, Koller T, Klug A (1979). Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol, 83(2 Pt 1): 403–427
|
| 72 |
Thomas L R, Foshage A M, Weissmiller A M, Tansey W P (2015b). The MYC-WDR5 Nexus and Cancer. Cancer Res, 75(19): 4012–4015
|
| 73 |
Thomas L R, Wang Q, Grieb B C, Phan J, Foshage A M, Sun Q, Olejniczak E T, Clark T, Dey S, Lorey S, Alicie B, Howard G C, Cawthon B, Ess K C, Eischen C M, Zhao Z, Fesik S W, Tansey W P (2015a). Interaction with WDR5 promotes target gene recognition and tumorigenesis by MYC. Mol Cell, 58(3): 440–452
|
| 74 |
Trievel R C, Shilatifard A (2009). WDR5, a complexed protein. Nat Struct Mol Biol, 16(7): 678–680
|
| 75 |
Usenovic M, Knight A L, Ray A, Wong V, Brown K R, Caldwell G A, Caldwell K A, Stagljar I, Krainc D (2012). Identification of novel ATP13A2 interactors and their role in α-synuclein misfolding and toxicity. Hum Mol Genet, 21(17): 3785–3794
|
| 76 |
van Nuland R, Smits A H, Pallaki P, Jansen P W, Vermeulen M, Timmers H T (2013). Quantitative dissection and stoichiometry determination of the human SET1/MLL histone methyltransferase complexes. Mol Cell Biol, 33(10): 2067–2077
|
| 77 |
Vinckenbosch N, Dupanloup I, Kaessmann H (2006). Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA, 103(9): 3220–3225
|
| 78 |
Wang K C, Yang Y W, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie B R, Protacio A, Flynn R A, Gupta R A, Wysocka J, Lei M, Dekker J, Helms J A, Chang H Y (2011). A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature, 472(7341): 120–124
|
| 79 |
Wang Y Y, Liu L J, Zhong B, Liu T T, Li Y, Yang Y, Ran Y, Li S, Tien P, Shu H B (2010). WDR5 is essential for assembly of the VISA-associated signaling complex and virus-triggered IRF3 and NF-kappaB activation. Proc Natl Acad Sci USA, 107(2): 815–820
|
| 80 |
Wang Y, Wysocka J, Sayegh J, Lee Y H, Perlin J R, Leonelli L, Sonbuchner L S, McDonald C H, Cook R G, Dou Y, Roeder R G, Clarke S, Stallcup M R, Allis C D, Coonrod S A (2004). Human PAD4 regulates histone arginine methylation levels via demethylimination. Science, 306(5694): 279–283
|
| 81 |
Wu M, Wang P F, Lee J S, Martin-Brown S, Florens L, Washburn M, Shilatifard A (2008). Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS. Mol Cell Biol, 28(24): 7337–7344
|
| 82 |
Xia B, Joubert A, Groves B, Vo K, Ashraf D, Djavaherian D, Awe J, Xiong Y, Cherfils J, Ma D (2010). Modulation of cell adhesion and migration by the histone methyltransferase subunit mDpy-30 and its interacting proteins. PLoS ONE, 5(7): e11771
|
| 83 |
Xu Z, Gong Q, Xia B, Groves B, Zimmermann M, Mugler C, Mu D, Matsumoto B, Seaman M, Ma D (2009). A role of histone H3 lysine 4 methyltransferase components in endosomal trafficking. J Cell Biol, 186(3): 343–353
|
| 84 |
Yagi H, Deguchi K, Aono A, Tani Y, Kishimoto T, Komori T (1998). Growth disturbance in fetal liver hematopoiesis of Mll-mutant mice. Blood, 92(1): 108–117
|
| 85 |
Yang Y W, Flynn R A, Chen Y, Qu K, Wan B, Wang K C, Lei M, Chang H Y (2014). Essential role of lncRNA binding for WDR5 maintenance of active chromatin and embryonic stem cell pluripotency. eLife, 3: e02046
|
| 86 |
Yu B D, Hess J L, Horning S E, Brown G A, Korsmeyer S J (1995). Altered Hox expression and segmental identity in Mll-mutant mice. Nature, 378(6556): 505–508
|
| 87 |
Zhang K, Lin W, Latham J A, Riefler G M, Schumacher J M, Chan C, Tatchell K, Hawke D H, Kobayashi R, Dent S Y (2005). The Set1 methyltransferase opposes Ipl1 aurora kinase functions in chromosome segregation. Cell, 122(5): 723–734
|
| 88 |
Zhang P, Bergamin E, Couture J F (2013). The many facets of MLL1 regulation. Biopolymers, 99(2): 136–145
|
| 89 |
Zhang P, Lee H, Brunzelle J S, Couture J F (2012). The plasticity of WDR5 peptide-binding cleft enables the binding of the SET1 family of histone methyltransferases. Nucleic Acids Res, 40(9): 4237–4246
|
| 90 |
Zhou P, Wang Z, Yuan X, Zhou C, Liu L, Wan X, Zhang F, Ding X, Wang C, Xiong S, Wang Z, Yuan J, Li Q, Zhang Y (2013). Mixed lineage leukemia 5 (MLL5) protein regulates cell cycle progression and E2F1-responsive gene expression via association with host cell factor-1 (HCF-1). J Biol Chem, 288(24): 17532–17543
|
| 91 |
Zhu E D, Demay M B, Gori F (2008). Wdr5 is essential for osteoblast differentiation. J Biol Chem, 283(12): 7361–7367
|
/
| 〈 |
|
〉 |