1Structural Genomics Consortium, University of Toronto, 101 College Street, Toronto, Ontario M5G 1L7, Canada.
2Department of Physiology, University of Toronto, Toronto, Ontario M5S 1A8, Canada.
Correspondence should be addressed to Jinrong Min: email@example.com
The PWWP domain is a small structural unit that can bind both DNA and histone, hence involved in chromatin targeting. Here we summarize the structural features of the human PWWP domains and highlight their ligand binding ability from a structural view. Their association with biological functions is also discussed.
The PWWP domain is a structural unit of 100-150 amino acids and named after the conserved Pro-Trp-Trp-Pro motif (Stec et al., 1998; Stec et al., 2000). It is found throughout eukaryotes, ranging from unicellular organisms to human. There are more than 20 PWWP domain containing proteins in the human genome, most of which are chromatin associated. Moreover, the PWWP domain is often found to coexist with other chromatin-associated domains, such as the PHD domain and Bromodomain, in a single polypeptide. More and more studies are revealing the involvement of the PWWP domain in chromatin biology. Here, we will first summarize the structural features of the PWWP domains, then move to their ligand binding ability, and finally discuss their association with biological functions.
The PWWP domain belongs to the Royal superfamily, which also includes chromodomain, Tudor domain, and MBT domain (Maurer-Stroh et al., 2003). The Royal superfamily shares a common structural feature, i.e., an antiparallel β-barrel-like structure formed by 3-5 β-strands. For PWWP domains, the β-barrel is consisted with 5 antiparallel β-strands (β1-β5). The linker between β2 and β3 may also contain additional secondary elements. The unique feature of the PWWP domain is the presence of a α-bundle of 1-6 α-helixes following the β-barrel (Wu et al., 2011). This α-bundle region is very variable and diverse at both the sequence and structural levels. Therefore, only the β-barrel part of the PWWP domain could be reliably predicted in protein domain databases, such as SMART and Human Protein Reference Database. The conserved Pro-Trp-Trp-Pro motif is located at the beginning of the β2 strand and it is packed against the α-bundle, indicating its critical roles in protein folding and stability. Generally speaking, the PWWP domain can fold as an independent functional unit. However, recent studies reveal that the PWWP domain of ZMYND11 (also known as BS69) functions together with the preceding Bromodomain and zinc finger as an integral functional module (Wang et al., 2014; Wen et al., 2014).
DNA binding ability of the PWWP domain
The first three-dimensional structure of a PWWP domain was determined for the mouse DNA methyltransferase Dnmt3b (Qiu et al., 2002). Structural analysis of this PWWP domain revealed a prominent positively charged surface, suggesting a potential role in DNA binding (Qiu et al., 2002). Moreover, it is a common feature that the PWWP domain is rich in lysine and arginine residues and has a predicted pI of more than 9. Indeed, other PWWP domains have been reported to be able to bind DNA, such as HDGF (Lukasik et al., 2006; Yang and Everett, 2007), MSH6 (Laguri et al., 2008), PSIP1 (also known as LEDGF and p75) (Eidahl et al., 2013; van Nuland et al., 2013), and ZMYND11 (Wang et al., 2014). In vitro binding assays revealed that the PWWP domain binds DNA in a nonspecific manner (Qiu et al., 2002; Lukasik et al., 2006; Laguri et al., 2008).
To date, no structure of a PWWP-DNA complex is available in protein structure database. Facilitated by NMR chemical shift perturbation experiments, several groups tried to map the DNA binding site on different PWWP domains (HDGF (Lukasik et al., 2006), MSH6 (Laguri et al., 2008), and PSIP1 (Eidahl et al., 2013; van Nuland et al., 2013)). Notably, the perturbed residues are consistently localized on one side of the protein, centering on the β1-β2 arch region and the PWWP motif, which also overlaps with the patch of highly positively charged surface area.
Histone binding ability of the PWWP domain
The structural similarity of the PWWP domain with other Royal superfamily members, which can recognize methylated lysine and arginine (Adams-Cioaba and Min, 2009), prompted people to propose the PWWP domain as a potential histone "reader" in 2005 (Nameki et al., 2005). Later on, it was demonstrated that the zebrafish Brpf1-PWWP domain can bind histones directly (Laue et al., 2008) and the fission yeast protein Pdp1 can recognize H4K20me specifically (Wang et al., 2009; Qiu et al., 2012). The crystal structure of BRPF1-H3K36me3 complex fully established the notion that the PWWP domain can recognize methylated histone (Vezzoli et al., 2010; Wu et al., 2011). After that, many other PWWP domains were reported to recognize methylated histone peptides, e.g., DNMT3A-H3K36me3 (Dhayalan et al., 2010), PSIP1-H3K36me3 (Pradeepa et al., 2012; Eidahl et al., 2013; van Nuland et al., 2013), MSH6-H3K36me3 (Li et al., 2013), HDGF2-H3K79me3 (Wu et al., 2011), HDGF2-H4K20me3 (Wu et al., 2011), and ZMYND11-H3.3K36me3 (Wen et al., 2014).
Figure 1. Complex structure of BRPF1-PWWP and H3K36me3 (PDB ID: 2X4X). Green: H3K36me3 peptide; magenta: β barrel; cyan: α-bundle; yellow: insertion elements between β2 and β3. Residues of the conserved PWWP motif, aromatic cage and methylated K36 are shown in stick mode.
Structural analysis of these PWWP-histone complex structures identified a conserved cage formed by three aromatic residues for methyl-lysine binding. The third residue (W/Y) of the PWWP motif and the residue (F/Y/W) immediately preceding this motif are involved in forming this cage. Another aromatic residue (F/Y/W) comes from the end of β3 strand (Wu et al., 2011). Sequence alignment reveals that most PWWP domains have this conserved cage for potential methylated-histone binding (Wu et al., 2011). However, several exceptions exist. The PWWP domains of RBBP1, RBBP1L1, MBD5, and NSD1 (N-terminal) have incomplete aromatic cage. RBBP1-PWWP indeed did not show any binding to methylated histone peptides (Gong et al., 2012).
The histone variant H3.3 possesses a signature motif 'S31...A87AIG90' that is distinct from the 'A31...S87AVM90' sequence signature of the canonical histone H3.1/2. The Bromo-Zinc-PWWP cassette of ZMYND11 specifically recognizes H3.3K36me3 (Wen et al., 2014). In addition to the K36me3 recognition by the conserved aromatic cage of PWWP domain, S31 of H3.3 is specifically recognized by the Bromodomain and Zinc finger domains synergistically. Glu251 from the Bromodomain and Asn266 from the Zinc finger form hydrogen bonds with the hydroxyl group of S31.
Nucleosome binding ability of the PWWP domain
The mentioned PWWP-binding sites H3K36, H3K79 and H4K20 are at a close proximity to DNA in nucleosome context. The fact that PWWP domain can bind both DNA and methylated histone suggests a synergy mechanism among these interactions. The binding affinities of PWWP domain towards histone peptide and DNA oligos are relatively too weak. But the affinity of PSIP1-PWWP for methylated nucleosomes (Kd ~1.5 mM) is four orders of magnitude higher than for a methylated peptide (Kd ~17 mM) and two orders higher than for isolated DNA (Kd ~150 mM) (van Nuland et al., 2013). In another study, similar trend was observed for PSIP1: H3KC36me3 nucleosome (Kd ~48 nM), H3K36me3 peptide (Kd >6.5 mM), and DNA (Kd ~1.5 mM) (Eidahl et al., 2013). Studies on ZMYND11 (Wen et al., 2014) and fission yeast Pdp1 (Qiu et al., 2012) show that a synergy was not detected in vitro assays using histone peptides and DNA oligos, so it is likely that the synergy between histone and DNA may contribute only at the nucleosomal level.
Strikingly, in all the available histone-PWWP complex structures, the histone peptides bind to PWWP domains in a similar orientation, that is, the peptides is almost perpendicular to the β4 strand. Further comparing the DNA binding surface identified by NMR and the histone binding mode suggests that PWWP domains may bind to nucleosome through a conserved mode, i.e., the PWWP domains adopt distinct and conserved interfaces to engage histone and DNA, respectively.
Functional roles of PWWP domain containing proteins
Although the PWWP domains mainly function as chromatin interactors and recognize H3K36me3 mark, they are involved in diverse biological processes, depending on the protein context they settled.
The first class of PWWP domain containing proteins is directly involved in modifying chromatin. DNMT3A/B are the de novo DNA methyltransferases responsible for the establishment of DNA methylation patterns during development (Chédin, 2011). The interaction of the PWWP domain with H3K36me3 is involved in targeting of DNMT3A to chromatin and guides DNA methylation (Dhayalan et al., 2010). Disruption of the PWWP domain abolishes the ability of DNMT3A and DNMT3B to methylate the major satellite repeats at pericentric heterochromatin (Chen et al., 2004; Ge et al., 2004). NSD1/2/3 are histone mono- and di-methylases for H3K36 (Wagner and Carpenter, 2012). Histone-modifying enzymes often contain "Reader" domains to bind their product to propagate the resultant mark along the chromatin. Indeed, the N-terminal PWWP domains of NSD2/NSD3 are able to recognize H3K36me2/3 in vitro (Wu et al., 2011). GLYR1 (also known as N-PAC), was found to be a cofactor of H3K4 demethylase LSD2, and GLYR1 positively regulates the H3K4 demethylase activity (Fang et al., 2013). BRPF1/2/3 are scaffold proteins of the MOZ/MORF histone acetyltransferase complexes (Ullah et al., 2008). Brpf1 is required for histone acetylation, the maintenance of cranial Hox gene expression, and the proper determination of pharyngeal segmental identities during development of zebrafish (Laue et al., 2008) and medaka fish (Hibiya et al., 2009). PWWP domains of BRPF1/2 are able to recognize H3K36me3 (Vezzoli et al., 2010; Wu et al., 2011), a mark present in transcribed Hox genes (Wang et al., 2007), consistent with BRPF1's crucial role in promoting the expression of these genes.
The second class of PWWP domain containing proteins is involved in DNA repair. MSH6 binds to H3K36me3 mark in a PWWP-dependent manner and this interaction mediates MutSa (one of the two DNA-mispair recognizing complexes) association with chromatin in cells (Li et al., 2013), hence contributing to DNA mismatch repair. MUM1 (also known as EXPAND1) contributes to the chromatin architecture and, via its direct interaction with the DNA damage mediator 53BP1, plays an accessory role to facilitate damage-induced chromatin changes and is important for efficient DNA repair and cell survival following DNA damage (Huen et al., 2010). In vivo chromatin association of MUM1 relies on its PWWP domain-mediated binding to nucleosomes, and in vitro assays revealed its preference of H3K36me3 (Wu et al., 2011). PSIP1 promotes the repair of double strand breaks (DSBs) by the homologous recombination repair pathway (Daugaard et al., 2012). PSIP1 is constitutively associated with chromatin through its PWWP domain that binds preferentially to methyl-lysine histone markers characteristic of active transcription units (probably H3K36me3). It also binds CtIP in a DNA damage-dependent manner, thereby enhancing its tethering to the active chromatin and facilitating its access to DNA DSBs.
ZMYND11 was originally identified as an adenovirus E1A-binding protein that inhibits the transactivation function of E1A (Hateboer et al., 1995). It also functions as a co-repressor of cellular transcription factors including the c-Myb (Ladendorff et al., 2001) and interacts with a set of chromatin remodeling factors, including ATP-dependent helicases, histone deacetylases, and histone methyltransferases (Velasco et al., 2006). Most recent study reveals that its Bromo-Zinc finger-PWWP cassette specific recognizes the histone variant H3.3K36me3 and regulates transcription elongation (Venkatesh and Workman, 2014; Wen et al., 2014). Although ZMYND11 is associated with highly expressed genes, it functions as an unconventional transcription co-repressor by modulating RNA polymerase II at the elongation stage. Overexpression of ZMYND11 suppresses cancer cell growth in vitro and tumour formation in mice (Wen et al., 2014).
PSIP1 was first isolated as an transcriptional co-activator (Ge et al., 1998a) and it associates with transcriptional activators and components of the basal transcriptional machinery including RNA pol II subunits (Ge et al., 1998b). It is also an essential subunit of the MLL complex in MLL oncogenic transformations via HOX gene regulation (Yokoyama and Cleary, 2008). PSIP1 short isoform (p52) can interact with splicing factors and contributes to the regulation of alternative splicing. PSIP1 can also interacts with the HIV integrase and directs viral cDNA integration into transcribed genes. Although there are multiple chromatin (DNA) binding domains in PSIP1 protein, the PWWP domain is essential for its in vivo functions, especially due to its recognition of H3K36me3.
It is becoming clear that the PWWP domain functions through its interactions with chromatin with methylated histone mark. However, the structural basis for these interactions in a nucleosome context remains unclear. Given the PWWP domains are often coexist with other chromatin interactors, further studies on their crosstalk are required to understand their biological functions. It is also valuable to consider these interactions in context of the protein/complex they settled. Overall, through binding chromatin, the PWWP domains are engaged in many essential cellular processes.
|BS69, a novel adenovirus E1A-associated protein that inhibits E1A transactivation.|
|Hateboer G, Gennissen A, Ramos YF, Kerkhoven RM, Sonntag-Buck V, Stunnenberg HG, Bernards R.|
|EMBO J. 1995 Jul 3;14(13):3159-69.|
|Isolation of cDNAs encoding novel transcription coactivators p52 and p75 reveals an alternate regulatory mechanism of transcriptional activation.|
|Ge H, Si Y, Roeder RG.|
|EMBO J. 1998a Nov 16;17(22):6723-9.|
|A novel transcriptional coactivator, p52, functionally interacts with the essential splicing factor ASF/SF2.|
|Ge H, Si Y, Wolffe AP.|
|Mol Cell. 1998b Dec;2(6):751-9.|
|WHSC1, a 90 kb SET domain-containing gene, expressed in early development and homologous to a Drosophila dysmorphy gene maps in the Wolf-Hirschhorn syndrome critical region and is fused to IgH in t(4;14) multiple myeloma.|
|Stec I, Wright TJ, van Ommen GJ, de Boer PA, van Haeringen A, Moorman AF, Altherr MR, den Dunnen JT.|
|Hum Mol Genet. 1998 Jul;7(7):1071-82.|
|The PWWP domain: a potential protein-protein interaction domain in nuclear proteins influencing differentiation?|
|Stec I, Nagl SB, van Ommen GJ, den Dunnen JT.|
|FEBS Lett. 2000 May 4;473(1):1-5. (REVIEW)|
|BS69, an adenovirus E1A-associated protein, inhibits the transcriptional activity of c-Myb.|
|Ladendorff NE, Wu S, Lipsick JS.|
|Oncogene. 2001 Jan 4;20(1):125-32.|
|The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds.|
|Qiu C, Sawada K, Zhang X, Cheng X.|
|Nat Struct Biol. 2002 Mar;9(3):217-24.|
|The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains.|
|Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CP.|
|Trends Biochem Sci. 2003 Feb;28(2):69-74.|
|The PWWP domain of Dnmt3a and Dnmt3b is required for directing DNA methylation to the major satellite repeats at pericentric heterochromatin.|
|Chen T, Tsujimoto N, Li E.|
|Mol Cell Biol. 2004 Oct;24(20):9048-58.|
|Chromatin targeting of de novo DNA methyltransferases by the PWWP domain.|
|Ge YZ, Pu MT, Gowher H, Wu HP, Ding JP, Jeltsch A, Xu GL.|
|J Biol Chem. 2004 Jun 11;279(24):25447-54. Epub 2004 Mar 3.|
|Solution structure of the PWWP domain of the hepatoma-derived growth factor family.|
|Nameki N, Tochio N, Koshiba S, Inoue M, Yabuki T, Aoki M, Seki E, Matsuda T, Fujikura Y, Saito M, Ikari M, Watanabe M, Terada T, Shirouzu M, Yoshida M, Hirota H, Tanaka A, Hayashizaki Y, Guntert P, Kigawa T, Yokoyama S.|
|Protein Sci. 2005 Mar;14(3):756-64. Epub 2005 Feb 2.|
|High resolution structure of the HDGF PWWP domain: a potential DNA binding domain.|
|Lukasik SM, Cierpicki T, Borloz M, Grembecka J, Everett A, Bushweller JH.|
|Protein Sci. 2006 Feb;15(2):314-23. Epub 2005 Dec 29.|
|New insights into BS69 functions.|
|Velasco G, Grkovic S, Ansieau S.|
|J Biol Chem. 2006 Jun 16;281(24):16546-50. Epub 2006 Mar 24.|
|NUP98-NSD1 links H3K36 methylation to Hox-A gene activation and leukaemogenesis.|
|Wang GG, Cai L, Pasillas MP, Kamps MP.|
|Nat Cell Biol. 2007 Jul;9(7):804-12. Epub 2007 Jun 24.|
|Hepatoma-derived growth factor binds DNA through the N-terminal PWWP domain.|
|Yang J, Everett AD.|
|BMC Mol Biol. 2007 Oct 31;8:101.|
|Human mismatch repair protein MSH6 contains a PWWP domain that targets double stranded DNA.|
|Laguri C, Duband-Goulet I, Friedrich N, Axt M, Belin P, Callebaut I, Gilquin B, Zinn-Justin S, Couprie J.|
|Biochemistry. 2008 Jun 10;47(23):6199-207. doi: 10.1021/bi7024639. Epub 2008 May 17.|
|The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity.|
|Laue K, Daujat S, Crump JG, Plaster N, Roehl HH; Tubingen 2000 Screen Consortium, Kimmel CB, Schneider R, Hammerschmidt M.|
|Development. 2008 Jun;135(11):1935-46. doi: 10.1242/dev.017160.|
|Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes.|
|Ullah M, Pelletier N, Xiao L, Zhao SP, Wang K, Degerny C, Tahmasebi S, Cayrou C, Doyon Y, Goh SL, Champagne N, Cote J, Yang XJ.|
|Mol Cell Biol. 2008 Nov;28(22):6828-43. doi: 10.1128/MCB.01297-08. Epub 2008 Sep 15.|
|Menin critically links MLL proteins with LEDGF on cancer-associated target genes.|
|Yokoyama A, Cleary ML.|
|Cancer Cell. 2008 Jul 8;14(1):36-46. doi: 10.1016/j.ccr.2008.05.003.|
|Structure and function of histone methylation binding proteins.|
|Adams-Cioaba MA, Min J.|
|Biochem Cell Biol. 2009 Feb;87(1):93-105. doi: 10.1139/O08-129. (REVIEW)|
|Brpf1, a subunit of the MOZ histone acetyl transferase complex, maintains expression of anterior and posterior Hox genes for proper patterning of craniofacial and caudal skeletons.|
|Hibiya K, Katsumoto T, Kondo T, Kitabayashi I, Kudo A.|
|Dev Biol. 2009 May 15;329(2):176-90. doi: 10.1016/j.ydbio.2009.02.021. Epub 2009 Feb 27.|
|Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein.|
|Wang Y, Reddy B, Thompson J, Wang H, Noma K, Yates JR 3rd, Jia S.|
|Mol Cell. 2009 Feb 27;33(4):428-37. doi: 10.1016/j.molcel.2009.02.002.|
|The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation.|
|Dhayalan A, Rajavelu A, Rathert P, Tamas R, Jurkowska RZ, Ragozin S, Jeltsch A.|
|J Biol Chem. 2010 Aug 20;285(34):26114-20. doi: 10.1074/jbc.M109.089433. Epub 2010 Jun 11.|
|Regulation of chromatin architecture by the PWWP domain-containing DNA damage-responsive factor EXPAND1/MUM1.|
|Huen MS, Huang J, Leung JW, Sy SM, Leung KM, Ching YP, Tsao SW, Chen J.|
|Mol Cell. 2010 Mar 26;37(6):854-64. doi: 10.1016/j.molcel.2009.12.040.|
|Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1.|
|Vezzoli A, Bonadies N, Allen MD, Freund SM, Santiveri CM, Kvinlaug BT, Huntly BJ, Gottgens B, Bycroft M.|
|Nat Struct Mol Biol. 2010 May;17(5):617-9. doi: 10.1038/nsmb.1797. Epub 2010 Apr 18.|
|The DNMT3 family of mammalian de novo DNA methyltransferases.|
|Prog Mol Biol Transl Sci. 2011;101:255-85. doi: 10.1016/B978-0-12-387685-0.00007-X. (REVIEW)|
|Structural and histone binding ability characterizations of human PWWP domains.|
|Wu H, Zeng H, Lam R, Tempel W, Amaya MF, Xu C, Dombrovski L, Qiu W, Wang Y, Min J.|
|PLoS One. 2011;6(6):e18919. doi: 10.1371/journal.pone.0018919. Epub 2011 Jun 20.|
|LEDGF (p75) promotes DNA-end resection and homologous recombination.|
|Daugaard M, Baude A, Fugger K, Povlsen LK, Beck H, Sorensen CS, Petersen NH, Sorensen PH, Lukas C, Bartek J, Lukas J, Rohde M, Jaattela M.|
|Nat Struct Mol Biol. 2012 Aug;19(8):803-10. doi: 10.1038/nsmb.2314. Epub 2012 Jul 8.|
|Structural insight into recognition of methylated histone tails by retinoblastoma-binding protein 1.|
|Gong W, Zhou T, Mo J, Perrett S, Wang J, Feng Y.|
|J Biol Chem. 2012 Mar 9;287(11):8531-40. doi: 10.1074/jbc.M111.299149. Epub 2012 Jan 12.|
|Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing.|
|Pradeepa MM, Sutherland HG, Ule J, Grimes GR, Bickmore WA.|
|PLoS Genet. 2012;8(5):e1002717. doi: 10.1371/journal.pgen.1002717. Epub 2012 May 17.|
|Solution structure of the Pdp1 PWWP domain reveals its unique binding sites for methylated H4K20 and DNA.|
|Qiu Y, Zhang W, Zhao C, Wang Y, Wang W, Zhang J, Zhang Z, Li G, Shi Y, Tu X, Wu J.|
|Biochem J. 2012 Mar 15;442(3):527-38. doi: 10.1042/BJ20111885.|
|Understanding the language of Lys36 methylation at histone H3.|
|Wagner EJ, Carpenter PB.|
|Nat Rev Mol Cell Biol. 2012 Jan 23;13(2):115-26. doi: 10.1038/nrm3274. (REVIEW)|
|Structural basis for high-affinity binding of LEDGF PWWP to mononucleosomes.|
|Eidahl JO, Crowe BL, North JA, McKee CJ, Shkriabai N, Feng L, Plumb M, Graham RL, Gorelick RJ, Hess S, Poirier MG, Foster MP, Kvaratskhelia M.|
|Nucleic Acids Res. 2013 Apr 1;41(6):3924-36. doi: 10.1093/nar/gkt074. Epub 2013 Feb 8.|
|LSD2/KDM1B and its cofactor NPAC/GLYR1 endow a structural and molecular model for regulation of H3K4 demethylation.|
|Fang R, Chen F, Dong Z, Hu D, Barbera AJ, Clark EA, Fang J, Yang Y, Mei P, Rutenberg M, Li Z, Zhang Y, Xu Y, Yang H, Wang P, Simon MD, Zhou Q, Li J, Marynick MP, Li X, Lu H, Kaiser UB, Kingston RE, Xu Y, Shi YG.|
|Mol Cell. 2013 Feb 7;49(3):558-70. doi: 10.1016/j.molcel.2012.11.019. Epub 2012 Dec 20.|
|The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSa.|
|Li F, Mao G, Tong D, Huang J, Gu L, Yang W, Li GM.|
|Cell. 2013 Apr 25;153(3):590-600. doi: 10.1016/j.cell.2013.03.025.|
|Nucleosomal DNA binding drives the recognition of H3K36-methylated nucleosomes by the PSIP1-PWWP domain.|
|van Nuland R, van Schaik FM, Simonis M, van Heesch S, Cuppen E, Boelens R, Timmers HM, van Ingen H.|
|Epigenetics Chromatin. 2013 May 8;6(1):12. doi: 10.1186/1756-8935-6-12.|
|Recognizing methylated histone variant H3.3 to prevent tumors.|
|Venkatesh S, Workman JL.|
|Cell Res. 2014 Jun;24(6):649-50. doi: 10.1038/cr.2014.50. Epub 2014 Apr 15.|
|Crystal structure of human BS69 Bromo-ZnF-PWWP reveals its role in H3K36me3 nucleosome binding.|
|Wang J, Qin S, Li F, Li S, Zhang W, Peng J, Zhang Z, Gong Q, Wu J, Shi Y.|
|Cell Res. 2014 Jul;24(7):890-3. doi: 10.1038/cr.2014.38. Epub 2014 Mar 28.|
|ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression.|
|Wen H, Li Y, Xi Y, Jiang S, Stratton S, Peng D, Tanaka K, Ren Y, Xia Z, Wu J, Li B, Barton MC, Li W, Li H, Shi X.|
|Nature. 2014 Apr 10;508(7495):263-8. doi: 10.1038/nature13045. Epub 2014 Mar 2.|
|Written||2014-06||Su Qin, Jinrong Min|
|Genomics Consortium, University of Toronto, 101 College Street, Toronto, Ontario M5G 1L7, Canada (SQ, JM); Department of Physiology, University of Toronto, Toronto, Ontario M5S 1A8, Canada (JM)|
|This paper should be referenced as such :|
|S Qin, J Min|
|Insights into structure, function of human PWWP domains.|
|Atlas Genet Cytogenet Oncol Haematol. 2015;19(2):155-159.|
|Free journal version : [ pdf ] [ DOI ]|
|On line version : http://AtlasGeneticsOncology.org/Deep/PWWPDomainsID20137.htm|
|© Atlas of Genetics and Cytogenetics in Oncology and Haematology||indexed on : Tue Mar 14 13:58:10 CET 2017|
For comments and suggestions or contributions, please contact us