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PMC0
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10.1016%2Fj.str.2013.12.004
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_:vb27729922 _:vb27729913 _:vb27729898
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_:vb27729898
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n8:Section
dc:title
introduction
n8:contains
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Ubiquitination is required for the strict regulation of a wide range of essential cellular processes, from protein degradation to DNA repair and cell-cycle control (Pickart and Eddins, >>2004<<). Consequently, defects that arise in the regulation of ubiquitination can lead to a variety of diseases, such as cancers and neurodegeneration.
n3:mentions
n2:15571809
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_:vb27729900
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n3:Context
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The E3-E2 pair also dictates the type of modification, ranging from monoubiquitination to Ub polymers (Ye and Rape, >>2009<<). The human genome encodes two E1 enzymes, approximately 40 E2s and over 600 E3 ligases, giving rise to thousands of possible permutations of E3-E2 pairings.
n3:mentions
n2:19851334
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(Bentley et al., 2011; Dou et al., 2012; Huang et al., 1999; Plechanovová et al., 2012; Pruneda et al., 2012; Yin et al., 2009; Zheng et al., >>2000<<). Furthermore, the conservation of the E2 UBC fold, along with the conservation of the hydrophobic residues for the E3-interacting interface, suggests that all E3s could function with all E2s (van Wijk and Timmers, 2010). Yet, this is not
n3:mentions
n2:21772249 n2:22885007 n2:22842904 n2:10966114 n2:10558980 n2:19465916 n2:22902369
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Furthermore, the conservation of the E2 UBC fold, along with the conservation of the hydrophobic residues for the E3-interacting interface, suggests that all E3s could function with all E2s (van Wijk and Timmers, >>2010<<). Yet, this is not what is observed in nature, as there is selectivity in E3-E2 pairs with some pairs being exclusive (Bailly et al., 1994; Chen et al., 2006). There have been great efforts using yeast-two-hybrid screens, computational
n3:mentions
n2:19940261
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_:vb27729903
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n3:Context
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Yet, this is not what is observed in nature, as there is selectivity in E3-E2 pairs with some pairs being exclusive (Bailly et al., 1994; Chen et al., >>2006<<). There have been great efforts using yeast-two-hybrid screens, computational biology, and modeling methods to determine E3-E2 pairs (Kar et al., 2012; Markson et al., 2009; van Wijk et al., 2009). A recent proteome scale modeling study,
n3:mentions
n2:7926769 n2:16407162
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_:vb27729904
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n3:Context
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There have been great efforts using yeast-two-hybrid screens, computational biology, and modeling methods to determine E3-E2 pairs (Kar et al., 2012; Markson et al., 2009; van Wijk et al., >>2009<<). A recent proteome scale modeling study, aimed at identifying determinants of E3-E2 specificity, predicts residues on loop 1 of the E2 to be important for E3 selection (Kar et al., 2012). Additionally, there is much interest in creating
n3:mentions
n2:19549727 n2:22149024 n2:19690564
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_:vb27729905
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A recent proteome scale modeling study, aimed at identifying determinants of E3-E2 specificity, predicts residues on loop 1 of the E2 to be important for E3 selection (Kar et al., >>2012<<). Additionally, there is much interest in creating new E3-E2 pairs or enhancing specificity (Starita et al., 2013; Winkler and Timmers, 2005), both for understanding ubiquitin biology and from a therapeutic perspective. However, these
n3:mentions
n2:22149024
Subject Item
_:vb27729906
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n3:Context
rdf:value
Additionally, there is much interest in creating new E3-E2 pairs or enhancing specificity (Starita et al., 2013; Winkler and Timmers, >>2005<<), both for understanding ubiquitin biology and from a therapeutic perspective.
n3:mentions
n2:16338368 n2:23509263
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An example of an exclusive E3-E2 pair is the catalytic center of the Fanconi Anemia (FA) pathway, FANCL-Ube2T (Alpi et al., 2008; Machida et al., >>2006<<). The FA pathway is required for DNA interstrand crosslink repair.
n3:mentions
n2:19111657 n2:16916645
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n3:Context
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Mutations in the FA pathway result in the genetic disorder known as Fanconi Anemia, where patients have high predispositions to cancers because of their genomic instabilities (Alter, >>1996<<). FANCL is a monomeric RING E3 ligase (Cole et al., 2010; Meetei et al., 2003), which specifically interacts with the E2, Ube2T (Alpi et al., 2008; Machida et al., 2006), for the strict monoubiquitination of FANCD2 (Garcia-Higuera et al.,
n3:mentions
n2:8892734
Subject Item
_:vb27729909
rdf:type
n3:Context
rdf:value
FANCL is a monomeric RING E3 ligase (Cole et al., 2010; Meetei et al., >>2003<<), which specifically interacts with the E2, Ube2T (Alpi et al., 2008; Machida et al., 2006), for the strict monoubiquitination of FANCD2 (Garcia-Higuera et al., 2001; Timmers et al., 2001).
n3:mentions
n2:20154706 n2:12973351
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n3:Context
rdf:value
FANCL is a monomeric RING E3 ligase (Cole et al., 2010; Meetei et al., 2003), which specifically interacts with the E2, Ube2T (Alpi et al., 2008; Machida et al., >>2006<<), for the strict monoubiquitination of FANCD2 (Garcia-Higuera et al., 2001; Timmers et al., 2001).
n3:mentions
n2:19111657 n2:16916645
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E3 ligase (Cole et al., 2010; Meetei et al., 2003), which specifically interacts with the E2, Ube2T (Alpi et al., 2008; Machida et al., 2006), for the strict monoubiquitination of FANCD2 (Garcia-Higuera et al., 2001; Timmers et al., >>2001<<). This monoubiquitination event is key in signaling the recruitment of downstream DNA repair factors (Kottemann and Smogorzewska, 2013).
n3:mentions
n2:11239453 n2:11239454
Subject Item
_:vb27729912
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This monoubiquitination event is key in signaling the recruitment of downstream DNA repair factors (Kottemann and Smogorzewska, >>2013<<).
n3:mentions
n2:23325218
Subject Item
_:vb27729913
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n8:Section
dc:title
results and discussion
n8:contains
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FANCL and Ube2T coelute as a 1:1 stoichiometric complex by size-exclusion chromatography and have an affinity with a dissociation constant (KD) of ∼0.5 μM (Hodson et al., >>2011<<). The complex crystallizes with a diffraction limit of ∼11 Å. In order to obtain high-resolution data to observe the interface, we fused human Ube2T to the C terminus of the human FANCL RING domain with a linker between the proteins.
n3:mentions
n2:21775430
Subject Item
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This unusual arrangement is also noted in the Drosophila FANCL structure (Cole et al., >>2010<<) and is conserved across all other FANCL homologs.
n3:mentions
n2:20154706
Subject Item
_:vb27729916
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rdf:value
In common with other RING domains, FANCL contains the helical element involved in E2 recognition (Figure 1B) (Deshaies and Joazeiro, >>2009<<). In complex with FANCL, Ube2T adopts a typical UBC-fold comprising a four-stranded beta meander, flanked by an N-terminal helix and two C-terminal helices (Figure 1C). In order to determine whether significant conformational changes
n3:mentions
n2:19489725
Subject Item
_:vb27729917
rdf:type
n3:Context
rdf:value
In order to determine whether significant conformational changes occur in Ube2T upon RING binding, we superimposed the bound Ube2T in our structure to unbound Ube2T (Protein Data Bank [PDB] ID code 1YH2) (Sheng et al., >>2012<<). The two structures align with an rmsd of 0.67 Å across all alpha-carbon atoms, indicating that no major structural rearrangements occur upon complex formation (Figure S1B).
n3:mentions
n2:22496338
Subject Item
_:vb27729918
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n3:Context
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and Pro100 of Ube2T and Ile309, Trp341, and Pro360 of FANCL (Figure 1D), as observed in other RING-E2 structures (Bentley et al., 2011; Dou et al., 2012; Plechanovová et al., 2012; Pruneda et al., 2012; Yin et al., 2009; Zheng et al., >>2000<<). However, the hydrophobic surface of FANCL is extended by Tyr311, which is involved in pi stacking between Arg6 and Arg9 (Figure 1D).
n3:mentions
n2:10966114 n2:22885007 n2:22842904 n2:19465916 n2:22902369 n2:21772249
Subject Item
_:vb27729919
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The very promiscuous E2, Ube2D3 (Brzovic and Klevit, >>2006<<) is capable of polyubiquitinating FANCD2 in the absence of FANCL (lane 5, Figure S2C).
n3:mentions
n2:17218787
Subject Item
_:vb27729920
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n3:Context
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These results further support the observed promiscuity of Ube2D3 for lysines (Wenzel et al., >>2011<<).
n3:mentions
n2:21532592
Subject Item
_:vb27729921
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n3:Context
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The residue equivalent to Arg60 in Ube2T is predicted to be important for this distinction in a recent proteome-scale modeling study (Kar et al., >>2012<<). Our study provides experimental support for the importance of this position in a more divergent E2. Arg60 of Ube2T forms a salt bridge with Glu340 of FANCL (Figure 1D). In other E3s, the equivalent residue is poorly conserved (Figure
n3:mentions
n2:22149024
Subject Item
_:vb27729922
rdf:type
n8:Section
dc:title
experimental procedures
n8:contains
_:vb27729932 _:vb27729933 _:vb27729928 _:vb27729929 _:vb27729930 _:vb27729931 _:vb27729924 _:vb27729925 _:vb27729926 _:vb27729927 _:vb27729923
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synthetic human FANCL DNA (GeneArt) codon-optimized for Escherichia coli expression and inserted N terminally to Ube2T encoded in a vector containing a N-terminal 6xHis-Smt3 tag, by restriction-free cloning (RF) (van den Ent and Löwe, >>2006<<). A 14 amino acid (TGSTGSTETGYTQG) linker was inserted between the C-terminal of the RING domain and N-terminal of Ube2T (Pellegrini et al., 2002) by Phusion site-directed mutagenesis.
n3:mentions
n2:16480772
Subject Item
_:vb27729924
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A 14 amino acid (TGSTGSTETGYTQG) linker was inserted between the C-terminal of the RING domain and N-terminal of Ube2T (Pellegrini et al., >>2002<<) by Phusion site-directed mutagenesis.
n3:mentions
n2:12442171
Subject Item
_:vb27729925
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We modified it to contain a N-terminal FLAG tag and prepared it as previously described (Knipscheer et al., >>2009<<).
n3:mentions
n2:19965384
Subject Item
_:vb27729926
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Iwai (Sato et al., >>2008<<). It was expressed in sf9 cells cultured at 27°C in sf-900 serum-free media (GIBCO) supplemented with antibiotics.
n3:mentions
n2:18758443
Subject Item
_:vb27729927
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Data were processed using D∗trek (Pflugrath, >>1999<<), showing diffraction to 2.25 Å resolution.
n3:mentions
n2:10531521
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Phases were generated by molecular replacement using the program Phaser (McCoy et al., >>2007<<) with Ube2T (residues 1–154, PDB ID code 1YH2) and Drosophila FANCL (residues 312–371, 3K1L) (Cole et al., 2010) as search models.
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Phases were generated by molecular replacement using the program Phaser (McCoy et al., 2007) with Ube2T (residues 1–154, PDB ID code 1YH2) and Drosophila FANCL (residues 312–371, 3K1L) (Cole et al., >>2010<<) as search models.
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refine (Afonine et al., >>2005<<) and manual model building using Coot (Emsley and Cowtan, 2004).
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refine (Afonine et al., 2005) and manual model building using Coot (Emsley and Cowtan, >>2004<<). Data were cut off to 2.4 Å resolution, and the last 400 images were omitted because of radiation damage. Omit maps were generated to check for model bias. The final model’s stereochemistry and geometry was checked with MolProbity (Davis
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The final model’s stereochemistry and geometry was checked with MolProbity (Davis et al., >>2004<<) analysis (Table 1) and for favored regions of the Ramachandran plot (97.52%).
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Interactions between RING domains and E2s were assessed by analytical size-exclusion chromatography, as described previously (Hodson et al., >>2011<<). Briefly, interactions were incubated in buffer containing 0.1 M NaCl, 0.1 M Tris (pH 8), and 250 μM TCEP in a total volume of 500 μl and left on ice for 1 hr.
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