Structural basis and selectivity of tankyrase inhibition by a Wnt signaling inhibitor WIKI4 - PubMed (original) (raw)
Structural basis and selectivity of tankyrase inhibition by a Wnt signaling inhibitor WIKI4
Teemu Haikarainen et al. PLoS One. 2013.
Abstract
Recently a novel inhibitor of Wnt signaling was discovered. The compound, WIKI4, was found to act through tankyrase inhibition and regulate β-catenin levels in many cancer cell lines and human embryonic stem cells. Here we confirm that WIKI4 is a high potency tankyrase inhibitor and that it selectively inhibits tankyrases over other ARTD enzymes tested. The binding mode of the compound to tankyrase 2 was determined by protein X-ray crystallography to 2.4 Å resolution. The structure revealed a novel binding mode to the adenosine subsite of the donor NAD(+) binding groove of the catalytic domain. Our results form a structural basis for further development of potent and selective tankyrase inhibitors based on the WIKI4 scaffold.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
Figure 1. Structure of TNKS2 ARTD domain.
Acceptor and donor NAD+ binding sites, including nicotinamide subsite (NI) and adenosine subsite (ADE) are labelled.
Figure 2. Potency of WIKI4 against TNKS1.
The in vitro dose response curves were measured three times with a fluorescence-based homogenous activity assay.
Figure 3. Profiling of inhibitor selectivity.
The selectivity of WIKI4 against 8 ARTDs polymerases was measured at 10 µM concentration. XAV939 and IWR-1 were used as controls.
Figure 4. Binding of WIKI4 to TNKS2.
a) An overview of TNKS2 structure showing the binding site of WIKI4 (lilac) and XAV939 (dark purple) (pdb accession code 3KR8). b) Comparison of apo TNKS2 structure (pink) (pdb accession code 3KR7) and WIKI4 (turquoise) bound structure of TNKS2. c) Surface electrostatic presentation of WIKI4 binding site. Positive (surface potential charge above 0.25 V) and negative (surface potential charge below −0.25 V) electrostatic regions are colored blue and red, respectively.
Figure 5. Interactions of WIKI4 with TNKS2 catalytic domain.
a) Chemical structure of WIKI4. b) Binding mode of WIKI4 to monomer A. c) Binding mode of WIKI4 to monomer B.
Figure 6. Comparison of WIKI4 binding to tankyrase 2 with other tankyrase selective inhibitors and with ARTD1-3 structures.
WIKI4 - TNKS2 protein structure is colored in turquoise and WIKI4 is colored in lilac. a) Comparison of the WIKI4 binding sites in TNKS2, ARTD1 (pink) (pdb accession code 3GJW), ARTD2 (green) (pdb accession code 3KCZ), and ARTD3 (red) (pdb accession code 3FHB). ARD, ARTD regulatory domain. b) Comparison of the binding of WIKI4 and IWR-1. Hydrogen bonds for WIKI4 and IWR-1 are shown in black and gray dotted lines, respectively. IWR-1 - TNKS2 protein structure is colored in pink and IWR-1 is colored in orange. c) Comparison of the binding of WIKI4 and G007-LK. Hydrogen bonds for WIKI4 and G007-LK are shown in black and gray dotted lines, respectively. G007-LK - TNKS2 protein structure is colored in pink and G007-LK is colored in orange.
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References
- Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, Hottiger MO, et al. (2010) Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142: 943–953 doi:10.1016/j.cell.2010.08.016 - DOI - PubMed
- Guettler S, LaRose J, Petsalaki E, Gish G, Scotter A, et al. (2011) Structural basis and sequence rules for substrate recognition by Tankyrase explain the basis for cherubism disease. Cell 147: 1340–1354 doi:10.1016/j.cell.2011.10.046 - DOI - PubMed
- Smith S, Giriat I, Schmitt A, De Lange T (1998) Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282: 1484–1487 doi: 10.1126/science.282.5393.1484. - PubMed
- Sbodio JI, Lodish HF, Chi N-W (2002) Tankyrase-2 oligomerizes with tankyrase-1 and binds to both TRF1 (telomere-repeat-binding factor 1) and IRAP (insulin-responsive aminopeptidase). Biochem J 361: 451–459 doi: 10.1042/0264-6021:3610451 - DOI - PMC - PubMed
- Riffell JL, Lord CJ, Ashworth A (2012) Tankyrase-targeted therapeutics: expanding opportunities in the PARP family. Nat Rev Drug Discov 11: 923–936 doi:10.1038/nrd3868 - DOI - PubMed
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The work was funded by Biocenter Oulu (http://www.oulu.fi/biocenter/) and by Sigrid Jusélius foundation (http://www.sigridjuselius.fi/). MN and HV are members of the National Doctoral Programme of Informational and Structural Biology. The research leading to these results has received funding from the European Community's Seventh Framework Programme (FP7/2007–2013) under BioStruct-X (grant agreement N°283570). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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