Tankyrases: Structure, function and therapeutic implications in cancer

Current Pharmaceutical Design

Volumn 20, Issue 41, 2014, Pages 6472-6488

  Haikarainen, Teemu ^a   Krauss, Stefan ^b   Lehtiö, Lari ^a  

^a UNIVERSITY OF OULU   (Finland)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Cancer; Drug design; Enzyme; Inhibitor; Tankyrase; Telomere; Wnt catenin signaling

Indexed keywords

ADENOSINE; ANKYRIN; AXIN; BETA CATENIN; GLUCOSE TRANSPORTER 4; NICOTINAMIDE; TANKYRASE; TANKYRASE INHIBITOR; WNT PROTEIN; ANTINEOPLASTIC AGENT;

ARTICLE; CENTROSOME; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; HUMAN; HYDROXYLATION; NEOPLASM; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TELOMERE; UBIQUITINATION; ANIMAL; CHEMISTRY; ENZYMOLOGY; METABOLISM; NEOPLASMS;

ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; NEOPLASMS; TANKYRASES;

EID: 84911462377     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612820666140630101525     Document Type: Article

References (173)

1. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F. In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 2005; 6: 139.
2. Kleine H, Poreba E, Lesniewicz K, et al Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol Cell 2008; 32: 57-69.
3. Li J, Mahajan A, Tsai M-D. Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry 2006; 45: 15168-78.
4. De Rycker M, Price CM. Tankyrase polymerization is controlled by its sterile alpha motif and poly(ADP-ribose) polymerase domains. Mol Cell Biol 2004; 24: 9802-12.
5. Hsiao SJ, Poitras MF, Cook BD, Liu Y, Smith S. Tankyrase 2 poly(ADP-ribose) polymerase domain-deleted mice exhibit growth defects but have normal telomere length and capping. Mol Cell Biol 2006; 26: 2044-54.
6. Chiang YJ, Nguyen M-L, Gurunathan S, et al. Generation and characterization of telomere length maintenance in tankyrase 2-deficient mice. Mol Cell Biol 2006; 26: 2037-43.
7. Yeh T-YJ, Beiswenger KK, Li P, et al. Hypermetabolism, hy-perphagia, and reduced adiposity in tankyrase-deficient mice. Diabetes 2009; 58: 2476-85.
8. Chiang YJ, Hsiao SJ, Yver D, et al. Tankyrase 1 and tankyrase 2 are essential but redundant for mouse embryonic development. PloS One 2008; 3: e2639.
9. Smith S, Giriat I, Schmitt A, de Lange T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 1998; 282: 1484-7.
10. Smith S, de Lange T. Tankyrase promotes telomere elongation in human cells. Curr Biol 2000; 10: 1299-302.
11. Kim MK, Smith S. Persistent telomere cohesion triggers a prolonged anaphase. Mol Biol Cell 2014; 25: 30-40.
12. Lyons RJ, Deane R, Lynch DK, et al. Identification of a novel human tankyrase through its interaction with the adaptor protein Grb14. J Biol Chem 2001; 276: 17172-80.
13. Chang W, Dynek JN, Smith S. NuMA is a major acceptor of poly(ADP-ribosyl)ation by tankyrase 1 in mitosis. Biochem J 2005; 391: 177-84.
14. Cho-Park PF, Steller H. Proteasome regulation by ADP-ribosylation. Cell 2013; 153: 614-27.
15. Huang S-MA, Mishina YM, Liu S, et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009; 461: 614-20.
16. Leung AKL, Todorova T, Ando Y, Chang P. Poly(ADP-ribose) regulates post-transcriptional gene regulation in the cytoplasm. RNA Biol 2012; 9: 542-8.
17. Scherag A, Dina C, Hinney A, et al. Two new Loci for body-weight regulation identified in a joint analysis of genome-wide association studies for early-onset extreme obesity in French and german study groups. PLoS Genet 2010; 6: e1000916.
18. Guettler S, LaRose J, Petsalaki E, et al. Structural basis and sequence rules for substrate recognition by Tankyrase explain the basis for cherubism disease. Cell 2011; 147: 1340-54.
19. Levaot N, Voytyuk O, Dimitriou I, et al. Loss of Tankyrase-mediated destruction of 3BP2 is the underlying pathogenic mechanism of cherubism. Cell 2011; 147: 1324-39.
20. Li Z, Yamauchi Y, Kamakura M, et al. Herpes simplex virus requires poly(ADP-ribose) polymerase activity for efficient replication and induces extracellular signal-related kinase-dependent phosphorylation and ICP0-dependent nuclear localization of tan-kyrase 1. J Virol 2012; 86: 492-503.
21. Deng Z, Atanasiu C, Zhao K, et al. Inhibition of Epstein-Barr virus OriP function by tankyrase, a telomere-associated poly-ADP ribose polymerase that binds and modifies EBNA1. J Virol 2005; 79: 4640-50.
22. Distler A, Deloch L, Huang J, et al. Inactivation of tankyrases reduces experimental fibrosis by inhibiting canonical Wnt signalling. Ann Rheum Dis 2013; 72: 1575-80.
23. Lau T, Chan E, Callow M, et al. A novel tankyrase small-molecule inhibitor suppresses APC mutation-driven colorectal tumor growth. Cancer Res 2013; 73: 3132-44.
24. Sangu N, Shimosato T, Inoda H, et al. Novel nucleotide mutation leading to a recurrent amino acid alteration in SH3BP2 in a patient with cherubism. Congenit Anom 2013; 53: 166-9.
25. Busch AM, Johnson KC, Stan RV, et al. Evidence for tankyrases as antineoplastic targets in lung cancer. BMC Cancer 2013; 13: 211.
26. Gao J, Zhang J, Long Y, Tian Y, Lu X. Expression of tankyrase 1 in gastric cancer and its correlation with telomerase activity. Pathol Oncol Res 2011; 17: 685-90.
27. Gelmini S, Quattrone S, Malentacchi F, et al. Tankyrase-1 mRNA expression in bladder cancer and paired urine sediment: preliminary experience. Clin Chem Lab Med 2007; 45: 862-6.
28. La Torre D, Conti A, Aguennouz MH, et al. Telomere length modulation in human astroglial brain tumors. PloS One 2013; 8: e64296.
29. Tang B, Wang J, Fang J, et al Expression of TNKS1 is correlated with pathologic grade and Wnt/β-catenin pathway in human astrocytomas. J Clin Neurosci 2012; 19: 139-43.
30. Zhao F, Vermeer B, Lehmann U, et al. Identification of a novel murine pancreatic tumour antigen, which elicits antibody responses in patients with pancreatic carcinoma. Immunology 2009; 128: 134-40.
31. Gelmini S, Poggesi M, Distante V, et al. Tankyrase, a positive regulator of telomere elongation, is over expressed in human breast cancer. Cancer Lett 2004; 216: 81-7.
32. Gelmini S, Poggesi M, Pinzani P, et al. Distribution of Tankyrase-1 mRNA expression in colon cancer and its prospective correlation with progression stage. Oncol Rep 2006; 16: 1261-6.
33. Shebzukhov YV, Lavrik IN, Karbach J, et al. Human tankyrases are aberrantly expressed in colon tumors and contain multiple epitopes that induce humoral and cellular immune responses in cancer patients. Cancer Immunol Immunother 2008; 57: 871-81.
34. McCabe N, Cerone MA, Ohishi T, Seimiya H, Lord CJ, Ashworth A. Targeting Tankyrase 1 as a therapeutic strategy for BRCA-associated cancer. Oncogene 2009; 28: 1465-70.
35. Zhang H, Yang M-H, Zhao J-J, et al. Inhibition of tankyrase 1 in human gastric cancer cells enhances telomere shortening by telom-erase inhibitors. Oncol Rep 2010; 24: 1059-65.
36. Bao R, Christova T, Song S, Angers S, Yan X, Attisano L. Inhibition of tankyrases induces Axin stabilization and blocks Wnt signalling in breast cancer cells. PloS One 2012; 7: e48670.
37. Casás-Selves M, Kim J, Zhang Z, et al. Tankyrase and the canonical Wnt pathway protect lung cancer cells from EGFR inhibition. Cancer Res 2012; 72: 4154-64.
38. Osherovich L. Targeting tankyrase. SciBX Sci.-Bus. Exch. [Internet]. 2013 [cited 2013 Nov 26]; 6. Available from: http://www. nature. com/scibx/journal/v6/n15/full/scibx. 2013. 353. html.
39. Curtin NJ, Szabo C. Therapeutic applications of PARP inhibitors: anticancer therapy and beyond. Mol Aspects Med 2013; 34: 1217-56.
40. Citarelli M, Teotia S, Lamb RS. Evolutionary history of the poly(ADP-ribose) polymerase gene family in eukaryotes. BMC Evol Biol 2010; 10: 308.
41. Lehtiö L, Collins R, van den Berg S, et al. Zinc binding catalytic domain of human tankyrase 1. J Mol Biol 2008; 379: 136-45.
42. Karlberg T, Markova N, Johansson I, et al. Structural basis for the interaction between tankyrase-2 and a potent Wnt-signaling inhibitor. J Med Chem 2010; 53: 5352-5.
43. Meruelo AD, Bowie JU. Identifying polymer-forming SAM domains. Proteins 2009; 74: 1-5.
44. Seimiya H, Smith S. The telomeric poly(ADP-ribose) polymerase, tankyrase 1, contains multiple binding sites for telomeric repeat binding factor 1 (TRF1) and a novel acceptor, 182-kDa tankyrase-binding protein (TAB182). J Biol Chem 2002; 277: 14116-26.
45. Morrone S, Cheng Z, Moon RT, Cong F, Xu W. Crystal structure of a Tankyrase-Axin complex and its implications for Axin turnover and Tankyrase substrate recruitment. Proc Natl Acad Sci USA 2012; 109: 1500-5.
46. Altmeyer M, Messner S, Hassa PO, Fey M, Hottiger MO. Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res 2009; 37: 3723-38.
47. Hottiger MO, Hassa PO, Lüscher B, Schüler H, Koch-Nolte F. Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 2010; 35: 208-19.
48. Ruf A, Mennissier de Murcia J, de Murcia G, Schulz GE. Structure of the catalytic fragment of poly(AD-ribose) polymerase from chicken. Proc Natl Acad Sci USA 1996; 93: 7481-5.
49. Ruf A, Rolli V, de Murcia G, Schulz GE. The mechanism of the elongation and branching reaction of poly(ADP-ribose) polymerase as derived from crystal structures and mutagenesis. J Mol Biol 1998; 278: 57-65.
50. Rippmann JF, Damm K, Schnapp A. Functional characterization of the poly(ADP-ribose) polymerase activity of tankyrase 1, a potential regulator of telomere length. J Mol Biol 2002; 323: 217-24.
51. Mueller-Dieckmann C, Kernstock S, Lisurek M, et al. The structure of human ADP-ribosylhydrolase 3 (ARH3) provides insights into the reversibility of protein ADP-ribosylation. Proc Natl Acad Sci USA 2006; 103: 15026-31.
52. Slade D, Dunstan MS, Barkauskaite E, et al. The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 2011; 477: 616-20.
53. Rosenthal F, Feijs KLH, Frugier E, et al. Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat Struct Mol Biol 2013; 20: 502-7.
54. Sharifi R, Morra R, Appel CD, et al. Deficiency of terminal ADP-ribose protein glycohydrolase TARG1/C6orf130 in neurodegenera-tive disease. EMBO J 2013; 32: 1225-37.
55. Callow MG, Tran H, Phu L, et al. Ubiquitin ligase RNF146 regulates tankyrase and Axin to promote Wnt signaling. PloS One 2011; 6: e22595.
56. Langelier M-F, Ruhl DD, Planck JL, Kraus WL, Pascal JM. The Zn3 domain of human poly(ADP-ribose) polymerase-1 (PARP-1) functions in both DNA-dependent poly(ADP-ribose) synthesis activity and chromatin compaction. J Biol Chem 2010; 285: 18877-87.
57. Langelier M-F, Planck JL, Roy S, Pascal JM. Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science 2012; 336: 728-32.
58. Sbodio JI, Lodish HF, Chi N-W. Tankyrase-2 oligomerizes with tankyrase-1 and binds to both TRF1 (telomere-repeat-binding factor 1) and IRAP (insulin-responsive aminopeptidase). Biochem J 2002; 361: 451-9.
59. Chi NW, Lodish HF. Tankyrase is a golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles. J Biol Chem 2000; 275: 38437-44.
60. Bell CE, Eisenberg D. Crystal structure of diphtheria toxin bound to nicotinamide adenine dinucleotide. Biochemistry 1996; 35: 1137-49.
61. Marsischky GT, Wilson BA, Collier RJ. Role of glutamic acid 988 of human poly-ADP-ribose polymerase in polymer formation. Evidence for active site similarities to the ADP-ribosylating toxins. J Biol Chem 1995; 270: 3247-54.
62. Narwal M, Venkannagari H, Lehtiö L. Structural basis of selective inhibition of human tankyrases. J Med Chem 2012; 55: 1360-7.
63. Haikarainen T, Narwal M, Joensuu P, Lehtiö L. Evaluation and Structural Basis for the Inhibition of Tankyrases by PARP Inhibitors. ACS Med Chem Lett 2014; 5: 18-22.
64. Li H, Fung K-L, Jin D-Y, et al. Solution structures, dynamics, and lipid-binding of the sterile alpha-motif domain of the deleted in liver cancer 2. Proteins 2007; 67: 1154-66.
65. Oberstrass FC, Lee A, Stefl R, Janis M, Chanfreau G, Allain FH-T. Shape-specific recognition in the structure of the Vts1p SAM domain with RNA. Nat Struct Mol Biol 2006; 13: 160-7.
66. Aviv T, Lin Z, Lau S, Rendl LM, Sicheri F, Smibert CA. The RNA-binding SAM domain of Smaug defines a new family of post-transcriptional regulators. Nat Struct Biol 2003; 10: 614-21.
67. Narwal M, Haikarainen T, Fallarero A, Vuorela PM, Lehtiö L. Screening and structural analysis of flavones inhibiting tankyrases. J Med Chem 2013; 56: 3507-17.
68. Narwal M, Koivunen J, Haikarainen T, et al. Discovery of Tan-kyrase Inhibiting Flavones with Increased Potency and Isoenzyme Selectivity. J Med Chem 2013; 56: 7880-9.
69. De Rycker M, Venkatesan RN, Wei C, Price CM. Vertebrate tan-kyrase domain structure and sterile alpha motif (SAM)-mediated multimerization. Biochem J 2003; 372: 87-96.
70. Seimiya H, Muramatsu Y, Smith S, Tsuruo T. Functional subdomain in the ankyrin domain of tankyrase 1 required for poly(ADP-ribosyl)ation of TRF1 and telomere elongation. Mol Cell Biol 2004; 24: 1944-55.
71. Waaler J, Machon O, Tumova L, et al. A novel tankyrase inhibitor decreases canonical Wnt signaling in colon carcinoma cells and reduces tumor growth in conditional APC mutant mice. Cancer Res 2012; 72: 2822-32.
72. Stamos JL, Weis WI. The β-catenin destruction complex. Cold Spring Harb. Perspect Biol 2013; 5: a007898.
73. Voronkov A, Krauss S. Wnt/beta-catenin signaling and small molecule inhibitors. Curr Pharm Des 2013; 19: 634-64.
74. Li VSW, Ng SS, Boersema PJ, et al. Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 2012; 149: 1245-56.
75. Bisht KK, Dudognon C, Chang WG, Sokol ES, Ramirez A, Smith S. GDP-mannose-4, 6-dehydratase is a cytosolic partner of tan-kyrase 1 that inhibits its poly(ADP-ribose) polymerase activity. Mol Cell Biol 2012; 32: 3044-53.
76. Lyakhovich A, Ramirez MJ, Castellanos A, et al. Fanconi anemia protein FANCD2 inhibits TRF1 polyADP-ribosylation through tankyrase1-dependent manner. Genome Integr 2011; 2: 4.
77. Zhang Y, Liu S, Mickanin C, et al. RNF146 is a poly(ADP-ribose)-directed E3 ligase that regulates axin degradation and Wnt signalling. Nat Cell Biol 2011; 13: 623-9.
78. Short B, Preisinger C, Körner R, Kopajtich R, Byron O, Barr FA. A GRASP55-rab2 effector complex linking Golgi structure to membrane traffic. J Cell Biol 2001; 155: 877-83.
79. Sbodio JI, Chi N-W. Identification of a tankyrase-binding motif shared by IRAP, TAB182, and human TRF1 but not mouse TRF1. NuMA contains this RXXPDG motif and is a novel tankyrase partner. J Biol Chem 2002; 277: 31887-92.
80. Deng Z, Lezina L, Chen C-J, Shtivelband S, So W, Lieberman PM. Telomeric proteins regulate episomal maintenance of Epstein-Barr virus origin of plasmid replication. Mol Cell 2002; 9: 493-503.
81. Fuchs U, Rehkamp GF, Slany R, Follo M, Borkhardt A. The formin-binding protein 17, FBP17, binds via a TNKS binding motif to tankyrase, a protein involved in telomere maintenance. FEBS Lett 2003; 554: 10-6.
82. Guo H-L, Zhang C, Liu Q, et al. The Axin/TNKS complex interacts with KIF3A and is required for insulin-stimulated GLUT4 translocation. Cell Res 2012; 22: 1246-57.
83. Bae J, Donigian JR, Hsueh AJW. Tankyrase 1 interacts with Mcl-1 proteins and inhibits their regulation of apoptosis. J Biol Chem 2003; 278: 5195-204.
84. Aravind L. The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem Sci 2001; 26: 273-5.
85. He F, Tsuda K, Takahashi M, et al. Structural insight into the interaction of ADP-ribose with the PARP WWE domains. FEBS Lett 2012; 586: 3858-64.
86. Forst AH, Karlberg T, Herzog N, et al. Recognition of mono-ADP-ribosylated ARTD10 substrates by ARTD8 macrodomains. Structure 2013; 21: 462-75.
87. Grabbe C, Husnjak K, Dikic I. The spatial and temporal organization of ubiquitin networks. Nat Rev Mol Cell Biol 2011; 12: 295-307.
88. Chau V, Tobias JW, Bachmair A, et al. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 1989; 243: 1576-83.
89. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM. Recognition of the polyubiquitin proteolytic signal. EMBO J 2000; 19: 94-102.
90. Feng X, Koh DW. Roles of poly(ADP-ribose) glycohydrolase in DNA damage and apoptosis. Int Rev Cell Mol Biol 2013; 304: 227-81.
91. Dunstan MS, Barkauskaite E, Lafite P, et al. Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase. Nat Com-mun 2012; 3: 878.
92. Barkauskaite E, Brassington A, Tan ES, et al. Visualization of poly(ADP-ribose) bound to PARG reveals inherent balance between exo-and endo-glycohydrolase activities. Nat Commun 2013; 4: 2164.
93. Jankevicius G, Hassler M, Golia B, et al. A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat Struct Mol Biol 2013; 20: 508-14.
94. Moss J, Stanley SJ, Nightingale MS, et al. Molecular and immunological characterization of ADP-ribosylarginine hydrolases. J Biol Chem 1992; 267: 10481-8.
95. Steffen JD, Pascal JM. New players to the field of ADP-ribosylation make the final cut. EMBO J 2013; 32: 1205-7.
96. Kato J, Zhu J, Liu C, et al. ADP-ribosylarginine hydrolase regulates cell proliferation and tumorigenesis. Cancer Res 2011; 71: 5327-35.
97. Ha G-H, Kim H-S, Go H, et al. Tankyrase-1 function at telomeres and during mitosis is regulated by Polo-like kinase-1-mediated phosphorylation. Cell Death Differ 2012; 19: 321-32.
98. Yeh T-YJ, Sbodio JI, Chi N-W. Mitotic phosphorylation of tankyrase, a PARP that promotes spindle assembly, by GSK3. Bio-chem Biophys Res Commun 2006; 350: 574-9.
99. Yang M, Chowdhury R, Ge W, et al. Factor-inhibiting hypoxia-inducible factor (FIH) catalyses the post-translational hydroxyla-tion of histidinyl residues within ankyrin repeat domains. FEBS J 2011; 278: 1086-97.
100. Cockman ME, Webb JD, Kramer HB, Kessler BM, Ratcliffe PJ. Proteomics-based identification of novel factor inhibiting hypoxia-inducible factor (FIH) substrates indicates widespread asparaginyl hydroxylation of ankyrin repeat domain-containing proteins. Mol Cell Proteomics 2009; 8: 535-46.
101. Coleman ML, McDonough MA, Hewitson KS, et al. Asparaginyl hydroxylation of the Notch ankyrin repeat domain by factor inhibiting hypoxia-inducible factor. J Biol Chem 2007; 282: 24027-38.
102. Smith S, de Lange T. Cell cycle dependent localization of the te-lomeric PARP, tankyrase, to nuclear pore complexes and centro-somes. J Cell Sci 1999; 112 (Pt 21): 3649-56.
103. Ozaki Y, Matsui H, Asou H, et al. Poly-ADP ribosylation of Miki by tankyrase-1 promotes centrosome maturation. Mol Cell 2012; 47: 694-706.
104. Yeh T-YJ, Meyer TN, Schwesinger C, Tsun Z-Y, Lee RM, Chi N-W. Tankyrase recruitment to the lateral membrane in polarized epithelial cells: regulation by cell-cell contact and protein poly(ADP-ribosyl)ation. Biochem J 2006; 399: 415-25.
105. Hsiao SJ, Smith S. Tankyrase function at telomeres, spindle poles, and beyond. Biochimie 2008; 90: 83-92.
106. Chang P, Coughlin M, Mitchison TJ. Interaction between Poly(ADP-ribose) and NuMA contributes to mitotic spindle pole assembly. Mol Biol Cell 2009; 20: 4575-85.
107. Kim MK, Dudognon C, Smith S. Tankyrase 1 regulates centrosome function by controlling CPAP stability. EMBO Rep. 2012; 13: 724-32.
108. Lan J, Zhu Y, Xu L, et al. The 68 kDa telomeric repeat binding factor 1 (TRF1) associated protein (TAP68) interacts with and recruits TRF1 to the spindle pole during mitosis. J Biol Chem 2014; doi: 10. 1074/jbc. M113. 526244.
109. Cong F, Varmus H. Nuclear-cytoplasmic shuttling of Axin regulates subcellular localization of beta-catenin. Proc Natl Acad Sci USA 2004; 101: 2882-7.
110. De la Roche M, Ibrahim AEK, Mieszczanek J, Bienz M. LEF1 and B9L shield β-catenin from inactivation by Axin, desensitizing colorectal cancer cells to tankyrase inhibitors. Cancer Res 2014; 74: 1495-505.
111. Parveen N, Hussain MU, Pandith AA, Mudassar S. Diversity of axin in signaling pathways and its relation to colorectal cancer. Med Oncol Northwood Lond Engl 2011; 28 Suppl 1: S259-267.
112. Kim S-M, Choi E-J, Song K-J, et al. Axin localizes to mitotic spindles and centrosomes in mitotic cells. Exp Cell Res 2009; 315: 943-54.
113. Yeh T-YJ, Sbodio JI, Tsun Z-Y, Luo B, Chi N-W. Insulin-stimulated exocytosis of GLUT4 is enhanced by IRAP and its partner tankyrase. Biochem J 2007; 402: 279-90.
114. Tacchelly-Benites O, Wang Z, Yang E, Lee E, Ahmed Y. Toggling a conformational switch in Wnt/β-catenin signaling: regulation of Axin phosphorylation. The phosphorylation state of Axin controls its scaffold function in two Wnt pathway protein complexes. Bioessays 2013; 35: 1063-70.
115. Ring L, Neth P, Weber C, Steffens S, Faussner A. β-Catenin-dependent pathway activation by both promiscuous "canonical" WNT3a-, and specific "noncanonical" WNT4-and WNT5a-FZD receptor combinations with strong differences in LRP5 and LRP6 dependency. Cell Signal 2014; 26: 260-7.
116. Wiechens N, Heinle K, Englmeier L, Schohl A, Fagotto F. Nucleo-cytoplasmic shuttling of Axin, a negative regulator of the Wnt-beta-catenin Pathway. J Biol Chem 2004; 279: 5263-7.
117. Anderson CB, Neufeld KL, White RL. Subcellular distribution of Wnt pathway proteins in normal and neoplastic colon. Proc Natl Acad Sci USA 2002; 99: 8683-8.
118. Salahshor S, Woodgett JR. The links between axin and carcinogenesis. J Clin Pathol 2005; 58: 225-36.
119. Wang Z, Michaud GA, Cheng Z, et al. Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl)ation-dependent ubiquitination. Genes Dev 2012; 26: 235-40.
120. Waaler J, Machon O, von Kries JP, et al. Novel synthetic antagonists of canonical Wnt signaling inhibit colorectal cancer cell growth. Cancer Res 2011; 71: 197-205.
121. Lui TTH, Lacroix C, Ahmed SM, et al. The ubiquitin-specific protease USP34 regulates axin stability and Wnt/β-catenin signaling. Mol Cell Biol 2011; 31: 2053-65.
122. Qian L, Mahaffey JP, Alcorn HL, Anderson KV. Tissue-specific roles of Axin2 in the inhibition and activation of Wnt signaling in the mouse embryo. Proc Natl Acad Sci USA 2011; 108: 8692-7.
123. Powell SM, Zilz N, Beazer-Barclay Y, et al. APC mutations occur early during colorectal tumorigenesis. Nature 1992; 359: 235-7.
124. Jin L-H, Shao Q-J, Luo W, Ye Z-Y, Li Q, Lin S-C. Detection of point mutations of the Axin1 gene in colorectal cancers. Int. J. Cancer J Int Cancer 2003; 107: 696-9.
125. Morin PJ, Sparks AB, Korinek V, et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997; 275: 1787-90.
126. Rajan P, Sudbery IM, Villasevil MEM, et al. Next-generation Sequencing of Advanced Prostate Cancer Treated with Androgen-deprivation Therapy. Eur Urol 2013; doi: 10. 1016/j. eururo. 2013. 08. 011.
127. Tenbaum SP, Ordóñez-Morán P, Puig I, et al. β-catenin confers resistance to PI3K and AKT inhibitors and subverts FOXO3a to promote metastasis in colon cancer. Nat Med 2012; 18: 892-901.
128. Bogan JS. Regulation of glucose transporter translocation in health and diabetes. Annu Rev Biochem 2012; 81: 507-32.
129. McBrayer SK, Cheng JC, Singhal S, Krett NL, Rosen ST, Shan-mugam M. Multiple myeloma exhibits novel dependence on GLUT4, GLUT8, and GLUT11: implications for glucose transporter-directed therapy. Blood 2012; 119: 4686-97.
130. Saveanu L, van Endert P. The role of insulin-regulated aminopepti-dase in MHC class I antigen presentation. Front Immunol 2012; 3: 57.
131. Chang P, Coughlin M, Mitchison TJ. Tankyrase-1 polymerization of poly(ADP-ribose) is required for spindle structure and function. Nat Cell Biol 2005; 7: 1133-9.
132. Boehler C, Gauthier LR, Mortusewicz O, et al. Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc Natl Acad Sci USA 2011; 108: 2783-8.
133. Masutani M, Fujimori H. Poly(ADP-ribosyl)ation in carcinogenesis. Mol Aspects Med 2013; 34: 1202-16.
134. Korzeniewski N, Hohenfellner M, Duensing S. The centrosome as potential target for cancer therapy and prevention. Expert Opin Ther Targets 2013; 17: 43-52.
135. De Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 2005; 19: 2100-10.
136. Dynek JN, Smith S. Resolution of sister telomere association is required for progression through mitosis. Science 2004; 304: 97-100.
137. Canudas S, Houghtaling BR, Kim JY, Dynek JN, Chang WG, Smith S. Protein requirements for sister telomere association in human cells. EMBO J 2007; 26: 4867-78.
138. Mathew CG. Fanconi anaemia genes and susceptibility to cancer. Oncogene 2006; 25: 5875-84.
139. Counter CM, Avilion AA, LeFeuvre CE, et al. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 1992; 11: 1921-9.
140. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science 1994; 266: 2011-5.
141. Dregalla RC, Zhou J, Idate RR, Battaglia CLR, Liber HL, Bailey SM. Regulatory roles of tankyrase 1 at telomeres and in DNA repair: suppression of T-SCE and stabilization of DNA-PKcs. Aging 2010; 2: 691-708.
142. Matsutani N, Yokozaki H, Tahara E, et al. Expression of telomeric repeat binding factor 1 and 2 and TRF1-interacting nuclear protein 2 in human gastric carcinomas. Int J Oncol 2001; 19: 507-12.
143. Shervington A, Patel R, Lu C, et al. Telomerase subunits expression variation between biopsy samples and cell lines derived from malignant glioma. Brain Res 2007; 1134: 45-52.
144. Seimiya H. The telomeric PARP, tankyrases, as targets for cancer therapy. Br J Cancer 2006; 94: 341-5.
145. Lu H, Lei Z, Lu Z, et al. Silencing tankyrase and telomerase promotes A549 human lung adenocarcinoma cell apoptosis and inhibits proliferation. Oncol Rep 2013; 30: 1745-52.
146. Levis RW, Ganesan R, Houtchens K, Tolar LA, Sheen FM. Trans-posons in place of telomeric repeats at a Drosophila telomere. Cell 1993; 75: 1083-93.
147. Ohn T, Anderson P. The role of posttranslational modifications in the assembly of stress granules. Wiley Interdiscip Rev RNA 2010; 1: 486-93.
148. Ji Y, Tulin AV. Post-transcriptional regulation by poly(ADP-ribosyl)ation of the RNA-binding proteins. Int J Mol Sci 2013; 14: 16168-83.
149. Leung AKL, Vyas S, Rood JE, Bhutkar A, Sharp PA, Chang P. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol Cell 2011; 42: 489-99.
150. Wessel Stratford E, Daffinrud J, Munthe E, et al. The tankyrase-specific inhibitor JW74 affects cell cycle progression and induces apoptosis and differentiation in osteosarcoma cell lines. Cancer Med 2014; 3: 36-46.
151. Chen B, Dodge ME, Tang W, et al. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 2009; 5: 100-7.
152. Kirby CA, Cheung A, Fazal A, Shultz MD, Stams T. Structure of human tankyrase 1 in complex with small-molecule inhibitors PJ34 and XAV939. Acta Crystallograph Sect F Struct Biol Cryst Com-mun 2012; 68: 115-8.
153. Gunaydin H, Gu Y, Huang X. Novel binding mode of a potent and selective tankyrase inhibitor. PloS One. 2012; 7: e33740.
154. Chuang H-C, Kapuriya N, Kulp SK, Chen C-S, Shapiro CL. Differential anti-proliferative activities of poly(ADP-ribose) polymerase (PARP) inhibitors in triple-negative breast cancer cells. Breast Cancer Res Treat 2012; 134: 649-59.
155. Patel AG, De Lorenzo SB, Flatten KS, Poirier GG, Kaufmann SH. Failure of iniparib to inhibit poly(ADP-Ribose) polymerase in vitro. Clin Cancer Res 2012; 18: 1655-62.
156. Wahlberg E, Karlberg T, Kouznetsova E, et al. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat Biotechnol 2012; 30: 283-8.
157. Haikarainen T, Koivunen J, Narwal M, et al. para-Substituted 2-Phenyl-3, 4-dihydroquinazolin-4-ones As Potent and Selective Tankyrase Inhibitors. ChemMedChem 2013; 8: 1978-85.
158. Nathubhai A, Wood PJ, Lloyd MD, Thompson AS, Threadgill MD. Design and Discovery of 2-Arylquinazolin-4-ones as Potent and Selective Inhibitors of Tankyrases. ACS Med Chem Lett 2013; 4: 1173-7.
159. Shultz MD, Cheung AK, Kirby CA, et al. Identification of NVP-TNKS656: The Use of Structure-Efficiency Relationships To Generate a Highly Potent, Selective, and Orally Active Tankyrase Inhibitor. J Med Chem 2013; 56: 6495-511.
160. Larsson EA, Jansson A, Ng FM, et al. Fragment-based ligand design of novel potent inhibitors of tankyrases. J Med Chem 2013; 56: 4497-508.
161. Shultz MD, Majumdar D, Chin DN, et al. Structure-efficiency relationship of [1, 2, 4]triazol-3-ylamines as novel nicotinamide isosteres that inhibit tankyrases. J Med Chem 2013; 56: 7049-59.
162. Haikarainen T, Venkannagari H, Narwal M, et al. Structural basis and selectivity of tankyrase inhibition by a Wnt signaling inhibitor WIKI4. PloS One 2013; 8: e65404.
163. James RG, Davidson KC, Bosch KA, et al WIKI4, a novel inhibitor of tankyrase and Wnt/ß-catenin signaling. PloS One 2012; 7: e50457.
164. Voronkov A, Holsworth DD, Waaler J, et al. Structural basis and SAR for G007-LK, a lead stage 1, 2, 4-triazole based specific tan-kyrase 1/2 inhibitor. J Med Chem 2013; 56: 3012-23.
165. Bregman H, Chakka N, Guzman-Perez A, et al. Discovery of novel, induced-pocket binding oxazolidinones as potent, selective, and orally bioavailable tankyrase inhibitors. J Med Chem 2013; 56: 4320-42.
166. Bregman H, Gunaydin H, Gu Y, et al. Discovery of a class of novel tankyrase inhibitors that bind to both the nicotinamide pocket and the induced pocket. J Med Chem 2013; 56: 1341-5.
167. Huang H, Guzman-Perez A, Acquaviva L, et al. Structure-Based Design of 2-Aminopyridine Oxazolidinones as Potent and Selective Tankyrase Inhibitors. ACS Med Chem Lett 2013; 4: 1218-23.
168. Shultz MD, Kirby CA, Stams T, et al. [1, 2, 4]triazol-3-ylsulfanylmethyl-3-phenyl-[1, 2, 4]oxadiazoles: antagonists of the Wnt pathway that inhibit tankyrases 1 and 2 via novel adenosine pocket binding. J Med Chem 2012; 55: 1127-36.
169. Olaparib Enters Phase III Clinical Testing. Cancer Discov. 2013; 3: 1210. doi: 10. 1158/2159-8290. CD-NB2013-141.
170. Jagtap PG, Southan GJ, Baloglu E, et al. The discovery and synthesis of novel adenosine substituted 2, 3-dihydro-1H-isoindol-1-ones: potent inhibitors of poly(ADP-ribose) polymerase-1 (PARP-1). Bioorg Med Chem Lett 2004; 14: 81-5.
171. Gangloff AR, Brown J, de Jong R, et al. Discovery of novel benzo[b][1, 4]oxazin-3(4H)-ones as poly(ADP-ribose)polymerase inhibitors. Bioorg Med Chem Lett 2013; 23: 4501-5.
172. Ye N, Chen C-H, Chen T, et al. Design, synthesis, and biological evaluation of a series of benzo[de][1, 7]naphthyridin-7(8H)-ones bearing a functionalized longer chain appendage as novel PARP1 inhibitors. J Med Chem 2013; 56: 2885-903.
173. Liscio P, Camaioni E, Carotti A, Pellicciari R, Macchiarulo A. From Polypharmacology to Target Specificity: The Case of PARP Inhibitors. Curr Top Med Chem 2013; 13: 2939-54.