Biomedical Science Letters (대한의생명과학회지)

The Korean Society for Biomedical Laboratory Sciences (대한의생명과학회)
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Tankyrase: Function and Tankyrase Inhibitor in Cancer

  • Kim, Mi Kyung (Department of Systems Biology, Yonsei University)
  • Received : 2018.05.28
  • Accepted : 2018.08.24
  • Published : 2018.09.30
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Abstract

Tankyrases are multifunctional poly (ADP-ribose) polymerases that regulate a variety of cellular processes including WNT signaling, telomere maintenance, regulation of mitosis, and many others. Tankyrases interact with target proteins and regulate their interactions and stability through poly (ADP-ribosyl) ation. In addition to their roles in telomere maintenance and regulation of mitosis, tankyrase proteins regulate tumor suppressors such as AXIN, PTEN, and AMOT. Therefore, tankyrases can be effective targets for cancer treatment. Tankyrase inhibitors could affect a variety of pathways that are carcinogenic (essential for the unlimited proliferation of human cancer cells), including WNT, AKT, YAP, telomere maintenance, and regulation of mitosis. Recently, new aspects of the function and mechanism of tankyrases have been reported and several tankyrase inhibitors have been identified. Also, it has been proposed that the combination of conventional chemotherapy agents with tankyrase inhibitors may have synergistic anti-cancer effects. Based on this, it is expected that more advanced and improved tankyrase inhibitors will be developed, enabling new therapeutic strategies against cancer and other tankyrase linked diseases. This review discusses tankyrase function and the role of tankyrase inhibitors in the treatment of cancer.

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References

  1. Arques O, Chicote I, Puig I, Tenbaum SP, Argiles G, Dienstmann R, Fernandez N, Caratu G, Matito J, Silberschmidt D, Rodon J, Landolfi S, Prat A, Espin E, Charco R, Nuciforo P, Vivancos A, Shao W, Tabernero J, Palmer HG. Tankyrase Inhibition Blocks $Wnt/{\beta}$-Catenin Pathway and Reverts Resistance to PI3K and AKT Inhibitors in the Treatment of Colorectal Cancer. Clinical Cancer Research. 2016. 22: 644-656. https://doi.org/10.1158/1078-0432.CCR-14-3081
  2. Bao R, Christova T, Song S, Angers S, Yan X, Attisano L. Inhibition of tankyrases induces Axin stabilization and blocks Wnt signaling in breast cancer cells. PloS One. 2012.7: e48670. https://doi.org/10.1371/journal.pone.0048670
  3. Beneke S, Bürkle A. Poly (ADP-ribosyl) ation in mammalian ageing. Nucleic Acids Research. 2007. 35: 7456-7465. https://doi.org/10.1093/nar/gkm735
  4. Blackburn EH, Gall JG. A tandemly repeated sequence at the termini of the extra chromosomal ribosomal RNA genes in Tetrahymena. Journal of Molecular Biology. 1978. 120: 33-53. https://doi.org/10.1016/0022-2836(78)90294-2
  5. Boveri T. Concerning the origin of malignant tumours by Theodor Boveri. Translated and annotated by Henry Harris. Journal of Cell Science. 2008. 121: 1-84.
  6. Bürkle A. Poly (ADP-ribose). The most elaborate metabolite of $NAD^{+}$. FEBS Journal. 2005. 272: 4576-4589. https://doi.org/10.1111/j.1742-4658.2005.04864.x
  7. Busch AM, Johnson KC, Stan RV, Sanglikar A, Ahmed Y, Dmitrovsky E, Freemantle SJ. Evidence for tankyrases as antineoplastic targets in lung cancer. BMC Cancer. 2013. 13: 211. https://doi.org/10.1186/1471-2407-13-211
  8. Casas-Selves M, Kim J, Zhang Z, Helfrich BA, Gao D, Porter CC, Scarborough HA, Bunn PA Jr, Chan DC, Tan AC, DeGregori J. Tankyrase and the canonical Wnt pathway protect lung cancer cells from EGFR inhibition. Cancer Research. 2012. 72: 4154 -4164. https://doi.org/10.1158/0008-5472.CAN-11-2848
  9. C.G.A. Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012. 487: 330-337. https://doi.org/10.1038/nature11252
  10. Chang P, Coughlin M, Mitchison TJ. Tankyrase-1 polymerization of poly (ADP-ribose) is required for spindle structure and function. Nature Cell Biology. 2005. 7: 1133-1139. https://doi.org/10.1038/ncb1322
  11. Chang W, Dynek JN, Smith S. TRF1 is degraded by ubiquitin- mediated proteolysis after release from telomeres. Genes & Development. 2003. 17: 1328-1333. https://doi.org/10.1101/gad.1077103
  12. Chang W, Dynek JN, Smith S. NuMA is a major acceptor of poly (ADPribosyl) ation by tankyrase 1 in mitosis. Biochemical Journal. 2005. 391: 177-184. https://doi.org/10.1042/BJ20050885
  13. Clevers H. Wnt/ ${\beta}$-catenin signaling in development and disease. Cell. 2006. 127: 469-480. https://doi.org/10.1016/j.cell.2006.10.018
  14. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell. 2007. 130: 1120-1133. https://doi.org/10.1016/j.cell.2007.07.019
  15. Duensing S, Munger K. Centrosome abnormalities, genomic instability and carcinogenic progression. Biochimica et Biophysica Acta . 2001. 2: 81-88.
  16. Ganem NJ, Godinho SA, Pellma D. A mechanism linking extra centrosomes to chromosomal instability. Nature. 2009. 460: 278-282. https://doi.org/10.1038/nature08136
  17. Guerrero AA, Martinez AC, van Wely KH. Merotelic attachments and non-homologous end joining are the basis of chromosomal instability. Cell Division. 2010. 5: 13. https://doi.org/10.1186/1747-1028-5-13
  18. Guettler S, LaRose J, Petsalaki E, Gish G, Scotter A, Pawson T, Rottapel R, Sicheri F. Structural basis and sequence rules for substrate recognition by tankyrase explain the basis for cheru- bism disease. Cell. 2011. 147: 1340-1354. https://doi.org/10.1016/j.cell.2011.10.046
  19. Guo HL, Zhang C, Liu Q, Li Q, Lian G, Wu D, Li X, Zhang W, Shen Y, Ye Z, Lin SY, Lin SC. The Axin/TNKS complex interacts with KIF3A and is required for insulin-stimulated GLUT4 translocation. Cell Research. 2012. 22: 1246-1257. https://doi.org/10.1038/cr.2012.52
  20. Ha GH, Kim HS, Go H, Lee H, Seimiya H, Chung DH, Lee CW. Tankyrase-1 function at telomeres and during mitosis is regulated by Polo-like kinase-1-mediated phosphorylation. Cell death and Differentiation. 2012. 19: 321-332. https://doi.org/10.1038/cdd.2011.101
  21. Haikarainen T, Krauss S, Lehtio L. Tankyrases: structure, function and therapeutic implications in cancer. Current Pharmaceutical Design. 2014. 20: 6472-6488. https://doi.org/10.2174/1381612820666140630101525
  22. Harvey KF, Zhang X, Thomas DM. The Hippo pathway and human cancer. Nature Reviews Cancer. 2013. 13: 246-257. https://doi.org/10.1038/nrc3458
  23. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, Michaud GA, Charlat O, Wiellette E, Zhang Y, Wiessner S, Hild M, Shi X, Wilson CJ, Mickanin C, Myer V, Fazal A, Tomlinson R, Serluca F, Shao W, Cheng H, Shultz M, Rau C, Schirle M, Schlegl J, Ghidelli S, Fawell S, Lu C, Curtis D, Kirschner MW, Lengauer C, Finan PM, Tallarico JA, Bouwmeester T, Porter JA, Bauer A, Cong F. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature. 2009. 461: 614-620. https://doi.org/10.1038/nature08356
  24. Kim MK, Dudognon C, Smith S. Tankyrase 1 regulates centrosome function by controlling CPAP stability. EMBO Reports. 2012. 13: 724-732. https://doi.org/10.1038/embor.2012.86
  25. Kim MK, Smith S. Persistent telomere cohesion triggers a prolonged anaphase. Molecular Biology of the Cell. 2014. 25: 30 -40. https://doi.org/10.1091/mbc.e13-08-0479
  26. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994. 266: 2011-2015. https://doi.org/10.1126/science.7605428
  27. Korzeniewski N, Hohenfellner M, Duensing S. The centrosome as potential target for cancer therapy and prevention. Expert Opinion on Therapeutic Targets. 2013. 17: 43-52. https://doi.org/10.1517/14728222.2013.731396
  28. Kraus W, Lis JT. PARP goes transcription. Cell. 2003. 113: 677 -683. https://doi.org/10.1016/S0092-8674(03)00433-1
  29. Lau T, Chan E, Callow M, Waaler J, Boggs J, Blake RA, Magnuson S, Sambrone A, Schutten M, Firestein R, Machon O, Korinek V, Choo E, Diaz D, Merchant M, Polakis P, Holsworth DD, Krauss S, Costa M. A novel tankyrase small-moleculeinhibitor suppresses APC mutation-driven colorectal tumor growth. Cancer Research. 2013. 73: 3132-3144. https://doi.org/10.1158/0008-5472.CAN-12-4562
  30. Levaot N, Voytyuk O, Dimitriou I, Sircoulomb F, Chandrakumar A, Deckert M, Krzyzanowski PM, Scotter A, Gu S, Janmohamed S, Cong F, Simoncic PD, Ueki Y, La Rose J, Rottapel R. Loss of tankyrase-mediated destruction of 3BP2 is the underlying pathogenic mechanism of cherubism. Cell. 2011. 147: 1324 -1339. https://doi.org/10.1016/j.cell.2011.10.045
  31. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. PTEN, a putative protein tyrosine phosphatase genemutated in human brain, breast, and prostate cancer. Science. 1997. 275: 1943-1947. https://doi.org/10.1126/science.275.5308.1943
  32. Li N, Zhang Y, Han X, Liang K, Wang J, Feng L, Wang W, Songyang Z, Lin C, Yang L, Yu Y, Chen J. Poly-ADP ribosylation of PTEN by tankyrases promotes PTEN degradation and tumor growth. Genes & Development. 2015. 29: 157-170. https://doi.org/10.1101/gad.251785.114
  33. Liaw D, Marsh DJ, Li J, Dahia PL, Wang SI, Zheng Z, Bose S, Call KM, Tsou HC, Peacocke M, Eng C, Parsons R. Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nature Genetics. 1997. 16: 64-67. https://doi.org/10.1038/ng0597-64
  34. Lin L, Sabnis AJ, Chan E, Olivas V, Cade L, Pazarentzos E, Asthana S, Neel D, Yan JJ, Lu X, Pham L, Wang MM, Karachaliou N, Cao MG, Manzano JL, Ramirez JL, Torres JM, Buttitta F, Rudin CM, Collisson EA, Algazi A, Robinson E, Osman I, Munoz-Couselo E, Cortes J, Frederick DT, Cooper ZA, McMahon M, Marchetti A, Rosell R, Flaherty KT, Wargo JA, Bivona TG. The Hippo effector YAP promotes resistance to RAF and MEK-targeted cancer therapies. Nature Genetics. 2015. 47: 250-256. https://doi.org/10.1038/ng.3218
  35. Lu H, Lei Z, Lu Z, Lu Q, Lu C, Chen W, Wang C, Tang Q, Kong Q. Silencing tankyrase and telomerase promotes A549 human lung adenocarcinoma cell apoptosis and inhibits proliferation. Oncology Reports. 2013. 30: 1745-1752. https://doi.org/10.3892/or.2013.2665
  36. Luo X, Kraus WL. On PAR with PARP: cellular stress signaling through poly (ADP-ribose) and PARP-1. Genes & Development. 2012. 26: 417-432. https://doi.org/10.1101/gad.183509.111
  37. Malanga M, Althaus FR. The role of poly (ADP-ribose) in the DNA damage signaling network. Biochemistry and Cell Biology. 2005. 83: 354-364. https://doi.org/10.1139/o05-038
  38. Mo JS, Park HW, Guan KL. The Hippo signaling pathway in stem cell biology and cancer. EMBO Reports. 2014. 15: 642-656.
  39. Nguyen DX, Chiang AC, Zhang XH, Kim JY, Kris MG, Ladanyi M, Gerald WL, Massague J. WNT/TCF Signaling through LEF1 and HOXB9 Mediates Lung Adenocarcinoma Metastasis. Cell. 2009. 138: 51-62. https://doi.org/10.1016/j.cell.2009.04.030
  40. Ozaki Y, Matsui H, Asou H, Nagamach, A, Aki D, Honda H, Yasunaga S, Takihara Y, Yamamoto T, Izumi S, Ohsugi M, Inaba T. Poly-ADP ribosylation of Miki by tankyrase-1 pro- motes centrosome maturation. Molecular Cell. 2012. 47: 694 -706. https://doi.org/10.1016/j.molcel.2012.06.033
  41. Pacheco-Pinedo EC, Durham AC, Stewart KM, Goss AM, Lu MM, Demayo FJ, Morrisey EE. $Wnt/{\beta}$-catenin signaling accelerates mouse lung tumorigenesis by imposing an embryonic distal progenitor phenotype on lung epithelium. Journal of Clinical Investigation. 2011. 121: 1935-1945. https://doi.org/10.1172/JCI44871
  42. Quackenbush KS, Bagby S, Tai WM, Messersmith WA, Schreiber A, Greene J, Kim J, Wang G, Purkey A, Pitts TM, Nguyen A, Gao D, Blatchford P, Capasso A, Schuller AG, Eckhardt SG, Arcaroli JJ. The novel tankyrase inhibitor (AZ1366) enhances irinotecan activity in tumors that exhibit elevated tankyrase and irinotecan resistance. Oncotarget. 2016. 7: 28273-28285.
  43. Riffell JL, Lord CJ, Ashworth A. Tankyrase-targeted therapeutics: expanding opportunities in the PARP family. Nature Reviews Drug Discovery. 2012. 11: 923-936. https://doi.org/10.1038/nrd3868
  44. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science. 1996. 272: 1023 -1026. https://doi.org/10.1126/science.272.5264.1023
  45. Scarborough HA, Helfrich BA, Casás-Selves M, Schuller AG, Grosskurth SE, Kim J, Tan AC, Chan DC, Zhang Z, Zaberezhnyy V, Bunn PA, DeGregori J. AZ1366: An Inhibitor of Tankyrase and the Canonical Wnt Pathway that Limits the Persistence of Non-Small Cell Lung Cancer Cells Following EGFR Inhibition. Clinical Cancer Research. 2017. 23: 1531 -1541. https://doi.org/10.1158/1078-0432.CCR-16-1179
  46. Shay JW, Bacchetti S. A survey of telomerase activity in human cancer. European Journal of Cancer. 1997. 33: 787-791. https://doi.org/10.1016/S0959-8049(97)00062-2
  47. Smith S, de Lange T. Tankyrase promotes telomere elongation in human cells. Current Biology. 2000. 10: 1299-1302. https://doi.org/10.1016/S0960-9822(00)00752-1
  48. Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH, Langford LA, Baumgard ML, Hattier T, Davis T, Frye C, Hu R, Swedlund B, Teng DH, Tavtigian SV. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nature Genetics. 1997. 15: 356-362. https://doi.org/10.1038/ng0497-356
  49. Stratford EW, Daffinrud J, Munthe E, Castro R, Waaler J, Krauss S, Myklebost O. The tankyrase-specific inhibitor JW74 affects cell cycle progression and induces apoptosis and differentiation in osteosarcoma cell lines. Cancer Medicine. 2014. 3: 36-46. https://doi.org/10.1002/cam4.170
  50. Thomson DW, Wagner AJ, Bantscheff M, Benson RE, Dittus L, Duempelfeld B, Drewes G, Krause J, Moore JT, Mueller K, Poeckel D, Rau C, Salzer E, Shewchuk L, Hopf C, Emery JG, Muelbaier M. Discovery of a Highly Selective Tankyrase Inhibitor Displaying Growth Inhibition Effects against a Diverse Range of Tumor Derived Cell Lines. Journal of Medicinal Chemistry. 2017. 60: 5455-5471. https://doi.org/10.1021/acs.jmedchem.7b00137
  51. Tian X, Hou W, Bai S, Fan J, Tong H, Xu H. XAV939 inhibits the stemness and migration of neuroblastoma cancer stem cells via repression of tankyrase 1. International Journal of Oncology. 2014. 45: 121-128. https://doi.org/10.3892/ijo.2014.2406
  52. Waaler J, Machon O, Tumova L, Dinh H, Korinek V, Wilson SR, Paulsen JE, Pedersen NM, Eide TJ, Machonova O, Gradl D, Voronkov A, von Kries JP, Krauss S. A novel tankyrase inhibitor decreases canonical Wnt signaling in colon carcinoma cells and reduces tumor growth in conditional APC mutant mice. Cancer Research. 2012. 72: 2822-2832. https://doi.org/10.1158/0008-5472.CAN-11-3336
  53. Wang H, Lu B, Castillo J, Castillo J, Zhang Y, Yang Z, McAllister G, Lindeman A, Reece-Hoyes J, Tallarico J, Russ C, Hoffman G, Xu W, Schirle M, Cong F. Tankyrase Inhibitor Sensitizes Lung Cancer Cells to Endothelial Growth Factor Receptor (EGFR) Inhibition via Stabilizing Angiomotins and Inhibiting YAP Signaling. Journal of Biological Chemistry. 2016. 291: 15256-15266. https://doi.org/10.1074/jbc.M116.722967
  54. Wang W, Huang J, Chen J. Angiomotin-like proteins associate with and negatively regulate YAP. Journal of Biological Chemistry. 2011. 286: 4364-4370. https://doi.org/10.1074/jbc.C110.205401
  55. Wang W, Li N, Li X, Tran MK, Han X, Chen J. Tankyrase inhibitors Target YAP by Stabilizing Angiomotin Family Proteins. Cell Reports. 2015. 13: 524-532. https://doi.org/10.1016/j.celrep.2015.09.014
  56. Wu X, Luo F, Li J, Zhong X, Liu K. Tankyrase 1 inhibitior XAV939 increases chemosensitivity in colon cancer cell lines via inhibition of the Wnt signaling pathway. International Journal of Oncology. 2016. 48: 1333-1340. https://doi.org/10.3892/ijo.2016.3360
  57. Yeh, TY, Sbodio JI, Tsun ZY, Luo B, Chi NW. Insulin-stimulated exocytosis of GLUT4 is enhanced by IRAP and its partner tankyrase. Biochemical Journal. 2007. 402: 279-290. https://doi.org/10.1042/BJ20060793
  58. Zhang H, Yang MH, Zhao JJ, Chen L, Yu ST, Tang XD, Fang DC, Yang SM. Inhibition of tankyrase 1 in human gastric cancer cells enhances telomere shortening by telomerase inhibitors. Oncology Reports. 2010. 24: 1059-1065.