Putative tumor suppression function of SIRT6 in endometrial cancer

FEBS Letters

Volumn 589, Issue 17, 2015, Pages 2274-2281

  Fukuda, Tomohiko ^a   Wada Hiraike, Osamu ^a   Oda, Katsutoshi ^a   Tanikawa, Michihiro ^a   Makii, Chinami ^a   Inaba, Kanako ^a   Miyasaka, Aki ^a   Miyamoto, Yuichiro ^a   Yano, Tetsu ^b   Maeda, Daichi ^a   Sasaki, Takeshi ^a   Kawana, Kei ^a   Fukayama, Masashi ^a   Osuga, Yutaka ^a   Fujii, Tomoyuki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

Author keywords

Apoptosis; Endometrial cancer; SIRT6; Survivin; YM155

Indexed keywords

SEPANTRONIUM BROMIDE; SIRTUIN 6; SURVIVIN; BIRC5 PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; INHIBITOR OF APOPTOSIS PROTEIN; NAPHTHOQUINONE; SIRT6 PROTEIN, HUMAN; SIRTUIN; TUMOR SUPPRESSOR PROTEIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOMETRIAL CANCER CELL LINE; ENDOMETRIUM CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANTAGONISTS AND INHIBITORS; CELL CYCLE; DRUG EFFECTS; ENDOMETRIUM TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; ENDOMETRIAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; INHIBITOR OF APOPTOSIS PROTEINS; KAPLAN-MEIER ESTIMATE; NAPHTHOQUINONES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIRTUINS; TUMOR SUPPRESSOR PROTEINS;

EID: 84938125432     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.06.043     Document Type: Article

References (57)

1. E. Michishita, J.Y. Park, J.M. Burneskis, J.C. Barrett, and I. Horikawa Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins Mol. Biol. Cell 16 2005 4623 4635
2. C. Sebastian, B.M. Zwaans, D.M. Silberman, M. Gymrek, A. Goren, L. Zhong, O. Ram, J. Truelove, A.R. Guimaraes, D. Toiber, C. Cosentino, J.K. Greenson, A.I. MacDonald, L. McGlynn, F. Maxwell, J. Edwards, S. Giacosa, E. Guccione, R. Weissleder, B.E. Bernstein, A. Regev, P.G. Shiels, D.B. Lombard, and R. Mostoslavsky The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism Cell 151 2012 1185 1199
3. L. Zhong, A. D'Urso, D. Toiber, C. Sebastian, R.E. Henry, D.D. Vadysirisack, A. Guimaraes, B. Marinelli, J.D. Wikstrom, T. Nir, C.B. Clish, B. Vaitheesvaran, O. Iliopoulos, I. Kurland, Y. Dor, R. Weissleder, O.S. Shirihai, L.W. Ellisen, J.M. Espinosa, and R. Mostoslavsky The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha Cell 140 2010 280 293
4. T.L. Kawahara, E. Michishita, A.S. Adler, M. Damian, E. Berber, M. Lin, R.A. McCord, K.C. Ongaigui, L.D. Boxer, H.Y. Chang, and K.F. Chua SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span Cell 136 2009 62 74
5. F. Van Gool, M. Galli, C. Gueydan, V. Kruys, P.P. Prevot, A. Bedalov, R. Mostoslavsky, F.W. Alt, T. De Smedt, and O. Leo Intracellular NAD levels regulate tumor necrosis factor protein synthesis in a sirtuin-dependent manner Nat. Med. 15 2009 206 210
6. R. Mostoslavsky, K.F. Chua, D.B. Lombard, W.W. Pang, M.R. Fischer, L. Gellon, P. Liu, G. Mostoslavsky, S. Franco, M.M. Murphy, K.D. Mills, P. Patel, J.T. Hsu, A.L. Hong, E. Ford, H.L. Cheng, C. Kennedy, N. Nunez, R. Bronson, D. Frendewey, W. Auerbach, D. Valenzuela, M. Karow, M.O. Hottiger, S. Hursting, J.C. Barrett, L. Guarente, R. Mulligan, B. Demple, G.D. Yancopoulos, and F.W. Alt Genomic instability and aging-like phenotype in the absence of mammalian SIRT6 Cell 124 2006 315 329
7. Y. Kanfi, S. Naiman, G. Amir, V. Peshti, G. Zinman, L. Nahum, Z. Bar-Joseph, and H.Y. Cohen The sirtuin SIRT6 regulates lifespan in male mice Nature 483 2012 218 221
8. E. Michishita, R.A. McCord, E. Berber, M. Kioi, H. Padilla-Nash, M. Damian, P. Cheung, R. Kusumoto, T.L. Kawahara, J.C. Barrett, H.Y. Chang, V.A. Bohr, T. Ried, O. Gozani, and K.F. Chua SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin Nature 452 2008 492 496
9. E. Michishita, R.A. McCord, L.D. Boxer, M.F. Barber, T. Hong, O. Gozani, and K.F. Chua Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6 Cell Cycle 8 2009 2664 2666
10. Z. Mao, C. Hine, X. Tian, M. Van Meter, M. Au, A. Vaidya, A. Seluanov, and V. Gorbunova SIRT6 promotes DNA repair under stress by activating PARP1 Science 332 2011 1443 1446
11. A. Kaidi, B.T. Weinert, C. Choudhary, and S.P. Jackson Human SIRT6 promotes DNA end resection through CtIP deacetylation Science 329 2010 1348 1353
12. R.A. McCord, E. Michishita, T. Hong, E. Berber, L.D. Boxer, R. Kusumoto, S. Guan, X. Shi, O. Gozani, A.L. Burlingame, V.A. Bohr, and K.F. Chua SIRT6 stabilizes DNA-dependent protein kinase at chromatin for DNA double-strand break repair Aging 1 2009 109 121
13. M. Van Meter, M. Kashyap, S. Rezazadeh, A.J. Geneva, T.D. Morello, A. Seluanov, and V. Gorbunova SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age Nat. Commun. 5 2014 5011
14. W.M. Burke, J. Orr, M. Leitao, E. Salom, P. Gehrig, A.B. Olawaiye, M. Brewer, D. Boruta, J. Villella, T. Herzog, and F. Abu Shahin Endometrial cancer: a review and current management strategies: part I Gynecol. Oncol. 134 2014 385 392
15. C. Liao, D. Zhang, C. Mungo, D.A. Tompkins, and A.M. Zeidan Is diabetes mellitus associated with increased incidence and disease-specific mortality in endometrial cancer? a systematic review and meta-analysis of cohort studies Gynecol. Oncol. 135 2014 163 171
16. A.G. Renehan, M. Tyson, M. Egger, R.F. Heller, and M. Zwahlen Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies Lancet 371 2008 569 578
17. N. Mu, Y. Zhu, Y. Wang, H. Zhang, and F. Xue Insulin resistance: a significant risk factor of endometrial cancer Gynecol. Oncol. 125 2012 751 757
18. V.N. Sivalingam, J. Myers, S. Nicholas, A.H. Balen, and E.J. Crosbie Metformin in reproductive health, pregnancy and gynaecological cancer: established and emerging indications Hum. Reprod. Update 20 2014 853 868
19. K. Oda, D. Stokoe, Y. Taketani, and F. McCormick High frequency of coexistent mutations of PIK3CA and PTEN genes in endometrial carcinoma Cancer Res. 65 2005 10669 10673
20. D. Kong, A. Suzuki, T.T. Zou, A. Sakurada, L.W. Kemp, S. Wakatsuki, T. Yokoyama, H. Yamakawa, T. Furukawa, M. Sato, N. Ohuchi, S. Sato, J. Yin, S. Wang, J.M. Abraham, R.F. Souza, K.N. Smolinski, S.J. Meltzer, and A. Horii PTEN1 is frequently mutated in primary endometrial carcinomas Nat. Genet. 17 1997 143 144
21. A.M. Oza, L. Elit, M.S. Tsao, S. Kamel-Reid, J. Biagi, D.M. Provencher, W.H. Gotlieb, P.J. Hoskins, P. Ghatage, K.S. Tonkin, H.J. Mackay, J. Mazurka, J. Sederias, P. Ivy, J.E. Dancey, and E.A. Eisenhauer Phase II study of temsirolimus in women with recurrent or metastatic endometrial cancer: a trial of the NCIC Clinical Trials Group J. Clin. Oncol. 29 2011 3278 3285
22. N. Colombo, D.S. McMeekin, P.E. Schwartz, C. Sessa, P.A. Gehrig, R. Holloway, P. Braly, D. Matei, A. Morosky, P.F. Dodion, M.H. Einstein, and F. Haluska Ridaforolimus as a single agent in advanced endometrial cancer: results of a single-arm, phase 2 trial Br. J. Cancer 108 2013 1021 1026
23. D.D. Sarbassov, D.A. Guertin, S.M. Ali, and D.M. Sabatini Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex Science 307 2005 1098 1101
24. X. Wan, B. Harkavy, N. Shen, P. Grohar, and L.J. Helman Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism Oncogene 26 2007 1932 1940
25. C. Kandoth, N. Schultz, A.D. Cherniack, R. Akbani, Y. Liu, H. Shen, A.G. Robertson, I. Pashtan, R. Shen, C.C. Benz, C. Yau, P.W. Laird, L. Ding, W. Zhang, G.B. Mills, R. Kucherlapati, E.R. Mardis, and D.A. Levine Integrated genomic characterization of endometrial carcinoma Nature 497 2013 67 73
26. N.R. Sundaresan, P. Vasudevan, L. Zhong, G. Kim, S. Samant, V. Parekh, V.B. Pillai, P.V. Ravindra, M. Gupta, V. Jeevanandam, J.M. Cunningham, C.X. Deng, D.B. Lombard, R. Mostoslavsky, and M.P. Gupta The sirtuin SIRT6 blocks IGF-Akt signaling and development of cardiac hypertrophy by targeting c-Jun Nat. Med. 18 2012 1643 1650
27. M. Van Meter, Z. Mao, V. Gorbunova, and A. Seluanov SIRT6 overexpression induces massive apoptosis in cancer cells but not in normal cells Cell Cycle 10 2011 3153 3158
28. Z.G. Zhang, and C.Y. Qin Sirt6 suppresses hepatocellular carcinoma cell growth via inhibiting the extracellular signal regulated kinase signaling pathway Mol. Med. Rep. 9 2014 882 888
29. A. Miyasaka, K. Oda, Y. Ikeda, O. Wada-Hiraike, T. Kashiyama, A. Enomoto, N. Hosoya, T. Koso, T. Fukuda, K. Inaba, K. Sone, Y. Uehara, R. Kurikawa, K. Nagasaka, Y. Matsumoto, T. Arimoto, S. Nakagawa, H. Kuramoto, K. Miyagawa, T. Yano, K. Kawana, Y. Osuga, and T. Fujii Anti-tumor activity of olaparib, a poly (ADP-ribose) polymerase (PARP) inhibitor, in cultured endometrial carcinoma cells BMC Cancer 14 2014 179
30. H. Kuramoto, M. Nishida, T. Morisawa, M. Hamano, H. Hata, Y. Kato, E. Ohno, and T. Iida Establishment and characterization of human endometrial cancer cell lines Ann. NY. Acad. Sci. 622 1991 402 421
31. Y. Mizumoto, S. Kyo, S. Ohno, M. Hashimoto, M. Nakamura, Y. Maida, J. Sakaguchi, M. Takakura, M. Inoue, and T. Kiyono Creation of tumorigenic human endometrial epithelial cells with intact chromosomes by introducing defined genetic elements Oncogene 25 2006 5673 5682
32. T. Kashiyama, K. Oda, Y. Ikeda, Y. Shiose, Y. Hirota, K. Inaba, C. Makii, R. Kurikawa, A. Miyasaka, T. Koso, T. Fukuda, M. Tanikawa, K. Shoji, K. Sone, T. Arimoto, O. Wada-Hiraike, K. Kawana, S. Nakagawa, K. Matsuda, F. McCormick, H. Aburatani, T. Yano, Y. Osuga, and T. Fujii Antitumor activity and induction of TP53-dependent apoptosis toward ovarian clear cell adenocarcinoma by the dual PI3K/mTOR inhibitor DS-7423 PLoS One 9 2014 e87220
33. R.H. Wang, Y. Zheng, H.S. Kim, X. Xu, L. Cao, T. Luhasen, M.H. Lee, C. Xiao, A. Vassilopoulos, W. Chen, K. Gardner, Y.G. Man, M.C. Hung, T. Finkel, and C.X. Deng Interplay among BRCA1, SIRT1, and Survivin during BRCA1-associated tumorigenesis Mol. Cell 32 2008 11 20
34. J.S. Chen, J.C. Liu, L. Shen, K.M. Rau, H.P. Kuo, Y.M. Li, D. Shi, Y.C. Lee, K.J. Chang, and M.C. Hung Cancer-specific activation of the survivin promoter and its potential use in gene therapy Cancer Gene Ther. 11 2004 740 747
35. H. Fu, O. Wada-Hiraike, M. Hirano, Y. Kawamura, A. Sakurabashi, A. Shirane, Y. Morita, W. Isono, H. Oishi, K. Koga, K. Oda, K. Kawana, T. Yano, H. Kurihara, Y. Osuga, and T. Fujii SIRT3 positively regulates the expression of folliculogenesis- and luteinization-related genes and progesterone secretion by manipulating oxidative stress in human luteinized granulosa cells Endocrinology 155 2014 3079 3087
36. A.W. Tolcher, D.I. Quinn, A. Ferrari, F. Ahmann, G. Giaccone, T. Drake, A. Keating, and J.S. de Bono A phase II study of YM155, a novel small-molecule suppressor of survivin, in castration-resistant taxane-pretreated prostate cancer Ann. Oncol. 23 2012 968 973
37. K.D. Lewis, W. Samlowski, J. Ward, J. Catlett, L. Cranmer, J. Kirkwood, D. Lawson, E. Whitman, and R. Gonzalez A multi-center phase II evaluation of the small molecule survivin suppressor YM155 in patients with unresectable stage III or IV melanoma Invest. New Drugs 29 2011 161 166
38. G. Giaccone, P. Zatloukal, J. Roubec, K. Floor, J. Musil, M. Kuta, R.J. van Klaveren, S. Chaudhary, A. Gunther, and S. Shamsili Multicenter phase II trial of YM155, a small-molecule suppressor of survivin, in patients with advanced, refractory, non-small-cell lung cancer J. Clin. Oncol. 27 2009 4481 4486
39. R.H. Wang, K. Sengupta, C. Li, H.S. Kim, L. Cao, C. Xiao, S. Kim, X. Xu, Y. Zheng, B. Chilton, R. Jia, Z.M. Zheng, E. Appella, X.W. Wang, T. Ried, and C.X. Deng Impaired DNA damage response, genome instability, and tumorigenesis in SIRT1 mutant mice Cancer Cell 14 2008 312 323
40. H. Vaziri, S.K. Dessain, E. Ng Eaton, S.I. Imai, R.A. Frye, T.K. Pandita, L. Guarente, and R.A. Weinberg HSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase Cell 107 2001 149 159
41. Y. Kamata, J. Watanabe, H. Hata, M. Hamano, and H. Kuramoto Quantitative study on the correlation between p53 gene mutation and its expression in endometrial carcinoma cell lines Eur. J. Gynaecol. Oncol. 25 2004 55 60
42. L. Min, Y. Ji, L. Bakiri, Z. Qiu, J. Cen, X. Chen, L. Chen, H. Scheuch, H. Zheng, L. Qin, K. Zatloukal, L. Hui, and E.F. Wagner Liver cancer initiation is controlled by AP-1 through SIRT6-dependent inhibition of survivin Nat. Cell Biol. 14 2012 1203 1211
43. D. Cibula, A. Gompel, A.O. Mueck, C. La Vecchia, P.C. Hannaford, S.O. Skouby, M. Zikan, and L. Dusek Hormonal contraception and risk of cancer Hum. Reprod. Update 16 2010 631 650
44. G. Ambrosini, C. Adida, and D.C. Altieri A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma Nat. Med. 3 1997 917 921
45. D.S. O'Connor, D. Grossman, J. Plescia, F. Li, H. Zhang, A. Villa, S. Tognin, P.C. Marchisio, and D.C. Altieri Regulation of apoptosis at cell division by p34cdc2 phosphorylation of survivin Proc. Natl. Acad. Sci. USA 97 2000 13103 13107
46. T. Dohi, K. Okada, F. Xia, C.E. Wilford, T. Samuel, K. Welsh, H. Marusawa, H. Zou, R. Armstrong, S. Matsuzawa, G.S. Salvesen, J.C. Reed, and D.C. Altieri An IAP-IAP complex inhibits apoptosis J. Biol. Chem. 279 2004 34087 34090
47. Z. Ai, L. Yin, X. Zhou, Y. Zhu, D. Zhu, Y. Yu, and Y. Feng Inhibition of survivin reduces cell proliferation and induces apoptosis in human endometrial cancer Cancer 107 2006 746 756
48. T. Nakahara, A. Kita, K. Yamanaka, M. Mori, N. Amino, M. Takeuchi, F. Tominaga, S. Hatakeyama, I. Kinoyama, A. Matsuhisa, M. Kudoh, and M. Sasamata YM155, a novel small-molecule survivin suppressant, induces regression of established human hormone-refractory prostate tumor xenografts Cancer Res. 67 2007 8014 8021
49. T. Nakahara, A. Kita, K. Yamanaka, M. Mori, N. Amino, M. Takeuchi, F. Tominaga, I. Kinoyama, A. Matsuhisa, M. Kudou, and M. Sasamata Broad spectrum and potent antitumor activities of YM155, a novel small-molecule survivin suppressant, in a wide variety of human cancer cell lines and xenograft models Cancer Sci. 102 2011 614 621
50. B.D. Cheson, N.L. Bartlett, J.M. Vose, A. Lopez-Hernandez, A.L. Seiz, A.T. Keating, S. Shamsili, and K.P. Papadopoulos A phase II study of the survivin suppressant YM155 in patients with refractory diffuse large B-cell lymphoma Cancer 118 2012 3128 3134
51. X. Zhao, W.M. Puszyk, Z. Lu, D. Ostrov, T. George, K. Robertson, and C. Liu Small molecule inhibitor YM155-mediated activation of death receptor 5 is crucial for chemotherapy-induced apoptosis in pancreatic carcinoma Mol. Cancer Ther. 2014
52. H. Tang, H. Shao, C. Yu, and J. Hou Mcl-1 downregulation by YM155 contributes to its synergistic anti-tumor activities with ABT-263 Biochem. Pharmacol. 82 2011 1066 1072
53. R. Lehner, T. Enomoto, J.A. McGregor, L. Shroyer, B.R. Haugen, U. Pugazhenthi, and K.R. Shroyer Correlation of survivin mRNA detection with histologic diagnosis in normal endometrium and endometrial carcinoma Acta Obstet. Gynecol. Scand. 81 2002 162 167
54. A. Brunner, P. Riss, G. Heinze, and H. Brustmann PHH3 and survivin are co-expressed in high-risk endometrial cancer and are prognostic relevant Br. J. Cancer 107 2012 84 90
55. E. Colas, C. Perez, S. Cabrera, N. Pedrola, M. Monge, J. Castellvi, F. Eyzaguirre, J. Gregorio, A. Ruiz, M. Llaurado, M. Rigau, M. Garcia, T. Ertekin, M. Montes, R. Lopez-Lopez, R. Carreras, J. Xercavins, A. Ortega, T. Maes, E. Rosell, A. Doll, M. Abal, J. Reventos, and A. Gil-Moreno Molecular markers of endometrial carcinoma detected in uterine aspirates Int. J. Cancer 129 2011 2435 2444
56. Y. Kanfi, R. Shalman, V. Peshti, S.N. Pilosof, Y.M. Gozlan, K.J. Pearson, B. Lerrer, D. Moazed, J.C. Marine, R. de Cabo, and H.Y. Cohen Regulation of SIRT6 protein levels by nutrient availability FEBS Lett. 582 2008 543 548
57. J.M. Harvey, G.M. Clark, C.K. Osborne, and D.C. Allred Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer J. Clin. Oncol. 17 1999 1474 1481