Transcriptional repressor DAXX promotes prostate cancer tumorigenicity via suppression of autophagy

Journal of Biological Chemistry

Volumn 290, Issue 25, 2015, Pages 15406-15420

  Lorena, A Puto ^a   John, Brognard ^b   Tony, Hunter ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; GENES; PROTEINS; TUMORS; UROLOGY;

APOPTOTIC CELL DEATH; CANCER BIOMARKERS; GROWTH ENHANCING EFFECTS; MALIGNANT TRANSFORMATIONS; PANCREATIC CANCERS; THERAPEUTIC MODALITY; TRANSCRIPTIONAL REPRESSORS; TUMOR SUPPRESSOR GENES;

DISEASES;

DAPK1 PROTEIN; DAPK3 PROTEIN; DAXX PROTEIN; SHORT HAIRPIN RNA; TUMOR SUPPRESSOR PROTEIN; ULK1 PROTEIN; UNCLASSIFIED DRUG; DAPK3 PROTEIN, HUMAN; DAXX PROTEIN, HUMAN; DEATH ASSOCIATED PROTEIN KINASE; NUCLEAR PROTEIN; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN; SERINE THREONINE PROTEIN KINASE ULK1; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR MARKER; ULK1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CANCER GROWTH; CARCINOGENICITY; CONTROLLED STUDY; DAPK1 GENE; DAPK3 GENE; DAXX GENE; DISEASE MARKER; FACTUAL DATABASE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; TUMOR PROMOTION; TUMOR XENOGRAFT; ANIMAL; BIOSYNTHESIS; CANCER TRANSPLANTATION; GENE SILENCING; GENETICS; METABOLISM; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE; XENOGRAFT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN-1 HOMOLOG; BIOMARKERS, TUMOR; CELL LINE, TUMOR; DEATH-ASSOCIATED PROTEIN KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; PANCREATIC NEOPLASMS; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; TUMOR SUPPRESSOR PROTEINS;

EID: 84940056415     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.658765     Document Type: Article

References (60)

1. Yang, X., Khosravi-Far, R., Chang, H. Y., and Baltimore, D. (1997) Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell 89, 1067-1076
2. Puto, L. A., and Reed, J. C. (2008) Daxx represses RelB target promoters via DNA methyltransferase recruitment and DNA hypermethylation. Genes Dev. 22, 998-1010
3. Lewis, P. W., Elsaesser, S. J., Noh, K. M., Stadler, S. C., and Allis, C. D. (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. 107, 14075-14080
4. Zalckvar, E., Berissi, H., Eisenstein, M., and Kimchi, A. (2009) Phosphorylation of Beclin 1 by DAP-kinase promotes autophagy by weakening its interactions with Bcl-2 and Bcl-XL. Autophagy 5, 720-722
5. Tang, H. W., Wang, Y. B., Wang, S. L., Wu, M. H., Lin, S. Y., and Chen, G. C. (2011) Atg1-mediated myosin II activation regulates autophagosome formation during starvation-induced autophagy. EMBO J. 30, 636-651
6. Michaelson, J. S., Bader, D., Kuo, F., Kozak, C., and Leder, P. (1999) Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development. Genes Dev. 13, 1918-1923
7. Kwan, P. S., Lau, C. C., Chiu, Y. T., Man, C., Liu, J., Tang, K. D., Wong, Y. C., and Ling, M. T. (2013) Daxx regulates mitotic progression and prostate cancer predisposition. Carcinogenesis 34, 750-759
8. Tsourlakis, M. C., Schoop, M., Plass, C., Huland, H., Graefen, M., Steuber, T., Schlomm, T., Simon, R., Sauter, G., Sirma, H., and Minner, S. (2013) Overexpression of the chromatin remodeler death-domain-associated protein in prostate cancer is an independent predictor of early prostate-specific antigen recurrence. Hum. Pathol. 44, 1789-1796
9. Zizzi, A., Montironi, M. A., Mazzucchelli, R., Scarpelli, M., Lopez-Beltran, A., Cheng, L., Paone, N., Castellini, P., and Montironi, R. (2013) Immunohistochemical analysis of chromatin remodeler DAXX in high grade urothelial carcinoma. Diagn. Pathol. 8, 111
10. Horvilleur, E., Sbarrato, T., Hill, K., Spriggs, R. V., Screen, M., Goodrem, P. J., Sawicka, K., Chaplin, L. C., Touriol, C., Packham, G., Potter, K. N., Dirnhofer, S., Tzankov, A., Dyer, M. J., Bushell, M., MacFarlane, M., and Willis, A. E. (2014) A role for eukaryotic initiation factor 4B overexpression in the pathogenesis of diffuse large B-cell lymphoma. Leukemia 28, 1092-1102
11. Jiao, Y., Shi, C., Edil, B. H., de Wilde, R. F., Klimstra, D. S., Maitra, A., Schulick, R. D., Tang, L. H., Wolfgang, C. L., Choti, M. A., Velculescu, V. E., Diaz, L. A., Jr., Vogelstein, B., Kinzler, K. W., Hruban, R. H., and Papadopoulos, N. (2011) DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331, 1199-1203
12. Heaphy, C. M., Subhawong, A. P., Hong, S. M., Goggins, M. G., Montgomery, E. A., Gabrielson, E., Netto, G. J., Epstein, J. I., Lotan, T. L., Westra, W. H., Shih, I. E. M., Iacobuzio-Donahue, C. A., Maitra, A., Li, Q. K., Eberhart, C. G., Taube, J. M., Rakheja, D., Kurman, R. J., Wu, T. C., Roden, R. B., Argani, P., De Marzo, A. M., Terracciano, L., Torbenson, M., and Meeker, A. K. (2011) Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes. Am. J. Pathol. 179, 1608-1615
13. Puto, L. A., Benner, C., and Hunter, T. (2015) The DAXX co-repressor is directly recruited to active regulatory elements genome-wide to regulate autophagy programs in a model of human prostate cancer. Oncoscience 2, 362-372
14. Loop, S. M., Rozanski, T. A., and Ostenson, R. C. (1993) Human primary prostate tumor cell line, ALVA-31: a new model for studying the hormonal regulation of prostate tumor cell growth. Prostate 22, 93-108
15. Tsuji, T., Du, W., Nishioka, T., Chen, L., Yamamoto, D., and Chen, C. Y. (2010) Phellinus linteus extract sensitizes advanced prostate cancer cells to apoptosis in athymic nude mice. PLoS One 5, e9885
16. Ouyang, D. Y., Xu, L. H., He, X. H., Zhang, Y. T., Zeng, L. H., Cai, J. Y., and Ren, S. (2013) Autophagy is differentially induced in prostate cancer LN-CaP, DU145 and PC-3 cells via distinct splicing profiles of ATG5. Autophagy 9, 20-32
17. Mizushima, N., and Yoshimori, T. (2007) How to interpret LC3 immunoblotting. Autophagy 3, 542-545
18. Puissant, A., Fenouille, N., and Auberger, P. (2012) When autophagy meets cancer through p62/SQSTM1. Am. J. Cancer Res. 2, 397-413
19. Mathew, R., Karp, C. M., Beaudoin, B., Vuong, N., Chen, G., Chen, H. Y., Bray, K., Reddy, A., Bhanot, G., Gelinas, C., Dipaola, R. S., Karantza-Wadsworth, V., and White, E. (2009) Autophagy suppresses tumorigenesis through elimination of p62. Cell 137, 1062-1075
20. Mizushima, N. (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 22, 132-139
21. Lee, E. J., and Tournier, C. (2011) The requirement of uncoordinated 51-like kinase 1 (ULK1) and ULK2 in the regulation of autophagy. Autophagy 7, 689-695
22. Lowe, B. A., and Listrom, M. B. (1988) Incidental carcinoma of the prostate: an analysis of the predictors of progression. J. Urol. 140, 1340-1344
23. Pan, W. W., Zhou, J. J., Liu, X. M., Xu, Y., Guo, L. J., Yu, C., Shi, Q. H., and Fan, H. Y. (2013) Death domain-associated protein DAXX promotes ovarian cancer development and chemoresistance. J. Biol. Chem. 288, 13620-13630
24. Russell, R. C., Tian, Y., Yuan, H., Park, H. W., Chang, Y. Y., Kim, J., Kim, H., Neufeld, T. P., Dillin, A., and Guan, K. L. (2013) ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol. 15, 741-750
25. Ramakrishnan, S., Nguyen, T. M., Subramanian, I. V., and Kelekar, A. (2007) Autophagy and angiogenesis inhibition. Autophagy 3, 512-515
26. Sakurai, T., Okumura, H., Matsumoto, M., Uchikado, Y., Setoyama, T., Omoto, I., Owaki, T., Maemura, K., Ishigami, S., and Natsugoe, S. (2013) The expression of LC-3 is related to tumor suppression through angiogenesis in esophageal cancer. Med. Oncol. 30, 701
27. Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676
28. Takamura, A., Komatsu, M., Hara, T., Sakamoto, A., Kishi, C., Waguri, S., Eishi, Y., Hino, O., Tanaka, K., and Mizushima, N. (2011) Autophagy-deficient mice develop multiple liver tumors. Genes Dev. 25, 795-800
29. Wang, R. C., Wei, Y., An, Z., Zou, Z., Xiao, G., Bhagat, G., White, M., Reichelt, J., and Levine, B. (2012) Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 338, 956-959
30. Liu, Z., Chen, P., Gao, H., Gu, Y., Yang, J., Peng, H., Xu, X., Wang, H., Yang, M., Liu, X., Fan, L., Chen, S., Zhou, J., Sun, Y., Ruan, K., Cheng, S., Komatsu, M., White, E., Li, L., Ji, H., Finley, D., and Hu, R. (2014) Ubiquitylation of autophagy receptor optineurin by HACE1 activates selective autophagy for tumor suppression. Cancer Cell 26, 106-120
31. Liu, X. D., Yao, J., Tripathi, D. N., Ding, Z., Xu, Y., Sun, M., Zhang, J., Bai, S., German, P., Hoang, A., Zhou, L., Jonasch, D., Zhang, X., Conti, C. J., Efstathiou, E., Tannir, N. M., Eissa, N. T., Mills, G. B., Walker, C. L., and Jonasch, E. (2014) Autophagy mediates HIF2α degradation and suppresses renal tumorigenesis. Oncogene 10.1038/onc.2014.199
32. Yang, S., Wang, X., Contino, G., Liesa, M., Sahin, E., Ying, H., Bause, A., Li, Y., Stommel, J. M., Dell'antonio, G., Mautner, J., Tonon, G., Haigis, M., Shirihai, O. S., Doglioni, C., Bardeesy, N., and Kimmelman, A. C. (2011) Pancreatic cancers require autophagy for tumor growth. Genes Dev. 25, 717-729
33. Strohecker, A. M., Guo, J. Y., Karsli-Uzunbas, G., Price, S. M., Chen, G. J., Mathew, R., McMahon, M., and White, E. (2013) Autophagy sustains mitochondrial glutamine metabolism and growth of BrafV600E-driven lung tumors. Cancer Discov. 3, 1272-1285
34. Karantza-Wadsworth, V., Patel, S., Kravchuk, O., Chen, G., Mathew, R., Jin, S., and White, E. (2007) Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 21, 1621-1635
35. Kaighn, M. E., Narayan, K. S., Ohnuki, Y., Lechner, J. F., and Jones, L. W. (1979) Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest. Urol. 17, 16-23
36. Chang, M. A., Morgado, M., Warren, C. R., Hinton, C. V., Farach-Carson, M. C., and Delk, N. A. (2014) p62/SQSTM1 is required for cell survival of apoptosis-resistant bone metastatic prostate cancer cell lines. Prostate 74, 149-163
37. Fernández-Medarde, A., and Santos, E. (2011) Ras in cancer and developmental diseases. Genes Cancer 2, 344-358
38. Guo, J. Y., Karsli-Uzunbas, G., Mathew, R., Aisner, S. C., Kamphorst, J. J., Strohecker, A. M., Chen, G., Price, S., Lu, W., Teng, X., Snyder, E., Santanam, U., Dipaola, R. S., Jacks, T., Rabinowitz, J. D., and White, E. (2013) Autophagy suppresses progression of K-ras-induced lung tumors to oncocytomas and maintains lipid homeostasis. Genes Dev. 27, 1447-1461
39. Elgendy, M., Sheridan, C., Brumatti, G., and Martin, S. J. (2011) Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival. Mol. Cell 42, 23-35
40. Kitanaka, C., Kato, K., Ijiri, R., Sakurada, K., Tomiyama, A., Noguchi, K., Nagashima, Y., Nakagawara, A., Momoi, T., Toyoda, Y., Kigasawa, H., Nishi, T., Shirouzu, M., Yokoyama, S., Tanaka, Y., and Kuchino, Y. (2002) Increased Ras expression and caspase-independent neuroblastoma cell death: possible mechanism of spontaneous neuroblastoma regression. J. Natl. Cancer Inst. 94, 358-368
41. Kohli, L., Kaza, N., Carroll, S. L., and Roth, K. A. (2013) Protector turns predator: autophagic death via selective degradation of KRAS. Autophagy 9, 1438-1439
42. Rosenfeldt, M. T., O'Prey, J., Morton, J. P., Nixon, C., MacKay, G., Mrowinska, A., Au, A., Rai, T. S., Zheng, L., Ridgway, R., Adams, P. D., Anderson, K. I., Gottlieb, E., Sansom, O. J., and Ryan, K. M. (2013) p53 status determines the role of autophagy in pancreatic tumour development. Nature 504, 296-300
43. van Bokhoven, A., Varella-Garcia, M., Korch, C., Hessels, D., and Miller, G. J. (2001) Widely used prostate carcinoma cell lines share common origins. Prostate 47, 36-51
44. Hostanska, K., Nisslein, T., Freudenstein, J., Reichling, J., and Saller, R. (2005) Apoptosis of human prostate androgen-dependent and -independent carcinoma cells induced by an isopropanolic extract of black cohosh involves degradation of cytokeratin (CK) 18. Anticancer Res. 25, 139-147
45. Moul, J. W., Friedrichs, P. A., Lance, R. S., Theune, S. M., and Chang, E. H. (1992) Infrequent RAS oncogene mutations in human prostate cancer. Prostate 20, 327-338
46. Guo, J., Zhu, T., Chen, L., Nishioka, T., Tsuji, T., Xiao, Z. X., and Chen, C. Y. (2010) Differential sensitization of different prostate cancer cells to apoptosis. Genes Cancer 1, 836-846
47. Jenkins, R. B., Qian, J., Lieber, M. M., and Bostwick, D. G. (1997) Detection of c-myc oncogene amplification and chromosomal anomalies in metastatic prostatic carcinoma by fluorescence in situ hybridization. Cancer Res. 57, 524-531
48. Dong, J. T. (2006) Prevalent mutations in prostate cancer. J. Cell. Biochem. 97, 433-447
49. Clegg, N. J., Couto, S. S., Wongvipat, J., Hieronymus, H., Carver, B. S., Taylor, B. S., Ellwood-Yen, K., Gerald, W. L., Sander, C., and Sawyers, C. L. (2011) MYC cooperates with AKT in prostate tumorigenesis and alters sensitivity to mTOR inhibitors. PLoS One 6, e17449
50. Degtyarev, M., De Mazière, A., Orr, C., Lin, J., Lee, B. B., Tien, J. Y., Prior, W. W., van Dijk, S., Wu, H., Gray, D. C., Davis, D. P., Stern, H. M., Murray, L. J., Hoeflich, K. P., Klumperman, J., Friedman, L. S., and Lin, K. (2008) Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J. Cell Biol. 183, 101-116
51. Phin, S., Moore, M. W., and Cotter, P. D. (2013) Genomic Rearrangements of PTEN in Prostate Cancer. Front. Oncol. 3, 240
52. Hollander, M. C., Blumenthal, G. M., and Dennis, P. A. (2011) PTEN loss in the continuum of common cancers, rare syndromes and mouse models. Nat. Rev. Cancer 11, 289-301
53. Festuccia, C., Muzi, P., Millimaggi, D., Biordi, L., Gravina, G. L., Speca, S., Angelucci, A., Dolo, V., Vicentini, C., and Bologna, M. (2005) Molecular aspects of gefitinib antiproliferative and pro-apoptotic effects in PTENpositive and PTEN-negative prostate cancer cell lines. Endocr. Relat. Cancer 12, 983-998
54. Ueno, T., Sato, W., Horie, Y., Komatsu, M., Tanida, I., Yoshida, M., Ohshima, S., Mak, T. W., Watanabe, S., and Kominami, E. (2008) Loss of Pten, a tumor suppressor, causes the strong inhibition of autophagy without affecting LC3 lipidation. Autophagy 4, 692-700
55. Roach, P. J. (2011) AMPK → ULK1 → autophagy. Mol. Cell. Biol. 31, 3082-3084
56. Magee, J. A., Araki, T., Patil, S., Ehrig, T., True, L., Humphrey, P. A., Catalona, W. J., Watson, M. A., and Milbrandt, J. (2001) Expression profiling reveals hepsin overexpression in prostate cancer. Cancer Res. 61, 5692-5696
57. Tomlins, S. A., Mehra, R., Rhodes, D. R., Cao, X., Wang, L., Dhanasekaran, S. M., Kalyana-Sundaram, S., Wei, J. T., Rubin, M. A., Pienta, K. J., Shah, R. B., and Chinnaiyan, A. M. (2007) Integrative molecular concept modeling of prostate cancer progression. Nat. Genet. 39, 41-51
58. Grasso, C. S., Wu, Y. M., Robinson, D. R., Cao, X., Dhanasekaran, S. M., Khan, A. P., Quist, M. J., Jing, X., Lonigro, R. J., Brenner, J. C., Asangani, I. A., Ateeq, B., Chun, S. Y., Siddiqui, J., Sam, L., Anstett, M., Mehra, R., Prensner, J. R., Palanisamy, N., Ryslik, G. A., Vandin, F., Raphael, B. J., Kunju, L. P., Rhodes, D. R., Pienta, K. J., Chinnaiyan, A. M., and Tomlins, S. A. (2012) The mutational landscape of lethal castration-resistant prostate cancer. Nature 487, 239-243
59. Welsh, J. B., Sapinoso, L. M., Su, A. I., Kern, S. G., Wang-Rodriguez, J., Moskaluk, C. A., Frierson, H. F., Jr., and Hampton, G. M. (2001) Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res. 61, 5974-5978
60. Wang, X. D., Reeves, K., Luo, F. R., Xu, L. A., Lee, F., Clark, E., and Huang, F. (2007) Identification of candidate predictive and surrogate molecular markers for dasatinib in prostate cancer: rationale for patient selection and efficacy monitoring. Genome Biol. 8, R255