Sestrin2 protein positively regulates AKT enzyme signaling and survival in human squamous cell carcinoma and melanoma cells

Journal of Biological Chemistry

Volumn 289, Issue 52, 2014, Pages 35806-35814

  Zhao, Baozhong ^a   Shah, Palak ^a   Budanov, Andrei V ^b   Qiang, Lei ^a   Ming, Mei ^a   Aplin, Andrew ^c   Sims, Diane M ^a   He, Yu Ying ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CELL DEATH; DERMATOLOGY; DISEASES; MAMMALS; ONCOLOGY; PROTEINS; RADIOTHERAPY;

AKT ACTIVATION; HUMAN KERATINOCYTES; INDUCED APOPTOSIS; MELANOMA CELLS; SKIN CANCERS; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH; UVB RADIATION;

CELL SIGNALING;

FLUOROURACIL; HEAT SHOCK PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SESTRIN 2; UNCLASSIFIED DRUG; VEMURAFENIB; ANTINEOPLASTIC AGENT; NUCLEAR PROTEIN; SESN2 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL LINE; CANCER INHIBITION; CANCER SURVIVAL; CARCINOGENICITY; CONTROLLED STUDY; DRUG SENSITIZATION; EMBRYO; ENZYME ACTIVATION; FEMALE; GENE DELETION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; MELANOCYTE; MELANOMA; MELANOMA CELL; METASTATIC MELANOMA; MOUSE; NEVUS; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; SKIN CARCINOMA; ULTRAVIOLET B RADIATION; UPREGULATION; ANIMAL; CANCER TRANSPLANTATION; CELL SURVIVAL; EXPERIMENTAL MELANOMA; HELA CELL LINE; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CELL SURVIVAL; FEMALE; HELA CELLS; HUMANS; MELANOMA, EXPERIMENTAL; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TUMOR BURDEN; UP-REGULATION;

EID: 84919799074     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.595397     Document Type: Article

References (41)

1. Rogers, H. W., Weinstock, M. A., Harris, A. R., Hinckley, M. R., Feldman, S. R., Fleischer, A. B., and Coldiron, B. M. (2010) Incidence estimate of nonmelanoma skin cancer in the United States, 2006. Arch. Dermatol. 146, 283-287
2. D'Orazio, J., Jarrett, S., Amaro-Ortiz, A., and Scott, T. (2013) UV Radiation and the Skin. Int. J. Mol. Sci. 14, 12222-12248
3. Tsao, H., Chin, L., Garraway, L. A., and Fisher, D. E. (2012) Melanoma: from mutations to medicine. Genes Dev. 26, 1131-1155
4. Claerhout, S., Verschooten, L., Van Kelst, S., De Vos, R., Proby, C., Agostinis, P., and Garmyn, M. (2010) Concomitant inhibition of AKT and autophagy is required for efficient cisplatin-induced apoptosis of metastatic skin carcinoma. Int. J. Cancer 127, 2790-2803
5. Budanov, A. V., Sablina, A. A., Feinstein, E., Koonin, E. V., and Chumakov, P. M. (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304, 596-600
6. Budanov, A. V., and Karin, M. (2008) p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134, 451-460
7. Bae, S. H., Sung, S. H., Oh, S. Y., Lim, J. M., Lee, S. K., Park, Y. N., Lee, H. E., Kang, D., and Rhee, S. G. (2013) Sestrins activate Nrf2 by promoting p62-dependent autophagic degradation of Keap1 and prevent oxidative liver damage. Cell Metab. 17, 73-84
8. Lee, J. H., Budanov, A. V., Park, E. J., Birse, R., Kim, T. E., Perkins, G. A., Ocorr, K., Ellisman, M. H., Bodmer, R., Bier, E., and Karin, M. (2010) Sestrin as a feedback inhibitor of TOR that prevents age-related pathologies. Science 327, 1223-1228
9. Yang, Y. L., Loh, K. S., Liou, B. Y., Chu, I. H., Kuo, C. J., Chen, H. D., and Chen, C. S. (2013) SESN-1 is a positive regulator of lifespan in Caenorhabditis elegans. Exp. Gerontol. 48, 371-379
10. Budanov, A. V., Shoshani, T., Faerman, A., Zelin, E., Kamer, I., Kalinski, H., Gorodin, S., Fishman, A., Chajut, A., Einat, P., Skaliter, R., Gudkov, A. V., Chumakov, P. M., and Feinstein, E. (2002) Identification of a novel stressresponsive gene Hi95 involved in regulation of cell viability. Oncogene 21, 6017-6031
11. Budanov, A. V. (2011) Stress-responsive sestrins link p53 with redox regulation and mammalian target of rapamycin signaling. Antioxid. Redox Signal. 15, 1679-1690
12. Sablina, A. A., Budanov, A. V., Ilyinskaya, G. V., Agapova, L. S., Kravchenko, J. E., and Chumakov, P. M. (2005) The antioxidant function of the p53 tumor suppressor. Nat. Med. 11, 1306-1313
13. Cam, M., Bid, H. K., Xiao, L., Zambetti, G. P., Houghton, P. J., and Cam, H. (2014) p53/TAp63 and AKT regulate mammalian target of rapamycin complex 1 (mTORC1) signaling through two independent parallel pathways in the presence of DNA damage. J. Biol. Chem. 289, 4083-4094
14. Velasco-Miguel, S., Buckbinder, L., Jean, P., Gelbert, L., Talbott, R., Laidlaw, J., Seizinger, B., and Kley, N. (1999) PA26, a novel target of the p53 tumor suppressor and member of the GADD family of DNA damage and growth arrest inducible genes. Oncogene 18, 127-137
15. Ragnarsson, G., Eiriksdottir, G., Johannsdottir, J. T., Jonasson, J. G., Egilsson, V., and Ingvarsson, S. (1999) Loss of heterozygosity at chromosome 1p in different solid human tumours: association with survival. Br. J. Cancer 79, 1468-1474
16. Schwab, M., Praml, C., and Amler, L. C. (1996) Genomic instability in 1p and human malignancies. Genes Chromosomes Cancer 16, 211-229
17. Lee, J. H., Budanov, A. V., Talukdar, S., Park, E. J., Park, H. L., Park, H. W., Bandyopadhyay, G., Li, N., Aghajan, M., Jang, I., Wolfe, A. M., Perkins, G. A., Ellisman, M. H., Bier, E., Scadeng, M., Foretz, M., Viollet, B., Olefsky, J., and Karin, M. (2012) Maintenance of metabolic homeostasis by Sestrin2 and Sestrin3. Cell Metab. 16, 311-321
18. Shao, Y., and Aplin, A. E. (2010) Akt3-mediated resistance to apoptosis in B-RAF-targeted melanoma cells. Cancer Res. 70, 6670-6681
19. Ming, M., Shea, C. R., Guo, X., Li, X., Soltani, K., Han, W., and He, Y. Y. (2010) Regulation of global genome nucleotide excision repair by SIRT1 through xeroderma pigmentosum C. Proc. Natl. Acad. Sci. U. S. A. 107, 22623-22628
20. Han, W., Ming, M., Zhao, R., Pi, J., Wu, C., and He, Y. Y. (2012) Nrf1 CNC-bZIP protein promotes cell survival and nucleotide excision repair through maintaining glutathione homeostasis. J. Biol. Chem. 287, 18788-18795
21. Wu, C. L., Qiang, L., Han, W., Ming, M., Viollet, B., and He, Y. Y. (2013) Role of AMPK in UVB-induced DNA damage repair and growth control. Oncogene 32, 2682-2689
22. Qiang, L., Yang, Y., Ma, Y. J., Chen, F. H., Zhang, L. B., Liu, W., Qi, Q., Lu, N., Tao, L., Wang, X. T., You, Q. D., and Guo, Q. L. (2009) Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett. 279, 13-21
23. Qiang, L., Wu, C., Ming, M., Viollet, B., and He, Y. Y. (2013) Autophagy controls p38 activation to promote cell survival under genotoxic stress. J. Biol. Chem. 288, 1603-1611
24. Qiang, L., and He, Y. Y. (2014) Autophagy deficiency stabilizes TWIST1 to promote epithelial-mesenchymal transition. Autophagy 10, 1864-1865
25. Han, W., Ming, M., He, T. C., and He, Y. Y. (2010) Immunosuppressive cyclosporin A activates AKT in keratinocytes through PTEN suppression: implications in skin carcinogenesis. J. Biol. Chem. 285, 11369-11377
26. Ming, M., Feng, L., Shea, C. R., Soltani, K., Zhao, B., Han, W., Smart, R. C., Trempus, C. S., and He, Y. Y. (2011) PTEN positively regulates UVBinduced DNA damage repair. Cancer Res. 71, 5287-5295
27. Hers, I., Vincent, E. E., and Tavaré, J. M. (2011) Akt signalling in health and disease. Cell. Signal. 23, 1515-1527
28. Lee, J. H., Budanov, A. V., and Karin, M. (2013) Sestrins orchestrate cellular metabolism to attenuate aging. Cell Metab. 18, 792-801
29. Lee, S. O., Andey, T., Jin, U. H., Kim, K., Singh, M., Sachdeva, M., and Safe, S. (2012) The nuclear receptor TR3 regulates mTORC1 signaling in lung cancer cells expressing wild-type p53. Oncogene 31, 3265-3276
30. Wei, C. L., Wu, Q., Vega, V. B., Chiu, K. P., Ng, P., Zhang, T., Shahab, A., Yong, H. C., Fu, Y., Weng, Z., Liu, J., Zhao, X. D., Chew, J. L., Lee, Y. L., Kuznetsov, V. A., Sung, W. K., Miller, L. D., Lim, B., Liu, E. T., Yu, Q., Ng, H. H., and Ruan, Y. (2006) A global map of p53 transcription-factor binding sites in the human genome. Cell 124, 207-219
31. Marionnet, C., Pierrard, C., Lejeune, F., Sok, J., Thomas, M., and Bernerd, F. (2010) Different oxidative stress response in keratinocytes and fibro-blasts of reconstructed skin exposed to non extreme daily-ultraviolet radiation. PLoS ONE 5, e12059
32. Lehman, T. A., Modali, R., Boukamp, P., Stanek, J., Bennett, W. P., Welsh, J. A., Metcalf, R. A., Stampfer, M. R., Fusenig, N., and Rogan, E. M. (1993) p53 mutations in human immortalized epithelial cell lines. Carcinogenesis 14, 833-839
33. Budanov, A. V., Lee, J. H., and Karin, M. (2010) Stressin' sestrins take an aging fight. EMBO Mol. Med. 2, 388-400
34. Sanli, T., Linher-Melville, K., Tsakiridis, T., and Singh, G. (2012) Sestrin2 modulates AMPK subunit expression and its response to ionizing radiation in breast cancer cells. PLoS ONE 7, e32035
35. Ben-Sahra, I., Dirat, B., Laurent, K., Puissant, A., Auberger, P., Budanov, A., Tanti, J. F., and Bost, F. (2013) Sestrin2 integrates Akt and mTOR signaling to protect cells against energetic stress-induced death. Cell Death Differ. 20, 611-619
36. Li, T., Kon, N., Jiang, L., Tan, M., Ludwig, T., Zhao, Y., Baer, R., and Gu, W. (2012) Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 149, 1269-1283
37. Cheung, E. C., Athineos, D., Lee, P., Ridgway, R. A., Lambie, W., Nixon, C., Strathdee, D., Blyth, K., Sansom, O. J., and Vousden, K. H. (2013) TIGAR is required for efficient intestinal regeneration and tumorigenesis. Dev. Cell 25, 463-477
38. DeNicola, G. M., Karreth, F. A., Humpton, T. J., Gopinathan, A., Wei, C., Frese, K., Mangal, D., Yu, K. H., Yeo, C. J., Calhoun, E. S., Scrimieri, F., Winter, J. M., Hruban, R. H., Iacobuzio-Donahue, C., Kern, S. E., Blair, I. A., and Tuveson, D. A. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475, 106-109
39. Kim, Y. R., Oh, J. E., Kim, M. S., Kang, M. R., Park, S. W., Han, J. Y., Eom, H. S., Yoo, N. J., and Lee, S. H. (2010) Oncogenic NRF2 mutations in squamous cell carcinomas of oesophagus and skin. J. Pathol. 220, 446-451
40. Miura, S., Shibazaki, M., Kasai, S., Yasuhira, S., Watanabe, A., Inoue, T., Kageshita, Y., Tsunoda, K., Takahashi, K., Akasaka, T., Masuda, T., and Maesawa, C. (2014) A Somatic mutation of the KEAP1 gene in malignant melanoma is involved in aberrant NRF2 activation and an increase in intrinsic drug resistance. J. Invest. Dermatol. 134, 553-556
41. Ren, D., Villeneuve, N. F., Jiang, T., Wu, T., Lau, A., Toppin, H. A., and Zhang, D. D. (2011) Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism. Proc. Natl. Acad. Sci. U. S. A. 108, 1433-1438