Inhibition of protein synthesis alters protein degradation through activation of protein kinase B (AKT)

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 23875-23883

  Dai, Chun Ling ^a   Shi, Jianhua ^a,b   Chen, Yanxing ^a   Iqbal, Khalid ^a   Liu, Fei ^a,b   Gong, Cheng Xin ^a,b  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b NANTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BIOSYNTHESIS; PROTEIN DEGRADATION; PROTEIN KINASE B; PROTEIN SYNTHESIS; SUBSTRATE PROTEINS; UBIQUITIN LIGASES;

BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES;

PROTEINS;

CYCLOHEXIMIDE; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; LIGASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AS160; PROTEIN KINASE B; PROTEIN MDM2; S6 KINASE; TRANSCRIPTION FACTOR FKHR; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION;

AKT; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; PROTEIN TURNOVER; SIGNAL TRANSDUCTION;

ANIMALS; CHROMONES; CYCLOHEXIMIDE; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; MICE; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MDM2; SIGNAL TRANSDUCTION; SIROLIMUS; SUBSTRATE SPECIFICITY; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84882402269     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.445148     Document Type: Article

References (61)

1. Baliga, B. S., Pronczuk, A. W., and Munro, H. N. (1969) Mechanism of cycloheximide inhibition of protein synthesis in a cell-free system prepared from rat liver. J. Biol. Chem. 244, 4480-4489
2. Fulda, S., Gorman, A. M., Hori, O., and Samali, A. (2010) Cellular stress responses: cell survival and cell death. Int. J. Cell Biol. 2010, 214074
3. Baskić, D., Popović, S., Ristić, P., and Arsenijević, N. N. (2006) Analysis of cycloheximide-induced apoptosis in human leukocytes: fluorescence microscopy using annexin V/propidium iodide versus acridine orange/ ethidium bromide. Cell Biol. Int. 30, 924-932
4. Ishii, H. H., Etheridge, M. R., and Gobé, G. C. (1995) Cycloheximideinduced apoptosis in Burkitt lymphoma (BJA-B) cells with and without Epstein-Barr virus infection. Immunol. Cell Biol. 73, 463-468
5. Tsuchida, T., Kato, T., Yamada, A., and Kawamoto, K. (2002) Cycloheximide induces apoptosis of astrocytes. Pathol. Int. 52, 181-185
6. Buzzi, F., Xu, L., Zuellig, R. A., Boller, S. B., Spinas, G. A., Hynx, D., Chang, Z., Yang, Z., Hemmings, B. A., Tschopp, O., and Niessen, M. (2010) Differential effects of protein kinase B/Akt isoforms on glucose homeostasis and islet mass. Mol. Cell. Biol. 30, 601-612
7. Alessi, D. R., Andjelkovic, M., Caudwell, B., Cron, P., Morrice, N., Cohen, P., and Hemmings, B. A. (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15, 6541-6551
8. Sun, S. Y., Rosenberg, L. M., Wang, X., Zhou, Z., Yue, P., Fu, H., and Khuri, F. R. (2005) Activation of Akt and eIF4E survival pathways by rapamycinmediated mammalian target of rapamycin inhibition. Cancer Res. 65, 7052-7058
9. Woodgett, J. R. (2005) Recent advances in the protein kinase B signaling pathway. Curr. Opin. Cell Biol. 17, 150-157
10. Garofalo, R. S., Orena, S. J., Rafidi, K., Torchia, A. J., Stock, J. L., Hildebrandt, A. L., Coskran, T., Black, S. C., Brees, D. J., Wicks, J. R., McNeish, J. D., and Coleman, K. G. (2003) Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB. J. Clin. Invest. 112, 197-208
11. Chen, W. S., Xu, P. Z., Gottlob, K., Chen, M. L., Sokol, K., Shiyanova, T., Roninson, I., Weng, W., Suzuki, R., Tobe, K., Kadowaki, T., and Hay, N. (2001) Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev. 15, 2203-2208
12. Cho, H., Thorvaldsen, J. L., Chu, Q., Feng, F., and Birnbaum, M. J. (2001) Akt1/PKB is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276, 38349-38352
13. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, E. B., 3rd, Kaestner, K. H., Bartolomei, M. S., Shulman, G. I., and Birnbaum, M. J. (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB). Science 292, 1728-1731
14. Easton, R. M., Cho, H., Roovers, K., Shineman, D. W., Mizrahi, M., Forman, M. S., Lee, V. M., Szabolcs, M., de Jong, R., Oltersdorf, T., Ludwig, T., Efstratiadis, A., and Birnbaum, M. J. (2005) Role for Akt3/protein kinase B in attainment of normal brain size. Mol. Cell. Biol. 25, 1869-1878
15. Tschopp, O., Yang, Z. Z., Brodbeck, D., Dummler, B. A., Hemmings-Mieszczak, M., Watanabe, T., Michaelis, T., Frahm, J., and Hemmings, B. A. (2005) Essential role of protein kinase B (PKB/Akt3) in postnatal brain development but not in glucose homeostasis. Development 132, 2943-2954
16. Yoshiura, S., Ohtsuka, T., Takenaka, Y., Nagahara, H., Yoshikawa, K., and Kageyama, R. (2007) Ultradian oscillations of Stat, Smad, and Hes1 expression in response to serum. Proc. Natl. Acad. Sci. U.S.A. 104, 11292-11297
17. Xue, Z., He, Y., Ye, K., Gu, Z., Mao, Y., and Qi, L. (2011) A conserved structural determinant located at the interdomain region of mammalian inositol-requiring enzyme 1. J. Biol. Chem. 286, 30859-30866
18. Novac, O., Guenier, A. S., and Pelletier, J. (2004) Inhibitors of protein synthesis identified by a high throughput multiplexed translation screen. Nucleic Acids Res. 32, 902-915
19. Hemi, R., Paz, K., Wertheim, N., Karasik, A., Zick, Y., and Kanety, H. (2002) Transactivation of ErbB2 and ErbB3 by tumor necrosis factor-and anisomycin leads to impaired insulin signaling through serine/threonine phosphorylation of IRS proteins. J. Biol. Chem. 277, 8961-8969
20. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101
21. Bae, I. H., Park, M. J., Yoon, S. H., Kang, S. W., Lee, S. S., Choi, K. M., and Um, H. D. (2006) Bcl-w promotes gastric cancer cell invasion by inducing matrix metalloproteinase-2 expression via phosphoinositide 3-kinase, Akt, and Sp1. Cancer Res. 66, 4991-4995
22. Chandrasekharan, U. M., Yang, L., Walters, A., Howe, P., and DiCorleto, P. E. (2004) Role of CL-100, a dual specificity phosphatase, in thrombininduced endothelial cell activation. J. Biol. Chem. 279, 46678-46685
23. Wan, X., Harkavy, B., Shen, N., Grohar, P., and Helman, L. J. (2007) Rapamycin induces feedback activation of Akt signaling through an IGF-1Rdependent mechanism. Oncogene 26, 1932-1940
24. O'Reilly, K. E., Rojo, F., She, Q. B., Solit, D., Mills, G. B., Smith, D., Lane, H., Hofmann, F., Hicklin, D. J., Ludwig, D. L., Baselga, J., and Rosen, N. (2006) mTORinhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res. 66, 1500-1508
25. Mayo, L. D., and Donner, D. B. (2001) A phosphatidylinositol 3-kinase/ Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc. Natl. Acad. Sci. U.S.A. 98, 11598-11603
26. Zhou, B. P., Liao, Y., Xia, W., Zou, Y., Spohn, B., and Hung, M. C. (2001) HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat. Cell Biol. 3, 973-982
27. Honda, R., and Yasuda, H. (1999) Association of p19ARF with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J. 18, 22-27
28. Fang, S., Jensen, J. P., Ludwig, R. L., Vousden, K. H., and Weissman, A. M. (2000) Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J. Biol. Chem. 275, 8945-8951
29. Feng, J., Tamaskovic, R., Yang, Z., Brazil, D. P., Merlo, A., Hess, D., and Hemmings, B. A. (2004) Stabilization of Mdm2 via decreased ubiquitination is mediated by protein kinase B/Akt-dependent phosphorylation. J. Biol. Chem. 279, 35510-35517
30. Wang, X., McCullough, K. D., Franke, T. F., and Holbrook, N. J. (2000) Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275, 14624-14631
31. Coxon, F. P., Benford, H. L., Russell, R. G., and Rogers, M. J. (1998) Protein synthesis is required for caspase activation and induction of apoptosis by bisphosphonate drugs. Mol. Pharmacol. 54, 631-638
32. Cohen, J. J., and Duke, R. C. (1984) Glucocorticoid activation of a calciumdependent endonuclease in thymocyte nuclei leads to cell death. J. Immunol. 132, 38-42
33. Cantley, L. C. (2002) The phosphoinositide 3-kinase pathway. Science 296, 1655-1657
34. Porter, A. G., and Jänicke, R. U. (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6, 99-104
35. del Peso, L., González-García, M., Page, C., Herrera, R., and Nuñez, G. (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278, 687-689
36. Cardone, M. H., Roy, N., Stennicke, H. R., Salvesen, G. S., Franke, T. F., Stanbridge, E., Frisch, S., and Reed, J. C. (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318-1321
37. Benjamin, D., Colombi, M., Moroni, C., and Hall, M. N. (2011) Rapamycin passes the torch: a new generation of mTOR inhibitors. Nat. Rev. Drug Discov. 10, 868-880
38. Sarbassov, D. D., Ali, S. M., Sengupta, S., Sheen, J. H., Hsu, P. P., Bagley, A. F., Markhard, A. L., and Sabatini, D. M. (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22, 159-168
39. Lee, J. C., and Peter, M. E. (2003) Regulation of apoptosis by ubiquitination. Immunol. Rev. 193, 39-47
40. Yang, Y., and Yu, X. (2003) Regulation of apoptosis: the ubiquitous way. FASEB J. 17, 790-799
41. Chen, Z. J. (2005) Ubiquitin signalling in the NFκB pathway. Nat. Cell Biol. 7, 758-765
42. Hershko, A., Heller, H., Elias, S., and Ciechanover, A. (1983) Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258, 8206-8214
43. Bhoj, V. G., and Chen, Z. J. (2009) Ubiquitylation in innate and adaptive immunity. Nature 458, 430-437
44. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature 387, 296-299
45. Honda, R., Tanaka, H., and Yasuda, H. (1997) Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420, 25-27
46. Kubbutat, M. H., Jones, S. N., and Vousden, K. H. (1997) Regulation of p53 stability by Mdm2. Nature 387, 299-303
47. Lin, H. K., Wang, L., Hu, Y. C., Altuwaijri, S., and Chang, C. (2002) Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase. EMBO J. 21, 4037-4048
48. Yogosawa, S., Miyauchi, Y., Honda, R., Tanaka, H., and Yasuda, H. (2003) Mammalian Numb is a target protein of Mdm2, ubiquitin ligase. Biochem. Biophys. Res. Commun. 302, 869-872
49. Juven-Gershon, T., Shifman, O., Unger, T., Elkeles, A., Haupt, Y., and Oren, M. (1998) The Mdm2 oncoprotein interacts with the cell fate regulator Numb. Mol. Cell. Biol. 18, 3974-3982
50. Cao, Z., Wu, X., Yen, L., Sweeney, C., and Carraway, K. L., 3rd (2007) Neuregulin-induced ErbB3 down-regulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1. Mol. Cell. Biol. 27, 2180-2188
51. Gao, D., Inuzuka, H., Tseng, A., Chin, R. Y., Toker, A., and Wei, W. (2009) Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat. Cell Biol. 11, 397-408
52. Marti, A., Wirbelauer, C., Scheffner, M., and Krek, W. (1999) Interaction between ubiquitin-protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation. Nat. Cell Biol. 1, 14-19
53. Kim, S. Y., Herbst, A., Tworkowski, K. A., Salghetti, S. E., and Tansey, W. P. (2003) Skp2 regulates Myc protein stability and activity. Mol. Cell 11, 1177-1188
54. von der Lehr, N., Johansson, S., Wu, S., Bahram, F., Castell, A., Cetinkaya, C., Hydbring, P., Weidung, I., Nakayama, K., Nakayama, K. I., Söderberg, O., Kerppola, T. K., and Larsson, L. G. (2003) The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol. Cell 11, 1189-1200
55. Bornstein, G., Bloom, J., Sitry-Shevah, D., Nakayama, K., Pagano, M., and Hershko, A. (2003) Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase. J. Biol. Chem. 278, 25752-25757
56. Nakayama, K., Nagahama, H., Minamishima, Y. A., Matsumoto, M., Nakamichi, I., Kitagawa, K., Shirane, M., Tsunematsu, R., Tsukiyama, T., Ishida, N., Kitagawa, M., Nakayama, K., and Hatakeyama, S. (2000) Targeted disruption of Skp2 results in accumulation of cyclin E and p27Kip1, polyploidy and centrosome overduplication. EMBO J. 19, 2069-2081
57. Huang, H., Regan, K. M., Wang, F., Wang, D., Smith, D. I., van Deursen, J. M., and Tindall, D. J. (2005) Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc. Natl. Acad. Sci. U.S.A. 102, 1649-1654
58. McVean, M., Xiao, H., Isobe, K., and Pelling, J. C. (2000) Increase in wildtype p53 stability and transactivational activity by the chemopreventive agent apigenin in keratinocytes. Carcinogenesis 21, 633-639
59. Kaur, P., Shukla, S., and Gupta, S. (2008) Plant flavonoid apigenin inactivates Akt to trigger apoptosis in human prostate cancer: an in vitro and in vivo study. Carcinogenesis 29, 2210-2217
60. Plas, D. R., and Thompson, C. B. (2003) Akt activation promotes degradation of tuberin and FOXO3a via the proteasome. J. Biol. Chem. 278, 12361-12366
61. Schneider-Poetsch, T., Ju, J., Eyler, D. E., Dang, Y., Bhat, S., Merrick, W. C., Green, R., Shen, B., and Liu, J. O. (2010) Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 6, 209-217