Modification of Akt2 by 4-hydroxynonenal inhibits insulin-dependent Akt signaling in HepG2 cells

Biochemistry

Volumn 50, Issue 19, 2011, Pages 3984-3996

  Shearn, C T ^a   Fritz, K S ^a   Reigan, P ^a   Petersen, Dennis R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4-HYDROXY-2-NONENAL; 4-HYDROXY-NONENAL; AKT PHOSPHORYLATION; HEPATIC DISEASE; HEPATOCELLULAR; HEPATOCELLULAR CARCINOMA CELL; HEPATOCYTES; HEPG2 CELLS; INSULIN RESISTANCE; INSULIN SIGNALING; KEY COMPONENT; LIVER CELLS; LIVER DISEASE; MALDI-TOF/TOF; MATRIX-ASSISTED LASER DESORPTION IONIZATION; MICHAEL ADDITIONS; MOLECULAR MODELING ANALYSIS; PEPTIDE BINDING; POTENTIAL MECHANISM; PRE-TREATMENT; SUBSTRATE BINDING; TANDEM MASS SPECTROMETRY; TIME OF FLIGHT; UNTREATED CONTROL;

ADDITION REACTIONS; ALDEHYDES; CARBONYLATION; CELL CULTURE; DESORPTION; ENZYME ACTIVITY; MASS SPECTROMETRY; PEPTIDES; PHOSPHORYLATION; SIGNALING; SUBSTRATES;

INSULIN;

4 HYDROXYNONENAL; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN MDM2;

ARTICLE; CARBONYLATION; HUMAN; HUMAN CELL; INSULIN RESISTANCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICHAEL ADDITION; MYRISTYLATION; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

ALDEHYDES; AMINO ACID SEQUENCE; DOWN-REGULATION; GLYCOGEN SYNTHASE KINASE 3; HEP G2 CELLS; HUMANS; INSULIN RESISTANCE; MOLECULAR SEQUENCE DATA; PEPTIDE MAPPING; PEPTIDES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 79955830382     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200029w     Document Type: Article

References (49)

1. Paradis, V., Kollinger, M., Fabre, M., Holstege, A., Poynard, T., and Bedossa, P. (1997) In situ detection of lipid peroxidation by-products in chronic liver diseases Hepatology 26, 135-142 (Pubitemid 27280317)
2. Paradis, V., Mathurin, P., Kollinger, M., Imbert-Bismut, F., Charlotte, F., Piton, A., Opolon, P., Holstege, A., Poynard, T., and Bedossa, P. (1997) In situ detection of lipid peroxidation in chronic hepatitis C: Correlation with pathological features J. Clin. Pathol. 50, 401-406 (Pubitemid 27278444)
3. Roede, J. R., Orlicky, D. J., Fisher, A. B., and Petersen, D. R. (2009) Overexpression of peroxiredoxin 6 does not prevent ethanol-mediated oxidative stress and may play a role in hepatic lipid accumulation J. Pharmacol. Exp. Ther. 330, 79-88
4. Roede, J. R., Stewart, B. J., and Petersen, D. R. (2008) Decreased expression of peroxiredoxin 6 in a mouse model of ethanol consumption Free Radical Biol. Med. 45, 1551-1558
5. Sampey, B. P., Korourian, S., Ronis, M. J., Badger, T. M., and Petersen, D. R. (2003) Immunohistochemical characterization of hepatic malondialdehyde and 4-hydroxynonenal modified proteins during early stages of ethanol-induced liver injury Alcohol.: Clin. Exp. Res. 27, 1015-1022 (Pubitemid 36759392)
6. Kohli, R., Kirby, M., Xanthakos, S. A., Softic, S., Feldstein, A. E., Saxena, V., Tang, P. H., Miles, L., Miles, M. V., Balistreri, W. F., Woods, S. C., and Seeley, R. J. (2010) High-fructose, medium chain trans fat diet induces liver fibrosis and elevates plasma coenzyme Q9 in a novel murine model of obesity and nonalcoholic steatohepatitis Hepatology 52, 934-944
7. Schaur, R. J. (2003) Basic aspects of the biochemical reactivity of 4-hydroxynonenal Mol. Aspects Med. 24, 149-159 (Pubitemid 36945015)
8. Benedetti, A., Comporti, M., Fulceri, R., and Esterbauer, H. (1984) Cytotoxic aldehydes originating from the peroxidation of liver microsomal lipids. Identification of 4,5-dihydroxydecenal Biochim. Biophys. Acta 792, 172-181
9. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radical Biol. Med. 11, 81-128 (Pubitemid 121003917)
10. Roede, J. R., Carbone, D. L., Doorn, J. A., Kirichenko, O. V., Reigan, P., and Petersen, D. R. (2008) In Vitro and in Silico Characterization of Peroxiredoxin 6 Modified by 4-Hydroxynonenal and 4-Oxononenal Chem. Res. Toxicol. 21, 2289-2299
11. Stewart, B. J., Doorn, J. A., and Petersen, D. R. (2007) Residue-specific adduction of tubulin by 4-hydroxynonenal and 4-oxononenal causes cross-linking and inhibits polymerization Chem. Res. Toxicol. 20, 1111-1119 (Pubitemid 47372989)
12. Shearn, C. T., Smathers, R. L., Stewart, B. J., Fritz, K. S., Galligan, J. J., Hail, N., and Petersen, D. R. PTEN Inhibition by 4-Hydroxynonenal Leads to Increased Akt Activation in Hepatocytes. Mol. Pharmacol. 2011, not supplied.
13. Calleja, V., Alcor, D., Laguerre, M., Park, J., Vojnovic, B., Hemmings, B. A., Downward, J., Parker, P. J., and Larijani, B. (2007) Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo PLoS Biol. 5, e95
14. Wu, W. I., Voegtli, W. C., Sturgis, H. L., Dizon, F. P., Vigers, G. P., and Brandhuber, B. J. (2010) Crystal structure of human AKT1 with an allosteric inhibitor reveals a new mode of kinase inhibition PLoS One 5, e12913
15. Calleja, V., Laguerre, M., and Larijani, B. (2009) 3-D structure and dynamics of protein kinase B: New mechanism for the allosteric regulation of an AGC kinase J. Chem. Biol. 2, 11-25
16. Liao, Y. and Hung, M. C. (2010) Physiological regulation of Akt activity and stability Am. J. Transl. Res. 2, 19-42
17. Leavens, K. F., Easton, R. M., Shulman, G. I., Previs, S. F., and Birnbaum, M. J. (2009) Akt2 is required for hepatic lipid accumulation in models of insulin resistance Cell Metab. 10, 405-418
18. Samuel, V. T., Petersen, K. F., and Shulman, G. I. (2010) Lipid-induced insulin resistance: Unravelling the mechanism Lancet 375, 2267-2277
19. Katome, T., Obata, T., Matsushima, R., Masuyama, N., Cantley, L. C., Gotoh, Y., Kishi, K., Shiota, H., and Ebina, Y. (2003) Use of RNA interference-mediated gene silencing and adenoviral overexpression to elucidate the roles of AKT/protein kinase B isoforms in insulin actions J. Biol. Chem. 278, 28312-28323 (Pubitemid 36900033)
20. Moro, L., Arbini, A. A., Yao, J. L., di SantAgnese, P. A., Marra, E., and Greco, M. (2009) Mitochondrial DNA depletion in prostate epithelial cells promotes anoikis resistance and invasion through activation of PI3K/Akt2 Cell Death Differ. 16, 571-583
21. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, E. B., III, 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 β) Science 292, 1728-1731 (Pubitemid 32506248)
22. Stiles, B., Wang, Y., Stahl, A., Bassilian, S., Lee, W. P., Kim, Y. J., Sherwin, R., Devaskar, S., Lesche, R., Magnuson, M. A., and Wu, H. (2004) Liver-specific deletion of negative regulator Pten results in fatty liver and insulin hypersensitivity [corrected] Proc. Natl. Acad. Sci. U.S.A. 101, 2082-2087 (Pubitemid 38229018)
23. He, L., Hou, X., Kanel, G., Zeng, N., Galicia, V., Wang, Y., Yang, J., Wu, H., Birnbaum, M. J., and Stiles, B. L. (2010) The critical role of AKT2 in hepatic steatosis induced by PTEN loss Am. J. Pathol. 176, 2302-2308
24. He, J., de la Monte, S., and Wands, J. R. (2007) Acute ethanol exposure inhibits insulin signaling in the liver Hepatology 46, 1791-1800
25. Liu, W., Akhand, A. A., Takeda, K., Kawamoto, Y., Itoigawa, M., Kato, M., Suzuki, H., Ishikawa, N., and Nakashima, I. (2003) Protein phosphatase 2A-linked and -unlinked caspase-dependent pathways for downregulation of Akt kinase triggered by 4-hydroxynonenal Cell Death Differ. 10, 772-781 (Pubitemid 36850238)
26. Yang, J., Cron, P., Good, V. M., Thompson, V., Hemmings, B. A., and Barford, D. (2002) Crystal structure of an activated Akt/protein kinase B ternary complex with GSK3-peptide and AMP-PNP Nat. Struct. Biol. 9, 940-944 (Pubitemid 35417064)
27. Brooks, B. R., III, Brooks, C. L., Mackerell, A. D., Jr., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: The biomolecular simulation program J. Comput. Chem. 30, 1545-1614
28. Onufriev, A., Case, D. A., and Bashford, D. (2002) Effective Born radii in the generalized Born approximation: The importance of being perfect J. Comput. Chem. 23, 1297-1304 (Pubitemid 35186231)
29. Ramos, J. W. (2008) The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells Int. J. Biochem. Cell Biol. 40, 2707-2719
30. Codreanu, S. G., Zhang, B., Sobecki, S. M., Billheimer, D. D., and Liebler, D. C. (2009) Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal Mol. Cell. Proteomics 8, 670-680
31. Dozza, B., Smith, M. A., Perry, G., Tabaton, M., and Strocchi, P. (2004) Regulation of glycogen synthase kinase-3β by products of lipid peroxidation in human neuroblastoma cells J. Neurochem. 89, 1224-1232 (Pubitemid 38715840)
32. 6-PKBβ/Akt2 and characterization of phospho-specific isoforms for design of inhibitors that stabilize inactive conformations Protein Expression Purif. 43, 44-56 (Pubitemid 41097383)
33. Chaudhary, P., Sharma, R., Sharma, A., Vatsyayan, R., Yadav, S., Singhal, S. S., Rauniyar, N., Prokai, L., Awasthi, S., and Awasthi, Y. C. (2010) Mechanisms of 4-hydroxy-2-nonenal induced pro- and anti-apoptotic signaling Biochemistry 49, 6263-6275
34. Sharma, R., Sharma, A., Dwivedi, S., Zimniak, P., Awasthi, S., and Awasthi, Y. C. (2008) 4-Hydroxynonenal self-limits fas-mediated DISC-independent apoptosis by promoting export of Daxx from the nucleus to the cytosol and its binding to Fas Biochemistry 47, 143-156
35. Kawaguchi, T. and Sata, M. (2010) Importance of hepatitis C virus-associated insulin resistance: Therapeutic strategies for insulin sensitization World J. Gastroenterol. 16, 1943-1952
36. Lockman, K. A. and Nyirenda, M. J. (2010) Interrelationships between hepatic fat and insulin resistance in non-alcoholic fatty liver disease Curr. Diabetes Rev. 6, 341-347
37. de la Monte, S. M., Yeon, J. E., Tong, M., Longato, L., Chaudhry, R., Pang, M. Y., Duan, K., and Wands, J. R. (2008) Insulin resistance in experimental alcohol-induced liver disease J. Gastroenterol. Hepatol. 23, e477-e486
38. Derdak, Z., Lang, C. H., Villegas, K. A., Tong, M., Mark, N. M., de la Monte, S. M., and Wands, J. R. (2010) Activation of p53 enhances apoptosis and insulin resistance in a rat model of alcoholic liver disease J. Hepatol. 54, 164-172
39. George, S., Rochford, J. J., Wolfrum, C., Gray, S. L., Schinner, S., Wilson, J. C., Soos, M. A., Murgatroyd, P. R., Williams, R. M., Acerini, C. L., Dunger, D. B., Barford, D., Umpleby, A. M., Wareham, N. J., Davies, H. A., Schafer, A. J., Stoffel, M., ORahilly, S., and Barroso, I. (2004) A family with severe insulin resistance and diabetes due to a mutation in AKT2 Science 304, 1325-1328 (Pubitemid 38697429)
40. Yun, S. J., Tucker, D. F., Kim, E. K., Kim, M. S., Do, K. H., Ha, J. M., Lee, S. Y., Yun, J., Kim, C. D., Birnbaum, M. J., and Bae, S. S. (2009) Differential regulation of Akt/protein kinase B isoforms during cell cycle progression FEBS Lett. 583, 685-690
41. Gonzalez, E. and McGraw, T. E. (2009) Insulin-modulated Akt subcellular localization determines Akt isoform-specific signaling Proc. Natl. Acad. Sci. U.S.A. 106, 7004-7009
42. Covey, T. M., Edes, K., and Fitzpatrick, F. A. (2007) Akt activation by arachidonic acid metabolism occurs via oxidation and inactivation of PTEN tumor suppressor Oncogene 26, 5784-5792 (Pubitemid 47312821)
43. Paajarvi, G., Roudier, E., Crisby, M., Hogberg, J., and Stenius, U. (2005) HMG-CoA reductase inhibitors, statins, induce phosphorylation of Mdm2 and attenuate the p53 response to DNA damage FASEB J. 19, 476-478 (Pubitemid 40316555)
44. Stewart, B. J., Roede, J. R., Doorn, J. A., and Petersen, D. R. (2009) Lipid aldehyde-mediated cross-linking of apolipoprotein B-100 inhibits secretion from HepG2 cells Biochim. Biophys. Acta 1791, 772-780
45. Cuevas, E. P., Escribano, O., Chiloeches, A., Ramirez Rubio, S., Roman, I. D., Fernandez-Moreno, M. D., and Guijarro, L. G. (2007) Role of insulin receptor substrate-4 in IGF-I-stimulated HEPG2 proliferation J. Hepatol. 46, 1089-1098 (Pubitemid 46669737)
46. Wagner, T. M., Mullally, J. E., and Fitzpatrick, F. A. (2006) Reactive lipid species from cyclooxygenase-2 inactivate tumor suppressor LKB1/STK11: Cyclopentenone prostaglandins and 4-hydroxy-2-nonenal covalently modify and inhibit the AMP-kinase kinase that modulates cellular energy homeostasis and protein translation J. Biol. Chem. 281, 2598-2604 (Pubitemid 43845720)
47. Huang, X., Begley, M., Morgenstern, K. A., Gu, Y., Rose, P., Zhao, H., and Zhu, X. (2003) Crystal structure of an inactive Akt2 kinase domain Structure 11, 21-30 (Pubitemid 36071494)
48. 3-poisoned rats Biochim. Biophys. Acta 712, 628-638 (Pubitemid 13198989)
49. 3 poisoning Biochim. Biophys. Acta 711, 345-356 (Pubitemid 12054119)