Inhibition of Hydrogen peroxide signaling by 4-hydroxynonenal due to differential regulation of Akt1 and Akt2 contributes to decreases in cell survival and proliferation in hepatocellular carcinoma cells

Free Radical Biology and Medicine

Volumn 53, Issue 1, 2012, Pages 1-11

  Shearn, Colin T ^a   Reigan, Philip ^a   Petersen, Dennis R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

4 hydroxynonenal; Akt; Hydrogen peroxide; Oxidative stress

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; 4 HYDROXYNONENAL; ACTIN; BETA CATENIN; BIOTIN; CYCLIN D1; ELECTROPHILE; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; HYDRAZIDE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN AKT1; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN MDM2; PROTEIN P46; PROTEIN P54; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CARBONYLATION; CARCINOMA CELL; CELL DAMAGE; CELL PROLIFERATION; CELL STRAIN HEPG2; CELL SURVIVAL; CHRONIC INFLAMMATION; CHRONIC LIVER DISEASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MYRISTYLATION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ALDEHYDES; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CELL SURVIVAL; CYSTEINE PROTEINASE INHIBITORS; HUMANS; HYDROGEN PEROXIDE; LIVER NEOPLASMS; OXIDANTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84861370262     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.04.021     Document Type: Article

References (55)

1. V. Paradis, M. Kollinger, M. Fabre, A. Holstege, T. Poynard, and P. Bedossa In situ detection of lipid peroxidation by-products in chronic liver diseases Hepatology 26 1997 135 142
2. V. Paradis, P. Mathurin, M. Kollinger, F. Imbert-Bismut, F. Charlotte, A. Piton, P. Opolon, A. Holstege, T. Poynard, and P. Bedossa In situ detection of lipid peroxidation in chronic hepatitis C: correlation with pathological features J. Clin. Pathol. 50 1997 401 406
3. J.R. Roede, D.J. Orlicky, A.B. Fisher, and D.R. Petersen 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 2009 79 88
4. J.R. Roede, B.J. Stewart, and D.R. Petersen Decreased expression of peroxiredoxin 6 in a mouse model of ethanol consumption Free Radic. Biol. Med. 45 2008 1551 1558
5. S. Ghatak, A. Biswas, G.K. Dhali, A. Chowdhury, J.L. Boyer, and A. Santra Oxidative stress and hepatic stellate cell activation are key events in arsenic induced liver fibrosis in mice Toxicol. Appl. Pharmacol. 251 2011 59 69
6. J.M. Schattenberg, R. Singh, Y. Wang, J.H. Lefkowitch, R.M. Rigoli, P.E. Scherer, and M.J. Czaja JNK1 but not JNK2 promotes the development of steatohepatitis in mice Hepatology 43 2006 163 172
7. A. Fourcot, D. Couchie, M.N. Chobert, E.S. Zafrani, P. Mavier, Y. Laperche, and A. Brouillet Gas6 deficiency prevents liver inflammation, steatohepatitis and fibrosis in mice Am. J. Physiol. Gastrointest. Liver Physiol. 2011
8. A. Vila, K.A. Tallman, A.T. Jacobs, D.C. Liebler, N.A. Porter, and L.J. Marnett Identification of protein targets of 4-hydroxynonenal using click chemistry for ex vivo biotinylation of azido and alkynyl derivatives Chem. Res. Toxicol. 21 2008 432 444
9. C.T. Shearn, R.L. Smathers, B.J. Stewart, K.S. Fritz, J.J. Galligan, N. Hail, and D.R. Petersen PTEN Inhibition by 4-hydroxynonenal leads to increased Akt activation in hepatocytes Mol. Pharmacol. 2011
10. T.M. Wagner, J.E. Mullally, and F.A. Fitzpatrick 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 2006 2598 2604
11. C.T. Shearn, K.S. Fritz, P. Reigan, and D.R. Petersen Modification of Akt2 by 4-hydroxynonenal inhibits insulin-dependent Akt signaling in HepG2 cells Biochemistry 2011
12. S.G. Codreanu, B. Zhang, S.M. Sobecki, D.D. Billheimer, and D.C. Liebler Global analysis of protein damage by the lipid electrophile 4-hydroxy-2-nonenal Mol. Cell. Proteomics 8 2009 670 680
13. S.M. Cheung, J.C. Kornelson, M. Al-Alwan, and A.J. Marshall Regulation of phosphoinositide 3-kinase signaling by oxidants: hydrogen peroxide selectively enhances immunoreceptor-induced recruitment of phosphatidylinositol (3,4) bisphosphate-binding PH domain proteins Cell Signal 19 2007 902 912
14. 2 J. Biol. Chem. 277 2002 20336 20342
15. L. Zhang, S. Sun, J. Zhou, J. Liu, J.H. Lv, X.Q. Yu, C. Li, L. Gong, Q. Yan, M. Deng, L. Xiao, H. Ma, J.P. Liu, Y.L. Peng, D. Wang, G.P. Liao, L.J. Zou, W.B. Liu, Y.M. Xiao, and D.W. Li Knockdown of Akt1 promotes Akt2 upregulation and resistance to oxidative stress-induced apoptosis through control of multiple signaling pathways including MDM2-p53-Bak, GSK3beta-MCL-1 and FOXO3A-Bim Antioxid. Redox Signal. 2011
16. V. Nogueira, Y. Park, C.C. Chen, P.Z. Xu, M.L. Chen, I. Tonic, T. Unterman, and N. Hay Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis Cancer Cell 14 2008 458 470
17. T.M. Covey, K. Edes, G.S. Coombs, D.M. Virshup, and F.A. Fitzpatrick Alkylation of the tumor suppressor PTEN activates Akt and beta-catenin signaling: a mechanism linking inflammation and oxidative stress with cancer PLoS One 5 e13545 2010
18. P. Pettazzoni, S. Pizzimenti, C. Toaldo, P. Sotomayor, L. Tagliavacca, S. Liu, D. Wang, R. Minelli, L. Ellis, P. Atadja, E. Ciamporcero, M.U. Dianzani, G. Barrera, and R. Pili Induction of cell cycle arrest and DNA damage by the HDAC inhibitor panobinostat (LBH589) and the lipid peroxidation end product 4-hydroxynonenal in prostate cancer cells Free Radic. Biol. Med. 50 2011 313 322
19. A. Sharma, R. Sharma, P. Chaudhary, R. Vatsyayan, V. Pearce, P.V. Jeyabal, P. Zimniak, S. Awasthi, and Y.C. Awasthi 4-Hydroxynonenal induces p53-mediated apoptosis in retinal pigment epithelial cells Arch. Biochem. Biophys. 480 2008 85 94
20. J.Y. Lee, M.B. Kang, S.H. Jang, T. Qian, H.J. Kim, C.H. Kim, Y. Kim, and G. Kong Id-1 activates Akt-mediated Wnt signaling and p27(Kip1) phosphorylation through PTEN inhibition Oncogene 28 2009 824 831
21. B.J. Stewart, J.A. Doorn, and D.R. Petersen Residue-specific adduction of tubulin by 4-hydroxynonenal and 4-oxononenal causes cross-linking and inhibits polymerization Chem. Res. Toxicol. 20 2007 1111 1119
22. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J. Immunol. Methods 65 1983 55 63
23. Z. Shao, K. Bhattacharya, E. Hsich, L. Park, B. Walters, U. Germann, Y.M. Wang, J. Kyriakis, R. Mohanlal, K. Kuida, M. Namchuk, F. Salituro, Y.M. Yao, W.M. Hou, X. Chen, M. Aronovitz, P.N. Tsichlis, S. Bhattacharya, T. Force, and H. Kilter c-Jun N-terminal kinases mediate reactivation of Akt and cardiomyocyte survival after hypoxic injury in vitro and in vivo Circ. Res. 98 2006 111 118
24. M. Parola, G. Robino, F. Marra, M. Pinzani, G. Bellomo, G. Leonarduzzi, P. Chiarugi, S. Camandola, G. Poli, G. Waeg, P. Gentilini, and M.U. Dianzani HNE interacts directly with JNK isoforms in human hepatic stellate cells J. Clin. Invest. 102 1998 1942 1950
25. P. Chaudhary, R. Sharma, A. Sharma, R. Vatsyayan, S. Yadav, S.S. Singhal, N. Rauniyar, L. Prokai, S. Awasthi, and Y.C. Awasthi Mechanisms of 4-hydroxy-2-nonenal induced pro- and anti-apoptotic signaling Biochemistry 49 2010 6263 6275
26. B.J. Stewart, J.R. Roede, J.A. Doorn, and D.R. Petersen Lipid aldehyde-mediated cross-linking of apolipoprotein B-100 inhibits secretion from HepG2 cells Biochim. Biophys. Acta 2009
27. Z. Feng, X. Fan, Y. Jiao, and K. Ban Mammalian target of rapamycin regulates expression of beta-catenin in hepatocellular carcinoma Hum. Pathol. 42 2010 659 668
28. Witzel, I.I.; Koh, L.F.; Perkins, N.D. Regulation of cyclin D1 gene expression. Biochem. Soc. Trans. 38:217-222.
29. N.K. Saxena, P.P. Fu, A. Nagalingam, J. Wang, J. Handy, C. Cohen, M. Tighiouart, D. Sharma, and F.A. Anania Adiponectin modulates C-jun N-terminal kinase and mammalian target of rapamycin and inhibits hepatocellular carcinoma Gastroenterology 139 2010 1762 1773 1773 e1761-1765
30. R.F. Schwabe, C.A. Bradham, T. Uehara, E. Hatano, B.L. Bennett, R. Schoonhoven, and D.A. Brenner c-Jun-N-terminal kinase drives cyclin D1 expression and proliferation during liver regeneration Hepatology 37 2003 824 832
31. R. Dai, R. Chen, and H. Li Cross-talk between PI3K/Akt and MEK/ERK pathways mediates endoplasmic reticulum stress-induced cell cycle progression and cell death in human hepatocellular carcinoma cells Int. J. Oncol. 34 2009 1749 1757
32. E. Sontag Protein phosphatase 2A: the Trojan Horse of cellular signaling Cell Signal 13 2001 7 16
33. Z. Wang, H. Yang, S.D. Tachado, J.E. Capo-Aponte, V.N. Bildin, H. Koziel, and P.S. Reinach Phosphatase-mediated crosstalk control of ERK and p38 MAPK signaling in corneal epithelial cells Invest. Ophthalmol. Vis. Sci. 47 2006 5267 5275
34. N. Auge, V. Garcia, F. Maupas-Schwalm, T. Levade, R. Salvayre, and A. Negre-Salvayre Oxidized LDL-induced smooth muscle cell proliferation involves the EGF receptor/PI-3 kinase/Akt and the sphingolipid signaling pathways Arterioscler. Thromb. Vasc. Biol. 22 2002 1990 1995
35. A. Negre-Salvayre, O. Vieira, I. Escargueil-Blanc, and R. Salvayre Oxidized LDL and 4-hydroxynonenal modulate tyrosine kinase receptor activity Mol. Aspects Med. 24 2003 251 261
36. S. Akiba, S. Kumazawa, H. Yamaguchi, N. Hontani, T. Matsumoto, T. Ikeda, M. Oka, and T. Sato Acceleration of matrix metalloproteinase-1 production and activation of platelet-derived growth factor receptor beta in human coronary smooth muscle cells by oxidized LDL and 4-hydroxynonenal Biochim. Biophys. Acta 797-804 1763 2006
37. R. Sharma, A. Sharma, S. Dwivedi, P. Zimniak, S. Awasthi, and Y.C. Awasthi 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 2008 143 156
38. Z. Chang, Q. Zhang, Q. Feng, J. Xu, T. Teng, Q. Luan, C. Shan, Y. Hu, B.A. Hemmings, X. Gao, and Z. Yang Deletion of Akt1 causes heart defects and abnormal cardiomyocyte proliferation Dev. Biol. 347 2010 384 391
39. B. DeBosch, N. Sambandam, C. Weinheimer, and M. Courtois Muslin, A. J. Akt2 regulates cardiac metabolism and cardiomyocyte survival J. Biol. Chem. 281 2006 32841 32851
40. S.A. Santi, and H. Lee Ablation of Akt2 induces autophagy through cell cycle arrest, the downregulation of p70S6K, and the deregulation of mitochondria in MDA-MB231 cells PLoS One 6 e14614 2011
41. L. Moro, A.A. Arbini, J.L. Yao, P.A. di SantAgnese, E. Marra, M. Greco, and D.N.A. Mitochondrial depletion in prostate epithelial cells promotes anoikis resistance and invasion through activation of PI3K/Akt2 Cell Death Differ 16 2009 571 583
42. P. Yang, J.J. Peairs, R. Tano, and G.J. Jaffe Oxidant-mediated Akt activation in human RPE cells Invest. Ophthalmol. Vis. Sci. 47 2006 4598 4606
43. S. Pikkarainen, R.A. Kennedy, A.K. Marshall, L. Tham el, K. Lay, T.A. Kriz, B.S. Handa, A. Clerk, and P.H. Sugden Regulation of expression of the rat orthologue of mouse double minute 2 (MDM2) by H(2)O(2)-induced oxidative stress in neonatal rat cardiac myocytes J. Biol. Chem. 284 2009 27195 27210
44. C.J. Lin, H.Y. Ho, M.L. Cheng, T.H. You, J.S. Yu, and D.T. Chiu Impaired dephosphorylation renders G6PD-knockdown HepG2 cells more susceptible to H(2)O(2)-induced apoptosis Free Radic. Biol. Med. 49 2010 361 373
45. T.K. Lee, K. Man, J.W. Ho, C.K. Sun, K.T. Ng, X.H. Wang, Y.C. Wong, I.O. Ng, R. Xu, and S.T. Fan FTY720 induces apoptosis of human hepatoma cell lines through PI3-K-mediated Akt dephosphorylation Carcinogenesis 25 2004 2397 2405
46. P. Parekh, L. Motiwale, N. Naik, and K.V. Rao Downregulation of cyclin D1 is associated with decreased levels of p38 MAP kinases, Akt/PKB and Pak1 during chemopreventive effects of resveratrol in liver cancer cells Exp. Toxicol. Pathol. 63 2011 167 173
47. X.H. Wang, X.W. Meng, X. Sun, B.R. Liu, M.Z. Han, Y.J. Du, Y.Y. Song, and W. Xu Wnt/beta-catenin signaling regulates MAPK and Akt1 expression and growth of hepatocellular carcinoma cells Neoplasma 58 2011 239 244
48. J.H. Lim, Y.M. Lee, Y.S. Chun, and J.W. Park Reactive oxygen species-mediated cyclin D1 degradation mediates tumor growth retardation in hypoxia, independently of p21cip1 and hypoxia-inducible factor Cancer Sci. 99 2008 1798 1805
49. T. Zhou, K.K. Zhou, K. Lee, G. Gao, T.J. Lyons, R. Kowluru, and J.X. Ma The role of lipid peroxidation products and oxidative stress in activation of the canonical wingless-type mMTV integration site (WNT) pathway in a rat model of diabetic retinopathy Diabetologia 54 2011 459 468
50. A.M. Brunati, M.A. Pagano, A. Bindoli, and M.P. Rigobello Thiol redox systems and protein kinases in hepatic stellate cell regulatory processes Free Radic. Res. 44 2010 363 378
51. Y. Liao, and M.C. Hung Physiological regulation of Akt activity and stability Am. J. Transl. Res. 2 2010 19 42
52. I.G. Maroulakou, W. Oemler, S.P. Naber, and P.N. Tsichlis Akt1 ablation inhibits, whereas Akt2 ablation accelerates, the development of mammary adenocarcinomas in mouse mammary tumor virus (MMTV)-ErbB2/neu and MMTV-polyoma middle T transgenic mice Cancer Res. 67 2007 167 177
53. T. Nemoto, T. Kanai, T. Yanagita, S. Satoh, T. Maruta, N. Yoshikawa, H. Kobayashi, and A. Wada Regulation of Akt mRNA and protein levels by glycogen synthase kinase-3beta in adrenal chromaffin cells: effects of LiCl and SB216763 Eur. J. Pharmacol. 586 2008 82 89
54. D.P. Ponce, J.L. Maturana, P. Cabello, R. Yefi, I. Niechi, E. Silva, R. Armisen, M. Galindo, M. Antonelli, and J.C. Tapia Phosphorylation of AKT/PKB by CK2 is necessary for the AKT-dependent up-regulation of beta-catenin transcriptional activity J. Cell. Physiol. 226 2010 1953 1959
55. D. Kimelman, and W. Xu Beta-catenin destruction complex: insights and questions from a structural perspective Oncogene 25 2006 7482 7491