Regulation of H2O2-induced necrosis by PKC and AMP-activated kinase signaling in primary cultured hepatocytes

American Journal of Physiology - Cell Physiology

Volumn 295, Issue 1, 2008, Pages

  Saberi, Behnam ^a   Shinohara, Mie ^a   Ybanez, Maria D ^a   Hanawa, Naoko ^a   Gaarde, William A ^b   Kaplowitz, Neil ^a   Han, Derick ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b ISIS PHARMACEUTICALS   (United States)

Author keywords

Akt; AMP activated kinase; Hydrogen peroxide; Necrosis; Protein kinase C

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; GLUTATHIONE; HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN KINASE C; AMP ACTIVATED PROTEIN KINASES; AMP-ACTIVATED PROTEIN KINASES; ISOENZYME; MULTIENZYME COMPLEX; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; LIVER CELL; MOUSE; NECROSIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TIME; UPREGULATION; ANIMAL; C57BL MOUSE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; ENZYME ACTIVATION; HEPATOCYTES; HYDROGEN PEROXIDE; ISOENZYMES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, INBRED C57BL; MULTIENZYME COMPLEXES; NECROSIS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 52749091386     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.90654.2007     Document Type: Article

References (62)

1. 2 induce apoptosis through Fenton chemistry independent of the cellular thiol state. Free Radic Biol Med 30: 1008-1018, 2001.
2. 2 gradients across biomembranes. FEBS Lett 475: 121-126, 2000.
3. Antunes F, Salvador A, Marinho HS, Alves R, Pinto RE. Lipid peroxidation in mitochondrial inner membranes. I. An integrative kinetic model. Free Radic Biol Med 21: 917-943, 1996.
4. Baker A, Santos BD, Powis G. Redox control of caspase-3 activity by thioredoxin and other reduced proteins. Biochem Biophys Res Commun 268: 78-81, 2000.
5. Cai J, Jones DP. Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273: 11401-11404, 1998.
6. Chan FK, Shisler J, Bixby JG, Felices M, Zheng L, Appel M, Orenstein J, Moss B, Lenardo MJ. A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J Biol Chem 278: 51613-51621, 2003.
7. Chauhan D, Li G, Hideshima T, Podar K, Mitsiades C, Mitsiades N, Munshi N, Kharbanda S, Anderson KC. JNK-dependent release of mitochondrial protein, Smac, during apoptosis in multiple myeloma (MM) cells. J Biol Chem 278: 17593-17596, 2003.
8. 2. Biochem Biophys Res Commun 287: 92-97, 2001.
9. Conde de la Rosa L, Schoemaker MH, Vrenken TE, Buist-Homan M, Havinga R, Jansen PL, Moshage H. Superoxide anions and hydrogen peroxide induce hepatocyte death by different mechanisms: involvement of JNK and ERK MAP kinases. J Hepatol 44: 918-929, 2006.
10. Croquet F, Brehier A, Gil S, Davy J, Feger J. Five isoenzymes of protein kinase C are expressed in normal and STZ-diabetic rat hepatocytes: effect of phorbol 12-myristate 13-acetate. Biochim Biophys Acta 1315: 163-168, 1996.
11. Czaja MJ. Cell signaling in oxidative stress-induced liver injury. Semin Liver Dis 27: 378-389, 2007.
12. Diaz-Guerra MJ, Bosca L. Lack of translocation of protein kinase C from the cytosol to the membranes in vasopressin-stimulated hepatocytes. Biochem J 269: 163-168, 1990.
13. Domenicotti C, Paola D, Vitali A, Nitti M, d'Abramo C, Cottalasso D, Maloberti G, Biasi F, Poli G, Chiarpotto E, Marinari UM, Pronzato MA. Glutathione depletion induces apoptosis of rat hepatocytes through activation of protein kinase C novel isoforms and dependent increase in AP-1 nuclear binding. Free Radic Biol Med 29: 1280-1290, 2000.
14. Emerling BM, Viollet B, Tormos KV, Chandel NS. Compound C inhibits hypoxic activation of HIF-1 independent of AMPK. FEBS Lett 581: 5727-5731, 2007.
15. Festjens N, Vanden Berghe T, Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757: 1371-1387, 2006.
16. Fukunaga M, Oka M, Ichihashi M, Yamamoto T, Matsuzaki H, Kikkawa U. UV-induced tyrosine phosphorylation of PKC delta and promotion of apoptosis in the HaCaT cell line. Biochem Biophys Res Commun 289: 573-579, 2001.
17. 2. Regulation of reactive oxygen species levels by phosphatidylinositol 3-kinase. J Biol Chem 276: 46379-46385, 2001.
18. Gopalakrishna R, Jaken S. Protein kinase C signaling and oxidative stress. Free Radic Biol Med 28: 1349-1361, 2000.
19. Grabarek J, Ware JA. Protein kinase C activation without membrane contact in platelets stimulated by bryostatin. J Biol Chem 268: 5543-5549, 1993.
20. Gujral JS, Knight TR, Farhood A, Bajt ML, Jaeschke H. Mode of cell death after acetaminophen overdose in mice: apoptosis or oncotic necrosis? Toxicol Sci 67: 322-328, 2002.
21. Gunawan BK, Liu ZX, Han D, Hanawa N, Gaarde WA, Kaplowitz N. c-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity. Gastroenterology 131: 165-178, 2006.
22. Hampton MB, Orrenius S. Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett 414: 552-556, 1997.
23. Han D, Canali R, Rettori D, Kaplowitz N. Effect of glutathione depletion on sites and topology of superoxide and hydrogen peroxide production in mitochondria. Mol Pharmacol 64: 1136-1144, 2003.
24. Han D, Hanawa N, Saberi B, Kaplowitz N. Hydrogen peroxide and redox modulation sensitize primary mouse hepatocytes to TNF-induced apoptosis. Free Radic Biol Med 41: 627-639, 2006.
25. Han D, Hanawa N, Saberi B, Kaplowitz N. Mechanisms of liver injury. III. Role of glutathione redox status in liver injury. Am J Physiol Gastrointest Liver Physiol 291: G1-G7, 2006.
26. Han D, Matsumaru K, Rettori D, Kaplowitz N. Usnic acid-induced necrosis of cultured mouse hepatocytes: inhibition of mitochondrial function and oxidative stress. Biochem Pharmacol 67: 439-451, 2004.
27. Hardie DG. AMP-activated protein kinase as a drug target. Annu Rev Pharmacol Toxicol 47: 185-210, 2007.
28. Hardie DG, Hawley SA, Scott JW. AMP-activated protein kinase-development of the energy sensor concept. J Physiol 574: 7-15, 2006.
29. Harvey PR, Ilson RG, Strasberg SM. The simultaneous determination of oxidized and reduced glutathiones in liver tissue by ion pairing reverse phase high performance liquid chromatography with a coulometric electrochemical detector. Clin Chim Acta 180: 203-212, 1989.
30. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B, Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immun 1: 489-495, 2000.
31. Hsu C, Hsieh YC, Hsu HK, Jao SC, Yang RC. Alteration of protein kinase C isoforms in the liver of septic rat. Shock 17: 41-46, 2002.
32. Jeon BW, Kim KT, Chang SI, Kim HY. Phosphoinositide 3-OH kinase/protein kinase B inhibits apoptotic cell death induced by reactive oxygen species in Saccharomyces cerevisiae. J Biochem 131: 693-699, 2002.
33. Jimenez-Lopez JM, Cederbaum AI. Protein kinase C signaling as a survival pathway against CYP2E1-derived oxidative stress and toxicity in HepG2 cells. J Pharmacol Exp Ther 312: 998-1006, 2005.
34. Kaplowitz N. Biochemical and cellular mechanisms of toxic liver injury. Semin Liver Dis 22: 137-144, 2002.
35. Kefas BA, Heimberg H, Vaulont S, Meisse D, Hue L, Pipeleers D, Van de Casteele M. AICA-riboside induces apoptosis of pancreatic beta cells through stimulation of AMP-activated protein kinase. Diabetologia 46: 250-254, 2003.
36. Kharbanda S, Saxena S, Yoshida K, Pandey P, Kaneki M, Wang Q, Cheng K, Chen YN, Campbell A, Sudha T, Yuan ZM, Narula J, Weichselbaum R, Nalin C, Kufe D. Translocation of SAPK/JNK to mitochondria and interaction with Bcl-xL in response to DNA damage. J Biol Chem 275: 322-327, 2000.
37. 2 cell cycle checkpoints. Cancer Res 63: 31-35, 2003.
38. Li L, Sampat K, Hu N, Zakari J, Yuspa SH. Protein kinase C negatively regulates Akt activity and modifies UVC-induced apoptosis in mouse keratinocytes. J Biol Chem 281: 3237-3243, 2006.
39. Liang J, Shao SH, Xu ZX, Hennessy B, Ding Z, Larrea M, Kondo S, Dumont DJ, Gutterman JU, Walker CL, Slingerland JM, Mills GB. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol 9: 218-224, 2007.
40. Lindsley CW, Zhao Z, Leister WH, Robinson RG, Barnett SF, Defeo-Jones D, Jones RE, Hartman GD, Huff JR, Huber HE, Duggan ME. Allosteric Akt (PKB) inhibitors: discovery and SAR of isozyme selective inhibitors. Bioorg Med Chem Lett 15: 761-764, 2005.
41. Liu H, Lo CR, Czaja MJ. NF-kappaB inhibition sensitizes hepatocytes to TNF-induced apoptosis through a sustained activation of JNK and c-Jun. Hepatology 35: 772-778, 2002.
42. Long YC, Zierath JR. AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest 116: 1776-1783, 2006.
43. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marme D, Schachtele C. Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J Biol Chem 268: 9194-9197, 1993.
44. Newton AC. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem Rev 101: 2353-2364, 2001.
45. Peralta C, Bartrons R, Serafin A, Blazquez C, Guzman M, Prats N, Xaus C, Cutillas B, Gelpi E, Rosello-Catafau J. Adenosine monophosphate-activated protein kinase mediates the protective effects of ischemic preconditioning on hepatic ischemia-reperfusion injury in the rat. Hepatology 34: 1164-1173, 2001.
46. Proskuryakov SY, Konoplyannikov AG, Gabai VL. Necrosis: a specific form of programmed cell death? Exp Cell Res 283: 1-16, 2003.
47. Russell RR, 3rd Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ, Young LH. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest 114: 495-503, 2004.
48. 2 occurs upstream of phosphatidylinositol 3-kinase: no evidence for oxidative inhibition of PTEN. Arch Biochem Biophys 386: 275-280, 2001.
49. Schroeter H, Boyd CS, Ahmed R, Spencer JP, Duncan RF, Rice-Evans C, Cadenas E. c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis. Biochem J 372: 359-369, 2003.
50. 2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem J 336: 241-246, 1998.
51. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 101: 3329-3335, 2004.
52. Stensman H, Raghunath A, Larsson C. Autophosphorylation suppresses whereas kinase inhibition augments the translocation of protein kinase Calpha in response to diacylglycerol. J Biol Chem 279: 40576-40583, 2004.
53. Takahashi H, Namiki H. Mechanism of membrane redistribution of protein kinase C by its ATP-competitive inhibitors. Biochem J 405: 331-340, 2007.
54. Tapodi A, Debreceni B, Hanto K, Bognar Z, Wittmann I, Gallyas F Jr, Varbiro G, Sumegi B. Pivotal role of Akt activation in mitochondrial protection and cell survival by poly(ADP-ribose)polymerase-1 inhibition in oxidative stress. J Biol Chem 280: 35767-35775, 2005.
55. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T, Ichijo H. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2: 222-228, 2001.
56. Tsuruta F, Sunayama J, Mori Y, Hattori S, Shimizu S, Tsujimoto Y, Yoshioka K, Masuyama N, Gotoh Y. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 23: 1889-1899, 2004.
57. Waldron RT, Rey O, Zhukova E, Rozengurt E. Oxidative stress induces protein kinase C-mediated activation loop phosphorylation and nuclear redistribution of protein kinase D. J Biol Chem 279: 27482-27493, 2004.
58. Wang Y, Schattenberg JM, Rigoli RM, Storz P, Czaja MJ. Hepatocyte resistance to oxidative stress is dependent on protein kinase C-mediated down-regulation of c-Jun/AP-1. J Biol Chem 279: 31089-31097, 2004.
59. Wen HC, Huang WC, Ali A, Woodgett JR, Lin WW. Negative regulation of phosphatidylinositol 3-kinase and Akt signalling pathway by PKC. Cell Signal 15: 37-45, 2003.
60. Wilkinson SE, Parker PJ, Nixon JS. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem J 294: 335-337, 1993.
61. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174, 2001.
62. Zhou Q, Lam PY, Han D, Cadenas E. c-Jun N-terminal kinase regulates mitochondrial bioenergetics by modulating pyruvate dehydrogenase activity in primary cortical neurons. J Neurochem 104: 325-335, 2008.