Protein tyrosine phosphatase 1B modulates GSK3b/Nrf2 and IGFIR signaling pathways in acetaminophen-induced hepatotoxicity

Cell Death and Disease

Volumn 4, Issue 5, 2013, Pages

  Mobasher, M A ^a,b   Gonzalez Rodriguez A ^a,b   Santamaria B ^a,b   Ramos, S ^c   Martin M A ^b,c   Goya, L ^c   Rada, P ^a,b   Letzig, L ^d   James, L P ^d   Cuadrado, A ^a,b   Martin Perez J ^a   Simpson, K J ^e   Muntane J ^f,g   Valverde, A M ^a,b  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INSTITUTE OF FOOD SCIENCE   (Spain)

^d ARKANSAS CHILDREN S HOSPITAL   (United States)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f Instituto de Biomedicina de Sevilla   (Spain)

^g INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Apoptosis; Liver injury; Oxidative stress; Survival signaling; Tyrosine phosphorylation

Indexed keywords

CASPASE 3; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; PARACETAMOL; PROTEIN BCL XL; PROTEIN KINASE B; PROTEIN MCL 1; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE 1B; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NRF2;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL DEATH; CELL IMMORTALIZATION; CELL SURVIVAL; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG OVERDOSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; LIVER CELL; LIVER GRAFT; LIVER PROTECTION; LIVER TOXICITY; LIVER TRANSPLANTATION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TOXIC HEPATITIS; UPREGULATION; WILD TYPE;

ACETAMINOPHEN; ANIMALS; APOPTOSIS; CELLS, CULTURED; DRUG-INDUCED LIVER INJURY; GLUTATHIONE; GLYCOGEN SYNTHASE KINASE 3; HEPATOCYTES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; RECEPTOR, IGF TYPE 1; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

MUS;

EID: 84879407019     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.150     Document Type: Article

References (49)

1. Rumack BH. Acetaminophen misconceptions. Hepatology 2004; 40: 10-15.
2. Lee WM. Acetaminophen and the U.S. Acute Liver Failure Study Group: lowering the risks of hepatic failure. Hepatology 2004; 40: 6-9.
3. Litovitz TL, Klein-Schwartz W, White S, Cobaugh DJ, Youniss J, Omslaer JC et al. 2000 Annual report of the American Association of Poison Control Centers Toxic Exposure Surveillance System. Am J Emerg Med 2001 19: 337-395.
4. Lee WM. Acetaminophen toxicity: changing perceptions on a social/medical issue. Hepatology 2007; 46: 966-970.
5. Kaplowitz N. Acetaminophen hepatoxicity: what do we know, what don't we know, and what do we do next? Hepatology 2004; 40: 23-26.
6. Ramachandran R, Kakar S. Histological patterns in drug-induced liver disease. J Clin Pathol 2009; 62: 481-492.
7. James LP, Mayeux PR, Hinson JA. Acetaminophen-induced hepatotoxicity. Drug Metab Dispos 2003; 31: 1499-1506.
8. Jaeschke H, Bajt ML. Intracellular signaling mechanisms of acetaminophen-induced liver cell death. Toxicol Sci 2006; 89: 31-41.
9. Han D, Shinohara M, Ybanez MD, Saberi B, Kaplowitz N. Signal transduction pathways involved in drug-induced liver injury. Handb Exp Pharmacol 2010; 196: 267-310.
10. Thummel KE, Lee CA, Kunze KL, Nelson SD, Slattery JT. Oxidation of acetaminophen to N-acetyl-p-aminobenzoquinone imine by human CYP3A4. Biochem Pharmacol 1993; 45: 1563-1569.
11. Newton JF, Hoefle D, Gemborys MW, Mudge GH, Hook JB. Metabolism and excretion of a glutathione conjugate of acetaminophen in the isolated perfused rat kidney. J Pharmacol Exp Ther 1986; 237: 519-524.
12. Ghosh A, Sil PC. Protection of acetaminophen induced mitochondrial dysfunctions and hepatic necrosis via Akt-NF-kappaB pathway: role of a novel plant protein. Chem Biol Interact 2009; 177: 96-106.
13. Reid AB, Kurten RC, McCullough SS, Brock RW, Hinson JA. Mechanisms of acetaminophen-induced hepatotoxicity: role of oxidative stress and mitochondrial permeability transition in freshly isolated mouse hepatocytes. J Pharmacol Exp Ther 2005; 312: 509-516.
14. Jaeschke H, McGill MR, Ramachandran A. Oxidant stress, mitochondria, and cell death mechanisms in drug-induced liver injury: lessons learned from acetaminophen hepatotoxicity. Drug Metab Rev 2012; 44: 88-106.
15. Enomoto A, Itoh K, Nagayoshi E, Haruta J, Kimura T, O'Connor T et al. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci 2001; 59: 169-177.
16. Tonks NK, Neel BG. Combinatorial control of the specificity of protein tyrosine phosphatases. Curr Opin Cell Biol 2001; 13: 182-195.
17. Frangioni JV, Beahm PH, Shifrin V, Jost CA, Neel BG. The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 1992; 68: 545-560.
18. Salmeen A, Andersen JN, Myers MP, Tonks NK, Barford D. Molecular basis for the dephosphorylation of the activation segment of the insulin receptor by protein tyrosine phosphatase 1B. Mol Cell 2000; 6: 1401-1412.
19. Zabolotny JM, Bence-Hanulec KK, Stricker-Krongrad A, Haj F, Wang Y, Minokoshi Y et al. PTP1B regulates leptin signal transduction in vivo. Dev Cell 2002; 2: 489-495.
20. Haj FG, Markova B, Klaman LD, Bohmer FD, Neel BG. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatase-1B. J Biol Chem 2003; 278: 739-744.
21. Sangwan V, Paliouras GN, Cheng A, Dube N, Tremblay ML, Park M. Protein-tyrosine phosphatase 1B deficiency protects against Fas-induced hepatic failure. J Biol Chem 2006; 281: 221-228.
22. Buckley DA, Cheng A, Kiely PA, Tremblay ML, O'Connor R. Regulation of insulin-like growth factor type I (IGF-I) receptor kinase activity by protein tyrosine phosphatase 1B (PTP-1B) and enhanced IGF-I-mediated suppression of apoptosis and motility in PTP-1B-deficient fibroblasts. Mol Cell Biol 2002; 22: 1998-2010.
23. Fabregat I, Herrera B, Fernandez M, Alvarez AM, Sanchez A, Roncero C et al. Epidermal growth factor impairs the cytochrome C/caspase-3 apoptotic pathway induced by transforming growth factor beta in rat fetal hepatocytes via a phosphoinositide 3-kinase-dependent pathway. Hepatology 2000; 32: 528-535.
24. Valverde AM, Fabregat I, Burks DJ, White MF, Benito M. IRS-2 mediates the antiapoptotic effect of insulin in neonatal hepatocytes. Hepatology 2004; 40: 1285-1294.
25. Gonzalez-Rodriguez A, Escribano O, Alba J, Rondinone CM, Benito M, Valverde AM. Levels of protein tyrosine phosphatase 1B determine susceptibility to apoptosis in serum-deprived hepatocytes. J Cell Physiol 2007; 212: 76-88.
26. Kon K, Kim JS, Jaeschke H, Lemasters JJ. Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 2004; 40: 1170-1179.
27. Niture SK, Jain AK, Shelton PM, Jaiswal AK. Src subfamily kinases regulate nuclear export and degradation of transcription factor Nrf2 to switch off Nrf2-mediated antioxidant activation of cytoprotective gene expression. J Biol Chem 2011; 286: 28821-28832.
28. Jain AK, Jaiswal AK. GSK-3beta acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J Biol Chem 2007; 282: 16502-16510.
29. Zabolotny JM, Kim YB, Welsh LA, Kershaw EE, Neel BG, Kahn BB. Protein-tyrosine phosphatase 1B expression is induced by inflammation in vivo. J Biol Chem 2008; 283: 14230-14241.
30. Sanderson SO, Smyrk TC. The use of protein tyrosine phosphatase 1B and insulin receptor immunostains to differentiate nonalcoholic from alcoholic steatohepatitis in liver biopsy specimens. Am J Clin Pathol 2005; 123: 503-509.
31. Garcia-Monzon C, Lo Iacono O, Mayoral R, Gonzalez-Rodriguez A, Miquilena-Colina ME, Lozano-Rodriguez T et al. Hepatic insulin resistance is associated with increased apoptosis and fibrogenesis in nonalcoholic steatohepatitis and chronic hepatitis C. J Hepatol 54: 142-152.
32. Bechmann LP, Jochum C, Kocabayoglu P, Sowa JP, Kassalik M, Gieseler RK et al. Cytokeratin 18-based modification of the MELD score improves prediction of spontaneous survival after acute liver injury. J Hepatol 53: 639-647.
33. Antoine DJ, Jenkins RE, Dear JW, Williams DP, McGill MR, Sharpe MR et al. Molecular forms of HMGB1 and keratin-18 as mechanistic biomarkers for mode of cell death and prognosis during clinical acetaminophen hepatotoxicity. J Hepatol May 56: 1070-1079.
34. Craig DG, Lee P, Pryde EA, Masterton GS, Hayes PC, Simpson KJ. Circulating apoptotic and necrotic cell death markers in patients with acute liver injury. Liver Int 31: 1127-1136.
35. McGregor AH, More LJ, Simpson KJ, Harrison DJ. Liver death and regeneration in paracetamol toxicity. Hum Exp Toxicol 2003; 22: 221-227.
36. Antoine DJ, Williams DP, Kipar A, Jenkins RE, Regan SL, Sathish JG et al. High-mobility group box-1 protein and keratin-18, circulating serum proteins informative of acetaminophen-induced necrosis and apoptosis in vivo. Toxicol Sci 2009; 112: 521-531.
37. Tovar V, Alsinet C, Villanueva A, Hoshida Y, Chiang DY, Sole M et al. IGF activation in a molecular subclass of hepatocellular carcinoma and pre-clinical efficacy of IGF-1R blockage. J Hepatol Apr 52: 550-559.
38. Vinayagamoorthi R, Bobby Z, Sridhar MG. Antioxidants preserve redox balance and inhibit c-Jun-N-terminal kinase pathway while improving insulin signaling in fat-fed rats: evidence for the role of oxidative stress on IRS-1 serine phosphorylation and insulin resistance. J Endocrinol 2008; 197: 287-296.
39. Nieto-Vazquez I, Fernandez-Veledo S, de Alvaro C, Lorenzo M. Dual role of interleukin-6 in regulating insulin sensitivity in murine skeletal muscle. Diabetes 2008; 57: 3211-3221.
40. Lu X, Malumbres R, Shields B, Jiang X, Sarosiek KA, Natkunam Y et al. PTP1B is a negative regulator of interleukin 4-induced STAT6 signaling. Blood 2008; 112: 4098-4108.
41. Gonzalez-Rodriguez A, Mas Gutierrez JA, Sanz-Gonzalez S, Ros M, Burks DJ, Valverde AM. Inhibition of PTP1B restores IRS1-mediated hepatic insulin signaling in IRS2-deficient mice. Diabetes 2010; 59: 588-599.
42. Pichard L, Raulet E, Fabre G, Ferrini JB, Ourlin JC, Maurel P. Human hepatocyte culture. Methods Mol Biol 2006; 320: 283-293.
43. Gonzalez-Rodriguez A, Clampit JE, Escribano O, Benito M, Rondinone CM, Valverde AM. Developmental switch from prolonged insulin action to increased insulin sensitivity in protein tyrosine phosphatase 1B-deficient hepatocytes. Endocrinology 2007; 148: 594-608.
44. Gonzalez-Rodriguez A, Mas-Gutierrez JA, Mirasierra M, Fernandez-Perez A, Lee YJ, Ko HJ et al. Essential role of protein tyrosine phosphatase 1B in obesity-induced inflammation and peripheral insulin resistance during aging. Aging Cell 2012; 11: 284-296.
45. Welder AA Acosta D. (ed) Enzyme Leakage As An Indicator of Cytotoxicity in Culture Cells. Academic Press: New York, NY, USA, 1994, p 3.
46. Hissin PJ, Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976; 74: 214-226.
47. Rodriguez-Ramiro I, Martin MA, Ramos S, Bravo L, Goya L. Comparative effects of dietary flavanols on antioxidant defences and their response to oxidant-induced stress on Caco2 cells. Eur J Nutr 50: 313-322.
48. Richert S, Wehr NB, Stadtman ER, Levine RL. Assessment of skin carbonyl content as a noninvasive measure of biological age. Arch Biochem Biophys 2002; 397: 430-432.
49. Muldrew KL, James LP, Coop L, McCullough SS, Hendrickson HP, Hinson JA et al. Determination of acetaminophen-protein adducts in mouse liver and serum and human serum after hepatotoxic doses of acetaminophen using high-performance liquid chromatography with electrochemical detection. Drug Metab Dispos 2002; 30: 446-451.