General Review Article

Acetaminophen Oxidation and Inflammatory Markers – A Review of Hepatic Molecular Mechanisms and Preclinical Studies

Author(s): Silvio Terra Stefanello, Nelson Rodrigues de Carvalho, Simone Beder Reis, Felix Alexandre Antunes Soares and Rômulo Pillon Barcelos*

Volume 21, Issue 12, 2020

Page: [1225 - 1236] Pages: 12

DOI: 10.2174/1389450121666200510014418

Price: $65

Abstract

Acetaminophen is a widely used analgesic for pain management, especially useful in chronic diseases, such as rheumatoid arthritis. However, easy access to this medicine has increased the occurrence of episodes of poisoning. Patients often develop severe liver damage, which may quickly lead to death. Consequently, numerous studies have been conducted to identify new biomarkers that allow the prediction of the degree of acetaminophen intoxication and thus intervene in a timely manner to save patients’ lives. This review highlights the main mechanisms of the induction and progression of liver damage arising from acetaminophen poisoning. In addition, we have discussed the possibility of using new clinical biomarkers for detecting acetaminophen poisoning.

Keywords: APAP, biomarkers, intoxication, NAPQI, liver damage, preclinical studies.

Graphical Abstract
[1]
Larson AM, Polson J, Fontana RJ, Davern TJ, Lalani E, Hynan LS, et al. Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study. Hepatology 2005; 42(6): 1364-72.http://doi.wiley.com/10.1002/hep.20948
[http://dx.doi.org/10.1002/hep.20948]
[2]
Clark R, Fisher JE, Sketris IS, Johnston GM. Population prevalence of high dose paracetamol in dispensed paracetamol/opioid prescription combinations: an observational study BMC Clin Pharmacol 12(1): 11 2012.http://link.springer.com/10.1186/1472-6904-12-11
[3]
Jaw S, Jeffery EH. Interaction of caffeine with acetaminophen. 1. Correlation of the effect of caffeine on acetaminophen hepatotoxicity and acetaminophen bioactivation following treatment of mice with various cytochrome P450 inducing agents Biochem Pharmacol 1993; 46(3): 493-501.http://www.ncbi.nlm.nih.gov/pubmed/8347173
[4]
Bernal W, Auzinger G, Dhawan A, Wendon J. Acute liver failure. Lancet (London, England) 2010; 376(9736): 190-201.https://linkinghub.elsevier.com/retrieve/pii/S0140673610602747
[http://dx.doi.org/10.1016/S0140-6736(10)60274-7]
[5]
Craig DGN, Bates CM, Davidson JS, Martin KG, Hayes PC, Simpson KJ. Overdose pattern and outcome in paracetamol-induced acute severe hepatotoxicity. Br J Clin Pharmacol 2011; 71(2): 273-82.http://doi.wiley.com/10.1111/j.1365-2125.2010.03819.x
[http://dx.doi.org/10.1111/j.1365-2125.2010.03819.x]
[6]
McGill MR, Jaeschke H. Biomarkers of drug-induced liver injury: progress and utility in research, medicine, and regulation Expert Rev Mol Diagn 2018; 18(9): 797-807. https://www.tandfonline.com/doi/full/10.1080/14737159.2018.1508998
[http://dx.doi.org/10.1080/14737159.2018.1508998]
[7]
Lee WM. Acetaminophen (APAP) hepatotoxicity—Isn’t it time for APAP to go away? J Hepatol 2017; 67(6): 1324-31.http://www.ncbi.nlm.nih.gov/pubmed/28734939
[8]
Bacle A, Pronier C, Gilardi H, Polard E, Potin S, Scailteux L-M. Hepatotoxicity risk factors and acetaminophen dose adjustment, do prescribers give this issue adequate consideration? A French university hospital study. Eur J Clin Pharmacol 2019; 75(8): 1143-51.http://link.springer.com/10.1007/s00228-019-02674-5
[9]
Lee WM. Acetaminophen and the U.S. acute liver failure study group: Lowering the risks of hepatic failure. Hepatology 2004; 40(1): 6-9.http://www.ncbi.nlm.nih.gov/pubmed/15239078
[10]
Knockaert L, Descatoire V, Vadrot N, Fromenty B, Robin M-A. Mitochondrial CYP2E1 is sufficient to mediate oxidative stress and cytotoxicity induced by ethanol and acetaminophen. Toxicol In Vitro 2011; 25(2): 475-84.https://linkinghub.elsevier.com/retrieve/pii/S0887233310003115
[11]
Hinson JA, Reid AB, McCullough SS, James LP. 2004.http://www.tandfonline.com/doi/full/10.1081/DMR-200033494
[12]
McGill MR, Jaeschke H. Metabolism and disposition of acetaminophen: recent advances in relation to hepatotoxicity and diagnosis Pharm Res 2013; 30(9): 2147-87.http://link.springer.com/10.1007/s11095-013-1007-6
[http://dx.doi.org/10.1007/s11095-013-1007-6]
[13]
Lancaster EM, Hiatt JR, Zarrinpar A. Acetaminophen hepatotoxicity: an updated review Arch Toxicol 2015; 89(2): 193-9.http://link.springer.com/10.1007/s00204-014-1432-2
[http://dx.doi.org/10.1007/s00204-014-1432-2]
[14]
Brune K, Renner B, Tiegs G. Acetaminophen/paracetamol: A history of errors, failures and false decisions. Eur J Pain 2015; 19(7): 953-65.http://doi.wiley.com/10.1002/ejp.621
[15]
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(1): 88-106.http://www.tandfonline.com/doi/full/10.3109/03602532.2011.602688
[http://dx.doi.org/10.3109/03602532.2011.602688]
[16]
Walubo A, Barr S, Abraham AM, Coetsee C. The role of cytochrome-P450 inhibitors in the prevention of hepatotoxicity after paracetamol overdose in rats. Hum Exp Toxicol 2004; 23(1): 49-54.http://journals.sagepub.com/doi/10.1191/0960327104ht415oa
[http://dx.doi.org/10.1191/0960327104ht415oa]
[17]
Abdelmegeed MA, Jang S, Banerjee A, Hardwick JP, Song B-J. Robust protein nitration contributes to acetaminophen-induced mitochondrial dysfunction and acute liver injury Free Radic Biol Med 2013; 60: 211-.https://linkinghub.elsevier.com/retrieve/pii/S0891584913000713
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.02.018]
[18]
Zhao P, Kalhorn TF, Slattery JT. Selective mitochondrial glutathione depletion by ethanol enhances acetaminophen toxicity in rat liver Hepatology 2002; 36(2): 326-5.http://doi.wiley.com/10.1053/jhep.2002.34943
[http://dx.doi.org/10.1053/jhep.2002.34943]
[19]
Panatto JP, Jeremias IC, Ferreira GK, Ramos AC, Rochi N, Gonçalves CL, et al. Inhibition of mitochondrial respiratory chain in the brain of rats after hepatic failure induced by acetaminophen Mol Cell Biochem 2011; 350(1-2): 149-54.http://link.springer.com/10.1007/s11010-010-0689-x
[http://dx.doi.org/10.1007/s11010-010-0689-x]
[20]
Ghosh J, Das J, Manna P, Sil PC. Acetaminophen induced renal injury via oxidative stress and TNF-alpha production: therapeutic potential of arjunolic acid. Toxicology 2010; 268(1-2): 8-18.https://linkinghub.elsevier.com/retrieve/pii/S0300483X09005873
[21]
Jaeschke H, McGill MR, Williams CD, Ramachandran A. Current issues with acetaminophen hepatotoxicity--a clinically relevant model to test the efficacy of natural products Life Sci. 2011; 88(17-18): 737-45.https://linkinghub.elsevier.com/retrieve/pii/S0024320511000609
[22]
Ni H-M, Boggess N, McGill MR, Lebofsky M, Borude P, Apte U, et al. Liver-specific loss of Atg5 causes persistent activation of Nrf2 and protects against acetaminophen-induced liver injury. Toxicol Sci 2012; 127(2): 438-50.https://academic.oup.com/toxsci/article/1711206/Liver-Specific
[http://dx.doi.org/10.1093/toxsci/kfs133]
[23]
Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA 2001; 98(8): 4611-6.http://www.pnas.org/cgi/doi/10.1073/pnas.081082098
[http://dx.doi.org/10.1073/pnas.081082098]
[24]
Tong HY, Medrano N, Borobia AM, Martínez AM, Martín J, Ruiz JA, et al. Hepatotoxicity induced by acute and chronic paracetamol overdose in adults Where do we stand? Regul Toxicol Pharmacol 2015; 72(2): 370-8.https://linkinghub.elsevier.com/retrieve/pii/S0273230015001105
[25]
McKinney AM, Lohman BD, Sarikaya B, Uhlmann E, Spanbauer J, Singewald T, et al. Acute hepatic encephalopathy: diffusion weighted and fluid-attenuated inversion recovery findings, and correlation with plasma ammonia level and clinical outcome AJNR Am J Neuroradiol 2010; 31(8): 1471-9.http://www.ajnr.org/lookup/doi/10.3174/ajnr.A2112
[http://dx.doi.org/10.3174/ajnr.A2112]
[26]
Mazer M, Perrone J. Acetaminophen-induced nephrotoxicity: pathophysiology, clinical manifestations, and management. J Med Toxicol 2008; 4(1): 2-6.http://www.ncbi.nlm.nih.gov/pubmed/18338302
[27]
Mossanen J, Tacke F. Acetaminophen-induced acute liver injury in mice Lab Anim 2015; 49(1): 30-6.http://www.ncbi.nlm.nih.gov/pubmed/25835736
[http://dx.doi.org/10.1177/0023677215570992]
[28]
Rahman TM, Hodgson HJ. Animal models of acute hepatic failure. Int J Exp Pathol 2000; 81(2): 145-57.http://www.ncbi.nlm.nih.gov/pubmed/10762442
[29]
Rahman TM, Selden AC, Hodgson HJF. A novel model of acetaminophen-induced acute hepatic failure in rabbits. J Surg Res 2002; 106(2): 264-72.http://www.ncbi.nlm.nih.gov/pubmed/12175977
[30]
Krasniak AE, Knipp GT, Svensson CK, Liu W. Pharmacogenomics of acetaminophen in pediatric populations: a moving target Front Genet 2014; 5: 314.http://journal.frontiersin.org/article/10.3389/fgene.2014.00314/abstract
[http://dx.doi.org/10.3389/fgene.2014.00314]
[31]
Gardner CR, Mishin V, Laskin JD, Laskin DL. Exacerbation of acetaminophen hepatotoxicity by the anthelmentic drug fenbendazole. Toxicol Sci 2012; 125(2): 607-12.https://academic.oup.com/toxsci/article/1612022/Exacerbation
[http://dx.doi.org/10.1093/toxsci/kfr301]
[32]
Martin-Murphy BV, Holt MP, Ju C. The role of damage associated molecular pattern molecules in acetaminophen-induced liver injury in mice. Toxicol Lett 2010; 192(3): 387-94.https://linkinghub.elsevier.com/retrieve/pii/S0378427409015306
[http://dx.doi.org/10.1016/j.toxlet.2009.11.016]
[33]
Jaeschke H, Knight TR, Bajt ML. The role of oxidant stress and reactive nitrogen species in acetaminophen hepatotoxicity Toxicol Lett 2003; 144(3): 279-88.http://www.ncbi.nlm.nih.gov/pubmed/12927346
[http://dx.doi.org/10.1016/S0378-4274(03)00239-X]
[34]
Baird L, Swift S, Llères D, Dinkova-Kostova AT. Monitoring Keap1-Nrf2 interactions in single live cells Biotechnol Adv 2014; 32(6): 1133-44.https://linkinghub.elsevier.com/retrieve/pii/S0734975014000408
[http://dx.doi.org/10.1016/j.biotechadv.2014.03.004]
[35]
Knight TR, Fariss MW, Farhood A, Jaeschke H. Role of lipid peroxidation as a mechanism of liver injury after acetaminophen overdose in mice. Toxicol Sci 2003; 76(1): 229-36.https://academic.oup.com/toxsci/article-lookup/doi/10.1093/toxsci/kfg220
[http://dx.doi.org/10.1093/toxsci/kfg220]
[36]
Paupe V, Dassa EP, Goncalves S, Auchère F, Lönn M, Holmgren A, et al. Impaired nuclear Nrf2 translocation undermines the oxidative stress response in Friedreich ataxia Andreu AL, editor PLoS One 2009; 4(1): 4253.https://dx.plos.org/10.1371/journal.pone. 0004253
[http://dx.doi.org/10.1371/journal.pone.0004253]
[37]
Dayoub R, Vogel A, Schuett J, Lupke M, Spieker SM, Kettern N, et al. Nrf2 activates augmenter of liver regeneration (ALR) via antioxidant response element and links oxidative stress to liver regeneration. Mol Med 2013; 19(1): 237-44.http://molmed.org/content/pdfstore/13_027_Dayoub.pdf
[38]
Williams CD, Bajt ML, Sharpe MR, McGill MR, Farhood A, Jaeschke H. Neutrophil activation during acetaminophen hepatotoxicity and repair in mice and humans Toxicol Appl Pharmacol 2014; 275(2): 122-33.https://linkinghub.elsevier.com/retrieve/pii/S0041008X14000064
[http://dx.doi.org/10.1016/j.taap.2014.01.004]
[39]
Jaeschke H, Williams CD, Ramachandran A, Bajt ML. Acetaminophen hepatotoxicity and repair: the role of sterile inflammation and innate immunity. Liver Int 2012; 32(1): 8-20.
[http://dx.doi.org/10.1111/j.1478-3231.2011.02501.x] [PMID: 21745276]
[40]
Antoniades CG, Khamri W, Abeles RD, et al. Secretory leukocyte protease inhibitor: a pivotal mediator of anti-inflammatory responses in acetaminophen-induced acute liver failure. Hepatology 2014; 59(4): 1564-76.
[http://dx.doi.org/10.1002/hep.26933] [PMID: 24282114]
[41]
Rolando N, Wade J, Davalos M, Wendon J, Philpott-Howard J, Williams R. The systemic inflammatory response syndrome in acute liver failure Hepatology 2000; 32(4): 734-9.http://doi.wiley.com/10.1053/jhep.2000.17687
[http://dx.doi.org/10.1053/jhep.2000.17687]
[42]
Leithead JA, Ferguson JW, Bates CM, Davidson JS, Lee A, Bathgate AJ, et al. The systemic inflammatory response syndrome is predictive of renal dysfunction in patients with non-paracetamol-induced acute liver failure Gut 2009; 58(3): 443-9.http://gut.bmj.com/cgi/doi/10.1136/gut.2008.154120
[http://dx.doi.org/10.1136/gut.2008.154120]
[43]
Jaeschke H. Role of inflammation in the mechanism of acetaminophen-induced hepatotoxicity. Expert Opin Drug Metab Toxicol 2005; 1(3): 389-97.
[http://dx.doi.org/10.1517/17425255.1.3.389 ] [PMID: 16863451]
[44]
Liu Z-X, Kaplowitz N. Role of innate immunity in acetaminophen-induced hepatotoxicity. Expert Opin Drug Metab Toxicol 2006; 2(4): 493-503.
[http://dx.doi.org/10.1517/17425255.2.4.493] [PMID: 16859400]
[45]
Possamai LA, Antoniades CG, Anstee QM, et al. Role of monocytes and macrophages in experimental and human acute liver failure. World J Gastroenterol 2010; 16(15): 1811-9.
[http://dx.doi.org/10.3748/wjg.v16.i15.1811] [PMID: 20397256]
[46]
Holt MP, Cheng L, Ju C. Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J Leukoc Biol 2008; 84(6): 1410-21.
[http://dx.doi.org/10.1189/jlb.0308173] [PMID: 18713872]
[47]
Antoniades CG, Quaglia A, Taams LS, et al. Source and characterization of hepatic macrophages in acetaminophen-induced acute liver failure in humans. Hepatology 2012; 56(2): 735-46.
[http://dx.doi.org/10.1002/hep.25657] [PMID: 22334567]
[48]
Hiraoka A, Horiike N, Akbar SM, Michitaka K, Matsuyama T, Onji M. Soluble CD163 in patients with liver diseases: very high levels of soluble CD163 in patients with fulminant hepatic failure. J Gastroenterol 2005; 40(1): 52-6.http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15692789[Internet].
[http://dx.doi.org/10.1007/s00535-004-1493-8] [PMID: 15692789]
[49]
Møller HJ, Grønbaek H, Schiødt FV, et al. Soluble CD163 from activated macrophages predicts mortality in acute liver failure. J Hepatol 2007; 47(5): 671-6.
[http://dx.doi.org/10.1016/j.jhep.2007.05.014] [PMID: 17629586]
[50]
Jaeschke H. Innate immunity and acetaminophen-induced liver injury: why so many controversies? Hepatology 2008; 48(3): 699-701.http://www.ncbi.nlm.nih.gov/pubmed/18752320
[http://dx.doi.org/10.1002/hep.22556]
[51]
Bernsmeier C, Antoniades CG, Wendon J. What’s new in acute liver failure? Intensive Care Med 2014; 40(10): 1545-8.http://www.ncbi.nlm.nih.gov/pubmed/24981954
[http://dx.doi.org/10.1007/s00134-014-3350-4]
[52]
Antoniades CG, Berry PA, Wendon JA, Vergani D. The importance of immune dysfunction in determining outcome in acute liver failure. J Hepatol 2008; 49(5): 845-61.
[http://dx.doi.org/10.1016/j.jhep.2008.08.009] [PMID: 18801592]
[53]
Lawson JA, Farhood A, Hopper RD, Bajt ML, Jaeschke H. The hepatic inflammatory response after acetaminophen overdose: role of neutrophils. Toxicol Sci 2000; 54(2): 509-16.
[http://dx.doi.org/10.1093/toxsci/54.2.509] [PMID: 10774834]
[54]
Woolbright BL, Jaeschke H. Role of the inflammasome in acetaminophen-induced liver injury and acute liver failure J Hepatol 2017; 66(4): 836-48.https://linkinghub.elsevier.com/retrieve/pii/S0168827816306936
[55]
Schwabe RF, Seki E, Brenner DA. Toll-like receptor signaling in the liver Gastroenterology 2006; 130(6): 1886-900.http://www. ncbi.nlm.nih.gov/pubmed/16697751
[http://dx.doi.org/10.1053/j.gastro.2006.01.038]
[56]
Chung RT, Stravitz RT, Fontana RJ, Schiodt FV, Mehal WZ, Reddy KR, et al. Pathogenesis of liver injury in acute liver failure Gastroenterology 2012; 43(3): e1-7.http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3641754&tool=pmcentrez&rendertype= abstract
[http://dx.doi.org/10.1053/j.gastro.2012.07.011]
[57]
Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418(6894): 191-5.
[http://dx.doi.org/10.1038/nature00858] [PMID: 12110890]
[58]
Craig DG, Lee P, Pryde EA, Hayes PC, Simpson KJ. Serum neopterin and soluble CD163 as markers of macrophage activation in paracetamol (acetaminophen)-induced human acute liver injury. Aliment Pharmacol Ther 2013; 38(11-12): 1395-404.http://www.ncbi.nlm.nih.gov/pubmed/24138337
[59]
Chazaud B. Macrophages: supportive cells for tissue repair and regeneration Immunobiology 2014; 219(3): 172-3.http://www.ncbi.nlm.nih.gov/pubmed/24080029
[http://dx.doi.org/10.1016/j.imbio.2013.09.001]
[60]
Chiu H, Gardner CR, Dambach DM, et al. Role of tumor necrosis factor receptor 1 (p55) in hepatocyte proliferation during acetaminophen-induced toxicity in mice. Toxicol Appl Pharmacol 2003; 193(2): 218-27.
[http://dx.doi.org/10.1016/j.taap.2003.07.003] [PMID: 14644624]
[61]
Kato T, Ito Y, Hosono K, et al. Vascular endothelial growth factor receptor-1 signaling promotes liver repair through restoration of liver microvasculature after acetaminophen hepatotoxicity. Toxicol Sci 2011; 120(1): 218-29.
[http://dx.doi.org/10.1093/toxsci/kfq366] [PMID: 21135413]
[62]
Donahower B, McCullough SS, Kurten R, et al. Vascular endothelial growth factor and hepatocyte regeneration in acetaminophen toxicity. Am J Physiol Gastrointest Liver Physiol 2006; 291(1): G102-9.
[http://dx.doi.org/10.1152/ajpgi.00575.2005] [PMID: 16565415]
[63]
Sica A, Invernizzi P, Mantovani A. Macrophage plasticity and polarization in liver homeostasis and pathology. Hepatology 2014; 59(5): 2034-42.
[http://dx.doi.org/10.1002/hep.26754] [PMID: 24115204]
[64]
Mehendale HM. Tissue repair: an important determinant of final outcome of toxicant-induced injury. Toxicol Pathol 2005; 33(1): 41-51.
[http://dx.doi.org/10.1080/01926230590881808] [PMID: 15805055]
[65]
Dambach DM, Watson LM, Gray KR, Durham SK, Laskin DL. Role of CCR2 in macrophage migration into the liver during acetaminophen-induced hepatotoxicity in the mouse. Hepatology 2002; 35(5): 1093-103.
[http://dx.doi.org/10.1053/jhep.2002.33162] [PMID: 11981759]
[66]
Abeles RD, McPhail MJ, Sowter D, Antoniades CG, Vergis N, Vijay GKM, et al. CD14, CD16 and HLA-DR reliably identifies human monocytes and their subsets in the context of pathologically reduced HLA-DR expression by CD14(hi) /CD16(neg) monocytes: Expansion of CD14(hi) /CD16(pos) and contraction of CD14(lo) /CD16(pos) monocytes in a Cytometry A 2012; 81(10): 823-34.http://www.ncbi.nlm.nih.gov/pubmed/22837127
[67]
Adams DH, Ju C, Ramaiah SK, Uetrecht J, Jaeschke H. Mechanisms of immune-mediated liver injury. Toxicol Sci 2010; 115(2): 307-21.
[http://dx.doi.org/10.1093/toxsci/kfq009] [PMID: 20071422]
[68]
Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling. J Pathol 2013; 229(2): 176-85.
[http://dx.doi.org/10.1002/path.4133] [PMID: 23096265]
[69]
Antoniades CG, Berry PA, Davies ET, et al. Reduced monocyte HLA-DR expression: a novel biomarker of disease severity and outcome in acetaminophen-induced acute liver failure. Hepatology 2006; 44(1): 34-43.
[http://dx.doi.org/10.1002/hep.21240] [PMID: 16799971]
[70]
Ilmakunnas M, Höckerstedt K, Mäkisalo H, Siitonen S, Repo H, Pesonen EJ. Endogenous protease inhibitor uptake within the graft during reperfusion in human liver transplantation. J Hepatobiliary Pancreat Sci 2010; 17(2): 158-65.
[http://dx.doi.org/10.1007/s00534-009-0125-3] [PMID: 19452123]
[71]
Zhang D, Simmen RCM, Michel FJ, Zhao G, Vale-Cruz D, Simmen FA. Secretory leukocyte protease inhibitor mediates proliferation of human endometrial epithelial cells by positive and negative regulation of growth-associated genes. J Biol Chem 2002; 277(33): 29999-30009.http://www.ncbi.nlm.nih.gov/pubmed/12023969
[72]
Sallenave JM, Si Tahar M, Cox G, Chignard M, Gauldie J. Secretory leukocyte proteinase inhibitor is a major leukocyte elastase inhibitor in human neutrophils. J Leukoc Biol 1997; 61(6): 695-702.http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9201260 Internet
[http://dx.doi.org/10.1002/jlb.61.6.695] [PMID: 9201260]
[73]
Triebel S, Bläser J, Gote T, et al. Evidence for the tissue inhibitor of metalloproteinases-1 (TIMP-1) in human polymorphonuclear leukocytes. Eur J Biochem 1995; 231(3): 714-9.
[http://dx.doi.org/10.1111/j.1432-1033.1995.0714d.x] [PMID: 7649172]
[74]
Lentsch AB, Yoshidome H, Warner RL, Ward PA, Edwards MJ. Secretory leukocyte protease inhibitor in mice regulates local and remote organ inflammatory injury induced by hepatic ischemia/reperfusion. Gastroenterology 1999; 117(4): 953-61.http://www.ncbi.nlm.nih.gov/pubmed/10500079
[75]
Zhang Y, DeWitt DL, McNeely TB, Wahl SM, Wahl LM. Secretory leukocyte protease inhibitor suppresses the production of monocyte prostaglandin H synthase-2, prostaglandin E2, and matrix metalloproteinases. J Clin Invest 1997; 99(5): 894-900.
[http://dx.doi.org/10.1172/JCI119254] [PMID: 9062347]
[76]
Greene CM, McElvaney NG, O’Neill SJ, Taggart CC. Secretory leucoprotease inhibitor impairs Toll-like receptor 2- and 4-mediated responses in monocytic cells. Infect Immun 2004; 72(6): 3684-7.
[http://dx.doi.org/10.1128/IAI.72.6.3684-3687.2004] [PMID: 15155685]
[77]
Jeong SJ, Kim SS, Bae CS, et al. Delayed healing and induction of secretory leukocyte protease inhibitor in polycystic ovary syndrome rat skin wounds. Int J Mol Med 2012; 29(2): 185-94.
[PMID: 22020578]
[78]
Sano C, Shimizu T, Tomioka H. Effects of secretory leukocyte protease inhibitor on the tumor necrosis factor-alpha production and NF-kappaB activation of lipopolysaccharide-stimulated macrophages. Cytokine 2003; 21(1): 38-42.http://www.ncbi.nlm.nih.gov/pubmed/2668158
[79]
Odaka C, Mizuochi T, Yang J, Ding A. Murine macrophages produce secretory leukocyte protease inhibitor during clearance of apoptotic cells: implications for resolution of the inflammatory response. J Immunol 2003; 171(3): 1507-4.http://www.ncbi.nlm. nih.gov/pubmed/12874244
[80]
Ghasemlou N, Bouhy D, Yang J, et al. Beneficial effects of secretory leukocyte protease inhibitor after spinal cord injury. Brain 2010; 133(Pt 1): 126-38.
[http://dx.doi.org/10.1093/brain/awp304] [PMID: 20047904]
[81]
Antoine DJ, Dear JW, Lewis PS, Platt V, Coyle J, Masson M, et al. Mechanistic biomarkers provide early and sensitive detection of acetaminophen-induced acute liver injury at first presentation to hospital. Hepatology 2013; 58(2): 777-87. http://www.pubmed central.nih.gov/articlerender.fcgi?artid=3842113&tool=pmcentrez &rendertype=abstract
[82]
Wang K, Zhang S, Marzolf B, et al. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA 2009; 106(11): 4402-7.
[http://dx.doi.org/10.1073/pnas.0813371106] [PMID: 19246379]
[83]
Sucher R, Schroecksnadel K, Weiss G, Margreiter R, Fuchs D, Brandacher G. Neopterin, a prognostic marker in human malignancies. Cancer Lett 2010; 287(1): 13-22.
[http://dx.doi.org/10.1016/j.canlet.2009.05.008] [PMID: 19500901]
[84]
Demirbas S, Cakir E, Akgul EO, Seyrek M, Cayci T, Kurt YG, et al. Elevated serum neopterin levels in acetaminophen-induced liver injury Environ Toxicol Pharmacol 2011; 31(1): 165-70.http://www.ncbi.nlm.nih.gov/pubmed/21787682
[http://dx.doi.org/10.1016/j.etap.2010.10.003]
[85]
Gieseg SP, Baxter-Parker G, Lindsay A. Neopterin, Inflammation, and Oxidative Stress: What Could We Be Missing? Antioxidants (Basel, Switzerland) 2018; 7(7)http://www.ncbi.nlm.nih.gov/pubmed/29949851
[86]
Goodwin GH, Sanders C, Johns EW. A new group of chromatin-associated proteins with a high content of acidic and basic amino acids Eur J Biochem 1973; 38(1): 14-9.http://www.ncbi.nlm. nih.gov/pubmed/4774120
[http://dx.doi.org/10.1111/j.1432-1033.1973.tb03026.x]
[87]
Ilmakunnas M, Tukiainen EM, Rouhiainen A, Rauvala H, Arola J, Nordin A, et al. High mobility group box 1 protein as a marker of hepatocellular injury in human liver transplantation Liver Transplant 2008; 14(10): 1517-25.http://www.ncbi.nlm.nih.gov/pubmed/18825712
[http://dx.doi.org/10.1002/lt.21573 ]
[88]
McGill MR, Sharpe MR, Williams CD, Taha M, Curry SC, Jaeschke H. The mechanism underlying acetaminophen-induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNA fragmentation. J Clin Invest 2012; 122(4): 1574-83.http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3314460&tool=pmcentrez&rendertype=abstract
[89]
Bonaldi T, Talamo F, Scaffidi P, et al. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 2003; 22(20): 5551-60.
[http://dx.doi.org/10.1093/emboj/cdg516] [PMID: 14532127]
[90]
Adebayo D, Mookerjee RP, Jalan R. Mechanistic biomarkers in acute liver injury: are we there yet? J Hepatol 2012; 56(5): 1003.(5).http://www.ncbi.nlm.nih.gov/pubmed/22322232
[91]
Cummings J, Ward TH, Greystoke A, Ranson M, Dive C. Biomarker method validation in anticancer drug development Br J Pharmacol 2008; 153(4): 646-56.http://www.ncbi.nlm.nih.gov/pubmed/17876307
[http://dx.doi.org/10.1038/sj.bjp.0707441]
[92]
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 2012; 56(5): 1070-9.https://linkinghub.elsevier.com/retrieve/pii/S0168827812000591
[93]
Weemhoff JL, Woolbright BL, Jenkins RE, McGill MR, Sharpe MR, Olson JC, et al. Plasma biomarkers to study mechanisms of liver injury in patients with hypoxic hepatitis. Liver Int 2017; 37(3): 377-84.http://www.ncbi.nlm.nih.gov/pubmed/27429052
[http://dx.doi.org/10.1111/liv.13202]
[94]
Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105(30): 10513-8.
[http://dx.doi.org/10.1073/pnas.0804549105] [PMID: 18663219]
[95]
Xu J, Zhang X, Monestier M, Esmon NL, Esmon CT. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol 2011; 187(5): 2626-31.
[http://dx.doi.org/10.4049/jimmunol.1003930] [PMID: 21784973]
[96]
Huang H, Evankovich J, Yan W, et al. Endogenous histones function as alarmins in sterile inflammatory liver injury through Toll-like receptor 9 in mice. Hepatology 2011; 54(3): 999-1008.
[http://dx.doi.org/10.1002/hep.24501] [PMID: 21721026]
[97]
Wen Z, Liu Y, Li F, et al. Circulating histones exacerbate inflammation in mice with acute liver failure. J Cell Biochem 2013; 114(10): 2384-91.
[http://dx.doi.org/10.1002/jcb.24588] [PMID: 23696007]
[98]
James LP, Simpson PM, Farrar HC, Kearns GL, Wasserman GS, Blumer JL, et al. Cytokines and toxicity in acetaminophen overdose. J Clin Pharmacol 2005; 45(10): 1165-71.http://doi.wiley.com/10.1177/0091270005280296
[99]
McGill MR, Staggs VS, Sharpe MR, Lee WM, Jaeschke H. Serum mitochondrial biomarkers and damage-associated molecular patterns are higher in acetaminophen overdose patients with poor outcome Hepatology 2014; 60(4): 1336-45.http://doi.wiley.com/10.1002/hep.27265
[http://dx.doi.org/10.1002/hep.27265]
[100]
Bessems JG, Vermeulen NP. Paracetamol (acetaminophen)-induced toxicity: molecular and biochemical mechanisms, analogues and protective approaches. Crit Rev Toxicol 2001; 31(1): 55-138.http://www.tandfonline.com/doi/full/10.1080/20014091111677
[101]
Hinson JA, Roberts DW, James LP. Mechanisms of Acetaminophen-Induced Liver Necrosis Handbook of experimental pharmacology 2010; 369-405.http://www.ncbi.nlm.nih.gov/pubmed/20020268
[http://dx.doi.org/10.1007/978-3-642-00663-0_12]
[102]
James LP, Mayeux PR, Hinson JA. ACETAMINOPHEN-INDUCED HEPATOTOXICITY. Drug Metab Dispos 2003; 31(22): 1499-506.http://www.ncbi.nlm.nih.gov/pubmed/14625346
[103]
Lores Arnaiz S, Llesuy S, Cutrín JC, Boveris A. Oxidative stress by acute acetaminophen administration in mouse liver. Free Radic Biol Med 1995; 19(3): 303-10.http://www.ncbi.nlm.nih.gov/pubmed/7557544
[104]
Moore M, Thor H, Moore G, Nelson S, Moldéus P, Orrenius S. The toxicity of acetaminophen and N-acetyl-p-benzoquinone imine in isolated hepatocytes is associated with thiol depletion and increased cytosolic Ca2+. J Biol Chem 1985; 260(24): 13035-40.http://www.ncbi.nlm.nih.gov/pubmed/2932433
[105]
Jaeschke H. Glutathione disulfide formation and oxidant stress during acetaminophen-induced hepatotoxicity in mice in vivo: the protective effect of allopurinol. J Pharmacol Exp Ther 1990; 255(3): 935-41.http://www.ncbi.nlm.nih.gov/pubmed/2262912
[106]
Hodgman MJ, Garrard AR. A Review of Acetaminophen Poisoning Crit Care Clin 2012; 28(4): 499-516.http://www.ncbi.nlm. nih.gov/pubmed/22998987
[http://dx.doi.org/10.1016/j.ccc.2012.07.006]
[107]
Rumack BH. Acetaminophen misconceptions. Hepatology 2004; 40(1): 10-5.http://www.ncbi.nlm.nih.gov/pubmed/15239079
[http://dx.doi.org/10.1002/hep.20300]
[108]
Acetaminophen: Old drug, new warnings. Cleve Clin J Med 2010; 77(1): 19-27.http://www.ncbi.nlm.nih.gov/pubmed/20048026
[109]
Harrison PM, Keays R, Bray GP, Alexander GJ, Williams R. Improved outcome of paracetamol-induced fulminant hepatic failure by late administration of acetylcysteine Lancet (London, England) 1990; 335(8705): 1572-3.http://www.ncbi.nlm.nih.gov/pubmed/1972496
[http://dx.doi.org/10.1016/0140-6736(90)91388-Q]
[110]
da Silva MH, da Rosa EJF, de Carvalho NR, Dobrachinski F, da Rocha JBT, Mauriz JL, et al. Acute Brain Damage Induced by Acetaminophen in Mice: Effect of Diphenyl Diselenide on Oxidative Stress and Mitochondrial Dysfunction Neurotox Res. 2012; 21(3): 334-44.http://www.ncbi.nlm.nih.gov/pubmed/22081409
[111]
Guicciardi ME, Malhi H, Mott JL, Gores GJ. Apoptosis and Necrosis in the Liver.Comprehensive Physiology Hoboken, NJ, USA: John Wiley & Sons, Inc. 2013; pp. 977-1010.http://www.ncbi.nlm. nih.gov/pubmed/23720337 Internet [cited 2019 Jun 5]
[http://dx.doi.org/10.1002/cphy.c120020]
[112]
Lu SC. Regulation of hepatic glutathione synthesis: current concepts and controversies FASEB J 1999; 13(10): 1169-83.http://www.ncbi.nlm.nih.gov/pubmed/10385608
[http://dx.doi.org/10.1096/fasebj.13.10.1169]
[113]
Mackavey CL, Hanks R. Hemostasis, Coagulation Abnormalities, and Liver Disease Crit Care Nurs Clin North Am. 2013; 25(4): 435-6.http://www.ncbi.nlm.nih.gov/pubmed/24267280
[114]
Levine M, O’Connor AD, Padilla-Jones A, Gerkin RD. Comparison of Prothrombin Time and Aspartate Aminotransferase in Predicting Hepatotoxicity After Acetaminophen Overdose J. Med Toxicol 2016; 12(1): 100-6.http://www.ncbi.nlm.nih.gov/pubmed/26341088
[115]
Fontana RJ. Acute Liver Failure Including Acetaminophen Overdose Med Clin North Am 2008; 92(4): 761-94.http://www.ncbi. nlm.nih.gov/pubmed/18570942
[http://dx.doi.org/10.1016/j.mcna.2008.03.005]
[116]
Coles B, Wilson I, Wardman P, Hinson JA, Nelson SD, Ketterer B. The spontaneous and enzymatic reaction of N-acetyl-p-benzoquinonimine with glutathione: a stopped-flow kinetic study. Arch Biochem Biophys 1988; 264(1): 253-60.http://www.ncbi.nlm.nih.gov/pubmed/395122
[117]
Beckett GJ, Chapman BJ, Dyson EH, Hayes JD. Plasma glutathione S-transferase measurements after paracetamol overdose: evidence for early hepatocellular damage. Gut 1985; 26(1): 26-31.http://www.ncbi.nlm.nih.gov/pubmed/3965363
[118]
Henderson CJ, Wolf CR, Kitteringham N, Powell H, Otto D, Park BK. Increased resistance to acetaminophen hepatotoxicity in mice lacking glutathione S-transferase Pi. Proc Natl Acad Sci USA 2000; 97(23): 12741-5.http://www.ncbi.nlm.nih.gov/pubmed/11058152
[119]
Ramachandran A, Jaeschke H. Acetaminophen Toxicity. Novel Insights Into Mechanisms and Future Perspectives Gene Expr 2018; 18(1): 19-30.http://www.ingentaconnect.com/content/10.3727/105221617X15084371374138
[120]
Moles A, Torres S, Baulies A, Garcia-Ruiz C, Fernandez-Checa JC. Mitochondrial–Lysosomal Axis in Acetaminophen Hepatotoxicity Front Pharmacol 2018; 9453http://journal.frontiersin.org/article/10.3389/fphar.2018.00453/full
[http://dx.doi.org/10.3389/fphar.2018.00453]
[121]
Masubuchi Y, Suda C, Horie T. Involvement of mitochondrial permeability transition in acetaminophen-induced liver injury in mice. J Hepatol 2005; 42(1): 110-6.https://linkinghub.elsevier.com/retrieve/pii/S0168827804004295
[122]
Niki E. Lipid peroxidation products as oxidative stress biomarkers Biofactors 2008; 34(2): 171-80.http://www.ncbi.nlm.nih.gov/pubmed/19706982
[http://dx.doi.org/10.1002/biof.5520340208]
[123]
Lewis M, Howdle PD. The neurology of liver failure. QJM 2003; 96(9): 623-33.http://www.ncbi.nlm.nih.gov/pubmed/12925717
[http://dx.doi.org/10.1093/qjmed/hcg110]
[124]
McGill MR, Li F, Sharpe MR, Williams CD, Curry SC, Ma X, et al. Circulating acylcarnitines as biomarkers of mitochondrial dysfunction after acetaminophen overdose in mice and humans Arch Toxicol 2014; 88(2): 391-401.http://www.ncbi.nlm.nih.gov/pubmed/23979652
[http://dx.doi.org/10.1007/s00204-013-1118-1]
[125]
Bajt ML, Cover C, Lemasters JJ, Jaeschke H. Nuclear Translocation of Endonuclease G and Apoptosis-Inducing Factor during Acetaminophen-Induced Liver Cell Injury. Toxicol Sci 2006; 94(1): 217-5.http://www.ncbi.nlm.nih.gov/pubmed/16896059
[126]
McGill MR, Jaeschke H. Mechanistic biomarkers in acetaminophen-induced hepatotoxicity and acute liver failure: from preclinical models to patients. Expert Opin Drug Metab Toxicol 2014; 10(7): 1005-7.http://www.ncbi.nlm.nih.gov/pubmed/24836926
[http://dx.doi.org/10.1517/17425255.2014.920823]
[127]
Orrenius S, Gogvadze V, Zhivotovsky B. Calcium and mitochondria in the regulation of cell death Biochem Biophys Res Commun 2015; 460(1): 72-81.http://www.ncbi.nlm.nih.gov/pubmed/25998735
[http://dx.doi.org/10.1016/j.bbrc.2015.01.137]
[128]
Woolbright BL, McGill MR, Staggs VS, Winefield RD, Gholami P, Olyaee M, et al. Glycodeoxycholic acid levels as prognostic biomarker in acetaminophen-induced acute liver failure patients Toxicol Sci 2014; 142(2): 436-.http://www.ncbi.nlm.nih.gov/pubmed/25239633
[http://dx.doi.org/10.1093/toxsci/kfu195]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy