Molecular mechanisms of liver injury: Apoptosis or necrosis

Experimental and Toxicologic Pathology

Volumn 66, Issue 8, 2014, Pages 351-356

  Wang, Kewei ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Acetaminophen; Cholestasis; Hepatic apoptosis; Hepatitis; Liver injury; Necrosis

Indexed keywords

CASPASE INHIBITOR; EMRICASAN; NIVOCASAN; PARACETAMOL; PF 03491390; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DEATH; CHOLESTASIS; DISEASE COURSE; DRUG OVERDOSE; DRUG POTENCY; HEPATITIS; HUMAN; INFLAMMATORY CELL; LIVER CANCER; LIVER INJURY; LIVER NECROSIS; NONHUMAN; PATHOGENESIS; REVIEW; TOXIC HEPATITIS; VIRUS HEPATITIS; ANIMAL; LIVER DISEASE; NECROSIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; HUMANS; LIVER DISEASES; NECROSIS;

EID: 84919341324     PISSN: 09402993     EISSN: 16181433     Source Type: Journal    
DOI: 10.1016/j.etp.2014.04.004     Document Type: Review

References (84)

1. Abbas Z., Moatter T., Hussainy A., Jafri W. Effect of cytokine gene polymorphism on histological activity index, viral load and response to treatment in patients with chronic hepatitis C genotype 3. World J Gastroenterol 2005, 11(42):6656-6661.
2. Apolinario A., Majano P.L., Alvarez-Perez E., Saez A., Lozano C., Vargas J., et al. Increased expression of T cell chemokines and their receptors in chronic hepatitis C: relationship with the histological activity of liver disease. Am J Gastroenterol 2002, 97(11):2861-2870.
3. Arzumanyan A., Reis H.M., Feitelson M.A. Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma. Nat Rev Cancer 2013, 13(2):123-135.
4. Bantel H., Schulze-Osthoff K. Apoptosis in hepatitis C virus infection. Cell Death Differ 2003, 10(Suppl. 1):S48-S58.
5. Barnes M.A., McMullen M.R., Roychowdhury S., Pisano S.G., Liu X., Stavitsky A.B., et al. Macrophage migration inhibitory factor contributes to ethanol-induced liver injury by mediating cell injury, steatohepatitis, and steatosis. Hepatology 2013, 57(5):1980-1991.
6. Barrett S., Collins M., Kenny C., Ryan E., Keane C.O., Crowe J. Polymorphisms in tumour necrosis factor-alpha, transforming growth factor-beta, interleukin-10, interleukin-6, interferon-gamma, and outcome of hepatitis C virus infection. J Med Virol 2003, 71(2):212-218.
7. Bechmann L.P., Kocabayoglu P., Sowa J.P., Sydor S., Best J., Schlattjan M., et al. Free fatty acids repress small heterodimer partner (SHP) activation and adiponectin counteracts bile acid-induced liver injury in superobese patients with nonalcoholic steatohepatitis. Hepatology 2013, 57(4):1394-1406.
8. Ben-Ari Z., Pappo O., Druzd T., Sulkes J., Klein T., Samra Z., et al. Role of cytokine gene polymorphism and hepatic transforming growth factor beta1 expression in recurrent hepatitis C after liver transplantation. Cytokine 2004, 27(1):7-14.
9. Borisov A.B., Carlson B.M. Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat Rec 2000, 258(3):305-318.
10. Cai B., Lyu H., Huang J., Wang S., Lee C.K., Gao C., et al. Combination of bendamustine and entinostat synergistically inhibits proliferation of multiple myeloma cells via induction of apoptosis and DNA damage response. Cancer lett 2013.
11. Calabrese F., Pontisso P., Pettenazzo E., Benvegnu L., Vario A., Chemello L., et al. Liver cell apoptosis in chronic hepatitis C correlates with histological but not biochemical activity or serum HCV-RNA levels. Hepatology 2000, 31(5):1153-1159.
12. Canbay A., Feldstein A.E., Higuchi H., Werneburg N., Grambihler A., Bronk S.F., et al. Kupffer cell engulfment of apoptotic bodies stimulates death ligand and cytokine expression. Hepatology 2003, 38(5):1188-1198.
13. Canbay A., Guicciardi M.E., Higuchi H., Feldstein A., Bronk S.F., Rydzewski R., et al. Cathepsin B inactivation attenuates hepatic injury and fibrosis during cholestasis. J Clin Invest 2003, 112(2):152-159.
14. Chen Y.L., Yu C.K., Lei H.Y. Propionibacterium acnes induces acute TNFalpha-mediated apoptosis of hepatocytes followed by inflammatory T-cell-mediated granulomatous hepatitis in mice. J Biomed Sci 1999, 6(5):349-356.
15. Cohen S.D., Khairallah E.A. Selective protein arylation and acetaminophen-induced hepatotoxicity. Drug Metab Rev 1997, 29(1-2):59-77.
16. Delemos A.S., Friedman L.S. Systemic causes of cholestasis. Clin Liver Dis 2013, 17(2):301-317.
17. Dolganiuc A., Norkina O., Kodys K., Catalano D., Bakis G., Marshall C., et al. Viral and host factors induce macrophage activation and loss of toll-like receptor tolerance in chronic HCV infection. Gastroenterology 2007, 133(5):1627-1636.
18. Dongiovanni P., Anstee Q.M., Valenti L. Genetic predisposition in NAFLD and NASH: impact on severity of liver disease and response to treatment. Curr Pharm Des 2013, 19(29):5219-5238.
19. Du J., Liang X., Liu Y., Qu Z., Gao L., Han L., et al. Hepatitis B virus core protein inhibits TRAIL-induced apoptosis of hepatocytes by blocking DR5 expression. Cell Death Differ 2009, 16(2):219-229.
20. Ehrmann J., Galuszkova D., Ehrmann J., Krc I., Jezdinska V., Vojtesek B., et al. Apoptosis-related proteins, BCL-2, BAX, FAS, FAS-L and PCNA in liver biopsies of patients with chronic hepatitis B virus infection. Pathol Oncol Res 2000, 6(2):130-135.
21. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007, 35(4):495-516.
22. Faouzi S., Burckhardt B.E., Hanson J.C., Campe C.B., Schrum L.W., Rippe R.A., et al. Anti-Fas induces hepatic chemokines and promotes inflammation by an NF-kappa B-independent, caspase-3-dependent pathway. J Biol Chem 2001, 276(52):49077-49082.
23. Feitelson M.A., Reis H.M., Tufan N.L., Sun B., Pan J., Lian Z. Putative roles of hepatitis B×antigen in the pathogenesis of chronic liver disease. Cancer lett 2009, 286(1):69-79.
24. Ghabril M., Fontana R., Rockey D., Jiezhun G., Chalasani N. Drug-induced liver injury caused by intravenously administered medications: the drug-induced liver injury network experience. J Clin Gastroenterol 2013, 47(6):553-558.
25. Guha M., Maity P., Choubey V., Mitra K., Reiter R.J., Bandyopadhyay U. Melatonin inhibits free radical-mediated mitochondrial-dependent hepatocyte apoptosis and liver damage induced during malarial infection. J Pineal Res 2007, 43(4):372-381.
26. Guicciardi M.E., Gores G.J. Apoptosis: a mechanism of acute and chronic liver injury. Gut 2005, 54(7):1024-1033.
27. Gujral J.S., Knight T.R., Farhood A., Bajt M.L., Jaeschke H. Mode of cell death after acetaminophen overdose in mice: apoptosis or oncotic necrosis?. T Toxicol Sci 2002, 67(2):322-328.
28. Gujral J.S., Liu J., Farhood A., Jaeschke H. Reduced oncotic necrosis in Fas receptor-deficient C57BL/6J-lpr mice after bile duct ligation. Hepatology 2004, 40(4):998-1007.
29. Halilbasic E., Claudel T., Trauner M. Bile acid transporters and regulatory nuclear receptors in the liver and beyond. J Hepatol 2013, 58(1):155-168.
30. Higuchi H., Miyoshi H., Bronk S.F., Zhang H., Dean N., Gores G.J. Bid antisense attenuates bile acid-induced apoptosis and cholestatic liver injury. J Pharmacol Exp Ther 2001, 299(3):866-873.
31. Hikita H., Takehara T., Kodama T., Shimizu S., Shigekawa M., Hosui A., et al. Delayed-onset caspase-dependent massive hepatocyte apoptosis upon Fas activation in Bak/Bax-deficient mice. Hepatology 2011, 54(1):240-251.
32. Hoglen N.C., Anselmo D.M., Katori M., Kaldas M., Shen X.D., Valentino K.L., et al. A caspase inhibitor, IDN-6556, ameliorates early hepatic injury in an ex vivo rat model of warm and cold ischemia. Liver Transpl 2007, 13(3):361-366.
33. Hu J., Yan D., Gao J., Xu C., Yuan Y., Zhu R., et al. rhIL-1Ra reduces hepatocellular apoptosis in mice with acetaminophen-induced acute liver failure. Lab Invest 2010, 90(12):1737-1746.
34. Invernizzi P. Human leukocyte antigen in primary biliary cirrhosis: an old story now reviving. Hepatology 2011, 54(2):714-723.
35. Jaeschke H., Lemasters J.J. Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 2003, 125(4):1246-1257.
36. Kaiser W.J., Upton J.W., Long A.B., Livingston-Rosanoff D., Daley-Bauer L.P., Hakem R., et al. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011, 471(7338):368-372.
37. Kato N. Genome of human hepatitis C virus (HCV): gene organization, sequence diversity, and variation. Microb Comp Genomics 2000, 5(3):129-151.
38. Knight T.R., Jaeschke H. Acetaminophen-induced inhibition of Fas receptor-mediated liver cell apoptosis: mitochondrial dysfunction versus glutathione depletion. Toxicol Appl Pharmacol 2002, 181(2):133-141.
39. Kon K., Kim J.S., Jaeschke H., Lemasters J.J. Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 2004, 40(5):1170-1179.
40. Kon K., Ikejima K., Okumura K., Aoyama T., Arai K., Takei Y., et al. Role of apoptosis in acetaminophen hepatotoxicity. J Gastroenterol Hepatol 2007, 22(Suppl. 1):S49-S52.
41. Lawson J.A., Fisher M.A., Simmons C.A., Farhood A., Jaeschke H. Inhibition of Fas receptor (CD95)-induced hepatic caspase activation and apoptosis by acetaminophen in mice. Toxicol Appl Pharmacol 1999, 156(3):179-186.
42. Lee W.M. Drug-induced hepatotoxicity. N Engl J Med 2003, 349(5):474-485.
43. Lee W.M. Acetaminophen and the U.S. Acute Liver Failure Study Group: lowering the risks of hepatic failure. Hepatology 2004, 40(1):6-9.
44. Lemasters J.J.V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am J Pathol 1999, 276(1 Pt 1):G1-G6.
45. Liang X., Liu Y., Zhang Q., Gao L., Han L., Ma C., et al. Hepatitis B virus sensitizes hepatocytes to TRAIL-induced apoptosis through Bax. J Immunol 2007, 178(1):503-510.
46. Liedtke C., Bangen J.M., Freimuth J., Beraza N., Lambertz D., Cubero F.J., et al. Loss of caspase-8 protects mice against inflammation-related hepatocarcinogenesis but induces non-apoptotic liver injury. Gastroenterology 2011, 141(6):2176-2187.
47. Lund L.R., Romer J., Thomasset N., Solberg H., Pyke C., Bissell M.J., et al. Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways. Development 1996, 122(1):181-193.
48. Malhi H., Gores G.J., Lemasters J.J. Apoptosis and necrosis in the liver: a tale of two deaths?. Hepatology 2006, 43(2 (Suppl. 1)):S31-S44.
49. Mason K.D., Lin A., Robb L., Josefsson E.C., Henley K.J., Gray D.H., et al. Proapoptotic Bak and Bax guard against fatal systemic and organ-specific autoimmune disease. Proc Natl Acad Sci U S A 2013, 110(7):2599-2604.
50. Miyoshi H., Rust C., Roberts P.J., Burgart L.J., Gores G.J. Hepatocyte apoptosis after bile duct ligation in the mouse involves Fas. Gastroenterology 1999, 117(3):669-677.
51. Miyoshi H., Rust C., Guicciardi M.E., Gores G.J. NF-kappaB is activated in cholestasis and functions to reduce liver injury. Am J Pathol 2001, 158(3):967-975.
52. Moreno C., Gustot T., Nicaise C., Quertinmont E., Nagy N., Parmentier M., et al. CCR5 deficiency exacerbates T-cell-mediated hepatitis in mice. Hepatology 2005, 42(4):854-862.
53. Mundt B., Wirth T., Zender L., Waltemathe M., Trautwein C., Manns M.P., et al. Tumour necrosis factor related apoptosis inducing ligand (TRAIL) induces hepatic steatosis in viral hepatitis and after alcohol intake. Gut 2005, 54(11):1590-1596.
54. Nalapareddy P., Schungel S., Hong J.Y., Manns M.P., Jaeschke H., Vogel A. The BH3-only protein bid does not mediate death-receptor-induced liver injury in obstructive cholestasis. Am J Pathol 2009, 175(3):1077-1085.
55. Nam J.H., Bukh J., Purcell R.H., Emerson S.U. High-level expression of hepatitis C virus (HCV) structural proteins by a chimeric HCV/BVDV genome propagated as a BVDV pseudotype. J Virol Methods 2001, 97(1-2):113-123.
56. Ni H.M., Bockus A., Boggess N., Jaeschke H., Ding W.X. Activation of autophagy protects against acetaminophen-induced hepatotoxicity. Hepatology 2012, 55(1):222-232.
57. Oberhammer F., Fritsch G., Schmied M., Pavelka M., Printz D., Purchio T., et al. Condensation of the chromatin at the membrane of an apoptotic nucleus is not associated with activation of an endonuclease. J Cell Sci 1993, 104(Pt 2):317-326.
58. Ola M.S., Nawaz M., Ahsan H. Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol Cell Biochem 2011, 351(1-2):41-58.
59. Ozawa T. Mechanism of somatic mitochondrial DNA mutations associated with age and diseases. Biochim Biophys Acta 1995, 1271(1):177-189.
60. Penna A., Pilli M., Zerbini A., Orlandini A., Mezzadri S., Sacchelli L., et al. Dysfunction and functional restoration of HCV-specific CD8 responses in chronic hepatitis C virus infection. Hepatology 2007, 45(3):588-601.
61. Pockros P.J., Schiff E.R., Shiffman M.L., McHutchison J.G., Gish R.G., Afdhal N.H., et al. Oral IDN-6556, an antiapoptotic caspase inhibitor, may lower aminotransferase activity in patients with chronic hepatitis C. Hepatology 2007, 46(2):324-329.
62. Raghuraman S., Abraham P., Daniel H.D., Ramakrishna B.S., Sridharan G. Characterization of soluble FAS, FAS ligand and tumour necrosis factor-alpha in patients with chronic HCV infection. J Clin Virol 2005, 34(1):63-70.
63. Ratziu V., Sheikh M.Y., Sanyal A.J., Lim J.K., Conjeevaram H., Chalasani N., et al. A phase 2, randomized, double-blind, placebo-controlled study of GS-9450 in subjects with nonalcoholic steatohepatitis. Hepatology 2012, 55(2):419-428.
64. Ray S.D., Mumaw V.R., Raje R.R., Fariss M.W. Protection of acetaminophen-induced hepatocellular apoptosis and necrosis by cholesteryl hemisuccinate pretreatment. J Pharmacol Exp Ther 1996, 279(3):1470-1483.
65. Resendes A.R., Majo N., Segales J., Espadamala J., Mateu E., Chianini F., et al. Apoptosis in normal lymphoid organs from healthy normal, conventional pigs at different ages detected by TUNEL and cleaved caspase-3 immunohistochemistry in paraffin-embedded tissues. Vet Immunol Immunopathol 2004, 99(3-4):203-213.
66. Roychowdhury S., McMullen M.R., Pisano S.G., Liu X., Nagy L.E. Absence of receptor interacting protein kinase 3 prevents ethanol-induced liver injury. Hepatology 2013, 57(5):1773-1783.
67. Sanz-Garcia C., Ferrer-Mayorga G., Gonzalez-Rodriguez A., Valverde A.M., Martin-Duce A., Velasco-Martin J.P., et al. Sterile inflammation in acetaminophen-induced liver injury is mediated by Cot/tpl2. J Biol Chem 2013, 288(21):15342-15351.
68. Sharma S.D. Hepatitis C virus 1b viral factors (Core NS3 and NS5A) and increased risk of hepatocellular carcinoma. Hepatology 2013, 38(2):491-493.
69. Shi J., Fujieda H., Kokubo Y., Wake K. Apoptosis of neutrophils and their elimination by Kupffer cells in rat liver. Hepatology 1996, 24(5):1256-1263.
70. Shiffman M.L., Pockros P., McHutchison J.G., Schiff E.R., Morris M., Burgess G. Clinical trial: the efficacy and safety of oral PF-03491390, a pancaspase inhibitor - a randomized placebo-controlled study in patients with chronic hepatitis C. Aliment Pharmacol Ther 2010, 31(9):969-978.
71. Shuh M., Bohorquez H., Loss G.E., Cohen A.J. Tumor necrosis factor-alpha: life and death of hepatocytes during liver ischemia/reperfusion injury. Ochsner J 2013, 13(1):119-130.
72. Sokol R.J., Dahl R., Devereaux M.W., Yerushalmi B., Kobak G.E., Gumpricht E. Human hepatic mitochondria generate reactive oxygen species and undergo the permeability transition in response to hydrophobic bile acids. J Pediatr Gastroenterol Nutr 2005, 41(2):235-243.
73. Tan X., Shi J., Fu Y., Gao C., Yang X., Li J., et al. Role of erythrocytes and platelets in the hypercoagulable status in polycythemia vera through phosphatidylserine exposure and microparticle generation. Thromb Haemost 2013, 109:6.
74. Tilly J.L., Kowalski K.I., Johnson A.L., Hsueh A.J. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 1991, 129(5):2799-2801.
75. Torchinsky A., Savion S., Gorivodsky M., Shepshelovich J., Zaslavsky Z., Fein A., et al. Cyclophosphamide-induced teratogenesis in ICR mice: the role of apoptosis. Teratog Carcinog Mutagen 1995, 15(4):179-190.
76. Trump B.F., Berezesky I.K., Chang S.H., Phelps P.C. The pathways of cell death: oncosis, apoptosis, and necrosis. Toxicol Pathol 1997, 25(1):82-88.
77. Valva P., De Matteo E., Galoppo M.C., Gismondi M.I., Preciado M.V. Apoptosis markers related to pathogenesis of pediatric chronic hepatitis C virus infection: M30 mirrors the severity of steatosis. J Med Virol 2010, 82(6):949-957.
78. Vick B., Weber A., Urbanik T., Maass T., Teufel A., Krammer P.H., et al. Knockout of myeloid cell leukemia-1 induces liver damage and increases apoptosis susceptibility of murine hepatocytes. Hepatology 2009, 49(2):627-636.
79. Wahl K., Siegemund M., Lehner F., Vondran F., Nussler A., Langer F., et al. Increased apoptosis induction in hepatocellular carcinoma by a novel tumor-targeted TRAIL fusion protein combined with bortezomib. Hepatology 2013, 57(2):625-636.
80. Wang K., Brems J.J., Gamelli R.L., Ding J. Reversibility of caspase activation and its role during glycochenodeoxycholate-induced hepatocyte apoptosis. J Biol Chem 2005, 280(25):23490-23495.
81. Wang K., Brems J.J., Gamelli R.L., Holterman A.X. Survivin signaling is regulated through nuclear factor-kappa B pathway during glycochenodeoxycholate-induced hepatocyte apoptosis. Biochim Biophys Acta 2010, 1803(12):1368-1375.
82. Younossi Z.M., Zheng L., Stepanova M., Venkatesan C., Mir H.M. Moderate, excessive or heavy alcohol consumption: each is significantly associated with increased mortality in patients with chronic hepatitis C. Aliment Pharmacol Ther 2013, 37(7):703-709.
83. Zhao M.X., Ji L.N., Mao Z.W. beta-Cyclodextrin/glycyrrhizic acid functionalised quantum dots selectively enter hepatic cells and induce apoptosis. Chemistry 2012, 18(6):1650-1658.
84. Zhu N., Ware C.F., Lai M.M., Hepatitis C virus core protein enhances FADD-mediated apoptosis and suppresses TRADD signaling of tumor necrosis factor receptor. Virology 2001, 283(2):178-187.