The role of hypoxia-inducible factor-1α in acetaminophen hepatotoxicity

Journal of Pharmacology and Experimental Therapeutics

Volumn 338, Issue 2, 2011, Pages 492-502

  Sparkenbaugh, Erica M ^a,c   Saini, Yogesh ^b,c   Greenwood, Krista K ^b,c   LaPres, John J ^b,c   Luyendyk, James P ^d   Copple, Bryan L ^d   Maddox, Jane F ^a,c   Ganey, Patricia E ^a,c   Roth, Robert A ^a,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 6; KERATINOCYTE CHEMOATTRACTANT; PARACETAMOL; THROMBIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; DRUG OVERDOSE; GENE DELETION; HEMOSTASIS; INFLAMMATION; LIVER PROTECTION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; T LYMPHOCYTE; TOXIC HEPATITIS;

ACETAMINOPHEN; ANIMALS; DRUG-INDUCED LIVER INJURY; HEPATOCYTES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OXIDATIVE STRESS;

EID: 79960481622     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.180521     Document Type: Article

References (42)

1. Bajt ML, Farhood A, Lemasters JJ, and Jaeschke H (2008a) Mitochondrial bax translocation accelerates DNA fragmentation and cell necrosis in a murine model of acetaminophen hepatotoxicity. J Pharmacol Exp Ther 324:8-14. (Pubitemid 350294184)
2. Bajt ML, Yan HM, Farhood A, and Jaeschke H (2008b) Plasminogen activator inhibitor-1 limits liver injury and facilitates regeneration after acetaminophen overdose. Toxicol Sci 104:419-427. (Pubitemid 352038264)
3. Bernhardt WM, Warnecke C, Willam C, Tanaka T, Wiesener MS, and Eckardt KU (2007) Organ protection by hypoxia and hypoxia-inducible factors. Methods Enzymol 435:221-245.
4. Chaudhuri S, McCullough SS, Hennings L, Letzig L, Simpson PM, Hinson JA, and James LP (2011) Acetaminophen hepatotoxicity and HIF-1α induction in acetaminophen toxicity in mice occurs without hypoxia. Toxicol Appl Pharmacol 252: 211-220.
5. Copple BL, Banes A, Ganey PE, and Roth RA (2002) Endothelial cell injury and fibrin deposition in rat liver after monocrotaline exposure. Toxicol Sci 65:309-318. (Pubitemid 34121123)
6. Copple BL, Bustamante JJ, Welch TP, Kim ND, and Moon JO (2009) Hypoxiainducible factor-dependent production of profibrotic mediators by hypoxic hepatocytes. Liver Int 29:1010-1021.
7. Cover C, Liu J, Farhood A, Malle E, Waalkes MP, Bajt ML, and Jaeschke H (2006) Pathophysiological role of the acute inflammatory response during acetaminophen hepatotoxicity. Toxicol Appl Pharmacol 216:98-107.
8. Cramer T, Yamanishi Y, Clausen BE, Förster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, et al. (2003) HIF-1α is essential for myeloid cell-mediated inflammation. Cell 112:645-657. (Pubitemid 36331777)
9. Cursio R, Miele C, Filippa N, Van Obberghen E, and Gugenheim J (2008) Liver HIF-1α induction precedes apoptosis following normothermic ischemiareperfusion in rats. Transplant Proc 40:2042-2045.
10. Donahower B, McCullough SS, Kurten R, Lamps LW, Simpson P, Hinson JA, and James LP (2006) Vascular endothelial growth factor and hepatocyte regeneration in acetaminophen toxicity. Am J Physiol Gastrointest Liver Physiol 291:G102-G109. (Pubitemid 44024667)
11. Ganey PE, Luyendyk JP, Newport SW, Eagle TM, Maddox JF, Mackman N, and Roth RA (2007) Role of the coagulation system in acetaminophen-induced hepatotoxicity in mice. Hepatology 46:1177-1186. (Pubitemid 350144782)
12. Görlach A, Diebold I, Schini-Kerth VB, Berchner-Pfannschmidt U, Roth U, Brandes RP, Kietzmann T, and Busse R (2001) Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: role of the p22(phox)- containing NADPH oxidase. Circ Res 89:47-54. (Pubitemid 34135491)
13. Ishida Y, Kondo T, Ohshima T, Fujiwara H, Iwakura Y, and Mukaida N (2002) A pivotal involvement of IFN-γ in the pathogenesis of acetaminophen-induced acute liver injury. FASEB J 16:1227-1236. (Pubitemid 34815410)
14. Ishida Y, Kondo T, Tsuneyama K, Lu P, Takayasu T, and Mukaida N (2004) The pathogenic roles of tumor necrosis factor receptor p55 in acetaminophen-induced liver injury in mice. J Leukoc Biol 75:59-67. (Pubitemid 38166780)
15. Jaeschke H (2008) Innate immunity and acetaminophen-induced liver injury: why so many controversies? Hepatology 48:699-701.
16. James LP, Donahower B, Burke AS, McCullough S, and Hinson JA (2006) Induction of the nuclear factor HIF-1α in acetaminophen toxicity: evidence for oxidative stress. Biochem Biophys Res Commun 343:171-176.
17. James LP, McCullough SS, Lamps LW, and Hinson JA (2003) Effect of N-acetylcysteine of acetaminophen toxicity in mice: relationship to reactive nitrogen and cytokine formation. Toxicol Sci 75:458-467. (Pubitemid 37220292)
18. James LP, Simpson PM, Farrar HC, Kearns GL, Wasserman GS, Blumer JL, Reed MD, Sullivan JE, and Hinson JA (2005) Cytokines and toxicity in acetaminophen overdose. J Clin Pharmacol 45:1165-1171. (Pubitemid 41361916)
19. James LP, Wells E, Beard RH, and Farrar HC (2002) Predictors of outcome after acetaminophen poisoning in children and adolescents. J Pediatr 140:522-526. (Pubitemid 34666720)
20. Jollow DJ, Mitchell JR, Potter WZ, Davis DC, Gillette JR, and Brodie BB (1973) Acetaminophen-induced hepatic necrosis. II. Role of covalent binding in vivo. J Pharmacol Exp Ther 187:195-202.
21. Kato T, Ito Y, Hosono K, Suzuki T, Tamaki H, Minamino T, Kato S, Sakagami H, Shibuya M, and Majima M (2011) Vascular endothelial growth factor receptor-1 signaling promotes liver repair through restoration of liver microvasculature after acetaminophen hepatotoxicity. Toxicol Sci 120:218-229.
22. Klimova T and Chandel NS (2008) Mitochondrial complex III regulates hypoxia activation of HIF. Cell Death Differ 15:660-666. (Pubitemid 351405069)
23. Lawson JA, Farhood A, Hopper RD, Bajt ML, and Jaeschke H (2000) The hepatic inflammatory response after acetaminophen overdose: role of neutrophils. Toxicol Sci 54:509-516. (Pubitemid 30185974)
24. Lee KA, Roth RA, and LaPres JJ (2007) Hypoxia, drug therapy and toxicity. Pharmacol Ther 113:229-246. (Pubitemid 46149044)
25. Lee WM (2007) Acetaminophen toxicity: changing perceptions on a social/medical issue. Hepatology 46:966-970.
26. Li L, Chen SH, Zhang Y, Yu CH, Li SD, and Li YM (2006) Is the hypoxia-inducible factor-1α mRNA expression activated by ethanol-induced injury, the mechanism underlying alcoholic liver disease? Hepatobiliary Pancreat Dis Int 5:560-563.
27. Liu ZX, Han D, Gunawan B, and Kaplowitz N (2006) Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 43:1220-1230. (Pubitemid 43980100)
28. Maddox JF, Amuzie CJ, Li M, Newport SW, Sparkenbaugh E, Cuff CF, Pestka JJ, Cantor GH, Roth RA, and Ganey PE (2010) Bacterial- and viral-induced inflammation increases sensitivity to acetaminophen hepatotoxicity. J Toxicol Environ Health A 73:58-73.
29. Masubuchi Y, Bourdi M, Reilly TP, Graf ML, George JW, and Pohl LR (2003) Role of interleukin-6 in hepatic heat shock protein expression and protection against acetaminophen-induced liver disease. Biochem Biophys Res Commun 304:207-212. (Pubitemid 36434217)
30. Mehendale HM (2005) Tissue repair: an important determinant of final outcome of toxicant-induced injury. Toxicol Pathol 33:41-51.
31. Murdoch C, Muthana M, and Lewis CE (2005) Hypoxia regulates macrophage functions in inflammation. J Immunol 175:6257-6263. (Pubitemid 41598863)
32. Peyssonnaux C, Cejudo-Martin P, Doedens A, Zinkernagel AS, Johnson RS, and Nizet V (2007) Cutting edge: Essential role of hypoxia inducible factor 1a in development of lipopolysaccharide-induced sepsis. J Immunol 178:7516-7519. (Pubitemid 46898018)
33. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, Gallo RL, Hurtado-Ziola N, Nizet V, and Johnson RS (2005) HIF-1α expression regulates the bactericidal capacity of phagocytes. J Clin Invest 115:1806-1815. (Pubitemid 40979719)
34. Ruzankina Y, Pinzon-Guzman C, Asare A, Ong T, Pontano L, Cotsarelis G, Zediak VP, Velez M, Bhandoola A, and Brown EJ (2007) Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell 1:113-126. (Pubitemid 46865802)
35. Ryan HE, Lo J, and Johnson RS (1998) HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J 17:3005-3015. (Pubitemid 28254373)
36. Saini Y, Harkema JR, and LaPres JJ (2008) HIF-1α is essential for normal intrauterine differentiation of alveolar epithelium and surfactant production in the newborn lung of mice. J Biol Chem 283:33650-33657.
37. Saito C, Lemasters JJ, and Jaeschke H (2010) c-Jun N-terminal kinase modulates oxidant stress and peroxynitrite formation independent of inducible nitric oxide synthase in acetaminophen hepatotoxicity. Toxicol Appl Pharmacol 246:8-17.
38. Walmsley SR, Cadwallader KA, and Chilvers ER (2005a) The role of HIF-1α in myeloid cell inflammation. TRENDS Immunol 26:434-439. (Pubitemid 41008080)
39. Walmsley SR, Print C, Farahi N, Peyssonnaux C, Johnson RS, Cramer T, Sobolewski A, Condliffe AM, Cowburn AS, Johnson N, et al. (2005b) Hypoxia-induced neutrophil survival is mediated by HIF-1α-dependent NF-κB activity. J Exp Med 201:105-115. (Pubitemid 40130088)
40. Williams CD, Farhood A, and Jaeschke H (2010) Role of caspase-1 and interleukin-1β in acetaminophen-induced hepatic inflammation and liver injury. Toxicol Appl Pharmacol 247:169-178.
41. Yan HM, Ramachandran A, Bajt ML, Lemasters JJ, and Jaeschke H (2010) The oxygen tension modulates acetaminophen-induced mitochondrial oxidant stress and cell injury in cultured hepatocytes. Toxicol Sci 117:515-523.
42. Zinkernagel AS, Johnson RS, and Nizet V (2007) Hypoxia inducible factor (HIF) in innate immunity and infection. J Mol Med 85:1339-1346. (Pubitemid 350234101)