HMGB1 neutralization is associated with bacterial translocation during acetaminophen hepatotoxicity

详细信息    查看全文

• 作者：Runkuan Yang (1) (2) (7)
  Xiaoping Zou (3)
  Jyrki Tenhunen (2) (4)
  Shengtao Zhu (5)
  Henri Kajander (6)
  Marja-Leena Koskinen (6)
  Tor Inge Tonnessen (7)
  
• 关键词：HMGB1 ; Acetaminophen ; Hepatotoxicity ; Gut bacterial translocation
• 刊名：BMC Gastroenterology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：14
• 期：1
• 全文大小：599 KB
• 参考文献：1. Lee WM: Acetaminophen and the U.S. Acute liver failure study group: lowering the risks of hepatic failure. / Hepatology 2004, 40:6-. CrossRef
  2. Kasravi FB, Wang LQ, Wang XD, Molin G, Bengmark S, Jeppsson B: Bacterial translocation in acute liver injury induced by D-galactosamine. / Hepatology 1996, 23:97-03.
  3. Cohen SD, Khairallah EA: Selective protein arylation and acetaminophen-induced hepatotoxicity. / Drug Metab Rev 1997, 29:59-7. CrossRef
  4. Cressman DE, Greenbaum LE, DeAngelis RA, Ciliberto G, Furth EE, Poli V, Taub R: Liver failure and defective. Hepatocyte regeneration in interleukin-6 deficient mice. / Science 1996, 274:1379-383. CrossRef
  5. Jaeschke H, Bajt ML: Intracellular signaling mechanisms of acetaminophen-induced liver cell death. / Toxicol Sci 2006, 89:31-1. CrossRef
  6. Yamada Y, Kirillova I, Peschon JJ, Fausto N: Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type 1 tumor necrosis factor receptor. / Proc Natl Acad Sci 1997, 94:1441-446. CrossRef
  7. Wang H, Li W, Goldstein R, Tracey KJ, Sama AE: HMGB1 as a potential therapeutic target. / Novartis Found Symp 2007, 280:73-5. CrossRef
  8. Yang H, Wang H, Czura CJ, Tracey KJ: The cytokine activity of HMGB1. / J Leukocyte Biol 2005, 78:1-. CrossRef
  9. Scaffidi P, Misteli T, Bianchi ME: Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. / Nature 2002, 418:191-95. CrossRef
  10. Ulloa L, Ochani M, Yang H, Tanovic M, Halperin D, Yang R, Czura CJ, Fink MP, Tracey KJ: Ethyl pyruvate prevents lethality in mice with established lethal sepsis and systemic inflammation. / Proc Natl Acad Sci 2002, 99:12351-2356. CrossRef
  11. Gazzar ME: HMGB1 modulates inflammatory responses in LPS-activated macrophages. / Inflamm Res 2007, 56:162-67. CrossRef
  12. Yang H, Hreggvidsdottir HS, Palmblad K, Wang H, Ochani M, Li J, Lu B, Chavan S, Rosas-Ballina M, Al-Abed Y, Akira S, Bierhaus A, Erlandsson-Harris H, Andersson U, Tracey KJ: A critical cysteine is required for HMGB1 binding to toll-like receptor 4 and activation of macrophage cytokine release. / PNAS 2010, 26:11942-1947. CrossRef
  13. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR: The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. / JEM 2005, 201:1135-143. CrossRef
  14. Sappington PL, Yang R, Yang H, Tracey KJ, Deluder RL, Fink MP: HMGB1 B box increases the permeability of Caco-2 enterocytic monolayers and impairs intestinal barrier function in mice. / Gastroenterology 2002, 123:790-02. CrossRef
  15. Yang R, Harada T, Mollen KP, Prince JM, Levy RM, Englert JA, Galloitsch-Peerta M, Yang L, Yang H, Tracey KJ, Harbrecht BG, Billiar TR, Fink MP: Anti- HMGB1 neutralizing antibody ameliorates gut barrier dysfunction and improves survival after hemorrhagic shock. / Mol Med 2006, 12:105-14. CrossRef
  16. Ganey PE, Luyendyk JP, Newport SW, Eagle TM, Maddox JF, Mackman N, Roth RA: Role of the coagulation system in acetaminophen induced hepatotoxicity in mice. / Hepatology 2007, 46:1177-186. CrossRef
  17. Yang R, Gallo DJ, Baust JJ, Uchiyama T, Watkins SK, Delude RL, Fink MP: Ethyl pyruvate modulates inflammatory gene expression in mice subjected to hemorrhagic shock. / Am J Physiol Gastrointest Liver Physiol 2002, 283:G212-G222.
  18. Zhang H, Radulescu A, Chen CL, Olson JK, Darbyshire AK, Besner GE: Mice overexpressing the gene for heparin-binding EGF-like growth factor (HB-EGF) have increased resistance to hemorrhagic shock and resuscitation. / Surgery 2011, 149:276-83. CrossRef
  19. Su GL, Gong K, Fan M, Kelley WM, Hsieh J, Sun JM, Hemmila MR, Arbabi S, Remick DG, Wang SC: Lipopolysaccharide-binding protein modulates acetaminophen-induced liver injury in mice. / Hepatology 2005, 41:187-95. CrossRef
  20. Biozzi G, Stiffel C: The physiopathology of the reticuloendothelial cells of the liver and the spleen. / Pro Liver Dis 1965, 2:166-91. CrossRef
  21. Yang R, Zhang S, Kajander H, Zhu S, Koskinen ML, Tenhunen J: Ringer’s lactate improves liver recovery in a murine model of acetaminophen toxicity. / BMC Gastroenterol 2011, 11:125. CrossRef
  22. Yang R, Zhang S, Cotoia A, Oksala N, Zhu S, Tenhunen J: High mobility group B1 impairs hepatocyte regeneration in acetaminophen hepatotoxicity. / BMC Gastroenterol 2012, 12:45. CrossRef
  23. Vaquero J, Belanger M, James L, Herrero R, Desjardins P, Cote J, Blei AT, Butterworth RF: Mild hypothermia attenuates liver injury and improves survival in mice with acetaminophen toxicity. / Gastroenterology 2007, 132:372-08. CrossRef
  24. Yang R, Zou X, Koskinen ML, Tenhunen J: Ethyl pyruvate reduces liver injury at early phase but impairs regeneration at late phase in acetaminophen overdose. / Crit Care 2012, 16:R9. CrossRef
  25. Fausto N: Liver regeneration. / J Hepatol 2000, 32:19-1. CrossRef
  26. Bianchi ME, Manfredi AA: High mobility group B1 (HMGB1) protein at the crossroads between innate and adaptive immunity. / Immunol Rev 2007, 220:35-6. CrossRef
  27. Trautwein C, Boker K, Manns MP: Hepatocyte and immune system: acute phase reaction as a contribution to early defense mechanisms. / Gut 1994, 35:1163-166. CrossRef
  28. Chanda S, Mehendale HM: Hepatic cell division and tissue repair: a key to survival after liver injury. / Mol Med Today 1996, 2:82-9. CrossRef
  29. Mehendale HM: Tissue repair: an important determinant of final outcome of toxicant-induced injury. / Toxicol Pathol 2005, 33:41-1. CrossRef
  30. Chiu H, Gardner CR, Dambach DM, Durham SK, Brittingham JA, Laskin JD, Laskin DL: Role of tumor necrosis factor receptor 1 (p55) in hepatocyte proliferation during acetaminophen-induced toxicity in mice. / Toxicol Appl Pharmacol 2003, 193:218-27. CrossRef
  31. Masubuchi Y, Bourdi M, Reilly TP, Graf ML, George JW, Pohl LR: Role of interleukin-6 in hepatic heat shock protein expression and protection against acetaminophen-induced liver disease. / Biochem Biophys Res Commun 2003, 304:207-12. CrossRef
  32. Yang Q, Shi Y, He JJ, Chen Z: The evolving story of macrophages in acute liver failure. / Immunol Lett 2012, 147:1-. CrossRef
  33. Laskin DL: Macrophages and inflammatory mediators in chemical toxicity: a battle of forces. / Chem Res Toxicol 2009, 22:1376-385. CrossRef
  34. Goldin RD, Ratnayaka ID, Breach CS, Brown IN, Wickramasinghe SN: Role of microphages in acetaminophen (paracetamol)-induced hepatotoxicity. / J Pathol 1996, 179:432-35. CrossRef
  35. Yang R, Miki K, Oksala N, Nakao A, Lindgren L, Killeen ME, Mennander A, Fink MP, Tenhunen J: Bile high mobility group box 1 contributes to gut barrier dysfunction in experimental endotoxemia. / Am J Physiol Rugul Integr Comp Physiol 2009, 297:R362-R369. CrossRef
  36. Yang R, Han X, Delude RL, Fink MP: Ethyl pyruvate ameliorates acute alcohol-induced liver injury and inflammation in mice. / J Lab Clin Med 2003, 142:322-31. CrossRef
  37. Yang R, Uchiyama T, Alber SM, Han X, Watkins SK, Delude RL, Fink MP: Ethyl pyruvate ameliorates distant organ injury in a murine model of acute necrotizing pancreatitis. / Crit Care Med 2004, 32:1453-459. CrossRef
  38. Fink MP: Leaky gut hypothesis: a historical perspective. / Crit Care Med 1990, 18:579-80. CrossRef
  39. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-230X/14/66/prepub
  
• 作者单位：Runkuan Yang (1) (2) (7)
  Xiaoping Zou (3)
  Jyrki Tenhunen (2) (4)
  Shengtao Zhu (5)
  Henri Kajander (6)
  Marja-Leena Koskinen (6)
  Tor Inge Tonnessen (7)
  
  1. Department of Critical Care Medicine, University of Pittsburgh Medical School, 3550 Terrace Street, Pittsburgh, PA, 15261, USA
  2. Department of Intensive Care Medicine, Tampere University Hospital, University of Tampere, 10 Bio Katu, Tampere, 33014, Finland
  7. Department of Anesthesiology and Intensive Care Medicine, Rikshospital, Oslo University, 4950 Nydalen, 0424, Oslo, Norway
  3. Department of Gastroenterology, Drum Tower Hospital, Nanjing University Medical School, 321 Zhongshan Street, 210008, Nanjing, China
  4. Department of Surgical Science, Anesthesiology and Intensive Care Medicine, Uppsala University, 751 85, Uppsala, Sweden
  5. Department of Gastroenterology, Beijing Friendship Hospital, Capital Medical University, 95 Yong An Road, 100050, Beijing, China
  6. Department of Pathology, University of Tampere Medical School, 10 Bio Katu, 33521, Tampere, Finland
  
• ISSN：1471-230X

文摘

Background Acetaminophen (APAP) hepatotoxicity is associated with a high rate of gram-negative enteric bacterial infection; however, the underlying mechanism is still unknown. APAP overdose induces massive hepatocyte necrosis, necrotic tissue releases high mobility group B1 (HMGB1) and exogenous HMGB1 is able to induce gut bacterial translocation (BT) in normal mice; therefore, it is possible that HMGB1 mediates gut BT in APAP hepatotoxicity. This study aims to test this hypothesis by using anti-HMGB1 neutralizing antibody to treat APAP overdose for 24-48 hours. Methods Male C57BL/6 mice were intraperitoneally (i.p.) injected with a single dose of APAP (350 mg/kg dissolved in 1 mL sterile saline). 2 hrs after APAP injection, the APAP challenged mice were randomized to receive treatment with either anti-HMGB1 antibody (400 μg per dose) or non-immune (sham) IgG every 24 h for a total of 2 doses. Results 24 and 48 hrs after APAP challenge, anti-HMGB1 treatment instead of sham IgG therapy significantly decreased serum HMGB1 concentrations and reduced BT by 85%; serum HMGB1 levels were positively correlated with the amount of BT; anti-HMGB1 therapy decreased hepatic BT at 48 h, which was associated with better recovered liver structure and better restored hepatic immune system that was shown by enhanced hepatic mRNA expression of TNF-α, IL-6 and extensive proliferation of inflammatory and reticuloendothelial cells; however, anti-HMGB1 treatment did not decrease gut mucosal permeability as compared to the sham IgG therapy at either 24 or 48 hrs. Conclusion HMGB1 neutralization is associated with bacterial translocation during APAP hepatotoxicity.