Low dose of carbon monoxide intraperitoneal injection provides potent protection against GalN/LPS-induced acute liver injury in mice

Journal of Applied Toxicology

Volumn 33, Issue 12, 2013, Pages 1424-1432

  Wen, Zongmei ^a,b   Liu, Yan ^c   Li, Feng ^d   Wen, Tao ^c  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Carbon monoxide; Hepatocyte apoptosis; Inflammation; Liver injury; Oxidative stress

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CARBON MONOXIDE; CARBOXYHEMOGLOBIN; CYTOKINE; GALACTOSAMINE; GLUTATHIONE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MALONALDEHYDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG EXPOSURE; DRUG MECHANISM; DRUG POTENCY; INJURY SEVERITY; LIVER CELL; LIVER INJURY; LIVER PROTECTION; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE;

MURINAE; MUS;

CARBON MONOXIDE; HEPATOCYTE APOPTOSIS; INFLAMMATION; LIVER INJURY; OXIDATIVE STRESS;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CARBON MONOXIDE; CARBOXYHEMOGLOBIN; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-INDUCED LIVER INJURY; GALACTOSAMINE; HEPATOCYTES; LIPOPOLYSACCHARIDES; LIVER; LIVER FUNCTION TESTS; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE; OXIDATIVE STRESS;

EID: 84886099852     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.2806     Document Type: Article

References (44)

1. Abu-Amara M, Yang SY, Tapuria N, Fuller B, Davidson B, Seifalian A. 2010. Liver ischemia/reperfusion injury: processes in inflammatory networks - a review. Liver Transpl. 16: 1016-1032.
2. Adams DH, Ju C, Ramaiah SK, Uetrecht J, Jaeschke H. 2010. Mechanisms of immune-mediated liver injury. Toxicol. Sci. 115: 307-321.
3. Amersi F, Shen XD, Anselmo D, Melinek J, Iyer S, Southard DJ, Katori M, Volk HD, Busuttil RW, Buelow R, Kupiec-Weglinski JW. 2002. Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway. Hepatology 35: 815-823.
4. Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE. 2008. Heme oxygenase and carbon monoxide initiate homeostatic signaling. J. Mol. Med. 86: 267-279.
5. Cepinskas G, Katada K, Bihari A, Potter RF. 2008. Carbon monoxide liberated from carbon monoxide-releasing molecule CORM-2 attenuates inflammation in the liver of septic mice. Am. J. Physiol. Gastrointest. Liver Physiol. 294: G184-G191.
6. Chen T, Zamora R, Zuckerbraun B, Billiar TR. 2003. Role of nitric oxide in liver injury. Curr. Mol. Med. 3: 519-526.
7. Chhikara M, Wang S, Kern SJ, Ferreyra G, Barb JJ, Munson PJ, Danner RL. 2009. Carbon monoxide blocks lipopolysaccharide-induced gene expression by interfering with proximal TLR4 to NF-kappaB signal transduction in human monocytes. PLoS One 4: e8139.
8. Chung SW, Liu X, Macias AA, Baron RM, Perrella MA. 2008. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J. Clin. Invest. 118: 239-247.
9. Chung J, Shin DY, Zheng M, Joe Y, Pae HO, Ryter SW, Chung HT. 2011. Carbon monoxide, a reaction product of heme oxygenase-1, suppresses the expression of C-reactive protein by endoplasmic reticulum stress through modulation of the unfolded protein response. Mol. Immunol. 48: 1793-1799.
10. Conde de la Rosa L, Vrenken TE, Hannivoort R, Buist-Homan M, Having R, Slebos DJ, Kauffman HF, Faber KN, Jansen PLM, Moshage H. 2008. Carbon monoxide blocks oxidative stress-induced hepatocyte apoptosis via inhibition of the p54 JNK isoform. Free Radic. Biol. Med. 44: 1323-1333.
11. Craig DGN, Lee P, Pryde E, Masterton GS, Hayes PC, Simpson KJ. 2011. Circulating apoptotic and necrotic cell death markers in patients with acute liver injury. Liver Int. 31: 1127-1136.
12. Foresti R, Bani-Hani MG, Motterlini R. 2008. Use of carbon monoxide as a therapeutic agent: promises and challenges. Intensive Care Med. 34: 649-658.
13. Guan L, Wen T, Zhang Y, Wang X, Zhao J.2009. Induction of heme oxygenase-1 with hemin attenuates hippocampal injury in rats after acute carbon monoxide poisoning. Toxicology 262: 146-152.
14. Hoetzel A, Dolinay T, Schmidt R, Choi AMK, Ryter SW. 2007. Carbon monoxide in sepsis. Antioxid. Redox Signal. 9: 2013-2026.
15. Jaeschke H, Hasegawa T. 2006. Role of neutrophils in acute inflammatory liver injury. Liver Int. 26: 912-919.
16. Jaeschke H, Gores GJ, Cederbaum AI, Hinson JA, Pessayre D, Lemasters JJ. 2002. Mechanisms of hepatotoxicity. Toxicol. Sci. 65: 166-176.
17. Kaizu T, Ikeda A, Nakao A, Tsung A, Toyokawa H, Ueki S, Geller D, Murase N. 2008. Protection of transplant-induced hepatic ischemia/reperfusion injury with carbon monoxide via MEK/ERK1/2 pathway downregulation. Am. J. Physiol. Gastrointest. Liver Physiol. 294: G236-G244.
18. Kim HP, Ryter SW, Choi AMK. 2006. CO as a cellular signaling molecule. Annu. Rev. Pharmacol. Toxicol. 46: 411-449.
19. Korhonen R, Lahti A, Kankaanranta H, Moilanen E. 2005. Nitric oxide production and signaling in inflammation. Curr. Drug Targets Inflamm. Allergy 4: 471-479.
20. Kuramitsu K, Gallo D, Yoon M, Chin BY, Csizmadia E, Hanto DW, Otterbein LE. 2011. Carbon monoxide enhances early liver regeneration in mice after hepatectomy. Hepatology 53: 2016-2026.
21. Leffler CW, Parfenova H, Jaggar JH. 2011. Carbon monoxide as an endogenous vascular modulator. Am. J. Physiol. Heart Circul. Physiol. 301: H1-H11.
22. Lin YT, Chen YH, Yang YH, Jao HC, Abiko Y, Yokoyama K, Hsu C. 2010. Heme oxygenase-1 suppresses the infiltration of neutrophils in rat liver during sepsis through inactivation of p38 MAPK. Shock 34: 615-621.
23. Liu SH, Ma K, Xu XR, Xu B. 2010. A single dose of carbon monoxide intraperitoneal administration protects rat intestine from injury induced by lipopolysaccharide. Cell Stress Chaperones 15: 717-727.
24. Malle E, Furtmüller PG, Sattler W, Obinger C. 2007. Myeloperoxidase: a target for new drug development? Br. J. Pharmacol. 152: 838-854.
25. Motterlini R, Otterbein LE. 2010. The therapeutic potential of carbon monoxide. Nat. Rev. Drug Discov. 9: 728-743.
26. Nakao A, Schmidt J, Harada T, Tsung A, Stoffels B, Cruz RJ, Kohmoto J, Peng X, Tomiyama K, Murase N, Bauer AJ, Fink MP. 2006. A single intraperitoneal dose of carbon monoxide-saturated ringer's lactate solution ameliorates postoperative ileus in mice. J. Pharmacol. Exp. Ther. 319: 1265-1275.
27. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell R, Choi M. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6: 422-428.
28. Otterbein LE, Hedblom A, Harris C, Csizmadia E, Gallo D, Wegiel B. 2011. Heme oxygenase-1 and carbon monoxide modulate DNA repair through ataxia-telangiectasia mutated (ATM) protein. Proc. Natl Acad. Sci. USA 108: 14491-14496.
29. Piantadosi C. 2008. Carbon monoxide, reactive oxygen signaling, and oxidative stress. Free Radic. Biol. Med. 45: 562-569.
30. Piantadosi C, Carraway MS, Suliman HB. 2006. Carbon monoxide, oxidative stress, and mitochondrial permeability pore transition. Free Radic. Biol. Med. 40: 1332-1339.
31. Ryter S, Alam J. 2006. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86: 583-650.
32. Ryter SW, Otterbein LE, Morse D, Choi AMK. 2002. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell. Biochem. 234-235: 249-263.
33. Ryter SW, Kim HP, Nakahira K, Zuckerbraun BS, Morse D, Choi AMK. 2007. Protective functions of heme oxygenase-1 and carbon monoxide in the respiratory system. Antioxid. Redox. Signal. 9: 2157-2173.
34. Sheng WS, Hu S, Nettles AR, Lokensgard JR, Vercellotti GM, Rock RB. 2010. Hemin inhibits NO production by IL-1β-stimulated human astrocytes through induction of heme oxygenase-1 and reduction of p38 MAPK activation. J. Neuroinflamm. 7: 51.
35. Thom SR, Weaver LK, Hampson NB. 2005. 'Therapeutic' carbon monoxide may be toxic. Am. J. Respir. Crit. Care Med. 171: 1318.
36. Tomiyama K, Ikeda A, Ueki S, Nakao A, Stolz DB, Koike Y, Afrazi A, Gandhi C, Tokita D, Geller D, Murase N. 2008. Inhibition of Kupffer cell-mediated early proinflammatory response with carbon monoxide in transplant-induced hepatic ischemia/reperfusion injury in rats. Hepatology 48: 1608-1620.
37. Tsui TY, Obed A, Siu YT, Yet SF, Prantl L, Schlitt HJ, Fan ST. 2007. Carbon monoxide inhalation rescues mice from fulminant hepatitis through improving hepatic energy metabolism. Shock 27: 165-171.
38. Wen T, Guan L, Zhang YL, Zhao JY. 2006. Dynamic changes of heme oxygenase-1 and carbon monoxide production in acute liver injury induced by carbon tetrachloride in rats. Toxicology 228: 51-57.
39. Wen T, Wu ZM, Liu Y, Tan Y, Ren F, Wu H.2007. Upregulation of heme oxygenase-1 with hemin prevents d-galactosamine and lipopolysaccharide-induced acute hepatic injury in rats. Toxicology 237: 184-193.
40. Wilson MR, O'Dea KP, Dorr AD, Yamamoto H, Goddard ME, Takata M. 2010. Efficacy and safety of inhaled carbon monoxide during pulmonary inflammation in mice. PLoS One 5: e11565.
41. Yao P, Hao L, Nussler N, Lehmann A, Song F, Zhao J, Neuhaus P, Liu L, Nussler A.2009. The protective role of HO-1 and its generated products (CO, bilirubin, and Fe) in ethanol-induced human hepatocyte damage. Am. J. Physiol. Gastrointest. Liver Physiol. 296: G1318-G1323.
42. Zeerleder S, Zwart B, Wuillemin W, Aarden L, Groeneveld BJ, Caliezi C, van Nieuwenhuijze AEM, van Mierlo GJ, Eerenberg AJM, Lämmle B, Hack CE. 2003. Elevated nucleosome levels in systemic inflammation and sepsis. Crit. Care Med. 31: 1947-1951.
43. Zhang R, Brennan ML, Fu X, Aviles RJ, Pearce GL, Penn MS, Topol EJ, Sprecher DL, Hazen SL. 2001. Association between myeloperoxidase levels and risk of coronary artery disease. JAMA 286: 2136-2142.
44. Zhang X, Shan P, Otterbein LE, Alam J, Flavell R, Davis RJ, Choi AMK, Lee PJ. 2003. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J. Biol. Chem. 278: 1248-1258.