Carbon monoxide-based therapy ameliorates acute pancreatitis via TLR4 inhibition

Journal of Clinical Investigation

Volumn 124, Issue 1, 2014, Pages 437-447

  Xue, Jing ^a   Habtezion, Aida ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; CARBON MONOXIDE RELEASING MOLECULE 2; CERULETIDE; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 1ALPHA; INTERLEUKIN 22; INTERLEUKIN 6; MYELOPEROXIDASE; PROTEIN MD 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACUTE PANCREATITIS; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EX VIVO STUDY; FEMALE; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; LUNG INJURY; MORTALITY; MOUSE; NONHUMAN; PANCREAS INJURY; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION;

EID: 84892922204     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI71362     Document Type: Article

References (52)

1. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov. 2010;9(9):728-743
2. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol. 1997;37:517-554
3. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin Invest. 1999;103(7):1047-1054
4. Soares MP, et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med. 1998;4(9):1073-1077
5. Hegazi RA, Rao KN, Mayle A, Sepulveda AR, Otterbein LE, Plevy SE. Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Exp Med. 2005; 202(12):1703-1713
6. Kaizu T, et al. Protection of transplant-induced hepatic ischemia/reperfusion injury with carbon monoxide via MEK/ERK1/2 pathway downregulation. American Journal of Physiology. Am J Physiol Gastrointest Liver Physiol. 2008; 294(1):G236-G244
7. Motterlini R, Clark JE, Foresti R, Sarathchandra P, Mann BE, Green CJ. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res. 2002;90(2):E17-E24
8. Sharif R, et al. Impact of toll-like receptor 4 on the severity of acute pancreatitis and pancreatitis-Associated lung injury in mice. Gut. 2009;58(6):813-819
9. Ohashi K, Burkart V, Flohe S, Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol. 2000;164(2):558-561
10. Apetoh L, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13(9):1050-1059
11. Park JS, et al. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem. 2004;279(9):7370-7377
12. Johnson GB, Brunn GJ, Platt JL. Cutting edge: an endogenous pathway to systemic inflammatory response syndrome (SIRS)-like reactions through Toll-like receptor 4. J Immunol. 2004;172(1):20-24
13. Erridge C. Endogenous ligands of TLR2 and TLR4: agonists or assistants? J Leuk Biol. 2010; 87(6):989-999
14. Yang H, et al. A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proc Natl Acad Sci U S A. 2010;107(26):11942-11947
15. Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leuk Biol. 2009;86(3):557-566
16. Park BS, Song DH, Kim HM, Choi BS, Lee H, Lee JO. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature. 2009;458(7242):1191-1195
17. Rocuts F, et al. Carbon monoxide suppresses membrane expression of TLR4 via myeloid differentiation factor-2 in betaTC3 cells. J Immunol. 2010;185(4):2134-2139
18. Li Y, et al. Toll-like receptor 4 detected in exocrine pancreas and the change of expression in ceruleininduced pancreatitis. Pancreas. 2005;30(4):375-381
19. Habtezion A, et al. Panhematin provides a therapeutic benefit in experimental pancreatitis. Gut. 2011;60(5):671-679
20. Nakamichi I, Habtezion A, Zhong B, Contag CH, Butcher EC, Omary MB. Hemin-Activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. J Clin Invest. 2005;115(11):3007- 3014
21. Wagener FA, et al. Different faces of the hemeheme oxygenase system in inflammation. Pharmacol Rev. 2003;55(3):551-571
22. Xue J, Nguyen DT, Habtezion A. Aryl hydrocarbon receptor regulates pancreatic IL-22 production and protects mice from acute pancreatitis. Gastroenterology. 2012;143(6):1670-1680
23. Chen P, et al. Effects of carbon monoxide releasing molecule-liberated CO on severe acute pancreatitis in rats. Cytokine. 2010;49(1):15-23
24. Makhija R, Kingsnorth AN. Cytokine storm in acute pancreatitis. J Hepatobiliary Pancreat Surg. 2002;9(4):401-410
25. Habtezion A, et al. Heme oxygenase-1 is induced in peripheral blood mononuclear cells of patients with acute pancreatitis: a potential therapeutic target. American journal of physiology. Am J Physiol Gastrointest Liver Physiol. 2011;300(1):G12-G20
26. Norman JG, Fink GW, Franz MG. Acute pancreatitis induces intrapancreatic tumor necrosis factor gene expression. Arch Surg. 1995;130(9):966-970
27. Norman JG, et al. Tissue-specific cytokine production during experimental acute pancreatitis. A probable mechanism for distant organ dysfunction. Dig Dis Sci. 1997;42(8):1783-1788
28. Wig JD, Kochhar R, Ray JD, Krishna Rao DV, Gupta NM, Ganguly NK. Endotoxemia predicts outcome in acute pancreatitis. J Clin Gastroenterol. 1998;26(2):121-124
29. Sharma M, et al. Alterations in intestinal permeability and endotoxemia in severe acute pancreatitis. Trop Gastroenterol. 2012;33(1):45-50
30. Hoque R, Malik AF, Gorelick F, Mehal WZ. Sterile inflammatory response in acute pancreatitis. Pancreas. 2012;41(3):353-357
31. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol. 2011;29:139-162
32. Kocsis AK, et al. Plasma concentrations of highmobility group box protein 1, soluble receptor for advanced glycation end-products and circulating DNA in patients with acute pancreatitis. Pancreatology. 2009;9(4):383-391
33. Yasuda T, et al. Increase of high-mobility group box chromosomal protein 1 in blood and injured organs in experimental severe acute pancreatitis. Pancreas. 2007;34(4):487-488
34. Nakahira K, et al. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med. 2006;203(10):2377-2389
35. Kim HM, et al. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell. 2007;130(5):906-917
36. Jara-Oseguera A, et al. Uncoupling charge movement from channel opening in voltage-gated potassium channels by ruthenium complexes. J Biol Chem. 2011;286(18):16414-16425
37. Dong DL, et al. Tricarbonyldichlororuthenium (II) dimer (CORM2) activates non-selective cation current in human endothelial cells independently of carbon monoxide releasing. Eur J Pharmacol. 2008;590(1-3):99-104
38. Stohs SJ, Bagchi D. Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med. 1995;18(2):321-336
39. Dolinay T, Szilasi M, Liu M, Choi AM. Inhaled carbon monoxide confers antiinflammatory effects against ventilator-induced lung injury. Am J Respir Crit Care Med. 2004;170(6):613-620
40. Thom SR, Weaver LK, Hampson NB. "Therapeutic" carbon monoxide may be toxic. Am J Respir Crit Care Med. 2005;171(11):1318
41. Desmard M, et al. Differential antibacterial activity against Pseudomonas aeruginosa by carbon monoxide-releasing molecules. Antioxid Redox Signal. 2012;16(2):153-163
42. Winburn IC, Gunatunga K, McKernan RD, Walker RJ, Sammut IA, Harrison JC. Cell damage following carbon monoxide releasing molecule exposure: implications for therapeutic applications. Basic Clin Pharmacol Toxicol. 2012;111(1):31-41
43. Rongione AJ, Kusske AM, Kwan K, Ashley SW, Reber HA, McFadden DW. Interleukin 10 reduces the severity of acute pancreatitis in rats. Gastroenterology. 1997;112(3):960-967
44. Soni H, Pandya G, Patel P, Acharya A, Jain M, Mehta AA. Beneficial effects of carbon monoxide- releasing molecule-2 (CORM-2) on acute doxorubicin cardiotoxicity in mice: role of oxidative stress and apoptosis. Toxicol Appl Pharmacol. 2011;253(1):70-80
45. Sun B, Sun Z, Jin Q, Chen X. CO-releasing molecules (CORM-2)-liberated CO attenuates leukocytes infiltration in the renal tissue of thermally injured mice. Int J Biol Sci. 2008;4(3):176-183
46. Wei Y, Chen P, de Bruyn M, Zhang W, Bremer E, Helfrich W. Carbon monoxide-releasing molecule- 2 (CORM-2) attenuates acute hepatic isch- emia reperfusion injury in rats. BMC Gastroenterol. 2010;10:42
47. Sawle P, Foresti R, Mann BE, Johnson TR, Green CJ, Motterlini R. Carbon monoxide-releasing molecules (CO-RMs) attenuate the inflammatory response elicited by lipopolysaccharide in RAW264.7 murine macrophages. Br J Pharmacol. 2005;145(6):800-810
48. Spormann H, Sokolowski A, Letko G. Experimental acute pancreatitis - a quantification of dynamics at enzymic and histomorphologic levels. Pathol Res Pract. 1989;185(3):358-362
49. Zhang X, Goncalves R, Mosser DM. The isolation and characterization of murine macrophages. Curr Protoc Immunol. 2008;Chapter 14:Unit 14.1
50. Weischenfeldt J, Porse B. Bone marrow-derived macrophages (BMM): isolation and applications. CSH Protoc. 2008;2008:pdb.prot5080
51. Hietaranta AJ, et al. Water immersion stress prevents caerulein-induced pancreatic acinar cell NF-kappa B activation by attenuating caeruleininduced intracellular Ca2+ changes. J Biol Chem. 2001;276(22):18742-18747
52. Gukovsky I, et al. Phosphatidylinositide 3-kinase gamma regulates key pathologic responses to cholecystokinin in pancreatic acinar cells. Gastroenterology. 2004;126(2):554-566.