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PMID: 24334457 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Carbon monoxide-based therapy ameliorates acute pancreatitis via TLR4 inhibition.

The Journal of clinical investigation ·Vol. 124 ·No. 1 ·2014-01-00 ·Pages 437-47

Xue J, Habtezion A

Abstract

The protective role of hemeoxygenase-1 (HO-1) in various inflammatory conditions is mediated in part by its products, carbon monoxide (CO) and biliverdin. Here we investigated a therapeutic role for CO and CO-primed cells in acute pancreatitis (AP). In a mouse model of AP, treatment with CO-releasing molecule-2 (CORM-2) decreased mortality, pancreatic damage, and lung injury. CORM-2 decreased systemic inflammatory cytokines, suppressed systemic and pancreatic macrophage TNF-α secretion, and inhibited macrophage TLR4 receptor complex expression. In both human and mouse cells, CORM-2 inhibited endogenous and exogenous ligand-dependent TLR4 activation, which indicates that CORM-2 could be therapeutic for both early and late stages of AP, which involve sterile- and endotoxin-mediated inflammation, respectively. Mice engrafted with TLR4-deficient hematopoietic cells were protected against caerulein-induced AP. In the absence of leukocyte TLR4 expression, CORM-2 did not confer additional protection, which indicates that CORM-2-dependent effects are mediated via suppression of macrophage TLR4 activation. We determined that CO was directly responsible for the protective effects of CORM-2 in AP, as inactive forms of CORM-2 were ineffective. Importantly, adoptive transfer of CORM-2-primed cells reduced AP. Such a therapeutic approach would translate the beneficial effects of CO-based therapies, avoiding CO- or CO-RM-mediated toxicities in AP and a wide range of diseases.

MeSH Terms
Acute Disease Adoptive Transfer Animals Carbon Monoxide/pharmacology,therapeutic use Cells, Cultured Female Humans Inflammation Mediators/metabolism Lipopolysaccharides/pharmacology Lymphocyte Antigen 96/metabolism Macrophages/metabolism Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout Organometallic Compounds/pharmacology,therapeutic use Pancreas/immunology,metabolism,pathology Pancreatitis/drug therapy,immunology Spleen/metabolism Toll-Like Receptor 4/antagonists & inhibitors,metabolism Tumor Necrosis Factor-alpha/metabolism
Chemicals
Inflammation Mediators Lipopolysaccharides Ly96 protein, mouse Lymphocyte Antigen 96 Organometallic Compounds Tlr4 protein, mouse Toll-Like Receptor 4 Tumor Necrosis Factor-alpha tricarbonyldichlororuthenium (II) dimer Carbon Monoxide
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Xue Jing
Habtezion Aida
References (52)
52 references, click to expand
  1. Carbon monoxide suppresses membrane expression of TLR4 via myeloid differentiation factor-2 in betaTC3 cells.
    J Immunol. 2010 Aug 15;185(4):2134-9 PMID: 20631306
  2. Protection of transplant-induced hepatic ischemia/reperfusion injury with carbon monoxide via MEK/ERK1/2 pathway downregulation.
    Am J Physiol Gastrointest Liver Physiol. 2008 Jan;294(1):G236-44 PMID: 18006605
  3. Heme oxygenase-1 is induced in peripheral blood mononuclear cells of patients with acute pancreatitis: a potential therapeutic target.
    Am J Physiol Gastrointest Liver Physiol. 2011 Jan;300(1):G12-20 PMID: 20966033
  4. The isolation and characterization of murine macrophages.
    Curr Protoc Immunol. 2008 Nov;Chapter 14:Unit 14.1 PMID: 19016445
  5. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein.
    J Biol Chem. 2004 Feb 27;279(9):7370-7 PMID: 14660645
  6. Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway.
    J Exp Med. 2005 Dec 19;202(12):1703-13 PMID: 16365149
  7. Aryl hydrocarbon receptor regulates pancreatic IL-22 production and protects mice from acute pancreatitis.
    Gastroenterology. 2012 Dec;143(6):1670-80 PMID: 23022954
  8. 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 May 15;253(1):70-80 PMID: 21443895
  9. Cytokine storm in acute pancreatitis.
    J Hepatobiliary Pancreat Surg. 2002;9(4):401-10 PMID: 12483260
  10. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities.
    Circ Res. 2002 Feb 8;90(2):E17-24 PMID: 11834719
  11. Oxidative mechanisms in the toxicity of metal ions.
    Free Radic Biol Med. 1995 Feb;18(2):321-36 PMID: 7744317
  12. Carbon monoxide-releasing molecule-2 (CORM-2) attenuates acute hepatic ischemia reperfusion injury in rats.
    BMC Gastroenterol. 2010 May 05;10:42 PMID: 20444253
  13. "Therapeutic" carbon monoxide may be toxic.
    Am J Respir Crit Care Med. 2005 Jun 1;171(11):1318 PMID: 15914571
  14. Plasma concentrations of high-mobility group box protein 1, soluble receptor for advanced glycation end-products and circulating DNA in patients with acute pancreatitis.
    Pancreatology. 2009;9(4):383-91 PMID: 19451748
  15. Increase of high-mobility group box chromosomal protein 1 in blood and injured organs in experimental severe acute pancreatitis.
    Pancreas. 2007 May;34(4):487-8 PMID: 17446855
  16. HMGB1 is a therapeutic target for sterile inflammation and infection.
    Annu Rev Immunol. 2011;29:139-62 PMID: 21219181
  17. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran.
    Cell. 2007 Sep 7;130(5):906-17 PMID: 17803912
  18. Acute pancreatitis induces intrapancreatic tumor necrosis factor gene expression.
    Arch Surg. 1995 Sep;130(9):966-70 PMID: 7661681
  19. Water immersion stress prevents caerulein-induced pancreatic acinar cell nf-kappa b activation by attenuating caerulein-induced intracellular Ca2+ changes.
    J Biol Chem. 2001 Jun 1;276(22):18742-7 PMID: 11278554
  20. Carbon monoxide-releasing molecules (CO-RMs) attenuate the inflammatory response elicited by lipopolysaccharide in RAW264.7 murine macrophages.
    Br J Pharmacol. 2005 Jul;145(6):800-10 PMID: 15880142
  21. Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction.
    J Clin Invest. 2005 Nov;115(11):3007-14 PMID: 16239966
  22. Tissue-specific cytokine production during experimental acute pancreatitis. A probable mechanism for distant organ dysfunction.
    Dig Dis Sci. 1997 Aug;42(8):1783-8 PMID: 9286248
  23. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex.
    Nature. 2009 Apr 30;458(7242):1191-5 PMID: 19252480
  24. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer.
    J Leukoc Biol. 2009 Sep;86(3):557-66 PMID: 19451397
  25. Sterile inflammatory response in acute pancreatitis.
    Pancreas. 2012 Apr;41(3):353-7 PMID: 22415665
  26. Endogenous ligands of TLR2 and TLR4: agonists or assistants?
    J Leukoc Biol. 2010 Jun;87(6):989-99 PMID: 20179153
  27. The heme oxygenase system: a regulator of second messenger gases.
    Annu Rev Pharmacol Toxicol. 1997;37:517-54 PMID: 9131263
  28. Panhematin provides a therapeutic benefit in experimental pancreatitis.
    Gut. 2011 May;60(5):671-9 PMID: 21159893
  29. Differential antibacterial activity against Pseudomonas aeruginosa by carbon monoxide-releasing molecules.
    Antioxid Redox Signal. 2012 Jan 15;16(2):153-63 PMID: 21864022
  30. Experimental acute pancreatitis--a quantification of dynamics at enzymic and histomorphologic levels.
    Pathol Res Pract. 1989 Sep;185(3):358-62 PMID: 2813189
  31. Phosphatidylinositide 3-kinase gamma regulates key pathologic responses to cholecystokinin in pancreatic acinar cells.
    Gastroenterology. 2004 Feb;126(2):554-66 PMID: 14762792
  32. Cutting edge: an endogenous pathway to systemic inflammatory response syndrome (SIRS)-like reactions through Toll-like receptor 4.
    J Immunol. 2004 Jan 1;172(1):20-4 PMID: 14688304
  33. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy.
    Nat Med. 2007 Sep;13(9):1050-9 PMID: 17704786
  34. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex.
    J Immunol. 2000 Jan 15;164(2):558-61 PMID: 10623794
  35. Uncoupling charge movement from channel opening in voltage-gated potassium channels by ruthenium complexes.
    J Biol Chem. 2011 May 6;286(18):16414-25 PMID: 21454671
  36. Expression of heme oxygenase-1 can determine cardiac xenograft survival.
    Nat Med. 1998 Sep;4(9):1073-7 PMID: 9734404
  37. Cell damage following carbon monoxide releasing molecule exposure: implications for therapeutic applications.
    Basic Clin Pharmacol Toxicol. 2012 Jul;111(1):31-41 PMID: 22269084
  38. Effects of carbon monoxide releasing molecule-liberated CO on severe acute pancreatitis in rats.
    Cytokine. 2010 Jan;49(1):15-23 PMID: 19900821
  39. Bone Marrow-Derived Macrophages (BMM): Isolation and Applications.
    CSH Protoc. 2008 Dec 01;2008:pdb.prot5080 PMID: 21356739
  40. Interleukin 10 reduces the severity of acute pancreatitis in rats.
    Gastroenterology. 1997 Mar;112(3):960-7 PMID: 9041259
  41. CO-releasing molecules (CORM-2)-liberated CO attenuates leukocytes infiltration in the renal tissue of thermally injured mice.
    Int J Biol Sci. 2008 Jun 16;4(3):176-83 PMID: 18566696
  42. Endotoxemia predicts outcome in acute pancreatitis.
    J Clin Gastroenterol. 1998 Mar;26(2):121-4 PMID: 9563923
  43. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts.
    J Exp Med. 2006 Oct 2;203(10):2377-89 PMID: 17000866
  44. Alterations in intestinal permeability and endotoxemia in severe acute pancreatitis.
    Trop Gastroenterol. 2012 Jan-Mar;33(1):45-50 PMID: 22803295
  45. Different faces of the heme-heme oxygenase system in inflammation.
    Pharmacol Rev. 2003 Sep;55(3):551-71 PMID: 12869663
  46. Impact of toll-like receptor 4 on the severity of acute pancreatitis and pancreatitis-associated lung injury in mice.
    Gut. 2009 Jun;58(6):813-9 PMID: 19201771
  47. 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 Jun 29;107(26):11942-7 PMID: 20547845
  48. Tricarbonyldichlororuthenium (II) dimer (CORM2) activates non-selective cation current in human endothelial cells independently of carbon monoxide releasing.
    Eur J Pharmacol. 2008 Aug 20;590(1-3):99-104 PMID: 18582862
  49. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury.
    J Clin Invest. 1999 Apr;103(7):1047-54 PMID: 10194478
  50. Toll-like receptor 4 detected in exocrine pancreas and the change of expression in cerulein-induced pancreatitis.
    Pancreas. 2005 May;30(4):375-81 PMID: 15841051
  51. The therapeutic potential of carbon monoxide.
    Nat Rev Drug Discov. 2010 Sep;9(9):728-43 PMID: 20811383
  52. Inhaled carbon monoxide confers antiinflammatory effects against ventilator-induced lung injury.
    Am J Respir Crit Care Med. 2004 Sep 15;170(6):613-20 PMID: 15142867
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
1558-8238
Published
2014-01-00
Epub
2013-00-16
Pages
437-47
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC3871246
Subset
IM
Grants
NIDDK NIH HHS · P30 DK056339 · United States
NIDDK NIH HHS · R01 DK092421 · United States
NIDDK NIH HHS · DK56339 · United States
NIDDK NIH HHS · DK092421 · United States
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