Abstract
The role of the Toll-like receptor 4 (TLR4), a component of the innate immune system, in the development of burn-induced acute lung injury (ALI) has not been completely defined. Recent data suggested that an intact TLR4 plays a major role in the development of organ injury in sterile inflammation. We hypothesized that burn-induced ALI is a TLR4-dependent process. Male C57BL/6J (TLR4 wild-type [WT]) and C57BL/10ScN (TLR4 knockout [KO]) mice were subjected to a 30% total body surface area steam burn. Animals were killed at 6 and 24 h after the insult. Lung specimens were harvested for histological examination after hematoxylin-eosin staining. In addition, lung myeloperoxidase (MPO) and intercellular adhesion molecule 1 immunostaining was performed. Lung MPO was measured by an enzymatic assay. Total lung keratinocyte-derived chemoattractant (IL-8) content was measured by enzyme-linked immunosorbent assay. Western blot was performed to quantify phosphorylated IκBα, phosphorylated nuclear factor κB p65 (NF-κBp65), and high mobility group box 1 expression. Acute lung injury, characterized by thickening of the alveolar-capillary membrane, hyaline membrane formation, intraalveolar hemorrhage, and neutrophil infiltration, was seen in WT but not KO animals at 24 h. Myeloperoxidase and intercellular adhesion molecule 1 immunostaining of KO animals was also similar to sham but elevated in WT animals. In addition, a reduction in MPO enzymatic activity was observed in KO mice as well as a reduction in IL-8 levels compared with their WT counterparts. Burn-induced ALI develops within 24 h after the initial thermal insult in our model. Toll-like receptor 4 KO animals were clearly protected and had a much less severe lung injury. Our data suggest that burn-induced ALI is a TLR4-dependent process.
MeSH Terms
Acute Lung Injury/metabolism
Animals
Blotting, Western
Burns/metabolism,physiopathology
Enzyme-Linked Immunosorbent Assay
High Mobility Group Proteins/metabolism
I-kappa B Proteins/metabolism
Intercellular Adhesion Molecule-1
Interleukin-8/metabolism
Male
Mice
Mice, Inbred C57BL
NF-KappaB Inhibitor alpha
Peroxidase/metabolism
Toll-Like Receptor 4/metabolism
Transcription Factor RelA/metabolism
Chemicals
High Mobility Group Proteins
I-kappa B Proteins
Interleukin-8
Nfkbia protein, mouse
Toll-Like Receptor 4
Transcription Factor RelA
Intercellular Adhesion Molecule-1
NF-KappaB Inhibitor alpha
Peroxidase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Krzyzaniak Michael
Division of Trauma, Surgical Critical Care, and Burns, Department of Surgery, University of California, San Diego School of Medicine, San Diego, California, USA.
Cheadle Gerald
Peterson Carrie
Loomis William
Putnam James
Wolf Paul
Baird Andrew
Eliceiri Brian
Bansal Vishal
Coimbra Raul
References (27)
27 references, click to expand
-
Role of Toll-like receptor 4 on pancreatic and pulmonary injury in a mice model of acute pancreatitis associated with endotoxemia.
Crit Care Med. 2004 Aug;32(8):1759-63
PMID: 15286555
-
TLR4 is essential in acute lung injury induced by unresuscitated hemorrhagic shock.
J Trauma. 2009 Jan;66(1):124-31
PMID: 19131815
-
Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction.
J Biol Chem. 1999 Apr 16;274(16):10689-92
PMID: 10196138
-
Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation.
Trends Biochem Sci. 2005 Jan;30(1):43-52
PMID: 15653325
-
A standard animal burn.
J Trauma. 1968 Nov;8(6):1049-51
PMID: 5722120
-
Burn-induced gut barrier injury is attenuated by phosphodiesterase inhibition: effects on tight junction structural proteins.
Shock. 2009 Apr;31(4):416-22
PMID: 18791495
-
The role of toll-like receptors in acute and chronic lung inflammation.
J Inflamm (Lond). 2010 Nov 25;7:57
PMID: 21108806
-
HMGB1 contributes to the development of acute lung injury after hemorrhage.
Am J Physiol Lung Cell Mol Physiol. 2005 May;288(5):L958-65
PMID: 15640285
-
Hydroxyethyl starch 130/0.4 exerts its anti-inflammatory effect in endotoxemic rats by inhibiting the TLR4/NF-kappaB signaling pathway.
Ann Clin Lab Sci. 2010 Summer;40(3):240-6
PMID: 20689135
-
Toll-like receptor-4 mediates intestinal barrier breakdown after thermal injury.
Surg Infect (Larchmt). 2010 Apr;11(2):137-44
PMID: 20374005
-
Incidence and mortality of acute lung injury and the acute respiratory distress syndrome in three Australian States.
Am J Respir Crit Care Med. 2002 Feb 15;165(4):443-8
PMID: 11850334
-
Circulating interleukin-1 beta and tumor necrosis factor-alpha concentrations after burn injury in humans.
Crit Care Med. 1992 Oct;20(10):1414-9
PMID: 1395662
-
Toll-like receptor 4-dependent responses to lung injury in a murine model of pulmonary contusion.
Shock. 2009 Apr;31(4):376-81
PMID: 18665044
-
HMGB1: endogenous danger signaling.
Mol Med. 2008 Jul-Aug;14(7-8):476-84
PMID: 18431461
-
Pentoxifylline attenuates lung injury and modulates transcription factor activity in hemorrhagic shock.
J Surg Res. 2007 Nov;143(1):99-108
PMID: 17950078
-
Systemic inflammation and remote organ injury following trauma require HMGB1.
Am J Physiol Regul Integr Comp Physiol. 2007 Oct;293(4):R1538-44
PMID: 17652366
-
Hemorrhage-induced acute lung injury is TLR-4 dependent.
Am J Physiol Regul Integr Comp Physiol. 2004 Sep;287(3):R592-9
PMID: 15072965
-
LPS-stimulated PMN activation and proinflammatory mediator synthesis is downregulated by phosphodiesterase inhibition: role of pentoxifylline.
J Trauma. 2004 Dec;57(6):1157-63
PMID: 15625444
-
Role of the neutrophil in adult respiratory distress syndrome.
Br J Surg. 1993 Jan;80(1):10-7
PMID: 8428262
-
HMG-1 as a mediator of acute lung inflammation.
J Immunol. 2000 Sep 15;165(6):2950-4
PMID: 10975801
-
Pulmonary complications in burn patients. A comparative study of 697 patients.
J Thorac Cardiovasc Surg. 1970 Jan;59(1):7-20
PMID: 5409956
-
HMGB1 signals through toll-like receptor (TLR) 4 and TLR2.
Shock. 2006 Aug;26(2):174-9
PMID: 16878026
-
TLR Cross-Talk Mechanism of Hemorrhagic Shock-Primed Pulmonary Neutrophil Infiltration.
Open Crit Care Med J. 2010 Jan 1;2:1-8
PMID: 20072711
-
Pattern recognition receptor-dependent mechanisms of acute lung injury.
Mol Med. 2010 Jan-Feb;16(1-2):69-82
PMID: 19949486
-
The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity.
Immunol Rev. 2007 Dec;220:60-81
PMID: 17979840
-
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
-
TLR-4, IL-1R and TNF-R signaling to NF-kappaB: variations on a common theme.
Cell Mol Life Sci. 2008 Oct;65(19):2964-78
PMID: 18535784