Trauma hemorrhagic shock-induced lung injury involves a gut-lymph-induced TLR4 pathway in mice
Open accessAbstract
BACKGROUND: Injurious non-microbial factors released from the stressed gut during shocked states contribute to the development of acute lung injury (ALI) and multiple organ dysfunction syndrome (MODS). Since Toll-like receptors (TLR) act as sensors of tissue injury as well as microbial invasion and TLR4 signaling occurs in both sepsis and noninfectious models of ischemia/reperfusion (I/R) injury, we hypothesized that factors in the intestinal mesenteric lymph after trauma hemorrhagic shock (T/HS) mediate gut-induced lung injury via TLR4 activation. METHODS/PRINCIPAL FINDINGS: The concept that factors in T/HS lymph exiting the gut recreates ALI is evidenced by our findings that the infusion of porcine lymph, collected from animals subjected to global T/HS injury, into naïve wildtype (WT) mice induced lung injury. Using C3H/HeJ mice that harbor a TLR4 mutation, we found that TLR4 activation was necessary for the development of T/HS porcine lymph-induced lung injury as determined by Evan's blue dye (EBD) lung permeability and myeloperoxidase (MPO) levels as well as the induction of the injurious pulmonary iNOS response. TRIF and Myd88 deficiency fully and partially attenuated T/HS lymph-induced increases in lung permeability respectively. Additional studies in TLR2 deficient mice showed that TLR2 activation was not involved in the pathology of T/HS lymph-induced lung injury. Lastly, the lymph samples were devoid of bacteria, endotoxin and bacterial DNA and passage of lymph through an endotoxin removal column did not abrogate the ability of T/HS lymph to cause lung injury in naïve mice. CONCLUSIONS/SIGNIFICANCE: Our findings suggest that non-microbial factors in the intestinal mesenteric lymph after T/HS are capable of recreating T/HS-induced lung injury via TLR4 activation.
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The toxicity of mesenteric lymph does not depend on the presence of endotoxin or of detectable bacteria, suggesting that other bacterial or tissue injury factors are important mediators of injury.
“the toxicity of this lymph does not depend on the presence of endotoxin or of detectable bacteria,104 which suggests that other bacterial or tissue injury factors are important mediators of injury.”
From The microbiome and critical illness (2016) · cites this paper as [104]
Harvested mesenteric lymph of critically ill animals can provoke lung injury in otherwise healthy animals.
“the harvested mesenteric lymph of critically ill animals can provoke lung injury in otherwise healthy animals.”
From The microbiome and critical illness (2016) · cites this paper as [104]
Substantial clinical and experimental evidence supports the gut-lymph hypothesis.
“Substantial clinical and experimental evidence supports the gut-lymph hypothesis.”
From The microbiome and critical illness (2016) · cites this paper as [104]
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- Authors
- Reino, D. C., Pisarenko, V., Palange, D., Doucet, D., Bonitz, R. P., Lu, Q., Colorado, I., Sheth, S. U., Chandler, B., Kannan, K. B., Ramanathan, M., Xu, D. Z., Deitch, E. A., & Feinman, R.
- Affiliations
- Rutgers New Jersey Medical School (US)
- Corresponding author
- Deitch, Edwin A.
- Feinman, Rena
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-08-04
- Volume
- 6
- Issue
- 8
- Pages
- e14829
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3150139
- OpenAlex
- W1967859572
- Cited by
- 97
- References
- 53
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 2 · 2023: 4 · 2022: 4 · 2020: 8 · 2019: 8 · 2018: 12 · 2017: 8 · 2016: 10 · 2015: 4 · 2014: 10 · 2013: 10 · 2012: 11
- FWCI
- 4.40
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (P50GM069790, T32GM069330, R01GM059841)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Trauma, Hemostasis, Coagulopathy, Resuscitation
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory Support and Mechanisms
- Keywords
- trauma-hemorrhagic shock, acute lung injury, TLR4 signaling, mesenteric lymph, TRIF, MyD88, TLR2, lung permeability, inducible nitric oxide synthase, multiple organ failure
- MeSH terms
- Animals, Base Sequence, Lung, Lymph Nodes, Male, Shock, Hemorrhagic, Swine, Swine, Miniature, Wounds and Injuries, Blotting, Western, Signal Transduction, Polymerase Chain Reaction, DNA Primers, Toll-Like Receptor 4, Mice, Nitric Oxide Synthase Type II, Lung Injury
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