Regulation of lung injury and repair by Toll-like receptors and hyaluronan
Abstract
Mechanisms that regulate inflammation and repair after acute lung injury are incompletely understood. The extracellular matrix glycosaminoglycan hyaluronan is produced after tissue injury and impaired clearance results in unremitting inflammation. Here we report that hyaluronan degradation products require MyD88 and both Toll-like receptor (TLR)4 and TLR2 in vitro and in vivo to initiate inflammatory responses in acute lung injury. Hyaluronan fragments isolated from serum of individuals with acute lung injury stimulated macrophage chemokine production in a TLR4- and TLR2-dependent manner. Myd88(-/-) and Tlr4(-/-)Tlr2(-/-) mice showed impaired transepithelial migration of inflammatory cells but decreased survival and enhanced epithelial cell apoptosis after lung injury. Lung epithelial cell-specific overexpression of high-molecular-mass hyaluronan was protective against acute lung injury. Furthermore, epithelial cell-surface hyaluronan was protective against apoptosis, in part, through TLR-dependent basal activation of NF-kappaB. Hyaluronan-TLR2 and hyaluronan-TLR4 interactions provide signals that initiate inflammatory responses, maintain epithelial cell integrity and promote recovery from acute lung injury.
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Endogenous products such as oxidized phospholipids and matrix breakdown products also drive inflammation through TLR4 and probably other TLRs, providing a mechanism for perpetuating inflammation when microbial products are being cleared from the lungs.
“endogenous products such as oxidized phospholipids and matrix breakdown products also drive inflammation through TLR4 and probably other TLRs, providing a mechanism for perpetuating inflammation when microbial products are being cleared from the lungs (68,72).”
From Into the Eye of the Cytokine Storm (2012) · cites this paper as [72]
There is evidence for a role of TLR2 and/or TLR4 in the induction of cytokine and chemokine production in response to extracellular matrix components, including hyaluronan fragments or soluble proteoglycan components, in vitro and in vivo.
“For example, there is evidence for a role of TLR2 and/or TLR4 in the induction of cytokine and chemokine production in response to extracellular matrix components, including hyaluronan fragments or soluble proteoglycan components, in vitro and in vivo31–34.”
From Sterile inflammation: sensing and reacting to damage (2010) · cites this paper as [31]
Mice deficient in both TLR2 and TLR4 or in MYD88 were protected against bleomycin-induced lung injury related to the generation of hyaluronan fragments.
“Mice deficient in both TLR2 and TLR4 or in myeloid differentiation primary-response protein 88 (MYD88), an adaptor protein for TLR and IL-1R signalling, were protected against bleomycin-induced lung injury related to the generation of hyaluronan fragments, and administration of a hyaluronan-blocking peptide to wild-type mice provided similar, although incomplete, protection31.”
From Sterile inflammation: sensing and reacting to damage (2010) · cites this paper as [31]
Administration of a hyaluronan-blocking peptide to wild-type mice provided similar, although incomplete, protection against bleomycin-induced lung injury.
“Mice deficient in both TLR2 and TLR4 or in myeloid differentiation primary-response protein 88 (MYD88), an adaptor protein for TLR and IL-1R signalling, were protected against bleomycin-induced lung injury related to the generation of hyaluronan fragments, and administration of a hyaluronan-blocking peptide to wild-type mice provided similar, although incomplete, protection31.”
From Sterile inflammation: sensing and reacting to damage (2010) · cites this paper as [31]
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- Authors
- Jiang, D., Liang, J., Fan, J., Yu, S., Chen, S., Luo, Y., Prestwich, G. D., Mascarenhas, M. M., Garg, H. G., Quinn, D. A., Homer, R. J., Goldstein, D. R., Bucala, R., Lee, P. J., Medzhitov, R., & Noble, P. W.
- Affiliations
- Yale University (US)
- University of Utah (US)
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Noble, Paul W
- ORCID
- Venue
- Nature Medicine
- Published
- 2005-10-23
- Volume
- 11
- Issue
- 11
- Pages
- 1173-1179
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W2061626698
- Cited by
- 1,401
- References
- 41
- Citations by year
- 2026: 19 · 2025: 30 · 2024: 45 · 2023: 46 · 2022: 48 · 2021: 72 · 2020: 59 · 2019: 56 · 2018: 73 · 2017: 58 · 2016: 71 · 2015: 80 · 2014: 79 · 2013: 86 · 2012: 109
- FWCI
- 27.05
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Defense
- Yale University
- National Institutes of Health
- National Heart, Lung, and Blood Institute (HL57486)
- National Institute of Allergy and Infectious Diseases (AI52487)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory Support and Mechanisms
- Keywords
- acute lung injury, hyaluronic acid, TLR4, TLR2, MyD88, lung repair, epithelial apoptosis, NF-κB activation, epithelial barrier integrity, inflammation
- MeSH terms
- Animals, Bronchoalveolar Lavage Fluid, Cells, Cultured, Enzyme-Linked Immunosorbent Assay, Epithelial Cells, Hyaluronic Acid, Lung, Mice, Transgenic, Molecular Weight, Wound Healing, Cytokines, Macrophages, Peritoneal, Mice, Knockout, Chemokines, Toll-Like Receptor 2, Toll-Like Receptor 4, Mice, Lung Injury
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