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PMID: 19258328 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

NLRP3/cryopyrin is necessary for interleukin-1beta (IL-1beta) release in response to hyaluronan, an endogenous trigger of inflammation in response to injury.

The Journal of biological chemistry ·Vol. 284 ·No. 19 ·2009-05-08 ·Pages 12762-71

Yamasaki K, Muto J, Taylor KR, Cogen AL, Audish D, Bertin J, Grant EP, Coyle AJ, Misaghi A, Hoffman HM, Gallo RL

Abstract

Inflammation under sterile conditions is a key event in autoimmunity and following trauma. Hyaluronan, a glycosaminoglycan released from the extracellular matrix after injury, acts as an endogenous signal of trauma and can trigger chemokine release in injured tissue. Here, we investigated whether NLRP3/cryopyrin, a component of the inflammasome, participates in the inflammatory response to injury or the cytokine response to hyaluronan. Mice with a targeted deletion in cryopyrin showed a normal increase in Cxcl2 in response to sterile injuries but had decreased inflammation and release of interleukin-1beta (IL-1beta). Similarly, the addition of hyaluronan to macrophages derived from cryopyrin-deficient mice increased release of Cxcl2 but did not increase IL-1beta release. To define the mechanism of hyaluronan-mediated activation of cryopyrin, elements of the hyaluronan recognition process were studied in detail. IL-1beta release was inhibited in peritoneal macrophages derived from CD44-deficient mice, in an MH-S macrophage cell line treated with antibodies to CD44, or by inhibitors of lysosome function. The requirement for CD44 binding and hyaluronan internalization could be bypassed by intracellular administration of hyaluronan oligosaccharides (10-18-mer) in lipopolysaccharide-primed macrophages. Therefore, the action of CD44 and subsequent hyaluronan catabolism trigger the intracellular cryopyrin --> IL-1beta pathway. These findings support the hypothesis that hyaluronan works through IL-1beta and the cryopyrin system to signal sterile inflammation.

MeSH Terms
Animals Carrier Proteins/physiology Cells, Cultured Enzyme-Linked Immunosorbent Assay Humans Hyaluronan Receptors/physiology Hyaluronic Acid/pharmacology Immunoblotting Inflammation/etiology Interleukin-1beta/metabolism Macrophages, Alveolar/metabolism Macrophages, Peritoneal/metabolism Mice Mice, Inbred C3H Mice, Inbred C57BL Mice, Knockout NLR Family, Pyrin Domain-Containing 3 Protein RNA, Messenger/genetics,metabolism Reverse Transcriptase Polymerase Chain Reaction Skin/drug effects,metabolism Toll-Like Receptor 4/physiology Umbilical Veins
Chemicals
Carrier Proteins Cd44 protein, mouse Hyaluronan Receptors Interleukin-1beta NLR Family, Pyrin Domain-Containing 3 Protein Nlrp3 protein, mouse RNA, Messenger Tlr4 protein, mouse Toll-Like Receptor 4 Hyaluronic Acid
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Yamasaki Kenshi
Division of Dermatology, University of California, and Veterans Affairs San Diego Health Care System, San Diego, CA 92161, USA.
Muto Jun
Taylor Kristen R
Cogen Anna L
Audish David
Bertin John
Grant Ethan P
Coyle Anthony J
Misaghi Amirhossein
Hoffman Hal M
Gallo Richard L
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Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2009-05-08
Epub
2009-00-03
Pages
12762-71
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2676006
Subset
IM
Grants
NHLBI NIH HHS · P01 HL057345 · United States
NHLBI NIH HHS · P01-HL057345 · United States
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