Interaction of CD44 and hyaluronan is the dominant mechanism for neutrophil sequestration in inflamed liver sinusoids

McDonald, Braedon; McAvoy, Erin F.; Lam, Florence; Gill, Varinder; Motte, Carol de la; Savani, Rashmin C.; Kubes, Paul

doi:10.1084/jem.20071765

Cited by 286 publications

(269 citation statements)

References 61 publications

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“…HA⅐HC complexes in synovial fluid of patients with rheumatoid arthritis correlated with the severity of the disease (49), and hepatic accumulation of HA⅐HC complexes was observed in lipopolysaccharide-treated mice suffering liver damage (40). However, low serum concentrations of I␣I in sepsis patients correlated with mortality (54), and more importantly, administration of I␣I reduced mortality in experimental sepsis in rats (59,60), strongly suggesting that I␣I has a protective role in sepsis.…”

Section: Discussionmentioning

confidence: 99%

“…A decrease of I␣I in plasma or serum has been associated with infectious disease and sepsis (32,(53)(54)(55). In lipopolysaccharide-treated mice, a model of sepsis, hepatic accumulation of HA⅐HC complexes has been observed (40), and HA⅐HC complexes have also been found in sera of patients with chronic liver disease associated with hepatitis virus infection (56). It is very likely that the decrease of I␣I concentrations in sepsis and the simultaneous generation of HA⅐HC complexes are related, and TSG-6 may be at least partially responsible for the HC transfer.…”

Section: Discussionmentioning

confidence: 99%

“…HA serves as a primary receptor for T cell extravasation in vivo (37)(38)(39) and for the infiltration of neutrophils in the liver of lipopolysaccharidetreated mice (40), with lymphocyte binding to HA being mediated by the cellular HA receptor CD 44 (38,(41)(42)(43)(44)(45). Therefore, we tested the possibility that modification of surface-bound HA by TSG-6-mediated HC transfer modulates the binding of BW 5147 cells that express fully activated CD 44 and bind readily to both HA in solution and to surface-bound HA (18,35).…”

Section: Discussionmentioning

confidence: 99%

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Transfer of Inter-α-inhibitor Heavy Chains to Hyaluronan by Surface-linked Hyaluronan-TSG-6 Complexes

Colón

Shytuhina

Cowman

et al. 2009

Journal of Biological Chemistry

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Inter-␣-inhibitor, TSG-6, and hyaluronan have important functions in fertility and inflammation. Two subunits of inter-␣-inhibitor, the heavy chains, form covalent bonds with TSG-6 or hyaluronan in vitro. TSG-6-heavy chain complexes serve as intermediates in the transfer of heavy chains from inter-␣-inhibitor to hyaluronan. In vivo, in addition to these complexes, stable ternary complexes of hyaluronan with both TSG-6 and heavy chains have been demonstrated in the ovulatory cumulus oophorus. In our ongoing efforts to characterize the multiple interactions between hyaluronan, TSG-6 and inter-␣-inhibitor, we recently characterized the formation of highly stable complexes of TSG-6 with hyaluronan that had been tethered to a solid surface. Here we show that these hyaluronan-TSG-6 complexes are functionally active and transfer heavy chain subunits from inter-␣-inhibitor to either free or surface-bound hyaluronan. Transitional hyaluronan-TSG-6-heavy chain complexes do not accumulate in vitro. Our data show the capability for heavy chain transfer by both free TSG-6 and preformed hyaluronan-TSG-6 complexes, suggesting that both might contribute to hyaluronan modification in vivo. Transfer of heavy chains to surface-tethered hyaluronan by either free TSG-6 or surface-tethered hyaluronan-TSG-6 complexes did not affect the CD 44-mediated binding of BW 5147 cells in vitro. We show how TSG-6 and hyaluronan together can deplete inter-␣-inhibitor and generate bikunin, as has been observed in sepsis, and discuss the role of TSG-6 in the generation of hyaluronan-heavy chain complexes associated with ovulation, arthritis, and sepsis.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Transfer of Inter-α-inhibitor Heavy Chains to Hyaluronan by Surface-linked Hyaluronan-TSG-6 Complexes

Colón

Shytuhina

Cowman

et al. 2009

Journal of Biological Chemistry

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“…In murine models of lung diseases, it promotes bronchial epithelial repair after naphthalene injury (20), promotes angiogenesis in fibrotic lung injury (21), prevents the development of airway hyperresponsiveness in an ovalbumin-induced asthma model (22), and mediates ozoneinduced airway injury (23). In addition, SHAP accelerates neutrophil adhesion to the hepatic sinusoidal endothelium in response to lipopolysaccharide by increasing the avidity of endothelial HA to cell surface CD44 (24,25). These findings indicate that SHAP plays important roles in the regulation of HA function in various disorders.…”

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confidence: 99%

Serum Level of SHAP as a Disease Marker: A Comparison with Hyaluronan

Zhuo

Kimata

2010

TIGG

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Hyaluronan (HA) has been reported to be associated with the progression of various inflammatory diseases and cancer malignancy. The serum level of HA is a clinical biomarker for rheumatoid arthritis and liver cirrhosis, conditions in which elevated HA levels are due to the enhanced production in the joint synovium and impaired uptake and clearance in the hepatic sinusoidal endothelium, respectively. We have discovered that inflammation is often accompanied by the covalent modification of HA by serumderived HA-associated protein (SHAP), derived from the heavy chains of the plasma protein inter-alpha-trypsin inhibitor, which changes the biological activity of HA and participates in regulation of the inflammatory response. We compared the serum levels of SHAP and HA in a number of diseases. The results indicated that the SHAP level was more closely correlated with disease stages and with the other related biomarkers than was HA. This review summarizes these findings and concludes that SHAP is superior to HA as a disease marker.

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“…One of the mechanisms by which neutrophils are recruited out of the bone marrow and into tissues is through the increased production of CXCL1 and CXCL2 (3,4), which are both induced by the interleukin 23 (IL-23)/IL-17 pathway (5,6). During lipopolysaccharide (LPS)-induced hepatic injury, hyaluronic acid (HA)-CD44 interactions facilitate neutrophil adherence to the endothelium and extravasation into the liver (7). Furthermore, injection of CXCL2 leads to a large influx of neutrophils at the site of injection, which is dependent on HA-CD44 interactions (8).…”

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confidence: 99%

Extracellular Superoxide Dismutase Enhances Recruitment of Immature Neutrophils to the Liver

et al. 2016

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Listeria monocytogenes is a Gram-positive intracellular pathogen that causes spontaneous abortion in pregnant women, as well as septicemia, meningitis, and gastroenteritis, primarily in immunocompromised individuals. Although L. monocytogenes can usually be effectively treated with antibiotics, there is still around a 25% mortality rate with individuals who develop clinical listeriosis. Neutrophils are innate immune cells required for the clearance of pathogenic organisms, including L. monocytogenes. The diverse roles of neutrophils during both infectious and noninfectious inflammation have recently gained much attention. However, the impact of reactive oxygen species, and the enzymes that control their production, on neutrophil recruitment and function is not well understood. Using congenic mice with varying levels of extracellular superoxide dismutase (ecSOD) activity, we have recently shown that the presence of ecSOD decreases clearance of L. monocytogenes while increasing the recruitment of neutrophils that are not protective in the liver. The data presented here show that ecSOD activity does not lead to a cell-intrinsic increase in neutrophil-homing potential or a decrease in protection against L. monocytogenes. Instead, ecSOD activity enhances the production of neutrophil-attracting factors and protects hyaluronic acid (HA) from damage. Furthermore, neutrophils from the livers of ecSOD-expressing mice have decreased intracellular and surface-bound myeloperoxidase, are less capable of killing phagocytosed L. monocytogenes, and have decreased oxidative burst. Collectively, our data reveal that ecSOD activity modulates neutrophil recruitment and function in a cell-extrinsic fashion, highlighting the importance of the enzyme in protecting tissues from oxidative damage. Listeria monocytogenes is a Gram-positive bacterium that can be found in the soil, fruits, vegetables, meats, and dairy products. Ingestion of L. monocytogenes-contaminated foods can cause spontaneous abortions in pregnant women, as well as septicemia, meningitis, and gastroenteritis, primarily in immunocompromised individuals (1). Surprisingly, clinical listeriosis results in an ϳ25% mortality rate despite the use of antibiotics (1), which makes understanding the immune response against the pathogen important. Furthermore, L. monocytogenes is a widely used model pathogen to study and understand host-pathogen interactions due to its ease of use and manipulation.Neutrophils are short-lived immune cells that differentiate in the bone marrow from the common myeloid progenitor (2). Under normal homeostatic conditions, most neutrophils are retained in the bone marrow until inflammation leads to signaling for their egress. One of the mechanisms by which neutrophils are recruited out of the bone marrow and into tissues is through the increased production of CXCL1 and CXCL2 (3, 4), which are both induced by the interleukin 23 (IL-23)/IL-17 pathway (5, 6). During lipopolysaccharide (LPS)-induced hepatic injury, hyaluronic acid (HA)-CD44 interactions faci...

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Interaction of CD44 and hyaluronan is the dominant mechanism for neutrophil sequestration in inflamed liver sinusoids

Cited by 286 publications

References 61 publications

Transfer of Inter-α-inhibitor Heavy Chains to Hyaluronan by Surface-linked Hyaluronan-TSG-6 Complexes

Transfer of Inter-α-inhibitor Heavy Chains to Hyaluronan by Surface-linked Hyaluronan-TSG-6 Complexes

Serum Level of SHAP as a Disease Marker: A Comparison with Hyaluronan

Extracellular Superoxide Dismutase Enhances Recruitment of Immature Neutrophils to the Liver

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