Constitutive Expression of Inter-α-inhibitor (IαI) Family Proteins and Tumor Necrosis Factor-stimulated Gene-6 (TSG-6) by Human Amniotic Membrane Epithelial and Stromal Cells Supporting Formation of the Heavy Chain-Hyaluronan (HC-HA) Complex

Zhang, Suzhen; He, Hua; Day, Anthony J.; Tseng, Scheffer C.G.

doi:10.1074/jbc.m112.342873

Cited by 60 publications

(80 citation statements)

References 80 publications

(123 reference statements)

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“…HC1 and PTX3, but Not HC2, Bikunin, and TSG-6, Are Present in HC-HA-We previously reported that HC-HA purified from human AM contains HC1 but not HC2 of I␣I (42). To further confirm this, HC-HA purified through two sequential runs of ultracentrifugation in CsCl, 4 M guanidine HCl was subjected to a mild NaOH (0.05 N) treatment to cleave the ester bond between HC and HA (47) or digestion with HAase to release HC.…”

Section: Resultsmentioning

confidence: 88%

“…This finding suggests that SHAP-HA has an inhibitory role in the development of airway hyper-responsiveness and allergic airway inflammation (66). Although both SHAP-HA and HC-HA purified from human AM are similar complexes, characterized by high molecular mass HA covalently linked to HC (42,43,64), there are important differences. In adult cells, SHAP-HA contains both HC1 and HC2 from serum I␣I (derived from the liver) (64).…”

Section: Discussionmentioning

confidence: 99%

“…Recently, we have purified HC-HA complex (HC-HA) from soluble AM extract. This complex, formed by a covalent linkage between hyaluronan (HA) and heavy chain 1 (HC1) of inter-␣-trypsin inhibitor (I␣I) via TSG-6 catalytic action (42), has been shown to be effective in promoting apoptosis of LPS-activated macrophages, inhibiting TGF-␤1 promoter activity in corneal stromal fibroblasts (43), and suppressing endothelial tube formation (44). Herein, we further demonstrate that HC-HA is indeed responsible for the anti-inflammatory effect of AM by promoting apoptosis of activated but not resting neutrophils and macrophages and by polarizing the M2 phenotype in LPSactivated macrophages for efficient phagocytosis of apoptotic neutrophils.…”

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confidence: 99%

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Immobilized Heavy Chain-Hyaluronic Acid Polarizes Lipopolysaccharide-activated Macrophages toward M2 Phenotype

He¹,

Zhang²,

Tighe³

et al. 2013

Journal of Biological Chemistry

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125

118

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Background: HC-HA is a unique anti-inflammatory matrix different from hyaluronic acid (HA). Results: Soluble HC-HA induces apoptosis of inflammatory neutrophils and macrophages, and immobilized HC-HA promotes M2 polarization upon LPS/TLR ligation while both enhancing macrophage phagocytosis. Conclusion: HC-HA exerts its anti-inflammatory action using multiple mechanisms. Significance: HC-HA is the first known matrix component to polarize M2b.Despite the known anti-inflammatory effect of amniotic membrane, its action mechanism remains largely unknown. HC-HA complex (HC-HA) purified from human amniotic membrane consists of high molecular weight hyaluronic acid (HA) covalently linked to the heavy chain (HC) 1 of inter-␣-trypsin inhibitor. In this study, we show that soluble HC-HA also contained pentraxin 3 and induced the apoptosis of both formyl-Met-Leu-Phe or LPS-activated neutrophils and LPS-activated macrophages while not affecting the resting cells. This enhanced apoptosis was caused by the inhibition of cell adhesion, spreading, and proliferation caused by HC-HA binding of LPS-activated macrophages and preventing adhesion to the plastic surface. Preferentially, soluble HC-HA promoted phagocytosis of apoptotic neutrophils in resting macrophages, whereas immobilized HC-HA promoted phagocytosis in LPSactivated macrophages. Upon concomitant LPS stimulation, immobilized HC-HA but not HA polarized macrophages toward the M2 phenotype by down-regulating IRF5 protein and preventing its nuclear localization and by down-regulating IL-12, TNF-␣, and NO synthase 2. Additionally, IL-10, TGF-␤1, peroxisome proliferator-activated receptor ␥, LIGHT (TNF superfamily 14), and sphingosine kinase-1 were up-regulated, and such M2 polarization was dependent on TLR ligation. Collectively, these data suggest that HC-HA is a unique matrix component different from HA and uses multiple mechanisms to suppress M1 while promoting M2 phenotype. This anti-inflammatory action of HC-HA is highly desirable to promote wound healing in diseases heightened by unsuccessful transition from M1 to M2 phenotypes.Inflammation serves as the first host response to real or perceived threats to tissue homeostasis. It is heralded by the recruitment of neutrophils, which eliminate pathogens and damaged tissues before eventually undergoing apoptosis (1-3). These apoptotic neutrophils are then removed by macrophages via phagocytosis, resulting in the restoration and maintenance of anti-inflammatory and tolerogenic milieu (4). On the contrary, delayed neutrophil apoptosis and/or impaired phagocytic clearance of apoptotic neutrophils by macrophages leads to prolonged inflammation that is the hallmark of a number of diseases (5-8). Hence, facilitation of neutrophil apoptosis and phagocytic clearance of apoptotic neutrophils by macrophages is an important strategy to limit inflammation-mediated tissue damage to restore tissue homeostasis (9 -11).Macrophages undergo phenotypic changes to adapt to the transition from proinflammatory to anti-inflammatory states of wou...

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Section: Resultsmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

Immobilized Heavy Chain-Hyaluronic Acid Polarizes Lipopolysaccharide-activated Macrophages toward M2 Phenotype

He¹,

Zhang²,

Tighe³

et al. 2013

Journal of Biological Chemistry

Self Cite

125

118

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“…I␣I has been described to be necessary for the cumulus formation of the ovary (31) and to play an important role in tissue repair (34,42,43). Moreover, an isoform of I␣I has been reported to be produced by the amniotic membrane, and the hyaluronan-HC (HC⅐HA) complex is present in amniotic fluid, giving evidence of TSG-6 mediated transfer of HCs to hyaluronan in amniotic tissue (32,44). These data suggest that the HCs play a role during embryonic development and may also be important for ES cell maintenance.…”

Section: Discussionmentioning

confidence: 99%

“…Another study by Sanggaard et al suggests that HC2 is necessary for the TSG-6-mediated transfer to take place, possibly explaining both the inability of HC1 alone to induce TEAD family and the need for higher concentrations of HC2 to induce a robust effect on TEAD activity (45). Interestingly, Zhang et al studied the presence of HCs coupled to hyaluronan in amniotic membrane, and found that whereas the amniotic membrane produces HC1, HC2, and HC3, only HC1⅐HA complex was found in physiological amniotic membrane extracts (44), which could account for the anti-inflammatory, anti-scarring, and anti-angiogenic effects that this particular HCŸHA complex yields (46).…”

Section: Discussionmentioning

confidence: 99%

Serum Inter-α-inhibitor Activates the Yes Tyrosine Kinase and YAP/TEAD Transcriptional Complex in Mouse Embryonic Stem Cells

Pijuan-Galito

Tamm

Annerén

2014

Journal of Biological Chemistry

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Background: Serum contributes to embryonic stem (ES) cell maintenance of pluripotency and activates Yes. Results: The serum protein Inter-␣-inhibitor (I␣I) was found to activate the Yes/YAP/TEAD transcription factor pathway and induce expression of Oct3/4 and Nanog in ES cells. Conclusion: I␣I activates key pluripotency pathways. Significance: I␣I may play a significant role in ES cell maintenance and self-renewal.

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Systemic Transplantation of Eyelid Adipose‐Derived Stem Cells for Antifibrotic Treatment

Fang

Chen

Teng

et al. 2020

Advanced Therapeutics

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Fibrosis is a result of the pathological wound‐healing response initiated by immune cells and leads to permanent scarring, such as corneal scarring, which impairs the vision of millions of people worldwide. However, there is currently no available treatment strategy that specifically targets the pathogenesis of fibrosis and can be translated in a safe and versatile way. Herein, it is illustrated that systemic transplantation of easily accessible human eyelid adipose‐derived stem cells (heADSCs) can successfully and safely exert antifibrotic effects in both corneal and skin scarring cases. Intravenous injection of heADSCs alleviates scar formation after rat corneal lamellar injury with accelerated epithelization, increases tumor necrosis factor‐stimulated gene‐6 (TSG‐6) in the epithelium, and decreases inflammatory factors. Cell tracing shows the presence of detectable signals until the 7th day, while no pulmonary embolism or other discomfort occurs. heADSCs effectively reduce corneal scarring by ameliorating stromal inflammation by increasing endogenous tissue‐protective TSG‐6 in the epithelium and macrophage phenotype switching, which is more effective with systemic transplantation than subconjunctival transplantation. Systemic transplantation of heADSCs shows safe antifibrotic effects in both corneal and skin scarring cases and this result identifies systemic transplantation with autologous adipose‐derived stem cells as a generally versatile and safe therapy for antifibrotic treatment.

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Constitutive Expression of Inter-α-inhibitor (IαI) Family Proteins and Tumor Necrosis Factor-stimulated Gene-6 (TSG-6) by Human Amniotic Membrane Epithelial and Stromal Cells Supporting Formation of the Heavy Chain-Hyaluronan (HC-HA) Complex

Cited by 60 publications

References 80 publications

Immobilized Heavy Chain-Hyaluronic Acid Polarizes Lipopolysaccharide-activated Macrophages toward M2 Phenotype

Immobilized Heavy Chain-Hyaluronic Acid Polarizes Lipopolysaccharide-activated Macrophages toward M2 Phenotype

Serum Inter-α-inhibitor Activates the Yes Tyrosine Kinase and YAP/TEAD Transcriptional Complex in Mouse Embryonic Stem Cells

Systemic Transplantation of Eyelid Adipose‐Derived Stem Cells for Antifibrotic Treatment

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