Transforming Growth Factor-β1 (TGF-β1)-stimulated Fibroblast to Myofibroblast Differentiation Is Mediated by Hyaluronan (HA)-facilitated Epidermal Growth Factor Receptor (EGFR) and CD44 Co-localization in Lipid Rafts

Fibroblast to myofibroblast differentiation drives effective wound healing and is largely regulated by the cytokine transforming growth factor-β1 (TGF-β1). Myofibroblasts express α-smooth muscle actin and are present in granulation tissue, where they are responsible for wound contraction. Our previo...

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Published inThe Journal of biological chemistry Vol. 288; no. 21; pp. 14824 - 14838
Main Authors Midgley, Adam C., Rogers, Mathew, Hallett, Maurice B., Clayton, Aled, Bowen, Timothy, Phillips, Aled O., Steadman, Robert
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 24.05.2013
American Society for Biochemistry and Molecular Biology
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Abstract Fibroblast to myofibroblast differentiation drives effective wound healing and is largely regulated by the cytokine transforming growth factor-β1 (TGF-β1). Myofibroblasts express α-smooth muscle actin and are present in granulation tissue, where they are responsible for wound contraction. Our previous studies show that fibroblast differentiation in response to TGF-β1 is dependent on and mediated by the linear polysaccharide hyaluronan (HA). Both the HA receptor, CD44, and the epidermal growth factor receptor (EGFR) are involved in this differentiation response. The aim of this study was to understand the mechanisms linking HA-, CD44-, and EGFR-regulated TGF-β1-dependent differentiation. CD44 and EGFR co-localization within membrane-bound lipid rafts was necessary for differentiation, and this triggered downstream mitogen-activated protein kinase (MAPK/ERK) and Ca2+/calmodulin kinase II (CaMKII) activation. We also found that ERK phosphorylation was upstream of CaMKII phosphorylation, that ERK activation was necessary for CaMKII signaling, and that both kinases were essential for differentiation. In addition, HA synthase-2 (HAS2) siRNA attenuated both ERK and CaMKII signaling and sequestration of CD44 into lipid rafts, preventing differentiation. In summary, the data suggest that HAS2-dependent production of HA facilitates TGF-β1-dependent fibroblast differentiation through promoting CD44 interaction with EGFR held within membrane-bound lipid rafts. This induces MAPK/ERK, followed by CaMKII activation, leading to differentiation. This pathway is synergistic with the classical TGF-β1-dependent SMAD-signaling pathway and may provide a novel opportunity for intervention in wound healing. Background: Wound healing and scarring are driven by transforming growth factor-β1 (TGF-β1)-dependent fibroblast to myofibroblast differentiation. Results: Cell surface CD44 and epidermal growth factor receptor (EGFR) co-localize in lipid rafts to signal through mitogen-activated protein kinase 1/2 (ERK1/2) and Ca2+/calmodulin kinase II (CaMKII). Conclusion: CD44 moves into lipid rafts in a TGF-β1- and hyaluronan-dependent manner, co-localizes with EGFR, and triggers differentiation. Significance: This pathway presents novel targets for the therapy of wound-healing and fibrosis.
AbstractList Background: Wound healing and scarring are driven by transforming growth factor-β1 (TGF-β1)-dependent fibroblast to myofibroblast differentiation. Results: Cell surface CD44 and epidermal growth factor receptor (EGFR) co-localize in lipid rafts to signal through mitogen-activated protein kinase 1/2 (ERK1/2) and Ca 2+ /calmodulin kinase II (CaMKII). Conclusion: CD44 moves into lipid rafts in a TGF-β1- and hyaluronan-dependent manner, co-localizes with EGFR, and triggers differentiation. Significance: This pathway presents novel targets for the therapy of wound-healing and fibrosis. Fibroblast to myofibroblast differentiation drives effective wound healing and is largely regulated by the cytokine transforming growth factor-β1 (TGF-β1). Myofibroblasts express α-smooth muscle actin and are present in granulation tissue, where they are responsible for wound contraction. Our previous studies show that fibroblast differentiation in response to TGF-β1 is dependent on and mediated by the linear polysaccharide hyaluronan (HA). Both the HA receptor, CD44, and the epidermal growth factor receptor (EGFR) are involved in this differentiation response. The aim of this study was to understand the mechanisms linking HA-, CD44-, and EGFR-regulated TGF-β1-dependent differentiation. CD44 and EGFR co-localization within membrane-bound lipid rafts was necessary for differentiation, and this triggered downstream mitogen-activated protein kinase (MAPK/ERK) and Ca 2+ /calmodulin kinase II (CaMKII) activation. We also found that ERK phosphorylation was upstream of CaMKII phosphorylation, that ERK activation was necessary for CaMKII signaling, and that both kinases were essential for differentiation. In addition, HA synthase-2 (HAS2) siRNA attenuated both ERK and CaMKII signaling and sequestration of CD44 into lipid rafts, preventing differentiation. In summary, the data suggest that HAS2-dependent production of HA facilitates TGF-β1-dependent fibroblast differentiation through promoting CD44 interaction with EGFR held within membrane-bound lipid rafts. This induces MAPK/ERK, followed by CaMKII activation, leading to differentiation. This pathway is synergistic with the classical TGF-β1-dependent SMAD-signaling pathway and may provide a novel opportunity for intervention in wound healing.
Fibroblast to myofibroblast differentiation drives effective wound healing and is largely regulated by the cytokine transforming growth factor-β1 (TGF-β1). Myofibroblasts express α-smooth muscle actin and are present in granulation tissue, where they are responsible for wound contraction. Our previous studies show that fibroblast differentiation in response to TGF-β1 is dependent on and mediated by the linear polysaccharide hyaluronan (HA). Both the HA receptor, CD44, and the epidermal growth factor receptor (EGFR) are involved in this differentiation response. The aim of this study was to understand the mechanisms linking HA-, CD44-, and EGFR-regulated TGF-β1-dependent differentiation. CD44 and EGFR co-localization within membrane-bound lipid rafts was necessary for differentiation, and this triggered downstream mitogen-activated protein kinase (MAPK/ERK) and Ca2+/calmodulin kinase II (CaMKII) activation. We also found that ERK phosphorylation was upstream of CaMKII phosphorylation, that ERK activation was necessary for CaMKII signaling, and that both kinases were essential for differentiation. In addition, HA synthase-2 (HAS2) siRNA attenuated both ERK and CaMKII signaling and sequestration of CD44 into lipid rafts, preventing differentiation. In summary, the data suggest that HAS2-dependent production of HA facilitates TGF-β1-dependent fibroblast differentiation through promoting CD44 interaction with EGFR held within membrane-bound lipid rafts. This induces MAPK/ERK, followed by CaMKII activation, leading to differentiation. This pathway is synergistic with the classical TGF-β1-dependent SMAD-signaling pathway and may provide a novel opportunity for intervention in wound healing. Background: Wound healing and scarring are driven by transforming growth factor-β1 (TGF-β1)-dependent fibroblast to myofibroblast differentiation. Results: Cell surface CD44 and epidermal growth factor receptor (EGFR) co-localize in lipid rafts to signal through mitogen-activated protein kinase 1/2 (ERK1/2) and Ca2+/calmodulin kinase II (CaMKII). Conclusion: CD44 moves into lipid rafts in a TGF-β1- and hyaluronan-dependent manner, co-localizes with EGFR, and triggers differentiation. Significance: This pathway presents novel targets for the therapy of wound-healing and fibrosis.
Fibroblast to myofibroblast differentiation drives effective wound healing and is largely regulated by the cytokine transforming growth factor-β1 (TGF-β1). Myofibroblasts express α-smooth muscle actin and are present in granulation tissue, where they are responsible for wound contraction. Our previous studies show that fibroblast differentiation in response to TGF-β1 is dependent on and mediated by the linear polysaccharide hyaluronan (HA). Both the HA receptor, CD44, and the epidermal growth factor receptor (EGFR) are involved in this differentiation response. The aim of this study was to understand the mechanisms linking HA-, CD44-, and EGFR-regulated TGF-β1-dependent differentiation. CD44 and EGFR co-localization within membrane-bound lipid rafts was necessary for differentiation, and this triggered downstream mitogen-activated protein kinase (MAPK/ERK) and Ca(2+)/calmodulin kinase II (CaMKII) activation. We also found that ERK phosphorylation was upstream of CaMKII phosphorylation, that ERK activation was necessary for CaMKII signaling, and that both kinases were essential for differentiation. In addition, HA synthase-2 (HAS2) siRNA attenuated both ERK and CaMKII signaling and sequestration of CD44 into lipid rafts, preventing differentiation. In summary, the data suggest that HAS2-dependent production of HA facilitates TGF-β1-dependent fibroblast differentiation through promoting CD44 interaction with EGFR held within membrane-bound lipid rafts. This induces MAPK/ERK, followed by CaMKII activation, leading to differentiation. This pathway is synergistic with the classical TGF-β1-dependent SMAD-signaling pathway and may provide a novel opportunity for intervention in wound healing.
Author Midgley, Adam C.
Rogers, Mathew
Hallett, Maurice B.
Clayton, Aled
Bowen, Timothy
Steadman, Robert
Phillips, Aled O.
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  surname: Midgley
  fullname: Midgley, Adam C.
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  givenname: Mathew
  surname: Rogers
  fullname: Rogers, Mathew
  organization: From the Institute of Nephrology and
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  givenname: Maurice B.
  surname: Hallett
  fullname: Hallett, Maurice B.
  organization: Neutrophil Signalling Group, Institute of Molecular and Experimental Medicine, School of Medicine and Cardiff Institute of Tissue Engineering and Repair, University of Cardiff, Heath Park, Cardiff CF14 4XN, United Kingdom and
– sequence: 4
  givenname: Aled
  surname: Clayton
  fullname: Clayton, Aled
  organization: the Institute of Cancer and Genetics, School of Medicine, Cardiff University, Velindre Cancer Centre, Whitchurch, Cardiff CF14 2TL, United Kingdom
– sequence: 5
  givenname: Timothy
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  fullname: Bowen, Timothy
  organization: From the Institute of Nephrology and
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  fullname: Phillips, Aled O.
  organization: From the Institute of Nephrology and
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  surname: Steadman
  fullname: Steadman, Robert
  email: steadmanr@cf.ac.uk
  organization: From the Institute of Nephrology and
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23589287$$D View this record in MEDLINE/PubMed
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Copyright 2013 © 2013 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.
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DocumentTitleAlternate EGFR and CD44 in Lipid Rafts Induce Myofibroblast Differentiation
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Issue 21
Keywords Lipid Raft
Hyaluronate
Epidermal Growth Factor Receptor (EGFR)
Myofibroblast
CD44
Language English
License This is an open access article under the CC BY license.
http://creativecommons.org/licenses/by/4.0
https://www.elsevier.com/tdm/userlicense/1.0
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Both authors contributed equally to this work.
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Snippet Fibroblast to myofibroblast differentiation drives effective wound healing and is largely regulated by the cytokine transforming growth factor-β1 (TGF-β1)....
Background: Wound healing and scarring are driven by transforming growth factor-β1 (TGF-β1)-dependent fibroblast to myofibroblast differentiation. Results:...
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SubjectTerms Calcium-Calmodulin-Dependent Protein Kinase Type 2 - genetics
Calcium-Calmodulin-Dependent Protein Kinase Type 2 - metabolism
CD44
Cell Differentiation - physiology
Cell Line, Transformed
Enzyme Activation - physiology
Epidermal Growth Factor Receptor (EGFR)
ErbB Receptors - genetics
ErbB Receptors - metabolism
Extracellular Signal-Regulated MAP Kinases - genetics
Extracellular Signal-Regulated MAP Kinases - metabolism
Glucuronosyltransferase - genetics
Glucuronosyltransferase - metabolism
Glycobiology and Extracellular Matrices
Humans
Hyaluronan Receptors - genetics
Hyaluronan Receptors - metabolism
Hyaluronan Synthases
Hyaluronate
Hyaluronic Acid - genetics
Hyaluronic Acid - metabolism
Lipid Raft
Membrane Microdomains - genetics
Membrane Microdomains - metabolism
Myofibroblast
Myofibroblasts - cytology
Myofibroblasts - metabolism
Signal Transduction - physiology
Smad Proteins - genetics
Smad Proteins - metabolism
Transforming Growth Factor beta1 - genetics
Transforming Growth Factor beta1 - metabolism
Wound Healing - physiology
Title Transforming Growth Factor-β1 (TGF-β1)-stimulated Fibroblast to Myofibroblast Differentiation Is Mediated by Hyaluronan (HA)-facilitated Epidermal Growth Factor Receptor (EGFR) and CD44 Co-localization in Lipid Rafts
URI https://dx.doi.org/10.1074/jbc.M113.451336
https://www.ncbi.nlm.nih.gov/pubmed/23589287
https://search.proquest.com/docview/1356392015
https://pubmed.ncbi.nlm.nih.gov/PMC3663506
Volume 288
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