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Endothelial to mesenchymal transition: a precursor to pulmonary arterial remodelling in patients with idiopathic pulmonary fibrosis

Archana Vijay Gaikwad, Wenying Lu, Surajit Dey, Prem Bhattarai, Greg Haug, Josie Larby, Collin Chia, Jade Jaffar, Glen Westall, Gurpreet Kaur Singhera, Tillie-Louise Hackett, Mathew Suji Eapen, Sukhwinder Singh Sohal
ERJ Open Research 2023; DOI: 10.1183/23120541.00487-2022
Archana Vijay Gaikwad
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
2National Health and Medical Research Council (NHMRC) Centre of Research Excellence (CRE) in Pulmonary Fibrosis, Respiratory Medicine and Sleep Unit, Royal Prince Alfred Hospital, Camperdown, NSW , Australia
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Wenying Lu
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
2National Health and Medical Research Council (NHMRC) Centre of Research Excellence (CRE) in Pulmonary Fibrosis, Respiratory Medicine and Sleep Unit, Royal Prince Alfred Hospital, Camperdown, NSW , Australia
3Launceston Respiratory and Sleep Centre, Launceston, TAS, Australia
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  • ORCID record for Wenying Lu
Surajit Dey
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
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Prem Bhattarai
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
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Greg Haug
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
4Department of Respiratory Medicine, Launceston General Hospital, Launceston, Tasmania, Australia
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Josie Larby
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
4Department of Respiratory Medicine, Launceston General Hospital, Launceston, Tasmania, Australia
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Collin Chia
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
3Launceston Respiratory and Sleep Centre, Launceston, TAS, Australia
4Department of Respiratory Medicine, Launceston General Hospital, Launceston, Tasmania, Australia
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Jade Jaffar
5Department of Allergy, Immunology and Respiratory Medicine, The Alfred Hospital, Melbourne, Australia
6Department of Immunology and Pathology, Monash University, Melbourne, Australia
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Glen Westall
5Department of Allergy, Immunology and Respiratory Medicine, The Alfred Hospital, Melbourne, Australia
6Department of Immunology and Pathology, Monash University, Melbourne, Australia
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Gurpreet Kaur Singhera
7Department of Anaesthesiology, Pharmacology and Therapeutics, University of British Columbia, Vancouver, BC, Canada
8Centre for Heart Lung Innovation, St. Paul's Hospital, Vancouver, BC, Canada
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Tillie-Louise Hackett
7Department of Anaesthesiology, Pharmacology and Therapeutics, University of British Columbia, Vancouver, BC, Canada
8Centre for Heart Lung Innovation, St. Paul's Hospital, Vancouver, BC, Canada
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Mathew Suji Eapen
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
2National Health and Medical Research Council (NHMRC) Centre of Research Excellence (CRE) in Pulmonary Fibrosis, Respiratory Medicine and Sleep Unit, Royal Prince Alfred Hospital, Camperdown, NSW , Australia
9These authors contributed equally to this work
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Sukhwinder Singh Sohal
1Respiratory Translational Research Group, Department of Laboratory Medicine, School of Health Sciences, College of Health and Medicine, University of Tasmania, Launceston, Tasmania, Australia
3Launceston Respiratory and Sleep Centre, Launceston, TAS, Australia
9These authors contributed equally to this work
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  • For correspondence: sukhwinder.sohal@utas.edu.au
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Abstract

Background We have previously reported arterial remodelling in patients with idiopathic pulmonary fibrosis (IPF) and suggested that endothelial to mesenchymal transition (EndMT) might be central these changes. This study aims to provide evidence for active EndMT in IPF patients.

Methods Lung resections from thirteen patients with IPF and fifteen normal controls (NC) were immunostained for EndMT biomarkers: VE-cadherin, N-cadherin, S100A4 and vimentin. Pulmonary arteries were analysed for EndMT markers by using computer and microscope assisted image analysis software Image ProPlus7.0. All the analysis was done with observer blinded to subject and diagnosis.

Results Increased expression of mesenchymal markers N-cadherin (p<0.0001), vimentin (p<0.0001), and S100A4 (p<0.05), was noted with downregulation of junctional endothelial VE-cadherin (p<0.01) in intimal layer of the arteries from patients with IPF compared to NC. Cadherin switch was observed in IPF patients, showing increase in endothelial N-cadherin and decrease in VE-cadherin (p<0.01). There was also VE-cadherin shift from junctions to cytoplasm (p<0.01), effecting endothelial cell integrity in patients with IPF. In IPF, individual mesenchymal markers vimentin and N-cadherin negatively correlated with diffusing capacity of the lungs for carbon monoxide (r'=-0.63, p=0.03 and r’=-0.66, p= 0.01). Further, N-cadherin positively correlated with arterial thickness (r'=0.58, p=0.03).

Conclusion This is the first study to demonstrate active EndMT in size based classified pulmonary arteries from IPF patients and potential role in driving remodelling changes. The mesenchymal markers had negative impact on the diffusing capacity of the lungs for carbon monoxide. This work also informs early origins of pulmonary hypertension in patients with IPF.

Footnotes

This manuscript has recently been accepted for publication in the ERJ Open Research. It is published here in its accepted form prior to copyediting and typesetting by our production team. After these production processes are complete and the authors have approved the resulting proofs, the article will move to the latest issue of the ERJOR online. Please open or download the PDF to view this article.

Conflict of interest: Sukhwinder Singh Sohal reports personal fees for lectures from Chiesi, travel support from Chiesi and AstraZeneca, and research grant from Boehringer Ingelheim outside the submitted work.

Conflict of interest: All the other authors do not have any conflict of interest to declare.

This is a PDF-only article. Please click on the PDF link above to read it.

  • Received October 3, 2022.
  • Accepted January 26, 2023.
  • Copyright ©The authors 2023
http://creativecommons.org/licenses/by-nc/4.0/

This version is distributed under the terms of the Creative Commons Attribution Non-Commercial Licence 4.0. For commercial reproduction rights and permissions contact permissions{at}ersnet.org

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Endothelial to mesenchymal transition: a precursor to pulmonary arterial remodelling in patients with idiopathic pulmonary fibrosis
Archana Vijay Gaikwad, Wenying Lu, Surajit Dey, Prem Bhattarai, Greg Haug, Josie Larby, Collin Chia, Jade Jaffar, Glen Westall, Gurpreet Kaur Singhera, Tillie-Louise Hackett, Mathew Suji Eapen, Sukhwinder Singh Sohal
ERJ Open Research Jan 2023, 00487-2022; DOI: 10.1183/23120541.00487-2022

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Endothelial to mesenchymal transition: a precursor to pulmonary arterial remodelling in patients with idiopathic pulmonary fibrosis
Archana Vijay Gaikwad, Wenying Lu, Surajit Dey, Prem Bhattarai, Greg Haug, Josie Larby, Collin Chia, Jade Jaffar, Glen Westall, Gurpreet Kaur Singhera, Tillie-Louise Hackett, Mathew Suji Eapen, Sukhwinder Singh Sohal
ERJ Open Research Jan 2023, 00487-2022; DOI: 10.1183/23120541.00487-2022
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