The mitigating effect of exogenous carbon monoxide on chronic allograft rejection and fibrosis post-lung transplantation.


Journal

The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation
ISSN: 1557-3117
Titre abrégé: J Heart Lung Transplant
Pays: United States
ID NLM: 9102703

Informations de publication

Date de publication:
03 2023
Historique:
received: 04 02 2022
revised: 22 10 2022
accepted: 15 11 2022
pubmed: 16 12 2022
medline: 25 2 2023
entrez: 15 12 2022
Statut: ppublish

Résumé

Small airway inflammation and fibrosis or bronchiolitis obliterans (BO) is the predominant presentation of chronic lung allograft dysfunction (CLAD) post-lung transplantation. Carbon monoxide (CO) is a critical endogenous signaling transducer with known anti-inflammatory and anti-fibrotic effects but its therapeutic potential in CLAD remains to be fully elucidated. Here we investigate the effect of inhaled CO in modulating chronic lung allograft rejection pathology in a murine orthotopic lung transplant model of BO (B6D2F1/J→DBA/2J). Additionally, the effects of CO on the activated phenotype of mesenchymal cells isolated from human lung transplant recipients with CLAD were studied. Murine lung allografts treated with CO (250 ppm × 30 minutes twice daily from days 7 to 40 post-transplantation) demonstrated decreased immune cell infiltration, fibrosis, and airway obliteration by flow cytometry, trichrome staining, and morphometric analysis, respectively. Decreased total collagen, with levels comparable to isografts, was noted in CO-treated allografts by quantitative hydroxyproline assay. In vitro, CO (250 ppm × 16h) was effective in reversing the fibrotic phenotype of human CLAD mesenchymal cells with decreased collagen I and β-catenin expression as well as an inhibitory effect on ERK1/2 MAPK, and mTORC1/2 signaling. Sildenafil, a phosphodiesterase 5 inhibitor, partially mimicked the effects of CO on CLAD mesenchymal cells and was partially effective in decreasing collagen deposition in murine allografts, suggesting the contribution of cGMP-dependent and -independent mechanisms in mediating the effect of CO. These results suggest a potential role for CO in alleviating allograft fibrosis and mitigating chronic rejection pathology post-lung transplant.

Sections du résumé

BACKGROUND
Small airway inflammation and fibrosis or bronchiolitis obliterans (BO) is the predominant presentation of chronic lung allograft dysfunction (CLAD) post-lung transplantation. Carbon monoxide (CO) is a critical endogenous signaling transducer with known anti-inflammatory and anti-fibrotic effects but its therapeutic potential in CLAD remains to be fully elucidated.
METHODS
Here we investigate the effect of inhaled CO in modulating chronic lung allograft rejection pathology in a murine orthotopic lung transplant model of BO (B6D2F1/J→DBA/2J). Additionally, the effects of CO on the activated phenotype of mesenchymal cells isolated from human lung transplant recipients with CLAD were studied.
RESULTS
Murine lung allografts treated with CO (250 ppm × 30 minutes twice daily from days 7 to 40 post-transplantation) demonstrated decreased immune cell infiltration, fibrosis, and airway obliteration by flow cytometry, trichrome staining, and morphometric analysis, respectively. Decreased total collagen, with levels comparable to isografts, was noted in CO-treated allografts by quantitative hydroxyproline assay. In vitro, CO (250 ppm × 16h) was effective in reversing the fibrotic phenotype of human CLAD mesenchymal cells with decreased collagen I and β-catenin expression as well as an inhibitory effect on ERK1/2 MAPK, and mTORC1/2 signaling. Sildenafil, a phosphodiesterase 5 inhibitor, partially mimicked the effects of CO on CLAD mesenchymal cells and was partially effective in decreasing collagen deposition in murine allografts, suggesting the contribution of cGMP-dependent and -independent mechanisms in mediating the effect of CO.
CONCLUSION
These results suggest a potential role for CO in alleviating allograft fibrosis and mitigating chronic rejection pathology post-lung transplant.

Identifiants

pubmed: 36522238
pii: S1053-2498(22)02221-5
doi: 10.1016/j.healun.2022.11.005
pii:
doi:

Substances chimiques

Carbon Monoxide 7U1EE4V452
Collagen 9007-34-5

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

317-326

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL150392
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL118017
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL007853
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL094622
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL162171
Pays : United States

Informations de copyright

Copyright © 2022 International Society for Heart and Lung Transplantation. All rights reserved.

Auteurs

Yoshiro Aoki (Y)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Natalie M Walker (NM)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Keizo Misumi (K)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Takeshi Mimura (T)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Ragini Vittal (R)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Aidan P McLinden (AP)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Linda Fitzgerald (L)

Department of Pharmacy Services, University of Michigan Health System, Ann Arbor, Michigan.

Michael P Combs (MP)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Dennis Lyu (D)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan.

John J Osterholzer (JJ)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan; Pulmonary Section, VA Ann Arbor Health System, Ann Arbor, Michigan.

David J Pinsky (DJ)

Cardiology, Department of Internal Medicine, University of Michigan Health System, Ann Arbor, Michigan.

Vibha N Lama (VN)

Divisions of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, Michigan. Electronic address: vlama@umich.edu.

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Classifications MeSH