Respiratory viral infection in lung transplantation induces exosomes that trigger chronic rejection.


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:
04 2020
Historique:
received: 26 04 2019
revised: 25 11 2019
accepted: 29 12 2019
pubmed: 9 2 2020
medline: 18 9 2020
entrez: 9 2 2020
Statut: ppublish

Résumé

Respiratory viral infections can increase the risk of chronic lung allograft dysfunction after lung transplantation, but the mechanisms are unknown. In this study, we determined whether symptomatic respiratory viral infections after lung transplantation induce circulating exosomes that contain lung-associated self-antigens and assessed whether these exosomes activate immune responses to self-antigens. Serum samples were collected from lung transplant recipients with symptomatic lower- and upper-tract respiratory viral infections and from non-symptomatic stable recipients. Exosomes were isolated via ultracentrifugation; purity was determined using sucrose cushion; and presence of lung self-antigens, 20S proteasome, and viral antigens for rhinovirus, coronavirus, and respiratory syncytial virus were determined using immunoblot. Mice were immunized with circulating exosomes from each group and resulting differential immune responses and lung histology were analyzed. Exosomes containing self-antigens, 20S proteasome, and viral antigens were detected at significantly higher levels (p < 0.05) in serum of recipients with symptomatic respiratory viral infections (n = 35) as compared with stable controls (n = 32). Mice immunized with exosomes from recipients with respiratory viral infections developed immune responses to self-antigens, fibrosis, small airway occlusion, and significant cellular infiltration; mice immunized with exosomes from controls did not (p < 0.05). Circulating exosomes isolated from lung transplant recipients diagnosed with respiratory viral infections contained lung self-antigens, viral antigens, and 20S proteasome and elicited immune responses to lung self-antigens that resulted in development of chronic lung allograft dysfunction in immunized mice.

Sections du résumé

BACKGROUND
Respiratory viral infections can increase the risk of chronic lung allograft dysfunction after lung transplantation, but the mechanisms are unknown. In this study, we determined whether symptomatic respiratory viral infections after lung transplantation induce circulating exosomes that contain lung-associated self-antigens and assessed whether these exosomes activate immune responses to self-antigens.
METHODS
Serum samples were collected from lung transplant recipients with symptomatic lower- and upper-tract respiratory viral infections and from non-symptomatic stable recipients. Exosomes were isolated via ultracentrifugation; purity was determined using sucrose cushion; and presence of lung self-antigens, 20S proteasome, and viral antigens for rhinovirus, coronavirus, and respiratory syncytial virus were determined using immunoblot. Mice were immunized with circulating exosomes from each group and resulting differential immune responses and lung histology were analyzed.
RESULTS
Exosomes containing self-antigens, 20S proteasome, and viral antigens were detected at significantly higher levels (p < 0.05) in serum of recipients with symptomatic respiratory viral infections (n = 35) as compared with stable controls (n = 32). Mice immunized with exosomes from recipients with respiratory viral infections developed immune responses to self-antigens, fibrosis, small airway occlusion, and significant cellular infiltration; mice immunized with exosomes from controls did not (p < 0.05).
CONCLUSIONS
Circulating exosomes isolated from lung transplant recipients diagnosed with respiratory viral infections contained lung self-antigens, viral antigens, and 20S proteasome and elicited immune responses to lung self-antigens that resulted in development of chronic lung allograft dysfunction in immunized mice.

Identifiants

pubmed: 32033844
pii: S1053-2498(20)30012-7
doi: 10.1016/j.healun.2019.12.009
pmc: PMC7102671
mid: NIHMS1550591
pii:
doi:

Substances chimiques

Antigens, Viral 0
Autoantigens 0
HLA Antigens 0
Proteasome Endopeptidase Complex EC 3.4.25.1

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

379-388

Subventions

Organisme : NHLBI NIH HHS
ID : K23 HL143050
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL056643
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL092514
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI123034
Pays : United States

Informations de copyright

Copyright © 2020 International Society for Heart and Lung Transplantation. Published by Elsevier Inc. All rights reserved.

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Auteurs

Muthukumar Gunasekaran (M)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Sandhya Bansal (S)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Ranjithkumar Ravichandran (R)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Monal Sharma (M)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Sudhir Perincheri (S)

Department of Pathology, Yale School of Medicine, New Haven, Connecticut.

Francisco Rodriguez (F)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Ramsey Hachem (R)

Department of Medicine, Washington University School of Medicine, St. Louis, Missouri.

Cynthia E Fisher (CE)

Division of Allergy and Infectious Diseases, University of Washington, Seattle, Washington.

Ajit P Limaye (AP)

Division of Allergy and Infectious Diseases, University of Washington, Seattle, Washington.

Ashraf Omar (A)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Michael A Smith (MA)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Ross M Bremner (RM)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona.

Thalachallour Mohanakumar (T)

St. Joseph's Hospital and Medical Center, Norton Thoracic Institute, Phoenix, Arizona. Electronic address: tm.kumar@dignityhealth.org.

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Classifications MeSH