Early Acute Microvascular Kidney Transplant Rejection in the Absence of Anti-HLA Antibodies Is Associated with Preformed IgG Antibodies against Diverse Glomerular Endothelial Cell Antigens.


Journal

Journal of the American Society of Nephrology : JASN
ISSN: 1533-3450
Titre abrégé: J Am Soc Nephrol
Pays: United States
ID NLM: 9013836

Informations de publication

Date de publication:
04 2019
Historique:
received: 25 08 2018
accepted: 31 01 2019
pubmed: 10 3 2019
medline: 19 12 2019
entrez: 10 3 2019
Statut: ppublish

Résumé

Although anti-HLA antibodies (Abs) cause most antibody-mediated rejections of renal allografts, non-anti-HLA Abs have also been postulated to contribute. A better understanding of such Abs in rejection is needed. We conducted a nationwide study to identify kidney transplant recipients without anti-HLA donor-specific Abs who experienced acute graft dysfunction within 3 months after transplantation and showed evidence of microvascular injury, called acute microvascular rejection (AMVR). We developed a crossmatch assay to assess serum reactivity to human microvascular endothelial cells, and used a combination of transcriptomic and proteomic approaches to identify non-HLA Abs. We identified a highly selected cohort of 38 patients with early acute AMVR. Biopsy specimens revealed intense microvascular inflammation and the presence of vasculitis (in 60.5%), interstitial hemorrhages (31.6%), or thrombotic microangiopathy (15.8%). Serum samples collected at the time of transplant showed that previously proposed anti-endothelial cell Abs-angiotensin type 1 receptor (AT1R), endothelin-1 type A and natural polyreactive Abs-did not increase significantly among patients with AMVR compared with a control group of stable kidney transplant recipients. However, 26% of the tested AMVR samples were positive for AT1R Abs when a threshold of 10 IU/ml was used. The crossmatch assay identified a common IgG response that was specifically directed against constitutively expressed antigens of microvascular glomerular cells in patients with AMVR. Transcriptomic and proteomic analyses identified new targets of non-HLA Abs, with little redundancy among individuals. Our findings indicate that preformed IgG Abs targeting non-HLA antigens expressed on glomerular endothelial cells are associated with early AMVR, and that

Sections du résumé

BACKGROUND
Although anti-HLA antibodies (Abs) cause most antibody-mediated rejections of renal allografts, non-anti-HLA Abs have also been postulated to contribute. A better understanding of such Abs in rejection is needed.
METHODS
We conducted a nationwide study to identify kidney transplant recipients without anti-HLA donor-specific Abs who experienced acute graft dysfunction within 3 months after transplantation and showed evidence of microvascular injury, called acute microvascular rejection (AMVR). We developed a crossmatch assay to assess serum reactivity to human microvascular endothelial cells, and used a combination of transcriptomic and proteomic approaches to identify non-HLA Abs.
RESULTS
We identified a highly selected cohort of 38 patients with early acute AMVR. Biopsy specimens revealed intense microvascular inflammation and the presence of vasculitis (in 60.5%), interstitial hemorrhages (31.6%), or thrombotic microangiopathy (15.8%). Serum samples collected at the time of transplant showed that previously proposed anti-endothelial cell Abs-angiotensin type 1 receptor (AT1R), endothelin-1 type A and natural polyreactive Abs-did not increase significantly among patients with AMVR compared with a control group of stable kidney transplant recipients. However, 26% of the tested AMVR samples were positive for AT1R Abs when a threshold of 10 IU/ml was used. The crossmatch assay identified a common IgG response that was specifically directed against constitutively expressed antigens of microvascular glomerular cells in patients with AMVR. Transcriptomic and proteomic analyses identified new targets of non-HLA Abs, with little redundancy among individuals.
CONCLUSIONS
Our findings indicate that preformed IgG Abs targeting non-HLA antigens expressed on glomerular endothelial cells are associated with early AMVR, and that

Identifiants

pubmed: 30850439
pii: ASN.2018080868
doi: 10.1681/ASN.2018080868
pmc: PMC6442343
doi:

Substances chimiques

Endothelin-1 0
Immunoglobulin G 0
Receptor, Angiotensin, Type 1 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

692-709

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI123342
Pays : United States

Informations de copyright

Copyright © 2019 by the American Society of Nephrology.

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Auteurs

Marianne Delville (M)

French National Institute of Health and Medical Research (INSERM) Unit 1163 and.
Department of Biotherapy, Necker Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.
Paris Descartes, Sorbonne Paris Cité University, Paris, France.

Baptiste Lamarthée (B)

Nantes Universtity, Nantes, France.

Sylvain Pagie (S)

Center for Research in Transplantation and Immunology, French National Institute of Health and Medical Research (INSERM) Unité Mixte de Recherche (UMR) 1064, Institut Hospitalo-Universitaire (IHU) Centre Européen des Sciences de la Transplantation et de l'Immunothérapie (CESTI), Laboratoire d'excellence (LabEx) Immunotherapy Graft Oncology (IGO), LabEx Transplantex, Nantes, France.
Nantes Universtity, Nantes, France.

Sarah B See (SB)

Columbia Center for Translational Immunology, Columbia University Medical Center, New York, New York.

Marion Rabant (M)

Paris Descartes, Sorbonne Paris Cité University, Paris, France.
Department of Renal Pathology, Necker Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

Carole Burger (C)

Paris Descartes, Sorbonne Paris Cité University, Paris, France.

Philippe Gatault (P)

Service de Néphrologie-Hypertension, Transplantation et Dialyses, University Hospital, Tours, France.
Equipe d'Accueil EA4245, Transplantation, Immunologie et Inflammation (T2I), University of Tours, Tours, France.

Magali Giral (M)

Nantes University Hospital, Institut de Transplantation-Urologie-Néphrologie (ITUN), Nantes, France.

Olivier Thaunat (O)

Hospices Civils de Lyon, Edouard Herriot Hospital, Department of Transplantation, Nephrology and Clinical Immunology.
INSERM Unit 1111, Lyon, France.
Claude Berna Saint-Etienne University Hospital rd University (Lyon 1), Lyon, France.

Nadia Arzouk (N)

Department of Urology, Nephrology and Kidney transplantation, Pitié Salpétrière Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

Alexandre Hertig (A)

Sorbonne University, Paris, France.
Urgences Néphrologiques et Transplantation Rénale, Assistance Publique-Hôpitaux de Paris (AP-HP), Tenon Hospital, Paris, France.

Marc Hazzan (M)

Department of Nephrology, Lille University Hospital, Lille, France.
Lille University, Lille, France.
French National Institute of Health and Medical Research (INSERM) Unité Mixte de Recherche (UMR) 995, Lille, France.

Marie Matignon (M)

Department of Nephrology and Renal Transplantation, Groupe Hospitalier Henri-Mondor/Albert-Chenevier, Assistance Publique-Hôpitaux de Paris (AP-HP), Créteil, France.
Paris-Est-Créteil University (UPEC), Créteil, France.
Institut Mondor de Recherche Biomédicale (IMRB), Equipe 21, French National Institute of Health and Medical Research (INSERM) Unit 955, Créteil, France.

Christophe Mariat (C)

Department of Nephrology, Dialysis and Renal Transplantation, Saint-Etienne University Hospital, Saint-Etienne, France.
Jean Monnet University, Saint-Etienne, France.

Sophie Caillard (S)

Department of Nephrology and Transplantation, Strasbourg, France.
French National Institute of Health and Medical Research (INSERM) Unité Mixte de Recherche (UMR) S1109, Fédération de Médecine Translationnelle de Strasbourg, Strasbourg, France.

Nassim Kamar (N)

Department of Nephrology and Organ Transplantation, Rangueil University Hospital, Toulouse, France.
French National Institute of Health and Medical Research (INSERM) Unit 1043, Institut Fédératif de Recherche Biomédicale de Toulouse (IFR-BMT), Paul Sabatier University, Toulouse, France.

Johnny Sayegh (J)

Angers University, Angers, France.
Department of Nephrology, Dialysis and Kidney Transplantation, Angers University Hospital, Angers, France.

Pierre-François Westeel (PF)

Department of Nephrology, Dialysis and Transplantation, University Hospital, Amiens, France.

Cyril Garrouste (C)

Department of Nephrology, Clermont-Ferrand University Hospital, Clermont-Ferrand, France.

Marc Ladrière (M)

Department of Nephrology and Kidney Transplantation, Nancy University Hospital, Nancy, France.

Vincent Vuiblet (V)

Department of Nephrology and Renal Transplantation, Reims University Hospital, Reims, France.

Joseph Rivalan (J)

Department of Nephrology, Pontchaillou University Hospital, Rennes, France.

Pierre Merville (P)

Department of Nephrology, Transplantation, Dialysis and Apheresis, Pellegrin University Hospital, Bordeaux, France.
Centre National de la Recherche Scientifique-Unité Mixte de Recherche (CNRS-UMR) 5164 Immuno ConcEpT, , Bordeaux, France.
Bordeaux University, Bordeaux, France.

Dominique Bertrand (D)

Nephrology, Dialysis and Kidney Transplantation, Rouen University Hospital, Rouen, France.

Alain Le Moine (A)

Erasme Hospital, Nephrology Dialysis and Transplantation Department, Bruxelles, Belgium.
Université Libre de Bruxelles, Brussels, Belgium.

Jean-Paul Duong Van Huyen (JP)

Paris Descartes, Sorbonne Paris Cité University, Paris, France.
Department of Renal Pathology, Necker Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

Anne Cesbron (A)

HLA Laboratory, Etablissement Français du Sang (EFS) Centre Pays de la Loire, Nantes, France.

Nicolas Cagnard (N)

Paris Descartes, Sorbonne Paris Cité University, Paris, France.
Bioinformatics, Structure Fédérative de Recherche Necker, French National Institute of Health and Medical Research (INSERM) US24/ Centre National de la Recherche Scientifique (CNRS) UMS3633, Paris, France.

Olivier Alibeu (O)

Paris Descartes, Sorbonne Paris Cité University, Paris, France.
Genomics Core Facility, Institut Imagine-Structure Fédérative de Recherche Necker, French National Institute of Health and Medical Research (INSERM) Unit 1163 and INSERM US24/ Centre National de la Recherche Scientifique (CNRS) UMS3633, Paris, France.

Simon C Satchell (SC)

Bristol Renal, Bristol Heart Institute, Translational Health Sciences, Bristol Medical School, University of Bristol, Great Britain.

Christophe Legendre (C)

Paris Descartes, Sorbonne Paris Cité University, Paris, France.
Necker-Enfants Malades Institute, French National Institute of Health and Medical Research (INSERM) Unit 1151, Paris, France.
Department of Nephrology and Kidney Transplantation, RTRS Centaure; LabEx Transplantex, Necker Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

Emmanuel Zorn (E)

Columbia Center for Translational Immunology, Columbia University Medical Center, New York, New York.

Jean-Luc Taupin (JL)

Immunology and Histocompatibility Laboratory, Saint-Louis Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.
French National Institute of Health and Medical Research (INSERM) Unit 1160, LabEx Transplantex, Paris France; and.
University Paris Diderot, Paris, France.

Béatrice Charreau (B)

Center for Research in Transplantation and Immunology, French National Institute of Health and Medical Research (INSERM) Unité Mixte de Recherche (UMR) 1064, Institut Hospitalo-Universitaire (IHU) Centre Européen des Sciences de la Transplantation et de l'Immunothérapie (CESTI), Laboratoire d'excellence (LabEx) Immunotherapy Graft Oncology (IGO), LabEx Transplantex, Nantes, France.
Nantes Universtity, Nantes, France.

Dany Anglicheau (D)

Paris Descartes, Sorbonne Paris Cité University, Paris, France; dany.anglicheau@aphp.fr.
Necker-Enfants Malades Institute, French National Institute of Health and Medical Research (INSERM) Unit 1151, Paris, France.
Department of Nephrology and Kidney Transplantation, RTRS Centaure; LabEx Transplantex, Necker Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France.

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