Immune response after pig-to-human kidney xenotransplantation: a multimodal phenotyping study.


Journal

Lancet (London, England)
ISSN: 1474-547X
Titre abrégé: Lancet
Pays: England
ID NLM: 2985213R

Informations de publication

Date de publication:
30 09 2023
Historique:
received: 30 05 2023
revised: 16 06 2023
accepted: 26 06 2023
medline: 2 10 2023
pubmed: 21 8 2023
entrez: 20 8 2023
Statut: ppublish

Résumé

Cross-species immunological incompatibilities have hampered pig-to-human xenotransplantation, but porcine genome engineering recently enabled the first successful experiments. However, little is known about the immune response after the transplantation of pig kidneys to human recipients. We aimed to precisely characterise the early immune responses to the xenotransplantation using a multimodal deep phenotyping approach. We did a complete phenotyping of two pig kidney xenografts transplanted to decedent humans. We used a multimodal strategy combining morphological evaluation, immunophenotyping (IgM, IgG, C4d, CD68, CD15, NKp46, CD3, CD20, and von Willebrand factor), gene expression profiling, and whole-transcriptome digital spatial profiling and cell deconvolution. Xenografts before implantation, wild-type pig kidney autografts, as well as wild-type, non-transplanted pig kidneys with and without ischaemia-reperfusion were used as controls. The data collected from xenografts suggested early signs of antibody-mediated rejection, characterised by microvascular inflammation with immune deposits, endothelial cell activation, and positive xenoreactive crossmatches. Capillary inflammation was mainly composed of intravascular CD68 Despite favourable short-term outcomes and absence of hyperacute injuries, our findings suggest that antibody-mediated rejection in pig-to-human kidney xenografts might be occurring. Our results suggest specific therapeutic targets towards the humoral arm of rejection to improve xenotransplantation results. OrganX and MSD Avenir.

Sections du résumé

BACKGROUND
Cross-species immunological incompatibilities have hampered pig-to-human xenotransplantation, but porcine genome engineering recently enabled the first successful experiments. However, little is known about the immune response after the transplantation of pig kidneys to human recipients. We aimed to precisely characterise the early immune responses to the xenotransplantation using a multimodal deep phenotyping approach.
METHODS
We did a complete phenotyping of two pig kidney xenografts transplanted to decedent humans. We used a multimodal strategy combining morphological evaluation, immunophenotyping (IgM, IgG, C4d, CD68, CD15, NKp46, CD3, CD20, and von Willebrand factor), gene expression profiling, and whole-transcriptome digital spatial profiling and cell deconvolution. Xenografts before implantation, wild-type pig kidney autografts, as well as wild-type, non-transplanted pig kidneys with and without ischaemia-reperfusion were used as controls.
FINDINGS
The data collected from xenografts suggested early signs of antibody-mediated rejection, characterised by microvascular inflammation with immune deposits, endothelial cell activation, and positive xenoreactive crossmatches. Capillary inflammation was mainly composed of intravascular CD68
INTERPRETATION
Despite favourable short-term outcomes and absence of hyperacute injuries, our findings suggest that antibody-mediated rejection in pig-to-human kidney xenografts might be occurring. Our results suggest specific therapeutic targets towards the humoral arm of rejection to improve xenotransplantation results.
FUNDING
OrganX and MSD Avenir.

Identifiants

pubmed: 37598688
pii: S0140-6736(23)01349-1
doi: 10.1016/S0140-6736(23)01349-1
pii:
doi:

Substances chimiques

Antibodies 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1158-1169

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2023 Elsevier Ltd. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests AD and DA are employees of Revivicor. All other authors declare no competing interests.

Auteurs

Alexandre Loupy (A)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France; Department of Kidney Transplantation, Necker Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France. Electronic address: alexandre.loupy@inserm.fr.

Valentin Goutaudier (V)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France; Department of Kidney Transplantation, Necker Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Alessia Giarraputo (A)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France; Cardiovascular Pathology and Pathological Anatomy, Department of Cardiac, Thoracic, Vascular Sciences and Public Health, University of Padua, Padua, Italy.

Fariza Mezine (F)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France.

Erwan Morgand (E)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France.

Blaise Robin (B)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France.

Karen Khalil (K)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Pharmacy, NYU Langone Health, New York, NY, USA.

Sapna Mehta (S)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Medicine, NYU Grossman School of Medicine, New York, NY, USA.

Brendan Keating (B)

Division of Transplantation, Department of Surgery, Perelman School of Medicine, The University of Pennsylvania, Philadelphia, PA, USA.

Amy Dandro (A)

Revivicor, Blacksburg, VA, USA.

Anaïs Certain (A)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France.

Pierre-Louis Tharaux (PL)

Paris Cardiovascular Research Center, PARCC, INSERM U970, Université Paris Cité, Paris, France.

Navneet Narula (N)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Pathology, NYU Grossman School of Medicine, New York, NY, USA.

Renaud Tissier (R)

Ecole Nationale Vétérinaire d'Alfort, IMRB, After ROSC Network, Maisons-Alfort, France.

Sébastien Giraud (S)

INSERM U1313, IRMETIST, Université de Poitiers et CHU de Poitiers, Poitiers, France.

Thierry Hauet (T)

INSERM U1313, IRMETIST, Université de Poitiers et CHU de Poitiers, Poitiers, France.

Harvey I Pass (HI)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Cardiothoracic Surgery, NYU Grossman School of Medicine, New York, NY, USA; Department of Surgery, NYU Grossman School of Medicine, New York, NY, USA.

Aurélie Sannier (A)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France; Department of Pathology, Bichat Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Ming Wu (M)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Pathology, NYU Grossman School of Medicine, New York, NY, USA.

Adam Griesemer (A)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Surgery, NYU Grossman School of Medicine, New York, NY, USA.

David Ayares (D)

Revivicor, Blacksburg, VA, USA.

Vasishta Tatapudi (V)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Medicine, NYU Grossman School of Medicine, New York, NY, USA.

Jeffrey Stern (J)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Surgery, NYU Grossman School of Medicine, New York, NY, USA.

Carmen Lefaucheur (C)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France; Kidney Transplant Department, Saint-Louis Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Patrick Bruneval (P)

Université Paris Cité, INSERM U970 PARCC, Paris Institute for Transplantation and Organ Regeneration, Paris, France; Department of Pathology, Georges Pompidou European Hospital, Assistance Publique - Hôpitaux de Paris, Paris, France.

Massimo Mangiola (M)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Pathology, NYU Grossman School of Medicine, New York, NY, USA.

Robert A Montgomery (RA)

NYU Langone Transplant Institute, NYU Langone Health, New York, NY, USA; Department of Surgery, NYU Grossman School of Medicine, New York, NY, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH