A conserved transcriptional program for MAIT cells across mammalian evolution-Reference-Cited by-同舟云学术

A conserved transcriptional program for MAIT cells across mammalian evolution

Published:2023-12-20 Issue:2 Volume:221 Page:
ISSN:0022-1007
Container-title:Journal of Experimental Medicine
language:en
Short-container-title:

Author:

Bugaut Hélène¹^ORCID,El Morr Yara¹^ORCID,Mestdagh Martin¹^ORCID,Darbois Aurélie¹^ORCID,Paiva Rafael A.¹^ORCID,Salou Marion¹^ORCID,Perrin Laetitia¹^ORCID,Fürstenheim Mariela¹²^ORCID,du Halgouet Anastasia¹^ORCID,Bilonda-Mutala Linda¹^ORCID,Le Gac Anne-Laure¹^ORCID,Arnaud Manon¹^ORCID,El Marjou Ahmed³^ORCID,Guerin Coralie⁴⁵^ORCID,Chaiyasitdhi Atitheb⁶⁷^ORCID,Piquet Julie⁸^ORCID,Smadja David M.⁵⁹^ORCID,Cieslak Agata¹⁰^ORCID,Ryffel Bernhard¹¹^ORCID,Maciulyte Valdone¹²^ORCID,Turner James M.A.¹²^ORCID,Bernardeau Karine¹³^ORCID,Montagutelli Xavier¹⁴^ORCID,Lantz Olivier¹¹⁵¹⁶^ORCID,Legoux François¹¹⁷^ORCID

Affiliation:

1. Institut Curie, Paris Sciences et Lettres University, Institut National de La Santé et de La Recherche Médicale U932, Immunity and Cancer 1 , Paris, France

2. Université Paris Cité 2 , Paris, France

3. Institut Curie 3 Recombinant Protein Facility, , Paris, France

4. CurieCoreTech, Institut Curie 4 Cytometry Platform, , Paris, France

5. Institut National de La Santé et de La Recherche Médicale, Université de Paris 5 Innovative Therapies in Haemostasis, , Paris, France

6. Institut Curie, Paris Sciences et Lettres Research University, Centre national de la recherche scientifique UMR168 6 Laboratoire Physico-Chimie Curie, , Paris, France

7. Sorbonne Université 7 , Paris, France

8. Carpentier Foundation 8 Biosurgical Research Laboratory, , Paris, France

9. Assistance Publique Hôpitaux de Paris-Centre-Université de Paris 9 Hematology Department and Biosurgical Research Lab (Carpentier Foundation), , Paris, France

10. Université de Paris (Descartes), Institut Necker-Enfants Malades, Institut National de La Santé et de La Recherche Médicale U1151, and Laboratory of Onco-Hematology, Assistance Publique-Hôpitaux de Paris, Hôpital Necker-Enfants Malades 10 , Paris, France

11. Université D’Orléans, Centre national de la recherche scientifique UMR7355 11 , Orléans, France

12. The Francis Crick Institute 12 Sex Chromosome Biology Laboratory, , London, UK

13. Nantes Université, Centre hospitalier universitaire de Nantes, Centre national de la recherche scientifique, Institut National de La Santé et de La Recherche Médicale, BioCore, US16, Plateforme P2R, Structure Fédérative de Recherche François Bonamy 13 , Nantes, France

14. Institut Pasteur, Université Paris Cité 14 Mouse Genetics Laboratory, , Paris, France

15. Institut Curie 15 Laboratoire D’immunologie Clinique, , Paris, France

16. Centre D’investigation Clinique en Biothérapie Gustave-Roussy Institut Curie 16 , Paris, France

17. Institut de Génétique et Développement de Rennes, Université de Rennes, Institut National de La Santé et de La Recherche Médicale ERL1305, Centre national de la recherche scientifique UMR6290 17 , Rennes, France

Abstract

Mucosal-associated invariant T (MAIT) cells harbor evolutionarily conserved TCRs, suggesting important functions. As human and mouse MAIT functional programs appear distinct, the evolutionarily conserved MAIT functional features remain unidentified. Using species-specific tetramers coupled to single-cell RNA sequencing, we characterized MAIT cell development in six species spanning 110 million years of evolution. Cross-species analyses revealed conserved transcriptional events underlying MAIT cell maturation, marked by ZBTB16 induction in all species. MAIT cells in human, sheep, cattle, and opossum acquired a shared type-1/17 transcriptional program, reflecting ancestral features. This program was also acquired by human iNKT cells, indicating common differentiation for innate-like T cells. Distinct type-1 and type-17 MAIT subsets developed in rodents, including pet mice and genetically diverse mouse strains. However, MAIT cells further matured in mouse intestines to acquire a remarkably conserved program characterized by concomitant expression of type-1, type-17, cytotoxicity, and tissue-repair genes. Altogether, the study provides a unifying view of the transcriptional features of innate-like T cells across evolution.

Funder

Agence Nationale de la Recherche

ITMO-Cancer Aviesann

SiRIC-Curie program

Institut National de la Santé et de la Recherche Médicale

Institut Curie

Institut Pasteur

European Research Council

Rennes Métropole

Société Française de Dermatologie

Novartis

Fondation pour la Recherche Médicale