Distinct subsets of multi-lymphoid progenitors support ontogeny-related changes in human lymphopoiesis

Seydou Keita¹, Samuel Diop², Shalva Lekiashvili¹, Emna Chabaane¹, Elisabeth Nelson¹, Marion Strullu³, Chloé Arfeuille³, Fabien Guimiot⁴, Thomas Domet⁵, Sophie Duchez⁶, Bertrand Evrard⁷, Thomas Darde⁸, Jerome Larghero⁵, Els Verhoeyen⁹, Ana Cumano¹⁰, Elizabeth A Macintyre¹¹, Zeinab Kasraian¹¹, François Jouen¹², Michele Goodhardt¹, David Garrick¹, Frederic Chalmel⁷, Kutaiba Alhaj Hussen¹³, Bruno Canque¹⁴

Affiliations

¹ INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France.
² INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France; Laboratoire Cognitions Humaine et Artificielle (CHArt) EA 4004 FED 4246, École Pratique des Hautes Études/PSL Research University, Paris, France.
³ Service d'Hémato-Immunologie Pédiatrique, Inserm U1131, Université de Paris, Hôpital Robert-Debré, AP-HP, Paris, France.
⁴ INSERM UMR 1141, Service de Biologie du Développement, Université de Paris, Hôpital Robert-Debré, AP-HP, Paris, France.
⁵ AP-HP, Hôpital Saint-Louis, Unité de Thérapie Cellulaire, CIC de Biothérapies, Université de Paris, INSERM U976, Paris, France.
⁶ Plateforme d'Imagerie et de Tri Cellulaire, Institut de Recherche Saint Louis, Paris, France.
⁷ INSERM, EHESP, IRSET (Institut de Recherche en Santé, Environnement et Travail), UMR_S 1085, University Rennes, Rennes, France.
⁸ SciLicium, Rennes, France.
⁹ CIRI, International Center for Infectiology Research, Université de Lyon, INSERM U1111, Lyon, France; Centre Mediterranéen de Médecine Moléculaire (C3M), INSERM U1065, Nice, France.
¹⁰ Unit of Lymphopoiesis, Immunology Department, Institut Pasteur, Paris, France.
¹¹ Institut Necker Enfants-Malades, Team 2, INSERM Unité 1151, Hôpital Necker Enfants-Malades, Laboratoire d'Onco-Hématologie, Assistance Publique-Hôpitaux de Paris (AP-HP), Université de Paris, Paris, France.
¹² Laboratoire Cognitions Humaine et Artificielle (CHArt) EA 4004 FED 4246, École Pratique des Hautes Études/PSL Research University, Paris, France.
¹³ INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France; Service de Biochimie, Université de Paris Saclay, Hôpital Paul Brousse, AP-HP, Paris, France. Electronic address: kutaiba.alhajhussen@aphp.fr.
¹⁴ INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France. Electronic address: bruno.canque@ephe.psl.eu.

PMID: 37294633
DOI: 10.1016/j.celrep.2023.112618

Free article

Distinct subsets of multi-lymphoid progenitors support ontogeny-related changes in human lymphopoiesis

Seydou Keita et al. Cell Rep. 2023.

Free article

. 2023 Jun 27;42(6):112618.

doi: 10.1016/j.celrep.2023.112618. Epub 2023 Jun 8.

Authors

Affiliations

¹ INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France.
² INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France; Laboratoire Cognitions Humaine et Artificielle (CHArt) EA 4004 FED 4246, École Pratique des Hautes Études/PSL Research University, Paris, France.
³ Service d'Hémato-Immunologie Pédiatrique, Inserm U1131, Université de Paris, Hôpital Robert-Debré, AP-HP, Paris, France.
⁴ INSERM UMR 1141, Service de Biologie du Développement, Université de Paris, Hôpital Robert-Debré, AP-HP, Paris, France.
⁵ AP-HP, Hôpital Saint-Louis, Unité de Thérapie Cellulaire, CIC de Biothérapies, Université de Paris, INSERM U976, Paris, France.
⁶ Plateforme d'Imagerie et de Tri Cellulaire, Institut de Recherche Saint Louis, Paris, France.
⁷ INSERM, EHESP, IRSET (Institut de Recherche en Santé, Environnement et Travail), UMR_S 1085, University Rennes, Rennes, France.
⁸ SciLicium, Rennes, France.
⁹ CIRI, International Center for Infectiology Research, Université de Lyon, INSERM U1111, Lyon, France; Centre Mediterranéen de Médecine Moléculaire (C3M), INSERM U1065, Nice, France.
¹⁰ Unit of Lymphopoiesis, Immunology Department, Institut Pasteur, Paris, France.
¹¹ Institut Necker Enfants-Malades, Team 2, INSERM Unité 1151, Hôpital Necker Enfants-Malades, Laboratoire d'Onco-Hématologie, Assistance Publique-Hôpitaux de Paris (AP-HP), Université de Paris, Paris, France.
¹² Laboratoire Cognitions Humaine et Artificielle (CHArt) EA 4004 FED 4246, École Pratique des Hautes Études/PSL Research University, Paris, France.
¹³ INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France; Service de Biochimie, Université de Paris Saclay, Hôpital Paul Brousse, AP-HP, Paris, France. Electronic address: kutaiba.alhajhussen@aphp.fr.
¹⁴ INSERM U976, Université de Paris, École Pratique des Hautes Études/PSL Research University, Institut de Recherche Saint Louis, Paris, France. Electronic address: bruno.canque@ephe.psl.eu.

PMID: 37294633
DOI: 10.1016/j.celrep.2023.112618

Abstract

Changes in lymphocyte production patterns occurring across human ontogeny remain poorly defined. In this study, we demonstrate that human lymphopoiesis is supported by three waves of embryonic, fetal, and postnatal multi-lymphoid progenitors (MLPs) differing in CD7 and CD10 expression and their output of CD127^-/+ early lymphoid progenitors (ELPs). In addition, our results reveal that, like the fetal-to-adult switch in erythropoiesis, transition to postnatal life coincides with a shift from multilineage to B lineage-biased lymphopoiesis and an increase in production of CD127⁺ ELPs, which persists until puberty. A further developmental transition is observed in elderly individuals whereby B cell differentiation bypasses the CD127⁺ compartment and branches directly from CD10⁺ MLPs. Functional analyses indicate that these changes are determined at the level of hematopoietic stem cells. These findings provide insights for understanding identity and function of human MLPs and the establishment and maintenance of adaptative immunity.

Keywords: CP: Developmental biology; CP: Immunology; adaptative immunity; aging; development; early lymphoid progenitors; human lymphopoiesis; lymphoid development architecture; multi-lymphoid progenitors.

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Declaration of interests The authors declare no competing interests.

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Distinct subsets of multi-lymphoid progenitors support ontogeny-related changes in human lymphopoiesis

Affiliations

Distinct subsets of multi-lymphoid progenitors support ontogeny-related changes in human lymphopoiesis

Authors

Affiliations

Abstract

Conflict of interest statement

Publication types

MeSH terms

LinkOut - more resources

Full Text Sources

Medical

Miscellaneous