Molecular and Functional Characterization of Lymphoid Progenitor Subsets Reveals a Bipartite Architecture of Human Lymphopoiesis

Immunity. 2017 Oct 17;47(4):680-696.e8. doi: 10.1016/j.immuni.2017.09.009.

Abstract

The classical model of hematopoiesis established in the mouse postulates that lymphoid cells originate from a founder population of common lymphoid progenitors. Here, using a modeling approach in humanized mice, we showed that human lymphoid development stemmed from distinct populations of CD127- and CD127+ early lymphoid progenitors (ELPs). Combining molecular analyses with in vitro and in vivo functional assays, we demonstrated that CD127- and CD127+ ELPs emerged independently from lympho-mono-dendritic progenitors, responded differently to Notch1 signals, underwent divergent modes of lineage restriction, and displayed both common and specific differentiation potentials. Whereas CD127- ELPs comprised precursors of T cells, marginal zone B cells, and natural killer (NK) and innate lymphoid cells (ILCs), CD127+ ELPs supported production of all NK cell, ILC, and B cell populations but lacked T potential. On the basis of these results, we propose a "two-family" model of human lymphoid development that differs from the prevailing model of hematopoiesis.

Keywords: B cell ontogeny; Human lymphopoiesis; T cell precursors; early lymphoid progenitors; natural killer and innate lymphoid cells differentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • B-Lymphocytes / cytology
  • B-Lymphocytes / metabolism*
  • Cell Differentiation / genetics
  • Cell Lineage / genetics
  • Cells, Cultured
  • Female
  • Gene Expression Profiling / methods
  • Humans
  • Interleukin Receptor Common gamma Subunit / deficiency
  • Interleukin Receptor Common gamma Subunit / genetics
  • Interleukin-7 Receptor alpha Subunit / genetics
  • Interleukin-7 Receptor alpha Subunit / metabolism
  • Killer Cells, Natural / cytology
  • Killer Cells, Natural / metabolism*
  • Lymphoid Progenitor Cells / cytology
  • Lymphoid Progenitor Cells / metabolism*
  • Lymphoid Progenitor Cells / transplantation
  • Lymphopoiesis / genetics*
  • Male
  • Mice, Inbred NOD
  • Mice, Knockout
  • Mice, SCID
  • Middle Aged
  • Stem Cell Transplantation
  • T-Lymphocytes / cytology
  • T-Lymphocytes / metabolism*
  • Transplantation, Heterologous
  • Young Adult

Substances

  • Il2rg protein, mouse
  • Interleukin Receptor Common gamma Subunit
  • Interleukin-7 Receptor alpha Subunit