Functional B-1 progenitor cells are present in the hematopoietic stem cell-deficient embryo and depend on<i>Cbfβ</i>for their development

Kobayashi, Michihiro; Shelley, W. Christopher; Seo, Wooseok; Vemula, Sasidhar; Yang, Lin; Liu, Yan; Kapur, Reuben; Taniuchi, Ichiro; Yoshimoto, Momoko

doi:10.1073/pnas.1407370111

Cited by 79 publications

(97 citation statements)

References 41 publications

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“…We (Barber et al, 2011; Montecino-Rodriguez et al, 2006) and others (Esplin et al, 2009; Ghosn et al, 2011; Holodick et al, 2014; Kobayashi et al, 2014; Yoshimoto et al, 2011) have reported that lineage negative (Lin − ) CD93 + CD19 + CD45R(B220) −/low (hereafter CD19 + CD45R −/low ) B-1 specified progenitors are phenotypically distinct from Lin − CD93 + CD19 − CD45R(B220) + CD43 + (hereafter CD19 − CD45R + ) B-2 progenitors (Figure S2). These populations are at a comparable pre-pro-B cell stage, as both have undergone heavy chain D-J, but not V-D-J gene rearrangement (Montecino-Rodriguez et al, 2006), and B-1 progenitors lack V H -D-J H transcripts (de Andres et al, 2002).…”

Section: Resultsmentioning

confidence: 86%

Distinct Genetic Networks Orchestrate the Emergence of Specific Waves of Fetal and Adult B-1 and B-2 Development

et al. 2016

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SUMMARY B cell development is often depicted as a linear process initiating in the fetus and continuing postnatally. Using a PU.1 hypomorphic mouse model, we found that B-1 and B-2 lymphopoiesis occurred in distinct fetal and adult waves differentially dependent on the Sfpi1 14 kB upstream regulatory element. The initial wave of fetal B-1 development was absent in PU.1 hypomorphic mice, while subsequent fetal and adult waves emerged. In contrast, B-2 lymphopoiesis occurred in distinct fetal and adult waves. Whole transcriptome profiling of fetal and adult B cell progenitors supported the existence of three waves of B-1 and two waves of B-2 development, and revealed that the network of transcription factors governing B lineage specification and commitment was highly divergent between B-1 and B-2 progenitors. These findings support the view that the B-1 and B-2 lineages are distinct and provide a genetic basis for layering of immune system development.

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Section: Resultsmentioning

confidence: 86%

Distinct Genetic Networks Orchestrate the Emergence of Specific Waves of Fetal and Adult B-1 and B-2 Development

et al. 2016

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“…B cell potential independent of HSC formation has been identified in the E9.5 yolk sac coincident with EMP formation (Kobayashi et al, 2014). However, EMPs lack IL7R and Flt3 cell surface markers and Pax5 transcription factor expression, which are associated with lymphoid progenitors arising from HSCs (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In the mouse, HSC-independent hematopoiesis is not only necessary, but sufficient to support the survival until birth of embryos lacking HSCs (Chen et al, 2011). Rare cells with lymphoid potential also arise before adult-transplantable HSCs, including HSC-independent B-1 cell progenitors and immature HSCs capable of becoming HSCs after ex vivo culture or when transplanted into specialized hosts (Arora et al, 2014; Kieusseian et al, 2012; Kobayashi et al, 2014; Yoder et al, 1997). However, the relationship of these cells with EMPs has not been resolved.…”

Section: Introductionmentioning

confidence: 99%

Distinct Sources of Hematopoietic Progenitors Emerge before HSCs and Provide Functional Blood Cells in the Mammalian Embryo

McGrath¹,

Frame²,

Fegan³

et al. 2015

Cell Reports

341

382

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Summary Hematopoietic potential arises in mammalian embryos before adult-repopulating hematopoietic stem cells (HSCs). At E9.5, we show the first murine definitive erythro-myeloid progenitors (EMPs) have an immunophenotype distinct from primitive hematopoietic progenitors, maturing megakaryocytes and macrophages, and rare B cell potential. EMPs emerge in the yolk sac with erythroid and broad myeloid, but not lymphoid, potential. EMPs migrate to the fetal liver and rapidly differentiate including production of circulating neutrophils by E11.5. While the surface markers, transcription factors and lineage potential associated with EMPs overlap with those found in adult definitive hematopoiesis, they are present in unique combinations or proportions that result in a specialized definitive embryonic progenitor. Further, we find that ES cell -derived hematopoiesis recapitulates early yolk sac hematopoiesis, including primitive, EMP and rare B cell potential. EMPs do not have long term potential when transplanted in immunocompromised adults, but can provide transient adult-like RBC reconstitution.

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“…Progenitors with B-cell and T-cell potential emerge around E9.0 both in the yolk sac and the embryo proper [9-11, 49]. These lymphoid progenitors migrate to and differentiate in the early fetal liver, and are thought to provide unique subsets of lymphoid cells that persist in the adult, for review see [50].…”

Section: Emergence Of Hematopoiesis In the Fetusmentioning

confidence: 99%

“…Macrophage colony-forming potential is associated temporally and spatially with each of these waves of primitive and definitive erythroid progenitors [4]. Recent cell marking studies have revealed that subsets of tissue-resident blood cells, including some tissue-resident macrophages, do not appear to be replenished by HSCs postnatally, and are instead regenerated by self-renewal of fetal-derived cells [6-11]. In this review, we will consider the developmental origin of fetal-derived macrophages in the context of the various waves of hematopoietic potential that emerge during early embryogenesis.…”

Section: Introductionmentioning

confidence: 99%

Early hematopoiesis and macrophage development

McGrath

Frame

Palis

2015

Seminars in Immunology

145

126

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The paradigm that all blood cells are derived from hematopoietic stem cells (HSCs) has been challenged by two findings. First, there are tissue-resident hematopoietic cells, including subsets of macrophages that are not replenished by adult HSCs, but instead are maintained by self-renewal of fetal-derived cells. Second, during embryogenesis, there is a conserved program of HSC-independent hematopoiesis that precedes HSC function and is required for embryonic survival. The presence of waves of HSC-independent hematopoiesis as well as fetal HSCs raises questions about the origin of fetal-derived adult tissue-resident macrophages. In the murine embryo, historical examination of embryonic macrophage and monocyte populations combined with recent reports utilizing genetic lineage-tracing approaches has led to a model of macrophage ontogeny that can be integrated with existing models of hematopoietic ontogeny. The first wave of hematopoiesis contains primitive erythroid, megakaryocyte and macrophage progenitors that arise in the yolk sac, and these macrophage progenitors are the source of early macrophages throughout the embryo, including the liver. A second wave of multipotential erythro-myeloid progenitors (EMPs) also arises in the yolk sac . EMPs colonize the fetal liver, initiating myelopoiesis and forming macrophages. Lineage tracing indicates that this second wave of macrophages are distributed in most fetal tissues, although not appreciably in the brain. Thus, fetal-derived adult tissue-resident macrophages, other than microglia, appear to predominately derive from EMPs. While HSCs emerge at midgestation and colonize the fetal liver, the relative contribution of fetal HSCs to tissue macrophages at later stages of development is unclear. The inclusion of macrophage potential in multiple waves of hematopoiesis is consistent with reports of their functional roles throughout development in innate immunity, phagocytosis, and tissue morphogenesis and remodeling. Understanding the influences of developmental origin, as well as local tissue-specific signals, will be necessary to fully decode the diverse functions and responses of tissue-resident macrophages.

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Functional B-1 progenitor cells are present in the hematopoietic stem cell-deficient embryo and depend onCbfβfor their development

Cited by 79 publications

References 41 publications

Distinct Genetic Networks Orchestrate the Emergence of Specific Waves of Fetal and Adult B-1 and B-2 Development

Distinct Genetic Networks Orchestrate the Emergence of Specific Waves of Fetal and Adult B-1 and B-2 Development

Distinct Sources of Hematopoietic Progenitors Emerge before HSCs and Provide Functional Blood Cells in the Mammalian Embryo

Early hematopoiesis and macrophage development

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