Dendritic cell potentials of early lymphoid and myeloid progenitors.

It has been proposed that there are at least 2 classes of dendritic cells (DCs), CD8alpha(+) DCs derived from the lymphoid lineage and CD8alpha(-) DCs derived from the myeloid lineage. Here, the abilities of lymphoid- and myeloid-restricted progenitors to generate DCs are compared, and their overall contributions to the DC compartment are evaluated. It has previously been shown that primitive myeloid-committed progenitors (common myeloid progenitors [CMPs]) are efficient precursors of both CD8alpha(+) and CD8alpha(-) DCs in vivo. Here it is shown that the earliest lymphoid-committed progenitors (common lymphoid progenitors [CLPs]) and CMPs and their progeny granulocyte-macrophage progenitors (GMPs) can give rise to functional DCs in vitro and in vivo. CLPs are more efficient in generating DCs than their T-lineage descendants, the early thymocyte progenitors and pro-T cells, and CMPs are more efficient DC precursors than the descendant GMPs, whereas pro-B cells and megakaryocyte-erythrocyte progenitors are incapable of generating DCs. Thus, DC developmental potential is preserved during T- but not B-lymphoid differentiation from CLP and during granulocyte-macrophage but not megakaryocyte-erythrocyte development from CMP. In vivo reconstitution experiments show that CLPs and CMPs can reconstitute CD8alpha(+) and CD8alpha(-) DCs with similar efficiency on a per cell basis. However, CMPs are 10-fold more numerous than CLPs, suggesting that at steady state, CLPs provide only a minority of splenic DCs and approximately half the DCs in thymus, whereas most DCs, including CD8alpha(+) and CD8alpha(-) subtypes, are of myeloid origin. (Blood. 2001;97:3333-3341)

[1]  I. Weissman,et al.  Development of CD8α-Positive Dendritic Cells from a Common Myeloid Progenitor , 2000 .

[2]  C. Arias,et al.  Concept of lymphoid versus myeloid dendritic cell lineages revisited: both CD8α− and CD8α+dendritic cells are generated from CD4lowlymphoid-committed precursors , 2000 .

[3]  I. Weissman,et al.  Cell-fate conversion of lymphoid-committed progenitors by instructive actions of cytokines , 2000, Nature.

[4]  M. Merad,et al.  Differentiation of myeloid dendritic cells into CD8α-positive dendritic cells in vivo , 2000 .

[5]  A. Sher,et al.  CCR5 provides a signal for microbial induced production of IL-12 by CD8α+ dendritic cells , 2000, Nature Immunology.

[6]  I. Weissman,et al.  AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Nussenzweig,et al.  DEC-205 as a marker of dendritic cells with regulatory effects on CD8 T cell responses. , 2000, International immunology.

[8]  H. Macdonald,et al.  Notch1 Deficiency Dissociates the Intrathymic Development of Dendritic Cells and T Cells , 2000, The Journal of experimental medicine.

[9]  I. Weissman,et al.  A clonogenic common myeloid progenitor that gives rise to all myeloid lineages , 2000, Nature.

[10]  R. Maki,et al.  Transcription Factor PU.1 Is Necessary for Development of Thymic and Myeloid Progenitor-Derived Dendritic Cells1 , 2000, The Journal of Immunology.

[11]  R. Steinman,et al.  The Induction of Tolerance by Dendritic Cells That Have Captured Apoptotic Cells , 2000, The Journal of experimental medicine.

[12]  L. Spain,et al.  PU.1 is required for myeloid-derived but not lymphoid-derived dendritic cells. , 2000, Blood.

[13]  H. Rodewald,et al.  Developmental dissociation of thymic dendritic cell and thymocyte lineages revealed in growth factor receptor mutant mice. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[14]  C. Figdor,et al.  Generation and functional characterization of mouse monocyte‐derived dendritic cells , 1999, European journal of immunology.

[15]  R. Maldonado-López,et al.  Role of CD8α+ and CD8α− dendritic cells in the induction of primary immune responses in vivo , 1999, Journal of leukocyte biology.

[16]  Mamoru Ito,et al.  Interleukin 12-dependent interferon gamma production by CD8alpha+ lymphoid dendritic cells. , 1999 .

[17]  K. Matsushima,et al.  Transforming Growth Factor-β1 Polarizes Murine Hematopoietic Progenitor Cells to Generate Langerhans Cell-Like Dendritic Cells Through a Monocyte/Macrophage Differentiation Pathway , 1999 .

[18]  B. Pulendran,et al.  Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R. Maldonado-López,et al.  CD8α+ and CD8α− Subclasses of Dendritic Cells Direct the Development of Distinct T Helper Cells In Vivo , 1999, The Journal of experimental medicine.

[20]  F. Anjuère,et al.  Definition of dendritic cell subpopulations present in the spleen, Peyer's patches, lymph nodes, and skin of the mouse. , 1999, Blood.

[21]  A. D'amico,et al.  RelB Is Essential for the Development of Myeloid-Related CD8α− Dendritic Cells but Not of Lymphoid-Related CD8α+ Dendritic Cells , 1998 .

[22]  P. Kincade,et al.  Cutting Edge: CD19+ Pro-B Cells Can Give Rise to Dendritic Cells In Vitro , 1998, The Journal of Immunology.

[23]  J. Cyster,et al.  Epstein-Barr Virus–induced Molecule 1 Ligand Chemokine Is Expressed by Dendritic Cells in Lymphoid Tissues and Strongly Attracts Naive T Cells and Activated B Cells , 1998, The Journal of experimental medicine.

[24]  R. Steinman,et al.  Dendritic cells and the control of immunity , 1998, Nature.

[25]  D. Klatzmann,et al.  Heterogeneity of mouse spleen dendritic cells: in vivo phagocytic activity, expression of macrophage markers, and subpopulation turnover. , 1998, Journal of immunology.

[26]  V. Kronin,et al.  The nature of the signals regulating CD8 T cell proliferative responses to CD8α+ or CD8α− dendritic cells , 1997 .

[27]  I. Weissman,et al.  Identification of Clonogenic Common Lymphoid Progenitors in Mouse Bone Marrow , 1997, Cell.

[28]  C. Caux,et al.  Dendritic Cell Development: Multiple Pathways to Nature's Adjuvants , 1997, Stem cells.

[29]  K. Georgopoulos,et al.  Cell-autonomous defects in dendritic cell populations of Ikaros mutant mice point to a developmental relationship with the lymphoid lineage. , 1997, Immunity.

[30]  B. Pulendran,et al.  Developmental pathways of dendritic cells in vivo: distinct function, phenotype, and localization of dendritic cell subsets in FLT3 ligand-treated mice. , 1997, Journal of immunology.

[31]  I. Weissman,et al.  Bcl-2 Rescues T Lymphopoiesis, but Not B or NK Cell Development, in Common γ Chain–Deficient Mice , 1997 .

[32]  I. Weissman,et al.  Bcl-2 Rescues T Lymphopoiesis in Interleukin-7 Receptor–Deficient Mice , 1997, Cell.

[33]  R. Steinman,et al.  Dendritic cells in the T‐cell areas of lymphoid organs , 1997, Immunological reviews.

[34]  Li Wu,et al.  Dendritic Cell Development in Culture from Thymic Precursor Cells in the Absence of Granulocyte/Macrophage Colony-stimulating Factor , 1996, The Journal of experimental medicine.

[35]  A. Kelso,et al.  A subclass of dendritic cells regulates the response of naive CD8 T cells by limiting their IL-2 production. , 1996, Journal of immunology.

[36]  P. De Baetselier,et al.  Regulation of Dendritic Cell Numbers and Maturation by Lipopolysaccharide in Vivo , 1996 .

[37]  K. Shortman,et al.  Thymic dendritic cell precursors: relationship to the T lymphocyte lineage and phenotype of the dendritic cell progeny , 1996, The Journal of experimental medicine.

[38]  K. Shortman,et al.  A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand- induced apoptosis , 1996, The Journal of experimental medicine.

[39]  Li Wu,et al.  Mouse thymus dendritic cells: kinetics of development and changes in surface markers during maturation , 1995, European journal of immunology.

[40]  I. Weissman.  Stem cells, clonal progenitors, and commitment to the three lymphocyte lineages: T, B, and NK cells. , 1994, Immunity.

[41]  F. Sallusto,et al.  Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha , 1994, The Journal of experimental medicine.

[42]  S. Carsons,et al.  Mechanisms of tumor necrosis factor-granulocyte-macrophage colony-stimulating factor-induced dendritic cell development. , 1993, Blood.

[43]  Li Wu,et al.  Thymic dendritic cells and T cells develop simultaneously in the thymus from a common precursor population , 1993, Nature.

[44]  R. Steinman,et al.  Granulocytes, macrophages, and dendritic cells arise from a common major histocompatibility complex class II-negative progenitor in mouse bone marrow. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[45]  R. Steinman,et al.  Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor , 1992, The Journal of experimental medicine.

[46]  J. Tikerpae,et al.  Interactions of tumor necrosis factor with granulocyte-macrophage colony-stimulating factor and other cytokines in the regulation of dendritic cell growth in vitro from early bipotent CD34+ progenitors in human bone marrow. , 1992, Journal of immunology.

[47]  M. Mehlig,et al.  Dendritic cells from mouse bone marrow: in vitro differentiation using low doses of recombinant granulocyte-macrophage colony-stimulating factor. , 1992, Journal of immunological methods.

[48]  Li Wu,et al.  The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells , 1992, The Journal of experimental medicine.

[49]  R. Steinman,et al.  Two populations of splenic dendritic cells detected with M342, a new monoclonal to an intracellular antigen of interdigitating dendritic cells and some B lymphocytes , 1992, Journal of leukocyte biology.

[50]  P. Dobrzanski,et al.  RelB, a new Rel family transcription activator that can interact with p50-NF-kappa B , 1992, Molecular and cellular biology.

[51]  M. Antica,et al.  Developmental potential of the earliest precursor cells from the adult mouse thymus , 1991, The Journal of experimental medicine.

[52]  M. Klemsz,et al.  The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene , 1990, Cell.

[53]  C Caux,et al.  Immunobiology of dendritic cells. , 2000, Annual review of immunology.

[54]  Stephen L. Nutt,et al.  Commitment to the B-lymphoid lineage depends on the transcription factor Pax5 , 1999, Nature.

[55]  P. Kincade,et al.  CD19+ pro-B cells can give rise to dendritic cells in vitro. , 1998, Journal of immunology.

[56]  I. Weissman,et al.  Bcl-2 rescues T lymphopoiesis, but not B or NK cell development, in common gamma chain-deficient mice. , 1997, Immunity.