Lymphotoxin-β Receptor Signaling through NF-κB2-RelB Pathway Reprograms Adipocyte Precursors as Lymph Node Stromal Cells

Lymph node development during embryogenesis involves lymphotoxin-β receptor engagement and subsequent differentiation of a poorly defined population of mesenchymal cells into lymphoid tissue organizer cells. Here, we showed that embryonic mesenchymal cells with characteristics of adipocyte precursor...

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Published in	Immunity (Cambridge, Mass.) Vol. 37; no. 4; pp. 721 - 734
Main Authors	Bénézech, Cécile, Mader, Emma, Desanti, Guillaume, Khan, Mahmood, Nakamura, Kyoko, White, Andrea, Ware, Carl F., Anderson, Graham, Caamaño, Jorge H.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 19.10.2012
Subjects	Adipocytes - cytology Adipocytes - immunology Animals Cell Differentiation Cell Movement Cells, Cultured Lymph Nodes - immunology Lymphotoxin beta Receptor - immunology Mice NF-kappa B p52 Subunit - immunology NF-kappa B p52 Subunit - metabolism Phenotype Signal Transduction Stromal Cells - immunology Transcription Factor RelB - immunology Transcription Factor RelB - metabolism
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Abstract	Lymph node development during embryogenesis involves lymphotoxin-β receptor engagement and subsequent differentiation of a poorly defined population of mesenchymal cells into lymphoid tissue organizer cells. Here, we showed that embryonic mesenchymal cells with characteristics of adipocyte precursors present in the microenvironment of lymph nodes gave rise to lymph node organizer cells. Signaling through the lymphotoxin-β receptor controlled the fate of adipocyte precursor cells by blocking adipogenesis and instead promoting lymphoid tissue stromal cell differentiation. This effect involved activation of the NF-κB2-RelB signaling pathway and inhibition of the expression of the key adipogenic factors Pparγ and Cebpα. In vivo organogenesis assays show that embryonic and adult adipocyte precursor cells can migrate into newborn lymph nodes and differentiate into a variety of lymph node stromal cells. Thus, we propose that adipose tissues act as a source of lymphoid stroma for lymph nodes and other lymphoid structures associated with fat. [Display omitted] ► Adipocyte progenitor cells give rise to lymph node anlage stromal cells ► Adipocyte progenitors’ differentiation is blocked by lymphotoxin-β receptor signaling ► LTβR signaling induces adipocyte progenitor cells to become lymphoid tissue stroma ► Adipocyte progenitor cells support lymphocyte survival ex vivo by expression of IL-7
AbstractList	Lymph node development during embryogenesis involves lymphotoxin-β receptor engagement and subsequent differentiation of a poorly defined population of mesenchymal cells into lymphoid tissue organizer cells. Here, we showed that embryonic mesenchymal cells with characteristics of adipocyte precursors present in the microenvironment of lymph nodes gave rise to lymph node organizer cells. Signaling through the lymphotoxin-β receptor controlled the fate of adipocyte precursor cells by blocking adipogenesis and instead promoting lymphoid tissue stromal cell differentiation. This effect involved activation of the NF-κB2-RelB signaling pathway and inhibition of the expression of the key adipogenic factors Pparγ and Cebpα. In vivo organogenesis assays show that embryonic and adult adipocyte precursor cells can migrate into newborn lymph nodes and differentiate into a variety of lymph node stromal cells. Thus, we propose that adipose tissues act as a source of lymphoid stroma for lymph nodes and other lymphoid structures associated with fat. Lymph node development during embryogenesis involves lymphotoxin-β receptor engagement and subsequent differentiation of a poorly defined population of mesenchymal cells into lymphoid tissue organizer cells. Here, we showed that embryonic mesenchymal cells with characteristics of adipocyte precursors present in the microenvironment of lymph nodes gave rise to lymph node organizer cells. Signaling through the lymphotoxin-β receptor controlled the fate of adipocyte precursor cells by blocking adipogenesis and instead promoting lymphoid tissue stromal cell differentiation. This effect involved activation of the NF-κB2-RelB signaling pathway and inhibition of the expression of the key adipogenic factors Pparγ and Cebpα. In vivo organogenesis assays show that embryonic and adult adipocyte precursor cells can migrate into newborn lymph nodes and differentiate into a variety of lymph node stromal cells. Thus, we propose that adipose tissues act as a source of lymphoid stroma for lymph nodes and other lymphoid structures associated with fat. [Display omitted] ► Adipocyte progenitor cells give rise to lymph node anlage stromal cells ► Adipocyte progenitors’ differentiation is blocked by lymphotoxin-β receptor signaling ► LTβR signaling induces adipocyte progenitor cells to become lymphoid tissue stroma ► Adipocyte progenitor cells support lymphocyte survival ex vivo by expression of IL-7 Lymph node development during embryogenesis involves lymphotoxin- beta receptor engagement and subsequent differentiation of a poorly defined population of mesenchymal cells into lymphoid tissue organizer cells. Here, we showed that embryonic mesenchymal cells with characteristics of adipocyte precursors present in the microenvironment of lymph nodes gave rise to lymph node organizer cells. Signaling through the lymphotoxin- beta receptor controlled the fate of adipocyte precursor cells by blocking adipogenesis and instead promoting lymphoid tissue stromal cell differentiation. This effect involved activation of the NF- Kappa B2-RelB signaling pathway and inhibition of the expression of the key adipogenic factors Ppar gamma and Cebp alpha . In vivo organogenesis assays show that embryonic and adult adipocyte precursor cells can migrate into newborn lymph nodes and differentiate into a variety of lymph node stromal cells. Thus, we propose that adipose tissues act as a source of lymphoid stroma for lymph nodes and other lymphoid structures associated with fat. Lymph node development during embryogenesis involves lymphotoxin-β receptor engagement and subsequent differentiation of a poorly defined population of mesenchymal cells into lymphoid tissue organizer cells. Here, we showed that embryonic mesenchymal cells with characteristics of adipocyte precursors present in the microenvironment of lymph nodes gave rise to lymph node organizer cells. Signaling through the lymphotoxin-β receptor controlled the fate of adipocyte precursor cells by blocking adipogenesis and instead promoting lymphoid tissue stromal cell differentiation. This effect involved activation of the NF-κB2-RelB signaling pathway and inhibition of the expression of the key adipogenic factors Pparγ and Cebpα . In vivo organogenesis assays show that embryonic and adult adipocyte precursor cells can migrate into newborn lymph nodes and differentiate into a variety of lymph node stromal cells. Thus, we propose that adipose tissues act as a source of lymphoid stroma for lymph nodes and other lymphoid structures associated with fat.
Author	Caamaño, Jorge H. Mader, Emma Khan, Mahmood Anderson, Graham Nakamura, Kyoko Ware, Carl F. Bénézech, Cécile Desanti, Guillaume White, Andrea
AuthorAffiliation	2 Infectious and Inflammatory Disease Center, Sanford Burnham Medical Research Institute, La Jolla, CA 92037, USA 1 School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK
AuthorAffiliation_xml	– name: 2 Infectious and Inflammatory Disease Center, Sanford Burnham Medical Research Institute, La Jolla, CA 92037, USA – name: 1 School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK
Author_xml	– sequence: 1 givenname: Cécile surname: Bénézech fullname: Bénézech, Cécile email: c.benezech@bham.ac.uk organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK – sequence: 2 givenname: Emma surname: Mader fullname: Mader, Emma organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK – sequence: 3 givenname: Guillaume surname: Desanti fullname: Desanti, Guillaume organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK – sequence: 4 givenname: Mahmood surname: Khan fullname: Khan, Mahmood organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK – sequence: 5 givenname: Kyoko surname: Nakamura fullname: Nakamura, Kyoko organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK – sequence: 6 givenname: Andrea surname: White fullname: White, Andrea organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK – sequence: 7 givenname: Carl F. surname: Ware fullname: Ware, Carl F. organization: Infectious and Inflammatory Disease Center, Sanford Burnham Medical Research Institute, La Jolla, CA 92037, USA – sequence: 8 givenname: Graham surname: Anderson fullname: Anderson, Graham organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK – sequence: 9 givenname: Jorge H. surname: Caamaño fullname: Caamaño, Jorge H. email: j.caamano@bham.ac.uk organization: School of Immunity and Infection, IBR-MRC Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/22940098$$D View this record in MEDLINE/PubMed
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Snippet	Lymph node development during embryogenesis involves lymphotoxin-β receptor engagement and subsequent differentiation of a poorly defined population of... Lymph node development during embryogenesis involves lymphotoxin- beta receptor engagement and subsequent differentiation of a poorly defined population of...
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SubjectTerms	Adipocytes - cytology Adipocytes - immunology Animals Cell Differentiation Cell Movement Cells, Cultured Lymph Nodes - immunology Lymphotoxin beta Receptor - immunology Mice NF-kappa B p52 Subunit - immunology NF-kappa B p52 Subunit - metabolism Phenotype Signal Transduction Stromal Cells - immunology Transcription Factor RelB - immunology Transcription Factor RelB - metabolism
Title	Lymphotoxin-β Receptor Signaling through NF-κB2-RelB Pathway Reprograms Adipocyte Precursors as Lymph Node Stromal Cells
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