Ontogeny of Stromal Organizer Cells during Lymph Node Development
The development of secondary lymphoid organs, such as lymph nodes (LNs), in the embryo results from the reciprocal action between lymphoid tissue inducer (LTi) cells and stromal cells. However, the initial events inducing LN anlagen formation before the LTi stromal cells cross-talk interactions take...
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Published in | The Journal of immunology (1950) Vol. 184; no. 8; pp. 4521 - 4530 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Am Assoc Immnol
15.04.2010
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Abstract | The development of secondary lymphoid organs, such as lymph nodes (LNs), in the embryo results from the reciprocal action between lymphoid tissue inducer (LTi) cells and stromal cells. However, the initial events inducing LN anlagen formation before the LTi stromal cells cross-talk interactions take place are not fully elucidated. In this study, we show that the inguinal LN anlagen in mouse embryos developed from mesenchymal cells surrounding the lymph sacs, spherical structures of endothelial cells that bud from veins. Using inguinal and mesenteric LNs (mLNs), we provide evidence supporting a two-step maturation model for stromal cells: first, ICAM-1(-)VCAM-1(-) mesenchymal precursor cells become ICAM-1(int)VCAM-1(int) cells, in a process independent of LTi cells and lymphotoxin beta receptor (LTbetaR) signaling. The second step involves the maturation of ICAM-1(int)VCAM-1(int) cells to ICAM-1(high)VCAM-1(high) mucosal addressin cell adhesion molecule-1(+) organizer cells and depends on both LTi cells and LTbetaR. Addition of alphaLTbetaR agonist to LN organ cultures was sufficient to induce ICAM-1(int)VCAM-1(int) cells to mature. In LtbetaR(-/-) embryos, both inguinal and mLN stromal cells showed a block at the ICAM-1(int)VCAM-1(int) stage, and, contrary to inguinal LNs, mLNs persist longer and contained LTi cells, which correlated with the sustained gene expression of Il-7, Cxcl13, and, to a lesser degree, Ccl21. Taken together, these results highlight the importance of the signals and cellular interactions that induce the maturation of stromal cells and ultimately lead to the formation of lymphoid tissues. |
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AbstractList | The development of secondary lymphoid organs, such as lymph nodes (LNs), in the embryo results from the reciprocal action between lymphoid tissue inducer (LTi) cells and stromal cells. However, the initial events inducing LN anlagen formation before the LTi stromal cells cross-talk interactions take place are not fully elucidated. In this study, we show that the inguinal LN anlagen in mouse embryos developed from mesenchymal cells surrounding the lymph sacs, spherical structures of endothelial cells that bud from veins. Using inguinal and mesenteric LNs (mLNs), we provide evidence supporting a two-step maturation model for stromal cells: first, ICAM-1
−
VCAM-1
−
mesenchymal precursor cells become ICAM-1
int
VCAM-1
int
cells, in a process independent of LTi cells and lymphotoxin β receptor (LTβR) signaling. The second step involves the maturation of ICAM-1
int
VCAM-1
int
cells to ICAM-1
high
VCAM-1
high
mucosal addressin cell adhesion molecule-1
+
organizer cells and depends on both LTi cells and LTβR. Addition of αLTβR agonist to LN organ cultures was sufficient to induce ICAM-1
int
VCAM-1
int
cells to mature. In
Lt
β
R
−/−
embryos, both inguinal and mLN stromal cells showed a block at the ICAM-1
int
VCAM-1
int
stage, and, contrary to inguinal LNs, mLNs persist longer and contained LTi cells, which correlated with the sustained gene expression of
Il-7
, C
xcl13
, and, to a lesser degree,
Ccl21
. Taken together, these results highlight the importance of the signals and cellular interactions that induce the maturation of stromal cells and ultimately lead to the formation of lymphoid tissues. The development of secondary lymphoid organs, such as lymph nodes (LNs), in the embryo results from the reciprocal action between lymphoid tissue inducer (LTi) cells and stromal cells. However, the initial events inducing LN anlagen formation before the LTi stromal cells cross-talk interactions take place are not fully elucidated. In this study, we show that the inguinal LN anlagen in mouse embryos developed from mesenchymal cells surrounding the lymph sacs, spherical structures of endothelial cells that bud from veins. Using inguinal and mesenteric LNs (mLNs), we provide evidence supporting a two-step maturation model for stromal cells: first, ICAM-1(-)VCAM-1(-) mesenchymal precursor cells become ICAM-1(int)VCAM-1(int) cells, in a process independent of LTi cells and lymphotoxin beta receptor (LTbetaR) signaling. The second step involves the maturation of ICAM-1(int)VCAM-1(int) cells to ICAM-1(high)VCAM-1(high) mucosal addressin cell adhesion molecule-1(+) organizer cells and depends on both LTi cells and LTbetaR. Addition of alphaLTbetaR agonist to LN organ cultures was sufficient to induce ICAM-1(int)VCAM-1(int) cells to mature. In LtbetaR(-/-) embryos, both inguinal and mLN stromal cells showed a block at the ICAM-1(int)VCAM-1(int) stage, and, contrary to inguinal LNs, mLNs persist longer and contained LTi cells, which correlated with the sustained gene expression of Il-7, Cxcl13, and, to a lesser degree, Ccl21. Taken together, these results highlight the importance of the signals and cellular interactions that induce the maturation of stromal cells and ultimately lead to the formation of lymphoid tissues. The development of secondary lymphoid organs, such as lymph nodes (LNs), in the embryo results from the reciprocal action between lymphoid tissue inducer (LTi) cells and stromal cells. However, the initial events inducing LN anlagen formation before the LTi stromal cells cross-talk interactions take place are not fully elucidated. In this study, we show that the inguinal LN anlagen in mouse embryos developed from mesenchymal cells surrounding the lymph sacs, spherical structures of endothelial cells that bud from veins. Using inguinal and mesenteric LNs (mLNs), we provide evidence supporting a two-step maturation model for stromal cells: first, ICAM-1−VCAM-1− mesenchymal precursor cells become ICAM-1intVCAM-1int cells, in a process independent of LTi cells and lymphotoxin β receptor (LTβR) signaling. The second step involves the maturation of ICAM-1intVCAM-1int cells to ICAM-1highVCAM-1high mucosal addressin cell adhesion molecule-1+ organizer cells and depends on both LTi cells and LTβR. Addition of αLTβR agonist to LN organ cultures was sufficient to induce ICAM-1intVCAM-1int cells to mature. In LtβR−/− embryos, both inguinal and mLN stromal cells showed a block at the ICAM-1intVCAM-1int stage, and, contrary to inguinal LNs, mLNs persist longer and contained LTi cells, which correlated with the sustained gene expression of Il-7, Cxcl13, and, to a lesser degree, Ccl21. Taken together, these results highlight the importance of the signals and cellular interactions that induce the maturation of stromal cells and ultimately lead to the formation of lymphoid tissues. |
Author | Benezech, Cecile Parnell, Sonia Caamano, Jorge H Mader, Emma Anderson, Graham Ware, Carl F Serre, Karine Pfeffer, Klaus White, Andrea |
AuthorAffiliation | Institut fur Medizinische Mikrobiologie und Krankenhaushygiene, Heinrich-Heine-University, Düsseldorf, Germany La Jolla Institute for Allergy and Immunology, La Jolla, CA 92037 School of Immunity and Infection, Institute for BioMedical Research-Medical Research Council Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom |
AuthorAffiliation_xml | – name: La Jolla Institute for Allergy and Immunology, La Jolla, CA 92037 – name: Institut fur Medizinische Mikrobiologie und Krankenhaushygiene, Heinrich-Heine-University, Düsseldorf, Germany – name: School of Immunity and Infection, Institute for BioMedical Research-Medical Research Council Centre for Immune Regulation, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdom |
Author_xml | – sequence: 1 fullname: Benezech, Cecile – sequence: 2 fullname: White, Andrea – sequence: 3 fullname: Mader, Emma – sequence: 4 fullname: Serre, Karine – sequence: 5 fullname: Parnell, Sonia – sequence: 6 fullname: Pfeffer, Klaus – sequence: 7 fullname: Ware, Carl F – sequence: 8 fullname: Anderson, Graham – sequence: 9 fullname: Caamano, Jorge H |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20237296$$D View this record in MEDLINE/PubMed |
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SubjectTerms | Animals B-Lymphocyte Subsets - cytology B-Lymphocyte Subsets - immunology B-Lymphocyte Subsets - metabolism Cell Differentiation - genetics Cell Differentiation - immunology Endothelium, Lymphatic - cytology Endothelium, Lymphatic - embryology Endothelium, Lymphatic - metabolism Immunophenotyping Lymph Nodes - cytology Lymph Nodes - embryology Lymph Nodes - immunology Lymph Nodes - metabolism Mesenchymal Stem Cells - cytology Mesenchymal Stem Cells - immunology Mesenchymal Stem Cells - metabolism Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout Organ Culture Techniques Stromal Cells - cytology Stromal Cells - immunology Stromal Cells - metabolism T-Lymphocyte Subsets - cytology T-Lymphocyte Subsets - immunology T-Lymphocyte Subsets - metabolism |
Title | Ontogeny of Stromal Organizer Cells during Lymph Node Development |
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