Rank Signaling Links the Development of Invariant γδ T Cell Progenitors and Aire+ Medullary Epithelium
The thymic medulla provides a specialized microenvironment for the negative selection of T cells, with the presence of autoimmune regulator (Aire)-expressing medullary thymic epithelial cells (mTECs) during the embryonic-neonatal period being both necessary and sufficient to establish long-lasting t...
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| Published in | Immunity (Cambridge, Mass.) Vol. 36; no. 3; pp. 427 - 437 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
23.03.2012
Cell Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The thymic medulla provides a specialized microenvironment for the negative selection of T cells, with the presence of autoimmune regulator (Aire)-expressing medullary thymic epithelial cells (mTECs) during the embryonic-neonatal period being both necessary and sufficient to establish long-lasting tolerance. Here we showed that emergence of the first cohorts of Aire+ mTECs at this key developmental stage, prior to αβ T cell repertoire selection, was jointly directed by Rankl+ lymphoid tissue inducer cells and invariant Vγ5+ dendritic epidermal T cell (DETC) progenitors that are the first thymocytes to express the products of gene rearrangement. In turn, generation of Aire+ mTECs then fostered Skint-1-dependent, but Aire-independent, DETC progenitor maturation and the emergence of an invariant DETC repertoire. Hence, our data attributed a functional importance to the temporal development of Vγ5+ γδ T cells during thymus medulla formation for αβ T cell tolerance induction and demonstrated a Rank-mediated reciprocal link between DETC and Aire+ mTEC maturation.
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► Invariant Vγ5+ thymocytes regulate formation of Aire+ medullary thymic epithelium ► Generation of an invariant Vγ5+ T cell population requires thymus medulla development ► Skint-1-mediated Vγ5+ thymocyte development is Aire independent ► Dependency on Tnfrsf11a links γδ T cell and medullary epithelium development |
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| AbstractList | The thymic medulla provides a specialized microenvironment for the negative selection of T cells, with the presence of autoimmune regulator (Aire)-expressing medullary thymic epithelial cells (mTECs) during the embryonic-neonatal period being both necessary and sufficient to establish long-lasting tolerance. Here we showed that emergence of the first cohorts of Aire(+) mTECs at this key developmental stage, prior to αβ T cell repertoire selection, was jointly directed by Rankl(+) lymphoid tissue inducer cells and invariant Vγ5(+) dendritic epidermal T cell (DETC) progenitors that are the first thymocytes to express the products of gene rearrangement. In turn, generation of Aire(+) mTECs then fostered Skint-1-dependent, but Aire-independent, DETC progenitor maturation and the emergence of an invariant DETC repertoire. Hence, our data attributed a functional importance to the temporal development of Vγ5(+) γδ T cells during thymus medulla formation for αβ T cell tolerance induction and demonstrated a Rank-mediated reciprocal link between DETC and Aire(+) mTEC maturation. The thymic medulla provides a specialized microenvironment for the negative selection of T cells, with the presence of autoimmune regulator (Aire)-expressing medullary thymic epithelial cells (mTECs) during the embryonic-neonatal period being both necessary and sufficient to establish long-lasting tolerance. Here we showed that emergence of the first cohorts of Aire+ mTECs at this key developmental stage, prior to αβ T cell repertoire selection, was jointly directed by Rankl+ lymphoid tissue inducer cells and invariant Vγ5+ dendritic epidermal T cell (DETC) progenitors that are the first thymocytes to express the products of gene rearrangement. In turn, generation of Aire+ mTECs then fostered Skint-1-dependent, but Aire-independent, DETC progenitor maturation and the emergence of an invariant DETC repertoire. Hence, our data attributed a functional importance to the temporal development of Vγ5+ γδ T cells during thymus medulla formation for αβ T cell tolerance induction and demonstrated a Rank-mediated reciprocal link between DETC and Aire+ mTEC maturation. [Display omitted] ► Invariant Vγ5+ thymocytes regulate formation of Aire+ medullary thymic epithelium ► Generation of an invariant Vγ5+ T cell population requires thymus medulla development ► Skint-1-mediated Vγ5+ thymocyte development is Aire independent ► Dependency on Tnfrsf11a links γδ T cell and medullary epithelium development The thymic medulla provides a specialized microenvironment for the negative selection of T cells, with the presence of autoimmune regulator (Aire)-expressing medullary thymic epithelial cells (mTECs) during the embryonic-neonatal period being both necessary and sufficient to establish long-lasting tolerance. Here we showed that emergence of the first cohorts of Aire + mTECs at this key developmental stage, prior to αβ T cell repertoire selection, was jointly directed by Rankl + lymphoid tissue inducer cells and invariant Vγ5 + dendritic epidermal T cell (DETC) progenitors that are the first thymocytes to express the products of gene rearrangement. In turn, generation of Aire + mTECs then fostered Skint-1-dependent, but Aire-independent, DETC progenitor maturation and the emergence of an invariant DETC repertoire. Hence, our data attributed a functional importance to the temporal development of Vγ5 + γδ T cells during thymus medulla formation for αβ T cell tolerance induction and demonstrated a Rank-mediated reciprocal link between DETC and Aire + mTEC maturation. |
| Author | Nitta, Takeshi Ohigashi, Izumi Lane, Peter J.L. Turchinovich, Gleb Hayday, Adrian C. White, Andrea J. Jenkinson, Eric J. Roberts, Natalie A. Nakamura, Kyoko Parnell, Sonia M. Caamano, Jorge H. Paolino, Magdalena Desanti, Guillaume E. Benezech, Cecile Jenkinson, William E. Simon, Anna Katharina Anderson, Graham Takahama, Yousuke Withers, David R. Cunningham, Adam F. Penninger, Josef M. McConnell, Fiona M. |
| AuthorAffiliation | 1 MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK 5 Human Immunology Unit, Nuffield Department of Medicine, University of Oxford, Oxford, OX3 9DS, UK 4 IMBA, Institute of Biotechnology of the Austrian Academy of Sciences, 1030 Vienna, Austria 6 Division of Experimental Immunology, Institute for Genome Research, University of Tokushima, Tokushima 770-8503, Japan 2 London Research Institute, Cancer Research UK, London, WC2A 3LY, UK 3 Peter Gorer Department of Immunobiology, Kings College at Guy's Hospital, London, SE1 9RT, UK |
| AuthorAffiliation_xml | – name: 6 Division of Experimental Immunology, Institute for Genome Research, University of Tokushima, Tokushima 770-8503, Japan – name: 4 IMBA, Institute of Biotechnology of the Austrian Academy of Sciences, 1030 Vienna, Austria – name: 1 MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – name: 5 Human Immunology Unit, Nuffield Department of Medicine, University of Oxford, Oxford, OX3 9DS, UK – name: 2 London Research Institute, Cancer Research UK, London, WC2A 3LY, UK – name: 3 Peter Gorer Department of Immunobiology, Kings College at Guy's Hospital, London, SE1 9RT, UK |
| Author_xml | – sequence: 1 givenname: Natalie A. surname: Roberts fullname: Roberts, Natalie A. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 2 givenname: Andrea J. surname: White fullname: White, Andrea J. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 3 givenname: William E. surname: Jenkinson fullname: Jenkinson, William E. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 4 givenname: Gleb surname: Turchinovich fullname: Turchinovich, Gleb organization: London Research Institute, Cancer Research UK, London, WC2A 3LY, UK – sequence: 5 givenname: Kyoko surname: Nakamura fullname: Nakamura, Kyoko organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 6 givenname: David R. surname: Withers fullname: Withers, David R. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 7 givenname: Fiona M. surname: McConnell fullname: McConnell, Fiona M. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 8 givenname: Guillaume E. surname: Desanti fullname: Desanti, Guillaume E. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 9 givenname: Cecile surname: Benezech fullname: Benezech, Cecile organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 10 givenname: Sonia M. surname: Parnell fullname: Parnell, Sonia M. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 11 givenname: Adam F. surname: Cunningham fullname: Cunningham, Adam F. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 12 givenname: Magdalena surname: Paolino fullname: Paolino, Magdalena organization: IMBA, Institute of Biotechnology of the Austrian Academy of Sciences, 1030 Vienna, Austria – sequence: 13 givenname: Josef M. surname: Penninger fullname: Penninger, Josef M. organization: IMBA, Institute of Biotechnology of the Austrian Academy of Sciences, 1030 Vienna, Austria – sequence: 14 givenname: Anna Katharina surname: Simon fullname: Simon, Anna Katharina organization: Human Immunology Unit, Nuffield Department of Medicine, University of Oxford, Oxford, OX3 9DS, UK – sequence: 15 givenname: Takeshi surname: Nitta fullname: Nitta, Takeshi organization: Division of Experimental Immunology, Institute for Genome Research, University of Tokushima, Tokushima 770-8503, Japan – sequence: 16 givenname: Izumi surname: Ohigashi fullname: Ohigashi, Izumi organization: Division of Experimental Immunology, Institute for Genome Research, University of Tokushima, Tokushima 770-8503, Japan – sequence: 17 givenname: Yousuke surname: Takahama fullname: Takahama, Yousuke organization: Division of Experimental Immunology, Institute for Genome Research, University of Tokushima, Tokushima 770-8503, Japan – sequence: 18 givenname: Jorge H. surname: Caamano fullname: Caamano, Jorge H. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 19 givenname: Adrian C. surname: Hayday fullname: Hayday, Adrian C. organization: London Research Institute, Cancer Research UK, London, WC2A 3LY, UK – sequence: 20 givenname: Peter J.L. surname: Lane fullname: Lane, Peter J.L. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 21 givenname: Eric J. surname: Jenkinson fullname: Jenkinson, Eric J. organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK – sequence: 22 givenname: Graham surname: Anderson fullname: Anderson, Graham email: g.anderson@bham.ac.uk organization: MRC Centre for Immune Regulation, University of Birmingham, Birmingham, B15 2TT, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22425250$$D View this record in MEDLINE/PubMed http://kipublications.ki.se/Default.aspx?queryparsed=id:124339631$$DView record from Swedish Publication Index |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work Present address: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520, USA |
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| SubjectTerms | AIRE Protein Animals Cell Differentiation - immunology Cellular Microenvironment Epithelial Cells - immunology Female Fetus - cytology Fetus - immunology Male Medicin och hälsovetenskap Mice Mice, Inbred C57BL Mice, Knockout Precursor Cells, T-Lymphoid - cytology Precursor Cells, T-Lymphoid - immunology Pregnancy Receptor Activator of Nuclear Factor-kappa B - immunology Receptors, Antigen, T-Cell, gamma-delta - metabolism Signal Transduction - immunology Thymus Gland - cytology Thymus Gland - immunology Transcription Factors - deficiency Transcription Factors - genetics Transcription Factors - immunology |
| Title | Rank Signaling Links the Development of Invariant γδ T Cell Progenitors and Aire+ Medullary Epithelium |
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