Foxp3+ CD25– CD4 T cells constitute a reservoir of committed regulatory cells that regain CD25 expression upon homeostatic expansion
Expression of the IL-2 receptor α chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used as a marker to identify regulatory T cells (T R ), although cells with regulatory properties are also found in the CD4 + CD25 – subset. By using...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 102; no. 11; pp. 4091 - 4096 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
National Acad Sciences
15.03.2005
National Academy of Sciences |
Subjects | |
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Abstract | Expression of the IL-2 receptor α chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used as a marker to identify regulatory T cells (T R ), although cells with regulatory properties are also found in the CD4 + CD25 – subset. By using in vivo functional assays and Foxp3 expression as a faithful marker of T R differentiation, we have evaluated the requirements for CD25 expression by peripheral T R . We first show that in vivo depletion of CD25 + cells prevents the development of spontaneous encephalomyelitis in recombination-activating gene (RAG)-deficient anti-myelin basic protein T cell antigen receptor (TCR) transgenic mice, and allows disease induction in otherwise healthy RAG-competent transgenic mice. Similar treatment in normal thymectomized animals is followed by the fast recovery of a normal number of CD25 + T R . Consistently, Foxp3-expressing T R encompassed in the CD25 – cell population convert to CD25 + after homeostatic expansion and are selectable by IL-2 in vitro . Surface expression of CD25 on T R is controlled by the activity of conventional CD4 cells and is fully labile because it can be lost and regained without affecting the functional potential of the cells. These findings reveal that Foxp3-expressing CD25 – cells constitute a peripheral reservoir of differentiated T R , recruited to the CD25 + pool upon homeostatic expansion and/or activation. This analysis, together with the notion that physiological commitment of T R takes place exclusively in the thymus should help for the interpretation of experiments assessing peripheral T R differentiation from naive CD4 T cells, defined as CD25 – . homeostasis mice T lymphocyte |
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AbstractList | Expression of the IL-2 receptor alpha chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used as a marker to identify regulatory T cells (T(R)), although cells with regulatory properties are also found in the CD4+CD25- subset. By using in vivo functional assays and Foxp3 expression as a faithful marker of T(R) differentiation, we have evaluated the requirements for CD25 expression by peripheral T(R). We first show that in vivo depletion of CD25+ cells prevents the development of spontaneous encephalomyelitis in recombination-activating gene (RAG)-deficient anti-myelin basic protein T cell antigen receptor (TCR) transgenic mice, and allows disease induction in otherwise healthy RAG-competent transgenic mice. Similar treatment in normal thymectomized animals is followed by the fast recovery of a normal number of CD25+ T(R). Consistently, Foxp3-expressing T(R) encompassed in the CD25- cell population convert to CD25+ after homeostatic expansion and are selectable by IL-2 in vitro. Surface expression of CD25 on T(R) is controlled by the activity of conventional CD4 cells and is fully labile because it can be lost and regained without affecting the functional potential of the cells. These findings reveal that Foxp3-expressing CD25- cells constitute a peripheral reservoir of differentiated T(R), recruited to the CD25+ pool upon homeostatic expansion and/or activation. This analysis, together with the notion that physiological commitment of T(R) takes place exclusively in the thymus should help for the interpretation of experiments assessing peripheral T(R) differentiation from naive CD4 T cells, defined as CD25-. Expression of the IL-2 receptor α chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used as a marker to identify regulatory T cells (T R ), although cells with regulatory properties are also found in the CD4 + CD25 – subset. By using in vivo functional assays and Foxp3 expression as a faithful marker of T R differentiation, we have evaluated the requirements for CD25 expression by peripheral T R . We first show that in vivo depletion of CD25 + cells prevents the development of spontaneous encephalomyelitis in recombination-activating gene (RAG)-deficient anti-myelin basic protein T cell antigen receptor (TCR) transgenic mice, and allows disease induction in otherwise healthy RAG-competent transgenic mice. Similar treatment in normal thymectomized animals is followed by the fast recovery of a normal number of CD25 + T R . Consistently, Foxp3-expressing T R encompassed in the CD25 – cell population convert to CD25 + after homeostatic expansion and are selectable by IL-2 in vitro . Surface expression of CD25 on T R is controlled by the activity of conventional CD4 cells and is fully labile because it can be lost and regained without affecting the functional potential of the cells. These findings reveal that Foxp3-expressing CD25 – cells constitute a peripheral reservoir of differentiated T R , recruited to the CD25 + pool upon homeostatic expansion and/or activation. This analysis, together with the notion that physiological commitment of T R takes place exclusively in the thymus should help for the interpretation of experiments assessing peripheral T R differentiation from naive CD4 T cells, defined as CD25 – . Expression of the IL-2 receptor α chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used as a marker to identify regulatory T cells (T R ), although cells with regulatory properties are also found in the CD4 + CD25 – subset. By using in vivo functional assays and Foxp3 expression as a faithful marker of T R differentiation, we have evaluated the requirements for CD25 expression by peripheral T R . We first show that in vivo depletion of CD25 + cells prevents the development of spontaneous encephalomyelitis in recombination-activating gene (RAG)-deficient anti-myelin basic protein T cell antigen receptor (TCR) transgenic mice, and allows disease induction in otherwise healthy RAG-competent transgenic mice. Similar treatment in normal thymectomized animals is followed by the fast recovery of a normal number of CD25 + T R . Consistently, Foxp3-expressing T R encompassed in the CD25 – cell population convert to CD25 + after homeostatic expansion and are selectable by IL-2 in vitro . Surface expression of CD25 on T R is controlled by the activity of conventional CD4 cells and is fully labile because it can be lost and regained without affecting the functional potential of the cells. These findings reveal that Foxp3-expressing CD25 – cells constitute a peripheral reservoir of differentiated T R , recruited to the CD25 + pool upon homeostatic expansion and/or activation. This analysis, together with the notion that physiological commitment of T R takes place exclusively in the thymus should help for the interpretation of experiments assessing peripheral T R differentiation from naive CD4 T cells, defined as CD25 – . homeostasis mice T lymphocyte Expression of the IL-2 receptor {alpha} chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used as a marker to identify regulatory T cells (TR), although cells with regulatory properties are also found in the CD4+CD25- subset. By using in vivo functional assays and Foxp3 expression as a faithful marker of TR differentiation, we have evaluated the requirements for CD25 expression by peripheral TR. We first show that in vivo depletion of CD25+ cells prevents the development of spontaneous encephalomyelitis in recombination-activating gene (RAG)-deficient anti-myelin basic protein T cell antigen receptor (TCR) transgenic mice, and allows disease induction in otherwise healthy RAG-competent transgenic mice. Similar treatment in normal thymectomized animals is followed by the fast recovery of a normal number of CD25+ TR. Consistently, Foxp3-expressing TR encompassed in the CD25- cell population convert to CD25+ after homeostatic expansion and are selectable by IL-2 in vitro. Surface expression of CD25 on TR is controlled by the activity of conventional CD4 cells and is fully labile because it can be lost and regained without affecting the functional potential of the cells. These findings reveal that Foxp3-expressing CD25- cells constitute a peripheral reservoir of differentiated TR, recruited to the CD25+ pool upon homeostatic expansion and/or activation. This analysis, together with the notion that physiological commitment of TR takes place exclusively in the thymus should help for the interpretation of experiments assessing peripheral TR differentiation from naive CD4 T cells, defined as CD25-. [PUBLICATION ABSTRACT] |
Author | Manuel Rebelo Maria Francisca Moraes-Fontes Iris Caramalho Santiago Zelenay Thiago Lopes-Carvalho Jocelyne Demengeot |
AuthorAffiliation | Instituto Gulbenkian de Ciência, Apartado 14, PT-2781-901 Oeiras, Portugal |
AuthorAffiliation_xml | – name: Instituto Gulbenkian de Ciência, Apartado 14, PT-2781-901 Oeiras, Portugal |
Author_xml | – sequence: 1 givenname: Santiago surname: Zelenay fullname: Zelenay, Santiago organization: Instituto Gulbenkian de Ciência, Apartado 14, PT-2781-901 Oeiras, Portugal – sequence: 2 givenname: Thiago surname: Lopes-Carvalho fullname: Lopes-Carvalho, Thiago – sequence: 3 givenname: Iris surname: Caramalho fullname: Caramalho, Iris – sequence: 4 givenname: Maria Francisca surname: Moraes-Fontes fullname: Moraes-Fontes, Maria Francisca – sequence: 5 givenname: Manuel surname: Rebelo fullname: Rebelo, Manuel – sequence: 6 givenname: Jocelyne surname: Demengeot fullname: Demengeot, Jocelyne |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/15753306$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 To whom correspondence should be addressed. E-mail: jocelyne@igc.gulbenkian.pt. Communicated by N. M. Le Douarin, Académie des Sciences de l'Institut de France, Paris, France, February 3, 2005 Present address: Department of Microbiology, University of Alabama at Birmingham, Birmingham, AL 35294. Author contributions: S.Z., T.L.-C., I.C., and J.D. designed research; S.Z., T.L.-C., I.C., M.F.M.-F., M.R., and J.D. performed research; S.Z., T.L.-C., I.C., M.F.M.-F., and J.D. analyzed data; and S.Z., T.L.-C., and J.D. wrote the paper. Abbreviations: TR, regulatory T cells; RAG, recombination-activating gene; TCR, T cell antigen receptor; T/R– and T/R+, anti-myelin basic protein TCR transgenic mice homo- and heterozygous for a null mutation of the RAG-1 gene; Tx, thymectomized; EAE, experimental autoimmune encephalomyelitis; LN, lymph node; PE, phycoerythrin. |
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Snippet | Expression of the IL-2 receptor α chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used as a... Expression of the IL-2 receptor alpha chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely used... Expression of the IL-2 receptor {alpha} chain (CD25) by peripheral CD4 T cells follows cellular activation. However, CD25 expression by CD4 cells is widely... |
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SubjectTerms | Animals Antibodies, Monoclonal - immunology Biological Sciences CD4-Positive T-Lymphocytes - cytology CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism Cell Division - immunology DNA-Binding Proteins - genetics DNA-Binding Proteins - immunology DNA-Binding Proteins - metabolism Forkhead Transcription Factors Gene expression Homeostasis - immunology Immunology Mice Mice, Inbred BALB C Mice, Inbred C57BL Receptors, Interleukin-2 - immunology T cell receptors Transgenic animals |
Title | Foxp3+ CD25– CD4 T cells constitute a reservoir of committed regulatory cells that regain CD25 expression upon homeostatic expansion |
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