Stability and function of regulatory T cells is maintained by a neuropilin-1–semaphorin-4a axis

Neuropilin-1 (Nrp1) on regulatory T (T reg ) cells is shown to interact with semaphorin-4a (Sema4a) to promote a program of T reg -cell stability and survival, in part through PTEN-mediated modulation of Akt signalling; Nrp1-deficient T reg cells can maintain immune homeostasis but fail to suppress...

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Published inNature (London) Vol. 501; no. 7466; pp. 252 - 256
Main Authors Delgoffe, Greg M., Woo, Seng-Ryong, Turnis, Meghan E., Gravano, David M., Guy, Cliff, Overacre, Abigail E., Bettini, Matthew L., Vogel, Peter, Finkelstein, David, Bonnevier, Jody, Workman, Creg J., Vignali, Dario A. A.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 12.09.2013
Nature Publishing Group
Subjects
631/250/1619/554/1898/1271
Animals
Autoimmune diseases
Autoimmunity - immunology
Cell adhesion & migration
Cell Survival
Colitis - immunology
Female
Forkhead Box Protein O3
Forkhead Transcription Factors - metabolism
HEK293 Cells
Homeostasis
Homeostasis - immunology
Humanities and Social Sciences
Humans
Immune system
Immune Tolerance - immunology
Immunological Synapses
Immunology
Immunosuppression
Kinases
Laboratory animals
letter
Lymphocytes
Lymphocytes, Tumor-Infiltrating - cytology
Lymphocytes, Tumor-Infiltrating - immunology
Lymphocytes, Tumor-Infiltrating - metabolism
Male
Melanoma
Mice
Mice, Inbred C57BL
multidisciplinary
Neoplasms - genetics
Neoplasms - immunology
Neoplasms - pathology
Neuropilin-1 - deficiency
Neuropilin-1 - metabolism
Phosphorylation
Physiological aspects
Properties
Proteins
Proto-Oncogene Proteins c-akt - metabolism
PTEN Phosphohydrolase - metabolism
Rodents
Science
Semaphorins
Semaphorins - metabolism
Signal Transduction
T cells
T-Lymphocytes, Regulatory - cytology
T-Lymphocytes, Regulatory - immunology
T-Lymphocytes, Regulatory - metabolism
TOR Serine-Threonine Kinases - metabolism
Vascular endothelial growth factor
United States
Online AccessGet full text

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Abstract Neuropilin-1 (Nrp1) on regulatory T (T reg ) cells is shown to interact with semaphorin-4a (Sema4a) to promote a program of T reg -cell stability and survival, in part through PTEN-mediated modulation of Akt signalling; Nrp1-deficient T reg cells can maintain immune homeostasis but fail to suppress in inflammatory sites, such as tumours, providing an attractive immunotherapeutic target for the treatment of cancers. Anti-tumour versus pro-immunity effects of T reg cells Regulatory T cells (T reg ) constitute a barrier to effective anti-tumour immunity. Their depletion can induce reduction and clearance of many tumours, but as the cells perform an important balancing role in the immune system, depletion also results in unchecked autoimmunity and death. This paper describes an interaction between semaphorin-4a — an activator for T-cell-mediated immunity — and the neuropilin receptor Nrp1 on T reg cells that is required for T reg cells to limit anti-tumour immune responses and to cure established inflammatory colitis, but is dispensable for suppression of autoimmunity and maintenance of immune homeostasis. It remains to be determined whether it is feasible to limit tumour growth by targeting T reg cells without unleashing autoimmunity. The two biological activities may be inseparable, but this work points to ways in which this important system can be further characterized. Regulatory T cells (T reg cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune homeostasis 1 . However, they also represent a major barrier to effective anti-tumour immunity and sterilizing immunity to chronic viral infections 1 . The transcription factor Foxp3 has a major role in the development and programming of T reg cells 2 , 3 . The relative stability of T reg cells at inflammatory disease sites has been a highly contentious subject 4 , 5 , 6 . There is considerable interest in identifying pathways that control the stability of T reg cells as many immune-mediated diseases are characterized by either exacerbated or limited T reg -cell function. Here we show that the immune-cell-expressed ligand semaphorin-4a (Sema4a) and the T reg -cell-expressed receptor neuropilin-1 (Nrp1) interact both in vitro , to potentiate T reg -cell function and survival, and in vivo , at inflammatory sites. Using mice with a T reg -cell-restricted deletion of Nrp1, we show that Nrp1 is dispensable for suppression of autoimmunity and maintenance of immune homeostasis, but is required by T reg cells to limit anti-tumour immune responses and to cure established inflammatory colitis. Sema4a ligation of Nrp1 restrained Akt phosphorylation cellularly and at the immunologic synapse by phosphatase and tensin homologue (PTEN), which increased nuclear localization of the transcription factor Foxo3a. The Nrp1-induced transcriptome promoted T reg -cell stability by enhancing quiescence and survival factors while inhibiting programs that promote differentiation. Importantly, this Nrp1-dependent molecular program is evident in intra-tumoral T reg cells. Our data support a model in which T reg -cell stability can be subverted in certain inflammatory sites, but is maintained by a Sema4a–Nrp1 axis, highlighting this pathway as a potential therapeutic target that could limit T reg -cell-mediated tumour-induced tolerance without inducing autoimmunity.
AbstractList Regulatory T cells ([T.sub.reg] cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune homeostasis (1). However, they also represent a major barrier to effective anti-tumour immunity and sterilizing immunity to chronic viral infections1. The transcription factor Foxp3 has a major role in the development and programming of [T.sub.reg] cells (2,3). The relative stability of [T.sub.reg] cells at inflammatory disease sites has been a highly contentious subject (4-6). There is considerable interest in identifying pathways that control the stability of [T.sub.reg] cells as many immune-mediated diseases are characterized by either exacerbated or limited [T.sub.reg]-cell function. Here we show that the immune-cell-expressed ligand semaphorin-4a (Sema4a) and the [T.sub.reg]-cell-expressed receptor neuropilin-1 (Nrp1) interact both in vitro, to potentiate [T.sub.reg]-cell function and survival, and in vivo, at inflammatory sites. Using mice with a [T.sub.reg]-cell-restricted deletion of Nrp1, we show that Nrp1 is dispensable for suppression of autoimmunity and maintenance of immune homeostasis, but is required by [T.sub.reg] cells to limit anti-tumour immune responses and to cure established inflammatory colitis. Sema4a ligation of Nrp1 restrained Akt phosphorylation cellularly and at the immunologic synapse by phosphatase and tensin homologue (PTEN), which increased nuclear localization of the transcription factor Foxo3a. The Nrp1-induced transcriptome promoted [T.sub.reg]-cell stability by enhancing quiescence and survival factors while inhibiting programs that promote differentiation. Importantly, this Nrp1-dependent molecular program is evident in intra-tumoral [T.sub.reg] cells. Our data support a model in which [T.sub.reg]-cell stability can be subverted in certain inflammatory sites, but is maintained by a Sema4a-Nrp1 axis, highlighting this pathway as a potential therapeutic target that could limit [T.sub.reg]-cell-mediated tumour-induced tolerance without inducing autoimmunity.
Regulatory T cells (Treg cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune homeostasis. However, they also represent a major barrier to effective anti-tumour immunity and sterilizing immunity to chronic viral infections. The transcription factor Foxp3 has a major role in the development and programming of Treg cells. The relative stability of Treg cells at inflammatory disease sites has been a highly contentious subject. There is considerable interest in identifying pathways that control the stability of Treg cells as many immune-mediated diseases are characterized by either exacerbated or limited Treg-cell function. Here we show that the immune-cell-expressed ligand semaphorin-4a (Sema4a) and the Treg-cell-expressed receptor neuropilin-1 (Nrp1) interact both in vitro, to potentiate Treg-cell function and survival, and in vivo, at inflammatory sites. Using mice with a Treg-cell-restricted deletion of Nrp1, we show that Nrp1 is dispensable for suppression of autoimmunity and maintenance of immune homeostasis, but is required by Treg cells to limit anti-tumour immune responses and to cure established inflammatory colitis. Sema4a ligation of Nrp1 restrained Akt phosphorylation cellularly and at the immunologic synapse by phosphatase and tensin homologue (PTEN), which increased nuclear localization of the transcription factor Foxo3a. The Nrp1-induced transcriptome promoted Treg-cell stability by enhancing quiescence and survival factors while inhibiting programs that promote differentiation. Importantly, this Nrp1-dependent molecular program is evident in intra-tumoral Treg cells. Our data support a model in which Treg-cell stability can be subverted in certain inflammatory sites, but is maintained by a Sema4a-Nrp1 axis, highlighting this pathway as a potential therapeutic target that could limit Treg-cell-mediated tumour-induced tolerance without inducing autoimmunity.Regulatory T cells (Treg cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune homeostasis. However, they also represent a major barrier to effective anti-tumour immunity and sterilizing immunity to chronic viral infections. The transcription factor Foxp3 has a major role in the development and programming of Treg cells. The relative stability of Treg cells at inflammatory disease sites has been a highly contentious subject. There is considerable interest in identifying pathways that control the stability of Treg cells as many immune-mediated diseases are characterized by either exacerbated or limited Treg-cell function. Here we show that the immune-cell-expressed ligand semaphorin-4a (Sema4a) and the Treg-cell-expressed receptor neuropilin-1 (Nrp1) interact both in vitro, to potentiate Treg-cell function and survival, and in vivo, at inflammatory sites. Using mice with a Treg-cell-restricted deletion of Nrp1, we show that Nrp1 is dispensable for suppression of autoimmunity and maintenance of immune homeostasis, but is required by Treg cells to limit anti-tumour immune responses and to cure established inflammatory colitis. Sema4a ligation of Nrp1 restrained Akt phosphorylation cellularly and at the immunologic synapse by phosphatase and tensin homologue (PTEN), which increased nuclear localization of the transcription factor Foxo3a. The Nrp1-induced transcriptome promoted Treg-cell stability by enhancing quiescence and survival factors while inhibiting programs that promote differentiation. Importantly, this Nrp1-dependent molecular program is evident in intra-tumoral Treg cells. Our data support a model in which Treg-cell stability can be subverted in certain inflammatory sites, but is maintained by a Sema4a-Nrp1 axis, highlighting this pathway as a potential therapeutic target that could limit Treg-cell-mediated tumour-induced tolerance without inducing autoimmunity.
Regulatory T cells (T^sub reg^ cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune homeostasis. However, they also represent a major barrier to effective anti-tumour immunity and sterilizing immunity to chronic viral infections. The transcription factor Foxp3 has a major role in the development and programming of T^sub reg^ cells. The relative stability of T^sub reg^a highly contentious cells at inflammatory disease sites has been a highly contentious subject. There is considerable interest in identifying pathways that control the stability of T^sub reg^ cells as many immune-mediated diseases are characterized by either exacerbated or limited T^sub reg^-cell function. Here we show that the immune-cell-expressed ligand semaphorin-4a (Sema4a) and the T^sub reg^-cell-expressed receptor neuropilin-1 (Nrp1) interact both invitro, to potentiate T^sub reg^-cell function and survival, and invivo,at inflammatory sites. Using mice with a T^sub reg^-cell-restricted deletion of Nrp1, we show that Nrp1 is dispensable for suppression of auto-immunity and maintenance of immune homeostasis, but is required by T^sub reg^ cells to limit anti-tumour immune responses and to cure established inflammatorycolitis. Sema4a ligation ofNrp1 restrained Akt phosphorylation cellularly and at the immunologic synapse by phosphatase and tensin homologue (PTEN), which increased nuclear localization of the transcription factor Foxo3a. The Nrp1- induced transcriptome promoted T^sub reg^-cell stability by enhancing quiescence and survival factors while inhibiting programs that promote differentiation. Importantly, this Nrp1-dependent molecular program is evident in intra-tumoral T^sub reg^ cells. Our data support a model in which T^sub reg^-cell stability can be subverted in certain inflammatory sites, but is maintained by a Sema4a-Nrp1 axis, highlighting this pathway as a potential therapeutic target that could limit T^sub reg^-cell-mediated tumour-induced tolerance without inducing autoimmunity. [PUBLICATION ABSTRACT]
Regulatory T cells (Treg cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune homeostasis. However, they also represent a major barrier to effective anti-tumour immunity and sterilizing immunity to chronic viral infections. The transcription factor Foxp3 has a major role in the development and programming of Treg cells. The relative stability of Treg cells at inflammatory disease sites has been a highly contentious subject. There is considerable interest in identifying pathways that control the stability of Treg cells as many immune-mediated diseases are characterized by either exacerbated or limited Treg-cell function. Here we show that the immune-cell-expressed ligand semaphorin-4a (Sema4a) and the Treg-cell-expressed receptor neuropilin-1 (Nrp1) interact both in vitro, to potentiate Treg-cell function and survival, and in vivo, at inflammatory sites. Using mice with a Treg-cell-restricted deletion of Nrp1, we show that Nrp1 is dispensable for suppression of autoimmunity and maintenance of immune homeostasis, but is required by Treg cells to limit anti-tumour immune responses and to cure established inflammatory colitis. Sema4a ligation of Nrp1 restrained Akt phosphorylation cellularly and at the immunologic synapse by phosphatase and tensin homologue (PTEN), which increased nuclear localization of the transcription factor Foxo3a. The Nrp1-induced transcriptome promoted Treg-cell stability by enhancing quiescence and survival factors while inhibiting programs that promote differentiation. Importantly, this Nrp1-dependent molecular program is evident in intra-tumoral Treg cells. Our data support a model in which Treg-cell stability can be subverted in certain inflammatory sites, but is maintained by a Sema4a-Nrp1 axis, highlighting this pathway as a potential therapeutic target that could limit Treg-cell-mediated tumour-induced tolerance without inducing autoimmunity.
Neuropilin-1 (Nrp1) on regulatory T (T reg ) cells is shown to interact with semaphorin-4a (Sema4a) to promote a program of T reg -cell stability and survival, in part through PTEN-mediated modulation of Akt signalling; Nrp1-deficient T reg cells can maintain immune homeostasis but fail to suppress in inflammatory sites, such as tumours, providing an attractive immunotherapeutic target for the treatment of cancers. Anti-tumour versus pro-immunity effects of T reg cells Regulatory T cells (T reg ) constitute a barrier to effective anti-tumour immunity. Their depletion can induce reduction and clearance of many tumours, but as the cells perform an important balancing role in the immune system, depletion also results in unchecked autoimmunity and death. This paper describes an interaction between semaphorin-4a — an activator for T-cell-mediated immunity — and the neuropilin receptor Nrp1 on T reg cells that is required for T reg cells to limit anti-tumour immune responses and to cure established inflammatory colitis, but is dispensable for suppression of autoimmunity and maintenance of immune homeostasis. It remains to be determined whether it is feasible to limit tumour growth by targeting T reg cells without unleashing autoimmunity. The two biological activities may be inseparable, but this work points to ways in which this important system can be further characterized. Regulatory T cells (T reg cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune homeostasis 1 . However, they also represent a major barrier to effective anti-tumour immunity and sterilizing immunity to chronic viral infections 1 . The transcription factor Foxp3 has a major role in the development and programming of T reg cells 2 , 3 . The relative stability of T reg cells at inflammatory disease sites has been a highly contentious subject 4 , 5 , 6 . There is considerable interest in identifying pathways that control the stability of T reg cells as many immune-mediated diseases are characterized by either exacerbated or limited T reg -cell function. Here we show that the immune-cell-expressed ligand semaphorin-4a (Sema4a) and the T reg -cell-expressed receptor neuropilin-1 (Nrp1) interact both in vitro , to potentiate T reg -cell function and survival, and in vivo , at inflammatory sites. Using mice with a T reg -cell-restricted deletion of Nrp1, we show that Nrp1 is dispensable for suppression of autoimmunity and maintenance of immune homeostasis, but is required by T reg cells to limit anti-tumour immune responses and to cure established inflammatory colitis. Sema4a ligation of Nrp1 restrained Akt phosphorylation cellularly and at the immunologic synapse by phosphatase and tensin homologue (PTEN), which increased nuclear localization of the transcription factor Foxo3a. The Nrp1-induced transcriptome promoted T reg -cell stability by enhancing quiescence and survival factors while inhibiting programs that promote differentiation. Importantly, this Nrp1-dependent molecular program is evident in intra-tumoral T reg cells. Our data support a model in which T reg -cell stability can be subverted in certain inflammatory sites, but is maintained by a Sema4a–Nrp1 axis, highlighting this pathway as a potential therapeutic target that could limit T reg -cell-mediated tumour-induced tolerance without inducing autoimmunity.
Audience Academic
Author Finkelstein, David
Workman, Creg J.
Guy, Cliff
Bettini, Matthew L.
Overacre, Abigail E.
Vignali, Dario A. A.
Vogel, Peter
Turnis, Meghan E.
Woo, Seng-Ryong
Bonnevier, Jody
Delgoffe, Greg M.
Gravano, David M.
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  givenname: Greg M.
  surname: Delgoffe
  fullname: Delgoffe, Greg M.
  organization: Department of Immunology, St Jude Children's Research Hospital
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  givenname: Seng-Ryong
  surname: Woo
  fullname: Woo, Seng-Ryong
  organization: Department of Immunology, St Jude Children's Research Hospital
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  givenname: Meghan E.
  surname: Turnis
  fullname: Turnis, Meghan E.
  organization: Department of Immunology, St Jude Children's Research Hospital
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  givenname: David M.
  surname: Gravano
  fullname: Gravano, David M.
  organization: Department of Immunology, St Jude Children's Research Hospital
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  givenname: Cliff
  surname: Guy
  fullname: Guy, Cliff
  organization: Department of Immunology, St Jude Children's Research Hospital
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  givenname: Abigail E.
  surname: Overacre
  fullname: Overacre, Abigail E.
  organization: Department of Immunology, St Jude Children's Research Hospital, Integrated Biomedical Sciences Program, University of Tennessee Health Science Center
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  givenname: Matthew L.
  surname: Bettini
  fullname: Bettini, Matthew L.
  organization: Department of Immunology, St Jude Children's Research Hospital
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  surname: Vogel
  fullname: Vogel, Peter
  organization: Department of Pathology, St Jude Children's Research Hospital
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  surname: Finkelstein
  fullname: Finkelstein, David
  organization: Computational Biology, St Jude Children's Research Hospital
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  surname: Bonnevier
  fullname: Bonnevier, Jody
  organization: R&D Systems Inc
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  givenname: Creg J.
  surname: Workman
  fullname: Workman, Creg J.
  organization: Department of Immunology, St Jude Children's Research Hospital
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  givenname: Dario A. A.
  surname: Vignali
  fullname: Vignali, Dario A. A.
  email: vignali.lab@stjude.org
  organization: Department of Immunology, St Jude Children's Research Hospital
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23913274$$D View this record in MEDLINE/PubMed
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COPYRIGHT 2013 Nature Publishing Group
Copyright Nature Publishing Group Sep 12, 2013
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Snippet Neuropilin-1 (Nrp1) on regulatory T (T reg ) cells is shown to interact with semaphorin-4a (Sema4a) to promote a program of T reg -cell stability and survival,...
Regulatory T cells (Treg cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune...
Regulatory T cells ([T.sub.reg] cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune...
Regulatory T cells (T^sub reg^ cells) have a crucial role in the immune system by preventing autoimmunity, limiting immunopathology, and maintaining immune...
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StartPage 252
SubjectTerms 631/250/1619/554/1898/1271
Animals
Autoimmune diseases
Autoimmunity - immunology
Cell adhesion & migration
Cell Survival
Colitis - immunology
Female
Forkhead Box Protein O3
Forkhead Transcription Factors - metabolism
HEK293 Cells
Homeostasis
Homeostasis - immunology
Humanities and Social Sciences
Humans
Immune system
Immune Tolerance - immunology
Immunological Synapses
Immunology
Immunosuppression
Kinases
Laboratory animals
letter
Lymphocytes
Lymphocytes, Tumor-Infiltrating - cytology
Lymphocytes, Tumor-Infiltrating - immunology
Lymphocytes, Tumor-Infiltrating - metabolism
Male
Melanoma
Mice
Mice, Inbred C57BL
multidisciplinary
Neoplasms - genetics
Neoplasms - immunology
Neoplasms - pathology
Neuropilin-1 - deficiency
Neuropilin-1 - metabolism
Phosphorylation
Physiological aspects
Properties
Proteins
Proto-Oncogene Proteins c-akt - metabolism
PTEN Phosphohydrolase - metabolism
Rodents
Science
Semaphorins
Semaphorins - metabolism
Signal Transduction
T cells
T-Lymphocytes, Regulatory - cytology
T-Lymphocytes, Regulatory - immunology
T-Lymphocytes, Regulatory - metabolism
TOR Serine-Threonine Kinases - metabolism
Vascular endothelial growth factor
Title Stability and function of regulatory T cells is maintained by a neuropilin-1–semaphorin-4a axis
URI https://link.springer.com/article/10.1038/nature12428
https://www.ncbi.nlm.nih.gov/pubmed/23913274
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https://www.proquest.com/docview/1432616878
Volume 501
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