Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes

Tissue-resident memory T (Trm) cells permanently localize to portals of pathogen entry, where they provide immediate protection against reinfection. To enforce tissue retention, Trm cells up-regulate CD69 and down-regulate molecules associated with tissue egress; however, a Trm-specific transcriptio...

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Published in	Science (American Association for the Advancement of Science) Vol. 352; no. 6284; pp. 459 - 463
Main Authors	Mackay, Laura K., Minnich, Martina, Kragten, Natasja A. M., Liao, Yang, Nota, Benjamin, Seillet, Cyril, Zaid, Ali, Man, Kevin, Preston, Simon, Freestone, David, Braun, Asolina, Wynne-Jones, Erica, Behr, Felix M., Stark, Regina, Pellicci, Daniel G., Godfrey, Dale I., Belz, Gabrielle T., Pellegrini, Marc, Gebhardt, Thomas, Busslinger, Meinrad, Shi, Wei, Carbone, Francis R., van Lier, René A. W., Kallies, Axel, van Gisbergen, Klaas P. J. M.
Format	Journal Article
Language	English
Published	United States American Association for the Advancement of Science 22.04.2016 The American Association for the Advancement of Science
Subjects	Animals Cellular biology Gastrointestinal Tract - immunology Gene Expression Regulation Genes, Regulator - genetics Genes, Regulator - physiology Immune system Immunologic Memory - genetics Kidney - immunology Killer Cells, Natural - immunology Liver - immunology Lymphocyte Activation Lymphocytes Mice Mice, Knockout Natural Killer T-Cells - immunology Pathogens Positive Regulatory Domain I-Binding Factor 1 Retention Skin - immunology Tissues Transcription Factors - genetics Transcription Factors - physiology Transcription, Genetic Up-Regulation
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Abstract	Tissue-resident memory T (Trm) cells permanently localize to portals of pathogen entry, where they provide immediate protection against reinfection. To enforce tissue retention, Trm cells up-regulate CD69 and down-regulate molecules associated with tissue egress; however, a Trm-specific transcriptional regulator has not been identified. Here, we show that the transcription factor Hobit is specifically up-regulated in Trm cells and, together with related Blimp1, mediates the development of Trm cells in skin, gut, liver, and kidney in mice. The Hobit-Blimp1 transcriptional module is also required for other populations of tissue-resident lymphocytes, including natural killer T (NKT) cells and liver-resident NK cells, all of which share a common transcriptional program. Our results identify Hobit and Blimp1 as central regulators of this universal program that instructs tissue retention in diverse tissue-resident lymphocyte populations.
AbstractList	Tissue-resident memory T (Trm) cells permanently localize to portals of pathogen entry, where they provide immediate protection against reinfection. To enforce tissue retention, Trm cells up-regulate CD69 and down-regulate molecules associated with tissue egress; however, a Trm-specific transcriptional regulator has not been identified. Here, we show that the transcription factor Hobit is specifically up-regulated in Trm cells and, together with related Blimp1, mediates the development of Trm cells in skin, gut, liver, and kidney in mice. The Hobit-Blimp1 transcriptional module is also required for other populations of tissue-resident lymphocytes, including natural killer T (NKT) cells and liver-resident NK cells, all of which share a common transcriptional program. Our results identify Hobit and Blimp1 as central regulators of this universal program that instructs tissue retention in diverse tissue-resident lymphocyte populations. The immune system fights microbial invaders by maintaining multiple lines of defense. For instance, specialized memory T cells [resident memory T cells (T rms )] colonize portals of pathogen entry, such as the skin, lung, and gut, to quickly halt reinfections. Mackay et al. now report that in mice, T rms as well as other tissue-dwelling lymphocyte populations such as natural killer cells share a common transcriptional program driven by the related transcription factors Hobit and Blimp1. Tissue residency and retention of lymphocytes require expression of Hobit and Blimp1, which, among other functions, suppress genes that promote tissue exit. Science , this issue p. 459 Tissue-dwelling lymphocyte populations share a common transcriptional signature. Tissue-resident memory T (Trm) cells permanently localize to portals of pathogen entry, where they provide immediate protection against reinfection. To enforce tissue retention, Trm cells up-regulate CD69 and down-regulate molecules associated with tissue egress; however, a Trm-specific transcriptional regulator has not been identified. Here, we show that the transcription factor Hobit is specifically up-regulated in Trm cells and, together with related Blimp1, mediates the development of Trm cells in skin, gut, liver, and kidney in mice. The Hobit-Blimp1 transcriptional module is also required for other populations of tissue-resident lymphocytes, including natural killer T (NKT) cells and liver-resident NK cells, all of which share a common transcriptional program. Our results identify Hobit and Blimp1 as central regulators of this universal program that instructs tissue retention in diverse tissue-resident lymphocyte populations. The immune system fights microbial invaders by maintaining multiple lines of defense. For instance, specialized memory T cells [resident memory T cells (Trms)] colonize portals of pathogen entry, such as the skin, lung, and gut, to quickly halt reinfections. Mackay et al. now report that in mice, Trms as well as other tissue-dwelling lymphocyte populations such as natural killer cells share a common transcriptional program driven by the related transcription factors Hobit and Blimp1. Tissue residency and retention of lymphocytes require expression of Hobit and Blimp1, which, among other functions, suppress genes that promote tissue exit. Science, this issue p. 459 Tissue-resident memory T (Trm) cells permanently localize to portals of pathogen entry, where they provide immediate protection against reinfection. To enforce tissue retention, Trm cells up-regulate CD69 and down-regulate molecules associated with tissue egress; however, a Trm-specific transcriptional regulator has not been identified. Here, we show that the transcription factor Hobit is specifically up-regulated in Trm cells and, together with related Blimp1, mediates the development of Trm cells in skin, gut, liver, and kidney in mice. The Hobit-Blimp1 transcriptional module is also required for other populations of tissue-resident lymphocytes, including natural killer T (NKT) cells and liver-resident NK cells, all of which share a common transcriptional program. Our results identify Hobit and Blimp1 as central regulators of this universal program that instructs tissue retention in diverse tissue-resident lymphocyte populations.
Author	Carbone, Francis R. Shi, Wei Busslinger, Meinrad Zaid, Ali Pellegrini, Marc Mackay, Laura K. Stark, Regina Godfrey, Dale I. Freestone, David Wynne-Jones, Erica Belz, Gabrielle T. Braun, Asolina van Lier, René A. W. Gebhardt, Thomas Nota, Benjamin Preston, Simon Kallies, Axel Liao, Yang Minnich, Martina Behr, Felix M. Kragten, Natasja A. M. Seillet, Cyril Man, Kevin Pellicci, Daniel G. van Gisbergen, Klaas P. J. M.
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/27102484$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	Copyright © 2016 American Association for the Advancement of Science Copyright © 2016, American Association for the Advancement of Science. Copyright © 2016, American Association for the Advancement of Science
Copyright_xml	– notice: Copyright © 2016 American Association for the Advancement of Science – notice: Copyright © 2016, American Association for the Advancement of Science. – notice: Copyright © 2016, American Association for the Advancement of Science
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Snippet	Tissue-resident memory T (Trm) cells permanently localize to portals of pathogen entry, where they provide immediate protection against reinfection. To enforce... The immune system fights microbial invaders by maintaining multiple lines of defense. For instance, specialized memory T cells [resident memory T cells (T rms... The immune system fights microbial invaders by maintaining multiple lines of defense. For instance, specialized memory T cells [resident memory T cells (Trms)]...
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SubjectTerms	Animals Cellular biology Gastrointestinal Tract - immunology Gene Expression Regulation Genes, Regulator - genetics Genes, Regulator - physiology Immune system Immunologic Memory - genetics Kidney - immunology Killer Cells, Natural - immunology Liver - immunology Lymphocyte Activation Lymphocytes Mice Mice, Knockout Natural Killer T-Cells - immunology Pathogens Positive Regulatory Domain I-Binding Factor 1 Retention Skin - immunology Tissues Transcription Factors - genetics Transcription Factors - physiology Transcription, Genetic Up-Regulation
Title	Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes
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