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

被引:757
作者
Mackay, Laura K. [1 ,2 ]
Minnich, Martina [3 ]
Kragten, Natasja A. M. [4 ]
Liao, Yang [5 ,6 ]
Nota, Benjamin [7 ]
Seillet, Cyril [5 ,6 ]
Zaid, Ali [1 ]
Man, Kevin [5 ,6 ]
Preston, Simon [5 ,6 ]
Freestone, David [1 ]
Braun, Asolina [1 ]
Wynne-Jones, Erica [1 ]
Behr, Felix M. [4 ,5 ,6 ,8 ]
Stark, Regina [4 ]
Pellicci, Daniel G. [1 ,2 ]
Godfrey, Dale I. [1 ,2 ]
Belz, Gabrielle T. [5 ,6 ]
Pellegrini, Marc [5 ,6 ]
Gebhardt, Thomas [1 ]
Busslinger, Meinrad [3 ]
Shi, Wei [5 ,9 ]
Carbone, Francis R. [1 ]
van Lier, Rene A. W. [4 ]
Kallies, Axel [5 ,6 ,7 ]
van Gisbergen, Klaas P. J. M. [4 ,5 ,6 ,7 ,8 ,9 ]
机构
[1] Univ Melbourne, Dept Microbiol & Immunol, Peter Doherty Inst Infect & Immun, Melbourne, Vic, Australia
[2] Univ Melbourne, ARC, Ctr Excellence Adv Mol Imaging, Melbourne, Vic, Australia
[3] Vienna Bioctr VBC, Res Inst Mol Pathol IMP, Vienna, Austria
[4] Univ Amsterdam, Acad Med Ctr, Dept Hematopoiesis, Sanquin Res & Landsteiner Lab, Meibergdreef 9, NL-1105 AZ Amsterdam, Netherlands
[5] Walter & Eliza Hall Inst Med Res, Melbourne, Vic 3050, Australia
[6] Univ Melbourne, Dept Med Biol, Melbourne, Vic, Australia
[7] Univ Amsterdam, AMC, Sanquin Res & Landsteiner Lab, Dept Blood Cell Res, Amsterdam, Netherlands
[8] AMC, Dept Expt Immunol, Amsterdam, Netherlands
[9] Univ Melbourne, Dept Comp & Informat Syst, Melbourne, Vic, Australia
基金
英国医学研究理事会; 澳大利亚国家健康与医学研究理事会; 欧洲研究理事会;
关键词
MEMORY T-CELLS; PERIPHERAL-TISSUES; DIFFERENTIATION; INFECTION; IMMUNITY; INNATE; SKIN; BET; PATHWAY; TRIGGER;
D O I
10.1126/science.aad2035
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
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.
引用
收藏
页码:459 / 463
页数:5
相关论文
共 30 条
[1]   Skin-resident memory CD8+ T cells trigger a state of tissue-wide pathogen alert [J].
Ariotti, Silvia ;
Hogenbirk, Marc A. ;
Dijkgraaf, Feline E. ;
Visser, Lindy L. ;
Hoekstra, Mirjam E. ;
Song, Ji-Ying ;
Jacobs, Heinz ;
Haanen, John B. ;
Schumacher, Ton N. .
SCIENCE, 2014, 346 (6205) :101-105
[2]   Long-term retention of mature NK1.1+ NKT cells in the thymus [J].
Berzins, Stuart P. ;
McNab, Finlay W. ;
Jones, Claerwen M. ;
Smyth, Mark J. ;
Godfrey, Dale I. .
JOURNAL OF IMMUNOLOGY, 2006, 176 (07) :4059-4065
[3]   Blimp-1 homolog Hobit identifies effector-type lymphocytes in humans [J].
Braga, Felipe A. Vieira ;
Hertoghs, Kirsten M. L. ;
Kragten, Natasja A. M. ;
Doody, Gina M. ;
Barnes, Nicholas A. ;
Remmerswaal, Ester B. M. ;
Hsiao, Cheng-Chih ;
Moerland, Perry D. ;
Wouters, Diana ;
Derks, Ingrid A. M. ;
van Stijn, Amber ;
Demkes, Marc ;
Hamann, Jorg ;
Eldering, Eric ;
Nolte, Martijn A. ;
Tooze, Reuben M. ;
ten Berge, Ineke J. M. ;
van Gisbergen, Klaas P. J. M. ;
van Lier, Rene A. W. .
EUROPEAN JOURNAL OF IMMUNOLOGY, 2015, 45 (10) :2945-2958
[4]   Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics [J].
Bromley, SK ;
Thomas, SY ;
Luster, AD .
NATURE IMMUNOLOGY, 2005, 6 (09) :895-901
[5]   T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow [J].
Daussy, Cecile ;
Faure, Fabrice ;
Mayol, Katia ;
Viel, Sebastien ;
Gasteiger, Georg ;
Charrier, Emily ;
Bienvenu, Jacques ;
Henry, Thomas ;
Debien, Emilie ;
Hasan, Uzma A. ;
Marvel, Jacqueline ;
Yoh, Keigyou ;
Takahashi, Satoru ;
Prinz, Immo ;
de Bernard, Simon ;
Buffat, Laurent ;
Walzer, Thierry .
JOURNAL OF EXPERIMENTAL MEDICINE, 2014, 211 (03) :563-577
[6]   Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues [J].
Debes, GF ;
Arnold, CN ;
Young, AJ ;
Krautwald, S ;
Lipp, M ;
Hay, JB ;
Butcher, EC .
NATURE IMMUNOLOGY, 2005, 6 (09) :889-894
[7]   Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs [J].
Gasteiger, Georg ;
Fan, Xiying ;
Dikiy, Stanislav ;
Lee, Sue Y. ;
Rudensky, Alexander Y. .
SCIENCE, 2015, 350 (6263) :981-985
[8]   Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells [J].
Gattinoni, Luca ;
Zhong, Xiao-Song ;
Palmer, Douglas C. ;
Ji, Yun ;
Hinrichs, Christian S. ;
Yu, Zhiya ;
Wrzesinski, Claudia ;
Boni, Andrea ;
Cassard, Lydie ;
Garvin, Lindsay M. ;
Paulos, Chrystal M. ;
Muranski, Pawel ;
Restifo, Nicholas P. .
NATURE MEDICINE, 2009, 15 (07) :808-U129
[9]   Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus [J].
Gebhardt, Thomas ;
Wakim, Linda M. ;
Eidsmo, Liv ;
Reading, Patrick C. ;
Heath, William R. ;
Carbone, Francis R. .
NATURE IMMUNOLOGY, 2009, 10 (05) :524-530
[10]   The Transcription Factors T-bet and Eomes Control Key Checkpoints of Natural Killer Cell Maturation [J].
Gordon, Scott M. ;
Chaix, Julie ;
Rupp, Levi J. ;
Wu, Junmin ;
Madera, Sharline ;
Sun, Joseph C. ;
Lindsten, Tullia ;
Reiner, Steven L. .
IMMUNITY, 2012, 36 (01) :55-67