BACH2 regulates CD8+ T cell differentiation by controlling access of AP-1 factors to enhancers

被引:203
|
作者
Roychoudhuri, Rahul [1 ,2 ]
Clever, David [1 ,3 ]
Li, Peng [4 ,5 ]
Wakabayashi, Yoshiyuki [6 ]
Quinn, Kylie M. [7 ]
Klebanoff, Christopher A. [1 ]
Ji, Yun [1 ]
Sukumar, Madhusudhanan [1 ]
Eil, Robert L. [1 ]
Yu, Zhiya [1 ]
Spolski, Rosanne [4 ,5 ]
Palmer, Douglas C. [1 ]
Pan, Jenny H. [1 ]
Patel, Shashank J. [1 ]
Macallan, Derek C. [8 ]
Fabozzi, Giulia [1 ]
Shih, Han-Yu [9 ]
Kanno, Yuka [9 ]
Muto, Akihiko [10 ,11 ]
Zhu, Jun [6 ]
Gattinoni, Luca [1 ]
O'Shea, John J. [9 ]
Okkenhaug, Klaus [2 ]
Igarashi, Kazuhiko [10 ,11 ]
Leonard, Warren J. [4 ,5 ]
Restifo, Nicholas P. [1 ,12 ]
机构
[1] NCI, NIH, Bethesda, MD 20892 USA
[2] Babraham Inst, Lab Lymphocyte Signalling & Dev, Cambridge, England
[3] Ohio State Univ, Coll Med, Med Scientist Training Program, Columbus, OH 43210 USA
[4] NHLBI, Lab Mol Immunol, NIH, Bldg 10, Bethesda, MD 20892 USA
[5] NHLBI, Ctr Immunol, NIH, Bldg 10, Bethesda, MD 20892 USA
[6] NHLBI, Syst Biol Ctr, NIH, Bldg 10, Bethesda, MD 20892 USA
[7] NIAID, Vaccine Res Ctr, NIH, Bethesda, MD USA
[8] St Georges Univ London, Inst Infect & Immun, London, England
[9] NIAMSD, Mol Immunol & Inflammat Branch, NIH, Bethesda, MD 20892 USA
[10] Tohoku Univ, Dept Biochem, Grad Sch Med, Sendai, Miyagi 980, Japan
[11] Japan Agcy Med Res & Dev, AMED CREST, Tokyo, Japan
[12] Georgetown Univ, Med Ctr, Grad Program Microbiol & Immunol, Washington, DC 20007 USA
基金
英国惠康基金; 英国生物技术与生命科学研究理事会;
关键词
TRANSCRIPTION FACTORS; EXPRESSION ANALYSIS; MEMORY PHENOTYPE; EFFECTOR; GENE; REPRESSES; LYMPHOCYTES; ACTIVATION; GENERATION; PROTEINS;
D O I
10.1038/ni.3441
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
T cell antigen receptor (TCR) signaling drives distinct responses depending on the differentiation state and context of CD8(+) T cells. We hypothesized that access of signal-dependent transcription factors (TFs) to enhancers is dynamically regulated to shape transcriptional responses to TCR signaling. We found that the TF BACH2 restrains terminal differentiation to enable generation of long-lived memory cells and protective immunity after viral infection. BACH2 was recruited to enhancers, where it limited expression of TCR-driven genes by attenuating the availability of activator protein-1 (AP-1) sites to Jun family signal-dependent TFs. In naive cells, this prevented TCR-driven induction of genes associated with terminal differentiation. Upon effector differentiation, reduced expression of BACH2 and its phosphorylation enabled unrestrained induction of TCR-driven effector programs.
引用
收藏
页码:851 / +
页数:12
相关论文
共 50 条
  • [41] Differentiation and Persistence of Memory CD8+ T Cells Depend on T Cell Factor 1
    Zhou, Xinyuan
    Yu, Shuyang
    Zhao, Dong-Mei
    Harty, John T.
    Badovinac, Vladimir P.
    Xue, Hai-Hui
    IMMUNITY, 2010, 33 (02) : 229 - 240
  • [42] MicroRNA-181a regulates IFN-γ expression in effector CD8+ T cell differentiation
    Tiago Amado
    Ana Amorim
    Francisco J. Enguita
    Paula V. Romero
    Daniel Inácio
    Marta Pires de Miranda
    Samantha J. Winter
    J. Pedro Simas
    Andreas Krueger
    Nina Schmolka
    Bruno Silva-Santos
    Anita Q. Gomes
    Journal of Molecular Medicine, 2020, 98 : 309 - 320
  • [43] STAT3 regulates CD8+ T cell differentiation and functions in cancer and acute infection
    Sun, Qinli
    Zhao, Xiaohong
    Li, Ruifeng
    Liu, Dingfeng
    Pan, Birui
    Xie, Bowen
    Chi, Xinxin
    Cai, Dongli
    Wei, Peng
    Xu, Wei
    Wei, Kun
    Zhao, Zixuan
    Fu, Yujie
    Ni, Ling
    Dong, Chen
    JOURNAL OF EXPERIMENTAL MEDICINE, 2023, 220 (04):
  • [44] MicroRNA-181a regulates IFN-γ expression in effector CD8+ T cell differentiation
    Amado, Tiago
    Amorim, Ana
    Enguita, Francisco J.
    Romero, Paula, V
    Inacio, Daniel
    de Miranda, Marta Pires
    Winter, Samantha J.
    Pedro Simas, J.
    Krueger, Andreas
    Schmolka, Nina
    Silva-Santos, Bruno
    Gomes, Anita Q.
    JOURNAL OF MOLECULAR MEDICINE-JMM, 2020, 98 (02): : 309 - 320
  • [45] Bach2 represses the AP-1-driven induction of interleukin-2 gene transcription in CD4+ T cells
    Jang, Eunkyeong
    Lee, Hye Rim
    Lee, Geon Hee
    Oh, Ah-Reum
    Cha, Ji-Young
    Igarashi, Kazuhiko
    Youn, Jeehee
    BMB REPORTS, 2017, 50 (09) : 472 - 477
  • [46] mTORC1 and mTORC2 selectively regulate CD8+ T cell differentiation
    Pollizzi, Kristen N.
    Patel, Chirag H.
    Sun, Im-Hong
    Oh, Min-Hee
    Waickman, Adam T.
    Wen, Jiayu
    Delgoffe, Greg M.
    Powell, Jonathan D.
    JOURNAL OF CLINICAL INVESTIGATION, 2015, 125 (05): : 2090 - 2108
  • [47] Erratum: Epigenetic landscapes reveal transcription factors that regulate CD8+ T cell differentiation
    Bingfei Yu
    Kai Zhang
    J Justin Milner
    Clara Toma
    Runqiang Chen
    James P Scott-Browne
    Renata M Pereira
    Shane Crotty
    John T Chang
    Matthew E Pipkin
    Wei Wang
    Ananda W Goldrath
    Nature Immunology, 2017, 18 (6) : 705 - 705
  • [48] One naive T cell, multiple fates in CD8+ T cell differentiation
    Gerlach, Carmen
    van Heijst, Jeroen W. J.
    Swart, Erwin
    Sie, Daoud
    Armstrong, Nicola
    Kerkhoven, Ron M.
    Zehn, Dietmar
    Bevan, Michael J.
    Schepers, Koen
    Schumacher, Ton N. M.
    JOURNAL OF EXPERIMENTAL MEDICINE, 2010, 207 (06): : 1235 - 1246
  • [49] BACH2 enforces the transcriptional and epigenetic programs of stem-like CD8+ T cells (vol 22, pg 370, 2021)
    Yao, Chen
    Lou, Guohua
    Sun, Hong-Wei
    Zhu, Ziang
    Sun, Yi
    Chen, Zeyu
    Chauss, Daniel
    Moseman, E. Ashley
    Cheng, Jun
    D'Antonio, Marc A.
    Shi, Wangke
    Shi, Junwei
    Kometani, Kohei
    Kurosaki, Tomohiro
    Wherry, E. John
    Afzali, Behdad
    Gattinoni, Luca
    Zhu, Yuwen
    McGavern, Dorian B.
    O'Shea, John J.
    Schwartzberg, Pamela L.
    Wu, Tuoqi
    NATURE IMMUNOLOGY, 2021, 22 (04) : 530 - 530
  • [50] Granzyme B Regulates Antiviral CD8+ T Cell Responses
    Salti, Suzan M.
    Hammelev, Erin M.
    Grewal, Jenny L.
    Reddy, Sreelatha T.
    Zemple, Sarah J.
    Grossman, William J.
    Grayson, Mitchell H.
    Verbsky, James W.
    JOURNAL OF IMMUNOLOGY, 2011, 187 (12): : 6301 - 6309