Please wait a minute...
Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

Postal Subscription Code 80-984

2018 Impact Factor: 7.575

Protein Cell    2020, Vol. 11 Issue (2) : 108-123    https://doi.org/10.1007/s13238-019-00662-0
RESEARCH ARTICLE
Contact-dependent delivery of IL-2 by dendritic cells to CD4 T cells in the contraction phase promotes their long-term survival
Dan Tong1, Li Zhang1, Fei Ning1, Ying Xu1, Xiaoyu Hu1(), Yan Shi1,2()
1. Tsinghua Institute for Immunology and Department of Basic Medical Sciences, Beijing Key Lab for Immunological Research on Chronic Diseases, School of Medicine, Tsinghua-Peking Center for Life Sciences, Tsinghua University, Beijing 100084, China
2. Department of Microbiology, Immunology and Infectious Diseases, Snyder Institute, University of Calgary, Calgary, Canada
 Download: PDF(1135 KB)  
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Common γ chain cytokines are important for immune memory formation. Among them, the role of IL-2 remains to be fully explored. It has been suggested that this cytokine is critically needed in the late phase of primary CD4 T cell activation. Lack of IL-2 at this stage sets for a diminished recall response in subsequent challenges. However, as IL-2 peak production is over at this point, the source and the exact mechanism that promotes its production remain elusive. We report here that resting, previously antigen-stimulated CD4 T cells maintain a minimalist response to dendritic cells after their peak activation in vitro. This subtle activation event may be induced by DCs without overt presence of antigen and appears to be stronger if IL-2 comes from the same dendritic cells. This encounter reactivates a miniature IL-2 production and leads a gene expression profile change in these previously activated CD4 T cells. The CD4 T cells so experienced show enhanced reactivation intensity upon secondary challenges later on. Although mostly relying on in vitro evidence, our work may implicate a subtle programing for CD4 T cell survival after primary activation in vitro.

Keywords dendritic cell      contact dependence      long term survival      T cell memory      IL-2     
Corresponding Author(s): Xiaoyu Hu,Yan Shi   
Issue Date: 04 March 2020
 Cite this article:   
Dan Tong,Li Zhang,Fei Ning, et al. Contact-dependent delivery of IL-2 by dendritic cells to CD4 T cells in the contraction phase promotes their long-term survival[J]. Protein Cell, 2020, 11(2): 108-123.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-019-00662-0
https://academic.hep.com.cn/pac/EN/Y2020/V11/I2/108
1 S Audic, JM Claverie (1997) The significance of digital gene expression profiles. Genome Res 7:986–995
https://doi.org/10.1101/gr.7.10.986
2 EB Bell, J Westermann (2008) CD4 memory T cells on trial: immunological memory without a memory T cell. Trends Immunol 29:405–411
https://doi.org/10.1016/j.it.2008.06.002
3 UY Choi, J-S Kang, YS Hwang, Y-J Kim(2015) Oligoadenylate synthase-like (OASL) proteins: dual functions and associations with diseases. Exp Mol Med 47:e144
https://doi.org/10.1038/emm.2014.110
4 A Ciabattini, E Pettini, P Andersen, G Pozzi, D Medaglini (2008) Primary activation of antigen-specific naive CD4+ and CD8+ T cells following intranasal vaccination with recombinant bacteria. Infect Immun 76:5817–5825
https://doi.org/10.1128/IAI.00793-08
5 S Feau, R Arens, S Togher, SP Schoenberger (2011) Autocrine IL-2 is required for secondary population expansion of CD8(+) memory T cells. Nat Immunol 12:908–913
https://doi.org/10.1038/ni.2079
6 DJ Gasper, MM Tejera, M Suresh (2014) CD4 T-cell memory generation and maintenance. Crit Rev Immunol 34:121–146
https://doi.org/10.1615/CritRevImmunol.2014010373
7 HS Goodridge, RM Simmons, DM Underhill (2007) Dectin-1 stimulation by Candida albicans yeast or zymosan triggers NFAT activation in macrophages and dendritic cells. J Immunol 178:3107–3115
https://doi.org/10.4049/jimmunol.178.5.3107
8 F Granucci, C Vizzardelli, N Pavelka, S Feau, M Persico, E Virzi, M Rescigno, G Moro, P Ricciardi-Castagnoli(2001) Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat Immunol 2:882–888
https://doi.org/10.1038/ni0901-882
9 F Granucci, S Feau, V Angeli, F Trottein, P Ricciardi-Castagnoli (2003) Early IL-2 production by mouse dendritic cells is the result of microbial-induced priming. J Immunol 170:5075–5081
https://doi.org/10.4049/jimmunol.170.10.5075
10 S Heink, N Yogev, C Garbers, M Herwerth, L Aly, C Gasperi, V, Husterer AL Croxford, K Moller-Hackbarth, HS Bartschet al. (2017) Trans-presentation of IL-6 by dendritic cells is required for the priming of pathogenic TH17 cells. Nat Immunol 18:74–85
https://doi.org/10.1038/ni.3632
11 T Kakiuchi, T Tamura, Y Gyotoku, H Nariuchi (1991) IL-2 production by B cells stimulated with a specific antigen. Cell Immunol 138:207–215
https://doi.org/10.1016/0008-8749(91)90145-2
12 V, Kalia S Sarkar, S Subramaniam, WN Haining, KA Smith, R Ahmed(2010) Prolonged interleukin-2Ralpha expression on virusspecific CD8+ T cells favors terminal-effector differentiation in vivo. Immunity 32:91–103
https://doi.org/10.1016/j.immuni.2009.11.010
13 WC Kieper, JT Burghardt, CD Surh (2004) A role for TCR affinity in regulating naive T cell homeostasis. J Immunol 172:40–44
https://doi.org/10.4049/jimmunol.172.1.40
14 W Liao, J-X, Lin WJ Leonard (2013) Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity 38:13–25
https://doi.org/10.1016/j.immuni.2013.01.004
15 MKL MacLeod, ET Clambey, JW Kappler, P Marrack (2009) CD4 memory T cells: what are they and what can they do? Semin Immunol 21:53–61
https://doi.org/10.1016/j.smim.2009.02.006
16 KK McKinstry, TM Strutt, B Bautista, W Zhang, Y Kuang, AM Cooper, SL Swain (2014) Effector CD4 T-cell transition to memory requires late cognate interactions that induce autocrine IL-2. Nat Commun 5:5377
https://doi.org/10.1038/ncomms6377
17 C Park, S, Li E Cha, C Schindler (2000) Immune response in Stat2 knockout mice. Immunity 13:795–804
https://doi.org/10.1016/S1074-7613(00)00077-7
18 ME Raeber, Y Zurbuchen, D Impellizzieri, O Boyman (2018) The role of cytokines in T-cell memory in health and disease. Immunol Rev 283:176–193
https://doi.org/10.1111/imr.12644
19 SH Ross, DA Cantrell (2018) Signaling and Function of Interleukin-2 in T Lymphocytes. Annu Rev Immunol 36:411–433
https://doi.org/10.1146/annurev-immunol-042617-053352
20 NE Schartz, N Chaput, J Taieb, P Bonnaventure, H Trebeden-Negre, M Terme, C Menard, C Lebbe, A Schimpl, P Ardouinet al. (2005) IL-2 production by dendritic cells is not critical for the activation of cognate and innate effectors in draining lymph nodes. Eur J Immunol 35:2840–2850
https://doi.org/10.1002/eji.200425628
21 KA Smith (2015) Commentary: the Interleukin-2 Tcell system: a new cell growth model. Front Immunol 6:414
https://doi.org/10.3389/fimmu.2015.00414
22 DK Sojka, D, Bruniquel RH Schwartz, NJ Singh (2004) IL-2 secretion by CD4+ T cells in vivo is rapid, transient, and influenced by TCR-specific competition. J Immunol 172:6136–6143
https://doi.org/10.4049/jimmunol.172.10.6136
23 R Spolski, D Gromer, WJ Leonard (2017) The γ (c) family of cytokines: fine-tuning signals from IL-2 and IL-21 in the regulation of the immune response. F1000Research 6:1872
https://doi.org/10.12688/f1000research.12202.1
24 QG Steiner, LA Otten, MJ Hicks, G Kaya, F Grosjean, E Saeuberli, C Lavanchy, F Beermann, KL McClain, H Acha-Orbea (2008) In vivo transformation of mouse conventional CD8alpha+ dendritic cells leads to progressive multisystem histiocytosis. Blood 111:2073–2082
https://doi.org/10.1182/blood-2007-06-097576
25 C Tanchot, FA Lemonnier, B Perarnau, AA Freitas, B Rocha (1997) Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 276:2057–2062
https://doi.org/10.1126/science.276.5321.2057
26 Y Tian, L Meng, Y Zhang (2017) Epigenetic regulation of dendritic cell development and function. Cancer J (Sudbury, Mass) 23:302–307
https://doi.org/10.1097/PPO.0000000000000280
27 S Venuta, R Mertelsmann, K Welte, SP Feldman, CY Wang, MA Moore (1983) Production and regulation of interleukin-2 in human lymphoblastic leukemias studied with T-cell monoclonal antibodies. Blood 61:781–789
https://doi.org/10.1182/blood.V61.4.781.781
28 AV Villarino, CM Tato, JS Stumhofer, Z Yao, YK Cui, L Hennighausen, JJ O’Shea, CA Hunter (2007) Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J Exp Med 204:65–71
https://doi.org/10.1084/jem.20061198
29 C von Mering, M Huynen, D Jaeggi, S Schmidt, P Bork, B Snel (2003) STRING: a database of predicted functional associations between proteins. Nucleic Acids Res 31:258–261
https://doi.org/10.1093/nar/gkg034
30 MA Williams, AJ Tyznik, MJ Bevan (2006) Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441:890–893
https://doi.org/10.1038/nature04790
31 SC Wuest, J Edwan, JF Martin, S Han, JSA Perry, CM Cartagena, E Matsuura, D Maric, TA Waldmann, B Bielekova (2011) A vital role for IL-2 trans-presentation in DC-mediated T cell activation in humans as revealed by daclizumab therapy. Nat Med 17:604–609
https://doi.org/10.1038/nm.2365
32 J Yang, X Liu, K Bhalla, CN Kim, AM Ibrado, J Cai, TI Peng, DP Jones, X Wang (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129–1132
https://doi.org/10.1126/science.275.5303.1129
33 C Zhao, MN Collins, TY Hsiang, RM Krug (2013) Interferon-induced ISG15 pathway: an ongoing virus-host battle. Trends Microbiol 21:181–186
https://doi.org/10.1016/j.tim.2013.01.005
34 MJ Zhou, FZ Chen, HC Chen, XX Wan, X Zhou, Q Fang, DZ Zhang (2017) ISG15 inhibits cancer cell growth and promotes apoptosis. Int J Mol Med 39:446–452
https://doi.org/10.3892/ijmm.2016.2845
[1] PAC-0108-19312-SY_suppl_1 Download
[1] Cécile Apert, Paola Romagnoli, Joost P. M. van Meerwijk. IL-2 and IL-15 dependent thymic development of Foxp3-expressing regulatory T lymphocytes[J]. Protein Cell, 2018, 9(4): 322-332.
[2] Haibo Zhou, Li Wu. The development and function of dendritic cell populations and their regulation by miRNAs[J]. Protein Cell, 2017, 8(7): 501-513.
[3] Zhujun Jiang,Jingtao Chen,Xuemei Du,Hang Cheng,Xiaohu Wang,Chen Dong. IL-25 blockade inhibits metastasis in breast cancer[J]. Protein Cell, 2017, 8(3): 191-201.
[4] Haisheng Yu,Peng Zhang,Xiangyun Yin,Zhao Yin,Quanxing Shi,Ya Cui,Guanyuan Liu,Shouli Wang,Pier Paolo Piccaluga,Taijiao Jiang,Liguo Zhang. Human BDCA2+CD123+CD56+ dendritic cells (DCs) related to blastic plasmacytoid dendritic cell neoplasm represent a unique myeloid DC subset[J]. Protein Cell, 2015, 6(4): 297-306.
[5] Juan Ma,Huamin Han,Li Ma,Changzhen Liu,Xin Xue,Pan Ma,Xiaomei Li,Hua Tao. The immunostimulatory effects of retinoblastoma cell supernatant on dendritic cells[J]. Protein Cell, 2014, 5(4): 307-316.
[6] Xiaoran Wu, Yi Tan, Qiao Xing, Shengdian Wang. IL-21 accelerates xenogeneic graft-versus-host disease correlated with increased B-cell proliferation[J]. Prot Cell, 2013, 4(11): 863-871.
[7] Musheng Bao, Yong-Jun Liu. Regulation of TLR7/9 signaling in plasmacytoid dendritic cells[J]. Prot Cell, 2013, 4(1): 40-52.
[8] Kelly Roney, Eda Holl, Jenny Ting. Immune plexins and semaphorins: old proteins, new immune functions[J]. Prot Cell, 2013, 4(1): 17-26.
[9] Yifan Zhan, Li Wu. Functional regulation of monocyte-derived dendritic cells by microRNAs[J]. Prot Cell, 2012, 3(7): 497-507.
[10] Natalie L. Patterson, Justine D. Mintern. Intersection of autophagy with pathways of antigen presentation[J]. Prot Cell, 2012, 3(12): 911-920.
[11] Priyanka Sathe, Li Wu. The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets[J]. Prot Cell, 2011, 2(8): 620-630.
[12] Dachuan Huang, Sylvia Lim, Rong Yuan Ray Chua, Hong Shi, Siew Heng Wong, Mah Lee Ng. A novel CARD containing splice-isoform of CIITA regulates nitric oxide synthesis in dendritic cells[J]. Protein Cell, 2010, 1(3): 291-306.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed