Protein SUMOylation Is Required for Regulatory T Cell Expansion and Function

被引:62
作者
Ding, Xiao [1 ]
Wang, Aibo [2 ,3 ,5 ]
Ma, Xiaopeng [1 ]
Demarque, Maud [4 ]
Jin, Wei [2 ,3 ]
Xin, Huawei [2 ,3 ]
Dejean, Anne [4 ]
Dong, Chen [2 ,3 ]
机构
[1] Tsinghua Univ, Sch Life Sci, Beijing 100084, Peoples R China
[2] Tsinghua Univ, Inst Immunol, Beijing 100084, Peoples R China
[3] Tsinghua Univ, Sch Med, Beijing 100084, Peoples R China
[4] Inst Pasteur, INSERM, U993, Nucl Org & Oncogenesis Unit, F-75015 Paris, France
[5] 5 Fuping 8 St,Xiaoping Ind Pk, Guangzhou 511400, Guangdong, Peoples R China
关键词
TRANSCRIPTION FACTOR FOXP3; NUCLEAR-PORE COMPLEX; LINEAGE COMMITMENT; TARGET GENES; CIS-ELEMENT; DIFFERENTIATION; MECHANISMS; REPRESSION; EXPRESSION; PHOSPHORYLATION;
D O I
10.1016/j.celrep.2016.06.056
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Foxp3-expressing regulatory T (Treg) cells are essential for immune tolerance; however, the molecular mechanisms underlying Treg cell expansion and function are still not well understood. SUMOylation is a protein post-translational modification characterized by covalent attachment of SUMO moieties to lysines. UBC9 is the only E2 conjugating enzyme involved in this process, and loss of UBC9 completely abolishes the SUMOylation pathway. Here, we report that selective deletion of Ubc9 within the Treg lineage results in fatal early-onset autoimmunity similar to Foxp3 mutant mice. Ubc9-deficient Treg cells exhibit severe defects in TCR-driven homeostatic proliferation, accompanied by impaired activation and compromised suppressor function. Importantly, TCR ligation enhanced SUMOylation of IRF4, a critical regulator of Treg cell function downstream of TCR signals, which regulates its stability in Treg cells. Our data thus have demonstrated an essential role of SUMOylation in the expansion and function of Treg cells.
引用
收藏
页码:1055 / 1066
页数:12
相关论文
共 59 条
[1]   CD28 costimulation mediates T cell expansion via IL-2-independent and IL-2-dependent regulation of cell cycle progression [J].
Appleman, LJ ;
Berezovskaya, A ;
Grass, I ;
Boussiotis, VA .
JOURNAL OF IMMUNOLOGY, 2000, 164 (01) :144-151
[2]   The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3 [J].
Bennett, CL ;
Christie, J ;
Ramsdell, F ;
Brunkow, ME ;
Ferguson, PJ ;
Whitesell, L ;
Kelly, TE ;
Saulsbury, FT ;
Chance, PF ;
Ochs, HD .
NATURE GENETICS, 2001, 27 (01) :20-21
[3]   Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse [J].
Brunkow, ME ;
Jeffery, EW ;
Hjerrild, KA ;
Paeper, B ;
Clark, LB ;
Yasayko, SA ;
Wilkinson, JE ;
Galas, D ;
Ziegler, SF ;
Ramsdell, F .
NATURE GENETICS, 2001, 27 (01) :68-73
[4]   Regulation and function of mTOR signalling in T cell fate decisions [J].
Chi, Hongbo .
NATURE REVIEWS IMMUNOLOGY, 2012, 12 (05) :325-338
[5]   The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells [J].
Cretney, Erika ;
Xin, Annie ;
Shi, Wei ;
Minnich, Martina ;
Masson, Frederick ;
Miasari, Maria ;
Belz, Gabrielle T. ;
Smyth, Gordon K. ;
Busslinger, Meinrad ;
Nutt, Stephen L. ;
Kallies, Axel .
NATURE IMMUNOLOGY, 2011, 12 (04) :304-U53
[6]   Follicular Helper CD4 T Cells (TFH) [J].
Crotty, Shane .
ANNUAL REVIEW OF IMMUNOLOGY, VOL 29, 2011, 29 :621-663
[7]   Regulation of protein tyrosine phosphatase 1B by sumoylation [J].
Dadke, Shrikrishna ;
Cotteret, Sophie ;
Yip, Shu-Chin ;
Jaffer, Zahara M. ;
Haj, Fawaz ;
Ivanov, Alexey ;
Rauscher, Frank, III ;
Shuai, Ke ;
Ng, Tony ;
Neel, Benjamin G. ;
Chernoff, Jonathan .
NATURE CELL BIOLOGY, 2007, 9 (01) :80-U102
[8]   Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIα [J].
Dawlaty, Meelad M. ;
Malureanu, Liviu ;
Jeganathan, Karthik B. ;
Kao, Esther ;
Sustmann, Claudio ;
Tahk, Samuel ;
Shuai, Ke ;
Grosschedl, Rudolf ;
van Deursen, Jan M. .
CELL, 2008, 133 (01) :103-115
[9]   Sumoylation coordinates the repression of inflammatory and anti-viral gene-expression programs during innate sensing [J].
Decque, Adrien ;
Joffre, Olivier ;
Magalhaes, Joao G. ;
Cossec, Jack-Christophe ;
Blecher-Gonen, Ronnie ;
Lapaquette, Pierre ;
Silvin', Aymeric ;
Manel, Nicolas ;
Joubert, Pierre -Emmanuel ;
Seeler, Jacob-Sebastian ;
Albert, Matthew L. ;
Amit, Ido ;
Amigorena, Sebastian ;
Dejean, Anne .
NATURE IMMUNOLOGY, 2016, 17 (02) :140-149
[10]   The mTOR Kinase Differentially Regulates Effector and Regulatory T Cell Lineage Commitment [J].
Delgoffe, Greg M. ;
Kole, Thomas P. ;
Zheng, Yan ;
Zarek, Paul E. ;
Matthews, Krystal L. ;
Xiao, Bo ;
Worley, Paul F. ;
Kozma, Sara C. ;
Powell, Jonathan D. .
IMMUNITY, 2009, 30 (06) :832-844