Inflammation negatively regulates FOXP3 and regulatory T-cell function via DBC1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 25, 2015, Pages E3246-E3254

  Gao, Yayi ^a,b   Tang, Jiayou ^c,d   Chen, Weiqian ^c   Li, Qiang ^c   Nie, Jia ^a   Lin, Fang ^a   Wu, Qingsi ^e   Chen, Zuojia ^a   Gao, Zhimei ^a   Fan, Huimin ^d   Tsun, Andy ^a   Shen, Jijia ^e   Chen, Guihua ^b   Liu, Zhongmin ^d   Lou, Zhenkun ^f   Olsen, Nancy J ^c   Zheng, Song Guo ^b,c   Li, Bin ^a  

^a INSTITUTE PASTEUR OF SHANGHAI   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d TONGJI UNIVERSITY   (China)

^e ANHUI MEDICAL UNIVERSITY   (China)

^f Mayo Clinic College of Medicine   (United States)

Author keywords

Deleted in breast cancer 1; Foxp3 complex; Inflammation; Regulatory T cells

Indexed keywords

CALMODULIN BINDING PROTEIN; CASPASE 8; DBC1 PROTEIN; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROTEIN; PROTEIN A; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; KIAA1967 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLITIS; CONTROLLED STUDY; DELETION MUTANT; ENCEPHALOMYELITIS; FLOW CYTOMETRY; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INFLAMMATION; INFLAMMATORY DISEASE; JURKAT CELL LINE; LYMPH NODE; LYMPHOCYTE FUNCTION; MASS SPECTROMETRY; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SPLEEN; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNOLOGY; PHYSIOLOGY;

MUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FORKHEAD TRANSCRIPTION FACTORS; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES, REGULATORY;

EID: 84934949643     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421463112     Document Type: Article

References (43)

1. Josefowicz SZ, Lu LF, Rudensky AY (2012) Regulatory T cells: Mechanisms of differentiation and function. Annu Rev Immunol 30:531-564.
2. Littman DR, Rudensky AY (2010) Th17 and regulatory T cells in mediating and restraining inflammation. Cell 140(6):845-858.
3. Sakaguchi S, Yamaguchi T, Nomura T, Ono M (2008) Regulatory T cells and immune tolerance. Cell 133(5):775-787.
4. Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4(4):330-336.
5. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299(5609):1057-1061.
6. Ziegler SF (2006) FOXP3: Of mice and men. Annu Rev Immunol 24:209-226.
7. Campbell DJ, Koch MA (2011) Phenotypical and functional specialization of FOXP3+ regulatory T cells. Nat Rev Immunol 11(2):119-130.
8. Gavin MA, et al. (2006) Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc Natl Acad Sci USA 103(17):6659-6664.
9. Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE (2007) Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 37(1):129-138.
10. Fu W, et al. (2012) A multiply redundant genetic switch 'locks in' the transcriptional signature of regulatory T cells. Nat Immunol 13(10):972-980.
11. Rudra D, et al. (2012) Transcription factor Foxp3 and its protein partners form a complex regulatory network. Nat Immunol 13(10):1010-1019.
12. Ohkura N, Kitagawa Y, Sakaguchi S (2013) Development and maintenance of regulatory T cells. Immunity 38(3):414-423.
13. Hori S (2012) The Foxp3 interactome: A network perspective of T(reg) cells. Nat Immunol 13(10):943-945.
14. Li B, et al. (2007) FOXP3 is a homo-oligomer and a component of a supramolecular regulatory complex disabled in the human XLAAD/IPEX autoimmune disease. Int Immunol 19(7):825-835.
15. Wang Y, Su MA, Wan YY (2011) An essential role of the transcription factor GATA-3 for the function of regulatory T cells. Immunity 35(3):337-348.
16. Du J, Huang C, Zhou B, Ziegler SF (2008) Isoform-specific inhibition of ROR alpha-mediated transcriptional activation by human FOXP3. J Immunol 180(7):4785-4792.
17. Pan F, et al. (2009) Eos mediates Foxp3-dependent gene silencing in CD4+ regulatory T cells. Science 325(5944):1142-1146.
18. Ono M, et al. (2007) Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446(7136):685-689.
19. Li B, et al. (2007) FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression. Proc Natl Acad Sci USA 104(11):4571-4576.
20. van Loosdregt J, et al. (2010) Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood 115(5):965-974.
21. van Loosdregt J, et al. (2011) Rapid temporal control of Foxp3 protein degradation by sirtuin-1. PLoS ONE 6(4):e19047.
22. Feuerer M, Hill JA, Mathis D, Benoist C (2009) Foxp3+ regulatory T cells: Differentiation, specification, subphenotypes. Nat Immunol 10(7):689-695.
23. Shevach EM (2009) Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 30(5):636-645.
24. Lu L, et al. (2014) Critical role of all-trans retinoic acid in stabilizing human natural regulatory T cells under inflammatory conditions. Proc Natl Acad Sci USA 111(33):E3432-E3440.
25. Chen Z, et al. (2013) The ubiquitin ligase Stub1 negatively modulates regulatory T cell suppressive activity by promoting degradation of the transcription factor Foxp3. Immunity 39(2):272-285.
26. Li Z, et al. (2014) PIM1 kinase phosphorylates the human transcription factor FOXP3 at serine 422 to negatively regulate its activity under inflammation. J Biol Chem 289(39):26872-26881.
27. Zhu J, Yamane H, Paul WE (2010) Differentiation of effector CD4 T cell populations (∗). Annu Rev Immunol 28:445-489.
28. Valencia X, et al. (2006) TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 108(1):253-261.
29. Nie H, et al. (2013) Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-α in rheumatoid arthritis. Nat Med 19(3):322-328.
30. Rubtsov YP, et al. (2010) Stability of the regulatory T cell lineage in vivo. Science 329(5999):1667-1671.
31. Escande C, et al. (2010) Deleted in breast cancer-1 regulates SIRT1 activity and contributes to high-fat diet-induced liver steatosis in mice. J Clin Invest 120(2):545-558.
32. Sundararajan R, Chen G, Mukherjee C, White E (2005) Caspase-dependent processing activates the proapoptotic activity of deleted in breast cancer-1 during tumor necrosis factor-alpha-mediated death signaling. Oncogene 24(31):4908-4920.
33. Lan Q, et al. (2012) Polyclonal CD4+Foxp3+ Treg cells induce TGFbeta-dependent tolerogenic dendritic cells that suppress murine lupus-like syndrome. J Mol Cell Biol 4(6):409-419.
34. Abraham MC, Shaham S (2004) Death without caspases, caspases without death. Trends Cell Biol 14(4):184-193.
35. Gao Y, et al. (2012) Molecular mechanisms underlying the regulation and functional plasticity of FOXP3(+) regulatory T cells. Genes Immun 13(1):1-13.
36. Koenen HJ, et al. (2008) Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 112(6):2340-2352.
37. Miyao T, et al. (2012) Plasticity of Foxp3(+) T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity 36(2):262-275.
38. Oldenhove G, et al. (2009) Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 31(5):772-786.
39. Wohlfert E, Belkaid Y (2010) Plasticity of T reg at infected sites. Mucosal Immunol 3(3): 213-215.
40. Grinberg-Bleyer Y, et al. (2010) Pathogenic T cells have a paradoxical protective effect in murine autoimmune diabetes by boosting Tregs. J Clin Invest 120(12):4558-4568.
41. Housley WJ, et al. (2011) Natural but not inducible regulatory T cells require TNF-alpha signaling for in vivo function. J Immunol 186(12):6779-6787.
42. Zhang Q, et al. (2013) TNF-α impairs differentiation and function of TGF-β-induced Treg cells in autoimmune diseases through Akt and Smad3 signaling pathway. J Mol Cell Biol 5(2):85-98.
43. Institute of Laboratory Animal Resources (US). Committee on Care and Use of Laboratory Animals (1996) Guide for the Care and Use of Laboratory Animals (Natl Inst Health, Bethesda), DHHS Publ No (NIH) 85-23.