Molecules and Cells

  • 제44권5호
  • /
  • Pages.318-327
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  • 2021
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  • 1016-8478(pISSN)
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  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
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Post-Translational Modifications in Transcription Factors that Determine T Helper Cell Differentiation

  • Kim, Hyo Kyeong (College of Pharmacy and Graduate School of Pharmaceutical Sciences, Ewha Womans University) ;
  • Jeong, Mi Gyeong (College of Pharmacy and Graduate School of Pharmaceutical Sciences, Ewha Womans University) ;
  • Hwang, Eun Sook (College of Pharmacy and Graduate School of Pharmaceutical Sciences, Ewha Womans University)
  • 투고 : 2021.03.11
  • 심사 : 2021.03.27
  • 발행 : 2021.05.31
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초록

CD4+ T helper (Th) cells play a crucial role in the modulation of innate and adaptive immune responses through the differentiation of Th precursor cells into several subsets, including Th1, Th2, Th17, and regulatory T (Treg) cells. Effector Th and Treg cells are distinguished by the production of signature cytokines and are important for eliminating intracellular and extracellular pathogens and maintaining immune homeostasis. Stimulation of naive Th cells by T cell receptor and specific cytokines activates master transcription factors and induces lineage specification during the differentiation of Th cells. The master transcription factors directly activate the transcription of signature cytokine genes and also undergo post-translational modifications to fine-tune cytokine production and maintain immune balance through cross-regulation with each other. This review highlights the post-translational modifications of master transcription factors that control the differentiation of effector Th and Treg cells and provides additional insights on the immune regulation mediated by protein argininemodifying enzymes in effector Th cells.

키워드

과제정보

This work was supported by grants from the National Research Foundation (2018R1A5A2025286 and 2020R1A2C2004679) funded by the Ministry of Education, Science, and Technology.

참고문헌

  1. Asano, M., Toda, M., Sakaguchi, N., and Sakaguchi, S. (1996). Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J. Exp. Med. 184, 387-396. https://doi.org/10.1084/jem.184.2.387
  2. Barber, K.W. and Rinehart, J. (2018). The ABCs of PTMs. Nat. Chem. Biol. 14, 188-192. https://doi.org/10.1038/nchembio.2572
  3. Beier, U.H., Akimova, T., Liu, Y., Wang, L., and Hancock, W.W. (2011). Histone/protein deacetylases control Foxp3 expression and the heat shock response of T-regulatory cells. Curr. Opin. Immunol. 23, 670-678. https://doi.org/10.1016/j.coi.2011.07.002
  4. Bennett, C.L., Yoshioka, R., Kiyosawa, H., Barker, D.F., Fain, P.R., Shigeoka, A.O., and Chance, P.F. (2000). X-Linked syndrome of polyendocrinopathy, immune dysfunction, and diarrhea maps to Xp11.23-Xq13.3. Am. J. Hum. Genet. 66, 461-468. https://doi.org/10.1086/302761
  5. Bettelli, E., Dastrange, M., and Oukka, M. (2005). Foxp3 interacts with nuclear factor of activated T cells and NF-kappa B to repress cytokine gene expression and effector functions of T helper cells. Proc. Natl. Acad. Sci. U. S. A. 102, 5138-5143. https://doi.org/10.1073/pnas.0501675102
  6. Boisvert, F.M., Rhie, A., Richard, S., and Doherty, A.J. (2005). The GAR motif of 53BP1 is arginine methylated by PRMT1 and is necessary for 53BP1 DNA binding activity. Cell Cycle 4, 1834-1841. https://doi.org/10.4161/cc.4.12.2250
  7. Celikkaya, H., Cosacak, M.I., Papadimitriou, C., Popova, S., Bhattarai, P., Biswas, S.N., Siddiqui, T., Wistorf, S., Nevado-Alcalde, I., Naumann, L., et al. (2019). GATA3 promotes the neural progenitor state but not neurogenesis in 3D traumatic injury model of primary human cortical astrocytes. Front. Cell. Neurosci. 13, 23. https://doi.org/10.3389/fncel.2019.00023
  8. Chang, S. and Aune, T.M. (2007). Dynamic changes in histone-methylation 'marks' across the locus encoding interferon-gamma during the differentiation of T helper type 2 cells. Nat. Immunol. 8, 723-731. https://doi.org/10.1038/ni1473
  9. Chang, Y.H., Weng, C.L., and Lin, K.I. (2020). O-GlcNAcylation and its role in the immune system. J. Biomed. Sci. 27, 57. https://doi.org/10.1186/s12929-020-00648-9
  10. Chemin, K., Gerstner, C., and Malmstrom, V. (2019). Effector functions of CD4+ T cells at the site of local autoimmune inflammation-lessons from rheumatoid arthritis. Front. Immunol. 10, 353. https://doi.org/10.3389/fimmu.2019.00353
  11. Chen, A., Lee, S.M., Gao, B., Shannon, S., Zhu, Z., and Fang, D. (2011). c-Abl-mediated tyrosine phosphorylation of the T-bet DNA-binding domain regulates CD4+ T-cell differentiation and allergic lung inflammation. Mol. Cell. Biol. 31, 3445-3456. https://doi.org/10.1128/MCB.05383-11
  12. Curran, A.M., Naik, P., Giles, J.T., and Darrah, E. (2020). PAD enzymes in rheumatoid arthritis: pathogenic effectors and autoimmune targets. Nat. Rev. Rheumatol. 16, 301-315. https://doi.org/10.1038/s41584-020-0409-1
  13. de Jesus, T.J., Tomalka, J.A., Centore, J.T., Staback Rodriguez, F.D., Agarwal, R.A., Liu, A.R., Kern, T.S., and Ramakrishnan, P. (2021). Negative regulation of FOXP3 expression by c-Rel O-GlcNAcylation. Glycobiology 2021 Jan 12 [Epub]. https://doi.org/10.1093/glycob/cwab001
  14. Deng, G., Nagai, Y., Xiao, Y., Li, Z., Dai, S., Ohtani, T., Banham, A., Li, B., Wu, S.L., Hancock, W., et al. (2015). Pim-2 kinase influences regulatory T cell function and stability by mediating Foxp3 protein N-terminal phosphorylation. J. Biol. Chem. 290, 20211-20220. https://doi.org/10.1074/jbc.M115.638221
  15. d'Hennezel, E., Bin Dhuban, K., Torgerson, T., and Piccirillo, C.A. (2012). The immunogenetics of immune dysregulation, polyendocrinopathy, enteropathy, X linked (IPEX) syndrome. J. Med. Genet. 49, 291-302. https://doi.org/10.1136/jmedgenet-2012-100759
  16. Donald, J.E., Kulp, D.W., and DeGrado, W.F. (2011). Salt bridges: geometrically specific, designable interactions. Proteins 79, 898-915. https://doi.org/10.1002/prot.22927
  17. Duan, G. and Walther, D. (2015). The roles of post-translational modifications in the context of protein interaction networks. PLoS Comput. Biol. 11, e1004049. https://doi.org/10.1371/journal.pcbi.1004049
  18. DuPage, M. and Bluestone, J.A. (2016). Harnessing the plasticity of CD4(+) T cells to treat immune-mediated disease. Nat. Rev. Immunol. 16, 149-163. https://doi.org/10.1038/nri.2015.18
  19. Fuhrmann, J., Clancy, K.W., and Thompson, P.R. (2015). Chemical biology of protein arginine modifications in epigenetic regulation. Chem. Rev. 115, 5413-5461. https://doi.org/10.1021/acs.chemrev.5b00003
  20. Glozak, M.A., Sengupta, N., Zhang, X., and Seto, E. (2005). Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23. https://doi.org/10.1016/j.gene.2005.09.010
  21. Guccione, E. and Richard, S. (2019). The regulation, functions and clinical relevance of arginine methylation. Nat. Rev. Mol. Cell Biol. 20, 642-657. https://doi.org/10.1038/s41580-019-0155-x
  22. Han, L., Yang, J., Wang, X., Wu, Q., Yin, S., Li, Z., Zhang, J., Xing, Y., Chen, Z., Tsun, A., et al. (2014). The E3 deubiquitinase USP17 is a positive regulator of retinoic acid-related orphan nuclear receptor gammat (RORgammat) in Th17 cells. J. Biol. Chem. 289, 25546-25555. https://doi.org/10.1074/jbc.M114.565291
  23. Harris, M.L., Darrah, E., Lam, G.K., Bartlett, S.J., Giles, J.T., Grant, A.V., Gao, P., Scott, W.W., Jr., El-Gabalawy, H., Casciola-Rosen, L., et al. (2008). Association of autoimmunity to peptidyl arginine deiminase type 4 with genotype and disease severity in rheumatoid arthritis. Arthritis Rheum. 58, 1958-1967. https://doi.org/10.1002/art.23596
  24. Ho, I.C., Hodge, M.R., Rooney, J.W., and Glimcher, L.H. (1996). The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85, 973-983. https://doi.org/10.1016/S0092-8674(00)81299-4
  25. Hori, S., Nomura, T., and Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061. https://doi.org/10.1126/science.1079490
  26. Hosokawa, H., Kato, M., Tohyama, H., Tamaki, Y., Endo, Y., Kimura, M.Y., Tumes, D.J., Motohashi, S., Matsumoto, M., Nakayama, K.I., et al. (2015). Methylation of Gata3 protein at Arg-261 regulates transactivation of the Il5 gene in T helper 2 cells. J. Biol. Chem. 290, 13095-13103. https://doi.org/10.1074/jbc.M114.621524
  27. Hosokawa, H., Tanaka, T., Endo, Y., Kato, M., Shinoda, K., Suzuki, A., Motohashi, S., Matsumoto, M., Nakayama, K.I., and Nakayama, T. (2016). Akt1-mediated Gata3 phosphorylation controls the repression of IFNgamma in memory-type Th2 cells. Nat. Commun. 7, 11289. https://doi.org/10.1038/ncomms11289
  28. Hsu, C.Y., Fu, S.H., Chien, M.W., Liu, Y.W., Chen, S.J., and Sytwu, H.K. (2020). Post-translational modifications of transcription factors harnessing the etiology and pathophysiology in colonic diseases. Int. J. Mol. Sci. 21, 3207. https://doi.org/10.3390/ijms21093207
  29. Hsu, C.Y., Yeh, L.T., Fu, S.H., Chien, M.W., Liu, Y.W., Miaw, S.C., Chang, D.M., and Sytwu, H.K. (2018). SUMO-defective c-Maf preferentially transactivates Il21 to exacerbate autoimmune diabetes. J. Clin. Invest. 128, 3779-3793. https://doi.org/10.1172/JCI98786
  30. Hwang, E.S., Hong, J.H., and Glimcher, L.H. (2005a). IL-2 production in developing Th1 cells is regulated by heterodimerization of RelA and T-bet and requires T-bet serine residue 508. J. Exp. Med. 202, 1289-1300. https://doi.org/10.1084/jem.20051044
  31. Hwang, E.S., Szabo, S.J., Schwartzberg, P.L., and Glimcher, L.H. (2005b). T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3. Science 307, 430-433. https://doi.org/10.1126/science.1103336
  32. Hwang, J.R., Byeon, Y., Kim, D., and Park, S.G. (2020). Recent insights of T cell receptor-mediated signaling pathways for T cell activation and development. Exp. Mol. Med. 52, 750-761. https://doi.org/10.1038/s12276-020-0435-8
  33. Imbratta, C., Hussein, H., Andris, F., and Verdeil, G. (2020). c-MAF, a Swiss army knife for tolerance in lymphocytes. Front. Immunol. 11, 206. https://doi.org/10.3389/fimmu.2020.00206
  34. Ivanov, I.I., McKenzie, B.S., Zhou, L., Tadokoro, C.E., Lepelley, A., Lafaille, J.J., Cua, D.J., and Littman, D.R. (2006). The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126, 1121-1133. https://doi.org/10.1016/j.cell.2006.07.035
  35. Jang, E.J., Park, H.R., Hong, J.H., and Hwang, E.S. (2013). Lysine 313 of T-box is crucial for modulation of protein stability, DNA binding, and threonine phosphorylation of T-bet. J. Immunol. 190, 5764-5770. https://doi.org/10.4049/jimmunol.1203403
  36. Jenner, R.G., Townsend, M.J., Jackson, I., Sun, K., Bouwman, R.D., Young, R.A., Glimcher, L.H., and Lord, G.M. (2009). The transcription factors T-bet and GATA-3 control alternative pathways of T-cell differentiation through a shared set of target genes. Proc. Natl. Acad. Sci. U. S. A. 106, 17876-17881. https://doi.org/10.1073/pnas.0909357106
  37. Kagoya, Y., Saijo, H., Matsunaga, Y., Guo, T., Saso, K., Anczurowski, M., Wang, C.H., Sugata, K., Murata, K., Butler, M.O., et al. (2019). Arginine methylation of FOXP3 is crucial for the suppressive function of regulatory T cells. J. Autoimmun. 97, 10-21. https://doi.org/10.1016/j.jaut.2018.09.011
  38. Kaplan, M.H., Schindler, U., Smiley, S.T., and Grusby, M.J. (1996). Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4, 313-319. https://doi.org/10.1016/S1074-7613(00)80439-2
  39. Kathania, M., Khare, P., Zeng, M., Cantarel, B., Zhang, H., Ueno, H., and Venuprasad, K. (2016). Itch inhibits IL-17-mediated colon inflammation and tumorigenesis by ROR-gammat ubiquitination. Nat. Immunol. 17, 997-1004. https://doi.org/10.1038/ni.3488
  40. Kitagawa, K., Shibata, K., Matsumoto, A., Matsumoto, M., Ohhata, T., Nakayama, K.I., Niida, H., and Kitagawa, M. (2014). Fbw7 targets GATA3 through cyclin-dependent kinase 2-dependent proteolysis and contributes to regulation of T-cell development. Mol. Cell. Biol. 34, 2732-2744. https://doi.org/10.1128/MCB.01549-13
  41. Kumar, S., Tsai, C.J., and Nussinov, R. (2000). Factors enhancing protein thermostability. Protein Eng. 13, 179-191. https://doi.org/10.1093/protein/13.3.179
  42. Kwon, H.S., Lim, H.W., Wu, J., Schnolzer, M., Verdin, E., and Ott, M. (2012). Three novel acetylation sites in the Foxp3 transcription factor regulate the suppressive activity of regulatory T cells. J. Immunol. 188, 2712-2721. https://doi.org/10.4049/jimmunol.1100903
  43. Lanouette, S., Mongeon, V., Figeys, D., and Couture, J.F. (2014). The functional diversity of protein lysine methylation. Mol. Syst. Biol. 10, 724. https://doi.org/10.1002/msb.134974
  44. Lazarevic, V., Chen, X., Shim, J.H., Hwang, E.S., Jang, E., Bolm, A.N., Oukka, M., Kuchroo, V.K., and Glimcher, L.H. (2011). T-bet represses T(H)17 differentiation by preventing Runx1-mediated activation of the gene encoding RORgammat. Nat. Immunol. 12, 96-104. https://doi.org/10.1038/ni.1969
  45. Leavenworth, J.W., Ma, X., Mo, Y.Y., and Pauza, M.E. (2009). SUMO conjugation contributes to immune deviation in nonobese diabetic mice by suppressing c-Maf transactivation of IL-4. J. Immunol. 183, 1110-1119. https://doi.org/10.4049/jimmunol.0803671
  46. Li, B., Samanta, A., Song, X., Iacono, K.T., Bembas, K., Tao, R., Basu, S., Riley, J.L., Hancock, W.W., Shen, Y., et al. (2007). FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression. Proc. Natl. Acad. Sci. U. S. A. 104, 4571-4576. https://doi.org/10.1073/pnas.0700298104
  47. Li, Y., Lu, Y., Wang, S., Han, Z., Zhu, F., Ni, Y., Liang, R., Zhang, Y., Leng, Q., Wei, G., et al. (2016). USP21 prevents the generation of T-helper-1-like Treg cells. Nat. Commun. 7, 13559. https://doi.org/10.1038/ncomms13559
  48. Li, Z., Lin, F., Zhuo, C., Deng, G., Chen, Z., Yin, S., Gao, Z., Piccioni, M., Tsun, A., Cai, S., 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, 26872-26881. https://doi.org/10.1074/jbc.M114.586651
  49. Lim, H.W., Kang, S.G., Ryu, J.K., Schilling, B., Fei, M., Lee, I.S., Kehasse, A., Shirakawa, K., Yokoyama, M., Schnolzer, M., et al. (2015). SIRT1 deacetylates RORgammat and enhances Th17 cell generation. J. Exp. Med. 212, 973. https://doi.org/10.1084/jem.2013237805062015c
  50. Lin, B.S., Tsai, P.Y., Hsieh, W.Y., Tsao, H.W., Liu, M.W., Grenningloh, R., Wang, L.F., Ho, I.C., and Miaw, S.C. (2010). SUMOylation attenuates c-Mafdependent IL-4 expression. Eur. J. Immunol. 40, 1174-1184. https://doi.org/10.1002/eji.200939788
  51. Liu, B., Salgado, O.C., Singh, S., Hippen, K.L., Maynard, J.C., Burlingame, A.L., Ball, L.E., Blazar, B.R., Farrar, M.A., Hogquist, K.A., et al. (2019). The lineage stability and suppressive program of regulatory T cells require protein O-GlcNAcylation. Nat. Commun. 10, 354. https://doi.org/10.1038/s41467-019-08300-3
  52. Liu, C.C., Lai, C.Y., Yen, W.F., Lin, Y.H., Chang, H.H., Tai, T.S., Lu, Y.J., Tsao, H.W., Ho, I.C., and Miaw, S.C. (2015). Reciprocal regulation of C-Maf tyrosine phosphorylation by Tec and Ptpn22. PLoS One 10, e0127617. https://doi.org/10.1371/journal.pone.0127617
  53. Liu, Y., Lightfoot, Y.L., Seto, N., Carmona-Rivera, C., Moore, E., Goel, R., O'Neil, L., Mistry, P., Hoffmann, V., Mondal, S., et al. (2018). Peptidylarginine deiminases 2 and 4 modulate innate and adaptive immune responses in TLR-7-dependent lupus. JCI Insight 3, e124729. https://doi.org/10.1172/jci.insight.124729
  54. Marth, J.D. and Grewal, P.K. (2008). Mammalian glycosylation in immunity. Nat. Rev. Immunol. 8, 874-887. https://doi.org/10.1038/nri2417
  55. Martinez-Sanchez, M.E., Huerta, L., Alvarez-Buylla, E.R., and Villarreal Lujan, C. (2018). Role of cytokine combinations on CD4+ T cell differentiation, partial polarization, and plasticity: continuous network modeling approach. Front. Physiol. 9, 877. https://doi.org/10.3389/fphys.2018.00877
  56. Morawski, P.A., Mehra, P., Chen, C., Bhatti, T., and Wells, A.D. (2013). Foxp3 protein stability is regulated by cyclin-dependent kinase 2. J. Biol. Chem. 288, 24494-24502. https://doi.org/10.1074/jbc.M113.467704
  57. Nagai, Y., Ji, M.Q., Zhu, F., Xiao, Y., Tanaka, Y., Kambayashi, T., Fujimoto, S., Goldberg, M.M., Zhang, H., Li, B., et al. (2019). PRMT5 associates with the FOXP3 homomer and when disabled enhances targeted p185(erbB2/neu) tumor immunotherapy. Front. Immunol. 10, 174. https://doi.org/10.3389/fimmu.2019.00174
  58. Nie, H., Zheng, Y., Li, R., Guo, T.B., He, D., Fang, L., Liu, X., Xiao, L., Chen, X., Wan, B., et al. (2013). Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-alpha in rheumatoid arthritis. Nat. Med. 19, 322-328. https://doi.org/10.1038/nm.3085
  59. Ono, M., Yaguchi, H., Ohkura, N., Kitabayashi, I., Nagamura, Y., Nomura, T., Miyachi, Y., Tsukada, T., and Sakaguchi, S. (2007). Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446, 685-689. https://doi.org/10.1038/nature05673
  60. Ostroumov, D., Fekete-Drimusz, N., Saborowski, M., Kuhnel, F., and Woller, N. (2018). CD4 and CD8 T lymphocyte interplay in controlling tumor growth. Cell. Mol. Life Sci. 75, 689-713. https://doi.org/10.1007/s00018-017-2686-7
  61. Pai, S.Y., Truitt, M.L., and Ho, I.C. (2004). GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells. Proc. Natl. Acad. Sci. U. S. A. 101, 1993-1998. https://doi.org/10.1073/pnas.0308697100
  62. Pan, F., Yu, H., Dang, E.V., Barbi, J., Pan, X., Grosso, J.F., Jinasena, D., Sharma, S.M., McCadden, E.M., Getnet, D., et al. (2009). Eos mediates Foxp3-dependent gene silencing in CD4+ regulatory T cells. Science 325, 1142-1146. https://doi.org/10.1126/science.1176077
  63. Pawlak, M., Ho, A.W., and Kuchroo, V.K. (2020). Cytokines and transcription factors in the differentiation of CD4(+) T helper cell subsets and induction of tissue inflammation and autoimmunity. Curr. Opin. Immunol. 67, 57-67. https://doi.org/10.1016/j.coi.2020.09.001
  64. Ramakrishnan, P., Clark, P.M., Mason, D.E., Peters, E.C., Hsieh-Wilson, L.C., and Baltimore, D. (2013). Activation of the transcriptional function of the NF-kappaB protein c-Rel by O-GlcNAc glycosylation. Sci. Signal. 6, ra75. https://doi.org/10.1126/scisignal.2004097
  65. Roberts, C.A., Dickinson, A.K., and Taams, L.S. (2015). The interplay between monocytes/macrophages and CD4(+) T cell subsets in rheumatoid arthritis. Front. Immunol. 6, 571.
  66. Ruterbusch, M., Pruner, K.B., Shehata, L., and Pepper, M. (2020). In vivo CD4(+) T cell differentiation and function: revisiting the Th1/Th2 paradigm. Annu. Rev. Immunol. 38, 705-725. https://doi.org/10.1146/annurev-immunol-103019-085803
  67. Rutz, S., Kayagaki, N., Phung, Q.T., Eidenschenk, C., Noubade, R., Wang, X., Lesch, J., Lu, R., Newton, K., Huang, O.W., et al. (2015). Deubiquitinase DUBA is a post-translational brake on interleukin-17 production in T cells. Nature 518, 417-421. https://doi.org/10.1038/nature13979
  68. Rutz, S. and Ouyang, W. (2016). The Itch to degrade ROR-gammat. Nat. Immunol. 17, 898-900. https://doi.org/10.1038/ni.3516
  69. Sen, S., He, Z., Ghosh, S., Dery, K.J., Yang, L., Zhang, J., and Sun, Z. (2018). PRMT1 plays a critical role in Th17 differentiation by regulating reciprocal recruitment of STAT3 and STAT5. J. Immunol. 201, 440-450. https://doi.org/10.4049/jimmunol.1701654
  70. Shevyrev, D. and Tereshchenko, V. (2019). Treg heterogeneity, function, and homeostasis. Front. Immunol. 10, 3100. https://doi.org/10.3389/fimmu.2019.03100
  71. Singh, A.K., Khare, P., Obaid, A., Conlon, K.P., Basrur, V., DePinho, R.A., and Venuprasad, K. (2018). SUMOylation of ROR-gammat inhibits IL-17 expression and inflammation via HDAC2. Nat. Commun. 9, 4515. https://doi.org/10.1038/s41467-018-06924-5
  72. Snyder, K.J., Zitzer, N.C., Gao, Y., Choe, H.K., Sell, N.E., Neidemire-Colley, L., Ignaci, A., Kale, C., Devine, R.D., Abad, M.G., et al. (2020). PRMT5 regulates T cell interferon response and is a target for acute graft-versus-host disease. JCI Insight 5, e131099. https://doi.org/10.1172/jci.insight.131099
  73. Song, N., Cao, C., Tang, Y., Bi, L., Jiang, Y., Zhou, Y., Song, X., Liu, L., and Ge, W. (2018). The ubiquitin ligase SCF(FBXW7alpha) promotes GATA3 degradation. J. Cell. Physiol. 233, 2366-2377. https://doi.org/10.1002/jcp.26108
  74. Sun, B., Chang, H.H., Salinger, A., Tomita, B., Bawadekar, M., Holmes, C.L., Shelef, M.A., Weerapana, E., Thompson, P.R., and Ho, I.C. (2019). Reciprocal regulation of Th2 and Th17 cells by PAD2-mediated citrullination. JCI Insight 4, e129687. https://doi.org/10.1172/jci.insight.129687
  75. Swiercz, R., Cheng, D., Kim, D., and Bedford, M.T. (2007). Ribosomal protein rpS2 is hypomethylated in PRMT3-deficient mice. J. Biol. Chem. 282, 16917-16923. https://doi.org/10.1074/jbc.M609778200
  76. Szabo, S.J., Kim, S.T., Costa, G.L., Zhang, X., Fathman, C.G., and Glimcher, L.H. (2000). A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655-669. https://doi.org/10.1016/S0092-8674(00)80702-3
  77. Szabo, S.J., Sullivan, B.M., Stemmann, C., Satoskar, A.R., Sleckman, B.P., and Glimcher, L.H. (2002). Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 295, 338-342. https://doi.org/10.1126/science.1065543
  78. Tanaka, Y., Nagai, Y., Okumura, M., Greene, M.I., and Kambayashi, T. (2020). PRMT5 is required for T cell survival and proliferation by maintaining cytokine signaling. Front. Immunol. 11, 621. https://doi.org/10.3389/fimmu.2020.00621
  79. Tay, C., Kanellakis, P., Hosseini, H., Cao, A., Toh, B.H., Bobik, A., and Kyaw, T. (2019). B cell and CD4 T cell interactions promote development of atherosclerosis. Front. Immunol. 10, 3046. https://doi.org/10.3389/fimmu.2019.03046
  80. van Loosdregt, J., Brunen, D., Fleskens, V., Pals, C.E., Lam, E.W., and Coffer, P.J. (2011). Rapid temporal control of Foxp3 protein degradation by sirtuin-1. PLoS One 6, e19047. https://doi.org/10.1371/journal.pone.0019047
  81. van Loosdregt, J., Fleskens, V., Fu, J., Brenkman, A.B., Bekker, C.P., Pals, C.E., Meerding, J., Berkers, C.R., Barbi, J., Grone, A., et al. (2013a). Stabilization of the transcription factor Foxp3 by the deubiquitinase USP7 increases Treg-cell-suppressive capacity. Immunity 39, 259-271. https://doi.org/10.1016/j.immuni.2013.05.018
  82. van Loosdregt, J., Fleskens, V., Tiemessen, M.M., Mokry, M., van Boxtel, R., Meerding, J., Pals, C.E., Kurek, D., Baert, M.R., Delemarre, E.M., et al. (2013b). Canonical Wnt signaling negatively modulates regulatory T cell function. Immunity 39, 298-310. https://doi.org/10.1016/j.immuni.2013.07.019
  83. van Loosdregt, J., Vercoulen, Y., Guichelaar, T., Gent, Y.Y., Beekman, J.M., van Beekum, O., Brenkman, A.B., Hijnen, D.J., Mutis, T., Kalkhoven, E., et al. (2010). Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood 115, 965-974. https://doi.org/10.1182/blood-2009-02-207118
  84. Virag, D., Dalmadi-Kiss, B., Vekey, K., Drahos, L., Klebovich, I., Antal, I., and Ludanyi, K. (2020). Current trends in the analysis of post-translational modifications. Chromatographia 83, 1-10. https://doi.org/10.1007/s10337-019-03796-9
  85. Walsh, G. and Jefferis, R. (2006). Post-translational modifications in the context of therapeutic proteins. Nat. Biotechnol. 24, 1241-1252. https://doi.org/10.1038/nbt1252
  86. Wang, A., Zhu, F., Liang, R., Li, D., and Li, B. (2019). Regulation of T cell differentiation and function by ubiquitin-specific proteases. Cell. Immunol. 340, 103922. https://doi.org/10.1016/j.cellimm.2019.103922
  87. Wang, L., de Zoeten, E.F., Greene, M.I., and Hancock, W.W. (2009). Immunomodulatory effects of deacetylase inhibitors: therapeutic targeting of FOXP3+ regulatory T cells. Nat. Rev. Drug Discov. 8, 969-981. https://doi.org/10.1038/nrd3031
  88. Wang, X., Yang, J., Han, L., Zhao, K., Wu, Q., Bao, L., Li, Z., Lv, L., and Li, B. (2015). TRAF5-mediated Lys-63-linked polyubiquitination plays an essential role in positive regulation of RORgammat in promoting IL-17A expression. J. Biol. Chem. 290, 29086-29094. https://doi.org/10.1074/jbc.M115.664573
  89. Webb, L.M., Amici, S.A., Jablonski, K.A., Savardekar, H., Panfil, A.R., Li, L., Zhou, W., Peine, K., Karkhanis, V., Bachelder, E.M., et al. (2017). PRMT5-selective inhibitors suppress inflammatory t cell responses and experimental autoimmune encephalomyelitis. J. Immunol. 198, 1439-1451. https://doi.org/10.4049/jimmunol.1601702
  90. Wu, Q., Nie, J., Gao, Y., Xu, P., Sun, Q., Yang, J., Han, L., Chen, Z., Wang, X., Lv, L., et al. (2015). Reciprocal regulation of RORgammat acetylation and function by p300 and HDAC1. Sci. Rep. 5, 16355. https://doi.org/10.1038/srep16355
  91. Wu, Y., Borde, M., Heissmeyer, V., Feuerer, M., Lapan, A.D., Stroud, J.C., Bates, D.L., Guo, L., Han, A., Ziegler, S.F., et al. (2006). FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 126, 375-387. https://doi.org/10.1016/j.cell.2006.05.042
  92. Yamagata, T., Mitani, K., Oda, H., Suzuki, T., Honda, H., Asai, T., Maki, K., Nakamoto, T., and Hirai, H. (2000). Acetylation of GATA-3 affects T-cell survival and homing to secondary lymphoid organs. EMBO J. 19, 4676-4687. https://doi.org/10.1093/emboj/19.17.4676
  93. Yamashita, M., Ukai-Tadenuma, M., Miyamoto, T., Sugaya, K., Hosokawa, H., Hasegawa, A., Kimura, M., Taniguchi, M., DeGregori, J., and Nakayama, T. (2004). Essential role of GATA3 for the maintenance of type 2 helper T (Th2) cytokine production and chromatin remodeling at the Th2 cytokine gene loci. J. Biol. Chem. 279, 26983-26990. https://doi.org/10.1074/jbc.M403688200
  94. Yan, F., Mo, X., Liu, J., Ye, S., Zeng, X., and Chen, D. (2017). Thymic function in the regulation of T cells, and molecular mechanisms underlying the modulation of cytokines and stress signaling (Review). Mol. Med. Rep. 16, 7175-7184. https://doi.org/10.3892/mmr.2017.7525
  95. Yang, Y. and Bedford, M.T. (2013). Protein arginine methyltransferases and cancer. Nat. Rev. Cancer 13, 37-50. https://doi.org/10.1038/nrc3409
  96. Yang, Y., He, Y., Wang, X., Liang, Z., He, G., Zhang, P., Zhu, H., Xu, N., and Liang, S. (2017). Protein SUMOylation modification and its associations with disease. Open Biol. 7, 170167. https://doi.org/10.1098/rsob.170167
  97. Young, R.L., Page, A.J., Cooper, N.J., Frisby, C.L., and Blackshaw, L.A. (2010). Sensory and motor innervation of the crural diaphragm by the vagus nerves. Gastroenterology 138, 1091-1101.e5. https://doi.org/10.1053/j.gastro.2009.08.053
  98. Zaidan, N. and Ottersbach, K. (2018). The multi-faceted role of Gata3 in developmental haematopoiesis. Open Biol. 8, 180152. https://doi.org/10.1098/rsob.180152
  99. Zhang, Z., Tong, J., Tang, X., Juan, J., Cao, B., Hurren, R., Chen, G., Taylor, P., Xu, X., Shi, C.X., et al. (2016). The ubiquitin ligase HERC4 mediates c-Maf ubiquitination and delays the growth of multiple myeloma xenografts in nude mice. Blood 127, 1676-1686. https://doi.org/10.1182/blood-2015-07-658203
  100. Zhao, X., Zheng, B., Huang, Y., Yang, D., Katzman, S., Chang, C., Fowell, D., and Zeng, W.P. (2007). Interaction between GATA-3 and the transcriptional coregulator Pias1 is important for the regulation of Th2 immune responses. J. Immunol. 179, 8297-8304. https://doi.org/10.4049/jimmunol.179.12.8297
  101. Zhu, J. (2017). GATA3 regulates the development and functions of innate lymphoid cell subsets at multiple stages. Front. Immunol. 8, 1571. https://doi.org/10.3389/fimmu.2017.01571
  102. Zhu, J., Jankovic, D., Oler, A.J., Wei, G., Sharma, S., Hu, G., Guo, L., Yagi, R., Yamane, H., Punkosdy, G., et al. (2012). The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses. Immunity 37, 660-673. https://doi.org/10.1016/j.immuni.2012.09.007
  103. Zhu, J., Yamane, H., and Paul, W.E. (2010). Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489. https://doi.org/10.1146/annurev-immunol-030409-101212

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