Two Histone/Protein Acetyltransferases, CBP and p300, Are Indispensable for Foxp3⁺ T-Regulatory Cell Development and Function

REFERENCES

• Roth SY, Denu JM, Allis CD. 2001. Histone acetyltransferases. Annu. Rev. Biochem. 70:81–120. http://dx.doi.org/10.1146/annurev.biochem.70.1.81.
   PubMed Web of Science ®Google Scholar
• Wang L, Tang Y, Cole PA, Marmorstein R. 2008. Structure and chemistry of the p300/CBP and Rtt109 histone acetyltransferases: implications for histone acetyltransferase evolution and function. Curr. Opin. Struct. Biol. 18:741–747. http://dx.doi.org/10.1016/j.sbi.2008.09.004.
   PubMed Web of Science ®Google Scholar
• Marmorstein R. 2001. Structure of histone acetyltransferases. J. Mol. Biol. 311:433–444. http://dx.doi.org/10.1006/jmbi.2001.4859.
   PubMed Web of Science ®Google Scholar
• Chan HM, La Thangue NB. 2001. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell Sci. 114:2363–2373.
   PubMed Web of Science ®Google Scholar
• Yao TP, Oh SP, Fuchs M, Zhou ND, Ch'ng LE, Newsome D, Bronson RT, Li E, Livingston DM, Eckner R. 1998. Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 93:361–372. http://dx.doi.org/10.1016/S0092-8674(00)81165-4.
   PubMed Web of Science ®Google Scholar
• Tanaka Y, Naruse I, Hongo T, Xu M, Nakahata T, Maekawa T, Ishii S. 2000. Extensive brain hemorrhage and embryonic lethality in a mouse null mutant of CREB-binding protein. Mech. Dev. 95:133–145. http://dx.doi.org/10.1016/S0925-4773(00)00360-9.
   PubMed Web of Science ®Google Scholar
• McManus KJ, Hendzel MJ. 2003. Quantitative analysis of CBP- and P300-induced histone acetylations in vivo using native chromatin. Mol. Cell. Biol. 23:7611–7627. http://dx.doi.org/10.1128/MCB.23.21.7611-7627.2003.
   PubMedGoogle Scholar
• Liu X, Wang L, Zhao K, Thompson PR, Hwang Y, Marmorstein R, Cole PA. 2008. The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 451:846–850. http://dx.doi.org/10.1038/nature06546.
   PubMed Web of Science ®Google Scholar
• Henry RA, Kuo YM, Andrews AJ. 2013. Differences in specificity and selectivity between CBP and p300 acetylation of histone H3 and H3/H4. Biochemistry 52:5746–5759. http://dx.doi.org/10.1021/bi400684q.
   PubMed Web of Science ®Google Scholar
• Ma H, Nguyen C, Lee KS, Kahn M. 2005. Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene 24:3619–3631. http://dx.doi.org/10.1038/sj.onc.1208433.
   PubMed Web of Science ®Google Scholar
• Kasper LH, Fukuyama T, Biesen MA, Boussouar F, Tong C, de Pauw A, Murray PJ, van Deursen JM, Brindle PK. 2006. Conditional knockout mice reveal distinct functions for the global transcriptional coactivators CBP and p300 in T-cell development. Mol. Cell. Biol. 26:789–809. http://dx.doi.org/10.1128/MCB.26.3.789-809.2006.
   PubMed Web of Science ®Google Scholar
• Fukuyama T, Kasper LH, Boussouar F, Jeevan T, van Deursen J, Brindle PK. 2009. Histone acetyltransferase CBP is vital to demarcate conventional and innate CD8+ T-cell development. Mol. Cell. Biol. 29:3894–3904. http://dx.doi.org/10.1128/MCB.01598-08.
   PubMedGoogle Scholar
• Kawasaki H, Eckner R, Yao TP, Taira K, Chiu R, Livingston DM, Yokoyama KK. 1998. Distinct roles of the co-activators p300 and CBP in retinoic-acid-induced F9-cell differentiation. Nature 393:284–289. http://dx.doi.org/10.1038/30538.
   PubMed Web of Science ®Google Scholar
• Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F. 2001. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27:68–73. http://dx.doi.org/10.1038/83784.
   PubMed Web of Science ®Google Scholar
• Khattri R, Kasprowicz D, Cox T, Mortrud M, Appleby MW, Brunkow ME, Ziegler SF, Ramsdell F. 2001. The amount of scurfin protein determines peripheral T cell number and responsiveness. J. Immunol. 167:6312–6320. http://dx.doi.org/10.4049/jimmunol.167.11.6312.
   PubMed Web of Science ®Google Scholar
• Liu B, Tahk S, Yee KM, Fan G, Shuai K. 2010. The ligase PIAS1 restricts natural regulatory T cell differentiation by epigenetic repression. Science 330:521–525. http://dx.doi.org/10.1126/science.1193787.
   PubMedGoogle Scholar
• Floess S, Freyer J, Siewert C, Baron U, Olek S, Polansky J, Schlawe K, Chang HD, Bopp T, Schmitt E, Klein-Hessling S, Serfling E, Hamann A, Huehn J. 2007. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 5:e38. http://dx.doi.org/10.1371/journal.pbio.0050038.
   PubMed Web of Science ®Google Scholar
• Bettini ML, Pan F, Bettini M, Finkelstein D, Rehg JE, Floess S, Bell BD, Ziegler SF, Huehn J, Pardoll DM, Vignali DA. 2012. Loss of epigenetic modification driven by the Foxp3 transcription factor leads to regulatory T cell insufficiency. Immunity 36:717–730. http://dx.doi.org/10.1016/j.immuni.2012.03.020.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang L, Predina J, Han R, Beier UH, Wang LC, Kapoor V, Bhatti TR, Akimova T, Singhal S, Brindle PK, Cole PA, Albelda SM, Hancock WW. 2013. Inhibition of p300 impairs Foxp3+ T regulatory cell function and promotes antitumor immunity. Nat. Med. 19:1173–1177. http://dx.doi.org/10.1038/nm.3286.
   PubMed Web of Science ®Google Scholar
• Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, Ye X, Treuting P, Siewe L, Roers A, Henderson WRJr, Muller W, Rudensky AY. 2008. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28:546–558. http://dx.doi.org/10.1016/j.immuni.2008.02.017.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang L, Han R, Beier UH, Hancock WW. 2012. Two lysines in the forkhead domain of foxp3 are key to T regulatory cell function. PLoS One 7:e29035. http://dx.doi.org/10.1371/journal.pone.0029035.
   PubMed Web of Science ®Google Scholar
• Koh KP, Sundrud MS, Rao A. 2009. Domain requirements and sequence specificity of DNA binding for the forkhead transcription factor FOXP3. PLoS One 4:e8109. http://dx.doi.org/10.1371/journal.pone.0008109.
   PubMed Web of Science ®Google Scholar
• Wang L, Liu Y, Beier UH, Han R, Bhatti TR, Akimova T, Hancock WW. 2013. Foxp3+ T-regulatory cells require DNA methyltransferase 1 expression to prevent development of lethal autoimmunity. Blood 121:3631–3639. http://dx.doi.org/10.1182/blood-2012-08-451765.
   PubMed Web of Science ®Google Scholar
• Battke F, Symons S, Nieselt K. 2010. Mayday–integrative analytics for expression data. BMC Bioinformatics 11:121. http://dx.doi.org/10.1186/1471-2105-11-121.
   PubMedGoogle Scholar
• Kim HP, Leonard WJ. 2007. CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: a role for DNA methylation. J. Exp. Med. 204:1543–1551. http://dx.doi.org/10.1084/jem.20070109.
   PubMed Web of Science ®Google Scholar
• Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH. 1993. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855–859. http://dx.doi.org/10.1038/365855a0.
   PubMed Web of Science ®Google Scholar
• Cardinaux JR, Notis JC, Zhang Q, Vo N, Craig JC, Fass DM, Brennan RG, Goodman RH. 2000. Recruitment of CREB binding protein is sufficient for CREB-mediated gene activation. Mol. Cell. Biol. 20:1546–1552. http://dx.doi.org/10.1128/MCB.20.5.1546-1552.2000.
   PubMed Web of Science ®Google Scholar
• Krenger W, Rossi S, Piali L, Hollander GA. 2000. Thymic atrophy in murine acute graft-versus-host disease is effected by impaired cell cycle progression of host pro-T and pre-T cells. Blood 96:347–354.
   PubMed Web of Science ®Google Scholar
• Belhacéne N, Gamas P, Gonçalvès D, Jacquin M, Beneteau M, Jacquel A, Colosetti P, Ricci JE, Wakkach A, Auberger P, Marchetti S. 2012. Severe thymic atrophy in a mouse model of skin inflammation accounts for impaired TNFR1 signaling. PLoS One 7:e47321. http://dx.doi.org/10.1371/journal.pone.0047321.
   PubMedGoogle Scholar
• Kitoh A, Ono M, Naoe Y, Ohkura N, Yamaguchi T, Yaguchi H, Kitabayashi I, Tsukada T, Nomura T, Miyachi Y, Taniuchi I, Sakaguchi S. 2009. Indispensable role of the Runx1-Cbfbeta transcription complex for in vivo-suppressive function of FoxP3+ regulatory T cells. Immunity 31:609–620. http://dx.doi.org/10.1016/j.immuni.2009.09.003.
   PubMed Web of Science ®Google Scholar
• Ruan Q, Kameswaran V, Tone Y, Li L, Liou HC, Greene MI, Tone M, Chen YH. 2009. Development of Foxp3(+) regulatory t cells is driven by the c-Rel enhanceosome. Immunity 31:932–940. http://dx.doi.org/10.1016/j.immuni.2009.10.006.
   PubMed Web of Science ®Google Scholar
• van Loosdregt J, Vercoulen Y, Guichelaar T, Gent YY, Beekman JM, van Beekum O, Brenkman AB, Hijnen DJ, Mutis T, Kalkhoven E, Prakken BJ, Coffer PJ. 2010. Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood 115:965–974. http://dx.doi.org/10.1182/blood-2009-02-207118.
   PubMed Web of Science ®Google Scholar
• Kwon HS, Lim HW, Wu J, Schnolzer M, Verdin E, 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. http://dx.doi.org/10.4049/jimmunol.1100903.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Josefowicz SZ, Kas A, Chu TT, Gavin MA, Rudensky AY. 2007. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445:936–940. http://dx.doi.org/10.1038/nature05563.
   PubMed Web of Science ®Google Scholar
• Pan F, Yu H, Dang EV, Barbi J, Pan X, Grosso JF, Jinasena D, Sharma SM, McCadden EM, Getnet D, Drake CG, Liu JO, Ostrowski MC, Pardoll DM. 2009. Eos mediates Foxp3-dependent gene silencing in CD4+ regulatory T cells. Science 325:1142–1146. http://dx.doi.org/10.1126/science.1176077.
   PubMed Web of Science ®Google Scholar
• Katoh H, Qin ZS, Liu R, Wang L, Li W, Li X, Wu L, Du Z, Lyons R, Liu CG, Liu X, Dou Y, Zheng P, Liu Y. 2011. FOXP3 orchestrates H4K16 acetylation and H3K4 trimethylation for activation of multiple genes by recruiting MOF and causing displacement of PLU-1. Mol. Cell 44:770–784. http://dx.doi.org/10.1016/j.molcel.2011.10.012.
   PubMed Web of Science ®Google Scholar
• Maruyama T, Li J, Vaque JP, Konkel JE, Wang W, Zhang B, Zhang P, Zamarron BF, Yu D, Wu Y, Zhuang Y, Gutkind JS, Chen W. 2011. Control of the differentiation of regulatory T cells and T(H)17 cells by the DNA-binding inhibitor Id3. Nat. Immunol. 12:86–95. http://dx.doi.org/10.1038/ni.1965.
   PubMedGoogle Scholar
• Li H, Dai M, Zhuang Y. 2004. A T cell intrinsic role of Id3 in a mouse model for primary Sjogren's syndrome. Immunity 21:551–560. http://dx.doi.org/10.1016/j.immuni.2004.08.013.
   PubMed Web of Science ®Google Scholar
• Rudra D, deRoos P, Chaudhry A, Niec RE, Arvey A, Samstein RM, Leslie C, Shaffer SA, Goodlett DR, Rudensky AY. 2012. Transcription factor Foxp3 and its protein partners form a complex regulatory network. Nat. Immunol. 13:1010–1019. http://dx.doi.org/10.1038/ni.2402.
   PubMed Web of Science ®Google Scholar
• Wang Y, Su MA, Wan YY. 2011. An essential role of the transcription factor GATA-3 for the function of regulatory T cells. Immunity 35:337–348. http://dx.doi.org/10.1016/j.immuni.2011.08.012.
   PubMed Web of Science ®Google Scholar
• Komatsu N, Mariotti-Ferrandiz ME, Wang Y, Malissen B, Waldmann H, Hori S. 2009. Heterogeneity of natural Foxp3+ T cells: a committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity. Proc. Natl. Acad. Sci. U. S. A. 106:1903–1908. http://dx.doi.org/10.1073/pnas.0811556106.
   PubMed Web of Science ®Google Scholar
• Zhou X, Bailey-Bucktrout SL, Jeker LT, Penaranda C, Martinez-Llordella M, Ashby M, Nakayama M, Rosenthal W, Bluestone JA. 2009. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 10:1000–1007. http://dx.doi.org/10.1038/ni.1774.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Josefowicz S, Chaudhry A, Peng XP, Forbush K, Rudensky AY. 2010. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 463:808–812. http://dx.doi.org/10.1038/nature08750.
   PubMed Web of Science ®Google Scholar
• Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-Hora M, Kodama T, Tanaka S, Bluestone JA, Takayanagi H. 2014. Pathogenic conversion of Foxp3(+) T cells into TH17 cells in autoimmune arthritis. Nat. Med. 20:62–68. http://dx.doi.org/10.1038/nm.3432.
   PubMed Web of Science ®Google Scholar
• Wohlfert EA, Grainger JR, Bouladoux N, Konkel JE, Oldenhove G, Ribeiro CH, Hall JA, Yagi R, Naik S, Bhairavabhotla R, Paul WE, Bosselut R, Wei G, Zhao K, Oukka M, Zhu J, Belkaid Y. 2011. GATA3 controls Foxp3(+) regulatory T cell fate during inflammation in mice. J. Clin. Invest. 121:4503–4515. http://dx.doi.org/10.1172/JCI57456.
   PubMed Web of Science ®Google Scholar
• Xu W, Fukuyama T, Ney PA, Wang D, Rehg J, Boyd K, van Deursen JM, Brindle PK. 2006. Global transcriptional coactivators CREB-binding protein and p300 are highly essential collectively but not individually in peripheral B cells. Blood 107:4407–4416. http://dx.doi.org/10.1182/blood-2005-08-3263.
   PubMed Web of Science ®Google Scholar
• Bedford DC, Kasper LH, Fukuyama T, Brindle PK. 2010. Target gene context influences the transcriptional requirement for the KAT3 family of CBP and p300 histone acetyltransferases. Epigenetics 5:9–15. http://dx.doi.org/10.4161/epi.5.1.10449.
   PubMed Web of Science ®Google Scholar
• Rudra D, Egawa T, Chong MM, Treuting P, Littman DR, Rudensky AY. 2009. Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 10:1170–1177. http://dx.doi.org/10.1038/ni.1795.
   PubMed Web of Science ®Google Scholar
• Burchill MA, Yang J, Vogtenhuber C, Blazar BR, Farrar MA. 2007. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J. Immunol. 178:280–290. http://dx.doi.org/10.4049/jimmunol.178.1.280.
   PubMed Web of Science ®Google Scholar
• Ouyang W, Beckett O, Ma Q, Paik JH, DePinho RA, Li MO. 2010. Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nat. Immunol. 11:618–627. http://dx.doi.org/10.1038/ni.1884.
   PubMed Web of Science ®Google Scholar
• Takaki H, Ichiyama K, Koga K, Chinen T, Takaesu G, Sugiyama Y, Kato S, Yoshimura A, Kobayashi T. 2008. STAT6 inhibits TGF-beta1-mediated Foxp3 induction through direct binding to the Foxp3 promoter, which is reverted by retinoic acid receptor. J. Biol. Chem. 283:14955–14962. http://dx.doi.org/10.1074/jbc.M801123200.
   PubMedGoogle Scholar
• Kang SG, Lim HW, Andrisani OM, Broxmeyer HE, Kim CH. 2007. Vitamin A metabolites induce gut-homing FoxP3+ regulatory T cells. J. Immunol. 179:3724–3733. http://dx.doi.org/10.4049/jimmunol.179.6.3724.
   PubMed Web of Science ®Google Scholar
• Dietze EC, Troch MM, Bowie ML, Yee L, Bean GR, Seewaldt VL. 2003. CBP/p300 induction is required for retinoic acid sensitivity in human mammary cells. Biochem. Biophys. Res. Commun. 302:841–848. http://dx.doi.org/10.1016/S0006-291X(03)00266-3.
   PubMedGoogle Scholar
• Gingras S, Simard J, Groner B, Pfitzner E. 1999. p300/CBP is required for transcriptional induction by interleukin-4 and interacts with Stat6. Nucleic Acids Res. 27:2722–2729. http://dx.doi.org/10.1093/nar/27.13.2722.
   PubMedGoogle Scholar