80
Views
6
CrossRef citations to date
0
Altmetric
Research Article

GATA2 and PU.1 Collaborate To Activate the Expression of the Mouse Ms4a2 Gene, Encoding FcεRIβ, through Distinct Mechanisms

, , , , , , , & show all
Article: e00314-19 | Received 16 Jul 2019, Accepted 02 Sep 2019, Published online: 03 Mar 2023

REFERENCES

  • Pevny L, Lin CS, D'Agati V, Simon MC, Orkin SH, Costantini F. 1995. Development of hematopoietic cells lacking transcription factor GATA-1. Development 121:163–172.
  • Fujiwara Y, Browne CP, Cunniff K, Goff SC, Orkin SH. 1996. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci U S A 93:12355–12358. https://doi.org/10.1073/pnas.93.22.12355.
  • Takahashi S, Onodera K, Motohashi H, Suwabe N, Hayashi N, Yanai N, Nabesima Y, Yamamoto M. 1997. Arrest in primitive erythroid cell development caused by promoter-specific disruption of the GATA-1 gene. J Biol Chem 272:12611–12615. https://doi.org/10.1074/jbc.272.19.12611.
  • Gutierrez L, Tsukamoto S, Suzuki M, Yamamoto-Mukai H, Yamamoto M, Philipsen S, Ohneda K. 2008. Ablation of Gata1 in adult mice results in aplastic crisis, revealing its essential role in steady-state and stress erythropoiesis. Blood 111:4375–4385. https://doi.org/10.1182/blood-2007-09-115121.
  • Tsai FY, Keller G, Kuo FC, Weiss M, Chen J, Rosenblatt M, Alt FW, Orkin SH. 1994. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371:221–226. https://doi.org/10.1038/371221a0.
  • Tsai FY, Orkin SH. 1997. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 89:3636–3643.
  • Scott EW, Simon MC, Anastasi J, Singh H. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265:1573–1577. https://doi.org/10.1126/science.8079170.
  • McKercher SR, Torbett BE, Anderson KL, Henkel GW, Vestal DJ, Baribault H, Klemsz M, Feeney AJ, Wu GE, Paige CJ, Maki RA. 1996. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 15:5647–5658. https://doi.org/10.1002/j.1460-2075.1996.tb00949.x.
  • Nerlov C, Graf T. 1998. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev 12:2403–2412. https://doi.org/10.1101/gad.12.15.2403.
  • Rekhtman N, Radparvar F, Evans T, Skoultchi AI. 1999. Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells. Genes Dev 13:1398–1411. https://doi.org/10.1101/gad.13.11.1398.
  • Zhang P, Behre G, Pan J, Iwama A, Wara-Aswapati N, Radomska HS, Auron PE, Tenen DG, Sun Z. 1999. Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc Natl Acad Sci U S A 96:8705–8710. https://doi.org/10.1073/pnas.96.15.8705.
  • Nerlov C, Querfurth E, Kulessa H, Graf T. 2000. GATA-1 interacts with the myeloid PU.1 transcription factor and represses PU.1-dependent transcription. Blood 95:2543–2551.
  • Zhang P, Zhang X, Iwama A, Yu C, Smith KA, Mueller BU, Narravula S, Torbett BE, Orkin SH, Tenen DG. 2000. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 96:2641–2648.
  • Arinobu Y, Mizuno S, Chong Y, Shigematsu H, Iino T, Iwasaki H, Graf T, Mayfield R, Chan S, Kastner P, Akashi K. 2007. Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 1:416–427. https://doi.org/10.1016/j.stem.2007.07.004.
  • Burda P, Vargova J, Curik N, Salek C, Papadopoulos GL, Strouboulis J, Stopka T. 2016. GATA-1 inhibits PU.1 gene via DNA and histone H3K9 methylation of its distal enhancer in erythroleukemia. PLoS One 11:e0152234. https://doi.org/10.1371/journal.pone.0152234.
  • Du J, Stankiewicz MJ, Liu Y, Xi Q, Schmitz JE, Lekstrom-Himes JA, Ackerman SJ. 2002. Novel combinatorial interactions of GATA-1, PU.1, and C/EBPepsilon isoforms regulate transcription of the gene encoding eosinophil granule major basic protein. J Biol Chem 277:43481–43494. https://doi.org/10.1074/jbc.M204777200.
  • Baba Y, Maeda K, Yashiro T, Inage E, Niyonsaba F, Hara M, Suzuki R, Ohtsuka Y, Shimizu T, Ogawa H, Okumura K, Nishiyama C. 2012. Involvement of PU.1 in mast cell/basophil-specific function of the human IL1RL1/ST2 promoter. Allergol Int 61:461–467. https://doi.org/10.2332/allergolint.12-OA-0424.
  • Ohneda K, Moriguchi T, Ohmori S, Ishijima Y, Satoh H, Philipsen S, Yamamoto M. 2014. Transcription factor GATA1 is dispensable for mast cell differentiation in adult mice. Mol Cell Biol 34:1812–1826. https://doi.org/10.1128/MCB.01524-13.
  • Ohmori S, Moriguchi T, Noguchi Y, Ikeda M, Kobayashi K, Tomaru N, Ishijima Y, Ohneda O, Yamamoto M, Ohneda K. 2015. GATA2 is critical for the maintenance of cellular identity in differentiated mast cells derived from mouse bone marrow. Blood 125:3306–3315. https://doi.org/10.1182/blood-2014-11-612465.
  • Maeda K, Nishiyama C, Tokura T, Akizawa Y, Nishiyama M, Ogawa H, Okumura K, Ra C. 2003. Regulation of cell type-specific mouse Fc epsilon RI beta-chain gene expression by GATA-1 via four GATA motifs in the promoter. J Immunol 170:334–340. https://doi.org/10.4049/jimmunol.170.1.334.
  • Nishiyama C, Ito T, Nishiyama M, Masaki S, Maeda K, Nakano N, Ng W, Fukuyama K, Yamamoto M, Okumura K, Ogawa H. 2005. GATA-1 is required for expression of Fc{epsilon}RI on mast cells: analysis of mast cells derived from GATA-1 knockdown mouse bone marrow. Int Immunol 17:847–856. https://doi.org/10.1093/intimm/dxh278.
  • Inage E, Kasakura K, Yashiro T, Suzuki R, Baba Y, Nakano N, Hara M, Tanabe A, Oboki K, Matsumoto K, Saito H, Niyonsaba F, Ohtsuka Y, Ogawa H, Okumura K, Shimizu T, Nishiyama C. 2014. Critical roles for PU.1, GATA1, and GATA2 in the expression of human FcepsilonRI on mast cells: PU.1 and GATA1 transactivate FCER1A, and GATA2 transactivates FCER1A and MS4A2. J Immunol 192:3936–3946. https://doi.org/10.4049/jimmunol.1302366.
  • Oda Y, Kasakura K, Fujigaki I, Kageyama A, Okumura K, Ogawa H, Yashiro T, Nishiyama C. 2018. The effect of PU.1 knockdown on gene expression and function of mast cells. Sci Rep 8:2005. https://doi.org/10.1038/s41598-018-19378-y.
  • Agulnick AD, Taira M, Breen JJ, Tanaka T, Dawid IB, Westphal H. 1996. Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins. Nature 384:270–272. https://doi.org/10.1038/384270a0.
  • Krivega I, Dean A. 2016. Chromatin looping as a target for altering erythroid gene expression. Ann N Y Acad Sci 1368:31–39. https://doi.org/10.1111/nyas.13012.
  • Wadman IA, Osada H, Grutz GG, Agulnick AD, Westphal H, Forster A, Rabbitts TH. 1997. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J 16:3145–3157. https://doi.org/10.1093/emboj/16.11.3145.
  • Deng W, Lee J, Wang H, Miller J, Reik A, Gregory PD, Dean A, Blobel GA. 2012. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 149:1233–1244. https://doi.org/10.1016/j.cell.2012.03.051.
  • Krivega I, Dale RK, Dean A. 2014. Role of LDB1 in the transition from chromatin looping to transcription activation. Genes Dev 28:1278–1290. https://doi.org/10.1101/gad.239749.114.
  • Stadhouders R, Thongjuea S, Andrieu-Soler C, Palstra RJ, Bryne JC, van den Heuvel A, Stevens M, de Boer E, Kockx C, van der Sloot A, van den Hout M, van Ijcken W, Eick D, Lenhard B, Grosveld F, Soler E. 2012. Dynamic long-range chromatin interactions control Myb proto-oncogene transcription during erythroid development. EMBO J 31:986–999. https://doi.org/10.1038/emboj.2011.450.
  • Schuetzmann D, Walter C, van Riel B, Kruse S, Konig T, Erdmann T, Tonges A, Bindels E, Weilemann A, Gebhard C, Wethmar K, Perrod C, Minderjahn J, Rehli M, Delwel R, Lenz G, Groschel S, Dugas M, Rosenbauer F. 2018. Temporal autoregulation during human PU.1 locus SubTAD formation. Blood 132:2643–2655. https://doi.org/10.1182/blood-2018-02-834721.
  • Kraft S, Kinet JP. 2007. New developments in FcepsilonRI regulation, function and inhibition. Nat Rev Immunol 7:365–378. https://doi.org/10.1038/nri2072.
  • Ra C, Nunomura S, Okayama Y. 2012. Fine-tuning of mast cell activation by FcepsilonRIbeta chain. Front Immunol 3:112. https://doi.org/10.3389/fimmu.2012.00112.
  • Blank U, Ra CS, Kinet JP. 1991. Characterization of truncated alpha chain products from human, rat, and mouse high affinity receptor for immunoglobulin E. J Biol Chem 266:2639–2646.
  • Hiraoka S, Furumoto Y, Koseki H, Takagaki Y, Taniguchi M, Okumura K, Ra C. 1999. Fc receptor beta subunit is required for full activation of mast cells through Fc receptor engagement. Int Immunol 11:199–207. https://doi.org/10.1093/intimm/11.2.199.
  • Donnadieu E, Jouvin MH, Kinet JP. 2000. A second amplifier function for the allergy-associated Fc(epsilon)RI-beta subunit. Immunity 12:515–523. https://doi.org/10.1016/S1074-7613(00)80203-4.
  • Pino-Yanes M, Corrales A, Cumplido J, Poza P, Sánchez-Machín I, Sánchez-Palacios A, Figueroa J, Acosta-Fernández O, Buset N, García-Robaina JC, Hernández M, Villar J, Carrillo T, Flores C. 2013. Assessing the validity of asthma associations for eight candidate genes and age at diagnosis effects. PLoS One 8:e73157. https://doi.org/10.1371/journal.pone.0073157.
  • Amo G, García-Menaya J, Campo P, Cordobés C, Serón MCP, Ayuso P, Esguevillas G, Blanca M, Agúndez JAG, García-Martín E. 2016. A nonsynonymous FCER1B SNP is associated with risk of developing allergic rhinitis and with IgE levels. Sci Rep 6:19724. https://doi.org/10.1038/srep19724.
  • Amo G, Cornejo-García JA, García-Menaya JM, Cordobes C, Torres MJ, Esguevillas G, Mayorga C, Martinez C, Blanca-Lopez N, Canto G, Ramos A, Blanca M, Agúndez JAG, García-Martín E. 2016. FCERI and histamine metabolism gene variability in selective responders to NSAIDs. Front Pharmacol 7:353. https://doi.org/10.3389/fphar.2016.00353.
  • Pavón-Romero GF, Pérez-Rubio G, Ramírez-Jiménez F, Ambrocio-Ortiz E, Bañuelos-Ortiz E, Alvarado-Franco N, Xochipa-Ruiz KE, Hernández-Juárez E, Flores-García BA, Camarena ÁE, Terán LM, Falfán-Valencia R. 2018. MS4A2-rs573790 is associated with aspirin-exacerbated respiratory disease: replicative study using a candidate gene strategy. Front Genet 9:363. https://doi.org/10.3389/fgene.2018.00363.
  • Hiroyama T, Miharada K, Sudo K, Danjo I, Aoki N, Nakamura Y. 2008. Establishment of mouse embryonic stem cell-derived erythroid progenitor cell lines able to produce functional red blood cells. PLoS One 3:e1544. https://doi.org/10.1371/journal.pone.0001544.
  • Calero-Nieto FJ, Ng FS, Wilson NK, Hannah R, Moignard V, Leal-Cervantes AI, Jimenez-Madrid I, Diamanti E, Wernisch L, Göttgens B. 2014. Key regulators control distinct transcriptional programmes in blood progenitor and mast cells. EMBO J 33:1212–1226. https://doi.org/10.1002/embj.201386825.
  • Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 107:21931–21936. https://doi.org/10.1073/pnas.1016071107.
  • Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279–283. https://doi.org/10.1038/nature09692.
  • Ohmori S, Takai J, Ishijima Y, Suzuki M, Moriguchi T, Philipsen S, Yamamoto M, Ohneda K. 2012. Regulation of GATA factor expression is distinct between erythroid and mast cell lineages. Mol Cell Biol 32:4742–4755. https://doi.org/10.1128/MCB.00718-12.
  • Dignam JD, Lebovitz RM, Roeder RG. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11:1475–1489. https://doi.org/10.1093/nar/11.5.1475.
  • Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281–2308. https://doi.org/10.1038/nprot.2013.143.
  • Dekker J, Heard E. 2015. Structural and functional diversity of topologically associating domains. FEBS Lett 589:2877–2884. https://doi.org/10.1016/j.febslet.2015.08.044.
  • Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Bluthgen N, Dekker J, Heard E. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–385. https://doi.org/10.1038/nature11049.
  • Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–380. https://doi.org/10.1038/nature11082.
  • Phillips-Cremins JE, Sauria ME, Sanyal A, Gerasimova TI, Lajoie BR, Bell JS, Ong CT, Hookway TA, Guo C, Sun Y, Bland MJ, Wagstaff W, Dalton S, McDevitt TC, Sen R, Dekker J, Taylor J, Corces VG. 2013. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153:1281–1295. https://doi.org/10.1016/j.cell.2013.04.053.
  • Catarino RR, Stark A. 2018. Assessing sufficiency and necessity of enhancer activities for gene expression and the mechanisms of transcription activation. Genes Dev 32:202–223. https://doi.org/10.1101/gad.310367.117.
  • Chen H, Du G, Song X, Li L. 2017. Non-coding transcripts from enhancers: new insights into enhancer activity and gene expression regulation. Genomics Proteomics Bioinformatics 15:201–207. https://doi.org/10.1016/j.gpb.2017.02.003.
  • Miyamoto T, Iwasaki H, Reizis B, Ye M, Graf T, Weissman IL, Akashi K. 2002. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev Cell 3:137–147. https://doi.org/10.1016/S1534-5807(02)00201-0.
  • Wontakal SN, Guo X, Smith C, MacCarthy T, Bresnick EH, Bergman A, Snyder MP, Weissman SM, Zheng D, Skoultchi AI. 2012. A core erythroid transcriptional network is repressed by a master regulator of myelo-lymphoid differentiation. Proc Natl Acad Sci U S A 109:3832–3837. https://doi.org/10.1073/pnas.1121019109.
  • May G, Soneji S, Tipping AJ, Teles J, McGowan SJ, Wu M, Guo Y, Fugazza C, Brown J, Karlsson G, Pina C, Olariu V, Taylor S, Tenen DG, Peterson C, Enver T. 2013. Dynamic analysis of gene expression and genome-wide transcription factor binding during lineage specification of multipotent progenitors. Cell Stem Cell 13:754–768. https://doi.org/10.1016/j.stem.2013.09.003.
  • Hoppe PS, Schwarzfischer M, Loeffler D, Kokkaliaris KD, Hilsenbeck O, Moritz N, Endele M, Filipczyk A, Gambardella A, Ahmed N, Etzrodt M, Coutu DL, Rieger MA, Marr C, Strasser MK, Schauberger B, Burtscher I, Ermakova O, Burger A, Lickert H, Nerlov C, Theis FJ, Schroeder T. 2016. Early myeloid lineage choice is not initiated by random PU.1 to GATA1 protein ratios. Nature 535:299–302. https://doi.org/10.1038/nature18320.
  • Strasser MK, Hoppe PS, Loeffler D, Kokkaliaris KD, Schroeder T, Theis FJ, Marr C. 2018. Lineage marker synchrony in hematopoietic genealogies refutes the PU.1/GATA1 toggle switch paradigm. Nat Commun 9:2697. https://doi.org/10.1038/s41467-018-05037-3.
  • Takahashi K, Nishiyama C, Hasegawa M, Akizawa Y, Ra C. 2003. Regulation of the human high affinity IgE receptor beta-chain gene expression via an intronic element. J Immunol 171:2478–2484. https://doi.org/10.4049/jimmunol.171.5.2478.
  • Takahashi K, Hayashi N, Kaminogawa S, Ra C. 2006. Molecular mechanisms for transcriptional regulation of human high-affinity IgE receptor beta-chain gene induced by GM-CSF. J Immunol 177:4605–4611. https://doi.org/10.4049/jimmunol.177.7.4605.
  • Iwasaki H, Somoza C, Shigematsu H, Duprez EA, Iwasaki-Arai J, Mizuno S, Arinobu Y, Geary K, Zhang P, Dayaram T, Fenyus ML, Elf S, Chan S, Kastner P, Huettner CS, Murray R, Tenen DG, Akashi K. 2005. Distinctive and indispensable roles of PU.1 in maintenance of hematopoietic stem cells and their differentiation. Blood 106:1590–1600. https://doi.org/10.1182/blood-2005-03-0860.
  • Charles MA, Saunders TL, Wood WM, Owens K, Parlow AF, Camper SA, Ridgway EC, Gordon DF. 2006. Pituitary-specific Gata2 knockout: effects on gonadotrope and thyrotrope function. Mol Endocrinol 20:1366–1377. https://doi.org/10.1210/me.2005-0378.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.