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Research Article

Coordination of Myeloid Differentiation with Reduced Cell Cycle Progression by PU.1 Induction of MicroRNAs Targeting Cell Cycle Regulators and Lipid Anabolism

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Article: e00013-17 | Received 11 Jan 2017, Accepted 14 Feb 2017, Published online: 17 Mar 2023

REFERENCES

  • Passegue E, Wagers AJ, Giuriato S, Anderson WC, Weissman IL. 2005. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J Exp Med 202:1599–1611. https://doi.org/10.1084/jem.20050967.
  • Perdiguero EG, Geissmann F. 2016. The development and maintenance of resident macrophages. Nat Immunol 17:2–8.
  • Sieweke MH, Allen JE. 2013. Beyond stem cells: self-renewal of differentiated macrophages. Science 342:1242974. https://doi.org/10.1126/science.1242974.
  • 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.
  • DeKoter RP, Singh H. 2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288:1439–1441. https://doi.org/10.1126/science.288.5470.1439.
  • Houston IB, Kamath MB, Schweitzer BL, Chlon TM, DeKoter RP. 2007. Reduction in PU.1 activity results in a block to B-cell development, abnormal myeloid proliferation, and neonatal lethality. Exp Hematol 35:1056–1068. https://doi.org/10.1016/j.exphem.2007.04.005.
  • Rosenbauer F, Wagner K, Kutok JL, Iwasaki H, Le Beau MM, Okuno Y, Akashi K, Fiering S, Tenen DG. 2004. Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, PU1. Nat Genet 36:624–630. https://doi.org/10.1038/ng1361.
  • Lavallee VP, Baccelli I, Krosl J, Wilhelm B, Barabe F, Gendron P, Boucher G, Lemieux S, Marinier A, Meloche S, Hebert J, Sauvageau G. 2015. The transcriptomic landscape and directed chemical interrogation of MLL-rearranged acute myeloid leukemias. Nat Genet 47:1030–1037. https://doi.org/10.1038/ng.3371.
  • Cook WD, McCaw BJ, Herring C, John DL, Foote SJ, Nutt SL, Adams JM. 2004. PU.1 is a suppressor of myeloid leukemia, inactivated in mice by gene deletion and mutation of its DNA binding domain. Blood 104:3437–3444. https://doi.org/10.1182/blood-2004-06-2234.
  • Staber PB, Zhang P, Ye M, Welner RS, Nombela-Arrieta C, Bach C, Kerenyi M, Bartholdy BA, Zhang H, Alberich-Jorda M, Lee S, Yang H, Ng F, Zhang J, Leddin M, Silberstein LE, Hoefler G, Orkin SH, Gottgens B, Rosenbauer F, Huang G, Tenen DG. 2013. Sustained PU.1 levels balance cell-cycle regulators to prevent exhaustion of adult hematopoietic stem cells. Mol Cell 49:934–946. https://doi.org/10.1016/j.molcel.2013.01.007.
  • Will B, Vogler TO, Narayanagari S, Bartholdy B, Todorova TI, da Silva Ferreira M, Chen J, Yu Y, Mayer J, Barreyro L, Carvajal L, Neriah DB, Roth M, van Oers J, Schaetzlein S, McMahon C, Edelmann W, Verma A, Steidl U. 2015. Minimal PU.1 reduction induces a preleukemic state and promotes development of acute myeloid leukemia. Nat Med 21:1172–1181. https://doi.org/10.1038/nm.3936.
  • Ziliotto R, Gruca MR, Podder S, Noel G, Ogle CK, Hess DA, DeKoter RP. 2014. PU.1 promotes cell cycle exit in the murine myeloid lineage associated with downregulation of E2F1. Exp Hematol 42:204–217.e1. https://doi.org/10.1016/j.exphem.2013.11.011.
  • Kamath MB, Houston IB, Janovski AJ, Zhu X, Gowrisankar S, Jegga AG, DeKoter RP. 2008. Dose-dependent repression of T-cell and natural killer cell genes by PU.1 enforces myeloid and B-cell identity. Leukemia 22:1214–1225. https://doi.org/10.1038/leu.2008.67.
  • Trikha P, Sharma N, Opavsky R, Reyes A, Pena C, Ostrowski MC, Roussel MF, Leone G. 2011. E2f1–3 are critical for myeloid development. J Biol Chem 286:4783–4795. https://doi.org/10.1074/jbc.M110.182733.
  • Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M, Nevins JR. 2001. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol 21:4684–4699. https://doi.org/10.1128/MCB.21.14.4684-4699.2001.
  • Denechaud PD, Lopez-Mejia IC, Giralt A, Lai Q, Blanchet E, Delacuisine B, Nicolay BN, Dyson NJ, Bonner C, Pattou F, Annicotte JS, Fajas L. 2016. E2F1 mediates sustained lipogenesis and contributes to hepatic steatosis. J Clin Invest 126:137–150. https://doi.org/10.1172/JCI81542.
  • Scaglia N, Tyekucheva S, Zadra G, Photopoulos C, Loda M. 2014. De novo fatty acid synthesis at the mitotic exit is required to complete cellular division. Cell Cycle 13:859–868. https://doi.org/10.4161/cc.27767.
  • O'Reilly D, Addley M, Quinn C, MacFarlane AJ, Gordon S, McKnight AJ, Greaves DR. 2004. Functional analysis of the murine Emr1 promoter identifies a novel purine-rich regulatory motif required for high-level gene expression in macrophages. Genomics 84:1030–1040. https://doi.org/10.1016/j.ygeno.2004.08.016.
  • Turkistany SA, DeKoter RP. 2011. The transcription factor PU.1 is a critical regulator of cellular communication in the immune system. Arch Immunol Ther Exp (Warsz) 59:431–440. https://doi.org/10.1007/s00005-011-0147-9.
  • Zaidi N, Swinnen JV, Smans K. 2012. ATP-citrate lyase: a key player in cancer metabolism. Cancer Res 72:3709–3714. https://doi.org/10.1158/0008-5472.CAN-11-4112.
  • Srere PA. 1972. The citrate enzymes: their structures, mechanisms, and biological functions. Curr Top Cell Regul 5:229–283. https://doi.org/10.1016/B978-0-12-152805-8.50013-7.
  • Holland SM. 2010. Chronic granulomatous disease. Clin Rev Allergy Immunol 38:3–10. https://doi.org/10.1007/s12016-009-8136-z.
  • Bauer DE, Hatzivassiliou G, Zhao F, Andreadis C, Thompson CB. 2005. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 24:6314–6322. https://doi.org/10.1038/sj.onc.1208773.
  • Hatzivassiliou G, Zhao F, Bauer DE, Andreadis C, Shaw AN, Dhanak D, Hingorani SR, Tuveson DA, Thompson CB. 2005. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 8:311–321. https://doi.org/10.1016/j.ccr.2005.09.008.
  • Li JJ, Wang H, Tino JA, Robl JA, Herpin TF, Lawrence RM, Biller S, Jamil H, Ponticiello R, Chen L, Chu CH, Flynn N, Cheng D, Zhao R, Chen B, Schnur D, Obermeier MT, Sasseville V, Padmanabha R, Pike K, Harrity T. 2007. 2-Hydroxy-N-arylbenzenesulfonamides as ATP-citrate lyase inhibitors. Bioorg Med Chem Lett 17:3208–3211. https://doi.org/10.1016/j.bmcl.2007.03.017.
  • DeGregori J, Leone G, Miron A, Jakoi L, Nevins JR. 1997. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc Natl Acad Sci U S A 94:7245–7250. https://doi.org/10.1073/pnas.94.14.7245.
  • Li SK, Abbas AK, Solomon LA, Groux GM, DeKoter RP. 2015. Nfkb1 activation by the E26 transformation-specific transcription factors PU.1 and Spi-B promotes Toll-like receptor-mediated splenic B cell proliferation. Mol Cell Biol 35:1619–1632. https://doi.org/10.1128/MCB.00117-15.
  • Hong SH, Kim KS, Oh IH. 2015. Concise review: Exploring miRNAs—toward a better understanding of hematopoiesis. Stem Cells 33:1–7. https://doi.org/10.1002/stem.1810.
  • Pulikkan JA, Dengler V, Peramangalam PS, Peer Zada AA, Muller-Tidow C, Bohlander SK, Tenen DG, Behre G. 2010. Cell-cycle regulator E2F1 and microRNA-223 comprise an autoregulatory negative feedback loop in acute myeloid leukemia. Blood 115:1768–1778. https://doi.org/10.1182/blood-2009-08-240101.
  • Fukao T, Fukuda Y, Kiga K, Sharif J, Hino K, Enomoto Y, Kawamura A, Nakamura K, Takeuchi T, Tanabe M. 2007. An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell 129:617–631. https://doi.org/10.1016/j.cell.2007.02.048.
  • Rosa A, Ballarino M, Sorrentino A, Sthandier O, De Angelis FG, Marchioni M, Masella B, Guarini A, Fatica A, Peschle C, Bozzoni I. 2007. The interplay between the master transcription factor PU.1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci U S A 104:19849–19854. https://doi.org/10.1073/pnas.0706963104.
  • Tai MC, Kajino T, Nakatochi M, Arima C, Shimada Y, Suzuki M, Miyoshi H, Yatabe Y, Yanagisawa K, Takahashi T. 2015. miR-342-3p regulates MYC transcriptional activity via direct repression of E2F1 in human lung cancer. Carcinogenesis 36:1464–1473. https://doi.org/10.1093/carcin/bgv152.
  • Cao AR, Rabinovich R, Xu M, Xu X, Jin VX, Farnham PJ. 2011. Genome-wide analysis of transcription factor E2F1 mutant proteins reveals that N- and C-terminal protein interaction domains do not participate in targeting E2F1 to the human genome. J Biol Chem 286:11985–11996. https://doi.org/10.1074/jbc.M110.217158.
  • Zhang JA, Mortazavi A, Williams BA, Wold BJ, Rothenberg EV. 2012. Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell 149:467–482. https://doi.org/10.1016/j.cell.2012.01.056.
  • Lara-Astiaso D, Weiner A, Lorenzo-Vivas E, Zaretsky I, Jaitin DA, David E, Keren-Shaul H, Mildner A, Winter D, Jung S, Friedman N, Amit I. 2014. Immunogenetics. Chromatin state dynamics during blood formation. Science 345:943–949. https://doi.org/10.1126/science.1256271.
  • Kueh HY, Champhekar A, Nutt SL, Elowitz MB, Rothenberg EV. 2013. Positive feedback between PU.1 and the cell cycle controls myeloid differentiation. Science 341:670–673. https://doi.org/10.1126/science.1240831.
  • Lee IH, Finkel T. 2013. Metabolic regulation of the cell cycle. Curr Opin Cell Biol 25:724–729. https://doi.org/10.1016/j.ceb.2013.07.002.
  • Aguilar V, Fajas L. 2010. Cycling through metabolism. EMBO Mol Med 2:338–348. https://doi.org/10.1002/emmm.201000089.
  • Pfaffl MW, Horgan GW, Dempfle L. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. https://doi.org/10.1093/nar/30.9.e36.
  • Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25.
  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137. https://doi.org/10.1186/gb-2008-9-9-r137.
  • McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28:495–501. https://doi.org/10.1038/nbt.1630.
  • Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57. https://doi.org/10.1038/nprot.2008.211.
  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C. 2015. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–D452. https://doi.org/10.1093/nar/gku1003.
  • Kozomara A, Griffiths-Jones S. 2014. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73. https://doi.org/10.1093/nar/gkt1181.
  • Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S, Rajewsky N. 2008. Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 26:407–415. https://doi.org/10.1038/nbt1394.
  • Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8.
  • Abbas AK, Le K, Pimmett VL, Bell DA, Cairns E, DeKoter RP. 2014. Negative regulation of the peptidylarginine deiminase type IV promoter by NF-κB in human myeloid cells. Gene 533:123–131. https://doi.org/10.1016/j.gene.2013.09.108.
  • Andrés-León E, González Peña D, Gómez-López G, Pisano DG. 2015. miRGate: a curated database of human, mouse and rat miRNA-mRNA targets. Database (Oxford) 2015:bav035. https://doi.org/10.1093/database/bav035.

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