Transcription factor regulation of ribosomal RNA in hematopoiesis.
Journal
Current opinion in hematology
ISSN: 1531-7048
Titre abrégé: Curr Opin Hematol
Pays: United States
ID NLM: 9430802
Informations de publication
Date de publication:
03 Apr 2024
03 Apr 2024
Historique:
medline:
3
4
2024
pubmed:
3
4
2024
entrez:
3
4
2024
Statut:
aheadofprint
Résumé
Ribosomal RNAs (rRNAs) are transcribed within nucleoli from rDNA repeats by RNA Polymerase I (Pol I). There is variation in rRNA transcription rates across the hematopoietic tree, and leukemic blast cells have prominent nucleoli, indicating abundant ribosome biogenesis. The mechanisms underlying these variations are poorly understood. The purpose of this review is to summarize findings of rDNA binding and Pol I regulation by hematopoietic transcription factors. Our group recently used custom genome assemblies optimized for human and mouse rDNA mapping to map nearly 2200 ChIP-Seq datasets for nearly 250 factors to rDNA, allowing us to identify conserved occupancy patterns for multiple transcription factors. We confirmed known rDNA occupancy of MYC and RUNX factors, and identified new binding sites for CEBP factors, IRF factors, and SPI1 at canonical motif sequences. We also showed that CEBPA degradation rapidly leads to reduced Pol I occupancy and nascent rRNA in mouse myeloid cells. We propose that a number of hematopoietic transcription factors bind rDNA and potentially regulate rRNA transcription. Our model has implications for normal and malignant hematopoiesis. This review summarizes the literature, and outlines experimental considerations to bear in mind while dissecting transcription factor roles on rDNA.
Identifiants
pubmed: 38568093
doi: 10.1097/MOH.0000000000000816
pii: 00062752-990000000-00069
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.
Références
Hori Y, Engel C, Kobayashi T. Regulation of ribosomal RNA gene copy number, transcription and nucleolus organization in eukaryotes. Nat Rev Mol Cell Biol 2023; 24:414–429.
Antony C, George SS, Blum J, et al. Control of ribosomal RNA synthesis by hematopoietic transcription factors. Mol Cell 2022; 82:3826–3839. e9.
George SS, Pimkin M, Paralkar VR. Construction and validation of customized genomes for human and mouse ribosomal DNA mapping. J Biol Chem 2023; 299:104766.
Mills EW, Green R. Ribosomopathies: there's strength in numbers. Science 2017; 358:eaan2755.
Dörner K, Ruggeri C, Zemp I, et al. Ribosome biogenesis factors-from names to functions. EMBO J 2023; 42:e112699.
Vlachos A. Acquired ribosomopathies in leukemia and solid tumors. Hematology Am Soc Hematol Educ Program 2017; 2017:716–719.
Moss T, Mars J-C, Tremblay MG, et al. The chromatin landscape of the ribosomal RNA genes in mouse and human. Chromosome Res 2019; 27:31–40.
Daiß JL, Griesenbeck J, Tschochner H, et al. Synthesis of the ribosomal RNA precursor in human cells: mechanisms, factors and regulation. Biol Chem 2023; 404:1003–1023.
Girbig M, Misiaszek AD, Müller CW. Structural insights into nuclear transcription by eukaryotic DNA-dependent RNA polymerases. Nat Rev Mol Cell Biol 2022; 23:603–622.
Bartsch I, Schoneberg C, Grummt I. Purification and characterization of TTFI, a factor that mediates termination of mouse ribosomal DNA transcription. Mol Cell Biol 1988; 8:3891–3897.
Németh A, Guibert S, Tiwari VK, et al. Epigenetic regulation of TTF-I-mediated promoter-terminator interactions of rRNA genes. EMBO J 2008; 27:1255–1265.
Dolznig H, Bartunek P, Nasmyth K, et al. Terminal differentiation of normal chicken erythroid progenitors: shortening of G1 correlates with loss of D-cyclin/cdk4 expression and altered cell size control. Cell Growth Differ 1995; 6:1341–1352.
Le Goff S, Boussaid I, Floquet C, et al. p53 activation during ribosome biogenesis regulates normal erythroid differentiation. Blood 2021; 137:89–102.
Hayashi Y, Kuroda T, Kishimoto H, et al. Downregulation of rRNA transcription triggers cell differentiation. PLoS One 2014; 9:e98586.
Jarzebowski L, Le Bouteiller M, Coqueran S, et al. Mouse adult hematopoietic stem cells actively synthesize ribosomal RNA. RNA 2018; 24:1803–1812.
Antony C, Somers P, Gray EM, et al. FISH-Flow to quantify nascent and mature ribosomal RNA in mouse and human cells. STAR Protoc 2023; 4:102463.
Sayers EW, Beck J, Bolton EE, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2024; 52:D33–D43.
Kim J-H, Dilthey AT, Nagaraja R, et al. Variation in human chromosome 21 ribosomal RNA genes characterized by TAR cloning and long-read sequencing. Nucleic Acids Res 2018; 46:6712–6725.
Grozdanov P, Georgiev O, Karagyozov L. Complete sequence of the 45-kb mouse ribosomal DNA repeat: analysis of the intergenic spacer. Genomics 2003; 82:637–643.
Zentner GE, Saiakhova A, Manaenkov P, et al. Integrative genomic analysis of human ribosomal DNA. Nucleic Acids Res 2011; 39:4949–4960.
Zentner GE, Balow SA, Scacheri PC. Genomic characterization of the mouse ribosomal DNA locus. G3 2014; 4:243–254.
Stengel KR, Ellis JD, Spielman CL, et al. Definition of a small core transcriptional circuit regulated by AML1-ETO. Mol Cell 2021; 81:530–545. e5.
Harada T, Kalfon J, Perez MW, et al. Leukemia core transcriptional circuitry is a sparsely interconnected hierarchy stabilized by incoherent feed-forward loops. bioRxiv 2023. doi: 10.1101/2023.03.13.532438.
Harada T, Perez MW, Kalfon J, et al. Rapid-kinetics degron benchmarking reveals off-target activities and mixed agonism-antagonism of MYB inhibitors. bioRxiv 2023. doi: 10.1101/2023.04.07.536032.
Comai L, Tanese N, Tjian R. The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1. Cell 1992; 68:965–976.
van de Nobelen S, Rosa-Garrido M, Leers J, et al. CTCF regulates the local epigenetic state of ribosomal DNA repeats. Epigenetics Chromatin 2010; 3:19.
van Riggelen J, Yetil A, Felsher DW. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 2010; 10:301–309.
Arabi A, Wu S, Ridderstråle K, et al. c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat Cell Biol 2005; 7:303–310.
Grandori C, Gomez-Roman N, Felton-Edkins ZA, et al. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat Cell Biol 2005; 7:311–318.
Poortinga G, Hannan KM, Snelling H, et al. MAD1 and c-MYC regulate UBF and rDNA transcription during granulocyte differentiation. EMBO J 2004; 23:3325–3335.
Poortinga G, Wall M, Sanij E, et al. c-MYC coordinately regulates ribosomal gene chromatin remodeling and Pol I availability during granulocyte differentiation. Nucleic Acids Res 2011; 39:3267–3281.
Lourenco C, Resetca D, Redel C, et al. MYC protein interactors in gene transcription and cancer. Nat Rev Cancer 2021; 21:579–591.
Tsukada J, Yoshida Y, Kominato Y, et al. The CCAAT/enhancer (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation. Cytokine 2011; 54:6–19.
Zhang D-E, Zhang P, Wang N-D, et al. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein-deficient mice. Proc Natl Acad Sci U S A 1997; 94:569–574.
Zhang P, Iwasaki-Arai J, Iwasaki H, et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity 2004; 21:853–863.
Müller C, Bremer A, Schreiber S, et al. Nucleolar retention of a translational C/EBPalpha isoform stimulates rDNA transcription and cell size. EMBO J 2010; 29:897–909.
Taube F, Georgi JA, Kramer M, et al. CEBPA mutations in 4708 patients with acute myeloid leukemia: differential impact of bZIP and TAD mutations on outcome. Blood 2022; 139:87–103.
Tamura T, Yanai H, Savitsky D, et al. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol 2008; 26:535–584.
Burda P, Laslo P, Stopka T. The role of PU.1 and GATA-1 transcription factors during normal and leukemogenic hematopoiesis. Leukemia 2010; 24:1249–1257.
Young DW, Hassan MQ, Pratap J, et al. Mitotic occupancy and lineage-specific transcriptional control of rRNA genes by Runx2. Nature 2007; 445:442–446.
Pande S, Ali SA, Dowdy C, et al. Subnuclear targeting of the Runx3 tumor suppressor and its epigenetic association with mitotic chromosomes. J Cell Physiol 2009; 218:473–479.
Bakshi R, Zaidi SK, Pande S, et al. The leukemogenic t(8;21) fusion protein AML1-ETO controls rRNA genes and associates with nucleolar-organizing regions at mitotic chromosomes. J Cell Sci 2008; 121:3981–3990.
Cai X, Gao L, Teng L, et al. Runx1 deficiency decreases ribosome biogenesis and confers stress resistance to hematopoietic stem and progenitor cells. Cell Stem Cell 2015; 17:165–177.