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Research Article

RNA-Binding Proteins PCBP1 and PCBP2 Are Critical Determinants of Murine Erythropoiesis

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Article: e00668-20 | Received 23 Dec 2020, Accepted 20 Jun 2021, Published online: 03 Mar 2023

REFERENCES

  • Liebhaber SA. 1997. mRNA stability and the control of gene expression. Nucleic Acids Symp Ser 1997:29–32.
  • Waggoner SA, Liebhaber SA. 2003. Regulation of alpha-globin mRNA stability. Exp Biol Med (Maywood) 228:387–395. https://doi.org/10.1177/153537020322800409.
  • Russell JE, Morales J, Liebhaber SA. 1997. The role of mRNA stability in the control of globin gene expression. Prog Nucleic Acids Res Mol Biol 57:249–287. https://doi.org/10.1016/s0079-6603(08)60283-4.
  • Weiss IM, Liebhaber SA. 1994. Erythroid cell-specific determinants of alpha-globin mRNA stability. Mol Cell Biol 14:8123–8132. https://doi.org/10.1128/MCB.14.12.8123.
  • Weiss IM, Liebhaber SA. 1995. Erythroid cell-specific mRNA stability elements in the alpha 2-globin 3′ nontranslated region. Mol Cell Biol 15:2457–2465. https://doi.org/10.1128/MCB.15.5.2457.
  • Waggoner SA, Liebhaber SA. 2003. Identification of mRNAs associated with alphaCP2-containing RNP complexes. Mol Cell Biol 23:7055–7067. https://doi.org/10.1128/MCB.23.19.7055-7067.2003.
  • Holcik M, Liebhaber SA. 1997. Four highly stable eukaryotic mRNAs assemble 3′ untranslated region RNA-protein complexes sharing cis and trans components. Proc Natl Acad Sci U S A 94:2410–2414. https://doi.org/10.1073/pnas.94.6.2410.
  • Ji X, Kong J, Liebhaber SA. 2011. An RNA-protein complex links enhanced nuclear 3′ processing with cytoplasmic mRNA stabilization. EMBO J 30:2622–2633. https://doi.org/10.1038/emboj.2011.171.
  • Ji X, Kong J, Carstens RP, Liebhaber SA. 2007. The 3′ untranslated region complex involved in stabilization of human alpha-globin mRNA assembles in the nucleus and serves an independent role as a splice enhancer. Mol Cell Biol 27:3290–3302. https://doi.org/10.1128/MCB.02289-05.
  • Ji X, Kong J, Liebhaber SA. 2003. In vivo association of the stability control protein alphaCP with actively translating mRNAs. Mol Cell Biol 23:899–907. https://doi.org/10.1128/MCB.23.3.899-907.2003.
  • Ji X, Park JW, Bahrami-Samani E, Lin L, Duncan-Lewis C, Pherribo G, Xing Y, Liebhaber SA. 2016. alphaCP binding to a cytosine-rich subset of polypyrimidine tracts drives a novel pathway of cassette exon splicing in the mammalian transcriptome. Nucleic Acids Res 44:2283–2297. https://doi.org/10.1093/nar/gkw088.
  • Ji X, Wan J, Vishnu M, Xing Y, Liebhaber SA. 2013. alphaCP poly(C) binding proteins act as global regulators of alternative polyadenylation. Mol Cell Biol 33:2560–2573. https://doi.org/10.1128/MCB.01380-12.
  • Chkheidze AN, Lyakhov DL, Makeyev AV, Morales J, Kong J, Liebhaber SA. 1999. Assembly of the alpha-globin mRNA stability complex reflects binary interaction between the pyrimidine-rich 3′ untranslated region determinant and poly(C) binding protein alphaCP. Mol Cell Biol 19:4572–4581. https://doi.org/10.1128/MCB.19.7.4572.
  • Makeyev AV, Chkheidze AN, Liebhaber SA. 1999. A set of highly conserved RNA-binding proteins, alphaCP-1 and alphaCP-2, implicated in mRNA stabilization, are coexpressed from an intronless gene and its intron-containing paralog. J Biol Chem 274:24849–24857. https://doi.org/10.1074/jbc.274.35.24849.
  • Makeyev AV, Eastmond DL, Liebhaber SA. 2002. Targeting a KH-domain protein with RNA decoys. RNA 8:1160–1173. https://doi.org/10.1017/s135583820202808x.
  • Makeyev AV, Liebhaber SA. 2000. Identification of two novel mammalian genes establishes a subfamily of KH-domain RNA-binding proteins. Genomics 67:301–316. https://doi.org/10.1006/geno.2000.6244.
  • Makeyev AV, Liebhaber SA. 2002. The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA 8:265–278. https://doi.org/10.1017/s1355838202024627.
  • Charroux B, Angelats C, Fasano L, Kerridge S, Vola C. 1999. The levels of the bancal product, a Drosophila homologue of vertebrate hnRNP K protein, affect cell proliferation and apoptosis in imaginal disc cells. Mol Cell Biol 19:7846–7856. https://doi.org/10.1128/MCB.19.11.7846.
  • Colaiacovo MP, Stanfield GM, Reddy KC, Reinke V, Kim SK, Villeneuve AM. 2002. A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 162:113–128. https://doi.org/10.1093/genetics/162.1.113.
  • Geng C, Macdonald PM. 2007. Identification of genes that influence gurken expression. Fly (Austin) 1:259–267. https://doi.org/10.4161/fly.5246.
  • Ghanem LR, Kromer A, Silverman IM, Chatterji P, Traxler E, Penzo-Mendez A, Weiss MJ, Stanger BZ, Liebhaber SA. 2016. The poly(C) binding protein Pcbp2, and its retrotransposed derivative Pcbp1, are independently essential to mouse development. Mol Cell Biol 36:304–319. https://doi.org/10.1128/MCB.00936-15.
  • Heinrich AC, Pelanda R, Klingmuller U. 2004. A mouse model for visualization and conditional mutations in the erythroid lineage. Blood 104:659–666. https://doi.org/10.1182/blood-2003-05-1442.
  • Wu H, Liu X, Jaenisch R, Lodish HF. 1995. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83:59–67. https://doi.org/10.1016/0092-8674(95)90234-1.
  • Friend C, Scher W, Holland JG, Sato T. 1971. Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethyl sulfoxide. Proc Natl Acad Sci U S A 68:378–382. https://doi.org/10.1073/pnas.68.2.378.
  • Kiledjian M, Wang X, Liebhaber SA. 1995. Identification of two KH domain proteins in the alpha-globin mRNP stability complex. EMBO J 14:4357–4364. https://doi.org/10.1002/j.1460-2075.1995.tb00110.x.
  • Ghanem LR, Kromer A, Silverman IM, Ji X, Gazzara M, Nguyen N, Aguilar G, Martinelli M, Barash Y, Liebhaber SA. 2018. Poly(C)-binding protein Pcbp2 enables differentiation of definitive erythropoiesis by directing functional splicing of the Runx1 transcript. Mol Cell Biol 38:e00175-18. https://doi.org/10.1128/MCB.00175-18.
  • Waggoner SA, Johannes GJ, Liebhaber SA. 2009. Depletion of the poly(C)-binding proteins alphaCP1 and alphaCP2 from K562 cells leads to p53-independent induction of cyclin-dependent kinase inhibitor (CDKN1A) and G1 arrest. J Biol Chem 284:9039–9049. https://doi.org/10.1074/jbc.M806986200.
  • Gamarnik AV, Andino R. 1997. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3:882–892.
  • Tang YS, Khan RA, Zhang Y, Xiao S, Wang M, Hansen DK, Jayaram HN, Antony A. 2011. Incrimination of heterogeneous nuclear ribonucleoprotein E1 (hnRNP-E1) as a candidate sensor of physiological folate deficiency. J Biol Chem 286:39100–39115. https://doi.org/10.1074/jbc.M111.230938.
  • Ryu MS, Zhang D, Protchenko O, Shakoury-Elizeh M, Philpott CC. 2017. PCBP1 and NCOA4 regulate erythroid iron storage and heme biosynthesis. J Clin Invest 127:1786–1797. https://doi.org/10.1172/JCI90519.
  • Perrotti D, Calabretta B. 2002. Post-transcriptional mechanisms in BCR/ABL leukemogenesis: role of shuttling RNA-binding proteins. Oncogene 21:8577–8583. https://doi.org/10.1038/sj.onc.1206085.
  • Woolaway K, Asai K, Emili A, Cochrane A. 2007. hnRNP E1 and E2 have distinct roles in modulating HIV-1 gene expression. Retrovirology 4:28. https://doi.org/10.1186/1742-4690-4-28.
  • Chaudhury A, Hussey GS, Ray PS, Jin G, Fox PL, Howe PH. 2010. TGF-beta-mediated phosphorylation of hnRNP E1 induces EMT via transcript-selective translational induction of Dab2 and ILEI. Nat Cell Biol 12:286–293. https://doi.org/10.1038/ncb2029.
  • Khandros E, Thom CS, D'Souza J, Weiss MJ. 2012. Integrated protein quality-control pathways regulate free α-globin in murine β-thalassemia. Blood 119:5265–5275. https://doi.org/10.1182/blood-2011-12-397729.
  • Zhang J, Socolovsky M, Gross AW, Lodish HF. 2003. Role of Ras signaling in erythroid differentiation of mouse fetal liver cells: functional analysis by a flow cytometry-based novel culture system. Blood 102:3938–3946. https://doi.org/10.1182/blood-2003-05-1479.
  • Pimkin M, Kossenkov AV, Mishra T, Morrissey CS, Wu W, Keller CA, Blobel GA, Lee D, Beer MA, Hardison RC, Weiss MJ. 2014. Divergent functions of hematopoietic transcription factors in lineage priming and differentiation during erythro-megakaryopoiesis. Genome Res 24:1932–1944. https://doi.org/10.1101/gr.164178.113.
  • An X, Schulz VP, Li J, Wu K, Liu J, Xue F, Hu J, Mohandas N, Gallagher PG. 2014. Global transcriptome analyses of human and murine terminal erythroid differentiation. Blood 123:3466–3477. https://doi.org/10.1182/blood-2014-01-548305.
  • Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, Li X, Gueroussov S, Albu M, Zheng H, Yang A, Na H, Irimia M, Matzat LH, Dale RK, Smith SA, Yarosh CA, Kelly SM, Nabet B, Mecenas D, Li W, Laishram RS, Qiao M, Lipshitz HD, Piano F, Corbett AH, Carstens RP, Frey BJ, Anderson RA, Lynch KW, Penalva LOF, Lei EP, Fraser AG, Blencowe BJ, Morris QD, Hughes TR. 2013. A compendium of RNA-binding motifs for decoding gene regulation. Nature 499:172–177. https://doi.org/10.1038/nature12311.
  • Alvarez-Dominguez JR, Zhang X, Hu W. 2017. Widespread and dynamic translational control of red blood cell development. Blood 129:619–629. https://doi.org/10.1182/blood-2016-09-741835.
  • Heinicke LA, Nabet B, Shen S, Jiang P, van Zalen S, Cieply B, Russell JE, Xing Y, Carstens RP. 2013. The RNA binding protein RBM38 (RNPC1) regulates splicing during late erythroid differentiation. PLoS One 8:e78031. https://doi.org/10.1371/journal.pone.0078031.
  • Ulirsch JC, Nandakumar SK, Wang L, Giani FC, Zhang X, Rogov P, Melnikov A, McDonel P, Do R, Mikkelsen TS, Sankaran VG. 2016. Systematic functional dissection of common genetic variation affecting red blood cell traits. Cell 165:1530–1545. https://doi.org/10.1016/j.cell.2016.04.048.
  • Zhang J, Xu E, Ren C, Yan W, Zhang M, Chen M, Cardiff RD, Imai DM, Wisner E, Chen X. 2014. Mice deficient in Rbm38, a target of the p53 family, are susceptible to accelerated aging and spontaneous tumors. Proc Natl Acad Sci U S A 111:18637–18642. https://doi.org/10.1073/pnas.1415607112.
  • Ji X, Humenik J, Liebhaber SA. 2019. A cytosine-rich splice regulatory determinant enforces functional processing of the human α-globin gene transcript. Blood 133:2338–2347. https://doi.org/10.1182/blood-2018-12-891408.
  • Ji X, Humenik J, Yang D, Liebhaber SA. 2018. PolyC-binding proteins enhance expression of the CDK2 cell cycle regulatory protein via alternative splicing. Nucleic Acids Res 46:2030–2044. https://doi.org/10.1093/nar/gkx1255.
  • Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA. 2009. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457:887–891. https://doi.org/10.1038/nature07619.
  • Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84:321–330. https://doi.org/10.1016/S0092-8674(00)80986-1.
  • Tober J, Maijenburg MW, Speck NA. 2016. Taking the leap: Runx1 in the formation of blood from endothelium. Curr Top Dev Biol 118:113–162. https://doi.org/10.1016/bs.ctdb.2016.01.008.
  • Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, Speck NA. 1996. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A 93:3444–3449. https://doi.org/10.1073/pnas.93.8.3444.
  • Conboy J, Kan YW, Shohet SB, Mohandas N. 1986. Molecular cloning of protein 4.1, a major structural element of the human erythrocyte membrane skeleton. Proc Natl Acad Sci U S A 83:9512–9516. https://doi.org/10.1073/pnas.83.24.9512.
  • Rana AP, Ruff P, Maalouf GJ, Speicher DW, Chishti AH. 1993. Cloning of human erythroid dematin reveals another member of the villin family. Proc Natl Acad Sci U S A 90:6651–6655. https://doi.org/10.1073/pnas.90.14.6651.
  • Siegel DL, Branton D. 1985. Partial purification and characterization of an actin-bundling protein, band 4.9, from human erythrocytes. J Cell Biol 100:775–785. https://doi.org/10.1083/jcb.100.3.775.
  • Conboy J, Mohandas N, Tchernia G, Kan YW. 1986. Molecular basis of hereditary elliptocytosis due to protein 4.1 deficiency. N Engl J Med 315:680–685. https://doi.org/10.1056/NEJM198609113151105.
  • Conboy JG, Chan J, Mohandas N, Kan YW. 1988. Multiple protein 4.1 isoforms produced by alternative splicing in human erythroid cells. Proc Natl Acad Sci U S A 85:9062–9065. https://doi.org/10.1073/pnas.85.23.9062.
  • Conboy JG, Chan JY, Chasis JA, Kan YW, Mohandas N. 1991. Tissue- and development-specific alternative RNA splicing regulates expression of multiple isoforms of erythroid membrane protein 4.1. J Biol Chem 266:8273–8280. https://doi.org/10.1016/S0021-9258(18)92973-X.
  • Huang SC, Zhang HS, Yu B, McMahon E, Nguyen DT, Yu FH, Ou AC, Ou JP, Benz EJ, Jr. 2017. Protein 4.1R exon 16 3′ splice site activation requires coordination among TIA1, Pcbp1, and RBM39 during terminal erythropoiesis. Mol Cell Biol 37:e00446-16. https://doi.org/10.1128/MCB.00446-16.
  • 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.
  • Doench JG, Fusi N, Sullender M, Hegde M, Vaimberg EW, Donovan KF, Smith I, Tothova Z, Wilen C, Orchard R, Virgin HW, Listgarten J, Root DE. 2016. Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat Biotechnol 34:184–191. https://doi.org/10.1038/nbt.3437.
  • Vaquero-Garcia J, Barrera A, Gazzara MR, González-Vallinas J, Lahens NF, Hogenesch JB, Lynch KW, Barash Y. 2016. A new view of transcriptome complexity and regulation through the lens of local splicing variations. eLife 5:e11752. https://doi.org/10.7554/eLife.11752.
  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. https://doi.org/10.1093/nar/gkp335.

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