A regulatory function of long non-coding RNAs in red blood cell development

  • Klaudia Kulczyńska
  • Miroslawa Siatecka Adam Mickiewicz University Institute of Experimental Biology Department of Genetics
Keywords: long non-coding RNA, erythropoiesis, red blood cells,

Abstract

During recent years it has been discovered that long non-coding RNAs are important regulators in many biological processes. In this review, we summarize the role of lncRNA in erythropoiesis. LncRNA are crucial for regulation of gene expression during both proliferation and differentiation stages of red blood cell development. Many are regulated by erythroidspecific transcription factors and some are expressed in a developmental stage-specific manner. The majority of individually studied lncRNAs are involved in regulating the terminal maturation stages of red cell differentiation. Their regulatory function is accomplished by various mechanisms, including direct regulation in cis or trans by the lncRNA product or by the cis-localized presence of the lncRNA transcription itself. These add additional levels of regulation of gene expression during erythropoiesis.

References

Alper SL (2009) Molecular physiology and genetics of Na+-independent SLC4 anion exchangers. J. Exp. Biol. 212: 1672–1683 http://doi.org/10.1242/jeb.029454

Alvarez-Dominguez JR, Hu W, Yuan B, Shi J, Park SS, Gromatzky AA, Van Oudenaarden A & Lodish HF (2014) Global discovery of erythroid long noncoding RNAs reveals novel regulators of red cell maturation. Blood 123: 570–581 http://doi.org/10.1182/blood-2013-10-530683

An X & Mohandas N (2011) Erythroblastic islands, terminal erythroid differentiation and reticulocyte maturation. Int. J. Hematol. 93: 139–143 http://doi.org/10.1007/s12185-011-0779-x

Arriaga-Canon C, Fonseca-Guzmán Y, Valdes-Quezada C, Arzate-Mejía R, Guerrero G & Recillas-Targa F (2014) A long non-coding RNA promotes full activation of adult gene expression in the chicken α-globin domain. Epigenetics 9: 173–181 http://doi.org/10.4161/epi.27030

Ashe HL, Monks J, Wijgerde M, Fraser P & Proudfoot NJ (1997) Intergenic transcription and transinduction of the human beta -globin locus. Genes Dev. 11: 2494–2509 http://doi.org/10.1101/gad.11.19.2494

Barker JE (1968) Development of the mouse hematopoietic system. Dev. Biol. 18: 14–29 http://doi.org/10.1016/0012-1606(68)90020-1

Batista PJ & Chang HY (2013) Long noncoding RNAs: Cellular address codes in development and disease. Cell 152: 1298–1307 http://doi.org/10.1016/j.cell.2013.02.012

Bender M, Bulger M, Close J & Groudine M (2000) β-globin Gene Switching and DNase I Sensitivity of the Endogenous β-globin Locus in Mice Do Not Require the Locus Control Region. Mol. Cell 5: 387–393 http://doi.org/10.1016/S1097-2765(00)80433-5

Gribnau J, Diderich K, Pruzina S, Calzolari R & Fraser P (2000) Intergenic Transcription and Developmental Remodeling of Chromatin Subdomains in the Human β-globin Locus. Mol. Cell 5: 377–386 http://doi.org/10.1016/S1097-2765(00)80432-3

Guttman M & Rinn JL (2012) Modular regulatory principles of large non-coding RNAs. Nature 482: 339–346 http://doi.org/10.1038/nature10887

Homma N, Takei Y, Tanaka Y, Nakata T, Terada S, Kikkawa M, Noda Y & Hirokawa N (2003) Kinesin Superfamily Protein 2A (KIF2A) Functions in Suppression of Collateral Branch Extension. Cell 114: 229–239 http://doi.org/10.1016/S0092-8674(03)00522-1

Hu W, Yuan B, Flygare J & Lodish HF (2011) Long noncoding RNA-mediated anti-apoptotic activity in murine erythroid terminal differentiation. Genes Dev. 25: 2573–2578 http://doi.org/10.1101/gad.178780.111

Ji P & Lodish HF (2010) Rac GTPases play multiple roles in erythropoiesis. Haematologica 95: 2–4 http://doi.org/10.3324/haematol.2009.015511

Klein U, Lia M, Crespo M, Siegel R, Shen Q, Mo T, Ambesi-Impiombato A, Califano A, Migliazza A, Bhagat G & Dalla-Favera R (2010) The DLEU2/miR-15a/16-1 Cluster Controls B Cell Proliferation and Its Deletion Leads to Chronic Lymphocytic Leukemia. Cancer Cell 17: 28–40 http://doi.org/10.1016/j.ccr.2009.11.019

Kung JTY, Colognori D & Lee JT (2013) Long Noncoding RNAs: Past, Present, and Future. Genetics 193: 651–669 http://doi.org/10.1534/genetics.112.146704

Lawrie CH (2009) microRNA expression in erythropoiesis and erythroid disorders. Br. J. Haematol. 150: 144–151 http://doi.org/10.1111/j.1365-2141.2009.07978.x

Lerner M, Harada M, Lovén J, Castro J, Davis Z, Oscier D, Henriksson M, Sangfelt O, Grandér D & Corcoran MM (2009) DLEU2, frequently deleted in malignancy, functions as a critical host gene of the cell cycle inhibitory microRNAs miR-15a and miR-16-1. Exp. Cell Res. 315: 2941–2952 http://doi.org/10.1016/j.yexcr.2009.07.001

Ling J, Ainol L, Zhang L, Yu X, Pi W & Tuan D (2004) HS2 Enhancer Function Is Blocked by a Transcriptional Terminator Inserted between the Enhancer and the Promoter. J. Biol. Chem. 279: 51704–51713 http://doi.org/10.1074/jbc.M404039200

Ling J, Baibakov B, Pi W, Emerson BM & Tuan D (2005) The HS2 Enhancer of the β-globin Locus Control Region Initiates Synthesis of Non-coding, Polyadenylated RNAs Independent of a cis-linked Globin Promoter. J. Mol. Biol. 350: 883–896 http://doi.org/10.1016/j.jmb.2005.05.039

Listowski M, Heger E, Bogusławska D, Machnicka B, Kuliczkowski K, Leluk J & Sikorski A (2013) microRNAs: fine tuning of erythropoiesis. Cell. Mol. Biol. Lett. 18: 34–46 http://doi.org/10.2478/s11658-012-0038-z

Lu J, Getz G, Miska E a, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando A a, Downing JR, Jacks T, Horvitz HR & Golub TR (2005) MicroRNA expression profiles classify human cancers. Nature 435: 834–838 http://doi.org/10.1038/nature03702

Manwani D & Bieker JJ (2008) Chapter 2 The Erythroblastic Island. In Current Topics in Developmental Biology pp 23–53. http://doi.org/10.1016/S0070-2153(07)00002-6

Miller IJ & Bieker JJ (1993) A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Krüppel family of nuclear proteins. Mol. Cell. Biol. 13: 2776–2786 http://doi.org/10.1128/MCB.13.5.2776

Novershtern N, Subramanian A, Lawton LN, Mak RH, Haining WN, McConkey ME, Habib N, Yosef N, Chang CY, Shay T, Frampton GM, Drake ACB, Leskov I, Nilsson B, Preffer F, Dombkowski D, Evans JW, Liefeld T, Smutko JS, Chen J, et al (2011) Densely Interconnected Transcriptional Circuits Control Cell States in Human Hematopoiesis. Cell 144: 296–309 http://doi.org/10.1016/j.cell.2011.01.004

Nuez B, Michalovich D, Bygrave A, Ploemacher R & Grosveld F (1995) Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375: 316–318 http://doi.org/10.1038/375316a0

Ohtsuka T, Ryu H, Minamishima Y a, Macip S, Sagara J, Nakayama KI, Aaronson S a & Lee SW (2004) ASC is a Bax adaptor and regulates the p53–Bax mitochondrial apoptosis pathway. Nat. Cell Biol. 6: 121–128 http://doi.org/10.1038/ncb1087

Orkin SH & Zon LI (2008) Hematopoiesis: An Evolving Paradigm for Stem Cell Biology. Cell 132: 631–644 http://doi.org/10.1016/j.cell.2008.01.025

Palis J (2014) Primitive and definitive erythropoiesis in mammals. Front. Physiol. 5: http://doi.org/10.3389/fphys.2014.00003

Paralkar VR, Mishra T, Luan J, Yao Y, Kossenkov A V., Anderson SM, Dunagin M, Pimkin M, Gore M, Sun D, Konuthula N, Raj A, An X, Mohandas N, Bodine DM, Hardison RC & Weiss MJ (2014) Lineage and species-specific long noncoding RNAs during erythro-megakaryocytic development. Blood 123: 1927–1937 http://doi.org/10.1182/blood-2013-12-544494

Paralkar VR & Weiss MJ (2011) A new ‘Linc’ between noncoding RNAs and blood development. Genes Dev. 25: 2555–2558 http://doi.org/10.1101/gad.183020.111

Perkins AC, Sharpe AH & Orkin SH (1995) Lethal β-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375: 318–322 http://doi.org/10.1038/375318a0

Ponting C, Schultz J & Bork P (1997) SPRY domains in ryanodine receptors (Ca2+-release channels). Trends Biochem. Sci. 22: 193–194 http://doi.org/10.1016/S0968-0004(97)01049-9

Rinn JL & Chang HY (2012) Genome Regulation by Long Noncoding RNAs. Annu. Rev. Biochem. 81: 145–166 http://doi.org/10.1146/annurev-biochem-051410-092902

Sánchez-López JY, Camacho-Torres AL, Ibarra B, Tintos JA & Perea FJ (2010) Analysis of the SLC4A1 gene in three Mexican patients with hereditary spherocytosis: report of a novel mutation. Genet. Mol. Biol. 33: 9–11 http://doi.org/10.1590/S1415-47572009005000109

Siatecka M & Bieker JJ (2011) The multifunctional role of EKLF/KLF1 during erythropoiesis. Blood 118: 2044–2054 http://doi.org/10.1182/blood-2011-03-331371

Sun L, Zhang Z, Bailey TL, Perkins AC, Tallack MR, Xu Z & Liu H (2012) Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. BMC Bioinformatics 13: 331 http://doi.org/10.1186/1471-2105-13-331

Uehara R, Tsukada Y, Kamasaki T, Poser I, Yoda K, Gerlich DW & Goshima G (2013) Aurora B and Kif2A control microtubule length for assembly of a functional central spindle during anaphase. J. Cell Biol. 202: 623–636 http://doi.org/10.1083/jcb.201302123

Villamizar O, Chambers CB, Mo Y-Y, Torry DS, Hofstrand R, Riberdy JM, Persons DA & Wilber A (2016) Fas-antisense long noncoding RNA is differentially expressed during maturation of human erythrocytes and confers resistance to Fas-mediated cell death. Blood Cells, Mol. Dis. 58: 57–66 http://doi.org/10.1016/j.bcmd.2016.03.002

Wang C, Wu X, Shen F, Li Y, Zhang Y & Yu D (2015) Shlnc-EC6 regulates murine erythroid enucleation by Rac1-PIP5K pathway. Dev. Growth Differ. 57: 466–73 http://doi.org/10.1111/dgd.12225

Wang KC & Chang HY (2011) Molecular Mechanisms of Long Noncoding RNAs. Mol. Cell 43: 904–914 http://doi.org/10.1016/j.molcel.2011.08.018

Wienholds E & Plasterk RHA (2005) MicroRNA function in animal development. FEBS Lett. 579: 5911–5922 http://doi.org/10.1016/j.febslet.2005.07.070

Wilusz JE, Sunwoo H & Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 23: 1494–1504 http://doi.org/10.1101/gad.1800909

Yan M-D (2005) Identification and characterization of a novel gene Saf transcribed from the opposite strand of Fas. Hum. Mol. Genet. 14: 1465–1474 http://doi.org/10.1093/hmg/ddi156

Zhao G, Yu D & Weiss MJ (2010) MicroRNAs in erythropoiesis. Curr. Opin. Hematol. 17: 1 http://doi.org/10.1097/MOH.0b013e328337ba6c

Published
2017-03-04