MicroRNAs in erythropoiesis and red blood cell disorders
Tóm tắt
MicroRNAs (miRNAs) are 19-24 nucleotide non-coding ribonucleic acids binding DNA or RNA and controlling gene expression via mRNA degradation or its transcription inhibition. Erythropoies is a multi step differentiation process of erythroid progenitors to nucleate red blood cells. Maturation, proliferation and differentiation of red blood cells is affected by erythroid factors, signaling pathways in niche of hematopoietic cells, transcription factors as well as miRNAs. Expression of different types of miRNAs during erythroid development provides a background for the study of these molecules to control erythroid differentiation and maturation as well as their use as diagnostic and prognostic markers to treat erythroid disorders like thalassemia, sickle cell disease and erythrocyte enzyme deficiencies. In this paper, with reference to biosynthesis of miRNAs, their function in normal and anemic erythropoiesis has been investigated. The target molecule of each of these miRNAs has been cited in an attempt to elucidate their role in erythropoiesis.
Tài liệu tham khảo
Aalto A P, Pasquinelli A E (2012). Small non-coding RNAs mount a silent revolution in gene expression. Curr Opin Cell Biol, 24(3): 333–340
Aerbajinai W, Giattina M, Lee Y T, Raffeld M, Miller J L (2003). The proapoptotic factor Nix is coexpressed with Bcl-xL during terminal erythroid differentiation. Blood, 102(2): 712–717
Andolfo I, De Falco L, Asci R, Russo R, Colucci S, Gorrese M, Zollo M, Iolascon A(2010). Regulation of divalent metal transporter 1 (DMT1) non-IRE isoform by the microRNA Let-7d in erythroid cells. Haematologica, 95(8): 1244–1252
Azzouzi I, Schmugge M, Speer O (2012). MicroRNAs as components of regulatory networks controlling erythropoiesis. Eur J Haematol, 89 (1): 1–9
Bakker W J, Blázquez-Domingo M, Kolbus A, Besooyen J, Steinlein P, Beug H, Coffer P J, Löwenberg B, von Lindern M, van Dijk T B (2004). FoxO3a regulates erythroid differentiation and induces BTG1, an activator of protein arginine methyl transferase 1. J Cell Biol, 164(2): 175–184
Bakker W J, van Dijk T B, Parren-van Amelsvoort M, Kolbus A, Yamamoto K, Steinlein P, Verhaak R G, Mak T W, Beug H, Löwenberg B, von Lindern M (2007). Differential regulation of Foxo3a target genes in erythropoiesis. Mol Cell Biol, 27(10): 3839–3854
Baltimore D, Boldin M P, O’Connell R M, Rao D S, Taganov K D (2008). MicroRNAs: new regulators of immune cell development and function. Nat Immunol, 9(8): 839–845
Bank A (2006). Regulation of human fetal hemoglobin: new players, new complexities. Blood, 107(2): 435–443
Basu P, Lung T K, Lemsaddek W, Sargent T G, Williams D C Jr, Basu M, Redmond L C, Lingrel J B, Haar J L, Lloyd J A (2007). EKLF and KLF2 have compensatory roles in embryonic ß-globin gene expression and primitive erythropoiesis. Blood, 110(9): 3417–3425
Bianchi E, Zini R, Salati S, Tenedini E, Norfo R, Tagliafico E, Manfredini R, Ferrari S (2010). c-myb supports erythropoiesis through the transactivation of KLF1 and LMO2 expression. Blood, 116(22): e99–e110
Bianchi N, Zuccato C, Finotti A, Lampronti I, Borgatti M, Gambari R (2012). Involvement of miRNA in erythroid differentiation. Epigenomics, 4(1): 51–65
Bianchi N, Zuccato C, Lampronti I, Borgatti M, Gambari R (2009). Expression of miR-210 during erythroid differentiation and induction of gamma-globin gene expression. BMB Rep, 42(8): 493–499
Bracht J R, Van Wynsberghe P M, Mondol V, Pasquinelli A E (2010). Regulation of lin-4 miRNA expression, organismal growth and development by a conserved RNA binding protein in C. elegans. Dev Biol, 348(2): 210–221
Bruchova H, Merkerova M, Prchal J T (2008). Aberrant expression of microRNA in polycythemia vera. Haematologica. 93(7): 1009–1016
Bruchova H, Yoon D, Agarwal A M, Mendell J, Prchal J T (2007). Regulated expression of microRNAs in normal and polycythemia vera erythropoiesis. Exp Hematol, 35(11): 1657–1667
Bruchova H, Yoon D, Agarwal A M, Swierczek S, Prchal J T (2009). Erythropoiesis in polycythemia vera is hyper-proliferative and has accelerated maturation. Blood Cells Mol Dis, 43(1): 81–87
Bruchova-Votavova H, Yoon D, Prchal J T (2010). miR-451 enhances erythroid differentiation in K562 cells. Leuk Lymphoma, 51(4): 686–693
Buccheri M A, Spina S, Ruberto C, Lombardo T, Labie D, Ragusa A A (2013). Annotated definition of BCL11A and HMIP-2 haplotypes through the analysis of sicilian ß-thalassemia patients with high levels of fetal hemoglobin. Hemoglobin, 37(5): 423–434
Byon J C, Papayannopoulou T (2012). MicroRNAs: Allies or foes in erythropoiesis? J Cell Physiol, 227(1): 7–13
Cantor A B, Orkin S H (2002). Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene, 21 (21): 3368–3376
Centis F, Tabellini L, Lucarelli G, Buffi O, Tonucci P, Persini B, Annibali M, Emiliani R, Iliescu A, Rapa S, Roßsi R, Ma L, Angelucci E, Schrier S L (2000). The importance of erythroid expansion in determining the extent of apoptosis in erythroid precursors in patients with β-thalassemia major. Blood, 96(10): 3624–3629
Cheloufi S, Dos Santos C O, Chong M M, Hannon G J (2010). A dicerindependent miRNA biogenesis pathway that requires Ago catalysis. Nature, 465(7298): 584–589
Chen S Y, Wang Y, Telen M J, Chi J T (2008). The genomic analysis of erythrocyte microRNA expression in sickle cell diseases. PLoS ONE, 3(6): e2360
Choong M L, Yang H H, McNiece I (2007). MicroRNA expression profiling during human cord blood-derived CD34 cell erythropoiesis. Exp Hematol, 35(4): 551–564
Davis M, Clarke S (2013). Influence of microRNA on the maintenance of human iron metabolism. Nutrients, 5(7): 2611–2628
Dore L C, Amigo J D, Dos Santos C O, Zhang Z, Gai X, Tobias J W, Yu D, Klein AM, Dorman C, Wu W, Hardison R C, Paw B H, Weiss MJ (2008). A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc Natl Acad Sci USA, 105(9): 3333–3338
Fabbri M, Garzon R, Andreeff M, Kantarjian H M, Garcia-Manero G, Calin G A (2008). MicroRNAs and noncoding RNAs in hematological malignancies: molecular, clinical and therapeutic implications. Leukemia, 22(6): 1095–1105
Fard A D, Hoßseini S A, Shahjahani M, Salari F, Jaseb K (2013). Evaluation of novel fetal hemoglobin inducer drugs in treatment of β-hemoglobinopathy disorders. Int J Hematol Oncol Stem Cell Res, 7 (3): 47–54
Felli N, Fontana L, Pelosi E, Botta R, Bonci D, Facchiano F, Liuzzi F, Lulli V, Morsilli O, Santoro S, Valtieri M, Calin G A, Liu C G, Sorrentino A, Croce C M, Peschle C (2005). MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci USA, 102(50): 18081–18086
Felli N, Pedini F, Romania P, Biffoni M, Morsilli O, Castelli G, Santoro S, Chicarella S, Sorrentino A, Peschle C, Marziali G (2009). MicroRNA 223-dependent expression of LMO2 regulates normal erythropoiesis. haematologica. Haematologica, 94(4): 479–86
Ferreira R, Ohneda K, Yamamoto M, Philipsen S (2005). GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol Cell Biol, 25(4): 1215–1227
Fu Y F, Du T T, Dong M, Zhu K Y, Jing C B, Zhang Y, Wang L, Fan H B, Chen Y, Jin Y, Yue G P, Chen S J, Chen Z, Huang Q H, Jing Q, Deng M, Liu T X (2009). Mir-144 selectively regulates embryonic a-hemoglobin synthesis during primitive erythropoiesis. Blood, 113(6): 1340–1349
García P, Frampton J (2008). Hematopoietic lineage commitment: miRNAs add specificity to a widely expressed transcription factor. Dev Cell, 14(6): 815–816
Garzon R, Pichiorri F, Palumbo T, Iuliano R, Cimmino A, Aqeilan R, Volinia S, Bhatt D, Alder H, Marcucci G, Calin G A, Liu C G, Bloomfield C D, Andreeff M, Croce C M (2006). MicroRNA fingerprints during human megakaryocytopoiesis. Proc Natl Acad Sci USA, 103(13): 5078–5083
Grebien F, Kerenyi M A, Kovacic B, Kolbe T, Becker V, Dolznig H, Pfeffer K, Klingmüller U, Müller M, Beug H, Müllner E W, Moriggl R (2008). Stat5 activation enables erythropoiesis in the absence of EpoR and Jak2. Blood, 111(9): 4511–4522
Guerau-de-Arellano M, Alder H, Ozer H G, Lovett-Racke A, RackeMK (2012). miRNA profiling for biomarker discovery in multiple sclerosis: from microarray to deep sequencing. J Neuroimmunol, 248(1-2): 32–39
Guglielmelli P, Tozzi L, Bogani C, Iacobucci I, Ponziani V, Martinelli G, Bosi A, Vannucchi A M, and the AGIMM (AIRC-Gruppo Italiano Malattie Mieloproliferative) Investigators (2011). Overexpression of microRNA-16-2 contributes to the abnormal erythropoiesis in polycythemia vera. Blood, 117(25): 6923–6927
Hansson A, Zetterblad J, Van Duren C, Axelson H, Jönsson J I (2007). The Lim-only protein LMO2 acts as a positive regulator of erythroid differentiation. Biochem Biophys Res Commun, 364(3): 675–681
Hattangadi S M, Wong P, Zhang L, Flygare J, Lodish H F (2011). From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood, 118 (24): 6258–6268
Havelange V, Garzon R (2010). MicroRNAs: emerging key regulators of hematopoiesis. Am J Hematol, 85(12): 935–942
Higgs D R, Garrick D, Anguita E, De Gobbi M, Hughes J, Muers M, Vernimmen D, Lower K, Law M, Argentaro A, Deville M A, Gibbons R (2005). Understanding a-globin gene regulation: Aiming to improve the management of thalassemia. Ann N Y Acad Sci, 1054 (1): 92–102
Hilliard L M, Berkow R L (1996). The thalassemia syndromes. Prim Care Update Ob Gyns, 3(5): 157–162
Huang X, Gschweng E, Van Handel B, Cheng D, Mikkolav H K, Witte O N (2011). Regulated expression of microRNAs-126/126* inhibits erythropoiesis from human embryonic stem cells. Blood, 117(7): 2157–2165
Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M (2000). Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem, 275(21): 16023–16029
James C (2008). The JAK2V617F mutation in polycythemia vera and other myeloproliferative disorders: one mutation for three diseases? Hematology (Am Soc Hematol Educ Program), 2008(1): 69–75
Kandhavelu M, Kandhavelu J (2012). pre-piRNA biogenesis mimics the pathway of miRNA. Biochem Syst Ecol, 43: 200–204
Karius T, Schnekenburger M, Dicato M, Diederich M (2012). MicroRNAs in cancer management and their modulation by dietary agents. Biochem Pharmacol, 83(12): 1591–1601
Kim M, Tan Y S, Cheng W C, Kingsbury T J, Heimfeld S, Civin C I (2014). MIR144 and MIR451 regulate human erythropoiesis via RAB14. Br J Haematol, 168(4): 583–597
Kim S I, Bresnick E H (2007). Transcriptional control of erythropoiesis: emerging mechanisms and principles. Oncogene, 26(47): 6777–6794
Kosaka N, Sugiura K, Yamamoto Y, Yoshioka Y, Miyazaki H, Komatsu N, Ochiya T, Kato T (2008). Identification of erythropoietin-induced microRNAs in haematopoietic cells during erythroid differentiation. Br J Haematol, 142(2): 293–300
Lawrie C H (2010). microRNA expression in erythropoiesis and erythroid disorders. Br J Haematol, 150(2): 144–151
Lee JM, Johnson J A (2004). An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol, 37(2): 139–143
Leonard M, Brice M, Engel J D, Papayannopoulou T (1993). Dynamics of GATA transcription factor expression during erythroid differentiation. Blood, 82(4): 1071–1079
Levine R L, Gilliland D G (2008). Myeloproliferative disorders. Blood, 112(6): 2190–2198
Listowski M A, Heger E, Boguslawska D M, Machnicka B, Kuliczkowski K, Leluk J, Sikorski A F (2013). microRNAs: fine tuning of erythropoiesis. Cell Mol Biol Lett, 18(1): 34–46
Lulli V, Romania P, Morsilli O, Cianciulli P, Gabbianelli M, Testa U, Giuliani A, Marziali G (2013). MicroRNA-486-3p regulates g-globin expression in human erythroid cells by directly modulating BCL11A. PLoS ONE, 8(4): e60436
Maniatis T, Fritsch E F, Lauer J, Lawn R M (1980). The molecular genetics of human hemoglobins. Annu Rev Genet, 14(1): 145–178
Masaki S, Ohtsuka R, Abe Y, Muta K, Umemura T (2007). Expression patterns of microRNAs 155 and 451 during normal human erythropoiesis. Biochem Biophys Res Commun, 364(3): 509–514
Mathias L A, Fisher T C, Zeng L, Meiselman H J, Weinberg K I, Hiti A L, Malik P (2000). Ineffective erythropoiesis in ß-thalassemia major is due to apoptosis at the polychromatophilic normoblast stage. Exp Hematol, 28(12): 1343–1353
Melotti P, Calabretta B (1996). Induction of hematopoietic commitment and erythromyeloid differentiation in embryonal stem cells constitutively expressing c-myb. Blood, 87(6): 2221–2234
Merkerova M, Belickova M, Bruchova H (2008). Differential expression of microRNAs in hematopoietic cell lineages. Eur J Haematol, 81(4): 304–310
Moritz K M, Lim G B, Wintour E M (1997). Developmental regulation of erythropoietin and erythropoiesis. Am J Physiol, 273(6 Pt 2): R1829–R1844
Motohashi H, Yamamoto M (2004). Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med, 10(11): 549–557
Munugalavadla V, Kapur R (2005). Role of c-Kit and erythropoietin receptor in erythropoiesis. Crit Rev Oncol Hematol, 54(1): 63–75
Noh S J, Miller S H, Lee Y T, Goh S H, Marincola F M, Stroncek D F, Reed C, Wang E, Miller J L (2009). Let-7 microRNAs are developmentally regulated in circulating human erythroid cells. J Transl Med, 7(1): 98
O’Carroll D, Mecklenbrauker I, Das P P, Santana A, Koenig U, Enright A J, Miska E A, Tarakhovsky A (2007). A Slicer-independent role for Argonaute 2 in hematopoiesis and the microRNA pathway. Genes Dev, 21(16): 1999–2004
O’Connell R M, Rao D S, Chaudhuri A A, Boldin M P, Taganov K D, Nicoll J, Paquette R L, Baltimore D (2008). Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med, 205(3): 585–594
Palis J (2008). Ontogeny of erythropoiesis. Curr Opin Hematol, 15(3): 155–161
Palis J (2014). Primitive and definitive erythropoiesis in mammals. Front Physiol, 5: 3
Papayannopoulou T, Kalmantis T, Stamatoyannopoulos G (1979). Cellular regulation of hemoglobin switching: evidence for inverse relationship between fetal hemoglobin synthesis and degree of maturity of human erythroid cells. Proc Natl Acad Sci USA, 76(12): 6420–6424
Pase L, Layton J E, Kloosterman W P, Carradice D, Waterhouse P M, Lieschke G J (2009). miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2. Blood, 113(8): 1794–1804
Patrick D M, Zhang C C, Tao Y, Yao H, Qi X, Schwartz R J, Jun-Shen Huang L, Olson E N (2010). Defective erythroid differentiation in miR-451 mutant mice mediated by 14-3-3ξ. Genes Dev, 24(15): 1614–1619
Pekarsky Y, Santanam U, Cimmino A, Palamarchuk A, Efanov A, Maximov V, Volinia S, Alder H, Liu C G, Rassenti L, Calin G A
Hagan J P, Kipps T, Croce C M (2006). Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res, 66(24): 11590–11593
Rasmussen K D, Simmini S, Abreu-Goodger C, Bartonicek N, Di Giacomo M, Bilbao-Cortes D, Horos R, Von Lindern M, Enright A J, O’Carroll D (2010). The miR-144/451 locus is required for erythroid homeostasis. J Exp Med, 207(7): 1351–1358
Saki N, Abroun S, Soleimani M, Hajizamani S, Shahjahani M, Kast R E, Mortazavi Y (2015). Involvement of microRNA in t-cell differentiation and malignancy. Int J Hematol Oncol Stem Cell Res, 9(1): 33–49
Sangokoya C, Telen MJ, Chi J T (2010). microRNA miR-144 modulates oxidative stress tolerance and associates with anemia severity in sickle cell disease. Blood, 116(20): 4338–4348
Sankaran V G (2011). Targeted therapeutic strategies for fetal hemoglobin induction. Hematology (Am Soc Hematol Educ Program), 2011(1): 459–465
Sarakul O, Vattanaviboon P, Tanaka Y, Fucharoen S, Abe Y, Svasti S, Umemura T (2013). Enhanced erythroid cell differentiation in hypoxic condition is in part contributed by miR-210. Blood Cells Mol Dis, 51(2): 98–103
Shiozaki M, Sakai R, Tabuchi M, Nakamura T, Sugino K, Sugino H, Eto Y (1992). Evidence for the participation of endogenous activin A/erythroid differentiation factor in the regulation of erythropoiesis. Proc Natl Acad Sci USA, 89(5): 1553–1556
Shivdasani R A (2006). MicroRNAs: regulators of gene expression and cell differentiation. Blood, 108(12): 3646–3653
Silva M, Benito A, Sanz C, Prosper F, Ekhterae D, Nuñez G, Fernandez- Luna J L (1999). Erythropoietin can induce the expression of bcl-x(L) through Stat5 in erythropoietin-dependent progenitor cell lines. J Biol Chem, 274(32): 22165–22169
Stamatoyannopoulos G (2005). Control of globin gene expression during development and erythroid differentiation. Exp Hematol, 33 (3): 259–271
Stenmark H (2009). Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol, 10(8): 513–525
Sturgeon C M, Chicha L, Ditadi A, Zhou Q, McGrath K E, Palis J, Hammond S M, Wang S, Olson E N, Keller G (2012). Primitive erythropoiesis is regulated by miR-126 via nonhematopoietic Vcam-1 + cells. Dev Cell, 23(1): 45–57
Svasti S, Masaki S, Penglong T, Abe Y, Winichagoon P, Fucharoen S, Umemura T (2010). Expression of microRNA-451 in normal and thalassemic erythropoiesis. Ann Hematol, 89(10): 953–958
Tsiftsoglou A S, Vizirianakis I S, Strouboulis J (2009). Erythropoiesis: model systems, molecular regulators, and developmental programs. IUBMB Life, 61(8): 800–830
Valencia-Sanchez M A, Liu J, Hannon G J, Parker R (2006). Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev, 20(5): 515–524
van de Loosdrecht A A, Vellenga E (2000). Myelodysplasia and apoptosis: new insights into ineffective erythropoiesis. Med Oncol, 17(1): 16–21
Vasilatou D, Papageorgiou S, Pappa V, Papageorgiou E, Dervenoulas J (2010). The role of microRNAs in normal and malignant hematopoiesis. Eur J Haematol, 84(1): 1–16
Wadman I A, Osada H, Grütz G G, Agulnick A D, Westphal H, Forster A, Rabbitts T H (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(11): 3145–3157
Walker A L, Steward S, Howard T A, Mortier N, Smeltzer M, Wang Y D, Ware R E (2011). Epigenetic and molecular profiles of erythroid cells after hydroxyurea treatment in sickle cell anemia. Blood, 118 (20): 5664–5670
Wall L, deBoer E, Grosveld F (1988). The human beta-globin gene 3' enhancer contains multiple binding sites for an erythroid-specific protein. Genes Dev, 2(9): 1089–1100
Wang F, Yu J, Yang G H, Wang X S, Zhang J W (2011). Regulation of erythroid differentiation by miR-376a and its targets. Cell Res, 21(8): 1196–1209
Wang F, Zhu Y, Guo L, Dong L, Liu H, Yin H, Zhang Z, Li Y, Liu C, Ma Y, Song W, He A, Wang Q, Wang L, Zhang J, Li J, Yu J (2013). A regulatory circuit comprising GATA1/2 switch and microRNA-27a/24 promotes erythropoiesis. Nucleic Acids Res, 42(1): 442–457
Wang L, Li L, Chu S, Shiang K, Li M, Sun H, Xu J, Xiao F J, Sun G, Rossi J J, Ho Y, Bhatia R (2014). MicroRNA-486 regulates normal erythropoiesis and enhances growth and modulates drug response in CML progenitors. Blood, 125(8):1302–1303
Wang Q, Huang Z, Xue H, Jin C, Ju X L, Han J D J, Chen Y G (2008). MicroRNA miR-24 inhibits erythropoiesis by targeting activin type I receptor ALK4. Blood, 111(2): 588–595
Warren A J, Colledge WH, Carlton MB, Evans MJ, Smith A J, Rabbitts T H (1994). The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development. Cell, 78(1): 45–57
Welch J J, Watts J A, Vakoc C R, Yao Y, Wang H, Hardison R C, Blobel G A, Chodosh L A, Weiss M J (2004). Global regulation of erythroid gene expression by transcription factor GATA-1. Blood, 104(10): 3136–3147
Williams D E, Eisenman J, Baird A, Rauch C, Van Ness K, March C J, Park L S, Martin U, Mochizuki D Y, Boswell H S, Burgess G S, Cosman D, Lyman S D (1990). Identification of a ligand for the c-kit proto-oncogene. Cell, 63(1): 167–174
Wu H, Liu X, Jaenisch R, Lodish H F (1995). Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell, 83(1): 59–67
Xu MJ, Sui X, Zhao R, Dai C, Krantz S B, Zhao Z J (2003). PTP-MEG2 is activated in polycythemia vera erythroid progenitor cells and is required for growth and expansion of erythroid cells. Blood, 102(13): 4354–4360
Xu R H, Sampsell-Barron T L, Gu F, Root S, Peck R M, Pan G, Yu J, Antosiewicz-Bourget J, Tian S, Stewart R, Thomson J A (2008). NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell, 3(2): 196–206
Yang J S, Lai E C (2011). Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell, 43(6): 892–903
Yu D, dos Santos C O, Zhao G, Jiang J, Amigo J D, Khandros E, Dore L C, Yao Y, D’Souza J, Zhang Z, Ghaffari S, Choi J, Friend S, Tong W, Orange J S, Paw B H, Weiss M J (2010). miR-451 protects against erythroid oxidant stress by repressing 14-3-3z. Genes Dev, 24(15): 1620–1633
Yuan J, Angelucci E, Lucarelli G, Aljurf M, Snyder LM, Kiefer C R, Ma L, Schrier S L (1993). Accelerated programmed cell death (apoptosis) in erythroid precursors of patients with severe betathalassemia (Cooley’s anemia). Blood, 82(2): 374–377
Zhai P F, Wang F, Su R, Lin H S, Jiang C L, Yang G H, Yu J, Zhang JW (2014). The regulatory roles of microRNA-146b-5p and its target platelet-derived growth factor receptor a (PDGFRA) in erythropoiesis and megakaryocytopoiesis. J Biol Chem, 289(33): 22600–22613
Zhan M, Miller C P, Papayannopoulou T, Stamatoyannopoulos G, Song C Z (2007). MicroRNA expression dynamics during murine and human erythroid differentiation. Exp Hematol, 35(7): 1015–1025
Zhang L, Flygare J, Wong P, Lim B, Lodish H F (2011). miR-191 regulates mouse erythroblast enucleation by down-regulating Riok3 and Mxi1. Genes Dev, 25(2): 119–124
Zhang L, Sankaran V G, Lodish H F (2012). MicroRNAs in erythroid and megakaryocytic differentiation and megakaryocyte-erythroid progenitor lineage commitment. Leukemia, 26(11): 2310–2316
Zhao H, Kalota A, Jin S, Gewirtz A M (2009). The c-myb protooncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood, 113(3): 505–516
Zhou D, Liu K, Sun C W, Pawlik K M, Townes T M (2010). KLF1 regulates BCL11A expression and gamma- to beta-globin gene switching. Nat Genet, 42(9): 742–744
Zhu Y, Wang D, Wang F, Li T, Dong L, Liu H, Ma Y, Jiang F, Yin H, Yan W, Luo M, Tang Z, Zhang G, Wang Q, Zhang J, Zhou J, Yu J (2013). A comprehensive analysis of GATA-1-regulated miRNAs reveals miR-23a to be a positive modulator of erythropoiesis. Nucleic Acids Res, 41(7): 4129–4143