Global discovery of erythroid long noncoding RNAs reveals novel regulators of red cell maturation

Blood

Volumn 123, Issue 4, 2014, Pages 570-581

  Alvarez Dominguez, Juan R ^a,b   Hu, Wenqian ^a   Yuan, Bingbing ^a   Shi, Jiahai ^a   Park, Staphany S ^a,b,c   Gromatzky, Austin A ^a,d   Van Oudenaarden, Alexander ^b,e,f   Lodish, Harvey F ^a,b,d  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c Department of Electrical Engineering and Computer Science   (United States)

^d USA   (United States)

^e HUBRECHT INSTITUTE   (Netherlands)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; POLYADENYLIC ACID; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR KLF1; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ERYTHROID KRUPPEL LIKE FACTOR; ERYTHROID KRUPPEL-LIKE FACTOR; GATA1 PROTEIN, HUMAN; GATA1 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; ONCOPROTEIN; TAL1 PROTEIN, HUMAN; TAL1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL SIZE; CHROMATIN; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENHANCER REGION; ENUCLEATION; ERYTHROCYTE PARAMETERS; ERYTHROID CELL; ERYTHROPOIESIS; FETUS LIVER; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCUS; HIGH THROUGHPUT SEQUENCING; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PSEUDOGENE; RNA SEQUENCE; TISSUE SPECIFICITY; ANIMAL; CELL NUCLEUS; CELL STRAIN K 562; CYTOLOGY; DNA MICROARRAY; ERYTHROCYTE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; GENOME; HUMAN; LIVER; METABOLISM; MOUSE; MUTATION; RETROVIRUS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL NUCLEUS; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; ERYTHROCYTES; ERYTHROID CELLS; ERYTHROPOIESIS; GATA1 TRANSCRIPTION FACTOR; GENE EXPRESSION PROFILING; GENOME; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; K562 CELLS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIVER; MICE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS; RETROVIRIDAE; RNA, LONG NONCODING; TRANSCRIPTION FACTORS;

EID: 84893115719     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-10-530683     Document Type: Article

References (60)

1. Hattangadi SM, Wong P, Zhang L, Flygare J, Lodish HF. From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood. 2011;118(24):6258-6268.
2. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene. 2002;21(21): 3368-3376. (Pubitemid 34587709)
3. Kerenyi MA, Orkin SH. Networking erythropoiesis. J Exp Med. 2010;207(12):2537-2541.
4. Bertone P, Stolc V, Royce TE, et al. Global identification of human transcribed sequences with genome tiling arrays. Science. 2004; 306(5705):2242-2246. (Pubitemid 40024458)
5. Carninci P, Kasukawa T, Katayama S, et al FANTOM Consortium; RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group). The transcriptional landscape of the mammalian genome. Science. 2005;309(5740): 1559-1563.
6. Birney E, Stamatoyannopoulos JA, Dutta A, et al ENCODE Project Consortium; NISC Comparative Sequencing Program; Baylor College of Medicine Human Genome Sequencing Center; Washington University Genome Sequencing Center; Broad Institute; Children's Hospital Oakland Research Institute. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007;447(7146): 799-816. (Pubitemid 46920138)
7. Ulitsky I, Bartel DP. lincRNAs: genomics, evolution, and mechanisms. Cell. 2013;154(1): 26-46.
8. Cabili MN, Trapnell C, Goff L, et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011;25(18):1915-1927.
9. Hu W, Alvarez-Dominguez JR, Lodish HF. Regulation of mammalian cell differentiation by long non-coding RNAs. EMBO Rep. 2012;13(11): 971-983.
10. Zhang J, Socolovsky M, Gross AW, Lodish HF. Role of Ras signaling in erythroid differentiation of mouse fetal liver cells: functional analysis by a flow cytometry-based novel culture system. Blood. 2003;102(12):3938-3946. (Pubitemid 37486974)
11. Hattangadi SM, Burke KA, Lodish HF. Homeodomain-interacting protein kinase 2 plays an important role in normal terminal erythroid differentiation. Blood. 2010;115(23):4853-4861.
12. Borodina T, Adjaye J, Sultan M. A strand-specific library preparation protocol for RNA sequencing. Methods Enzymol. 2011;500:79-98.
13. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105-1111.
14. Trapnell C, Williams BA, Pertea G, et al. Transcript assembly and quantification by RNASeq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-515.
15. Flygare J, Rayon Estrada V, Shin C, Gupta S, Lodish HF. HIF1alpha synergizes with glucocorticoids to promote BFU-E progenitor self-renewal. Blood. 2011;117(12):3435-3444.
16. Stamatoyannopoulos JA, Snyder M, Hardison R, et al Mouse ENCODE Consortium. An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol. 2012;13(8):418.
17. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106.
18. Flicek P, Amode MR, Barrell D, et al. Ensembl 2012. Nucleic Acids Res. 2012;40(Database issue):D84-D90.
19. Pruitt KD, Tatusova T, Brown GR, Maglott DR. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res. 2012;40(Database issue):D130-D135.
20. Dreszer TR, Karolchik D, Zweig AS, et al. The UCSC Genome Browser database: extensions and updates 2011. Nucleic Acids Res. 2012; 40(Database issue):D918-D923.
21. Shen Y, Yue F, McCleary DF, et al. A map of the cis-regulatory sequences in the mouse genome. Nature. 2012;488(7409):116-120.
22. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods. 2008;5(10):877-879.
23. Neuert G, Munsky B, Tan RZ, Teytelman L, Khammash M, van Oudenaarden A. Systematic identification of signal-activated stochastic gene regulation. Science. 2013;339(6119):584-587.
24. Ji P, Jayapal SR, Lodish HF. Enucleation of cultured mouse fetal erythroblasts requires Rac GTPases and mDia2. Nat Cell Biol. 2008;10(3): 314-321. (Pubitemid 351331018)
25. Heintzman ND, Hon GC, Hawkins RD, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature. 2009;459(7243):108-112.
26. Creyghton MP, Cheng AW, Welstead GG, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci USA. 2010;107(50): 21931-21936.
27. Guttman M, Amit I, Garber M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458(7235):223-227.
28. Guttman M, Garber M, Levin JZ, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol. 2010;28(5): 503-510.
29. Marques AC, Ponting CP. Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol. 2009;10(11):R124.
30. Derrien T, Johnson R, Bussotti G, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012;22(9): 1775-1789.
31. Pilon AM, Ajay SS, Kumar SA, et al NISC Comparative Sequencing Center. Genome-wide ChIP-Seq reveals a dramatic shift in the binding of the transcription factor erythroid Kruppel-like factor during erythrocyte differentiation. Blood. 2011;118(17):e139-e148.
32. Wu W, Cheng Y, Keller CA, et al. Dynamics of the epigenetic landscape during erythroid differentiation after GATA1 restoration. Genome Res. 2011;21(10):1659-1671.
33. Zhang Y, Liu T, Meyer CA, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9(9):R137.
34. Wontakal SN, Guo X, Smith C, et al. A core erythroid transcriptional network is repressed by a master regulator of myelo-lymphoid differentiation. Proc Natl Acad Sci USA. 2012; 109(10):3832-3837.
35. Yu M, Riva L, Xie HF, et al. Insights into GATA-1- mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell. 2009;36(4):682-695.
36. Welch JJ, Watts JA, Vakoc CR, et al. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood. 2004;104(10): 3136-3147. (Pubitemid 39507127)
37. Weiss MJ, Yu CN, Orkin SH. Erythroid-cellspecific properties of transcription factor GATA-1 revealed by phenotypic rescue of a gene-targeted cell line. Mol Cell Biol. 1997;17(3):1642-1651. (Pubitemid 27097393)
38. Hu W, Yuan B, Flygare J, Lodish HF. Long noncoding RNA-mediated anti-apoptotic activity in murine erythroid terminal differentiation. Genes Dev. 2011;25(24):2573-2578.
39. Tallack MR, Magor GW, Dartigues B, et al. Novel roles for KLF1 in erythropoiesis revealed by mRNA-seq. Genome Res. 2012;22(12): 2385-2398.
40. Khalil AM, Guttman M, Huarte M, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA. 2009;106(28):11667-11672.
41. Wang KC, Yang YW, Liu B, et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature. 2011;472(7341):120- 124.
42. Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs. Nature. 2012;482(7385):339-346.
43. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81: 145-166.
44. Mercer TR, Dinger ME, Mattick JS. Long noncoding RNAs: insights into functions. Nat Rev Genet. 2009;10(3):155-159.
45. Ponting C, Schultz J, Bork P. SPRY domains in ryanodine receptors (Ca(21)-release channels). Trends Biochem Sci. 1997;22(6):193-194. (Pubitemid 27246632)
46. Garding A, Bhattacharya N, Claus R, et al. Epigenetic upregulation of lncRNAs at 13q14.3 in leukemia is linked to the In Cis downregulation of a gene cluster that targets NF-kB. PLoS Genet. 2013;9(4):e1003373.
47. Debernardi S, Fontanella E, De Gregorio L, Pierotti MA, Delia D. Identification of a novel human kinesin-related gene (HK2) by the cDNA differential display technique. Genomics. 1997; 42(1):67-73. (Pubitemid 27215127)
48. Homma N, Takei Y, Tanaka Y, et al. Kinesin superfamily protein 2A (KIF2A) functions in suppression of collateral branch extension. Cell. 2003;114(2):229-239. (Pubitemid 36936916)
49. De Santa F, Barozzi I, Mietton F, et al. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol. 2010;8(5): e1000384.
50. Kim TK, Hemberg M, Gray JM, et al. Widespread transcription at neuronal activity-regulated enhancers. Nature. 2010;465(7295):182-187.
51. Kowalczyk MS, Hughes JR, Garrick D, et al. Intragenic enhancers act as alternative promoters. Mol Cell. 2012;45(4):447-458.
52. Bruce LJ, Robinson HC, Guizouarn H, et al. Monovalent cation leaks in human red cells caused by single amino-acid substitutions in the transport domain of the band 3 chloridebicarbonate exchanger, AE1. Nat Genet. 2005; 37(11):1258-1263. (Pubitemid 41568710)
53. Jarolim P, Palek J, Rubin HL, Prchal JT, Korsgren C, Cohen CM. Band 3 Tuscaloosa: Pro327 - Arg327 substitution in the cytoplasmic domain of erythrocyte band 3 protein associated with spherocytic hemolytic anemia and partial deficiency of protein 4.2. Blood. 1992;80(2): 523-529.
54. Fullwood MJ, Liu MH, Pan YF, et al. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature. 2009;462(7269): 58-64.
55. Guttman M, Donaghey J, Carey BW, et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature. 2011; 477(7364):295-300.
56. Döhner H, Stilgenbauer S, Benner A, et al. Genomic aberrations and survival in chronic lymphocytic leukemia. N Engl J Med. 2000; 343(26):1910-1916. (Pubitemid 32064784)
57. Liu Y, Corcoran M, Rasool O, et al. Cloning of two candidate tumor suppressor genes within a 10 kb region on chromosome 13q14, frequently deleted in chronic lymphocytic leukemia. Oncogene. 1997;15(20):2463-2473. (Pubitemid 27503532)
58. Klein U, Lia M, Crespo M, et al. The DLEU2/miR- 15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell. 2010;17(1):28-40.
59. Lerner M, Harada M, Lovén J, et al. 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. 2009;315(17):2941-2952.
60. Lia M, Carette A, Tang HY, et al. Functional dissection of the chromosome 13q14 tumorsuppressor locus using transgenic mouse lines. Blood. 2012;119(13):2981-2990.