The non-coding RNA landscape of human hematopoiesis and leukemia

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Schwarzer, Adrian ^a   Emmrich, Stephan ^a   Schmidt, Franziska ^a   Beck, Dominik ^b,c   Ng, Michelle ^a   Reimer, Christina ^a   Adams, Felix Ferdinand ^a   Grasedieck, Sarah ^d   Witte, Damian ^a   Käbler, Sebastian ^a   Wong, Jason W H ^b   Shah, Anushi ^b   Huang, Yizhou ^b   Jammal, Razan ^a   Maroz, Aliaksandra ^a   Jongen Lavrencic, Mojca ^e   Schambach, Axel ^a   Kuchenbauer, Florian ^d   Pimanda, John E ^b,c   Reinhardt, Dirk ^f   Heckl, Dirk ^a   Klusmann, Jan Henning ^a   more..

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^d UNIVERSITY HOSPITAL ULM   (Germany)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

UNTRANSLATED RNA; LONG NONCODING RNA LINC00173, HUMAN; LONG UNTRANSLATED RNA;

BLOOD; CELLS AND CELL COMPONENTS; GENE EXPRESSION; MAINTENANCE; RNA;

ACUTE MYELOID LEUKEMIA; ARTICLE; BLOOD CELL; CANCER PROGNOSIS; CELL POPULATION; GENE EXPRESSION; GRANULOCYTE; GRANULOPOIESIS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PREDICTIVE VALUE; CELL LINEAGE; GENE EXPRESSION PROFILING; HEK293 CELL LINE; LEUKEMIA; METABOLISM; PHYSIOLOGY;

CELL LINEAGE; GENE EXPRESSION PROFILING; HEK293 CELLS; HEMATOPOIESIS; HUMANS; LEUKEMIA; RNA, LONG NONCODING; RNA, UNTRANSLATED;

EID: 85027224264     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00212-4     Document Type: Article

References (69)

1. Mattick, J. S. & Rinn, J. L. Discovery and annotation of long noncoding RNAs. Nat. Struct. Mol. Biol. 22, 5-7 (2015).
2. Quinn, J. J. & Chang, H. Y. Unique features of long non-coding RNA biogenesis and function. Nat. Rev. Genet. 17, 47-62 (2016).
3. Washietl, S., Kellis, M. & Garber, M. Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res. 24, 616-628 (2014).
4. Cabili, M. N. et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 25, 1915-1927 (2011).
5. Petriv, O. I. et al. Comprehensive microRNA expression profiling of the hematopoietic hierarchy. Proc. Natl Acad. Sci. USA 107, 15443-15448 (2010).
6. Emmrich, S. et al. miR-139-5p controls translation in myeloid leukemia through EIF4G2. Oncogene 35, 1822-1831 (2016).
7. Qian, P. et al. The Dlk1-Gtl2 locus preserves LT-HSC Function by Inhibiting the PI3K-mTOR pathway to restrict mitochondrial metabolism. Cell Stem Cell 18, 214-228 (2016).
8. Luo, M. et al. Long non-coding RNAs control hematopoietic stem cell function. Cell Stem Cell 16, 426-438 (2015).
9. Emmrich, S. et al. LincRNAs MONC and MIR100HG act as oncogenes in acute megakaryoblastic leukemia. Mol. Cancer 13, 171 (2014).
10. Trimarchi, T. et al. Genome-wide mapping and characterization of notchregulated long noncoding RNAs in acute leukemia. Cell 158, 593-606 (2014).
11. Yildirim, E. et al. Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 152, 727-742 (2013).
12. Novershtern, N. et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 144, 296-309 (2011).
13. van der Maaten, L. & Hinton, G. Visualizing high-dimensional data using t-SNE. J. Mach. Learn. Res. 9, 2579-2605 (2008).
14. Wirth, H., Löffler, M., von Bergen, M. & Binder, H. Expression cartography of human tissues using self organizing maps. BMC Bioinformatics 12, 306 (2011).
15. Ritchie, M. E. et al. limma powers differential expression analyses for RNAsequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
16. Guttman, M. et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 457, 223-227 (2009).
17. Kim, S.-Y. & Volsky, D. J. PAGE-parametric analysis of gene set enrichment. BMC Bioinformatics 6, 144 (2005).
18. Subramanian, A. et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).
19. Zhang, X. et al. A myelopoiesis-associated regulatory intergenic noncoding RNA transcript within the human HOXA cluster. Blood 113, 2526-2534 (2009).
20. Zhang, X., Weissman, S. M. & Newburger, P. E. Long intergenic non-coding RNA HOTAIRM1 regulates cell cycle progression during myeloid maturation in NB4 human promyelocytic leukemia cells. RNA Biol. 11, 777-787 (2014).
21. Wouters, B. J. et al. Double CEBPA mutations, but not single CEBPA mutations, define a subgroup of acute myeloid leukemia with a distinctive gene expression profile that is uniquely associated with a favorable outcome. Blood 113, 3088-3091 (2009).
22. Kohlmann, A. et al. Gene expression profiling in AML with normal karyotype can predict mutations for molecular markers and allows novel insights into perturbed biological pathways. Leukemia 24, 1216-1220 (2010).
23. Sun, S. M. et al. Transition of highly specific microRNA expression patterns in association with discrete maturation stages of human granulopoiesis. Br. J. Haematol. 155, 395-398 (2011).
24. Martens, J. H. A. & Stunnenberg, H. G. BLUEPRINT: Mapping human blood cell epigenomes. Haematologica 98, 1487-1489 (2013).
25. Hon, C.-C. et al. An atlas of human long non-coding RNAs with accurate 5' ends. Nature 543, 199-204 (2017).
26. Davydov, E. V. et al. Identifying a high fraction of the human genome to be under selective constraint using GERP. PLoS. Comput. Biol. 6, e1001025 (2010).
27. Danis, E. et al. Ezh2 controls an early hematopoietic program and growth and survival signaling in early T cell precursor acute lymphoblastic leukemia. Cell Rep. 14, 1953-1965 (2016).
28. Kerenyi, M. A. et al. Histone demethylase Lsd1 represses hematopoietic stem and progenitor cell signatures during blood cell maturation. Elife 2, 1-23 (2013).
29. Gilbert, L. A. et al. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159, 647-661 (2014).
30. Marchese, F. P. & Huarte, M. Long non-coding RNAs and chromatin modifiers. Epigenetics 9, 21-26 (2014).
31. Collins, C. T. & Hess, J. L. Role of HOXA9 in leukemia: Dysregulation, cofactors and essential targets. Oncogene 35, 1090-1098 (2016).
32. Seitz, H. et al. A large imprinted microRNA gene cluster at the mouse Dlk1- Gtl2 domain. Genome Res. 14, 1741-1748 (2004).
33. da Rocha, S. T., Edwards, C. A., Ito, M., Ogata, T. & Ferguson-Smith, A. C. Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet. 24, 306-316 (2008).
34. Lee, E., Chuang, H.-Y., Kim, J.-W., Ideker, T. & Lee, D. Inferring pathway activity toward precise disease classification. PLoS Comput. Biol. 4, e1000217-e1000219 (2008).
35. Becher, B. et al. High-dimensional analysis of the murine myeloid cell system. Nat. Immunol. 15, 1181-1189 (2014).
36. Krivtsov, A. V. et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442, 818-822 (2006).
37. Diffner, E. et al. Activity of a heptad of transcription factors is associated with stem cell programs and clinical outcome in acute myeloid leukemia. Blood 121, 2289-2300 (2013).
38. The Cancer Genome Atlas Research Network. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368, 2059-2074 (2013).
39. Ng, S. W. K. et al. A 17-gene stemness score for rapid determination of risk in acute leukaemia. Nature 540, 433-437 (2016).
40. Huang, H. & Cantor, A. B. Common features of megakaryocytes and hematopoietic stem cells: What's the connection? J. Cell. Biochem. 107, 857-864 (2009).
41. Notta, F. et al. Distinct routes of lineage development reshape the human blood hierarchy across ontogeny. Science 351, aab2116 (2016).
42. Wittrup, A. & Lieberman, J. Knocking down disease: A progress report on siRNA therapeutics. Nat. Rev. Genet. 16, 543-552 (2015).
43. Klusmann, J.-H. et al. miR-125b-2 is a potential oncomiR on human chromosome 21 in megakaryoblastic leukemia. Genes Dev. 24, 478-490 (2010).
44. Klusmann, J.-H. et al. Developmental stage-specific interplay of GATA1 and IGF signaling in fetal megakaryopoiesis and leukemogenesis. Genes Dev. 24, 1659-1672 (2010).
45. Gentleman, R. C. et al. Bioconductor: Open software development for computational biology and bioinformatics. Genome. Biol. 5, R80 (2004).
46. Lee, J. K. et al. Comparing cDNA and oligonucleotide array data: Concordance of gene expression across platforms for the NCI-60 cancer cells. Genome. Biol. 4, R82 (2003).
47. Harrow, J. et al. GENCODE: The reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760-1774 (2012).
48. Volders, P. J. et al. An update on LNCipedia: A database for annotated human lncRNA sequences. Nucleic Acids Res. 43, D174-D180 (2015).
49. Zhao, Y. et al. NONCODE 2016: An informative and valuable data source of long non-coding RNAs. Nucleic Acids Res. 44, D203-D208 (2016).
50. Leek, J. T., Johnson, W. E., Parker, H. S., Jaffe, A. E. & Storey, J. D. The sva package for removing batch effects and other unwanted variation in highthroughput experiments. Bioinformatics 28, 882-883 (2012).
51. Harvey, R. C. et al. Identification of novel cluster groups in pediatric high-risk B-precursor acute lymphoblastic leukemia with gene expression profiling: Correlation with genome-wide DNA copy number alterations, clinical characteristics, and outcome. Blood 116, 4874-4884 (2010).
52. Merico, D., Isserlin, R., Stueker, O., Emili, A. & Bader, G. D. Enrichment map: A network-based method for gene-set enrichment visualization and interpretation. PLoS ONE 5, e13984 (2010).
53. Gautier, L., Cope, L., Bolstad, B. M. & Irizarry, R. A. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307-315 (2004).
54. Hänzelmann, S., Castelo, R. & Guinney, J. GSVA: Gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics 14, 7 (2013).
55. Zhang, H., Meltzer, P. & Davis, S. RCircos: An R package for Circos 2D track plots. BMC Bioinformatics 14, 244 (2013).
56. Dobin, A. et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
57. Anders, S., Pyl, P. T. & Huber, W. HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015).
58. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
59. Kim, D. et al. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome. Biol. 14, R36 (2013).
60. Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome. Biol. 11, R25 (2010).
61. Fellmann, C. et al. Functional identification of optimized RNAi triggers using a massively parallel sensor assay. Mol. Cell. 41, 733-746 (2011).
62. Fellmann, C. et al. An optimized microRNA backbone for effective single-copy RNAi. Cell Rep. 5, 1704-1713 (2013).
63. Stemmer, M., Thumberger, T., del Sol Keyer, M., Wittbrodt, J. & Mateo, J. L. CCTop: An intuitive, flexible and reliable CRISPR/Cas9 target prediction tool. PLoS ONE 10, e0124633 (2015).
64. Emmrich, S. et al. miR-99a/100~125b tricistrons regulate hematopoietic stem and progenitor cell homeostasis by shifting the balance between TGFbeta and Wnt signaling. Genes Dev. 28, 858-874 (2014).
65. Keene, J. D., Komisarow, J. M. & Friedersdorf, M. B. RIP-Chip: The isolation and identification of mRNAs, microRNAs and protein components of ribonucleoprotein complexes from cell extracts. Nat. Protoc. 1, 302-307 (2006).
66. Beck, D. et al. Genome-wide analysis of transcriptional regulators in human HSPCs reveals a densely interconnected network of coding and noncoding genes. Blood 122, e12-e22 (2013).
67. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595 (2010).
68. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
69. Ye, T. et al. seqMINER: An integrated ChIP-seq data interpretation platform. Nucleic Acids Res. 39, e35-e35 (2010).