Implication of Long noncoding RNAs in the endothelial cell response to hypoxia revealed by RNA-sequencing

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Voellenkle, C ^a   Garcia Manteiga, J M ^b   Pedrotti, S ^a   Perfetti, A ^a   De Toma, I ^a   Da Silva, D ^a   Maimone, B ^a   Greco, S ^a   Fasanaro, P ^a   Creo, P ^a   Zaccagnini, G ^a   Gaetano, C ^c   Martelli, F ^a  

^a IRCCS POLICLINICO SAN DONATO   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; H19 LONG NON-CODING RNA; LONG UNTRANSLATED RNA; TRANSCRIPTOME;

ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL HYPOXIA; CHEMISTRY; DISEASE MODEL; G1 PHASE CELL CYCLE CHECKPOINT; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNOHISTOCHEMISTRY; ISCHEMIA; MALE; METABOLISM; MOUSE; PATHOLOGY; RNA INTERFERENCE; SEQUENCE ANALYSIS; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CELL HYPOXIA; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DISEASE MODELS, ANIMAL; G1 PHASE CELL CYCLE CHECKPOINTS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; ISCHEMIA; MALE; MICE; MICE, INBRED C57BL; OLIGORIBONUCLEOTIDES, ANTISENSE; RNA INTERFERENCE; RNA, LONG NONCODING; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84963837811     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24141     Document Type: Article

References (59)

1. Cech, T. R. and Steitz, J. A. The Noncoding RNA Revolution-Trashing Old Rules to Forge New Ones. Cell 157, 77-94 (2014).
2. Mercer, T. R., Dinger, M. E. and Mattick, J. S. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10, 155-159 (2009).
3. Uchida, S. and Dimmeler, S. Long Noncoding RNAs in Cardiovascular Diseases. Circ. Res. 116, 737-750 (2015).
4. Kung, J. T. Y., Colognori, D. and Lee, J. T. Long noncoding RNAs: past, present, and future. Genetics 193, 651-669 (2013).
5. Greco, S., Gorospe, M. and Martelli, F. Noncoding RNA in age-related cardiovascular diseases. J. Mol. Cell. Cardiol. 83, 142-155 (2015).
6. Archer, K. et al. Long Non-Coding RNAs as Master Regulators in Cardiovascular Diseases. Int. J. Mol. Sci. 16, 23651-23667 (2015).
7. Wang, K. C. et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120-124 (2011).
8. Yang, F., Zhang, H., Mei, Y. and Wu, M. Reciprocal Regulation of HIF-1α and LincRNA-p21 Modulates the Warburg Effect. Mol. Cell 53, 88-100 (2014).
9. Semenza, G. L. Oxygen Sensing, Homeostasis, and Disease. N. Engl. J. Med. 365, 537-547 (2015).
10. Fish, J. E. et al. Hypoxia-inducible expression of a natural cis-antisense transcript inhibits endothelial nitric-oxide synthase. J. Biol. Chem. 282, 15652-15666 (2007).
11. Michalik, K. M. et al. Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ. Res. 114, 1389-1397 (2014).
12. Fiedler, J. et al. Development of Long Noncoding RNA-Based Strategies to Modulate Tissue Vascularization. J. Am. Coll. Cardiol. 66, 2005-2015 (2015).
13. Bell, R. D. et al. Identification and initial functional characterization of a human vascular cell-enriched long noncoding RNA. Arterioscler. Thromb. Vasc. Biol. 34, 1249-1259 (2014).
14. Miano, J. M. and Long, X. The short and long of noncoding sequences in the control of vascular cell phenotypes. Cell. Mol. Life Sci. 72, 3457-3488 (2015).
15. Attwooll, C., Lazzerini Denchi, E. and Helin, K. The E2F family: specific functions and overlapping interests. EMBO J. 23, 4709-16 (2004).
16. Laoukili, J. et al. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat. Cell Biol. 7, 126-136 (2005).
17. Greco, S., Gaetano, C. and Martelli, F. HypoxamiR Regulation and Function in Ischemic Cardiovascular Diseases. Antioxid. Redox Signal. 21, 1202-1219 (2014).
18. Zaccagnini, G. et al. Magnetic Resonance Imaging Allows the Evaluation of Tissue Damage and Regeneration in a Mouse Model of Critical Limb Ischemia. PLoS One 10, e0142111 (2015).
19. Lo, K. A. et al. Analysis of in vitro insulin-resistance models and their physiological relevance to in vivo diet-induced adipose insulin resistance. Cell Rep. 5, 259-270 (2013).
20. Schodel, J. et al. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 117, e207-17 (2011).
21. Kim, D. K., Zhang, L., Dzau, V. J. and Pratt, R. E. H19, a developmentally regulated gene, is reexpressed in rat vascular smooth muscle cells after injury. J. Clin. Invest. 93, 355-360 (1994).
22. Jiang, X. et al. Increased level of H19 long noncoding RNA promotes invasion, angiogenesis, and stemness of glioblastoma cells. J. Neurosurg. 124, 129-36 (2015).
23. Wang, J., Duncan, D., Shi, Z. and Zhang, B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res. 41, W77-83 (2013).
24. Khoo, C. P., Micklem, K. and Watt, S. M. A Comparison of Methods for Quantifying Angiogenesis in the Matrigel Assay In Vitro. Tissue Eng. Part C Methods 17, 895-906 (2011).
25. Huang, Z. et al. Identification of Differentially Expressed Long Non-coding RNAs in Polarized Macrophages. Sci. Rep. 6, 19705 (2016).
26. Yang, L., Duff, M. O., Graveley, B. R., Carmichael, G. G. and Chen, L.-L. Genomewide characterization of non-polyadenylated RNAs. Genome Biol. 12, R16 (2011).
27. Wilusz, J. E. Long noncoding RNAs: Re-writing dogmas of RNA processing and stability. Biochim. Biophys. Acta - Gene Regul. Mech. 1859, 128-138 (2016).
28. Iyer, M. K. et al. The landscape of long noncoding RNAs in the human transcriptome. Nat. Genet. 47, 199-208 (2015).
29. Semenza, G. L. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr. Opin. Genet. Dev. 8, 588-594 (1998).
30. Gilkes, D. M., Bajpai, S., Chaturvedi, P., Wirtz, D. and Semenza, G. L. Hypoxia-inducible f0actor 1 (HIF-1) promotes extracellular matrix remodeling under hypoxic conditions by inducing P4HA1, P4HA2, and PLOD2 expression in fibroblasts. J. Biol. Chem. 288, 10819-10829 (2013).
31. Ebert, B. L. and Bunn, H. F. Regulation of transcription by hypoxia requires a multiprotein complex that includes hypoxia-inducible factor 1, an adjacent transcription factor, and p300/CREB binding protein. Mol. Cell. Biol. 18, 4089-4096 (1998).
32. Yamashita, K., Discher, D. J., Hu, J., Bishopric, N. H. and Webster, K. a. Molecular regulation of the endothelin-1 gene by hypoxia. Contributions of hypoxia-inducible factor-1, activator protein-1, GATA-2, and p300/CBP. J. Biol. Chem. 276, 12645-12653 (2001).
33. Lin, J. J. et al. The Long Noncoding RNA Landscape in Hypoxic and Inflammatory Renal Epithelial Injury. Am. J. Physiol. - Ren. Physiol. 309, F901-13 (2015).
34. McCarty, G. and Loeb, D. M. Hypoxia-sensitive epigenetic regulation of an antisense-oriented lncRNA controls WT1 expression in myeloid leukemia cells. PLoS One 10, e0119837 (2015).
35. Clark, B. S. and Blackshaw, S. Long non-coding RNA-dependent transcriptional regulation in neuronal development and disease. Front. Genet. 5, 1-19 (2014).
36. Clark, M. B. et al. Genome-wide analysis of long noncoding RNA stability. Genome Res. 22, 885-898 (2012).
37. Cicchillitti, L. et al. Hypoxia-inducible factor 1-α induces miR-210 in normoxic differentiating myoblasts. J. Biol. Chem. 287, 44761-44771 (2012).
38. Choudhry, H. et al. Extensive regulation of the non-coding transcriptome by hypoxia: Role of HIF in releasing paused RNApol2. EMBO Rep. 15, 70-76 (2014).
39. Huang, X. et al. Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol. Cell 35, 856-867 (2009).
40. Kulshreshtha, R. et al. A MicroRNA Signature of Hypoxia. Mol. Cell. Biol. 27, 1859-1867 (2007).
41. Matouk, I. J. et al. Oncofetal H19 RNA promotes tumor metastasis. Biochim. Biophys. Acta 1843, 1414-1426 (2014).
42. Luo, M. et al. Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression. Cancer Lett. 333, 213-221 (2013).
43. Conigliaro, A. et al. CD90+ liver cancer cells modulate endothelial cell phenotype through the release of exosomes containing H19 lncRNA. Mol. Cancer 14, 155 (2015).
44. Raveh, E., Matouk, I. J., Gilon, M. and Hochberg, A. The H19 Long non-coding RNA in cancer initiation, progression and metastasis - a proposed unifying theory. Mol. Cancer 14, 184 (2015).
45. Fasanaro, P., Capogrossi, M. C. and Martelli, F. Regulation of the endothelial cell cycle by the ubiquitin-proteasome system. Cardiovasc. Res. 85, 272-280 (2010).
46. Li, C. et al. H19 derived microRNA-675 regulates cell proliferation and migration through CDK6 in glioma. Am. J. Transl. Res. 7, 1747-1764 (2015).
47. Voellenkle, C. et al. Deep-sequencing of endothelial cells exposed to hypoxia reveals the complexity of known and novel microRNAs. RNA 18, 472-484 (2012).
48. Kallen, A. N. et al. The Imprinted H19 LncRNA Antagonizes Let-7 MicroRNAs. Mol. Cell 52, 101-112 (2013).
49. Chen, Z. et al. Hypoxia-responsive miRNAs target argonaute 1 to promote angiogenesis. J. Clin. Invest. 123, 1057-1067 (2013).
50. Giovarelli, M. et al. H19 long noncoding RNA controls the mRNA decay promoting function of KSRP. Proc. Natl. Acad. Sci. 111, E5023-8 (2014).
51. Ruggiero, T. et al. Identification of a set of KSRP target transcripts upregulated by PI3K-AKT signaling. BMC Mol. Biol. 8, 28 (2007).
52. Magenta, a. et al. miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ. 18, 1628-1639 (2011).
53. Huang, S. et al. SOAPsplice: Genome-Wide ab initio Detection of Splice Junctions from RNA-Seq Data. Front. Genet. 2, 46 (2011).
54. Anders, S., Pyl, P. T. and Huber, W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2015).
55. Love, M. I., Huber, W. and Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
56. Chen, E. Y. et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128 (2013).
57. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
58. Roberts, A., Pimentel, H., Trapnell, C. and Pachter, L. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 27, 2325-2329 (2011).
59. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).