TRNA-Derived Small Non-Coding RNAs in Response to Ischemia Inhibit Angiogenesis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Li, Qing ^a   Hu, Bin ^a   Hu, Guo Wen ^a,b   Chen, Chun Yuan ^a,b   Niu, Xin ^a   Liu, Juan ^a   Zhou, Shu Min ^a   Zhang, Chang Qing ^a   Wang, Yang ^a   Deng, Zhi Feng ^a  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^b NANCHANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIN; GLYCINE TRANSFER RNA; PANCREATIC RIBONUCLEASE; SMALL UNTRANSLATED RNA; VALINE TRANSFER RNA;

ANGIOGENESIS; ANIMAL; BIOLOGY; BRAIN; BRAIN ISCHEMIA; CELL HYPOXIA; CELL MOTION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; HINDLIMB; HUMAN; MALE; METABOLISM; MOUSE; PATHOLOGY; PROTEIN DEGRADATION; RAT; RNA CLEAVAGE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ANIMALS; BRAIN; BRAIN ISCHEMIA; CELL HYPOXIA; CELL MOVEMENT; CELL PROLIFERATION; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION; HINDLIMB; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEOLYSIS; RATS; RATS, SPRAGUE-DAWLEY; RIBONUCLEASE, PANCREATIC; RNA CLEAVAGE; RNA, SMALL UNTRANSLATED; RNA, TRANSFER, GLY; RNA, TRANSFER, VAL; SIGNAL TRANSDUCTION;

EID: 84958559519     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20850     Document Type: Article

References (45)

1. Lou, Y. L. et al. miR-210 activates notch signaling pathway in angiogenesis induced by cerebral ischemia. Mol Cell Biochem 370, 45-51 (2012).
2. Liu, H. M. Neovasculature and blood-brain barrier in ischemic brain infarct. Acta Neuropathol 75, 422-426 (1988).
3. Kovacs, Z., Ikezaki, K., Samoto, K., Inamura, T. & Fukui, M. VEGF and flt. Expression time kinetics in rat brain infarct. Stroke 27, 1865-1872; discussion 1872-1863 (1996).
4. Arai, K., Jin, G., Navaratna, D. & Lo, E. H. Brain angiogenesis in developmental and pathological processes: neurovascular injury and angiogenic recovery after stroke. FEBS J 276, 4644-4652 (2009).
5. Ohab, J. J., Fleming, S., Blesch, A. & Carmichael, S. T. A neurovascular niche for neurogenesis after stroke. J Neurosci 26, 13007-13016 (2006).
6. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
7. Yin, K. J., Hamblin, M. & Chen, Y. E. Non-coding RNAs in cerebral endothelial pathophysiology: Emerging roles in stroke. Neurochem Int 77, 9-16 (2014).
8. Kane, N. M., Thrasher, A. J., Angelini, G. D. & Emanueli, C. Concise Review: MicroRNAs as Modulators of Stem Cells and Angiogenesis. Stem Cells 32, 1059-1066 (2014).
9. Di Bernardini, E. et al. Endothelial lineage differentiation from induced pluripotent stem cells is regulated by microRNA-21 and transforming growth factor beta2 (TGF-beta2) pathways. J Biol Chem 289, 3383-3393 (2014).
10. Ye, P., Liu, J., He, F., Xu, W. & Yao, K. Hypoxia-induced deregulation of miR-126 and its regulative effect on VEGF and MMP-9 expression. Int J Med Sci 11, 17-23 (2014).
11. Bao, M. H. et al. Let-7 in cardiovascular diseases, heart development and cardiovascular differentiation from stem cells. Int J Mol Sci 14, 23086-23102 (2013).
12. Kaluza, D. et al. Histone deacetylase 9 promotes angiogenesis by targeting the antiangiogenic microRNA-17-92 cluster in endothelial cells. Arterioscler Thromb Vasc Biol 33, 533-543 (2013).
13. Yan, H. et al. piRNA-823 contributes to tumorigenesis by regulating de novo DNA methylation and angiogenesis in multiple myeloma. Leukemia 29, 196-206 (2014).
14. Phizicky, E. M. & Hopper, A. K. tRNA biology charges to the front. Genes Dev 24, 1832-1860 (2010).
15. Parisien, M., Wang, X. & Pan, T. Diversity of human tRNA genes from the 1000-genomes project. RNA Biol 10, 1853-1867 (2013).
16. Begley, U. et al. Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 28, 860-870 (2007).
17. Francklyn, C. S. & Minajigi, A. tRNA as an active chemical scaffold for diverse chemical transformations. FEBS Lett 584, 366-375 (2010).
18. Green, N. J., Grundy, F. J. & Henkin, T. M. The T box mechanism: tRNA as a regulatory molecule. FEBS Lett 584, 318-324 (2010).
19. Mei, Y. et al. tRNA binds to cytochrome c and inhibits caspase activation. Mol Cell 37, 668-678 (2010).
20. Lee, Y. S., Shibata, Y., Malhotra, A. & Dutta, A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 23, 2639-2649 (2009).
21. Kumar, P., Anaya, J., Mudunuri, S. B. & Dutta, A. Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets. BMC Biol 12, 78 (2014).
22. Fu, H. et al. Identification of human fetal liver miRNAs by a novel method. FEBS Lett 579, 3849-3854 (2005).
23. Yamasaki, S., Ivanov, P., Hu, G. F. & Anderson, P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 185, 35-42 (2009).
24. Ivanov, P., Emara, M. M., Villen, J., Gygi, S. P. & Anderson, P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell 43, 613-623 (2011).
25. Gebetsberger, J. & Polacek, N. Slicing tRNAs to boost functional ncRNA diversity. RNA Biol 10, 1798-1806 (2013).
26. Fu, H. et al. Stress induces tRNA cleavage by angiogenin in mammalian cells. FEBS Lett 583, 437-442 (2009).
27. Li, S. & Hu, G. F. Emerging role of angiogenin in stress response and cell survival under adverse conditions. J Cell Physiol 227, 2822-2826 (2012).
28. Huang, L., Huang, Y. & Guo, H. Dominant expression of angiogenin in NeuN positive cells in the focal ischemic rat brain. J Neurol Sci 285, 220-223 (2009).
29. Nakamura, M. et al. Hypoxic conditions stimulate the production of angiogenin and vascular endothelial growth factor by human renal proximal tubular epithelial cells in culture. Nephrol Dial Transplant 21, 1489-1495 (2006).
30. Anderson, P. & Ivanov, P. tRNA fragments in human health and disease. FEBS Lett 588, 4297-4304 (2014).
31. Vemuganti, R. All's well that transcribes well: non-coding RNAs and post-stroke brain damage. Neurochem Int 63, 438-449 (2013).
32. Dharap, A., Bowen, K., Place, R., Li, L. C. & Vemuganti, R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 29, 675-687 (2009).
33. Dharap, A., Nakka, V. P. & Vemuganti, R. Altered expression of PIWI RNA in the rat brain after transient focal ischemia. Stroke 42, 1105-1109 (2011).
34. Sobala, A. & Hutvagner, G. Transfer RNA-derived fragments: origins, processing, and functions. Wiley Interdiscip Rev RNA 2, 853-862 (2011).
35. Yeung, M. L. et al. Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: evidence for the processing of a viral-cellular double-stranded RNA hybrid. Nucleic Acids Res 37, 6575-6586 (2009).
36. Haussecker, D. et al. Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 16, 673-695 (2010).
37. Kawaji, H. et al. Hidden layers of human small RNAs. BMC Genomics 9, 157 (2008).
38. Couvillion, M. T., Sachidanandam, R. & Collins, K. A growth-essential Tetrahymena Piwi protein carries tRNA fragment cargo. Genes Dev 24, 2742-2747 (2010).
39. Gong, B. et al. Compartmentalized, functional role of angiogenin during spotted fever group rickettsia-induced endothelial barrier dysfunction: evidence of possible mediation by host tRNA-derived small noncoding RNAs. BMC Infect Dis 13, 285 (2013).
40. Selitsky, S. R. et al. Small tRNA-derived RNAs are increased and more abundant than microRNAs in chronic hepatitis B and C. Sci Rep 5, 7675 (2015).
41. Martens-Uzunova, E. S., Olvedy, M. & Jenster, G. Beyond microRNA-novel RNAs derived from small non-coding RNA and their implication in cancer. Cancer Lett 340, 201-211 (2013).
42. Emara, M. M. et al. Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J Biol Chem 285, 10959-10968 (2010).
43. Saikia, M. et al. Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Mol Cell Biol 34, 2450-2463 (2014).
44. Yuan, T. et al. Human induced pluripotent stem cell-derived neural stem cells survive, migrate, differentiate, and improve neurologic function in a rat model of middle cerebral artery occlusion. Stem Cell Res Ther 4, 73 (2013).
45. Longa, E. Z., Weinstein, P. R., Carlson, S. & Cummins, R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20, 84-91 (1989).