The Malat1 long non-coding RNA is upregulated by signalling through the PERK axis of unfolded protein response during flavivirus infection

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bhattacharyya, Sankar ^a   Vrati, Sudhanshu ^a  

^a TRANSLATIONAL HEALTH SCIENCE AND TECHNOLOGY INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ATF6 PROTEIN, HUMAN; EIF2AK3 PROTEIN, HUMAN; ERN1 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; LONG UNTRANSLATED RNA; MALAT1 LONG NON-CODING RNA, HUMAN; MOLECULAR CHAPERONE GRP78; PROTEIN KINASE R; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE;

ANTAGONISTS AND INHIBITORS; APOPTOSIS; BIOSYNTHESIS; DRUG EFFECTS; ENDOPLASMIC RETICULUM; FLAVIVIRUS; FLAVIVIRUS INFECTION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; PATHOGENICITY; PATHOLOGY; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

ACTIVATING TRANSCRIPTION FACTOR 6; APOPTOSIS; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; FLAVIVIRUS; FLAVIVIRUS INFECTIONS; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN-SERINE-THREONINE KINASES; RNA, LONG NONCODING; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84949267292     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17794     Document Type: Article

References (53)

1. Lindenbach, Brett D., Charles, H.-J. u. T. and Rice, M. Flaviviridae: The Viruses and Their Replication (ed. D. M. Knipe and P. M. Howley) (Lippincott-Raven, Philadelphia, 2007).
2. Medigeshi, G. R. et al. West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J Virol 81, 10849-10860 (2007).
3. Su, H. L., Liao, C. L. and Lin, Y. L. Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response. J Virol 76, 4162-4171 (2002).
4. Yu, C. Y., Hsu, Y. W., Liao, C. L. and Lin, Y. L. Flavivirus infection activates the XBP1 pathway of the unfolded protein response to cope with endoplasmic reticulum stress. J Virol 80, 11868-11880 (2006).
5. Chan, S. W. The unfolded protein response in virus infections. Front Microbiol 5, 518 (2014).
6. Schroder, M. and Kaufman, R. J. ER stress and the unfolded protein response. Mutat Res 569, 29-63 (2005).
7. Hollien, J. and Weissman, J. S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107 (2006).
8. Cullinan, S. B. et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23, 7198-7209 (2003).
9. Harding, H. P., Zhang, Y. and Ron, D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274 (1999).
10. Harding, H. P. et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11, 619-633 (2003).
11. Fawcett, T. W., Martindale, J. L., Guyton, K. Z., Hai, T. and Holbrook, N. J. Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem J 339 (Pt 1), 135-141 (1999).
12. Yoshida, H. et al. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol Cell Biol 20, 6755-6767 (2000).
13. Mercer, T. R., Dinger, M. E. and Mattick, J. S. Long non-coding RNAs: insights into functions. Nat Rev Genet 10, 155-159 (2009).
14. West, J. A. et al. The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. Mol Cell 55, 791-802 (2014).
15. Tripathi, V. et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39, 925-938 (2010).
16. Xia, T. et al. Long noncoding RNA associated-competing endogenous RNAs in gastric cancer. Sci Rep 4, 6088 (2014).
17. Pickard, M. R., Mourtada-Maarabouni, M. and Williams, G. T. Long non-coding RNA GAS5 regulates apoptosis in prostate cancer cell lines. Biochim Biophys Acta 1832, 1613-1623 (2013).
18. Atmadibrata, B. et al. The novel long noncoding RNA linc00467 promotes cell survival but is down-regulated by N-Myc. PLoS One 9, e88112 (2014).
19. Ji, P. et al. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 22, 8031-8041 (2003).
20. Hirata, H. et al. Long Noncoding RNA MALAT1 Promotes Aggressive Renal Cell Carcinoma through Ezh2 and Interacts with miR-205. Cancer Res 75, 1322-1331 (2015).
21. Tripathi, V. et al. Long noncoding RNA MALAT1 controls cell cycle progression by regulating the expression of oncogenic transcription factor B-MYB. PLoS Genet 9, e1003368 (2013).
22. Zhang, B. et al. The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep 2, 111-123 (2012).
23. Vrati, S., Agarwal, V., Malik, P., Wani, S. A. and Saini, M. Molecular characterization of an Indian isolate of Japanese encephalitis virus that shows an extended lag phase during growth. J Gen Virol 80 (Pt 7), 1665-1671 (1999).
24. Axten, J. M. et al. Discovery of 7-methyl-5-(1-{[3-(trifluoromethyl)phenyl]acetyl}-2,3-dihydro-1H-indol-5-yl)-7H-p yrrolo[2,3-d] pyrimidin-4-amine (GSK2606414), a potent and selective first-in-class inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK). J Med Chem 55, 7193-7207 (2012).
25. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891 (2001).
26. Papandreou, I. et al. Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma. Blood 117, 1311-1314 (2011).
27. Bhattacharyya, S., Sen, U. and Vrati, S. Regulated IRE1-dependent decay pathway is activated during Japanese encephalitis virusinduced unfolded protein response and benefits viral replication. J Gen Virol 95, 71-79 (2014).
28. Ma, Y. and Hendershot, L. M. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem 278, 34864-34873 (2003).
29. Stockwell, S. R. et al. Mechanism-based screen for G1/S checkpoint activators identifies a selective activator of EIF2AK3/PERK signalling. PLoS One 7, e28568 (2012).
30. Chitnis, N., Pytel, D. and Diehl, J. A. UPR-inducible miRNAs contribute to stressful situations. Trends Biochem Sci 38, 447-452 (2013).
31. Leucci, E. et al. microRNA-9 targets the long non-coding RNA MALAT1 for degradation in the nucleus. Sci Rep 3, 2535 (2013).
32. Wang, X. et al. Silencing of long noncoding RNA MALAT1 by miR-101 and miR-217 inhibits proliferation, migration, and invasion of esophageal squamous cell carcinoma cells. J Biol Chem 290, 3925-3935 (2015).
33. Lee, A. H., Iwakoshi, N. N. and Glimcher, L. H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23, 7448-7459 (2003).
34. Averous, J. et al. Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J Biol Chem 279, 5288-5297 (2004).
35. Hollien, J. et al. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186, 323-331 (2009).
36. Domingo, E., Sheldon, J. and Perales, C. Viral quasispecies evolution. Microbiol Mol Biol Rev 76, 159-216 (2012).
37. Hu, L. et al. Up-regulation of long noncoding RNA MALAT1 contributes to proliferation and metastasis in esophageal squamous cell carcinoma. J Exp Clin Cancer Res 34, 7 (2015).
38. Michalik, K. M. et al. Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ Res 114, 1389-1397 (2014).
39. Bi, M. et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. Embo J 24, 3470-3481 (2005).
40. Fan, Y. et al. TGF-beta-induced upregulation of malat1 promotes bladder cancer metastasis by associating with suz12. Clin Cancer Res 20, 1531-1541 (2014).
41. Li, S. et al. Sp1-mediated transcriptional regulation of MALAT1 plays a critical role in tumor. J Cancer Res Clin Oncol (2015).
42. Gutschner, T. et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res 73, 1180-1189 (2013).
43. Miyagawa, R. et al. Identification of cis- and trans-acting factors involved in the localization of MALAT-1 noncoding RNA to nuclear speckles. Rna 18, 738-751 (2012).
44. Nakagawa, S. et al. Malat1 is not an essential component of nuclear speckles in mice. Rna 18, 1487-1499 (2012).
45. Engreitz, J. M. et al. RNA-RNA interactions enable specific targeting of noncoding RNAs to nascent Pre-mRNAs and chromatin sites. Cell 159, 188-199 (2014).
46. Dong, Y. et al. MALAT1 promotes the proliferation and metastasis of osteosarcoma cells by activating the PI3K/Akt pathway. Tumour Biol 36, 1477-1486 (2015).
47. Wu, X. S. et al. MALAT1 promotes the proliferation and metastasis of gallbladder cancer cells by activating the ERK/MAPK pathway. Cancer Biol Ther 15, 806-814 (2014).
48. Puthanveetil, P., Chen, S., Feng, B., Gautam, A. and Chakrabarti, S. Long non-coding RNA MALAT1 regulates hyperglycaemia induced inflammatory process in the endothelial cells. J Cell Mol Med 19, 1418-1425 (2015).
49. Han, X., Yang, F., Cao, H. and Liang, Z. Malat1 regulates serum response factor through miR-133 as a competing endogenous RNA in myogenesis. Faseb J (2015).
50. Liu, Y. P. et al. Endoplasmic reticulum stress regulates the innate immunity critical transcription factor IRF3. J Immunol 189, 4630-4639 (2012).
51. Saha, S., Murthy, S. and Rangarajan, P. N. Identification and characterization of a virus-inducible non-coding RNA in mouse brain. J Gen Virol 87, 1991-1995 (2006).
52. Jiang, Y. et al. The role of MALAT1 correlates with HPV in cervical cancer. Oncol Lett 7, 2135-2141 (2014).
53. Zhang, Q., Chen, C. Y., Yedavalli, V. S. and Jeang, K. T. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 4, e00596-00512 (2013).