Long Noncoding RNA NEAT1-Dependent SFPQ Relocation from Promoter Region to Paraspeckle Mediates IL8 Expression upon Immune Stimuli

Molecular Cell

Volumn 53, Issue 3, 2014, Pages 393-406

  Imamura, Katsutoshi ^a   Imamachi, Naoto ^a   Akizuki, Gen ^a   Kumakura, Michiko ^b   Kawaguchi, Atsushi ^b   Nagata, Kyosuke ^b   Kato, Akihisa ^a   Kawaguchi, Yasushi ^a   Sato, Hiroki ^a   Yoneda, Misako ^a   Kai, Chieko ^a   Yada, Tetsushi ^c   Suzuki, Yutaka ^a   Yamada, Toshimichi ^a   Ozawa, Takeaki ^a   Kaneki, Kiyomi ^d   Inoue, Tsuyoshi ^d   Kobayashi, Mika ^d   Kodama, Tatsuhiko ^d   Wada, Youichiro ^a,d   Sekimizu, Kazuhisa ^a   Akimitsu, Nobuyoshi ^a   more..

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c KYUSHU INSTITUTE OF TECHNOLOGY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 8; LONG UNTRANSLATED RNA; NUCLEAR ENRICHED ABUNDANT TRANSCRIPT 1; POLYINOSINIC POLYCYTIDYLIC ACID; RNA BINDING PROTEIN; SPLICING FACTOR PROLINE GLUTAMINE RICH PROTEIN; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; BETA ACTIN; BINDING PROTEIN; NUCLEAR PROTEIN; SPLICING FACTOR PROLINE GLUTAMINE RICH;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE INDUCTION; HELA CELL; HERPES SIMPLEX; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INFLUENZA; INNATE IMMUNITY; INTERLEUKIN 8 GENE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN RELOCATION; REPRESSOR GENE; TRANSCRIPTION INITIATION; BIOINFORMATICS; CELL NUCLEUS INCLUSION BODY; CHROMATIN IMMUNOPRECIPITATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION; HELA CELL LINE; HERPES SIMPLEX VIRUS; HERPES SIMPLEX VIRUS 1; IMMUNE RESPONSE; IMMUNOPRECIPITATION; JAPANESE ENCEPHALITIS; MICROARRAY ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROCESSING; REPORTER GENE;

GENE EXPRESSION REGULATION; HELA CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-8; MEASLES VIRUS; ORTHOMYXOVIRIDAE; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; RNA, LONG NONCODING; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC;

ORTHOMYXOVIRIDAE; SIMPLEXVIRUS;

EID: 84893452948     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.01.009     Document Type: Article

References (53)

1. Arpaia N., Barton G.M. Toll-like receptors: key players in antiviral immunity. Curr Opin Virol 2011, 1:447-454.
2. Berghäll H., Sirén J., Sarkar D., Julkunen I., Fisher P.B., Vainionpää R., Matikainen S. The interferon-inducible RNA helicase, mda-5, isinvolved in measles virus-induced expression of antiviral cytokines. Microbes Infect. 2006, 8:2138-2144.
3. Bernard D., Prasanth K.V., Tripathi V., Colasse S., Nakamura T., Xuan Z., Zhang M.Q., Sedel F., Jourdren L., Coulpier F., et al. A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J. 2010, 29:3082-3093.
4. Carninci P., Kasukawa T., Katayama S., Gough J., Frith M.C., Maeda N., Oyama R., Ravasi T., Lenhard B., Wells C., et al. The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-1563. FANTOM Consortium, RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group)RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group).
5. Chen L.L., Carmichael G.G. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol. Cell 2009, 35:467-478.
6. Chen L.L., Carmichael G.G. Decoding the function of nuclear long non-coding RNAs. Curr. Opin. Cell Biol. 2010, 22:357-364.
7. Clemson C.M., Hutchinson J.N., Sara S.A., Ensminger A.W., Fox A.H., Chess A., Lawrence J.B. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell 2009, 33:717-726.
8. Davidovich C., Zheng L., Goodrich K.J., Cech T.R. Promiscuous RNA binding by Polycomb repressive complex 2. Nat. Struct. Mol. Biol. 2013, 20:1250-1257.
9. Fox A.H., Lamond A.I. Paraspeckles. Cold Spring Harb. Perspect. Biol. 2010, 2:a000687.
10. Guillot L., Le Goffic R., Bloch S., Escriou N., Akira S., Chignard M., Si-Tahar M. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J.Biol. Chem. 2005, 280:5571-5580.
11. Gupta R.A., Shah N., Wang K.C., Kim J., Horlings H.M., Wong D.J., Tsai M.C., Hung T., Argani P., Rinn J.L., et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464:1071-1076.
12. Guttman M., Amit I., Garber M., French C., Lin M.F., Feldser D., Huarte M., Zuk O., Carey B.W., Cassady J.P., et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458:223-227.
13. Hirose T., Virnicchi G., Tanigawa A., Naganuma T., Li R., Kimura H., Yokoi T., Nakagawa S., Bénard M., Fox A.H., Pierron G. NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol. Biol. Cell 2014, 25:169-183.
14. Hoffmann E., Dittrich-Breiholz O., Holtmann H., Kracht M. Multiple control of interleukin-8 gene expression. J.Leukoc. Biol. 2002, 72:847-855.
15. Huarte M., Rinn J.L. Large non-coding RNAs: missing links in cancer?. Hum. Mol. Genet. 2010, 19(R2):R152-R161.
16. Hutchinson J.N., Ensminger A.W., Clemson C.M., Lynch C.R., Lawrence J.B., Chess A. A screen for nuclear transcripts identifies twolinkednoncoding RNAs associated with SC35 splicing domains. BMC Genomics 2007, 8:39.
17. Iacobazzi V., Infantino V., Costanzo P., Izzo P., Palmieri F. Functional analysis of the promoter of the mitochondrial phosphate carrier human gene: identification of activator and repressor elements and their transcription factors. Biochem. J. 2005, 391:613-621.
18. Kapranov P., Willingham A.T., Gingeras T.R. Genome-wide transcription and the implications for genomic organization. Nat. Rev. Genet. 2007, 8:413-423.
19. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
20. Kino T., Hurt D.E., Ichijo T., Nader N., Chrousos G.P. Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci. Signal. 2010, 3:ra8.
21. Koide M., Kinugawa S., Takahashi N., Udagawa N. Osteoclastic bone resorption induced by innate immune responses. Periodontol. 2000 2010, 54:235-246.
22. Lafaille F.G., Pessach I.M., Zhang S.Y., Ciancanelli M.J., Herman M., Abhyankar A., Ying S.W., Keros S., Goldstein P.A., Mostoslavsky G., et al. Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 2012, 491:769-773.
23. Mao Y.S., Zhang B., Spector D.L. Biogenesis and function of nuclear bodies. Trends Genet. 2011, 27:295-306.
24. Mercer T.R., Dinger M.E., Mattick J.S. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 2009, 10:155-159.
25. Miyagawa R., Tano K., Mizuno R., Nakamura Y., Ijiri K., Rakwal R., Shibato J., Masuo Y., Mayeda A., Hirose T., Akimitsu N. Identification of cis- and trans-acting factors involved in the localization of MALAT-1 noncoding RNA to nuclear speckles. RNA 2012, 18:738-751.
26. Mizutani R., Wakamatsu A., Tanaka N., Yoshida H., Tochigi N., Suzuki Y., Oonishi T., Tani H., Tano K., Ijiri K., et al. Identification and characterization of novel genotoxic stress-inducible nuclear long noncoding RNAs in mammalian cells. PLoS ONE 2012, 7:e34949.
27. Naganuma T., Hirose T. Paraspeckle formation during the biogenesis of long non-coding RNAs. RNA Biol. 2013, 10:456-461.
28. Naganuma T., Nakagawa S., Tanigawa A., Sasaki Y.F., Goshima N., Hirose T. Alternative 3'-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J. 2012, 31:4020-4034.
29. Nakagawa S., Hirose T. Paraspeckle nuclear bodies-useful uselessness?. Cell. Mol. Life Sci. 2012, 69:3027-3036.
30. Oakland T.E., Haselton K.J., Randall G. EWSR1 binds the hepatitis C virus cis-acting replication element and is required for efficient viral replication. J.Virol. 2013, 87:6625-6634.
31. Peng R., Dye B.T., Pérez I., Barnard D.C., Thompson A.B., Patton J.G. PSF and p54nrb bind a conserved stem in U5 snRNA. RNA 2002, 8:1334-1347.
32. Ponting C.P., Oliver P.L., Reik W. Evolution and functions of long noncoding RNAs. Cell 2009, 136:629-641.
33. Prasanth K.V., Spector D.L. Eukaryotic regulatory RNAs: an answer to the 'genome complexity' conundrum. Genes Dev. 2007, 21:11-42.
34. Rathinam V.A., Fitzgerald K.A. Cytosolic surveillance and antiviral immunity. Curr Opin Virol 2011, 1:455-462.
35. Ray D., Kazan H., Cook K.B., Weirauch M.T., Najafabadi H.S., Li X., Gueroussov S., Albu M., Zheng H., Yang A., et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 2013, 499:172-177.
36. Saha S., Murthy S., Rangarajan P.N. Identification and characterization of a virus-inducible non-coding RNA in mouse brain. J.Gen. Virol. 2006, 87:1991-1995.
37. Sasaki Y.T., Ideue T., Sano M., Mituyama T., Hirose T. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc. Natl. Acad. Sci. USA 2009, 106:2525-2530.
38. Scaria V., Pasha A. Long Non-Coding RNAs in Infection Biology. Front Genet 2012, 3:308.
39. Sonenberg N. Measures and countermeasures in the modulation of initiation factor activities by viruses. New Biol. 1990, 2:402-409.
40. Song X., Sui A., Garen A. Binding of mouse VL30 retrotransposon RNA to PSF protein induces genes repressed by PSF: effects on steroidogenesis and oncogenesis. Proc. Natl. Acad. Sci. USA 2004, 101:621-626.
41. Sunwoo H., Dinger M.E., Wilusz J.E., Amaral P.P., Mattick J.S., Spector D.L. MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res. 2009, 19:347-359.
42. Tani H., Mizutani R., Salam K.A., Tano K., Ijiri K., Wakamatsu A., Isogai T., Suzuki Y., Akimitsu N. Genome-wide determination of RNA stability reveals hundreds of short-lived noncoding transcripts in mammals. Genome Res. 2012, 22:947-956.
43. Tani H., Torimura M., Akimitsu N. The RNA degradation pathway regulates the function of GAS5 a non-coding RNA in mammalian cells. PLoS ONE 2013, 8:e55684.
44. Tano K., Mizuno R., Okada T., Rakwal R., Shibato J., Masuo Y., Ijiri K., Akimitsu N. MALAT-1 enhances cell motility of lung adenocarcinoma cells by influencing the expression of motility-related genes. FEBS Lett. 2010, 584:4575-4580.
45. Thompson M.R., Kaminski J.J., Kurt-Jones E.A., Fitzgerald K.A. Pattern recognition receptors and the innate immune response to viral infection. Viruses 2011, 3:920-940.
46. Urban R.J., Bodenburg Y., Kurosky A., Wood T.G., Gasic S. Polypyrimidine tract-binding protein-associated splicing factor is a negative regulator of transcriptional activity of the porcine p450scc insulin-like growth factor response element. Mol. Endocrinol. 2000, 14:774-782.
47. Wang K.C., Chang H.Y. Molecular mechanisms of long noncoding RNAs. Mol. Cell 2011, 43:904-914.
48. Yang L., Lin C., Liu W., Zhang J., Ohgi K.A., Grinstein J.D., Dorrestein P.C., Rosenfeld M.G. ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 2011, 147:773-788.
49. Yoon J.H., Abdelmohsen K., Gorospe M. Posttranscriptional Gene Regulation by Long Noncoding RNA. J.Mol. Biol. 2013, 425:3723-3730.
50. Zhang S.Y., Jouanguy E., Ugolini S., Smahi A., Elain G., Romero P., Segal D., Sancho-Shimizu V., Lorenzo L., Puel A., et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science 2007, 317:1522-1527.
51. Zhang W., Zhang X., Tian C., Wang T., Sarkis P.T., Fang Y., Zheng S., Yu X.F., Xu R. Cytidine deaminase APOBEC3B interacts with heterogeneous nuclear ribonucleoprotein K and suppresses hepatitis B virus expression. Cell. Microbiol. 2008, 10:112-121.
52. Zhang Q., Chen C.Y., Yedavalli V.S., Jeang K.T. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 2013, 4. e00596-e12.
53. Zolotukhin A.S., Michalowski D., Bear J., Smulevitch S.V., Traish A.M., Peng R., Patton J., Shatsky I.N., Felber B.K. PSF acts through the human immunodeficiency virus type 1 mRNA instability elements to regulate virus expression. Mol. Cell. Biol. 2003, 23:6618-6630.