Structural, super-resolution microscopy analysis of paraspeckle nuclear body organization

Journal of Cell Biology

Volumn 214, Issue 7, 2016, Pages

  West, Jason A ^a,b   Mito, Mari ^c   Kurosaka, Satoshi ^d   Takumi, Toru ^d   Tanegashima, Chiharu ^c   Chujo, Takeshi ^e   Yanaka, Kaori ^c   Kingston, Robert E ^a,b   Hirose, Tetsuro ^e   Bond, Charles ^f   Fox, Archa ^f,g   Nakagawa, Shinichi ^c,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c RIKEN   (Japan)

^d RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^e HOKKAIDO UNIVERSITY   (Japan)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^g PATHWEST LABORATORY MEDICINE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; RNA; LONG UNTRANSLATED RNA; NEAT1 LONG NON-CODING RNA, MOUSE; RNA BINDING PROTEIN FUS;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL NUCLEUS INCLUSION BODY; CELL STRUCTURE; FEMALE; GENE; MICROSCOPY; MOUSE; NEAT1 GENE; NONHUMAN; NUCLEOPLASM; PARASPECKLE; PRIORITY JOURNAL; RNA SEQUENCE; ANIMAL; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROCEDURES; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; FEMALE; FIBROBLASTS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRANUCLEAR INCLUSION BODIES; MICE; MICROSCOPY; RNA, LONG NONCODING; RNA-BINDING PROTEIN FUS; SEQUENCE ANALYSIS, RNA;

EID: 84991256820     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201601071     Document Type: Article

References (47)

1. Bond, C.S., and A.H. Fox. 2009. Paraspeckles: nuclear bodies built on long noncoding RNA. J. Cell Biol. 186:637-644. doi:10.1083/jcb.200906113
2. Cardinale, S., B. Cisterna, P. Bonetti, C. Aringhieri, M. Biggiogera, and S.M. Barabino. 2007. Subnuclear localization and dynamics of the Pre-mRNA 3' end processing factor mammalian cleavage factor I 68-kDa subunit. Mol. Biol. Cell. 18:1282-1292. doi:10.1091/mbc.E06-09-0846
3. Cerase, A., D. Smeets, Y.A. Tang, M. Gdula, F. Kraus, M. Spivakov, B. Moindrot, M. Leleu, A. Tattermusch, J. Demmerle, et al. 2014. Spatial separation of Xist RNA and polycomb proteins revealed by superresolution microscopy. Proc. Natl. Acad. Sci. USA. 111:2235-2240. doi:10.1073/pnas.1312951111
4. Chakravarty, D., A. Sboner, S.S. Nair, E. Giannopoulou, R. Li, S. Hennig, J.M. Mosquera, J. Pauwels, K. Park, M. Kossai, et al. 2014. The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nat. Commun. 5:5383. doi:10.1038/ncomms6383
5. Chen, L.L., and G.G. Carmichael. 2009. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol. Cell. 35:467-478. doi:10.1016/j.molcel.2009.06.027
6. Chu, C., Q.C. Zhang, S.T. da Rocha, R.A. Flynn, M. Bharadwaj, J.M. Calabrese, T. Magnuson, E. Heard, and H.Y. Chang. 2015. Systematic discovery of Xist RNA binding proteins. Cell. 161:404-416. doi:10.1016/j.cell.2015.03.025
7. Clemson, C.M., J.N. Hutchinson, S.A. Sara, A.W. Ensminger, A.H. Fox, A. Chess, and J.B. Lawrence. 2009. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell. 33:717-726. doi:10.1016/j.molcel.2009.01.026
8. Davis, C.P., and J.A. West. 2015. Purification of specific chromatin regions using oligonucleotides: capture hybridization analysis of RNA targets (CHART). Methods Mol. Biol. 1262:167-182. doi:10.1007/978-1-4939-2253-6_10
9. Dong, B., D.S. Horowitz, R. Kobayashi, and A.R. Krainer. 1993. Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6. Nucleic Acids Res. 21:4085-4092. doi:10.1093/nar/21.17.4085
10. Fox, A.H., Y.W. Lam, A.K.L. Leung, C.E. Lyon, J. Andersen, M. Mann, and A.I. Lamond. 2002. Paraspeckles: a novel nuclear domain. Curr. Biol. 12:13-25. doi:10.1016/S0960-9822(01)00632-7
11. Fox, A.H., C.S. Bond, and A.I. Lamond. 2005. P54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner. Mol. Biol. Cell. 16:5304-5315. doi:10.1091/mbc.E05-06-0587
12. Gustafsson, M.G. 2000. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198:82-87. doi:10.1046/j.1365-2818.2000.00710.x
13. Han, T.W., M. Kato, S. Xie, L.C. Wu, H. Mirzaei, J. Pei, M. Chen, Y. Xie, J. Allen, G. Xiao, and S.L. McKnight. 2012. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell. 149:768-779. doi:10.1016/j.cell.2012.04.016
14. Hennig, S., G. Kong, T. Mannen, A. Sadowska, S. Kobelke, A. Blythe, G.J. Knott, K.S. Iyer, D. Ho, E.A. Newcombe, et al. 2015. Prion-like domains in RNA binding proteins are essential for building subnuclear paraspeckles. J. Cell Biol. 210:529-539. doi:10.1083/jcb.201504117
15. Hicks, G.G., N. Singh, A. Nashabi, S. Mai, G. Bozek, L. Klewes, D. Arapovic, E.K. White, M.J. Koury, E.M. Oltz, et al. 2000. Fus deficiency in mice results in defective B-lymphocyte development and activation, high levels of chromosomal instability and perinatal death. Nat. Genet. 24:175-179. doi:10.1038/72842
16. Hirose, T., G. Virnicchi, A. Tanigawa, T. Naganuma, R. Li, H. Kimura, T. Yokoi, S. Nakagawa, M. Bénard, A.H. Fox, and G. Pierron. 2014. NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol. Biol. Cell. 25:169-183. doi:10.1091/mbc.E13-09-0558
17. Hoell, J.I., E. Larsson, S. Runge, J.D. Nusbaum, S. Duggimpudi, T.A. Farazi, M. Hafner, A. Borkhardt, C. Sander, and T. Tuschl. 2011. RNA targets of wild-type and mutant FET family proteins. Nat. Struct. Mol. Biol. 18:1428-1431. doi:10.1038/nsmb.2163
18. Imamura, K., N. Imamachi, G. Akizuki, M. Kumakura, A. Kawaguchi, K. Nagata, A. Kato, Y. Kawaguchi, H. Sato, M. Yoneda, et al. 2014. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell. 53:393-406. (published erratum appears in Mol. Cell. 2014. 540:1055) doi:10.1016/j.molcel.2014.01.009
19. Kato, M., T.W. Han, S. Xie, K. Shi, X. Du, L.C. Wu, H. Mirzaei, E.J. Goldsmith, J. Longgood, J. Pei, et al. 2012. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell. 149:753-767. doi:10.1016/j.cell.2012.04.017
20. Lagier-Tourenne, C., M. Polymenidou, K.R. Hutt, A.Q. Vu, M. Baughn, S.C. Huelga, K.M. Clutario, S.C. Ling, T.Y. Liang, C. Mazur, et al. 2012. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat. Neurosci. 15:1488-1497. doi:10.1038/nn.3230
21. Mao, Y.S., H. Sunwoo, B. Zhang, and D.L. Spector. 2011. Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat. Cell Biol. 13:95-101. doi:10.1038/ncb2140
22. McHugh, C.A., C.K. Chen, A. Chow, C.F. Surka, C. Tran, P. McDonel, A. Pandya-Jones, M. Blanco, C. Burghard, A. Moradian, et al. 2015. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature. 521:232-236. doi:10.1038/nature14443
23. Mito, M., T. Kawaguchi, T. Hirose, and S. Nakagawa. 2016. Simultaneous multicolor detection of RNA and proteins using super-resolution microscopy. Methods. 98:158-165. doi:10.1016/j.ymeth.2015.11.007
24. Moindrot, B., A. Cerase, H. Coker, O. Masui, A. Grijzenhout, G. Pintacuda, L. Schermelleh, T.B. Nesterova, and N. Brockdorff. 2015. A Pooled shRNA Screen Identifies Rbm15, Spen, and Wtap as Factors Required for Xist RNA-Mediated Silencing. Cell Reports. 12:562-572. doi:10.1016/j.celrep.2015.06.053
25. Naganuma, T., S. Nakagawa, A. Tanigawa, Y.F. Sasaki, N. Goshima, and T. Hirose. 2012. Alternative 3'-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J. 31:4020-4034. doi:10.1038/emboj.2012.251
26. Nakagawa, S., T. Naganuma, G. Shioi, and T. Hirose. 2011. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J. Cell Biol. 193:31-39. doi:10.1083/jcb.201011110
27. Nakagawa, S., M. Shimada, K. Yanaka, M. Mito, T. Arai, E. Takahashi, Y. Fujita, T. Fujimori, L. Standaert, J.C. Marine, and T. Hirose. 2014. The lncRNA Neat1 is required for corpus luteum formation and the establishment of pregnancy in a subpopulation of mice. Development. 141:4618-4627. doi:10.1242/dev.110544
28. P. JeanteurPlatani, M., and A. Lamond. 2004. Nuclear organisation and subnuclear bodies. In RNA Trafficking and Nuclear Structure Dynamics. Vol. 35. P. Jeanteur, editor. Springer, Berlin. 1-22
29. Polymenidou, M., C. Lagier-Tourenne, K.R. Hutt, S.C. Huelga, J. Moran, T.Y. Liang, S.C. Ling, E. Sun, E. Wancewicz, C. Mazur, et al. 2011. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci. 14:459-468. doi:10.1038/nn.2779
30. Prasanth, K.V., S.G. Prasanth, Z. Xuan, S. Hearn, S.M. Freier, C.F. Bennett, M.Q. Zhang, and D.L. Spector. 2005. Regulating gene expression through RNA nuclear retention. Cell. 123:249-263. doi:10.1016/j.cell.2005.08.033
31. Quinn, J.J., I.A. Ilik, K. Qu, P. Georgiev, C. Chu, A. Akhtar, and H.Y. Chang. 2014. Revealing long noncoding RNA architecture and functions using domain-specific chromatin isolation by RNA purification. Nat. Biotechnol. 32:933-940. doi:10.1038/nbt.2943
32. Rogelj, B., L.E. Easton, G.K. Bogu, L.W. Stanton, G. Rot, T. Curk, B. Zupan, Y. Sugimoto, M. Modic, N. Haberman, et al. 2012. Widespread binding of FUS along nascent RNA regulates alternative splicing in the brain. Sci. Rep. 2:603. doi:10.1038/srep00603
33. Sasaki, Y.T., T. Ideue, M. Sano, T. Mituyama, and T. Hirose. 2009. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc. Natl. Acad. Sci. USA. 106:2525-2530. doi:10.1073/pnas.0807899106
34. Schermelleh, L., R. Heintzmann, and H. Leonhardt. 2010. A guide to super-resolution fluorescence microscopy. J. Cell Biol. 190:165-175. doi:10.1083/jcb.201002018
35. Schwartz, J.C., C.C. Ebmeier, E.R. Podell, J. Heimiller, D.J. Taatjes, and T.R. Cech. 2012. FUS binds the CTD of RNA polymerase II and regulates its phosphorylation at Ser2. Genes Dev. 26:2690-2695. doi:10.1101/gad.204602.112
36. Shamir, L., N. Orlov, D.M. Eckley, T. Macura, J. Johnston, and I.G. Goldberg. 2008. Wndchrm-an open source utility for biological image analysis. Source Code Biol. Med. 3:13. doi:10.1186/1751-0473-3-13
37. Shav-Tal, Y., and D. Zipori. 2002. PSF and p54(nrb)/NonO-multi-functional nuclear proteins. FEBS Lett. 531:109-114. doi:10.1016/S0014-5793(02)03447-6
38. Shelkovnikova, T.A., H.K. Robinson, C. Troakes, N. Ninkina, and V.L. Buchman. 2014. Compromised paraspeckle formation as a pathogenic factor in FUSopathies. Hum. Mol. Genet. 23:2298-2312. doi:10.1093/hmg/ddt622
39. Shevtsov, S.P., and M. Dundr. 2011. Nucleation of nuclear bodies by RNA. Nat. Cell Biol. 13:167-173. doi:10.1038/ncb2157
40. Simon, M.D., C.I. Wang, P.V. Kharchenko, J.A. West, B.A. Chapman, A.A. Alekseyenko, M.L. Borowsky, M.I. Kuroda, and R.E. Kingston. 2011. The genomic binding sites of a noncoding RNA. Proc. Natl. Acad. Sci. USA. 108:20497-20502. doi:10.1073/pnas.1113536108
41. Simon, M.D., S.F. Pinter, R. Fang, K. Sarma, M. Rutenberg-Schoenberg, S.K. Bowman, B.A. Kesner, V.K. Maier, R.E. Kingston, and J.T. Lee. 2013. High-resolution Xist binding maps reveal two-step spreading during X-chromosome inactivation. Nature. 504:465-469. doi:10.1038/nature12719
42. Souquere, S., G. Beauclair, F. Harper, A. Fox, and G. Pierron. 2010. Highly ordered spatial organization of the structural long noncoding NEAT1 RNAs within paraspeckle nuclear bodies. Mol. Biol. Cell. 21:4020-4027. doi:10.1091/mbc.E10-08-0690
43. Spector, D.L. 2006. SnapShot: Cellular bodies. Cell. 127:1071. doi:10.1016/j.cell.2006.11.026
44. Standaert, L., C. Adriaens, E. Radaelli, A. Van Keymeulen, C. Blanpain, T. Hirose, S. Nakagawa, and J.C. Marine. 2014. The long noncoding RNA Neat1 is required for mammary gland development and lactation. RNA. 20:1844-1849. doi:10.1261/rna.047332.114
45. Sunwoo, H., M.E. Dinger, J.E. Wilusz, P.P. Amaral, J.S. Mattick, and D.L. Spector. 2009. MEN e/βnuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res. 19:347-359. doi:10.1101/gr.087775.108
46. Tollervey, J.R., T. Curk, B. Rogelj, M. Briese, M. Cereda, M. Kayikci, J. König, T. Hortobágyi, A.L. Nishimura, V. Zupunski, et al. 2011. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. 14:452-458. doi:10.1038/nn.2778
47. West, J.A., C.P. Davis, H. Sunwoo, M.D. Simon, R.I. Sadreyev, P.I. Wang, M.Y. Tolstorukov, and R.E. Kingston. 2014. The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. Mol. Cell. 55:791-802. doi:10.1016/j.molcel.2014.07.012