Functional conservation of the lncRNA NEAT1 in the ancestrally diverged marsupial lineage: Evidence for NEAT1 expression and associated paraspeckle assembly during late gestation in the opossum Monodelphis domestica

RNA Biology

Volumn 13, Issue 9, 2016, Pages 826-836

  Cornelis, Guillaume ^a,b   Souquere, Sylvie ^a   Vernochet, Cécile ^a   Heidmann, Thierry ^a   Pierron, Gérard ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Immuno electron microscopy; lncRNAs; NEAT1; nuclear bodies; opossum; paraspeckles; pregnancy; ultrastructure; uterine glands

Indexed keywords

LONG UNTRANSLATED RNA; RIBONUCLEASE P; RNA ISOFORM;

ARTICLE; CELL NUCLEUS INCLUSION BODY; CLINICAL FEATURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE; GENE EXPRESSION; GENE SEQUENCE; IMMUNOELECTRON MICROSCOPY; IMMUNOGOLD ELECTRON MICROSCOPY; IN SITU HYBRIDIZATION; KIDNEY CELL; MARSUPIAL; MONODELPHIS DOMESTICA; NONHUMAN; NUCLEAR ENRICHED ABUNDANT TRANSCRIPT 1 GENE; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA CLEAVAGE; THIRD TRIMESTER PREGNANCY; TISSUE SPECIFICITY; ANIMAL; ANTIBODY SPECIFICITY; CELL LINE; CELL NUCLEUS; CHEMISTRY; CHROMOSOMAL MAPPING; CONFORMATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MONODELPHIS; NUCLEOTIDE SEQUENCE; ORGANOGENESIS;

ANIMALS; BASE SEQUENCE; CELL LINE; CELL NUCLEUS; CHROMOSOME MAPPING; EVOLUTION, MOLECULAR; GENE EXPRESSION; MONODELPHIS; NUCLEIC ACID CONFORMATION; ORGAN SPECIFICITY; ORGANOGENESIS; RNA ISOFORMS; RNA, LONG NONCODING;

EID: 84978516329     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2016.1197482     Document Type: Article

References (42)

1. J.G.Gall. The centennial of the Cajal body. Nat Rev Mol Cell Biol 2003; 4:975-80; PMID:14685175; http://dx.doi.org/10.1038/nrm1262
2. V.Lallemand-Breitenbach, H.de The. PML nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2:a000661; PMID:20452955; http://dx.doi.org/10.1101/cshperspect.a000661
3. Y.S.Mao, B.Zhang, D.L.Spector. Biogenesis and function of nuclear bodies. Trends Genet 2011; 27:295-306; PMID:21680045; http://dx.doi.org/10.1016/j.tig.2011.05.006
4. J.E.Sleeman, L.Trinkle-Mulcahy. Nuclear bodies:new insights into assembly/dynamics and disease relevance. Curr Opin Cell Biol 2014; 28:76-83; PMID:24704702; http://dx.doi.org/10.1016/j.ceb.2014.03.004
5. S.Souquere, D.Weil, G.Pierron. Comparative ultrastructure of CRM1-Nucleolar bodies (CNoBs), Intranucleolar bodies (INBs) and hybrid PML/p62 bodies uncovers new facets of nuclear body dynamic and diversity. Nucleus 2015; 6:326-38; PMID:26275159; http://dx.doi.org/10.1080/19491034.2015.1082695
6. D.L.Spector. SnapShot:Cellular bodies. Cell 2006; 127:1071; PMID:17129789; http://dx.doi.org/10.1016/j.cell.2006.11.026
7. S.Nakagawa, T.Naganuma, G.Shioi, T.Hirose. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J Cell Biol 2011; 193:31-9; PMID:21444682; http://dx.doi.org/10.1083/jcb.201011110
8. K.L.Borden. Pondering the promyelocytic leukemia protein (PML) puzzle:possible functions for PML nuclear bodies. Mol Cell Biol 2002; 22:5259-69; PMID:12101223; http://dx.doi.org/10.1128/MCB.22.15.5259-5269.2002
9. A.H.Fox, Y.W.Lam, A.K.Leung, C.E.Lyon, J.Andersen, M.Mann, A.I.Lamond. Paraspeckles:a novel nuclear domain. Curr Biol 2002; 12:13-25; PMID:11790299; http://dx.doi.org/10.1016/S0960-9822(01)00632-7
10. N.Visa, F.Puvion-Dutilleul, J.P.Bachellerie, E.Puvion. Intranuclear distribution of U1 and U2 snRNAs visualized by high resolution in situ hybridization:revelation of a novel compartment containing U1 but not U2 snRNA in HeLa cells. Eur J Cell Biol 1993; 60:308-21; PMID:8330629
11. Y.S.Mao, H.Sunwoo, B.Zhang, D.L.Spector. Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat Cell Biol 2011; 13:95-101; PMID:21170033; http://dx.doi.org/10.1038/ncb2140
12. H.Sunwoo, M.E.Dinger, J.E.Wilusz, P.P.Amaral, J.S.Mattick, D.L.Spector. MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res 2009; 19:347-59; PMID:19106332; http://dx.doi.org/10.1101/gr.087775.108
13. Y.T.Sasaki, T.Ideue, M.Sano, T.Mituyama, T.Hirose. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc Natl Acad Sci U S A 2009; 106:2525-30; PMID:19188602; http://dx.doi.org/10.1073/pnas.0807899106
14. C.M.Clemson, J.N.Hutchinson, S.A.Sara, A.W.Ensminger, A.H.Fox, A.Chess, J.B.Lawrence. An architectural role for a nuclear noncoding RNA:NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 2009; 33:717-26; PMID:19217333; http://dx.doi.org/10.1016/j.molcel.2009.01.026
15. J.N.Hutchinson, A.W.Ensminger, C.M.Clemson, C.R.Lynch, J.B.Lawrence, A.Chess. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC Genomics 2007; 8:39; PMID:17270048; http://dx.doi.org/10.1186/1471-2164-8-39
16. J.A.Brown, M.L.Valenstein, T.A.Yario, K.T.Tycowski, J.A.Steitz. Formation of triple-helical structures by the 3′-end sequences of MALAT1 and MENbeta noncoding RNAs. Proc Natl Acad Sci U S A 2012; 109:19202-7; PMID:23129630; http://dx.doi.org/10.1073/pnas.1217338109
17. J.E.Wilusz, S.M.Freier, D.L.Spector. 3′ end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 2008; 135:919-32; PMID:19041754; http://dx.doi.org/10.1016/j.cell.2008.10.012
18. J.E.Wilusz, C.K.JnBaptiste, L.Y.Lu, C.D.Kuhn, L.Joshua-Tor, P.A.Sharp. A triple helix stabilizes the 3′ ends of long noncoding RNAs that lack poly(A) tails. Genes Dev 2015; 26:2392-407; PMID:23073843; http://dx.doi.org/10.1101/gad.204438.112
19. T.Naganuma, S.Nakagawa, A.Tanigawa, Y.F.Sasaki, N.Goshima, T.Hirose. Alternative 3′-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. Embo J 2012; 31:4020-34; PMID:22960638; http://dx.doi.org/10.1038/emboj.2012.251
20. S.Souquere, G.Beauclair, F.Harper, A.Fox, G.Pierron. Highly ordered spatial organization of the structural long noncoding NEAT1 RNAs within paraspeckle nuclear bodies. Mol Biol Cell 2010; 21:4020-7; PMID:20881053; http://dx.doi.org/10.1091/mbc.E10-08-0690
21. A.H.Fox, C.S.Bond, A.I.Lamond. P54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner. Mol Biol Cell 2005; 16:5304-15; PMID:16148043; http://dx.doi.org/10.1091/mbc.E05-06-0587
22. K.V.Prasanth, S.G.Prasanth, Z.Xuan, S.Hearn, S.M.Freier, C.F.Bennett, M.Q.Zhang, D.L.Spector. Regulating gene expression through RNA nuclear retention. Cell 2005; 123:249-63; PMID:16239143; http://dx.doi.org/10.1016/j.cell.2005.08.033
23. S.Hennig, G.Kong, T.Mannen, A.Sadowska, S.Kobelke, A.Blythe, G.J.Knott, K.S.Iyer, D.Ho, E.A.Newcombe, et al. Prion-like domains in RNA binding proteins are essential for building subnuclear paraspeckles. J Cell Biol 2015; 210:529-39; PMID:26283796; http://dx.doi.org/10.1083/jcb.201504117
24. T.Yamazaki, T.Hirose. The building process of the functional paraspeckle with long non-coding RNAs. Front Biosci (Elite Ed) 2015; 7:1-41; PMID:25553361; http:/dx.doi.org/10.2741/e715
25. L.L.Chen, G.G.Carmichael. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells:functional role of a nuclear noncoding RNA. Mol Cell 2009; 35:467-78; PMID:19716791; http://dx.doi.org/10.1016/j.molcel.2009.06.027
26. R.A.Elbarbary, L.E.Maquat. CARMing down the SINEs of anarchy:two paths to freedom from paraspeckle detention. Genes Dev 2015; 29:687-9; PMID:25838539; http://dx.doi.org/10.1101/gad.261438.115
27. T.Hirose, G.Virnicchi, A.Tanigawa, T.Naganuma, R.Li, H.Kimura, T.Yokoi, S.Nakagawa, M.Benard, A.H.Fox, et al. NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol Biol Cell 2014; 25:169-83; PMID:24173718; http://dx.doi.org/10.1091/mbc.E13-09-0558
28. K.Imamura, N.Imamachi, G.Akizuki, M.Kumakura, A.Kawaguchi, K.Nagata, A.Kato, Y.Kawaguchi, H.Sato, M.Yoneda, et al. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol Cell 2014; 53:393-406; PMID:24507715; http://dx.doi.org/10.1016/j.molcel.2014.01.009
29. H.Choudhry, A.Albukhari, M.Morotti, S.Haider, D.Moralli, J.Smythies, J.Schodel, C.M.Green, C.Camps, F.Buffa, et al. Tumor hypoxia induces nuclear paraspeckle formation through HIF-2alpha dependent transcriptional activation of NEAT1 leading to cancer cell survival. Oncogene 2015; 34:4546; PMID:26289678; http://dx.doi.org/10.1038/onc.2014.431
30. Y.Li, Y.Li, W.Chen, F.He, Z.Tan, J.Zheng, W.Wang, Q.Zhao, J.Li. NEAT expression is associated with tumor recurrence and unfavorable prognosis in colorectal cancer. Oncotarget 2015; 6:27641-50; PMID:26314847; http://dx.doi.org/10.18632/oncotarget.4737
31. D.Chakravarty, A.Sboner, S.S.Nair, E.Giannopoulou, R.Li, S.Hennig, J.M.Mosquera, J.Pauwels, K.Park, M.Kossai, et al. The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nat Commun 2014; 5:5383; PMID:25415230; http://dx.doi.org/10.1038/ncomms6383
32. L.Standaert, C.Adriaens, E.Radaelli, A.Van Keymeulen, C.Blanpain, T.Hirose, S.Nakagawa, J.C.Marine. The long noncoding RNA Neat1 is required for mammary gland development and lactation. Rna 2014; 20:1844-9; PMID:25316907; http://dx.doi.org/10.1261/rna.047332.114
33. S.Nakagawa, M.Shimada, K.Yanaka, M.Mito, T.Arai, E.Takahashi, Y.Fujita, T.Fujimori, L.Standaert, J.C.Marine, et al. The lncRNA Neat1 is required for corpus luteum formation and the establishment of pregnancy in a subpopulation of mice. Development 2014; 141:4618-27; PMID:25359727; http://dx.doi.org/10.1242/dev.110544
34. G.Cornelis, C.Vernochet, Q.Carradec, S.Souquere, B.Mulot, F.Catzeflis, M.A.Nilsson, B.R.Menzies, M.B.Renfree, G.Pierron, et al. Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci U S A 2015; 112:E487-96; PMID:25605903; http://dx.doi.org/10.1073/pnas.1417000112
35. U.Zeller, C.Freyer. Early ontogeny and placentation of the grey short-tailed opossum, Monodelphis domestica (Didelphidae:Marsupialia):contribution to the reconstruction of the marsupial morphotype. J Zool Syst Evol Research 2001; 39:137-58; http://dx.doi.org/10.1046/j.1439-0469.2001.00167.x
36. D.Cmarko, P.J.Verschure, T.E.Martin, M.E.Dahmus, S.Krause, X.D.Fu, R.van Driel, S.Fakan. Ultrastructural analysis of transcription and splicing in the cell nucleus after bromo-UTP microinjection. Mol Biol Cell 1999; 10:211-23; PMID:9880337; http://dx.doi.org/10.1091/mbc.10.1.211
37. M.Malatesta, S.Fakan, U.Fischer. The Sm core domain mediates targeting of U1 snRNP to subnuclear compartments involved in transcription and splicing. Exp Cell Res 1999; 249:189-98; PMID:10366418; http://dx.doi.org/10.1006/excr.1999.4468
38. J.A.West, C.P.Davis, H.Sunwoo, M.D.Simon, R.I.Sadreyev, P.I.Wang, M.Y.Tolstorukov, R.E.Kingston. The long noncoding RNAs NEAT1 and MALAT1 bind active chromatin sites. Mol Cell 2014; 55:791-802; PMID:25155612; http://dx.doi.org/10.1016/j.molcel.2014.07.012
39. P.Stadler. Evolution of the Long Non-coding RNAs MALAT1 and MENβ/ϵ. Adv Bioinformatics Comput Biol 2010;1-12; http://dx.doi.org/10.1007/978-3-642-15060-9_1
40. S.Saha, S.Murthy, P.N.Rangarajan. Identification and characterization of a virus-inducible non-coding RNA in mouse brain. J Gen Virol 2006; 87:1991-5; PMID:16760401; http://dx.doi.org/10.1099/vir.0.81768-0
41. Q.Zhang, C.Y.Chen, V.S.Yedavalli, K.T.Jeang. NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio 2013; 4:e00596-12; PMID:23362321; http://dx.doi.org/10.1128/mBio.00596-12
42. S.Souquere, S.Mollet, M.Kress, F.Dautry, G.Pierron, D.Weil. Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J Cell Sci 2009; 122:3619-26; PMID:19812307; http://dx.doi.org/10.1242/jcs.054437