A novel long intergenic noncoding RNA indispensable for the cleavage of mouse two-cell embryos

EMBO Reports

Volumn 17, Issue 10, 2016, Pages 1452-1470

  Wang, Jiaqiang ^a,b   Li, Xin ^a,b   Wang, Leyun ^a,b   Li, Jingyu ^a   Zhao, Yanhua ^a   Bou, Gerelchimeg ^a   Li, Yufei ^b   Jiao, Guanyi ^b   Shen, Xinghui ^c   Wei, Renyue ^a   Liu, Shichao ^a   Xie, Bingteng ^a   Lei, Lei ^c   Li, Wei ^b   Zhou, Qi ^b   Liu, Zhonghua ^a  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF ZOOLOGY   (China)

^c HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

ERV; exon skipping; lincRNA; transcription regulation; two cell block

Indexed keywords

CELL PROTEIN; FUBP PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U; HNRNPU PROTEIN; INTERLEUKIN ENHANCER BINDING FACTOR 2; LONG UNTRANSLATED RNA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENDOGENOUS RETROVIRUS; EXON; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; LONG TERMINAL REPEAT; MOUSE; NONHUMAN; OOCYTE CLEAVAGE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN RNA BINDING; SIGNAL TRANSDUCTION;

EID: 84989965982     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201642051     Document Type: Article

References (83)

1. Probst AV, Almouzni G (2011) Heterochromatin establishment in the context of genome-wide epigenetic reprogramming. Trends Genet 27: 177–185
2. Schultz RM (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8: 323–331
3. Bedzhov I, Graham SJ, Leung CY, Zernicka-Goetz M (2014) Developmental plasticity, cell fate specification and morphogenesis in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci 369: 20130538
4. Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM, Bonanomi D, Firth A, Singer O, Trono D, Pfaff SL (2012) Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487: 57–63
5. Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L, Bourque G, Yandell M, Feschotte C (2013) Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 9: e1003470
6. Peaston AE, Evsikov AV, Graber JH, de Vries WN, Holbrook AE, Solter D, Knowles BB (2004) Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 7: 597–606
7. Evsikov AV, de Vries WN, Peaston AE, Radford EE, Fancher KS, Chen FH, Blake JA, Bult CJ, Latham KE, Solter D et al (2004) Systems biology of the 2-cell mouse embryo. Cytogenet Genome Res 105: 240–250
8. Wang J, Xie G, Singh M, Ghanbarian AT, Rasko T, Szvetnik A, Cai H, Besser D, Prigione A, Fuchs NV et al (2014) Primate-specific endogenous retrovirus-driven transcription defines naive-like stem cells. Nature 516: 405–409
9. Lu X, Sachs F, Ramsay L, Jacques PE, Goke J, Bourque G, Ng HH (2014) The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity. Nat Struct Mol Biol 21: 423–425
10. Ohnuki M, Tanabe K, Sutou K, Teramoto I, Sawamura Y, Narita M, Nakamura M, Tokunaga Y, Nakamura M, Watanabe A et al (2014) Dynamic regulation of human endogenous retroviruses mediates factor-induced reprogramming and differentiation potential. Proc Natl Acad Sci USA 111: 12426–12431
11. Grow EJ, Flynn RA, Chavez SL, Bayless NL, Wossidlo M, Wesche DJ, Martin L, Ware CB, Blish CA, Chang HY et al (2015) Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells. Nature 522: 221–225
12. Durruthy-Durruthy J, Sebastiano V, Wossidlo M, Cepeda D, Cui J, Grow EJ, Davila J, Mall M, Wong WH, Wysocka J et al (2015) The primate-specific noncoding RNA HPAT5 regulates pluripotency during human preimplantation development and nuclear reprogramming. Nat Genet 48: 44–52
13. Gendrel AV, Heard E (2014) Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu Rev Cell Dev Biol 30: 561–580
14. Koerner MV, Pauler FM, Huang R, Barlow DP (2009) The function of non-coding RNAs in genomic imprinting. Development 136: 1771–1783
15. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689–693
16. Bertani S, Sauer S, Bolotin E, Sauer F (2011) The noncoding RNA Mistral activates Hoxa6 and Hoxa7 expression and stem cell differentiation by recruiting MLL1 to chromatin. Mol Cell 43: 1040–1046
17. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147: 1537–1550
18. Hawkins PG, Morris KV (2010) Transcriptional regulation of Oct4 by a long non-coding RNA antisense to Oct4-pseudogene 5. Transcription 1: 165–175
19. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295–300
20. Rosa A, Ballarino M (2016) Long noncoding RNA regulation of pluripotency. Stem Cells Int 2016: 1797692
21. Williams GT, Mourtada-Maarabouni M, Farzaneh F (2011) A critical role for non-coding RNA GAS5 in growth arrest and rapamycin inhibition in human T-lymphocytes. Biochem Soc Trans 39: 482–486
22. Johnsson P, Ackley A, Vidarsdottir L, Lui WO, Corcoran M, Grander D, Morris KV (2013) A pseudogene long-noncoding-RNA network regulates PTEN transcription and translation in human cells. Nat Struct Mol Biol 20: 440–446
23. Gomez JA, Wapinski OL, Yang YW, Bureau JF, Gopinath S, Monack DM, Chang HY, Brahic M, Kirkegaard K (2013) The NeST long ncRNA controls microbial susceptibility and epigenetic activation of the interferon-gamma locus. Cell 152: 743–754
24. Wang P, Xue Y, Han Y, Lin L, Wu C, Xu S, Jiang Z, Xu J, Liu Q, Cao X (2014) The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science 344: 310–313
25. Wang K, Sun T, Li N, Wang Y, Wang JX, Zhou LY, Long B, Liu CY, Liu F, Li PF (2014) MDRL lncRNA regulates the processing of miR-484 primary transcript by targeting miR-361. PLoS Genet 10: e1004467
26. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311–1323
27. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750–756
28. Bond AM, Vangompel MJ, Sametsky EA, Clark MF, Savage JC, Disterhoft JF, Kohtz JD (2009) Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat Neurosci 12: 1020–1027
29. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R (2008) Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454: 126–130
30. Imamura T, Yamamoto S, Ohgane J, Hattori N, Tanaka S, Shiota K (2004) Non-coding RNA directed DNA demethylation of Sphk1 CpG island. Biochem Biophys Res Commun 322: 593–600
31. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143: 46–58
32. Orom UA, Shiekhattar R (2011) Noncoding RNAs and enhancers: complications of a long-distance relationship. Trends Genet 27: 433–439
33. Lefevre P, Witham J, Lacroix CE, Cockerill PN, Bonifer C (2008) The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription. Mol Cell 32: 129–139
34. Bumgarner SL, Dowell RD, Grisafi P, Gifford DK, Fink GR (2009) Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. Proc Natl Acad Sci USA 106: 18321–18326
35. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP (2010) Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3: ra8
36. Beltran M, Puig I, Pena C, Garcia JM, Alvarez AB, Pena R, Bonilla F, de Herreros AG (2008) A natural antisense transcript regulates Zeb2/Sip1 gene expression during Snail1-induced epithelial-mesenchymal transition. Genes Dev 22: 756–769
37. Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE, Finch CE, St Laurent G III, Kenny PJ, Wahlestedt C (2008) Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat Med 14: 723–730
38. Wang Y, Xu Z, Jiang J, Xu C, Kang J, Xiao L, Wu M, Xiong J, Guo X, Liu H (2013) Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal. Dev Cell 25: 69–80
39. Cao S, Han J, Wu J, Li Q, Liu S, Zhang W, Pei Y, Ruan X, Liu Z, Wang X (2014) Specific gene-regulation networks during the pre-implantation development of the pig embryo as revealed by deep sequencing. BMC Genom 15: 4
40. Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G (2010) A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 19: 625–638
41. van Attikum H, Gasser SM (2009) Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol 19: 207–217
42. Minami N, Suzuki T, Tsukamoto S (2007) Zygotic gene activation and maternal factors in mammals. J Reprod Dev 53: 707–715
43. Chu DP, Tian S, Qi L, Hao CJ, Xia HF, Ma X (2013) Abnormality of maternal-to-embryonic transition contributes to MEHP-induced mouse 2-cell block. J Cell Physiol 228: 753–763
44. Qiu JJ, Zhang WW, Wu ZL, Wang YH, Qian M, Li YP (2003) Delay of ZGA initiation occurred in 2-cell blocked mouse embryos. Cell Res 13: 179–185
45. Maekawa M, Yamamoto T, Kohno M, Takeichi M, Nishida E (2007) Requirement for ERK MAP kinase in mouse preimplantation development. Development 134: 2751–2759
46. Ranpura SA, Deshmukh U, Reddi PP (2008) NF45 and NF90 in murine seminiferous epithelium: potential role in SP-10 gene transcription. J Androl 29: 186–197
47. Kiesler P, Haynes PA, Shi L, Kao PN, Wysocki VH, Vercelli D (2010) NF45 and NF90 regulate HS4-dependent interleukin-13 transcription in T cells. J Biol Chem 285: 8256–8267
48. Zhao G, Shi L, Qiu D, Hu H, Kao PN (2005) NF45/ILF2 tissue expression, promoter analysis, and interleukin-2 transactivating function. Exp Cell Res 305: 312–323
49. Bi HS, Yang XY, Yuan JH, Yang F, Xu D, Guo YJ, Zhang L, Zhou CC, Wang F, Sun SH (2013) H19 inhibits RNA polymerase II-mediated transcription by disrupting the hnRNP U-actin complex. Biochim Biophys Acta 1830: 4899–4906
50. Vizlin-Hodzic D, Johansson H, Ryme J, Simonsson T, Simonsson S (2011) SAF-A has a role in transcriptional regulation of Oct4 in ES cells through promoter binding. Cell Reprogram 13: 13–27
51. Vizlin-Hodzic D, Runnberg R, Ryme J, Simonsson S, Simonsson T (2011) SAF-A forms a complex with BRG1 and both components are required for RNA polymerase II mediated transcription. PLoS ONE 6: e28049
52. Zhao J, Ding J, Li Y, Ren K, Sha J, Zhu M, Gao X (2009) HnRNP U mediates the long-range regulation of Shh expression during limb development. Hum Mol Genet 18: 3090–3097
53. Rabenhorst U, Thalheimer FB, Gerlach K, Kijonka M, Bohm S, Krause DS, Vauti F, Arnold HH, Schroeder T, Schnutgen F (2015) Single-stranded DNA-binding transcriptional regulator FUBP1 Is essential for fetal and adult hematopoietic stem cell self-renewal. Cell Rep 11: 1847–1855
54. Vu NT, Park MA, Shultz JC, Goehe RW, Hoeferlin LA, Shultz MD, Smith SA, Lynch KW, Chalfant CE (2013) hnRNP U enhances caspase-9 splicing and is modulated by AKT-dependent phosphorylation of hnRNP L. J Biol Chem 288: 8575–8584
55. Xiao R, Tang P, Yang B, Huang J, Zhou Y, Shao C, Li H, Sun H, Zhang Y, Fu XD (2012) Nuclear matrix factor hnRNP U/SAF-A exerts a global control of alternative splicing by regulating U2 snRNP maturation. Mol Cell 45: 656–668
56. Obrdlik A, Kukalev A, Louvet E, Ostlund Farrants AK, Caputo L, Percipalle P (2008) The histone acetyltransferase PCAF associates with actin and hnRNP U for RNA polymerase II transcription. Mol Cell Biol 28: 6342–6357
57. Rigo F, Hua Y, Chun SJ, Prakash TP, Krainer AR, Bennett CF (2012) Synthetic oligonucleotides recruit ILF2/3 to RNA transcripts to modulate splicing. Nat Chem Biol 8: 555–561
58. Jacob AG, Singh RK, Mohammad F, Bebee TW, Chandler DS (2014) The splicing factor FUBP1 is required for the efficient splicing of oncogene MDM2 pre-mRNA. J Biol Chem 289: 17350–17364
59. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39: 925–938
60. Lai F, Orom UA, Cesaroni M, Beringer M, Taatjes DJ, Blobel GA, Shiekhattar R (2013) Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature 494: 497–501
61. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J, Wei CL, Natoli G (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8: e1000384
62. Pi W, Zhu X, Wu M, Wang Y, Fulzele S, Eroglu A, Ling J, Tuan D (2010) Long-range function of an intergenic retrotransposon. Proc Natl Acad Sci USA 107: 12992–12997
63. Li J, Akagi K, Hu Y, Trivett AL, Hlynialuk CJ, Swing DA, Volfovsky N, Morgan TC, Golubeva Y, Stephens RM (2012) Mouse endogenous retroviruses can trigger premature transcriptional termination at a distance. Genome Res 22: 870–884
64. Yan L, Yang M, Guo H, Yang L, Wu J, Li R, Liu P, Lian Y, Zheng X, Yan J (2013) Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 20: 1131–1139
65. Shen S, Park JW, Lu ZX, Lin L, Henry MD, Wu YN, Zhou Q, Xing Y (2014) rMATS: robust and flexible detection of differential alternative splicing from replicate RNA-Seq data. Proc Natl Acad Sci USA 111: E5593–E5601
66. Wee CD, Havens MA, Jodelka FM, Hastings ML (2014) Targeting SR proteins improves SMN expression in spinal muscular atrophy cells. PLoS ONE 9: e115205
67. Miro J, Laaref AM, Rofidal V, Lagrafeuille R, Hem S, Thorel D, Mechin D, Mamchaoui K, Mouly V, Claustres M (2015) FUBP1: a new protagonist in splicing regulation of the DMD gene. Nucleic Acids Res 43: 2378–2389
68. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, Swift S, Rastan S (1992) The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 71: 515–526
69. Brown CJ, Hendrich BD, Rupert JL, Lafreniere RG, Xing Y, Lawrence J, Willard HF (1992) The human xist gene – analysis of a 17 Kb inactive X-specific Rna that contains conserved repeats and is highly localized within the nucleus. Cell 71: 527–542
70. Wu SC, Zhang Y (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11: 607–620
71. Papaioannou VE (1982) Lineage analysis of inner cell mass and trophectoderm using microsurgically reconstituted mouse blastocysts. J Embryol Exp Morphol 68: 199–209
72. Hamazaki N, Uesaka M, Nakashima K, Agata K, Imamura T (2015) Gene activation-associated long noncoding RNAs function in mouse preimplantation development. Development 142: 910–920
73. Bernard D, Prasanth KV, Tripathi V, Colasse S, Nakamura T, Xuan Z, Zhang MQ, Sedel F, Jourdren L, Coulpier F (2010) A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J 29: 3082–3093
74. Ciarlo E, Massone S, Penna I, Nizzari M, Gigoni A, Dieci G, Russo C, Florio T, Cancedda R, Pagano A (2013) An intronic ncRNA-dependent regulation of SORL1 expression affecting Abeta formation is upregulated in post-mortem Alzheimer's disease brain samples. Dis Model Mech 6: 424–433
75. Duncan R, Bazar L, Michelotti G, Tomonaga T, Krutzsch H, Avigan M, Levens D (1994) Sequence-specific, single-strand binding-protein activates the far upstream element of C-Myc and defines a new DNA-binding motif. Genes Dev 8: 465–480
76. Zhang F, Tian Q, Wang Y (2013) Far upstream element-binding protein 1 (FUBP1) is overexpressed in human gastric cancer tissue compared to non-cancerous tissue. Onkologie 36: 650–655
77. Shamanna RA, Hoque M, Pe'ery T, Mathews MB (2013) Induction of p53, p21 and apoptosis by silencing the NF90/NF45 complex in human papilloma virus-transformed cervical carcinoma cells. Oncogene 32: 5176–5185
78. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628
79. Huang S, Zhang J, Li R, Zhang W, He Z, Lam TW, Peng Z, Yiu SM (2011) SOAPsplice: genome-Wide ab initio detection of splice junctions from RNA-Seq data. Front Genet 2: 46
80. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111
81. Au KF, Jiang H, Lin L, Xing Y, Wong WH (2010) Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic Acids Res 38: 4570–4578
82. Wang K, Singh D, Zeng Z, Coleman SJ, Huang Y, Savich GL, He X, Mieczkowski P, Grimm SA, Perou CM (2010) MapSplice: accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Res 38: e178
83. Li H, Ruan J, Durbin R (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851–1858