Diverse phenotypes and specific transcription patterns in twenty mouse lines with ablated lincRNAs

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Lai, Ka Man Venus ^a   Gong, Guochun ^a   Atanasio, Amanda ^a   Rojas, José ^a   Quispe, Joseph ^a   Posca, Julita ^a   White, Derek ^a   Huang, Mei ^a   Fedorova, Daria ^a   Grant, Craig ^a   Miloscio, Lawrence ^a   Droguett, Gustavo ^a   Poueymirou, William T ^a   Auerbach, Wojtek ^a   Yancopoulos, George D ^a   Frendewey, David ^a   Rinn, John ^b,c   Valenzuela, David M ^a  

^a REGENERON PHARMACEUTICALS INC   (United States)

^b Harvard University   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; CARRIER PROTEIN; LACTOSE PERMEASE; TRANSCRIPTOME;

ADULT; ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTOLOGY; HOMEOSTASIS; KNOCKOUT MOUSE; LUNG; MICRO-COMPUTED TOMOGRAPHY; MORPHOLOGY; MOUSE; MUSCLE; MUTANT; NONHUMAN; PHENOTYPE; PREMATURE AGING; SKELETON; TAIL SUSPENSION TEST; ANIMAL; C57BL MOUSE; FEMALE; GENETICS; MALE; MAMMAL; REPORTER GENE;

MAMMALIA;

ALLELES; ANIMALS; EMBRYONIC DEVELOPMENT; FEMALE; GENES, REPORTER; MALE; MAMMALS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; RNA, LONG NONCODING; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84929379150     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125522     Document Type: Article

References (42)

1. Mattick JS. The genetic signatures of noncoding RNAs. PLoS Genet 2009; 5: e1000459. doi: 10.1371/journal.pgen.1000459 PMID: 19390609
2. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, et al. The transcriptional landscape of the mammalian genome. Science. 2005; 309: 1559-1563. PMID: 16141072
3. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, et al. Landscape of transcription in human cells. Nature. 2012; 489: 101-108. doi: 10.1038/nature11233 PMID: 22955620
4. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science. 2007; 316: 1484-1488. PMID: 17510325
5. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012; 22: 1775-1789. doi: 10.1101/gr.132159.111 PMID: 22955988
6. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009; 458: 223-227. doi: 10.1038/nature07672 PMID: 19182780
7. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A. 2009; 106: 11667-11672. doi: 10.1073/pnas.0904715106 PMID: 19571010
8. Capecchi MR. Generating mice with targeted mutations. Nat Med. 2001; 7: 1086-1090. PMID: 11590420
9. Evans MJ. The cultural mouse. Nat Med. 2001; 7: 1081-1083. PMID: 11590418
10. Smithies O. Forty years with homologous recombination. Nat Med. 2001; 7: 1083-1086. PMID: 11590419
11. Prosser HM, Koike-Yusa H, Cooper JD, Law FC, Bradley A. A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat Biotechnol. 2011; 29: 840-845. doi: 10.1038/nbt.1929 PMID: 21822254
12. Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev. 1997; 11: 156-166. PMID: 9009199
13. Sado T, Wang Z, Sasaki H, Li E. Regulation of imprinted X-chromosome inactivation in mice by Tsix. Development. 2001; 128: 1275-1286. PMID: 11262229
14. Leighton PA, Ingram RS, Eggenschwiler J, Efstratiadis A, Tilghman SM. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature. 1995; 375: 34-39. PMID: 7536897
15. Mohammad F, Mondal T, Guseva N, Pandey GK, Kanduri C. Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development. 2010; 137: 2493-2499. doi: 10.1242/dev.048181 PMID: 20573698
16. Sleutels F, Zwart R, Barlow DP. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature. 2002; 415: 810-813. PMID: 11845212
17. Takahashi N, Okamoto A, Kobayashi R, Shirai M, Obata Y, Ogawa H, et al. Deletion of Gtl2, imprinted non-coding RNA, with its differentially methylated region induces lethal parent-origin-dependent defects in mice. Hum Mol Genet 2009; 18: 1879-1888. doi: 10.1093/hmg/ddp108 PMID: 19264764
18. Grote P, Wittler L, Hendrix D, Koch F, Wahrisch S, Beisaw A, et al. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell. 2013; 24: 206-214. doi: 10.1016/j.devcel.2012.12.012 PMID: 23369715
19. Zambrowicz BP, Imamoto A, Fiering S, Herzenberg LA, Kerr WG, Soriano P. Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc Natl Acad Sci U S A 1997; 94: 3789-3794. PMID: 9108056
20. Zhang B, Arun G, Mao YS, Lazar Z, Hung G, Bhattacharjee G, et al. The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2012; 2: 111-123. doi: 10.1016/j.celrep.2012.06.003 PMID: 22840402
21. Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, et al. Regulation of the germinal center response by microRNA-155. Science. 2007; 316: 604-608. PMID: 17463289
22. Valenzuela DM, Murphy AJ, Frendewey D, Gale NW, Economides AN, Auerbach W, et al. Highthroughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat Biotechnol. 2003; 21: 652-659. PMID: 12730667
23. Adams DJ, Quail MA, Cox T, van der Weyden L, Gorick BD, Su Q, et al. A genome-wide, end-sequenced 129Sv BAC library resource for targeting vector construction. Genomics. 2005; 86: 753-758. PMID: 16257172
24. Frendewey D, Chernomorsky R, Esau L, Om J, Xue Y, Murphy AJ, et al. The loss-of-allele assay for ES cell screening and mouse genotyping. Methods Enzymol. 2010; 476: 295-307. doi: 10.1016/S0076-6879(10)76017-1 PMID: 20691873
25. Dechiara TM, Poueymirou WT, Auerbach W, Frendewey D, Yancopoulos GD, Valenzuela DM. Veloci-Mouse: fully ES cell-derived F0-generation mice obtained from the injection of ES cells into eight-cell-stage embryos. Methods Mol Biol. 2009; 530: 311-324. doi: 10.1007/978-1-59745-471-1-16 PMID: 19266341
26. DeChiara TM, Poueymirou WT, Auerbach W, Frendewey D, Yancopoulos GD, Valenzuela DM. Producing fully ES cell-derived mice from eight-cell stage embryo injections. Methods Enzymol. 2010; 476: 285-294. doi: 10.1016/S0076-6879(10)76016-X PMID: 20691872
27. Poueymirou WT, Auerbach W, Frendewey D, Hickey JF, Escaravage JM, Esau L, et al. F0 generation mice fully derived from gene-targeted embryonic stem cells allowing immediate phenotypic analyses. Nat Biotechnol. 2007; 25: 91-99. PMID: 17187059
28. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011; 25: 1915-1927. doi: 10.1101/gad.17446611 PMID: 21890647
29. Sauvageau M, Goff LA, Lodato S, Bonev B, Groff AF, Gerhardinger C, et al. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife (Cambridge). 2013; 2: e01749. doi: 10.7554/eLife.01749 PMID: 24381249
30. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010; 329: 689-693. doi: 10.1126/science.1192002 PMID: 20616235
31. Kozak M. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 1987; 15: 8125-8148. PMID: 3313277
32. Hostikka SL, Capecchi MR. The mouse Hoxc11 gene: genomic structure and expression pattern. Mech Dev. 1998; 70: 133-145. PMID: 9510030
33. Lu P, Yu Y, Perdue Y, Werb Z. The apical ectodermal ridge is a timer for generating distal limb progenitors. Development. 2008; 135: 1395-1405. doi: 10.1242/dev.018945 PMID: 18359901
34. Schorderet P, Duboule D. Structural and functional differences in the long non-coding RNA hotair in mouse and human. PLoS Genet. 2011; 7: e1002071. doi: 10.1371/journal.pgen.1002071 PMID: 21637793
35. Nagy A. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2003.
36. Dimri G, Lee X, Basile G, Acosta M, Scott G, Roskelley C, et al. A biomarker that identifies sensescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995; 92: 9363-9367. PMID: 7568133
37. Carpenter S, Aiello D, Atianand MK, Ricci EP, Gandhi P, Hall LL, et al. A long noncoding RNA mediates both activation and repression of immune response genes. Science. 2013; 341: 789-792. doi: 10.1126/science.1240925 PMID: 23907535
38. Li L, Liu B, Wapinski OL, Tsai MC, Qu K, Zhang J, et al. Targeted disruption of Hotair leads to homeotic transformation and gene derepression. Cell Rep. 2013; 5: 3-12. doi: 10.1016/j.celrep.2013.09.003 PMID: 24075995
39. Bishop NB, Stankiewicz P, Steinhorn RH. Alveolar capillary dysplasia. Am J Respir Crit Care Med. 2011; 184: 172-179. doi: 10.1164/rccm.201010-1697CI PMID: 21471096
40. Szafranski P, Dharmadhikari AV, Brosens E, Gurha P, Kolodziejska KE, Zhishuo O, et al. Small noncoding differentially methylated copy-number variants, including lncRNA genes, cause a lethal lung developmental disorder. Genome Res. 2013; 23: 23-33. doi: 10.1101/gr.141887.112 PMID: 23034409
41. Marin-Bejar O, Marchese FP, Athie A, Sanchez Y, Gonzalez J, Segura V, et al. Pint lincRNA connects the p53 pathway with epigenetic silencing by the Polycomb repressive complex 2. Genome Biol. 2013; 14: R104. PMID: 24070194
42. Rufini A, Tucci P, Celardo I, Melino G. Senescence and aging: the critical roles of p53. Oncogene. 2013; 32: 5129-5143. doi: 10.1038/onc.2012.640 PMID: 23416979