Minor introns are embedded molecular switches regulated by highly unstable U6atac snRNA

eLife

Volumn 2013, Issue 2, 2013, Pages

  Younis, Ihab ^a   Dittmar, Kimberly ^a   Wang, Wei ^b   Foley, Shawn W ^a   Berg, Michael G ^a   Hu, Karen Y ^a   Wei, Zhi ^b   Wan, Lili ^a   Dreyfuss, Gideon ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b University Heights   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5, 6 DICHLOROBENZIMIDAZOLE RIBOSIDE; ANISOMYCIN; CYCLOHEXIMIDE; DACTINOMYCIN; DNA DIRECTED RNA POLYMERASE III; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NOCODAZOLE; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; RIBONUCLEASE H; RIBOSOME RNA; RNA POLYMERASE II; SMALL NUCLEAR RNA; SMALL NUCLEOLAR RNA; TRANSCRIPTOME; TRANSFER RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; PRIMER DNA;

ARTICLE; CELLULAR STRESS SIGNAL; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE SWITCHING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTRON; MICROARRAY ANALYSIS; MOLECULAR HYBRIDIZATION; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; RNA SPLICING; RNA TRANSLATION; SIGNAL TRANSDUCTION; SPLICEOSOME; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; UPREGULATION;

BASE SEQUENCE; DNA PRIMERS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; INTRONS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REAL-TIME POLYMERASE CHAIN REACTION; RNA SPLICING; RNA, SMALL NUCLEAR; UP-REGULATION;

EID: 84881083550     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00780     Document Type: Article

References (47)

1. Abdel-Salam GM, Miyake N, Eid MM, Abdel-Hamid MS, Hassan NA, Eid OM, et al. 2011. A homozygous mutation in RNU4ATAC as a cause of microcephalic osteodysplastic primordial dwarfism type I (MOPD I) with associated pigmentary disorder. Am J Med Genet A 155A:2885-96. doi: 10.1002/ajmg.a.34299.
2. Alimonti A, Carracedo A, Clohessy JG, Trotman LC, Nardella C, Egia A, et al. 2010. Subtle variations in Pten dose determine cancer susceptibility. Nat Genet 42:454-8. doi: 10.1038/ng.556.
3. Alioto TS. 2007. U12DB: a database of orthologous U12-type spliceosomal introns. Nucleic Acids Res 35:D110-5. doi: 10.1093/nar/gkl796.
4. Bartschat S, Samuelsson T. 2010. U12 type introns were lost at multiple occasions during evolution. BMC Genomics 11:106. doi: 10.1186/1471-2164-11-106.
5. Basu MK, Makalowski W, Rogozin IB, Koonin EV. 2008. U12 intron positions are more strongly conserved between animals and plants than U2 intron positions. Biol Direct 3:19. doi: 10.1186/1745-6150-3-19.
6. Berg MG, Singh LN, Younis I, Liu Q, Pinto AM, Kaida D, et al. 2012. U1 snRNP determines mRNA length and regulates isoform expression. Cell 150:53-64. doi: 10.1016/j.cell.2012.05.029.
7. Bunyard P, Handley M, Pollara G, Rutault K, Wood I, Chaudry M, et al. 2003. Ribotoxic stress activates p38 and JNK kinases and modulates the antigen-presenting activity of dendritic cells. Mol Immunol 39:815-27. doi: 10.1016/S0161-5890(02)00262-6.
8. Burge CB, Padgett RA, Sharp PA. 1998. Evolutionary fates and origins of U12-type introns. Mol Cell 2:773-85. doi: 10.1016/S1097-2765(00)80292-0.
9. Chang JH, Park JY, Kim SK. 2006. Dependence on p38 MAPK signalling in the up-regulation of TLR2, TLR4 and TLR9 gene expression in Trichomonas vaginalis-treated HeLa cells. Immunology 118:164-70. doi: 10.1111/j.1365-2567.2006.02347.x.
10. Davies SP, Reddy H, Caivano M, Cohen P. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105. doi: 10.1042/0264-6021:3510095.
11. Davison TS, Johnson CD, Andruss BF. 2006. Analyzing micro-RNA expression using microarrays. Methods Enzymol 411:14-34. doi: 10.1016/S0076-6879(06)11002-2.
12. Dolken L, Ruzsics Z, Radle B, Friedel CC, Zimmer R, Mages J, et al. 2008. High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 14:1959-72. doi: 10.1261/rna.1136108.
13. Edery P, Marcaillou C, Sahbatou M, Labalme A, Chastang J, Touraine R, et al. 2011. Association of TALS developmental disorder with defect in minor splicing component U4atac snRNA. Science 332:240-3. doi: 10.1126/science.1202205.
14. Furgeson SB, Simpson PA, Park I, Vanputten V, Horita H, Kontos CD, et al. 2010. Inactivation of the tumour suppressor, PTEN, in smooth muscle promotes a pro-inflammatory phenotype and enhances neointima formation. Cardiovasc Res 86:274-82. doi: 10.1093/cvr/cvp425.
15. Furumoto Y, Brooks S, Olivera A, Takagi Y, Miyagishi M, Taira K, et al. 2006. Cutting Edge: Lentiviral short hairpin RNA silencing of PTEN in human mast cells reveals constitutive signals that promote cytokine secretion and cell survival. J Immunol 176:5167-71.
16. Fury MG, Zieve GW. 1996. U6 snRNA maturation and stability. Exp Cell Res 228:160-3. doi: 10.1006/excr.1996.0311.
17. Hall SL, Padgett RA. 1996. Requirement of U12 snRNA for in vivo splicing of a minor class of eukaryotic nuclear pre-mRNA introns. Science 271:1716-8. doi: 10.1126/science.271.5256.1716.
18. He H, Liyanarachchi S, Akagi K, Nagy R, Li J, Dietrich RC, et al. 2011. Mutations in U4atac snRNA, a component of the minor spliceosome, in the developmental disorder MOPD I. Science 332:238-40. doi: 10.1126/science.1200587.
19. Heo YS, Kim SK, Seo CI, Kim YK, Sung BJ, Lee HS, et al. 2004. Structural basis for the selective inhibition of JNK1 by the scaffolding protein JIP1 and SP600125. EMBO J 23:2185-95. doi: 10.1038/sj.emboj.7600212.
20. Hiley SL, Jackman J, Babak T, Trochesset M, Morris QD, Phizicky E, et al. 2005. Detection and discovery of RNA modifications using microarrays. Nucleic Acids Res 33:e2. doi: 10.1093/nar/gni002.
21. Kaida D, Berg MG, Younis I, Kasim M, Singh LN, Wan L, et al. 2010. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468:664-8. doi: 10.1038/nature09479.
22. Katz Y, Wang ET, Airoldi EM, Burge CB. 2010. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat Methods 7:1009-15. doi: 10.1038/nmeth.1528.
23. Kickhoefer VA, Liu Y, Kong LB, Snow BE, Stewart PL, Harrington L, et al. 2001. The Telomerase/vault-associated protein TEP1 is required for vault RNA stability and its association with the vault particle. J Cell Biol 152:157-64. doi: 10.1083/jcb.152.1.157.
24. Konig H, Matter N, Bader R, Thiele W, Muller F. 2007. Splicing segregation: the minor spliceosome acts outside the nucleus and controls cell proliferation. Cell 131:718-29. doi: 10.1016/j.cell.2007.09.043.
25. Listerman I, Bledau AS, Grishina I, Neugebauer KM. 2007. Extragenic accumulation of RNA polymerase II enhances transcription by RNA polymerase III. PLOS Genet 3:e212. doi: 10.1371/journal.pgen.0030212.
26. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621-8. doi: 10.1038/nmeth.1226.
27. Otake LR, Scamborova P, Hashimoto C, Steitz JA. 2002. The divergent U12-type spliceosome is required for pre-mRNA splicing and is essential for development in Drosophila. Mol Cell 9:439-46. doi: 10.1016/S1097-2765(02)00441-0.
28. Patel AA, McCarthy M, Steitz JA. 2002. The splicing of U12-type introns can be a rate-limiting step in gene expression. EMBO J 21:3804-15. doi: 10.1093/emboj/cdf297.
29. Patel AA, Steitz JA. 2003. Splicing double: insights from the second spliceosome. Nat Rev Mol Cell Biol 4:960-70. doi: 10.1038/nrm1259.
30. Qian J, Ling S, Castillo AC, Long B, Birnbaum Y, Ye Y. 2012. Regulation of phosphatase and tensin homolog on chromosome 10 in response to hypoxia. Am J Physiol Heart Circ Physiol 302:H1806-17. doi: 10.1152/ajpheart.00929.2011.
31. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-2. doi: 10.1093/bioinformatics/btq033.
32. Russell AG, Charette JM, Spencer DF, Gray MW. 2006. An early evolutionary origin for the minor spliceosome. Nature 443:863-6. doi: 10.1038/nature05228.
33. Scamborova P, Wong A, Steitz JA. 2004. An intronic enhancer regulates splicing of the twintron of Drosophila melanogaster prospero pre-mRNA by two different spliceosomes. Mol Cell Biol 24:1855-69. doi: 10.1128/MCB.24.5.1855-1869.2004.
34. Shen YH, Zhang L, Gan Y, Wang X, Wang J, LeMaire SA, et al. 2006. Up-regulation of PTEN (phosphatase and tensin homolog deleted on chromosome ten) mediates p38 MAPK stress signal-induced inhibition of insulin signaling. A cross-talk between stress signaling and insulin signaling in resistin-treated human endothelial cells. J Biol Chem 281:7727-36. doi: 10.1074/jbc.M511105200.
35. Sheth N, Roca X, Hastings ML, Roeder T, Krainer AR, Sachidanandam R. 2006. Comprehensive splice-site analysis using comparative genomics. Nucleic Acids Res 34:3955-67. doi: 10.1093/nar/gkl556.
36. Shukla GC, Padgett RA. 1999. Conservation of functional features of U6atac and U12 snRNAs between vertebrates and higher plants. RNA 5:525-38. doi: 10.1017/S1355838299982213.
37. Singh J, Padgett RA. 2009. Rates of in situ transcription and splicing in large human genes. Nat Struct Mol Biol 16:1128-33. doi: 10.1038/nsmb.1666.
38. Tamguney T, Stokoe D. 2007. New insights into PTEN. J Cell Sci 120:4071-9. doi: 10.1242/jcs.015230.
39. Tarn WY, Steitz JA. 1996. A novel spliceosome containing U11, U12, and U5 snRNPs excises a minor class (AT-AC) intron in vitro. Cell 84:801-11. doi: 10.1016/S0092-8674(00)81057-0.
40. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-11. doi: 10.1093/bioinformatics/btp120.
41. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562-78. doi: 10.1038/nprot.2012.016.
42. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511-5. doi: 10.1038/nbt.1621.
43. Turunen JJ, Niemela EH, Verma B, Frilander MJ. 2012. The significant other: splicing by the minor spliceosome. Wiley Interdiscip Rev RNA 4:61-76. doi: 10.1002/wrna.1141.
44. Wahl MC, Will CL, Luhrmann R. 2009. The spliceosome: design principles of a dynamic RNP machine. Cell 136:701-18. doi: 10.1016/j.cell.2009.02.009.
45. Yong J, Kasim M, Bachorik JL, Wan L, Dreyfuss G. 2010. Gemin5 delivers snRNA precursors to the SMN complex for snRNP biogenesis. Mol Cell 38:551-62. doi: 10.1016/j.molcel.2010.03.014.
46. Younis I, Berg M, Kaida D, Dittmar K, Wang C, Dreyfuss G. 2010. Rapid-response splicing reporter screens identify differential regulators of constitutive and alternative splicing. Mol Cell Biol 30:1718-28. doi: 10.1128/MCB.01301-09.
47. Zhang Z, Lotti F, Dittmar K, Younis I, Wan L, Kasim M, et al. 2008. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 133:585-600. doi: 10.1016/j.cell.2008.03.031.