Ultraconserved cDNA segments in the human transcriptome exhibit resistance to folding and implicate function in translation and alternative splicing

Nucleic Acids Research

Volumn 39, Issue 6, 2011, Pages 1967-1979

  Sathirapongsasuti, J Fah ^a,b,c   Sathira, Nuankanya ^a   Suzuki, Yutaka ^a   Huttenhower, Curtis ^c   Sugano, Sumio ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b STANFORD UNIVERSITY   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA; TRANSCRIPTOME;

5' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; EXON; EXPRESSED SEQUENCE TAG; GENE SILENCING; GENETIC CONSERVATION; HUMAN; HUMAN CELL; NONSENSE MEDIATED MRNA DECAY; OPEN READING FRAME; ORTHOLOGY; PRIORITY JOURNAL; RNA DEGRADATION; RNA SECONDARY STRUCTURE; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; SEQUENCE ALIGNMENT; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

5' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; CODON, INITIATOR; CODON, NONSENSE; CONSERVED SEQUENCE; DISEASE; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MICE; MICRORNAS; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RATS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS;

MAMMALIA; RATTUS; RODENTIA;

EID: 79953712632     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq949     Document Type: Article

References (62)

1. Boffelli,D., Nobrega,M.A. and Rubin,E.M. (2004) Comparative genomics at the vertebrate extremes. Nat. Rev. Genet., 5, 456-465.
2. Dermitzakis,E.T., Reymond,A. and Antonarakis,S.E. (2005) Conserved non-genic sequences - an unexpected feature of mammalian genomes. Nat. Rev. Genet., 6, 151-157.
3. Waterston,R.H., Lindblad-Toh,K., Birney,E., Rogers,J., Abril,J.F., Agarwal,P., Agarwala,R., Ainscough,R., Alexandersson,M., An,P. et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature, 420, 520-562.
4. Bejerano,G., Pheasant,M., Makunin,I., Stephen,S., Kent,W.J., Mattick,J.S. and Haussler,D. (2004) Ultraconserved elements in the human genome. Science, 304, 1321-1325. (Pubitemid 38697428)
5. Sakuraba,Y., Kimura,T., Masuya,H., Noguchi,H., Sezutsu,H., Takahasi,K.R., Toyoda,A., Fukumura,R., Murata,T., Sakaki,Y. et al. (2008) Identification and characterization of new long conserved noncoding sequences in vertebrates. Mamm. Genome, 19, 703-712.
6. Thomas,J.W., Touchman,J.W., Blakesley,R.W., Bouffard,G.G., Beckstrom-Sternberg,S.M., Margulies,E.H., Blanchette,M., Siepel,A.C., Thomas,P.J., McDowell,J.C. et al. (2003) Comparative analyses of multi-species sequences from targeted genomic regions. Nature, 424, 788-793. (Pubitemid 37021709)
7. Duret,L., Dorkeld,F. and Gautier,C. (1993) Strong conservation of non-coding sequences during vertebrates evolution: potential involvement in post-transcriptional regulation of gene expression. Nucleic Acids Res., 21, 2315-2322. (Pubitemid 23180805)
8. Calin,G.A., Liu,C.G., Ferracin,M., Hyslop,T., Spizzo,R., Sevignani,C., Fabbri,M., Cimmino,A., Lee,E.J., Wojcik,S.E. et al. (2007) Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer Cell, 12, 215-229. (Pubitemid 47333418)
9. Paparidis,Z., Abbasi,A.A., Malik,S., Goode,D.K., Callaway,H., Elgar,G., deGraaff,E., Lopez-Rios,J., Zeller,R. and Grzeschik,K.H. (2007) Ultraconserved non-coding sequence element controls a subset of spatiotemporal GLI3 expression. Dev. Growth Differ., 49, 543-553.
10. Pennacchio,L.A., Ahituv,N., Moses,A.M., Prabhakar,S., Nobrega,M.A., Shoukry,M., Minovitsky,S., Dubchak,I., Holt,A., Lewis,K.D. et al. (2006) In vivo enhancer analysis of human conserved non-coding sequences. Nature, 444, 499-502.
11. Lareau,L.F., Inada,M., Green,R.E., Wengrod,J.C. and Brenner,S.E. (2007) Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature, 446, 926-929. (Pubitemid 46633161)
12. Ni,J.Z., Grate,L., Donohue,J.P., Preston,C., Nobida,N., O'Brien,G., Shiue,L., Clark,T.A., Blume,J.E. and Ares,M. Jr (2007) Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev., 21, 708-718. (Pubitemid 46440292)
13. Feng,J., Bi,C., Clark,B.S., Mady,R., Shah,P. and Kohtz,J.D. (2006) The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev., 20, 1470-1484. (Pubitemid 43830654)
14. Nobrega,M.A., Ovcharenko,I., Afzal,V. and Rubin,E.M. (2003) Scanning human gene deserts for long-range enhancers. Science, 302, 413. (Pubitemid 37296259)
15. Ota,T., Suzuki,Y., Nishikawa,T., Otsuki,T., Sugiyama,T., Irie,R., Wakamatsu,A., Hayashi,K., Sato,H., Nagai,K. et al. (2004) Complete sequencing and characterization of 21,243 full-length human cDNAs. Nat. Genet., 36, 40-45.
16. Suzuki,Y. and Sugano,S. (2003) Construction of a full-length enriched and a 5′-end enriched cDNA library using the oligo-capping method. Methods Mol. Biol., 221, 73-91.
17. Blanchette,M., Kent,W.J., Riemer,C., Elnitski,L., Smit,A.F., Roskin,K.M., Baertsch,R., Rosenbloom,K., Clawson,H., Green,E.D. et al. (2004) Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res., 14, 708-715. (Pubitemid 38500244)
18. Giardine,B., Riemer,C., Hardison,R.C., Burhans,R., Elnitski,L., Shah,P., Zhang,Y., Blankenberg,D., Albert,I., Taylor,J. et al. (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res., 15, 1451-1455. (Pubitemid 41400913)
19. Wakaguri,H., Yamashita,R., Suzuki,Y., Sugano,S. and Nakai,K. (2008) DBTSS: database of transcription start sites, progress report 2008. Nucleic Acids Res., 36, D97-D101. (Pubitemid 351149703)
20. Mortazavi,A., Williams,B.A., McCue,K., Schaeffer,L. and Wold,B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621-628.
21. Wang,E.T., Sandberg,R., Luo,S., Khrebtukova,I., Zhang,L., Mayr,C., Kingsmore,S.F., Schroth,G.P. and Burge,C.B. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature, 456, 470-476. (Pubitemid 352759009)
22. Karolchik,D., Kuhn,R.M., Baertsch,R., Barber,G.P., Clawson,H., Diekhans,M., Giardine,B., Harte,R.A., Hinrichs,A.S., Hsu,F. et al. (2008) The UCSC Genome Browser Database: 2008 update. Nucleic Acids Res., 36, D773-D779. (Pubitemid 351149822)
23. Huang da,W., Sherman,B.T. and Lempicki,R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
24. Matlin,A.J., Clark,F. and Smith,C.W. (2005) Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol., 6, 386-398.
25. Zuker,M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
26. Suzuki,Y., Ishihara,D., Sasaki,M., Nakagawa,H., Hata,H., Tsunoda,T., Watanabe,M., Komatsu,T., Ota,T., Isogai,T. et al. (2000) Statistical analysis of the 5′ untranslated region of human mRNA using "Oligo-Capped" cDNA libraries. Genomics, 64, 286-297.
27. Griffiths-Jones,S., Saini,H.K., van Dongen,S. and Enright,A.J. (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res., 36, D154-D158.
28. Smith,C.W. and Valcarcel,J. (2000) Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem. Sci., 25, 381-388.
29. Black,D.L. (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem., 72, 291-336.
30. Caceres,J.F. and Kornblihtt,A.R. (2002) Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet., 18, 186-193. (Pubitemid 34273739)
31. Martinez-Contreras,R., Cloutier,P., Shkreta,L., Fisette,J.F., Revil,T. and Chabot,B. (2007) hnRNP proteins and splicing control. Adv. Exp. Med. Biol., 623, 123-147.
32. Parmley,J.L., Chamary,J.V. and Hurst,L.D. (2006) Evidence for purifying selection against synonymous mutations in mammalian exonic splicing enhancers. Mol. Biol. Evol., 23, 301-309.
33. Kim,E., Goren,A. and Ast,G. (2008) Alternative splicing: current perspectives. Bioessays, 30, 38-47.
34. Lewis,B.P., Green,R.E. and Brenner,S.E. (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl Acad. Sci. USA, 100, 189-192.
35. Baek,D. and Green,P. (2005) Sequence conservation, relative isoform frequencies, and nonsense-mediated decay in evolutionarily conserved alternative splicing. Proc. Natl Acad. Sci. USA, 102, 12813-12818.
36. Shepard,P.J. and Hertel,K.J. (2009) The SR protein family. Genome Biol., 10, 242.
37. Rahman,L., Bliskovski,V., Kaye,F.J. and Zajac-Kaye,M. (2004) Evolutionary conservation of a 2-kb intronic sequence flanking a tissue-specific alternative exon in the PTBP2 gene. Genomics, 83, 76-84. (Pubitemid 37518262)
38. Wollerton,M.C., Gooding,C., Wagner,E.J., Garcia-Blanco,M.A. and Smith,C.W. (2004) Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell, 13, 91-100.
39. Ji,H., Zhang,Y., Zheng,W., Wu,Z., Lee,S. and Sandberg,K. (2004) Translational regulation of angiotensin type 1a receptor expression and signaling by upstream AUGs in the 5′ leader sequence. J. Biol. Chem., 279, 45322-45328.
40. Song,K.Y., Hwang,C.K., Kim,C.S., Choi,H.S., Law,P.Y., Wei,L.N. and Loh,H.H. (2007) Translational repression of mouse mu opioid receptor expression via leaky scanning. Nucleic Acids Res., 35, 1501-1513.
41. Churbanov,A., Rogozin,I.B., Babenko,V.N., Ali,H. and Koonin,E.V. (2005) Evolutionary conservation suggests a regulatory function of AUG triplets in 5′-UTRs of eukaryotic genes. Nucleic Acids Res., 33, 5512-5520. (Pubitemid 41548817)
42. Resch,A.M., Ogurtsov,A.Y., Rogozin,I.B., Shabalina,S.A. and Koonin,E.V. (2009) Evolution of alternative and constitutive regions of mammalian 5′UTRs. BMC Genomics, 10, 162.
43. Hughes,T.A. and Brady,H.J. (2005) Expression of axin2 is regulated by the alternative 5′-untranslated regions of its mRNA. J. Biol. Chem., 280, 8581-8588.
44. Newton,D.C., Bevan,S.C., Choi,S., Robb,G.B., Millar,A., Wang,Y. and Marsden,P.A. (2003) Translational regulation of human neuronal nitric-oxide synthase by an alternatively spliced 5′-untranslated region leader exon. J. Biol. Chem., 278, 636-644.
45. Pan,Y.X. (2005) Diversity and complexity of the mu opioid receptor gene: alternative pre-mRNA splicing and promoters. DNA Cell Biol., 24, 736-750.
46. Davuluri,R.V., Suzuki,Y., Sugano,S. and Zhang,M.Q. (2000) CART classification of human 5′ UTR sequences. Genome Res., 10, 1807-1816.
47. Iacono,M., Mignone,F. and Pesole,G. (2005) uAUG and uORFs in human and rodent 5′untranslated mRNAs. Gene, 349, 97-105.
48. Pesole,G., Gissi,C., Grillo,G., Licciulli,F., Liuni,S. and Saccone,C. (2000) Analysis of oligonucleotide AUG start codon context in eukariotic mRNAs. Gene, 261, 85-91. (Pubitemid 32103526)
49. Friedman,R.C., Farh,K.K., Burge,C.B. and Bartel,D.P. (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res., 19, 92-105.
50. Griffiths-Jones,S., Grocock,R.J., van Dongen,S., Bateman,A. and Enright,A.J. (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res., 34, D140-D144.
51. Washietl,S., Hofacker,I.L., Lukasser,M., Huttenhofer,A. and Stadler,P.F. (2005) Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome. Nat. Biotechnol., 23, 1383-1390.
52. Chamary,J.V. and Hurst,L.D. (2005) Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol., 6, R75.
53. Katzman,S., Kern,A.D., Bejerano,G., Fewell,G., Fulton,L., Wilson,R.K., Salama,S.R. and Haussler,D. (2007) Human genome ultraconserved elements are ultraselected. Science, 317, 915. (Pubitemid 47301312)
54. Sharova,L.V., Sharov,A.A., Nedorezov,T., Piao,Y., Shaik,N. and Ko,M.S. (2009) Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res., 16, 45-58.
55. Becker,K.G., Barnes,K.C., Bright,T.J. and Wang,S.A. (2004) The genetic association database. Nat. Genet., 36, 431-432.
56. Bertone,P., Stolc,V., Royce,T.E., Rozowsky,J.S., Urban,A.E., Zhu,X., Rinn,J.L., Tongprasit,W., Samanta,M., Weissman,S. et al. (2004) Global identification of human transcribed sequences with genome tiling arrays. Science, 306, 2242-2246. (Pubitemid 40024458)
57. Kapranov,P., Cheng,J., Dike,S., Nix,D.A., Duttagupta,R., Willingham,A.T., Stadler,P.F., Hertel,J., Hackermuller,J., Hofacker,I.L. et al. (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science, 316, 1484-1488. (Pubitemid 46906616)
58. van Bakel,H., Nislow,C., Blencowe,B.J. and Hughes,T.R. (2010) Most "dark matter" transcripts are associated with known genes. PLoS Biol, 8, e1000371.
59. Visel,A., Prabhakar,S., Akiyama,J.A., Shoukry,M., Lewis,K.D., Holt,A., Plajzer-Frick,I., Afzal,V., Rubin,E.M. and Pennacchio,L.A. (2008) Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet., 40, 158-160.
60. Siepel,A., Bejerano,G., Pedersen,J.S., Hinrichs,A.S., Hou,M., Rosenbloom,K., Clawson,H., Spieth,J., Hillier,L.W., Richards,S. et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res., 15, 1034-1050. (Pubitemid 41126859)
61. Tseng,H.H. and Tompa,M. (2009) Algorithms for locating extremely conserved elements in multiple sequence alignments. BMC Bioinformatics, 10, 432.
62. Prabhakar,S., Poulin,F., Shoukry,M., Afzal,V., Rubin,E.M., Couronne,O. and Pennacchio,L.A. (2006) Close sequence comparisons are sufficient to identify human cis-regulatory elements. Genome Res., 16, 855-863. (Pubitemid 43992909)