Differential GC Content between Exons and Introns Establishes Distinct Strategies of Splice-Site Recognition

Cell Reports

Volumn 1, Issue 5, 2012, Pages 543-556

  Amit, Maayan ^a   Donyo, Maya ^a   Hollander, Dror ^a   Goren, Amir ^a   Kim, Eddo ^a   Gelfman, Sahar ^a   Lev Maor, Galit ^a   Burstein, David ^a   Schwartz, Schraga ^b   Postolsky, Benny ^a   Pupko, Tal ^a   Ast, Gil ^a  

^a TEL AVIV UNIVERSITY   (Israel)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; GUANOSINE;

ANURA; ARABIDOPSIS; ARTICLE; CAENORHABDITIS ELEGANS; CHICKEN; CONTROLLED STUDY; COW; DNA CONTENT; DNA SPLICING; EXON; EXON SKIPPING; GENE MUTATION; HUMAN; INTRON; MOUSE; NONHUMAN; NUCLEOSOME; OPOSSUM; PLATYPUS; PUFFER FISH; SPLICEOSOME; ZEBRA FISH;

BASE COMPOSITION; DNA; DNA, RECOMBINANT; EVOLUTION, MOLECULAR; EXONS; HUMANS; INTRONS; MODELS, GENETIC; MUTATION; RNA SPLICE SITES; RNA SPLICING; SPLICEOSOMES;

EID: 84861694712     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.03.013     Document Type: Article

References (63)

1. Ast G. How did alternative splicing evolve?. Nat. Rev. Genet. 2004, 5:773-782.
2. Barbosa-Morais N.L., Carmo-Fonseca M., Aparício S. Systematic genome-wide annotation of spliceosomal proteins reveals differential gene family expansion. Genome Res. 2006, 16:66-77.
3. Berget S.M. Exon recognition in vertebrate splicing. J. Biol. Chem. 1995, 270:2411-2414.
4. Bernardi G. The vertebrate genome: isochores and evolution. Mol. Biol. Evol. 1993, 10:186-204.
5. Bernardi G. Isochores and the evolutionary genomics of vertebrates. Gene 2000, 241:3-17.
6. Bernardi G. Misunderstandings about isochores. Part 1. Gene 2001, 276:3-13.
7. Bernardi G., Olofsson B., Filipski J., Zerial M., Salinas J., Cuny G., Meunier-Rotival M., Rodier F. The mosaic genome of warm-blooded vertebrates. Science 1985, 228:953-958.
8. Blencowe B.J. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 2000, 25:106-110.
9. Cartegni L., Wang J., Zhu Z., Zhang M.Q., Krainer A.R. ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res. 2003, 31:3568-3571.
10. Castle J.C., Zhang C., Shah J.K., Kulkarni A.V., Kalsotra A., Cooper T.A., Johnson J.M. Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat. Genet. 2008, 40:1416-1425.
11. Collins L., Penny D. Complex spliceosomal organization ancestral to extant eukaryotes. Mol. Biol. Evol. 2005, 22:1053-1066.
12. Cooper T.A., Mattox W. The regulation of splice-site selection, and its role in human disease. Am. J. Hum. Genet. 1997, 61:259-266.
13. Cooper T.A., Wan L., Dreyfuss G. RNA and disease. Cell 2009, 136:777-793.
14. Cross S.H., Clark V.H., Simmen M.W., Bickmore W.A., Maroon H., Langford C.F., Carter N.P., Bird A.P. CpG island libraries from human chromosomes 18 and 22: landmarks for novel genes. Mamm. Genome 2000, 11:373-383.
15. de Almeida S.F., Grosso A.R., Koch F., Fenouil R., Carvalho S., Andrade J., Levezinho H., Gut M., Eick D., Gut I., et al. Splicing enhances recruitment of methyltransferase HYPB/Setd2 and methylation of histone H3 Lys36. Nat. Struct. Mol. Biol. 2011, 18:977-983.
16. Desmet F.O., Hamroun D., Lalande M., Collod-Béroud G., Claustres M., Béroud C. Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res. 2009, 37:e67.
17. Deutsch M., Long M. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 1999, 27:3219-3228.
18. Eisenberg E., Levanon E.Y. Human housekeeping genes are compact. Trends Genet. 2003, 19:362-365.
19. Fairbrother W.G., Holste D., Burge C.B., Sharp P.A. Single nucleotide polymorphism-based validation of exonic splicing enhancers. PLoS Biol. 2004, 2:E268.
20. Fox-Walsh K.L., Dou Y., Lam B.J., Hung S.P., Baldi P.F., Hertel K.J. The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc. Natl. Acad. Sci. USA 2005, 102:16176-16181.
21. Gelfman S., Burstein D., Penn O., Savchenko A., Amit M., Schwartz S., Pupko T., Ast G. Changes in exon-intron structure during vertebrate evolution affect the splicing pattern of exons. Genome Res. 2012, 22:35-50.
22. Guo M., Lo P.C., Mount S.M. Species-specific signals for the splicing of a short Drosophila intron in vitro. Mol. Cell. Biol. 1993, 13:1104-1118.
23. Hastings M.L., Krainer A.R. Pre-mRNA splicing in the new millennium. Curr. Opin. Cell Biol. 2001, 13:302-309.
24. Hertel K.J. Combinatorial control of exon recognition. J. Biol. Chem. 2008, 283:1211-1215.
25. Keren H., Lev-Maor G., Ast G. Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet. 2010, 11:345-355.
26. Kim E., Magen A., Ast G. Different levels of alternative splicing among eukaryotes. Nucleic Acids Res. 2007, 35:125-131.
27. Kim S., Kim H., Fong N., Erickson B., Bentley D.L. Pre-mRNA splicing is a determinant of histone H3K36 methylation. Proc. Natl. Acad. Sci. USA 2011, 108:13564-13569.
28. Kolasinska-Zwierz P., Down T., Latorre I., Liu T., Liu X.S., Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat. Genet. 2009, 41:376-381.
29. Kornblihtt A.R., Schor I.E., Allo M., Blencowe B.J. When chromatin meets splicing. Nat. Struct. Mol. Biol. 2009, 16:902-903.
30. Krawczak M., Reiss J., Cooper D.N. The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes and consequences. Hum. Genet. 1992, 90:41-54.
31. Krawczak M., Thomas N.S., Hundrieser B., Mort M., Wittig M., Hampe J., Cooper D.N. Single base-pair substitutions in exon-intron junctions of human genes: nature, distribution, and consequences for mRNA splicing. Hum. Mutat. 2007, 28:150-158.
32. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921. International Human Genome Sequencing Consortium.
33. Lercher M.J., Urrutia A.O., Pavlícek A., Hurst L.D. A unification of mosaic structures in the human genome. Hum. Mol. Genet. 2003, 12:2411-2415.
34. Licatalosi D.D., Mele A., Fak J.J., Ule J., Kayikci M., Chi S.W., Clark T.A., Schweitzer A.C., Blume J.E., Wang X., et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
35. Lynch M., Conery J.S. The origins of genome complexity. Science 2003, 302:1401-1404.
36. Majewski J., Ott J. Distribution and characterization of regulatory elements in the human genome. Genome Res. 2002, 12:1827-1836.
37. Nakai K., Sakamoto H. Construction of a novel database containing aberrant splicing mutations of mammalian genes. Gene 1994, 141:171-177.
38. Niu D.K. Exon definition as a potential negative force against intron losses in evolution. Biol. Direct 2008, 3:46.
39. Nogues G., Kadener S., Cramer P., Bentley D., Kornblihtt A.R. Transcriptional activators differ in their abilities to control alternative splicing. J. Biol. Chem. 2002, 277:43110-43114.
40. Pan Q., Shai O., Lee L.J., Frey B.J., Blencowe B.J. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 2008, 40:1413-1415.
41. Prendergast J.G., Semple C.A. Widespread signatures of recent selection linked to nucleosome positioning in the human lineage. Genome Res. 2011, 21:1777-1787.
42. Ram O., Ast G. SR proteins: a foot on the exon before the transition from intron to exon definition. Trends Genet. 2007, 23:5-7.
43. Roca X., Sachidanandam R., Krainer A.R. Intrinsic differences between authentic and cryptic 5' splice sites. Nucleic Acids Res. 2003, 31:6321-6333.
44. Roy S.W., Gilbert W. The evolution of spliceosomal introns: patterns, puzzles and progress. Nat. Rev. Genet. 2006, 7:211-221.
45. Schones D.E., Cui K., Cuddapah S., Roh T.Y., Barski A., Wang Z., Wei G., Zhao K. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008, 132:887-898.
46. Schor I.E., Rascovan N., Pelisch F., Alló M., Kornblihtt A.R. Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing. Proc. Natl. Acad. Sci. USA 2009, 106:4325-4330.
47. Schwartz S., Ast G. Chromatin density and splicing destiny: on the cross-talk between chromatin structure and splicing. EMBO J. 2010, 29:1629-1636.
48. Schwartz S., Meshorer E., Ast G. Chromatin organization marks exon-intron structure. Nat. Struct. Mol. Biol. 2009, 16:990-995.
49. Schwartz S.H., Silva J., Burstein D., Pupko T., Eyras E., Ast G. Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes. Genome Res. 2008, 18:88-103.
50. Shapiro M.B., Senapathy P. RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res. 1987, 15:7155-7174.
51. Sorek R., Ast G. Intronic sequences flanking alternatively spliced exons are conserved between human and mouse. Genome Res. 2003, 13:1631-1637.
52. Spies N., Nielsen C.B., Padgett R.A., Burge C.B. Biased chromatin signatures around polyadenylation sites and exons. Mol. Cell 2009, 36:245-254.
53. Sterner D.A., Carlo T., Berget S.M. Architectural limits on split genes. Proc. Natl. Acad. Sci. USA 1996, 93:15081-15085.
54. Subtil-Rodríguez A., Reyes J.C. BRG1 helps RNA polymerase II to overcome a nucleosomal barrier during elongation, in vivo. EMBO Rep. 2010, 11:751-757.
55. Sugnet C.W., Srinivasan K., Clark T.A., O'Brien G., Cline M.S., Wang H., Williams A., Kulp D., Blume J.E., Haussler D., Ares M. Unusual intron conservation near tissue-regulated exons found by splicing microarrays. PLoS Comput. Biol. 2006, 2:e4.
56. Talerico M., Berget S.M. Intron definition in splicing of small Drosophila introns. Mol. Cell. Biol. 1994, 14:3434-3445.
57. Tilgner H., Nikolaou C., Althammer S., Sammeth M., Beato M., Valcárcel J., Guigó R. Nucleosome positioning as a determinant of exon recognition. Nat. Struct. Mol. Biol. 2009, 16:996-1001.
58. Tillo D., Hughes T.R. G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 2009, 10:442.
59. Wang E.T., Sandberg R., Luo S., Khrebtukova I., Zhang L., Mayr C., Kingsmore S.F., Schroth G.P., Burge C.B. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476.
60. Yandell M., Mungall C.J., Smith C., Prochnik S., Kaminker J., Hartzell G., Lewis S., Rubin G.M. Large-scale trends in the evolution of gene structures within 11 animal genomes. PLoS Comput. Biol. 2006, 2:e15.
61. Yeo G., Hoon S., Venkatesh B., Burge C.B. Variation in sequence and organization of splicing regulatory elements in vertebrate genes. Proc. Natl. Acad. Sci. USA 2004, 101:15700-15705.
62. Yeo G.W., Van Nostrand E.L., Liang T.Y. Discovery and analysis of evolutionarily conserved intronic splicing regulatory elements. PLoS Genet. 2007, 3:e85.
63. Zhang C., Darnell R.B. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat. Biotechnol. 2011, 29:607-614.