Where do introns come from?

PLoS Biology

Volumn 6, Issue 11, 2008, Pages 2354-2361

  Catania, Francesco ^a   Lynch, Michael ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; DNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ALLELE; ALTERNATIVE RNA SPLICING; CODON; DNA SEQUENCE; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; INTRON; PHENOTYPE; REVIEW; SPLICEOSOME; ARTICLE; GENETICS; METABOLISM; RNA SPLICING; STOP CODON; UNTRANSLATED REGION;

CODON, NONSENSE; DNA; INTRONS; RNA SPLICING; RNA, MESSENGER; SPLICEOSOMES; UNTRANSLATED REGIONS;

EID: 56849118754     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0060283     Document Type: Review

References (137)

1. Burge CB, Tuschl T, Sharp PA (1999) Splicing of precursors to mRNAs by the spliceosomes. In: Gesteland RF, Cech T, Atkins JF, editors. The RNA world. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press. pp. 525-560.
2. Qiu WG, Schisler N, Stoltzfus A (2004) The evolutionary gain of spliceosomal introns: Sequence and phase preferences. Mol Biol Evol 21: 1252-1263.
3. Roy SW, Fedorov A, Gilbert W (2003) Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc Natl Acad Sci U S A 100: 7158-7162.
4. Juneau K, Palm C, Miranda M, Davis RW (2007) High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing. Proc Natl Acad Sci U S A 104: 1522-1527.
5. Mourier T, Jeffares DC (2003) Eukaryotic intron loss. Science 300: 1393.
6. Gilbert W (1978) Why genes in pieces. Nature 271: 501-501.
7. Cavalier-Smith T (1991) Intron phylogeny - A new hypothesis. Trends Genet 7: 145-148.
8. Sharp PA (1985) On the origin of RNA splicing and introns. Cell 42: 397-400.
9. Cech TR (1986) The generality of self-splicing RNA - Relationship to nuclear messenger-RNA splicing. Cell 44: 207-210.
10. Jacquier A (1990) Self-splicing group-ii and nuclear pre-messenger-rna introns - How similar are they. Trends Biochem Sci 15: 351-354.
11. Roy SW, Gilbert W (2006) The evolution of spliceosomal introns: Patterns, puzzles and progress. Nat Rev Genet 7: 211-221.
12. Coulombe-Huntington J, Majewski J (2007) Intron loss and gain in Drosophila. Mol Biol Evol 24: 2842-2850.
13. Sverdlov AV, Babenko VN, Rogozin IB, Koonin EV (2004) Preferential loss and gain of introns in 3′ portions of genes suggests a reverse-transcription mechanism of intron insertion. Gene 338: 85-91.
14. Roy SW, Penny D (2007) A very high fraction of unique intron positions in the intron-rich diatom Thalassiosira pseudonana indicates widespread intron gain. Mol Biol Evol 24: 1447-1457.
15. Wang W, Zheng HK, Yang S, Yu HJ, Li J, et al. (2005) Origin and evolution of new exons in rodents. Genome Res 15: 1258-1264.
16. Alekseyenko AV, Kim N, Lee CJ (2007) Global analysis of exon creation versus loss and the role of alternative splicing in 17 vertebrate genomes. RNA 13: 661-670.
17. Gromoll J, Lahrmann L, Godmann M, Muller T, Michel C, et al. (2007) Genomic checkpoints for exon 10 usage in the luteinizing hormone receptor type 1 and type 2. Mol Endocrinol 21: 1984-1996.
18. Zhuo D, Madden R, Elela SA, Chabot B (2007) Modern origin of numerous alternatively spliced human introns from tandem arrays. Proc Natl Acad Sci U S A 104: 882-886.
19. Luehrsen KR, Walbot V (1994) Intron creation and polyadenylation in maize are directed by AU-rich RNA. Genes Dev 8: 1117-1130.
20. Simpson CG, Brown JW (1993) Efficient splicing of an AU-rich antisense intron sequence. Plant Mol Biol 21: 205-211.
21. Rushforth AM, Anderson P (1996) Splicing removes the Caenorhabditis elegans transposon Tc1 from most mutant pre-mRNAs. Mol Cell Biol 16: 422-429.
22. Fridell RA, Pret AM, Searles LL (1990) A retrotransposon 412 insertion within an exon of the Drosophila melanogaster vermilion gene is spliced from the precursor RNA. Genes Dev 4: 559-566.
23. Giroux MJ, Clancy M, Baier J, Ingham L, McCarty D, et al. (1994) De novo synthesis of an intron by the maize transposable element Dissociation. Proc Natl Acad Sci U S A 91: 12150-12154.
24. Cartegni L, Chew SL, Krainer AR (2002) Listening to silence and understanding nonsense: Exonic mutations that affect splicing. Nat Rev Genet 3: 285-298.
25. Valentine CR (1998) The association of nonsense codons with exon skipping. Mutat Res 411: 87-117.
26. Dietz HC, Kendzior RJ Jr. (1994) Maintenance of an open reading frame as an additional level of scrutiny during splice site selection. Nat Genet 8: 183-188.
27. Dietz HC, Valle D, Francomano CA, Kendzior RJ Jr., Pyeritz RE, et al. (1993) The skipping of constitutive exons in vivo induced by nonsense mutations. Science 259: 680-683.
28. Wang J, Hamilton JI, Carter MS, Li S, Wilkinson MF (2002) Alternatively spliced TCR mRNA induced by disruption of reading frame. Science 297: 108-110.
29. Gersappe A, Burger L, Pintel DJ (1999) A premature termination codon in either exon of minute virus of mice P4 promoter-generated pre-mRNA can inhibit nuclear splicing of the intervening intron in an open reading frame-dependent manner. J Biol Chem 274: 22452-22458.
30. Naeger LK, Schoborg RV, Zhao Q, Tullis GE, Pintel DJ (1992) Nonsense mutations inhibit splicing of MVM RNA in cis when they interrupt the reading frame of either exon of the final spliced product. Genes Dev 6: 1107-1119.
31. Hentze MW, Kulozik AE (1999) A perfect message: RNA surveillance and nonsense-mediated decay. Cell 96: 307-310.
32. Li BH, Wachtel C, Miriami E, Yahalom G, Friedlander G, et al. (2002) Stop codons affect 5′ splice site selection by surveillance of splicing. Proc Natl Acad Sci U S A 99: 5277-5282.
33. Chang YF, Imam JS, Wilkinson MF (2007) The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 76: 51-74.
34. Lu QL, Morris GE, Wilton SD, Ly T, Artem'yeva OV, et al. (2000) Massive idiosyncratic exon skipping corrects the nonsense mutation in dystrophic mouse muscle and produces functional revertant fibers by clonal expansion. J Cell Biol 148: 985-996.
35. Matsuzaki Y, Nakano A, Jiang QJ, Pulkkinen L, Uitto J (2005) Tissue-specific expression of the ABCC6 gene. J Invest Dermatol 125: 900-905.
36. Dominski Z, Kole R (1991) Selection of splice sites in pre-mRNAs with short internal exons. Mol Cell Biol 11: 6075-6083.
37. Ast G (2004) How did alternative splicing evolve? Nat Rev Genet 5: 773-782.
38. Lev-Maor G, Goren A, Sela N, Kim E, Keren H, et al. (2007) The "alternative" choice of constitutive exons throughout evolution. PLoS Genet 3(11): e203. doi:10.1371/journal.pgen.0030203
39. Koren E, Lev-Maor G, Ast G (2007) The emergence of alternative 3′ and 5′ splice site exons from constitutive exons. PLoS Comput Biol 3(5): e95. doi:10.1371/journal.pcbi.0030095
40. Galante PA, Sakabe NJ, Kirschbaum-Slager N, de Souza SJ (2004) Detection and evaluation of intron retention events in the human transcriptome. RNA 10: 757-765.
41. Irimia M, Rukov JL, Penny D, Vinther J, Garcia-Fernandez J, et al. (2008) Origin of introns by 'intronization' of exonic sequences. Trends Genet 24: 378-381.
42. Modrek B, Lee CJ (2003) Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet 34: 177-180.
43. Zhang XHF, Chasin LA (2006) Comparison of multiple vertebrate genomes reveals the birth and evolution of human exons. Proc Natl Acad Sci U S A 103: 13427-13432.
44. Sela N, Mersch B, Gal-Mark N, Lev-Maor G, Hotz-Wagenblatt A, et al. (2007) Comparative analysis of transposed element insertion within human and mouse genomes reveals Alu's unique role in shaping the human transcriptome. Genome Biol 8: R127.
45. Wang W, Kirkness EF (2005) Short interspersed elements (SINEs) are a major source of canine genomic diversity. Genome Res 15: 1798-1808.
46. Krull M, Petrusma M, Makalowski W, Brosius J, Schmitz J (2007) Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Res 17: 1139-1145.
47. Sorek R, Ast G, Graur D (2002) Alu-containing exons are alternatively spliced. Genome Res 12: 1060-1067.
48. Resch A, Xing Y, Alekseyenko A, Modrek B, Lee C (2004) Evidence for a subpopulation of conserved alternative splicing events under selection pressure for protein reading frame preservation. Nucleic Acids Res 32: 1261-1269.
49. Xing Y, Lee C (2005) Assessing the application of Ka/Ks ratio test to alternatively spliced exons. Bioinformatics 21: 3701-3703.
50. Sorek R, Shamir R, Ast G (2004) How prevalent is functional alternative splicing in the human genome? Trends Genet 20: 68-71.
51. Romero PR, Zaidi S, Fang YY, Uversky VN, Radivojac P, et al. (2006) Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc Natl Acad Sci U S A 103: 8390-8395.
52. Kriventseva EV, Koch I, Apweiler R, Vingron M, Bork P, et al. (2003) Increase of functional diversity by alternative splicing. Trends Genet 19: 124-128.
53. Clark F, Thanaraj TA (2002) Categorization and characterization of transcript-confirmed constitutively and alternatively spliced introns and exons from human. Hum Mol Genet 11: 451-464.
54. Zavolan M, Kondo S, Schonbach C, Adachi J, Hume DA, et al. (2003) Impact of alternative initiation, splicing, and termination on the diversity of the mRNA transcripts encoded by the mouse transcriptome. Genome Res 13: 1290-1300.
55. Baek D, Green P (2005) Sequence conservation, relative isoform frequencies, and nonsense-mediated decay in evolutionarily conserved alternative splicing. Proc Natl Acad Sci U S A 102: 12813-12818.
56. Zheng CL, Fu XD, Gribskov M (2005) Characteristics and regulatory elements defining constitutive splicing and different modes of alternative splicing in human and mouse. RNA 11: 1777-1787.
57. Itoh H, Washio T, Tomita M (2004) Computational comparative analyses of alternative splicing regulation using full-length cDNA of various eukaryotes. RNA 10: 1005-1018.
58. Xing Y, Lee CJ (2005) Protein modularity of alternatively spliced exons is associated with tissue-specific regulation of alternative splicing. PLoS Genet 1(3): e34. doi:10.1371/journal.pgen.0010034
59. Garg K, Green P (2007) Differing patterns of selection in alternative and constitutive splice sites. Genome Res 17: 1015-1022.
60. Xing Y, Lee C (2005) Evidence of functional selection pressure for alternative splicing events that accelerate evolution of protein subsequences. Proc Natl Acad Sci U S A 102: 13526-13531.
61. Maniatis T, Reed R (2002) An extensive network of coupling among gene expression machines. Nature 416: 499-506.
62. Banerjee AK (1980) 5′-terminal cap structure in eucaryotic messenger ribonucleic acids. Microbiol Rev 44: 175-205.
63. Cooke C, Hans H, Alwine JC (1999) Utilization of splicing elements and polyadenylation signal elements in the coupling of polyadenylation and last-intron removal. Mol Cell Biol 19: 4971-4979.
64. Ortiz DF, Strommer JN (1990) The Mu1 maize transposable element induces tissue-specific aberrant splicing and polyadenylation in two Adh1 mutants. Mol Cell Biol 10: 2090-2095.
65. Dye MJ, Proudfoot NJ (1999) Terminal exon definition occurs cotranscriptionally and promotes termination of RNA polymerase II. Mol Cell 3: 371-378.
66. Pandey NB, Chodchoy N, Liu TJ, Marzluff WF (1990) Introns in histone genes alter the distribution of 3′ ends. Nucleic Acids Res 18: 3161-3170.
67. Vagner S, Vagner C, Mattaj IW (2000) The carboxyl terminus of vertebrate poly(A) polymerase interacts with U2AF 65 to couple 3′-end processing and splicing. Genes Dev 14: 403-413.
68. Gunderson SI, Beyer K, Martin G, Keller W, Boelens WC, et al. (1994) The human U1A snRNP protein regulates polyadenylation via a direct interaction with poly(A) polymerase. Cell 76: 531-541.
69. Lutz CS, Murthy KG, Schek N, O'Connor JP, Manley JL, et al. (1996) Interaction between the U1 snRNP-A protein and the 160-kD subunit of cleavage-polyadenylation specificity factor increases polyadenylation efficiency in vitro. Genes Dev 10: 325-337.
70. Kyburz A, Friedlein A, Langen H, Keller W (2006) Direct interactions between subunits of CPSF and the U2 snRNP contribute to the coupling of pre-mRNA 3′ end processing and splicing. Mol Cell 23: 195-205.
71. Proudfoot NJ, Furger A, Dye MJ (2002) Integrating rnRNA processing with transcription. Cell 108: 501-512.
72. Peterson ML, Perry RP (1989) The regulated production of mu m and mu s mRNA is dependent on the relative efficiencies of mu s poly(A) site usage and the c mu 4-to-M1 splice. Mol Cell Biol 9: 726-738.
73. Takagaki Y, Seipelt RL, Peterson ML, Manley JL (1996) The polyadenylation factor CstF-64 regulates alternative processing of IgM heavy chain pre-mRNA during B cell differentiation. Cell 87: 941-952.
74. Leff SE, Evans RM, Rosenfeld MG (1987) Splice commitment dictates neuron-specific alternative RNA processing in calcitonin/CGRP gene expression. Cell 48: 517-524.
75. Lou H, Neugebauer KM, Gagel RF, Berget SM (1998) Regulation of alternative polyadenylation by U1 snRNPs and SRp20. Mol Cell Biol 18: 4977-4985.
76. Ko CH, Brendel V, Taylor RD, Walbot V (1998) U-richness is a defining feature of plant introns and may function as an intron recognition signal in maize. Plant Mol Biol 36: 573-583.
77. Goodall GJ, Filipowicz W (1989) The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell 58: 473-483.
78. Gniadkowski M, Hemmings-Mieszczak M, Klahre U, Liu HX, Filipowicz W (1996) Characterization of intronic uridine-rich sequence elements acting as possible targets for nuclear proteins during pre-mRNA splicing in Nicotiana plumbaginifolia. Nucleic Acids Res 24: 619-627.
79. Zhao J, Hyman L, Moore C (1999) Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63: 405-445.
80. Singh R, Valcarcel J, Green MR (1995) Distinct binding specificities and functions of higher eukaryotic polypyrimidine tractbinding proteins. Science 268: 1173-1176.
81. Furth PA, Baker CC (1991) An element in the bovine papillomavirus late 3′ untranslated region reduces polyadenylated cytoplasmic RNA levels. J Virol 65: 5806-5812.
82. Furth PA, Choe WT, Rex JH, Byrne JC, Baker CC (1994) Sequences homologous to 5′ splice sites are required for the inhibitory activity of papillomavirus late 3′ untranslated regions. Mol Cell Biol 14: 5278-5289.
83. Ashe MP, Griffin P, James W, Proudfoot NJ (1995) Poly(A) site selection in the HIV-1 provirus: inhibition of promoter-proximal polyadenylation by the downstream major splice donor site. Genes Dev 9: 3008-3025.
84. Ashe MP, Pearson LH, Proudfoot NJ (1997) The HIV-1 5′ LTR poly(A) site is inactivated by U1 snRNP interaction with the downstream major splice donor site. Embo J 16: 5752-5763.
85. Vagner S, Ruegsegger U, Gunderson SI, Keller W, Mattaj IW (2000) Position-dependent inhibition of the cleavage step of pre-mRNA 3′-end processing by U1 snRNP. RNA 6: 178-188.
86. Abad X, Vera M, Jung SP, Oswald E, Romero I, et al. (2008) Requirements for gene silencing mediated by U1 snRNA binding to a target sequence. Nucleic Acids Res 36: 2338-2352.
87. Smith CWJ, Valcarcel J (2000) Alternative premRNA splicing: the logic of combinatorial control. Trends Biochem Sci 25: 381-388.
88. Cramer P, Pesce CG, Baralle FE, Kornblihtt AR (1997) Functional association between promoter structure and transcript alternative splicing. Proc Natl Acad Sci U S A 94: 11456-11460.
89. de la Mata M, Alonso CR, Kadener S, Fededa JP, Blaustein M, et al. (2003) A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell 12: 525-532.
90. Eperon LP, Graham IR, Griffiths AD, Eperon IC (1988) Effects of RNA secondary structure on alternative splicing of premRNA: Is folding limited to a region behind the transcribing RNA polymerase? Cell 54: 393-401.
91. Ares M Jr., Grate L, Pauling MH (1999) A handful of intron-containing genes produces the lion's share of yeast mRNA. RNA 5: 1138-1139.
92. Fong YW, Zhou Q (2001) Stimulatory effect of splicing factors on transcriptional elongation. Nature 414: 929-933.
93. McCracken S, Lambermon M, Blencowe BJ (2002) SRm160 splicing coactivator promotes transcript 3′-end cleavage. Mol Cell Biol 22: 148-160.
94. Lewis JD, Izaurralde E, Jarmolowski A, McGuigan C, Mattaj IW (1996) A nuclear cap-binding complex facilitates association of U1 snRNP with the cap-proximal 5′ splice site. Genes Dev 10: 1683-1698.
95. Inoue K, Ohno M, Sakamoto H, Shimura Y (1989) Effect of the cap structure on premRNA splicing in Xenopus oocyte nuclei. Genes Dev 3: 1472-1479.
96. Ohno M, Sakamoto H, Shimura Y (1987) Preferential excision of the 5′ proximal intron from mRNA precursors with two introns as mediated by the cap structure. Proc Natl Acad Sci U S A 84: 5187-5191.
97. Caceres JF, Stamm S, Helfman DM, Krainer AR (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265: 1706-1709.
98. Garcia-Blanco MA, Jamison SF, Sharp PA (1989) Identification and purification of a 62,000-dalton protein that binds specifically to the polypyrimidine tract of introns. Genes Dev 3: 1874-1886.
99. Wagner EJ, Garcia-Blanco MA (2001) Polypyrimidine tract binding protein antagonizes exon definition. Mol Cell Biol 21: 3281-3288.
100. Sharma S, Falick AM, Black DL (2005) Polypyrimidine tract binding protein blocks the 5′ splice site-dependent assembly of U2AF and the prespliceosomal E complex. Mol Cell 19: 485-496.
101. van Hoof A, Green PJ (1996) Premature nonsense codons decrease the stability of phytohemagglutinin mRNA in a position-dependent manner. Plant J 10: 415-424.
102. Baumann B, Potash MJ, Kohler G (1985) Consequences of frameshift mutations at the immunoglobulin heavy chain locus of the mouse. Embo J 4: 351-359.
103. Longman D, Plasterk RH, Johnstone IL, Caceres JF (2007) Mechanistic insights and identification of two novel factors in the C. elegans NMD pathway. Genes Dev 21: 1075-1085.
104. Silva AL, Pereira FJ, Morgado A, Kong J, Martins R, et al. (2006) The canonical UPF1-dependent nonsense-mediated mRNA decay is inhibited in transcripts carrying a short open reading frame independent of sequence context. RNA 12: 2160-2170.
105. Lynch M, Hong X, Scofield DG (2006) NMD and the evolution of eukaryotyic gene structure. In: Maquat LE, editor. Nonsense-mediated mRNA decay. Georgetown (TX): Landes Bioscience. pp. 197-211.
106. Mendell JT, Medghalchi SM, Lake RG, Noensie EN, Dietz HC (2000) Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol Cell Biol 20: 8944-8957.
107. Pulak R, Anderson P (1993) Messenger-RNA surveillance by the Caenorhabditis-elegans smg genes. Genes Dev 7: 1885-1897.
108. Gatfield D, Unterholzner L, Ciccarelli FD, Bork P, Izaurralde E (2003) Nonsense-mediated mRNA decay in Drosophila: At the intersection of the yeast and mammalian pathways. Embo J 22: 3960-3970.
109. Rajavel KS, Neufeld EF (2001) Nonsense-mediated decay of human HEXA mRNA. Mol Cell Biol 21: 5512-5519.
110. Buhler M, Steiner S, Mohn F, Paillusson A, Muhlemann O (2006) EJC-independent degradation of nonsense immunoglobulin-mu mRNA depends on 3′ UTR length. Nat Struct Mol Biol 13: 462-464.
111. Singh G, Rebbapragada I, Lykke-Andersen J (2008) A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol 6(4): e111. doi:10.1371/journal.pbio. 0060111
112. Jaillon O, Bouhouche K, Gout JF, Aury JM, Noel B, et al. (2008) Translational control of intron splicing in eukaryotes. Nature 451: 359-362.
113. Pesole G, Mignone F, Gissi C, Grillo G, Licciulli F, et al. (2001) Structural and functional features of eukaryotic mRNA untranslated regions. Gene 276: 73-81.
114. Hong X, Scofield DG, Lynch M (2006) Intron size, abundance, and distribution within untranslated regions of genes. Mol Biol Evol 23: 2392-2404.
115. Roy SW, Penny D, Neafsey DE (2007) Evolutionary conservation of UTR intron boundaries in Cryptococcus. Mol Biol Evol 24: 1140-1148.
116. Oyama M, Itagaki C, Hata H, Suzuki Y, Izumi T, et al. (2004) Analysis of small human proteins reveals the translation of upstream open reading frames of mRNAs. Genome Res 14: 2048-2052.
117. Oyama M, Kozuka-Hata H, Suzuki Y, Semba K, Yamamoto T, et al. (2007) Diversity of translation start sites may define increased complexity of the human short ORFeome. Mol Cell Proteomics 6: 1000-1006.
118. Diba F, Watson CS, Gametchu B (2001) 5′UTR sequences of the glucocorticoid receptor 1A transcript encode a peptide associated with translational regulation of the glucocorticoid receptor. J Cell Biochem 81: 149-161.
119. Crowe ML, Wang XQ, Rothnagel JA (2006) Evidence for conservation and selection of upstream open reading frames suggests probable encoding of bioactive peptides. BMC Genomics 7: 16.
120. Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3: REVIEWS0004.
121. Bhattacharya D, Lutzoni F, Reeb V, Simon D, Nason J, et al. (2000) Widespread occurrence of spliceosomal introns in the rDNA genes of ascomycetes. Mol Biol Evol 17: 1971-1984.
122. Takahashi Y, Urushiyama S, Tani T, Ohshima Y (1993) An mRNA-type intron is present in the Rhodotorula hasegawae U2 small nuclear RNA gene. Mol Cell Biol 13: 5613-5619.
123. Reinisch KM, Wolin SL (2007) Emerging themes in non-coding RNA quality control. Curr Opin Struct Biol 17: 209-214.
124. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, et al. (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724.
125. LaRiviere FJ, Cole SE, Ferullo DJ, Moore MJ (2006) A late-acting quality control process for mature eukaryotic rRNAs. Mol Cell 24: 619-626.
126. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, et al. (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.
127. Brosius J (1991) Retroposons - Seeds of evolution. Science 251: 753.
128. Chang DD, Sharp PA (1989) Regulation by HIV Rev depends upon recognition of splice sites. Cell 59: 789-795.
129. Legrain P, Rosbash M (1989) Some cis- and trans-acting mutants for splicing target premRNA to the cytoplasm. Cell 57: 573-583.
130. Bray M, Prasad S, Dubay JW, Hunter E, Jeang KT, et al. (1994) A small element from the Mason-Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Rev-independent. Proc Natl Acad Sci U S A 91: 1256-1260.
131. Huang Y, Carmichael GG (1997) The mouse histone H2a gene contains a small element that facilitates cytoplasmic accumulation of intronless gene transcripts and of unspliced HIV-1-related mRNAs. Proc Natl Acad Sci U S A 94: 10104-10109.
132. Tang H, Gaietta GM, Fischer WH, Ellisman MH, Wong-Staal F (1997) A cellular cofactor for the constitutive transport element of type D retrovirus. Science 276: 1412-1415.
133. Guang S, Mertz JE (2005) Pre-mRNA processing enhancer (PPE) elements from intronless genes play additional roles in mRNA biogenesis than do ones from intron-containing genes. Nucleic Acids Res 33: 2215-2226.
134. Huang Y, Wimler KM, Carmichael GG (1999) Intronless mRNA transport elements may affect multiple steps of pre-mRNA processing. Embo J 18: 1642-1652.
135. Liu X, Mertz JE (1995) HnRNP L binds a cisacting RNA sequence element that enables intron-dependent gene expression. Genes Dev 9: 1766-1780.
136. Lynch M (2002) Intron evolution as a population-genetic process. Proc Natl Acad Sci U S A 99: 6118-6123.
137. Lev-Maor G, Sorek R, Levanon EY, Paz N, Eisenberg E, et al. (2007) RNA-editing-mediated exon evolution. Genome Biol 8: R29.