InTRONs in biotech

Molecular Biotechnology

Volumn 48, Issue 3, 2011, Pages 290-297

  Skoko, Natasa ^a   Baralle, Marco ^a   Tisminetzky, Sergio ^a   Buratti, Emanuele ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Exons; Gene expression; Introns; mRNA splicing; mRNA stability

Indexed keywords

BIOTECHNOLOGY APPLICATIONS; EUKARYOTIC GENE EXPRESSION; EUKARYOTIC GENOME; EXONS; GENE TRANSCRIPTIONS; INTRONS; MOLECULAR MACHINERY; MRNA SPLICING; MRNA STABILITY; PRE-MRNA; PRODUCTION STRATEGY; PROTEIN TRANSLATION; RIBONUCLEOPROTEINS; SPLICEOSOMES;

BIOTECHNOLOGY; COORDINATION REACTIONS; CYTOLOGY; MACHINERY; TRANSCRIPTION;

GENE EXPRESSION REGULATION;

MESSENGER RNA; RIBONUCLEOPROTEIN;

BIOTECHNOLOGY; EXON; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; INTRON; MACROMOLECULE; MOLECULAR MECHANICS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROCESSING; REVIEW; RNA SPLICING; RNA STABILITY; SPLICEOSOME; ANIMAL; BIOLOGICAL MODEL; HUMAN; METHODOLOGY;

EUKARYOTA;

ANIMALS; BIOTECHNOLOGY; HUMANS; INTRONS; MODELS, GENETIC; RNA SPLICING; RNA STABILITY;

EID: 80054037647     PISSN: 10736085     EISSN: 15590305     Source Type: Journal    
DOI: 10.1007/s12033-011-9390-x     Document Type: Review

References (87)

1. Black, D. L. (2003). Mechanisms of alternative pre-messenger RNA splicing. Annual Review of Biochemistry, 72, 291-336. (Pubitemid 36930448)
2. Cartegni, L., Chew, S. L., & Krainer, A. R. (2002). Listening to silence and understanding nonsense: Exonic mutations that affect splicing. Nature Reviews Genetics, 3, 285-298. (Pubitemid 34279797)
3. Nilsen, T. W. (2003). The spliceosome: The most complex macromolecular machine in the cell? Bioessays, 25, 1147-1149. (Pubitemid 37499313)
4. Wahl, M. C., Will, C. L., & Luhrmann, R. (2009). The spliceo-some: Design principles of a dynamic RNP machine. Cell, 136, 701-718.
5. Jurica, M. S., & Moore, M. J. (2003). Pre-mRNA splicing: Awash in a sea of proteins. Molecular Cell, 12, 5-14. (Pubitemid 36945033)
6. Zhou, Z., Licklider, L. J., Gygi, S. P., & Reed, R. (2002). Comprehensive proteomic analysis of the human spliceosome. Nature, 419, 182-185. (Pubitemid 35025448)
7. Blencowe, B. J. (2006). Alternative splicing: New insights from global analyses. Cell, 126, 37-47. (Pubitemid 44040990)
8. Nilsen, T. W., & Graveley, B. R. (2010). Expansion of the eukaryotic proteome by alternative splicing. Nature, 463, 457-463.
9. Lareau, L. F., Green, R. E., Bhatnagar, R. S., & Brenner, S. E. (2004). The evolving roles of alternative splicing. Current Opinion in Structural Biology, 14, 273-282. (Pubitemid 38749054)
10. Roy, S. W., & Gilbert, W. (2006). The evolution of spliceosomal introns: Patterns, puzzles and progress. Nature Reviews Genetics, 7, 211-221. (Pubitemid 43361532)
11. Keren, H., Lev-Maor, G., & Ast, G. (2010). Alternative splicing and evolution: Diversification, exon definition and function. Nature Reviews Genetics, 11, 345-355.
12. Venables, J. P. (2007). Downstream intronic splicing enhancers. FEBS Letters, 581, 4127-4131. (Pubitemid 47301872)
13. Xiao, X., Wang, Z., Jang, M., Nutiu, R., Wang, E. T., & Burge, C. B. (2009). Splice site strength-dependent activity and genetic buffering by poly-G runs. Nature Structural & Molecular Biology, 16, 1094-1100.
14. Dhir, A., & Buratti, E. (2010). Alternative splicing: Role of pseudoexons in human disease and potential therapeutic strategies. FEBS Journal, 277, 841-855.
15. Pillai, R. S., Bhattacharyya, S. N., & Filipowicz, W. (2007). Repression of protein synthesis by miRNAs: How many mechanisms? Trends in Cell Biology, 17, 118-126. (Pubitemid 46357525)
16. Rodriguez, A., Griffiths-Jones, S., Ashurst, J. L., & Bradley, A. (2004). Identification of mammalian microRNA host genes and transcription units. Genome Research, 14, 1902-1910. (Pubitemid 39386503)
17. Dieci, G., Preti, M., & Montanini, B. (2009). Eukaryotic snoR-NAs: A paradigm for gene expression flexibility. Genomics, 94, 83-88.
18. Castillo-Davis, C. I., Mekhedov, S. L., Hartl, D. L., Koonin, E. V., & Kondrashov, F. A. (2002). Selection for short introns in highly expressed genes. Nature Genetics, 31, 415-418. (Pubitemid 35154453)
19. Ares, M., Jr., Grate, L., & Pauling, M. H. (1999). A handful of intron-containing genes produces the lion's share of yeast mRNA. RNA, 5, 1138-1139. (Pubitemid 29422755)
20. Spingola, M., Grate, L., Haussler, D., & Ares, M., Jr. (1999). Genome-wide bioinformatic and molecular analysis of introns in Saccharomyces cerevisiae. RNA, 5, 221-234. (Pubitemid 29079282)
21. Lopez, P. J., & Seraphin, B. (1999). Genomic-scale quantitative analysis of yeast pre-mRNA splicing: Implications for splice-site recognition. RNA, 5, 1135-1137. (Pubitemid 29422754)
22. Furger, A., O'Sullivan, J. M., Binnie, A., Lee, B. A., & Proudfoot, N. J. (2002). Promoter proximal splice sites enhance transcription. Genes and Development, 16, 2792-2799. (Pubitemid 35253147)
23. Juneau, K., Miranda, M., Hillenmeyer, M. E., Nislow, C., & Davis, R. W. (2006). Introns regulate RNA and protein abundance in yeast. Genetics, 174, 511-518. (Pubitemid 44427691)
24. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., et al. (2001). Initial sequencing and analysis of the human genome. Nature, 409, 860-921. (Pubitemid 32165345)
25. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., et al. (2001). The sequence of the human genome. Science, 291, 1304-1351. (Pubitemid 32173090)
26. Buchman, A. R., & Berg, P. (1988). Comparison of intron-dependent and intron-independent gene expression. Molecular and Cellular Biology, 8, 4395-4405.
27. Lu, S., & Cullen, B. R. (2003). Analysis of the stimulatory effect of splicing on mRNA production and utilization in mammalian cells. RNA, 9, 618-630. (Pubitemid 36505459)
28. Nott, A., Meislin, S. H., & Moore, M. J. (2003). A quantitative analysis of intron effects on mammalian gene expression. RNA, 9, 607-617. (Pubitemid 36505458)
29. Ryu, W. S., & Mertz, J. E. (1989). Simian virus 40 late transcripts lacking excisable intervening sequences are defective in both stability in the nucleus and transport to the cytoplasm. Journal of Virology, 63, 4386-4394. (Pubitemid 19229437)
30. Jonsson, J. J., Foresman, M.D., Wilson, N., & McIvor, R.S. (1992). Intron requirement for expression of the human purine nucleoside phosphorylase gene. Nucleic Acids Research, 20, 3191-3198.
31. Deng, T. L., Li, Y., & Johnson, L. F. (1989). Thymidylate syn-thase gene expression is stimulated by some (but not all) introns. Nucleic Acids Research, 17, 645-658. (Pubitemid 19042300)
32. Korb, M., Ke, Y., & Johnson, L. F. (1993). Stimulation of gene expression by introns: Conversion of an inhibitory intron to a stimulatory intron by alteration of the splice donor sequence. Nucleic Acids Research, 21, 5901-5908. (Pubitemid 24023705)
33. Callis, J., Fromm, M., & Walbot, V. (1987). Introns increase gene expression in cultured maize cells. Genes and Development, 1, 1183-1200.
34. Collis, P., Antoniou, M., & Grosveld, F. (1990). Definition of the minimal requirements within the human beta-globin gene and the dominant control region for high level expression. EMBO Journal, 9, 233-240.
35. Luehrsen, K. R., & Walbot, V. (1991). Intron enhancement of gene expression and the splicing efficiency of introns in maize cells. Molecular and General Genetics, 225, 81-93.
36. Bourdon, V., Harvey, A., & Lonsdale, D. M. (2001). Introns and their positions affect the translational activity of mRNA in plant cells. EMBO Reports, 2, 394-398. (Pubitemid 32509954)
37. Rose, A. B. (2004). The effect of intron location on intron-mediated enhancement of gene expression in Arabidopsis. The Plant Journal, 40, 744-751. (Pubitemid 39623248)
38. Maniatis, T., & Reed, R. (2002). An extensive network of coupling among gene expression machines. Nature, 416, 499-506. (Pubitemid 34288845)
39. Le Hir, H., Nott, A., & Moore, M. J. (2003). How introns influence and enhance eukaryotic gene expression. Trends in Biochemical Sciences, 28, 215-220. (Pubitemid 36507161)
40. Hirose, Y., Tacke, R., & Manley, J. L. (1999). Phosphorylated RNA polymerase II stimulates pre-mRNA splicing. Genes and Development, 13, 1234-1239. (Pubitemid 29250190)
41. Das, R., Yu, J., Zhang, Z., Gygi, M. P., Krainer, A. R., Gygi, S. P., et al. (2007). SR proteins function in coupling RNAP II transcription to pre-mRNA splicing. Molecular Cell, 26, 867-881. (Pubitemid 46921010)
42. Tian, H. (2001). RNA ligands generated against complex nuclear targets indicate a role for U1 snRNP in co-ordinating transcription and RNA splicing. FEBS Letters, 509, 282-286. (Pubitemid 34015958)
43. Buratti, E., & Baralle, D. (2010). Novel roles of U1 snRNP in alternative splicing regulation. RNA Biology, 7, 412-419.
44. Morris, D. P., & Greenleaf, A. L. (2000). The splicing factor, Prp40, binds the phosphorylated carboxyl-terminal domain of RNA polymerase II. The Journal of Biological Chemistry, 275, 39935-39943. (Pubitemid 32064615)
45. Kwek, K. Y., Murphy, S., Furger, A., Thomas, B., O'Gorman, W., Kimura, H., et al. (2002). U1 snRNA associates with TFIIH and regulates transcriptional initiation. Nature Structural Biology, 9, 800-805. (Pubitemid 35257777)
46. Fong, Y. W., & Zhou, Q. (2001). Stimulatory effect of splicing factors on transcriptional elongation. Nature, 414, 929-933. (Pubitemid 34024746)
47. Batsche, E., Yaniv, M., & Muchardt, C. (2006). The human SWI/SNF subunit Brm is a regulator of alternative splicing. Nature Structural & Molecular Biology, 13, 22-29. (Pubitemid 43049398)
48. Cramer, P., Caceres, J. F., Cazalla, D., Kadener, S., Muro, A. F., Baralle, F. E., et al. (1999). Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer. Molecular Cell, 4, 251-258. (Pubitemid 29456893)
49. Kornblihtt, A. R. (2007). Coupling transcription and alternative splicing. Advances in Experimental Medicine and Biology, 623, 175-189.
50. Sims, R. J., 3rd, Millhouse, S., Chen, C. F., Lewis, B. A., Erdjument-Bromage, H., Tempst, P., et al. (2007). Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Molecular Cell, 28, 665-676. (Pubitemid 350137805)
51. Tilgner, H., Nikolaou, C., Althammer, S., Sammeth, M., Beato, M., Valcarcel, J., et al. (2009). Nucleosome positioning as a determinant of exon recognition. Nature Structural & Molecular Biology, 16, 996-1001.
52. Schwartz, S., Gal-Mark, N., Kfir, N., Oren, R., Kim, E., & Ast, G. (2009). Alu exonization events reveal features required for precise recognition of exons by the splicing machinery. PLoS Computational Biology, 5, e1000300.
53. Luco, R. F., Allo, M., Schor, I. E., Kornblihtt, A. R., & Misteli, T. (2011). Epigenetics in alternative Pre-mRNA splicing. Cell, 144, 16-26.
54. Luo, M. J., & Reed, R. (1999). Splicing is required for rapid and efficient mRNA export in metazoans. Proceedings of the National Academy of Sciences of the United States of America, 96, 14937-14942. (Pubitemid 30019743)
55. Rafiq, M., Suen, C. K., Choudhury, N., Joannou, C. L., White, K. N., & Evans, R. W. (1997). Expression of recombinant human ceruloplasmin-an absolute requirement for splicing signals in the expression cassette. FEBS Letters, 407, 132-136. (Pubitemid 27199479)
56. Valencia, P., Dias, A. P., & Reed, R. (2008). Splicing promotes rapid and efficient mRNA export in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America, 105, 3386-3391. (Pubitemid 351723562)
57. Zhou, Z., Luo, M. J., Straesser, K., Katahira, J., Hurt, E., & Reed, R. (2000). The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans. Nature, 407, 401-405.
58. Luo, M. L., Zhou, Z., Magni, K., Christoforides, C., Rappsilber, J., Mann, M., et al. (2001). Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature, 413, 644-647. (Pubitemid 32964065)
59. Le Hir, H., Gatfield, D., Izaurralde, E., & Moore, M. J. (2001). The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO Journal, 20, 4987-4997. (Pubitemid 32848650)
60. Zolotukhin, A. S., Tan, W., Bear, J., Smulevitch, S., & Felber, B. K. (2002). U2AF participates in the binding of TAP (NXF1) to mRNA. The Journal of Biological Chemistry, 277, 3935-3942. (Pubitemid 34968646)
61. Le Hir, H., Izaurralde, E., Maquat, L. E., & Moore, M. J. (2000). The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO Journal, 19, 6860-6869. (Pubitemid 32011679)
62. Le Hir, H., Moore, M. J., & Maquat, L. E. (2000). Pre-mRNA splicing alters mRNP composition: Evidence for stable association of proteins at exon-exon junctions. Genes and Development, 14, 1098-1108. (Pubitemid 30324423)
63. Reed, R., & Hurt, E. (2002). A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell, 108, 523-531. (Pubitemid 34260877)
64. Tange, T. O., Nott, A., & Moore, M. J. (2004). The ever-increasing complexities of the exon junction complex. Current Opinion in Cell Biology, 16, 279-284. (Pubitemid 38610408)
65. Wiegand, H. L., Lu, S., & Cullen, B. R. (2003). Exon junction complexes mediate the enhancing effect of splicing on mRNA expression. Proceedings of the National Academy of Sciences of the United States of America, 100, 11327-11332. (Pubitemid 37205934)
66. Gatfield, D., & Izaurralde, E. (2002). REF1/Aly and the additional exon junction complex proteins are dispensable for nuclear mRNA export. Journal of Cell Biology, 159, 579-588.
67. Lei, E. P., Krebber, H., & Silver, P. A. (2001). Messenger RNAs are recruited for nuclear export during transcription. Genes and Development, 15, 1771-1782. (Pubitemid 32905635)
68. Strasser, K., Masuda, S., Mason, P., Pfannstiel, J., Oppizzi, M., Rodriguez-Navarro, S., et al. (2002). TREX is a conserved complex coupling transcription with messenger RNA export. Nature, 417, 304-308. (Pubitemid 34534714)
69. Zenklusen, D., Vinciguerra, P., Wyss, J. C., & Stutz, F. (2002). Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p. Molecular and Cellular Biology, 22, 8241-8253. (Pubitemid 35304057)
70. Rodrigues, J. P., Rode, M., Gatfield, D., Blencowe, B. J., Carmo-Fonseca, M., & Izaurralde, E. (2001). REF proteins mediate the export of spliced and unspliced mRNAs from the nucleus. Proceedings of the National Academy of Sciences of the United States of America, 98, 1030-1035. (Pubitemid 32121181)
71. Wang, H. F., Feng, L., & Niu, D. K. (2007). Relationship between mRNA stability and intron presence. Biochemical and Biophysical Research Communications, 354, 203-208. (Pubitemid 46123220)
72. Martinez-Contreras, R., Cloutier, P., Shkreta, L., Fisette, J. F., Revil, T., & Chabot, B. (2007). hnRNP proteins and splicing control. Advances in Experimental Medicine and Biology, 623, 123-147.
73. Han, S. P., Tang, Y. H., & Smith, R. (2010). Functional diversity of the hnRNPs: Past, present and perspectives. Biochemical Journal, 430, 379-392.
74. Braddock, M., Muckenthaler, M., White, M. R., Thorburn, A. M., Sommerville, J., Kingsman, A. J., et al. (1994). Intron-less RNA injected into the nucleus of Xenopus oocytes accesses a regulated translation control pathway. Nucleic Acids Research, 22, 5255-5264.
75. Matsumoto, K., Wassarman, K. M., & Wolffe, A. P. (1998). Nuclear history of a pre-mRNA determines the translational activity of cytoplasmic mRNA. EMBO Journal, 17, 2107-2121. (Pubitemid 28154539)
76. Noe, V., MacKenzie, S., & Ciudad, C. J. (2003). An intron is required for dihydrofolate reductase protein stability. The Journal of Biological Chemistry, 278, 38292-38300. (Pubitemid 37221720)
77. Gudikote, J. P., Imam, J. S., Garcia, R. F., & Wilkinson, M. F. (2005). RNA splicing promotes translation and RNA surveillance. Nature Structural & Molecular Biology, 12, 801-809. (Pubitemid 43086255)
78. Nott, A., Le Hir, H., & Moore, M. J. (2004). Splicing enhances translation in mammalian cells: An additional function of the exon junction complex. Genes and Development, 18, 210-222. (Pubitemid 38141788)
79. Long, J. C., & Caceres, J. F. (2009). The SR protein family of splicing factors: Master regulators of gene expression. Biochemical Journal, 417, 15-27.
80. Shepard, P. J., & Hertel, K. J. (2009). The SR protein family. Genome Biology, 10, 242.
81. Sanford, J. R., Gray, N. K., Beckmann, K., & Caceres, J. F. (2004). A novel role for shuttling SR proteins in mRNA translation. Genes and Development, 18, 755-768. (Pubitemid 38480888)
82. Sun, S., Zhang, Z., Sinha, R., Karni, R., & Krainer, A. R. (2010). SF2/ASF autoregulation involves multiple layers of post-tran-scriptional and translational control. Nature Structural & Molecular Biology, 17, 306-312.
83. Ostareck, D. H., Ostareck-Lederer, A., Wilm, M., Thiele, B. J., Mann, M., & Hentze, M. W. (1997). mRNA silencing in ery-throid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3 end. Cell, 89, 597-606. (Pubitemid 27511770)
84. Chang, C. Y., Hong, W. W., Chong, P., & Wu, S. C. (2006). Influence of intron and exon splicing enhancers on mammalian cell expression of a truncated spike protein of SARS-CoV and its implication for subunit vaccine development. Vaccine, 24, 1132-1141. (Pubitemid 43202259)
85. Zago, P., Baralle, M., Ayala, Y. M., Skoko, N., Zacchigna, S., Buratti, E., et al. (2009). Improving human interferon-beta production in mammalian cell lines by insertion of an intronic sequence within its naturally uninterrupted gene. Biotechnology and Applied Biochemistry, 52, 191-198.
86. Lacy-Hulbert, A., Thomas, R., Li, X. P., Lilley, C. E., Coffin, R. S., & Roes, J. (2001). Interruption of coding sequences by het-erologous introns can enhance the functional expression of recombinant genes. Gene Therapy, 8, 649-653. (Pubitemid 32422060)
87. Colwill, K., Wells, C. D., Elder, K., Goudreault, M., Hersi, K., Kulkarni, S., et al. (2006). Modification of the creator recombination system for proteomics applications-improved expression by addition of splice sites. BMC Biotechnology, 6, 13.