Diverse forms of RPS9 splicing are part of an evolving autoregulatory circuit

PLoS Genetics

Volumn 8, Issue 3, 2012, Pages

  Plocik, Alex M ^a   Guthrie, Christine ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBOSOME PROTEIN; RPS9 PROTEIN; UNCLASSIFIED DRUG; RIBOSOMAL PROTEIN S9;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; AUTOREGULATION; CIONA INTESTINALIS; COMPARATIVE STUDY; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EXPRESSED SEQUENCE TAG; FUNGAL STRAIN; GENE; GENE CONTROL; GENE DELETION; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; INTRON; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; OPERON; PREDICTION; PROTEIN ENCODING GENE; RPS9 GENE; RPS9A GENE; RPS9B GENE; SACCHAROMYCES CEREVISIAE; ANIMAL; CULTURE TECHNIQUE; GENETICS; MOLECULAR EVOLUTION;

ANIMALIA; CIONA INTESTINALIS; DROSOPHILA MELANOGASTER; EUKARYOTA; HOMO SAPIENS; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

ALTERNATIVE SPLICING; ANIMALS; CELL CULTURE TECHNIQUES; CIONA INTESTINALIS; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION REGULATION; HUMANS; INTRONS; NONSENSE MEDIATED MRNA DECAY; RIBOSOMAL PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION;

EID: 84859224256     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002620     Document Type: Article

References (64)

1. Bon E, Casaregola S, Blandin G, Llorente B, Neuvéglise C, et al. (2003) Molecular evolution of eukaryotic genomes: hemiascomycetous yeast spliceosomal introns. Nucleic Acids Res 31: 1121-1135.
2. Mitrovich QM, Tuch BB, Guthrie C, Johnson AD, (2007) Computational and experimental approaches double the number of known introns in the pathogenic yeast Candida albicans. Genome Res 17: 492-502.
3. Warner JR, (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437-440.
4. Juneau K, Miranda M, Hillenmeyer ME, Nislow C, Davis RW, (2006) Introns regulate RNA and protein abundance in yeast. Genetics 174: 511-518.
5. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C, (2007) Rapid, transcript-specific changes in splicing in response to environmental stress. Mol Cell 27: 928-937.
6. Dabeva MD, Warner JR, (1993) Ribosomal protein L32 of Saccharomyces cerevisiae regulates both splicing and translation of its own transcript. J Biol Chem 268: 19669-19674.
7. Fewell SW, Woolford JL Jr, (1999) Ribosomal protein S14 of Saccharomyces cerevisiae regulates its expression by binding to RPS14B pre-mRNA and to 18S rRNA. Mol Cell Biol 19: 826-834.
8. Dean D, Nomura M, (1980) Feedback regulation of ribosomal protein gene expression in Escherichia coli. Proc Natl Acad Sci USA 77: 3590-3594.
9. Nomura M, Gourse R, Baughman G, (1984) Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem 53: 75-117.
10. Hedges SB, Dudley J, Kumar S, (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22: 2971-2972.
11. Wolfe KH, Shields DC, (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713.
12. 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 USA 104: 1522-1527.
13. Zhang Z, Hesselberth JR, Fields S, (2007) Genome-wide identification of spliced introns using a tiling microarray. Genome Res 17: 503-509.
14. Byrne KP, Wolfe KH, (2005) The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15: 1456-1461.
15. Stajich JE, Dietrich FS, Roy SW, (2007) Comparative genomic analysis of fungal genomes reveals intron-rich ancestors. Genome Biol 8: R223.
16. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C, (2007) Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol 5: e90 doi:10.1371/journal.pbio.0050090.
17. Li Z, Paulovich AG, Woolford JL Jr, (1995) Feedback inhibition of the yeast ribosomal protein gene CRY2 is mediated by the nucleotide sequence and secondary structure of CRY2 pre-mRNA. Mol Cell Biol 15: 6454-6464.
18. Clark TA, Sugnet CW, Ares M Jr, (2002) Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296: 907-910.
19. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, et al. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349.
20. Mitrovich QM, Anderson P, (2000) Unproductively spliced ribosomal protein mRNAs are natural targets of mRNA surveillance in C. elegans. Genes Dev 14: 2173-2184.
21. Cuccurese M, Russo G, Russo A, Pietropaolo C, (2005) Alternative splicing and nonsense-mediated mRNA decay regulate mammalian ribosomal gene expression. Nucleic Acids Res 33: 5965-5977.
22. Ivanov AV, Malygin AA, Karpova GG, (2005) Human ribosomal protein S26 suppresses the splicing of its pre-mRNA. Biochim Biophys Acta 1727: 134-140.
23. Malygin AA, Parakhnevitch NM, Ivanov AV, Eperon IC, Karpova GG, (2007) Human ribosomal protein S13 regulates expression of its own gene at the splicing step by a feedback mechanism. Nucleic Acids Res 35: 6414-6423.
24. Lareau LF, Brooks AN, Soergel DAW, Meng Q, Brenner SE, (2007) The coupling of alternative splicing and nonsense-mediated mRNA decay. Adv Exp Med Biol 623: 190-211.
25. Hansen KD, Lareau LF, Blanchette M, Green RE, Meng Q, et al. (2009) Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila. PLoS Genet 5: e1000525 doi:10.1371/journal.pgen.1000525.
26. Washietl S, Hofacker IL, Stadler PF, (2005) Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci USA 102: 2454-2459.
27. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996-1006.
28. Jeffares DC, Mourier T, Penny D, (2006) The biology of intron gain and loss. Trends Genet 22: 16-22.
29. 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.
30. Spingola M, Grate L, Haussler D, Ares M, (1999) Genome-wide bioinformatic and molecular analysis of introns in Saccharomyces cerevisiae. RNA 5: 221-234.
31. Katinka MD, Duprat S, Cornillot E, Méténier G, Thomarat F, et al. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450-453.
32. Lee RCH, Gill EE, Roy SW, Fast NM, (2010) Constrained intron structures in a microsporidian. Mol Biol Evol 27: 1979-1982.
33. Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, et al. (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410: 1091-1096.
34. Fink GR, (1987) Pseudogenes in yeast? Cell 49: 5-6.
35. Nilsen TW, Graveley BR, (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463.
36. Grund SE, Fischer T, Cabal GG, Antúnez O, Pérez-Ortín JE, et al. (2008) The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. J Cell Biol 182: 897-910.
37. Juneau K, Nislow C, Davis RW, (2009) Alternative splicing of PTC7 in Saccharomyces cerevisiae determines protein localization. Genetics 183: 185-194.
38. Brinster RL, Allen JM, Behringer RR, Gelinas RE, Palmiter RD, (1988) Introns increase transcriptional efficiency in transgenic mice. Proc Natl Acad Sci USA 85: 836-840.
39. Mattox W, Ryner L, Baker BS, (1992) Autoregulation and multifunctionality among trans-acting factors that regulate alternative pre-mRNA processing. J Biol Chem 267: 19023-19026.
40. Lareau LF, Inada M, Green RE, Wengrod JC, Brenner SE, (2007) Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446: 926-929.
41. Ni JZ, Grate L, Donohue JP, Preston C, Nobida N, et al. (2007) Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 21: 708-718.
42. Saltzman AL, Kim YK, Pan Q, Fagnani MM, Maquat LE, et al. (2008) Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol Cell Biol 28: 4320-4330.
43. Tang CK, Draper DE, (1989) Unusual mRNA pseudoknot structure is recognized by a protein translational repressor. Cell 57: 531-536.
44. Sano K, Taguchi A, Furumoto H, Uda T, Itoh T, (1999) Cloning, sequencing, and characterization of ribosomal protein and RNA polymerase genes from the region analogous to the alpha-operon of escherichia coli in halophilic archaea, halobacterium halobium. Biochem Biophys Res Commun 264: 24-28.
45. Von Hippel PH, Kowalczykowski SC, Lonberg N, Newport JW, Paul LS, et al. (1982) Autoregulation of gene expression. Quantitative evaluation of the expression and function of the bacteriophage T4 gene 32 (single-stranded DNA binding) protein system. J Mol Biol 162: 795-818.
46. Rossbach O, Hung L-H, Schreiner S, Grishina I, Heiner M, et al. (2009) Auto- and Cross-Regulation of the hnRNP L Proteins by Alternative Splicing. Mol Cell Biol 29: 1442-1451.
47. Spellman R, Llorian M, Smith CWJ, (2007) Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Mol Cell 27: 420-434.
48. Komili S, Farny NG, Roth FP, Silver PA, (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131: 557-571.
49. Pnueli L, Arava Y, (2007) Genome-wide polysomal analysis of a yeast strain with mutated ribosomal protein S9. BMC Genomics 8: 285.
50. Grundy FJ, Henkin TM, (1991) The rpsD gene, encoding ribosomal protein S4, is autogenously regulated in Bacillus subtilis. J Bacteriol 173: 4595-4602.
51. Shubin N, Tabin C, Carroll S, (2009) Deep homology and the origins of evolutionary novelty. Nature 457: 818-823.
52. Parenteau J, Durand M, Véronneau S, Lacombe A-A, Morin G, et al. (2008) Deletion of many yeast introns reveals a minority of genes that require splicing for function. Mol Biol Cell 19: 1932-1941.
53. Storici F, Durham CL, Gordenin DA, Resnick MA, (2003) Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast. Proc Natl Acad Sci USA 100: 14994-14999.
54. Rogers SL, Rogers GC, (2008) Culture of Drosophila S2 cells and their use for RNAi-mediated loss-of-function studies and immunofluorescence microscopy. Nat Protoc 3: 606-611.
55. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
56. Lemoine S, Combes F, Servant N, Le Crom S, (2006) Goulphar: rapid access and expertise for standard two-color microarray normalization methods. BMC Bioinformatics 7: 467.
57. Rozen S, Skaletsky H, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
58. Cherry JM, Ball C, Weng S, Juvik G, Schmidt R, et al. (1997) Genetic and physical maps of Saccharomyces cerevisiae. Nature 387: 67-73.
59. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
60. Wickham H, (2009) ggplot2: Elegant Graphics for Data Analysis Springer New York.
61. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, (2011) GenBank. Nucleic Acids Res 39: D32-37.
62. R Development Core Team (2011) Development Core Team, R: A language and environment for statistical computing Vienna, Austria R Foundation for Statistical Computing.
63. Hedtke SM, Townsend TM, Hillis DM, (2006) Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Syst Biol 55: 522-529.
64. Sato K, Kato Y, Hamada M, Akutsu T, Asai K, (2011) IPknot: fast and accurate prediction of RNA secondary structures with pseudoknots using integer programming. Bioinformatics 27: i85-93.