Sounds of silence: Synonymous nucleotides as a key to biological regulation and complexity

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2073-2094

  Shabalina, Svetlana A ^a   Spiridonov, Nikolay A ^b   Kashina, Anna ^c  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; RIBOSOME RNA; TRANSFER RNA;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BASE PAIRING; CAENORHABDITIS ELEGANS; CODON; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; EUKARYOTE; GENE EXPRESSION REGULATION; GENETIC CODE; GENETIC CONSERVATION; GENETIC PARAMETERS; GENETIC REGULATION; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN RNA BINDING; REVIEW; RNA FOLDING; RNA HYBRIDIZATION; RNA SELECTION PRESSURE; RNA SEQUENCE; RNA SPLICING; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; START CODON; STOP CODON;

CODON; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; NUCLEOTIDES; PROTEIN BIOSYNTHESIS; PROTEINS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA FOLDING; RNA STABILITY; RNA, MESSENGER;

EUKARYOTA; PROKARYOTA;

EID: 84876348105     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1205     Document Type: Review

References (221)

1. Claverie, J.M. (2001) Gene number What if there are only 30, 000 human genes? Science, 291, 1255-1257.
2. Pennisi, E. (2003) Human genome. A low number wins the GeneSweep Pool. Science, 300, 1484.
3. Stein, L.D. (2004) Human genome: end of the beginning. Nature, 431, 915-916.
4. Shabalina, S.A. and Spiridonov, N.A. (2004) The mammalian transcriptome and the function of non-coding DNA sequences. Genome Biol., 5, 105.
5. Sultan, M., Schulz, M.H., Richard, H., Magen, A., Klingenhoff, A., Scherf, M., Seifert, M., Borodina, T., Soldatov, A., Parkhomchuk, D. et al. (2008) A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science, 321, 956-960.
6. Shabalina, S.A., Spiridonov, A.N., Spiridonov, N.A. and Koonin, E.V. (2010) Connections between alternative transcription and alternative splicing in mammals. Genome Biol. Evol., 2, 791-799.
7. Dethoff, E.A., Chugh, J., Mustoe, A.M. and Al-Hashimi, H.M. (2012) Functional complexity and regulation through RNA dynamics. Nature, 482, 322-330.
8. Plotkin, J.B. and Kudla, G. (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat. Rev. Genet., 12, 32-42.
9. Chamary, J.V., Parmley, J.L. and Hurst, L.D. (2006) Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat. Rev. Genet., 7, 98-108.
10. Shabalina, S.A., Ogurtsov, A.Y. and Spiridonov, N.A. (2006) A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res., 34, 2428-2437.
11. Parmley, J.L. and Hurst, L.D. (2007) How do synonymous mutations affect fitness? Bioessays, 29, 515-519.
12. Itzkovitz, S., Hodis, E. and Segal, E. (2010) Overlapping codes within protein-coding sequences. Genome Res., 20, 1582-1589.
13. Tranque, P., Hu, M.C., Edelman, G.M. and Mauro, V.P. (1998) rRNA complementarity within mRNAs: a possible basis for mRNA-ribosome interactions and translational control. Proc. Natl Acad. Sci. USA, 95, 12238-12243.
14. Matveeva, O.V. and Shabalina, S.A. (1993) Intermolecular mRNA-rRNA hybridization and the distribution of potential interaction regions in murine 18S rRNA. Nucleic Acids Res., 21, 1007-1011.
15. Salmena, L., Poliseno, L., Tay, Y., Kats, L. and Pandolfi, P.P. (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell, 146, 353-358.
16. Chen, S.L., Lee, W., Hottes, A.K., Shapiro, L. and McAdams, H.H. (2004) Codon usage between genomes is constrained by genomewide mutational processes. Proc. Natl Acad. Sci. USA, 101, 3480-3485.
17. Katz, L. and Burge, C.B. (2003) Widespread selection for local RNA secondary structure in coding regions of bacterial genes. Genome Res., 13, 2042-2051.
18. Carlini, D.B. (2005) Context-dependent codon bias and messenger RNA longevity in the yeast transcriptome. Mol. Biol. Evol., 22, 1403-1411.
19. Jia, M., Luo, L. and Liu, C. (2004) Statistical correlation between protein secondary structure and messenger RNA stem-loop structure. Biopolymers, 73, 16-26.
20. Lobry, J.R. (1996) Asymmetric substitution patterns in the two DNA strands of bacteria. Mol. Biol. Evol., 13, 660-665.
21. Francino, M.P. and Ochman, H. (2001) Deamination as the basis of strand-asymmetric evolution in transcribed Escherichia coli sequences. Mol. Biol. Evol., 18, 1147-1150.
22. Hershberg, R. and Petrov, D.A. (2008) Selection on codon bias. Annu. Rev. Genet., 42, 287-299.
23. Kimura, M. (1968) Evolutionary rate at the molecular level. Nature, 217, 624-626.
24. Cartegni, L., Chew, S.L. and Krainer, A.R. (2002) Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet., 3, 285-298.
25. Buratti, E., Muro, A.F., Giombi, M., Gherbassi, D., Iaconcig, A. and Baralle, F.E. (2004) RNA folding affects the recruitment of SR proteins by mouse and human polypurinic enhancer elements in the fibronectin EDA exon. Mol. Cell. Biol., 24, 1387-1400.
26. Fairbrother, W.G., Holste, D., Burge, C.B. and Sharp, P.A. (2004) Single nucleotide polymorphism-based validation of exonic splicing enhancers. PLoS Biol., 2, E268.
27. Pagani, F. and Baralle, F.E. (2004) Genomic variants in exons and introns: identifying the splicing spoilers. Nat. Rev. Genet., 5, 389-396.
28. Xing, Y. and Lee, C. (2005) Evidence of functional selection pressure for alternative splicing events that accelerate evolution of protein subsequences. Proc. Natl Acad. Sci. USA, 102, 13526-13531.
29. Nackley, A.G., Shabalina, S.A., Tchivileva, I.E., Satterfield, K., Korchynskyi, O., Makarov, S.S., Maixner, W. and Diatchenko, L. (2006) Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science, 314, 1930-1933.
30. Akashi, H., Kliman, R.M. and Eyre-Walker, A. (1998) Mutation pressure, natural selection, and the evolution of base composition in Drosophila. Genetica, 102-103, 49-60.
31. Bulmer, M. (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics, 129, 897-907.
32. Duret, L. (2002) Evolution of synonymous codon usage in metazoans. Curr. Opin. Genet. Dev., 12, 640-649.
33. Hershberg, R. and Petrov, D.A. (2009) General rules for optimal codon choice. PLoS Genet., 5, e1000556.
34. Kondrashov, F.A., Ogurtsov, A.Y. and Kondrashov, A.S. (2006) Selection in favor of nucleotides G and C diversifies evolution rates and levels of polymorphism at mammalian synonymous sites. J. Theor. Biol., 240, 616-626.
35. Eyre-Walker, A. (1999) Evidence of selection on silent site base composition in mammals: potential implications for the evolution of isochores and junk DNA. Genetics, 152, 675-683.
36. Smith, N.G. and Eyre-Walker, A. (2001) Synonymous codon bias is not caused by mutation bias in G+C-rich genes in humans. Mol. Biol. Evol., 18, 982-986.
37. Hartl, D.L., Moriyama, E.N. and Sawyer, S.A. (1994) Selection intensity for codon bias. Genetics, 138, 227-234.
38. Najafabadi, H.S., Goodarzi, H. and Salavati, R. (2009) Universal function-specificity of codon usage. Nucleic Acids Res., 37, 7014-7023.
39. Rocha, E.P. (2006) The quest for the universals of protein evolution. Trends Genet., 22, 412-416.
40. Shabalina, S.A., Ogurtsov, A.Y., Spiridonov, A.N., Novichkov, P.S., Spiridonov, N.A. and Koonin, E.V. (2010) Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Mol. Biol. Evol., 27, 1745-1749.
41. Ikemura, T. (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol., 2, 13-34.
42. Bulmer, M. (1987) Coevolution of codon usage and transfer RNA abundance. Nature, 325, 728-730.
43. Duret, L. (2000) tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet., 16, 287-289.
44. Akashi, H. (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics, 136, 927-935.
45. Sharp, P.M., Bailes, E., Grocock, R.J., Peden, J.F. and Sockett, R.E. (2005) Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res., 33, 1141-1153.
46. Pedersen, S. (1984) Escherichia coli ribosomes translate in vivo with variable rate. EMBO J., 3, 2895-2898.
47. Varenne, S., Buc, J., Lloubes, R. and Lazdunski, C. (1984) Translation is a non-uniform process. Effect of tRNA availability on the rate of elongation of nascent polypeptide chains. J. Mol. Biol., 180, 549-576.
48. Sorensen, M.A. and Pedersen, S. (1991) Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. J. Mol. Biol., 222, 265-280.
49. Curran, J.F. and Yarus, M. (1989) Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J. Mol. Biol., 209, 65-77.
50. Sorensen, M.A., Kurland, C.G. and Pedersen, S. (1989) Codon usage determines translation rate in Escherichia coli. J. Mol. Biol., 207, 365-377.
51. Whittle, C.A., Sun, Y. and Johannesson, H. (2012) Genome-wide selection on codon usage at the population level in the fungal model organism Neurospora crassa. Mol. Biol. Evol., 29, 1975-1986.
52. dos Reis, M., Savva, R. and Wernisch, L. (2004) Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res., 32, 5036-5044.
53. Chamary, J.V. and Hurst, L.D. (2004) Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: evidence for selectively driven codon usage. Mol. Biol. Evol., 21, 1014-1023.
54. Smith, D.W. and McNamara, A.L. (1971) Specialization of rabbit reticulocyte transfer RNA content for hemoglobin synthesis. Science, 171, 577-579.
55. Smith, D.W., Meltzer, V.N. and McNamara, A.L. (1974) A comparison of rabbit liver and reticulocyte transfer RNA: evidence of unique species in reticulocytes. Biochim. Biophys. Acta, 349, 366-375.
56. Comeron, J.M. (2004) Selective and mutational patterns associated with gene expression in humans: influences on synonymous composition and intron presence. Genetics, 167, 1293-1304.
57. Urrutia, A.O. and Hurst, L.D. (2001) Codon usage bias covaries with expression breadth and the rate of synonymous evolution in humans, but this is not evidence for selection. Genetics, 159, 1191-1199.
58. Urrutia, A.O. and Hurst, L.D. (2003) The signature of selection mediated by expression on human genes. Genome Res., 13, 2260-2264.
59. Kanaya, S., Yamada, Y., Kinouchi, M., Kudo, Y. and Ikemura, T. (2001) Codon usage and tRNA genes in eukaryotes: correlation of codon usage diversity with translation efficiency and with CG-dinucleotide usage as assessed by multivariate analysis. J. Mol. Evol., 53, 290-298.
60. Lavner, Y. and Kotlar, D. (2005) Codon bias as a factor in regulating expression via translation rate in the human genome. Gene, 345, 127-138.
61. Misawa, K. and Kikuno, R.F. (2011) Relationship between amino acid composition and gene expression in the mouse genome. BMC Res. Notes, 4, 20.
62. Singh, N.D., Bauer DuMont, V.L., Hubisz, M.J., Nielsen, R. and Aquadro, C.F. (2007) Patterns of mutation and selection at synonymous sites in Drosophila. Mol. Biol. Evol., 24, 2687-2697.
63. Thanaraj, T.A. and Argos, P. (1996) Protein secondary structural types are differentially coded on messenger RNA. Protein Sci., 5, 1973-1983.
64. Komar, A.A., Lesnik, T. and Reiss, C. (1999) Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation. FEBS Lett., 462, 387-391.
65. Drummond, D.A. and Wilke, C.O. (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell, 134, 341-352.
66. Stoletzki, N. and Eyre-Walker, A. (2007) Synonymous codon usage in Escherichia coli: selection for translational accuracy. Mol. Biol. Evol., 24, 374-381.
67. Gingold, H. and Pilpel, Y. (2011) Determinants of translation efficiency and accuracy. Mol. Syst. Biol., 7, 481.
68. Zhou, T., Weems, M. and Wilke, C.O. (2009) Translationally optimal codons associate with structurally sensitive sites in proteins. Mol. Biol. Evol., 26, 1571-1580.
69. Resch, A.M., Carmel, L., Marino-Ramirez, L., Ogurtsov, A.Y., Shabalina, S.A., Rogozin, I.B. and Koonin, E.V. (2007) Widespread positive selection in synonymous sites of mammalian genes. Mol. Biol. Evol., 24, 1821-1831.
70. Shields, D.C., Sharp, P.M., Higgins, D.G. and Wright, F. (1988) "Silent" sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol. Biol. Evol., 5, 704-716.
71. Botzman, M. and Margalit, H. (2011) Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biol., 12, R109.
72. Withers, M., Wernisch, L. and dos Reis, M. (2006) Archaeology and evolution of transfer RNA genes in the Escherichia coli genome. RNA, 12, 933-942.
73. Gonos, E.S. and Goddard, J.P. (1990) Human tRNAGlu genes: their copy number and organisation. FEBS Lett., 276, 138-142.
74. Dong, H., Nilsson, L. and Kurland, C.G. (1996) Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J. Mol. Biol., 260, 649-663.
75. Kanaya, S., Yamada, Y., Kudo, Y. and Ikemura, T. (1999) Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene, 238, 143-155.
76. Agris, P.F., Vendeix, F.A. and Graham, W.D. (2007) tRNA's wobble decoding of the genome: 40 years of modification. J. Mol. Biol., 366, 1-13.
77. Novoa, E.M., Pavon-Eternod, M., Pan, T. and Ribas de Pouplana, L. (2012) A role for tRNA modifications in genome structure and codon usage. Cell, 149, 202-213.
78. Moura, G.R., Pinheiro, M., Freitas, A., Oliveira, J.L., Frommlet, J.C., Carreto, L., Soares, A.R., Bezerra, A.R. and Santos, M.A. (2011) Species-specific codon context rules unveil non-neutrality effects of synonymous mutations. PLoS One, 6, e26817.
79. Lipman, D.J. and Wilbur, W.J. (1984) Interaction of silent and replacement changes in eukaryotic coding sequences. J. Mol. Evol., 21, 161-167.
80. Trotta, E. (2011) The 3-base periodicity and codon usage of coding sequences are correlated with gene expression at the level of transcription elongation. PLoS One, 6, e21590.
81. White, H.B. 3rd, Laux, B.E. and Dennis, D. (1972) Messenger RNA structure: compatibility of hairpin loops with protein sequence. Science, 175, 1264-1266.
82. Fitch, W.M. (1974) The large extent of putative secondary nucleic acid structure in random nucleotide sequences or amino acid derived messenger-RNA. J. Mol. Evol., 3, 279-291.
83. Meyer, I.M. and Miklos, I. (2005) Statistical evidence for conserved, local secondary structure in the coding regions of eukaryotic mRNAs and pre-mRNAs. Nucleic Acids Res., 33, 6338-6348.
84. Sharp, P.M., Averof, M., Lloyd, A.T., Matassi, G. and Peden, J.F. (1995) DNA sequence evolution: the sounds of silence. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 349, 241-247.
85. Mita, K., Ichimura, S., Zama, M. and James, T.C. (1988) Specific codon usage pattern and its implications on the secondary structure of silk fibroin mRNA. J. Mol. Biol., 203, 917-925.
86. Zama, M. (1999) Correlation between mRNA structure of the coding region and translational pauses. Nucleic Acids Symp. Ser., 81-82.
87. Kozak, M. (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene, 299, 1-34.
88. Seffens, W. and Digby, D. (1999) mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. Nucleic Acids Res., 27, 1578-1584.
89. 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.
90. Shabalina, S.A., Ogurtsov, A.Y. and Spiridonov, N.A. (2007) Periodic pattern of secondary structures in prokaryotic and eukaryotic mRNAs. FEBS J., 274, 366-366.
91. Wan, Y., Qu, K., Ouyang, Z., Kertesz, M., Li, J., Tibshirani, R., Makino, D.L., Nutter, R.C., Segal, E. and Chang, H.Y. (2012) Genome-wide Measurement of RNA Folding Energies. Mol. Cell, 48, 169-181.
92. Kertesz, M., Wan, Y., Mazor, E., Rinn, J.L., Nutter, R.C., Chang, H.Y. and Segal, E. (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature, 467, 103-107.
93. Shabalina, S.A., Ogurtsov, A.Y., Rogozin, I.B., Koonin, E.V. and Lipman, D.J. (2004) Comparative analysis of orthologous eukaryotic mRNAs: potential hidden functional signals. Nucleic Acids Res., 32, 1774-1782.
94. Gu, W., Zhou, T. and Wilke, C.O. (2010) A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes. PLoS Comput. Biol., 6, e1000664.
95. Kudla, G., Murray, A.W., Tollervey, D. and Plotkin, J.B. (2009) Coding-sequence determinants of gene expression in Escherichia coli. Science, 324, 255-258.
96. Diatchenko, L., Slade, G.D., Nackley, A.G., Bhalang, K., Sigurdsson, A., Belfer, I., Goldman, D., Xu, K., Shabalina, S.A., Shagin, D. et al. (2005) Genetic basis for individual variations in pain perception and the development of a chronic pain condition. Hum. Mol. Genet., 14, 135-143.
97. Tsao, D., Shabalina, S.A., Gauthier, J., Dokholyan, N.V. and Diatchenko, L. (2011) Disruptive mRNA folding increases translational efficiency of catechol-O-methyltransferase variant. Nucleic Acids Res., 39, 6201-6212.
98. Bonnefoy, N., Bsat, N. and Fox, T.D. (2001) Mitochondrial translation of Saccharomyces cerevisiae COX2 mRNA is controlled by the nucleotide sequence specifying the pre-Cox2p leader peptide. Mol. Cell. Biol., 21, 2359-2372.
99. Williams, E.H. and Fox, T.D. (2003) Antagonistic signals within the COX2 mRNA coding sequence control its translation in Saccharomyces cerevisiae mitochondria. RNA, 9, 419-431.
100. Duan, J., Wainwright, M.S., Comeron, J.M., Saitou, N., Sanders, A.R., Gelernter, J. and Gejman, P.V. (2003) Synonymous mutations in the human dopamine receptor D2 (DRD2) affect mRNA stability and synthesis of the receptor. Hum. Mol. Genet., 12, 205-216.
101. Shen, L.X., Basilion, J.P. and Stanton, V.P. Jr (1999) Single-nucleotide polymorphisms can cause different structural folds of mRNA. Proc. Natl Acad. Sci. USA, 96, 7871-7876.
102. Duan, J. and Antezana, M.A. (2003) Mammalian mutation pressure, synonymous codon choice, and mRNA degradation. J. Mol. Evol., 57, 694-701.
103. Zhang, F., Saha, S., Shabalina, S.A. and Kashina, A. (2010) Differential arginylation of actin isoforms is regulated by coding sequence-dependent degradation. Science, 329, 1534-1537.
104. Karakozova, M., Kozak, M., Wong, C.C., Bailey, A.O., Yates, J.R. 3rd, Mogilner, A., Zebroski, H. and Kashina, A. (2006) Arginylation of beta-actin regulates actin cytoskeleton and cell motility. Science, 313, 192-196.
105. Tsai, C.J., Sauna, Z.E., Kimchi-Sarfaty, C., Ambudkar, S.V., Gottesman, M.M. and Nussinov, R. (2008) Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. J. Mol. Biol., 383, 281-291.
106. Kimchi-Sarfaty, C., Oh, J.M., Kim, I.W., Sauna, Z.E., Calcagno, A.M., Ambudkar, S.V. and Gottesman, M.M. (2007) A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science, 315, 525-528.
107. Shabalina, S.A. (2002) [Region of intermolecular complementarity in Escherichia coli 16S rRNA, mRNA, and tRNA molecules]. Mol. Biol. (Mosk), 36, 460-465.
108. Nechipurenko Iu, D., Popov, N.V., Shabalina, S.A., Isaev, M.A. and Matveeva, O.V. (1995) [A model of multiple contacts, describing the interaction of rRNA sites with mRNA]. Biofizika, 40, 1208-1213.
109. Li, G.W., Oh, E. and Weissman, J.S. (2012) The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature, 484, 538-541.
110. Barendt, P.A., Shah, N.A., Barendt, G.A. and Sarkar, C.A. (2012) Broad-specificity mRNA-rRNA complementarity in efficient protein translation. PLoS Genet., 8, e1002598.
111. Kozak, M. (1989) The scanning model for translation: an update. J. Cell. Biol, 108, 229-241.
112. Sarge, K.D. and Maxwell, E.S. (1991) Intermolecular hybridization of 5S rRNA with 18S rRNA: identification of a 50-terminally-located nucleotide sequence in mouse 5S rRNA which base-pairs with two specific complementary sequences in 18S rRNA. Biochim. Biophys. Acta, 1088, 57-70.
113. Mauro, V.P. and Edelman, G.M. (1997) rRNA-like sequences occur in diverse primary transcripts: implications for the control of gene expression. Proc. Natl Acad. Sci. USA, 94, 422-427.
114. Ogurtsov, A.Y., Marino-Ramirez, L., Johnson, G.R., Landsman, D., Shabalina, S.A. and Spiridonov, N.A. (2008) Expression patterns of protein kinases correlate with gene architecture and evolutionary rates. PLoS One, 3, e3599.
115. Panopoulos, P. and Mauro, V.P. (2008) Antisense masking reveals contributions of mRNA-rRNA base pairing to translation of Gtx and FGF2 mRNAs. J. Biol. Chem., 283, 33087-33093.
116. Dresios, J., Chappell, S.A., Zhou, W. and Mauro, V.P. (2006) An mRNA-rRNA base-pairing mechanism for translation initiation in eukaryotes. Nat. Struct. Mol. Biol., 13, 30-34.
117. Sauna, Z.E. and Kimchi-Sarfaty, C. (2011) Understanding the contribution of synonymous mutations to human disease. Nat. Rev. Genet., 12, 683-691.
118. Gu, W., Wang, X., Zhai, C., Xie, X. and Zhou, T. (2012) Selection on synonymous sites for increased accessibility around mirna binding sites in plants. Mol. Biol. Evol., 29, 3037-3044.
119. Lewis, B.P., Burge, C.B. and Bartel, D.P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15-20.
120. Nakamoto, M., Jin, P., O'Donnell, W.T. and Warren, S.T. (2005) Physiological identification of human transcripts translationally regulated by a specific microRNA. Hum. Mol. Genet., 14, 3813-3821.
121. Stark, A., Lin, M.F., Kheradpour, P., Pedersen, J.S., Parts, L., Carlson, J.W., Crosby, M.A., Rasmussen, M.D., Roy, S., Deoras, A.N. et al. (2007) Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature, 450, 219-232.
122. Shabalina, S.A. and Koonin, E.V. (2008) Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol., 23, 578-587.
123. Duursma, A.M., Kedde, M., Schrier, M., le Sage, C. and Agami, R. (2008) miR-148 targets human DNMT3b protein coding region. RNA, 14, 872-877.
124. Forman, J.J., Legesse-Miller, A. and Coller, H.A. (2008) A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc. Natl Acad. Sci. USA, 105, 14879-14884.
125. Rigoutsos, I. (2009) New tricks for animal microRNAS: targeting of amino acid coding regions at conserved and nonconserved sites. Cancer Res., 69, 3245-3248.
126. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
127. Schnall-Levin, M., Rissland, O.S., Johnston, W.K., Perrimon, N., Bartel, D.P. and Berger, B. (2011) Unusually effective microRNA targeting within repeat-rich coding regions of mammalian mRNAs. Genome Res., 21, 1395-1403.
128. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S. and Johnson, J.M. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature, 433, 769-773.
129. Grimson, A., Farh, K.K., Johnston, W.K., Garrett-Engele, P., Lim, L.P. and Bartel, D.P. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell, 27, 91-105.
130. Baek, D., Villen, J., Shin, C., Camargo, F.D., Gygi, S.P. and Bartel, D.P. (2008) The impact of microRNAs on protein output. Nature, 455, 64-71.
131. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature, 455, 58-63.
132. Elcheva, I., Goswami, S., Noubissi, F.K. and Spiegelman, V.S. (2009) CRD-BP protects the coding region of betaTrCP1 mRNA from miR-183-mediated degradation. Mol. Cell, 35, 240-246.
133. Huang, S., Wu, S., Ding, J., Lin, J., Wei, L., Gu, J. and He, X. (2010) MicroRNA-181a modulates gene expression of zinc finger family members by directly targeting their coding regions. Nucleic Acids Res., 38, 7211-7218.
134. Schnall-Levin, M., Zhao, Y., Perrimon, N. and Berger, B. (2010) Conserved microRNA targeting in Drosophila is as widespread in coding regions as in 30UTRs. Proc. Natl Acad. Sci. USA, 107, 15751-15756.
135. Brest, P., Lapaquette, P., Souidi, M., Lebrigand, K., Cesaro, A., Vouret-Craviari, V., Mari, B., Barbry, P., Mosnier, J.F., Hebuterne, X. et al. (2011) A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease. Nat. Genet., 43, 242-245.
136. Pan, Q., Shai, O., Lee, L.J., Frey, B.J. and Blencowe, B.J. (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet., 40, 1413-1415.
137. Yamashita, R., Wakaguri, H., Sugano, S., Suzuki, Y. and Nakai, K. (2010) DBTSS provides a tissue specific dynamic view of Transcription Start Sites. Nucleic Acids Res., 38, D98-D104.
138. Baek, D., Davis, C., Ewing, B., Gordon, D. and Green, P. (2007) Characterization and predictive discovery of evolutionarily conserved mammalian alternative promoters. Genome Res., 17, 145-155.
139. Warf, M.B. and Berglund, J.A. (2010) Role of RNA structure in regulating pre-mRNA splicing. Trends Biochem. Sci., 35, 169-178.
140. Bentley, D.L. (2005) Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr. Opin. Cell Biol., 17, 251-256.
141. Patel, A.A. and Steitz, J.A. (2003) Splicing double: insights from the second spliceosome. Nat. Rev. Mol. Cell Biol., 4, 960-970.
142. Wang, P., Lyman, R.F., Shabalina, S.A., Mackay, T.F. and Anholt, R.R. (2007) Association of polymorphisms in odorant-binding protein genes with variation in olfactory response to benzaldehyde in Drosophila. Genetics, 177, 1655-1665.
143. Wang, Z., Rolish, M.E., Yeo, G., Tung, V., Mawson, M. and Burge, C.B. (2004) Systematic identification and analysis of exonic splicing silencers. Cell, 119, 831-845.
144. Fairbrother, W.G., Yeh, R.F., Sharp, P.A. and Burge, C.B. (2002) Predictive identification of exonic splicing enhancers in human genes. Science, 297, 1007-1013.
145. Chamary, J.V. and Hurst, L.D. (2005) Biased codon usage near intron-exon junctions: selection on splicing enhancers, splice-site recognition or something else? Trends Genet., 21, 256-259.
146. Gray, M.W. (2012) Evolutionary origin of RNA editing. Biochemistry, 51, 5235-5242.
147. Kawahara, Y., Megraw, M., Kreider, E., Iizasa, H., Valente, L., Hatzigeorgiou, A.G. and Nishikura, K. (2008) Frequency and fate of microRNA editing in human brain. Nucleic Acids Res., 36, 5270-5280.
148. Casey, J.L. (2006) RNA editing in hepatitis delta virus. Curr. Top. Microbiol. Immunol., 307, 67-89.
149. Kolakofsky, D., Roux, L., Garcin, D. and Ruigrok, R.W. (2005) Paramyxovirus mRNA editing, the "rule of six" and error catastrophe: a hypothesis. J. Gen. Virol., 86, 1869-1877.
150. Kiran, A. and Baranov, P.V. (2010) DARNED: a DAtabase of RNa EDiting in humans. Bioinformatics, 26, 1772-1776.
151. Park, E., Williams, B., Wold, B.J. and Mortazavi, A. (2012) RNA editing in the human ENCODE RNA-seq data. Genome Res., 22, 1626-1633.
152. Lev-Maor, G., Sorek, R., Levanon, E.Y., Paz, N., Eisenberg, E. and Ast, G. (2007) RNA-editing-mediated exon evolution. Genome Biol., 8, R29.
153. Sorek, R. (2007) The birth of new exons: mechanisms and evolutionary consequences. RNA, 13, 1603-1608.
154. Maas, S. and Gommans, W.M. (2009) Novel exon of mammalian ADAR2 extends open reading frame. PLoS One, 4, e4225.
155. Baranov, P.V., Gesteland, R.F. and Atkins, J.F. (2002) Recoding: translational bifurcations in gene expression. Gene, 286, 187-201.
156. Namy, O., Rousset, J.P., Napthine, S. and Brierley, I. (2004) Reprogrammed genetic decoding in cellular gene expression. Mol Cell, 13, 157-168.
157. Paz-Yaacov, N., Levanon, E.Y., Nevo, E., Kinar, Y., Harmelin, A., Jacob-Hirsch, J., Amariglio, N., Eisenberg, E. and Rechavi, G. (2010) Adenosine-to-inosine RNA editing shapes transcriptome diversity in primates. Proc. Natl Acad. Sci. USA, 107, 12174-12179.
158. Howard, M.T., Aggarwal, G., Anderson, C.B., Khatri, S., Flanigan, K.M. and Atkins, J.F. (2005) Recoding elements located adjacent to a subset of eukaryal selenocysteine-specifying UGA codons. EMBO J., 24, 1596-1607.
159. Firth, A.E. and Brierley, I. (2012) Non-canonical translation in RNA viruses. J. Gen. Virol., 93, 1385-1409.
160. Firth, A.E., Wills, N.M., Gesteland, R.F. and Atkins, J.F. (2011) Stimulation of stop codon readthrough: frequent presence of an extended 30 RNA structural element. Nucleic Acids Res., 39, 6679-6691.
161. Ivanov, I.P. and Atkins, J.F. (2007) Ribosomal frameshifting in decoding antizyme mRNAs from yeast and protists to humans: close to 300 cases reveal remarkable diversity despite underlying conservation. Nucleic Acids Res., 35, 1842-1858.
162. Bekaert, M., Ivanov, I.P., Atkins, J.F. and Baranov, P.V. (2008) Ornithine decarboxylase antizyme finder (OAF): fast and reliable detection of antizymes with frameshifts in mRNAs. BMC Bioinformatics, 9, 178.
163. Mazzoni, C. and Falcone, C. (2011) mRNA stability and control of cell proliferation. Biochem. Soc. Trans., 39, 1461-1465.
164. Isken, O. and Maquat, L.E. (2007) Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev., 21, 1833-1856.
165. Gatfield, D., Unterholzner, L., Ciccarelli, F.D., Bork, P. and Izaurralde, E. (2003) Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J., 22, 3960-3970.
166. Hwang, J. and Maquat, L.E. (2011) Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. Curr. Opin. Genet. Dev., 21, 422-430.
167. van Hoof, A., Frischmeyer, P.A., Dietz, H.C. and Parker, R. (2002) Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science, 295, 2262-2264.
168. Doma, M.K. and Parker, R. (2006) Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature, 440, 561-564.
169. Zhang, Z., Zhou, L., Hu, L., Zhu, Y., Xu, H., Liu, Y., Chen, X., Yi, X., Kong, X. and Hurst, L.D. (2010) Nonsense-mediated decay targets have multiple sequence-related features that can inhibit translation. Mol. Syst. Biol., 6, 442.
170. Zhang, S., Ruiz-Echevarria, M.J., Quan, Y. and Peltz, S.W. (1995) Identification and characterization of a sequence motif involved in nonsense-mediated mRNA decay. Mol. Cell. Biol., 15, 2231-2244.
171. Ruiz-Echevarria, M.J., Munshi, R., Tomback, J., Kinzy, T.G. and Peltz, S.W. (2001) Characterization of a general stabilizer element that blocks deadenylation-dependent mRNA decay. J. Biol. Chem., 276, 30995-31003.
172. Grosset, C., Chen, C.Y., Xu, N., Sonenberg, N., Jacquemin-Sablon, H. and Shyu, A.B. (2000) A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell, 103, 29-40.
173. Wilusz, C.J., Wormington, M. and Peltz, S.W. (2001) The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell. Biol., 2, 237-246.
174. Hennigan, A.N. and Jacobson, A. (1996) Functional mapping of the translation-dependent instability element of yeast MATa lpha1 mRNA. Mol. Cell. Biol., 16, 3833-3843.
175. Zhang, Z., Xin, D., Wang, P., Zhou, L., Hu, L., Kong, X. and Hurst, L.D. (2009) Noisy splicing, more than expression regulation, explains why some exons are subject to nonsense-mediated mRNA decay. BMC Biol., 7, 23.
176. Cusack, B.P., Arndt, P.F., Duret, L. and Roest Crollius, H. (2011) Preventing dangerous nonsense: selection for robustness to transcriptional error in human genes. PLoS Genet., 7, e1002276.
177. de Lima Morais, D.A. and Harrison, P.M. (2010) Large-scale evidence for conservation of NMD candidature across mammals. PLoS One, 5, e11695.
178. Galanello, R. and Cao, A. (1998) Relationship between genotype and phenotype. Thalassemia intermedia. Ann. N. Y. Acad. Sci., 850, 325-333.
179. Bartoszewski, R.A., Jablonsky, M., Bartoszewska, S., Stevenson, L., Dai, Q., Kappes, J., Collawn, J.F. and Bebok, Z. (2010) A synonymous single nucleotide polymorphism in DeltaF508 CFTR alters the secondary structure of the mRNA and the expression of the mutant protein. J. Biol. Chem., 285, 28741-28748.
180. Day, J.W. and Ranum, L.P. (2005) RNA pathogenesis of the myotonic dystrophies. Neuromuscul. Disord., 15, 5-16.
181. Sakaguchi, N., Maeda, K. and Kuwahara, K. (2011) Molecular mechanism of immunoglobulin V-region diversification regulated by transcription and RNA metabolism in antigen-driven B cells. Scand. J. Immunol., 73, 520-526.
182. Kislauskis, E.H., Zhu, X. and Singer, R.H. (1994) Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J. Cell. Biol., 127, 441-451.
183. Jansen, R.P. and Niessing, D. (2012) Assembly of mRNA-protein complexes for directional mRNA transport in eukaryotes-an overview. Curr. Protein. Pept. Sci., 13, 284-293.
184. Ross, A.F., Oleynikov, Y., Kislauskis, E.H., Taneja, K.L. and Singer, R.H. (1997) Characterization of a beta-actin mRNA zipcode-binding protein. Mol Cell Biol, 17, 2158-2165.
185. Pan, F., Huttelmaier, S., Singer, R.H. and Gu, W. (2007) ZBP2 facilitates binding of ZBP1 to beta-actin mRNA during transcription. Mol. Cell. Biol., 27, 8340-8351.
186. Chao, J.A., Patskovsky, Y., Patel, V., Levy, M., Almo, S.C. and Singer, R.H. (2010) ZBP1 recognition of beta-actin zipcode induces RNA looping. Genes Dev., 24, 148-158.
187. Welshhans, K. and Bassell, G.J. (2011) Netrin-1-induced local beta-actin synthesis and growth cone guidance requires zipcode binding protein 1. J. Neurosci., 31, 9800-9813.
188. Sasaki, Y., Welshhans, K., Wen, Z., Yao, J., Xu, M., Goshima, Y., Zheng, J.Q. and Bassell, G.J. (2010) Phosphorylation of zipcode binding protein 1 is required for brain-derived neurotrophic factor signaling of local beta-actin synthesis and growth cone turning. J. Neurosci., 30, 9349-9358.
189. Perycz, M., Urbanska, A.S., Krawczyk, P.S., Parobczak, K. and Jaworski, J. (2011) Zipcode binding protein 1 regulates the development of dendritic arbors in hippocampal neurons. J. Neurosci., 31, 5271-5285.
190. Liao, G., Ma, X. and Liu, G. (2011) An RNA-zipcode-independent mechanism that localizes Dia1 mRNA to the perinuclear ER through interactions between Dia1 nascent peptide and Rho-GTP. J. Cell Sci., 124, 589-599.
191. Lapidus, K., Wyckoff, J., Mouneimne, G., Lorenz, M., Soon, L., Condeelis, J.S. and Singer, R.H. (2007) ZBP1 enhances cell polarity and reduces chemotaxis. J. Cell Sci., 120, 3173-3178.
192. Stohr, N., Lederer, M., Reinke, C., Meyer, S., Hatzfeld, M., Singer, R.H. and Huttelmaier, S. (2006) ZBP1 regulates mRNA stability during cellular stress. J. Cell Biol., 175, 527-534.
193. Warnecke, T., Batada, N.N. and Hurst, L.D. (2008) The impact of the nucleosome code on protein-coding sequence evolution in yeast. PLoS Genet., 4, e1000250.
194. Trifonov, E.N., Volkovich, Z. and Frenkel, Z.M. (2012) Multiple levels of meaning in DNA sequences, and one more. Ann. N. Y. Acad. Sci., 1267, 35-38.
195. Akashi, H. and Eyre-Walker, A. (1998) Translational selection and molecular evolution. Curr. Opin. Genet. Dev., 8, 688-693.
196. Akashi, H. (2003) Translational selection and yeast proteome evolution. Genetics, 164, 1291-1303.
197. Shabalina, S.A., Ogurtsov, A.Y., Kondrashov, V.A. and Kondrashov, A.S. (2001) Selective constraint in intergenic regions of human and mouse genomes. Trends Genet., 17, 373-376.
198. Kondrashov, A.S. and Shabalina, S.A. (2002) Classification of common conserved sequences in mammalian intergenic regions. Hum. Mol. Genet., 11, 669-674.
199. Shabalina, S.A. and Kondrashov, A.S. (1999) Pattern of selective constraint in C. elegans and C. briggsae genomes. Genet Res., 74, 23-30.
200. Xing, Y. and Lee, C. (2006) Can RNA selection pressure distort the measurement of Ka/Ks? Gene, 370, 1-5.
201. Yang, Z. and Bielawski, J.P. (2000) Statistical methods for detecting molecular adaptation. Trends Ecol. Evol., 15, 496-503.
202. Lu, H., Lin, L., Sato, S., Xing, Y. and Lee, C.J. (2009) Predicting functional alternative splicing by measuring RNA selection pressure from multigenome alignments. PLoS Comput. Biol., 5, e1000608.
203. Bazykin, G.A., Kondrashov, F.A., Ogurtsov, A.Y., Sunyaev, S. and Kondrashov, A.S. (2004) Positive selection at sites of multiple amino acid replacements since rat-mouse divergence. Nature, 429, 558-562.
204. Hughes, A.L. and Yeager, M. (1997) Comparative evolutionary rates of introns and exons in murine rodents. J. Mol. Evol., 45, 125-130.
205. Keightley, P.D. and Gaffney, D.J. (2003) Functional constraints and frequency of deleterious mutations in noncoding DNA of rodents. Proc. Natl Acad. Sci. USA, 100, 13402-13406.
206. Webster, M.T. and Smith, N.G. (2004) Fixation biases affecting human SNPs. Trends Genet., 20, 122-126.
207. Li, W.H. (1987) Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. J. Mol. Evol., 24, 337-345.
208. Akashi, H. (1996) Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster. Genetics, 144, 1297-1307.
209. Innan, H. and Stephan, W. (2001) Selection intensity against deleterious mutations in RNA secondary structures and rate of compensatory nucleotide substitutions. Genetics, 159, 389-399.
210. Hellmann, I., Zollner, S., Enard, W., Ebersberger, I., Nickel, B. and Paabo, S. (2003) Selection on human genes as revealed by comparisons to chimpanzee cDNA. Genome Res., 13, 831-837.
211. Watts, J.M., Dang, K.K., Gorelick, R.J., Leonard, C.W., Bess, J.W. Jr, Swanstrom, R., Burch, C.L. and Weeks, K.M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature, 460, 711-716.
212. Sanjuan, R. and Borderia, A.V. (2011) Interplay between RNA structure and protein evolution in HIV-1. Mol Biol Evol, 28, 1333-1338.
213. Lin, M.F., Kheradpour, P., Washietl, S., Parker, B.J., Pedersen, J.S. and Kellis, M. (2011) Locating protein-coding sequences under selection for additional, overlapping functions in 29 mammalian genomes. Genome Res., 21, 1916-1928.
214. Iida, K. and Akashi, H. (2000) A test of translational selection at 'silent' sites in the human genome: base composition comparisons in alternatively spliced genes. Gene, 261, 93-105.
215. Shabalina, S.A., Zaykin, D.V., Gris, P., Ogurtsov, A.Y., Gauthier, J., Shibata, K., Tchivileva, I.E., Belfer, I., Mishra, B., Kiselycznyk, C. et al. (2009) Expansion of the human mu-opioid receptor gene architecture: novel functional variants. Hum. Mol. Genet., 18, 1037-1051.
216. Tuller, T., Waldman, Y.Y., Kupiec, M. and Ruppin, E. (2010) Translation efficiency is determined by both codon bias and folding energy. Proc. Natl Acad. Sci. USA, 107, 3645-3650.
217. Moss, W.N., Priore, S.F. and Turner, D.H. (2011) Identification of potential conserved RNA secondary structure throughout influenza A coding regions. RNA, 17, 991-1011.
218. Stoletzki, N. and Eyre-Walker, A. (2011) The positive correlation between dN/dS and dS in mammals is due to runs of adjacent substitutions. Mol. Biol. Evol., 28, 1371-1380.
219. Lagunez-Otero, J. and Trifonov, E.N. (1992) mRNA periodical infrastructure complementary to the proof-reading site in the ribosome. J. Biomol. Struct. Dyn., 10, 455-464.
220. Wan, Y., Kertesz, M., Spitale, R.C., Segal, E. and Chang, H.Y. (2011) Understanding the transcriptome through RNA structure. Nat. Rev. Genet., 12, 641-655.
221. Bindewald, E., Wendeler, M., Legiewicz, M., Bona, M.K., Wang, Y., Pritt, M.J., Le Grice, S.F. and Shapiro, B.A. (2011) Correlating SHAPE signatures with three-dimensional RNA structures. RNA, 17, 1688-1696.