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BMC Evol Biol
2005 Feb 13;5:15. doi: 10.1186/1471-2148-5-15.
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The architecture of mammalian ribosomal protein promoters.
Perry RP
.
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BACKGROUND: Mammalian ribosomes contain 79 different proteins encoded by widely scattered single copy genes. Coordinate expression of these genes at transcriptional and post-transcriptional levels is required to ensure a roughly equimolar accumulation of ribosomal proteins. To date, detailed studies of only a very few ribosomal protein (rp) promoters have been made. To elucidate the general features of rp promoter architecture, I made a detailed sequence comparison of the promoter regions of the entire set of orthologous human and mouse rp genes.
RESULTS: A striking evolutionarily conserved feature of most rp genes is the separation by an intron of the sequences involved in transcriptional and translational regulation from the sequences with protein encoding function. Another conserved feature is the polypyrimidine initiator, which conforms to the consensus (Y)2C+1TY(T)2(Y)3. At least 60 % of the rp promoters contain a largely conserved TATA box or A/T-rich motif, which should theoretically have TBP-binding capability. A remarkably high proportion of the promoters contain conserved binding sites for transcription factors that were previously implicated in rp gene expression, namely upstream GABP and Sp1 sites and downstream YY1 sites. Over 80 % of human and mouse rp genes contain a transposable element residue within 900 bp of 5' flanking sequence; very little sequence identity between human and mouse orthologues was evident more than 200 bp upstream of the transcriptional start point.
CONCLUSIONS: This analysis has provided some valuable insights into the general architecture of mammalian rp promoters and has identified parameters that might coordinately regulate the transcriptional activity of certain subsets of rp genes.
Figure 1. The location of insertion elements in the 5'-flanking regions of rp genes. Insertion (ins) elements were identified by the RepeatMasker program in scans of up to one kilobase of sequence 5' of the tsp, and the location of the element nearest to the tsp recorded for 79 human and mouse rp genes [see Additional file 2]. The distance from the tsp was divided into 200 bp intervals, the percentage of rp genes with an element within each interval determined, and the values plotted cumulatively against the distance from the tsp.
Figure 2. Criteria for rp promoter annotation. (a). Quality of the TATA box for TBP binding based on a structural analysis of TBP-DNA complexes. Rules adopted for + and +/- ranking and some examples in rp promoters are shown at the right. (b). Criteria used for identification of potential transcription factor-binding sites by the rVISTA program for motifs aligned in human-mouse promoter sequence comparisons and with the FindPatterns program for unaligned motifs.
Figure 3. Examples of comparisons of human and mouse rp promoter sequences from -200 to +100. Exon I is in uppercase letters, highlighted in yellow with the ATG translation initiation codon, if present, highlighted in gray. The sequences evaluated for TATA box quality are highlighted in green. Putative transcription factor-binding sites in aligned sequences are shown above the sequences, highlighted in fuchsia; sites in unaligned sequences are shown above the human or below the mouse sequences and enclosed in carets. An upstream sequence identified as an insertion element is in red letters. Gaps inserted by the alignment program to maximize overall sequence identity are indicated by dashes. (a) rpS18 , (b) rpL30 , (c) rpS4 , (d) rpL13a . In rpL30 the elements with known functional relevance are underlined with asterisks.
Figure 4. The consensus initiator sequence of mammalian rp genes. Seventy-nine pairs of orthologous human and mouse rp gene sequences were compared at positions -8 to +10 and the occurrence of each nucleotide or pair of nucleotides depicted by the height of the letters: A, G, C. T, Y = C/T, R = A/G, W = A/T, K = G/T, S = C/G, M = C/A. The tsp is the C at position +1.
Figure 5. Comparison of rpS3 promoter sequences in human (Hs), mouse (Mm), Xenopus laevis (Xl) and Fugu rubripes (Fr). Alignment by the ClustalW program with 100% and 75% identities enclosed in boxes. The first exon is highlighted in yellow with the ATG translation initiation codon in gray. Putative binding sites for TBP, GABP, Sp1 and YY1 are highlighted in green, red, blue and pink, respectively.
Figure 6. Classification of rp gene promoters. The data in Table 1 were used to classify the rp promoters into eight groups according to whether they contain aligned sites for GABP, Sp1, YY1, or various combinations of these factors. The promoters highlighted in green are those in which the TATA box quality of both orthologues was ranked as + or in which one ranked as + and the other as +/-. The promoters highlighted in yellow are those in which both orthologues ranked as +/- or in which one ranked as + and the other as -. Non highlighted promoters are those in which both orthologues ranked as â or in which one ranked as +/- and the other as -.
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