Functional adaptation of tRNAs to fibroin biosynthesis in the silkgland of <i>Bombyx mori L</i>

Garel, Jean‐Pierre; Mandel, P.; Chavancy, Gérard; Daillie, J.

doi:10.1016/0014-5793(70)80196-x

Cited by 96 publications

(23 citation statements)

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“…The level of the tRNATIP pool in any tissue might be modulated to match the demands of translation in those tissues. In the case of the posterior silk gland of Bombyx mori, the pool of tRNAs is adapted to the codon content of the predominant mRNA (15,37). This presumably optimizes translational efficiency or fidelity.…”

Section: Discussionmentioning

confidence: 99%

“…Nonetheless, there are examples in which differential control of gene expression may exist. For example, tRNA pool sizes are known to change as tissues differentiate, presumably in response to the demands of protein synthesis in that tissue (15,37). In the case of the posterior silk gland of Bombyx mori, Sprague and coworkers have been able to find silk gland-specific tRNAA"a genes whose tissue-specific expression might be controlled by a small 5'-flanking sequence (37,38,49).…”

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confidence: 97%

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Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans.

1988

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Caenorhabditis elegans has 12 tRNA T,pG genes as defined by Southern analysis. In order to evaluate the function of the individual members of this multigene family, we sought to recover amber (UAG)-suppressing mutations from reversion experiments with animals carrying amber mutations in a nervous system-affecting gene (unc-13) or a sex-determining gene (tra-3). Revertants were analyzed by Southern blot, exploiting the fact that the CCA to CTA change at the anticodon creates a new XbaI site. Five different members of the tRNATrP gene family were identified as suppressors: sup-7 X, sup-5 III, sup-24 IV, sup-28 X, and sup-29 IV. All five suppressor genes were sequenced and found to encode identical tRNATrpG molecules with a single base change (CCA to CTA) at the anticodon compared with their wild-type counterparts. The flanking sequences had only limited homology. The relative expression of these five genes was determined by measuring the efficiencies of suppressors against amber mutations in genes affecting the nervous system, hypodermis, muscle, and sex determination. The results of these cross-suppression tests showed that the five members of the tRNATrP gene family were differentially regulated in a tissue-or development stage-specific manner.

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Section: Discussionmentioning

confidence: 99%

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confidence: 97%

Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans.

1988

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“…A dramatic example occurs in the silkworm, Bombyx mori, where the distribution of tRNAs in the mature silk gland matches the amino acid composition of the gland's chief protein product, silk fibroin: 44% glycine, 29% alanine, and 12% serine (26,47). The corresponding enrichment of the cognate tRNAs (5,15,29) and aminoacyl-tRNA synthetases (6,8,27,33) in the posterior silk gland represents extreme specialization of the protein-synthetic machinery, which can be tolerated because little other synthetic activity is required of the terminally differentiated silk gland cells. Spiders have apparently adopted a similar strategy to maximize the production of silk for webs (4).…”

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confidence: 99%

Silkworm TFIIIB Binds both Constitutive and Silk Gland-Specific tRNA^Ala Promoters but Protects Only the Constitutive Promoter from DNase I Cleavage

Young

Ahnert

Sprague

1996

Molecular and Cellular Biology

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We have identified a complex between TFIIIB and the upstream promoter of silkworm tRNA Ala genes that is detectable by gel retardation and DNase I footprinting. Formation of this complex depends on the integrity of previously identified upstream promoter elements and on the presence of other silkworm transcription factors, either TFIIID or a fraction that contains both TFIIIC and TFIIID. We have used this complex to compare the interactions of TFIIIB with two kinds of tRNA Ala genes whose different in vitro transcription properties are conferred by the upstream segments of their promoters. These are the tRNA C Ala genes, which are transcribed constitutively, and the tRNA SG Ala genes, which are transcribed only in the silk gland. We find that TFIIIB binds tRNA SG Ala genes with lower affinity than it binds tRNA C Ala genes. In addition, the TFIIIB complexes formed on tRNA SG Ala genes differ qualitatively from those formed on tRNA C Ala genes. Both the transcriptional activity of tRNA SG Ala complexes and the ability of the complexes to protect upstream DNA from DNase I digestion are reduced.

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“…The demand for fibroin, the principal protein of silk, requires highly efficient transcription and translation of the fibroin gene in cells of the silk gland. Translational efficiency in these cells is maximized by the quantitative adaptation of the tRNA population to the composition of fibroin: 44% glycine, 29% alanine, and 12% serine (5,29,30,42). In the case of tRNA Ala , enrichment is achieved both by increasing the level of the constitutive type of tRNA Ala (tRNA C Ala ) and by synthesizing an additional, silk gland-specific, type (tRNA SG Ala ) (31,44).…”

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confidence: 99%

TATA-Binding Protein–TATA Interaction Is a Key Determinant of Differential Transcription of Silkworm Constitutive and Silk Gland-Specific tRNA^Ala Genes

Ouyang

Martinez

Young

et al. 2000

Molecular and Cellular Biology

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We have investigated the contribution of specific TATA-binding protein (TBP)-TATA interactions to the promoter activity of a constitutively expressed silkworm tRNA C Ala gene and have also asked whether the lack of similar interactions accounts for the low promoter activity of a silk gland-specific tRNA SG Ala gene. We compared TBP binding, TFIIIB-promoter complex stability (measured by heparin resistance), and in vitro transcriptional activity in a series of mutant tRNA C Ala promoters and found that specific TBP-TATA contacts are important for TFIIIB-promoter interaction and for transcriptional activity. Although the wild-type tRNA C Ala promoter contains two functional TBP binding sequences that overlap, the tRNA SG Ala promoter lacks any TBP binding site in the corresponding region. This feature appears to account for the inefficiency of the tRNA SG Ala promoter since provision of either of the wild-type TATA sequences derived from the tRNA C Ala promoter confers robust transcriptional activity. Transcriptional impairment of the wild-type tRNA SG Ala gene is not due to reduced incorporation of TBP into transcription complexes since both the tRNA C Ala and tRNA SG Ala promoters form transcription complexes that contain the same amount of TBP. Thus, the deleterious consequences of the lack of appropriate TBP-TATA contacts in the tRNA SG Ala promoter must come from failure to incorporate some other essential transcription factor(s) or to stabilize the complete complex in an active conformation.The silkworm Bombyx mori provides a clear example of regulated tRNA gene expression. The demand for fibroin, the principal protein of silk, requires highly efficient transcription and translation of the fibroin gene in cells of the silk gland. Translational efficiency in these cells is maximized by the quantitative adaptation of the tRNA population to the composition of fibroin: 44% glycine, 29% alanine, and 12% serine (5,29,30,42). In the case of tRNA Ala , enrichment is achieved both by increasing the level of the constitutive type of tRNA Ala (tRNA C Ala ) and by synthesizing an additional, silk gland-specific, type (tRNA SG Ala ) (31,44). In vitro studies of representative tRNA C Ala and tRNA SG Ala genes have revealed transcription properties consistent with the patterns of tRNA C Ala and tRNA SG Ala accumulation in vivo. That is, in a variety of extracts from non-silk gland cells, the tRNA C Ala gene directs transcription much more efficiently than does the tRNA SG Ala gene, but in concentrated extracts from silk gland, the two genes are equally efficient (60). To understand how these two genes are differentially regulated, we have investigated the basis of the transcriptional impairment of the tRNA SG Ala gene that is observed under typical in vitro conditions. Transcription of silkworm tRNA Ala genes is driven by both internal and external promoter elements (26,36,56). The critical difference between the tRNA C Ala and tRNA SG Ala genes is in the interaction of their 5Ј flanking promoter elements with the transcri...

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Functional adaptation of tRNAs to fibroin biosynthesis in the silkgland of Bombyx mori L

Cited by 96 publications

References 5 publications

Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans.

Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans.

Silkworm TFIIIB Binds both Constitutive and Silk Gland-Specific tRNA^Ala Promoters but Protects Only the Constitutive Promoter from DNase I Cleavage

TATA-Binding Protein–TATA Interaction Is a Key Determinant of Differential Transcription of Silkworm Constitutive and Silk Gland-Specific tRNA^Ala Genes

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Functional adaptation of tRNAs to fibroin biosynthesis in the silkgland of Bombyx mori L

Cited by 96 publications

References 5 publications

Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans.

Differential expression of five tRNA(UAGTrp) amber suppressors in Caenorhabditis elegans.

Silkworm TFIIIB Binds both Constitutive and Silk Gland-Specific tRNAAla Promoters but Protects Only the Constitutive Promoter from DNase I Cleavage

TATA-Binding Protein–TATA Interaction Is a Key Determinant of Differential Transcription of Silkworm Constitutive and Silk Gland-Specific tRNAAla Genes

Contact Info

Product

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Silkworm TFIIIB Binds both Constitutive and Silk Gland-Specific tRNA^Ala Promoters but Protects Only the Constitutive Promoter from DNase I Cleavage

TATA-Binding Protein–TATA Interaction Is a Key Determinant of Differential Transcription of Silkworm Constitutive and Silk Gland-Specific tRNA^Ala Genes