The dsg gene of Myxococcus xanthus encodes a protein similar to translation initiation factor IF3

Cheng, Yvonne; Kalman, Lisa V.; Kaiser, Dale

doi:10.1128/jb.176.5.1427-1433.1994

Cited by 37 publications

(19 citation statements)

References 20 publications

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“…The amino acid sequences of Dsg and IF3 are 50% homologous throughout the length of IF3 (5). Dsg, however, extends 66 amino acids beyond the carboxy terminus of E. coli or B. stearothermophilus IF3.…”

Section: Resultsmentioning

confidence: 99%

The Myxococcus xanthus dsg gene product performs functions of translation initiation factor IF3 in vivo

1994

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The amino acid sequence of the Dsg protein is 50%o identical to that of translation initiation factor IF3 of Escherichia coli, the product of its infC gene. dsg mutants are able to initiate the developmental process, but their development goes awry when the cells have formed loose asymmetric aggregates, at about 6 to 10 h. These mutants are unable to transcribe a particular set of developmentally regulated genes (3). The dsg mutation also affects the cells during vegetative growth. Mutants form compact, heaped, smooth-edged colonies, unlike the flat, spreading wild-type colonies. These mutants are also defective in the phase variation of colony color. In the accompanying paper (5), we describe the sequence of the dsg gene, which contains a missense mutation in dsg mutants. The amino acid sequence of Dsg is 50% and 51% identical to that of translation initiation factor IF3 of both Escherichia coli and Bacillus stearothermophilus, respectively. We also show that like IF3, Dsg begins with a unique initiation codon and contains conserved residues which are critical for the function of IF3. The Dsg protein extends 66 more amino acids to its C terminus than the IF3 proteins of E. coli, other enteric bacteria, and B. stearothermophilus.An important role of IF3 in translation initiation is to help the ribosome select the initiation codon on the mRNA. Thus, IF3 ensures the fidelity of translation by preventing initiation at an incorrect location in the message or in the wrong reading frame (12,13,26 codon. The IF3 protein, which is associated with the 30S ribosomal subunit during initiation, inspects the codons near the Shine-Dalgarno site for one which will pair correctly with the anticodon on the initiator tRNA, fMet-tRNA et, which is also associated with the 30S subunit. When the proper initiation codon is located, the 50S ribosomal subunit joins the 30S initiation complex to form the 70S ribosome, and the initiation factors are released (8).The infC gene, which encodes IF3 in E. coli, begins with the atypical AUU initiation codon (21). Recent work shows that IF3 selects against initiation at AUU codons and for initiation at AUG, GUG, and UUG codons, the typical initiators. In fact, this atypical AUU initiation codon is involved in the translational autoregulation of infC expression (2,9,26). When IF3 levels are high, the mRNA encoding infC is not translated because IF3 does not recognize AUU for the initiation of translation. However, when IF3 levels are low, the infC message is translated because, in the absence of IF3, the ribosome shows low selectivity for the typical initiation codons. Translation of infC from AUU continues until the levels of IF3 are high enough to restrict translation from an AUU initiation codon, thus regulating the cellular level of the IF3 protein according to its function (1, 2, 9).In this work, we show that Dsg reacts with anti-IF3 serum. Using anti-Dsg antibodies, we show that Dsg is present at constant levels at all times during vegetative growth and development, as would be expected of ...

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Section: Resultsmentioning

confidence: 99%

The Myxococcus xanthus dsg gene product performs functions of translation initiation factor IF3 in vivo

1994

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“…Measurements were made in both red light (RL) and green light (GL). infCa mRNA levels were normalized by using ribosomal RNA values for each sample (13 signal (Dsg) plays a role in both translation initiation and developmental processes, such as controlling sporulation and fruiting body development (30,39). In the purple nonsulfur bacterium Rhodobacter sphaeroides, the IF3-like protein PifC influences the production of bacteriochlorophyll and photosynthetic complexes (40).…”

Section: Discussionmentioning

confidence: 99%

Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression

Gutu

Nesbit²,

Alverson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Significance The regulation of photosynthesis is important, yet poorly understood. Our work reveals a previously undescribed form of photosynthesis gene regulation in cyanobacteria that apparently also controls gene expression in plants, including commercially important crops. This finding may provide a unique approach to modifying the environmental responses and developmental programs of agriculturally important species. In addition, translation is a key biological process, and many of its important features and regulation remain to be described. Initiation is the rate-limiting step of translation, making it a critical point for regulation. Our finding that translation initiation factor 3 families exist with common roles in initiation and individual roles in regulating gene expression provides additional insights into the translation mechanism and its regulation.

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“…For another sporulating bacterium, Bacillus subtilis, Tipper et al (45) suggested that some components of the translational machinery, namely ribosomal proteins and elongation factor G, could play a specific role during the spore formation process. In agreement with this idea, Cheng et al (6) identified the lesions in a Myxococcus xanthus development-deficient strain displaying a mutation in dsg, encoding a protein similar to translation initiation factor IF3. Compared to IF3s from other species, the Myxococcus IF3 is much larger and bears a C-terminal extension which was shown to be necessary for developmental functions but not for viability, even though during vegetative growth, colonies were shown to be more compact and to be a darker tan color (19).…”

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confidence: 73%

Translation initiation factor IF2 of the myxobacterium Stigmatella aurantiaca: presence of a single species with an unusual N-terminal sequence

et al. 1997

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The structural gene for translation initiation factor IF2 (infB) was isolated from the myxobacterium Stigmatella aurantiaca on a 5.18-kb BamHI genomic restriction fragment. The infB gene (ca. 3.16 kb) encodes a 1,054-residue polypeptide with extensive homology within its G domain and C terminus with the equivalent regions of IF2s from Escherichia coli, Bacillus subtilis, Bacillus stearothermophilus, and Streptococcus faecium. The N-terminal region does not display any significant homology to other known proteins. The S. aurantiaca infB gene encodes a single protein which cross-reacted with antiserum to E. coli IF2 and was able to complement an E. coli infB mutant. The S. aurantiaca IF2 is distinguished from all other IF2s by a sequence of 160 residues near the N terminus that has an unusual composition, made up essentially of alanine, proline, valine, and glutamic acid. Within this sequence, the pattern PXXXAP is repeated nine times. Complete deletion of this sequence did not affect the factor's function in initiation of translation and even increased its capacity to complement the E. coli infB mutant.Myxobacteria are gram-negative, rod-shaped soil bacteria which, in response to starvation, undergo a developmental cycle leading to multicellular structures termed fruiting bodies. These specialized structures enclose dormant cells, the myxospores (41). Multicellular development of myxobacteria is regulated by intercellular signals, with some of them presumably transduced by GTP-binding proteins as in eukaryotes (8,25), and by cell-cell interactions (10). The expression of specific sets of genes is coordinated via various signalling compounds, thus triggering the different stages of multicellular development (24). For another sporulating bacterium, Bacillus subtilis, Tipper et al. (45) suggested that some components of the translational machinery, namely ribosomal proteins and elongation factor G, could play a specific role during the spore formation process. In agreement with this idea, Cheng et al. (6) identified the lesions in a Myxococcus xanthus development-deficient strain displaying a mutation in dsg, encoding a protein similar to translation initiation factor IF3. Compared to IF3s from other species, the Myxococcus IF3 is much larger and bears a C-terminal extension which was shown to be necessary for developmental functions but not for viability, even though during vegetative growth, colonies were shown to be more compact and to be a darker tan color (19).In addition to IF3, at least two other factors, IF1 and IF2, are required for the initiation of mRNA translation in prokaryotes. The genes for all three factors, namely, infA (IF1), infB (IF2), and infC (IF3), were first cloned in Escherichia coli (30,36,43). These three proteins play essential roles in several steps of translation initiation, from the selection of the initiator tRNA (15) to the control of the entry into the elongation cycle (26).The infB gene, encoding IF2, is located on the E. coli chromosome at 69 min and is part of a complex polycis...

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The dsg gene of Myxococcus xanthus encodes a protein similar to translation initiation factor IF3

Cited by 37 publications

References 20 publications

The Myxococcus xanthus dsg gene product performs functions of translation initiation factor IF3 in vivo

The Myxococcus xanthus dsg gene product performs functions of translation initiation factor IF3 in vivo

Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression

Translation initiation factor IF2 of the myxobacterium Stigmatella aurantiaca: presence of a single species with an unusual N-terminal sequence

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