Processing of unstable bacteriophage T4 gene 32 mRNAs into a stable species requires Escherichia coli ribonuclease E.

Mudd, Elisabeth A.; Prentki, Pierre; Belin, Dominique; Krisch, Henry

doi:10.1002/j.1460-2075.1988.tb03238.x

Cited by 127 publications

(84 citation statements)

References 56 publications

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“…6). Presence of such a stemloop-like structure downstream of the cleavage site has been reported to be required for the cleavage by RNase E. 25) Thus, it is possible that TS-2 may be attributable to a post-transcriptional cleavage of TS-1.…”

Section: Analysis Of 5?-terminal Region Of the A Vinelandii Icd Mrnamentioning

confidence: 99%

Cloning, Sequencing, and Expression of a Gene Encoding the Monomeric Isocitrate Dehydrogenase of the Nitrogen-fixing Bacterium,Azotobacter vinelandii

Sahara

Takada

Takeuchi

et al. 2002

Bioscience, Biotechnology, and Biochemistry

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Section: Analysis Of 5?-terminal Region Of the A Vinelandii Icd Mrnamentioning

confidence: 99%

Cloning, Sequencing, and Expression of a Gene Encoding the Monomeric Isocitrate Dehydrogenase of the Nitrogen-fixing Bacterium,Azotobacter vinelandii

Sahara

Takada

Takeuchi

et al. 2002

Bioscience, Biotechnology, and Biochemistry

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“…The enzyme is involved in the processing of mRNA from bacteriophage T4 genes 32 and 59 in vivo. Processing of these messages resulted in destabilization of the portion of the mRNA upstream of the cleavage site (Mudd et al 1988;Carpousis et al 1989) and thus may have a role in retroregulation (Schmeissner et al 1984) of upstream gene expression. A comparison of the cleavage sites found in the noncoding RNAs and the T4 mRNAs revealed similarities in sequence at the cleavage sites and in the potential to form RNA secondary structure just downstream of the sites (Tomcs~inyi and Apirion 1985;Mudd et al 1988;Carpousis et al 1989).…”

mentioning

confidence: 99%

Escherichia coli RNase E has a role in the decay of bacteriophage T4 mRNA.

Mudd¹,

Carpousis²,

Krisch³

1990

Genes Dev.

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Bacteriophage T4 mRNAs are markedly stabilized, both chemically and functionally, in an Escherichia coli strain deficient in the RNA-processing endonuclease RNase E. The functional stability of total T4 messages increased 6-fold; we were unable to detect a T4 message whose functional stability was not increased. There was a 4-fold increase in the chemical stability of total T4 RNA. The degree of chemical stabilization of six specific T4 mRNAs examined varied from a maximum of 28-fold to a minimum of 1.5-fold. In the RNase Edeficient strain, several minutes delay and a slower rate of progeny production led to a reduction in final phage yield of -50%. Although the effect of the rne temperature-sensitive mutation could be indirect, the simplest interpretation of our results is that RNase E acts directly in the degradation of many T4 mRNAs.[Key Words: Bacteriophage T4; mRNA decay; mRNA processing; mRNA stability; ribonuclease El Received September 13, 1989; revised version accepted February 7, 1990.Escherichia coli RNase E is an endoribonuclease that has been shown to process 9S RNA to a precursor of 5S rRNA (Ghora and Apirion 1978) and also to process RNA1, the inhibitor of ColE1 plasmid replication (Tomcs~inyi and Apirion 1985) both in vitro and in vivo. RNase E did not appear to have a general role in mRNA decay in E. coli (Apirion and Gitelman 1980}, although the synthesis of some E. coli proteins was affected by the mutation (Gitelman and Apirion 1980). The enzyme is involved in the processing of mRNA from bacteriophage T4 genes 32 and 59 in vivo. Processing of these messages resulted in destabilization of the portion of the mRNA upstream of the cleavage site (Mudd et al. 1988;Carpousis et al. 1989) and thus may have a role in retroregulation (Schmeissner et al. 1984) of upstream gene expression. A comparison of the cleavage sites found in the noncoding RNAs and the T4 mRNAs revealed similarities in sequence at the cleavage sites and in the potential to form RNA secondary structure just downstream of the sites (Tomcs~inyi and Apirion 1985;Mudd et al. 1988;Carpousis et al. 1989).As yet, the nucleases that determine the rate of functional decay of total mRNA in E. coil or its phage have not been identified. A mutation in the E. coli ams gene was found to have a five-to sixfold effect on the chemical stability of total E. coli RNAs, but it did not affect functional stability significantly (Kuwano et al. 1977;Ono and Kuwano 1979). E. coli RNases III (see Portier et al. 1987), E (Mudd et al. 1988;Carpousis et al. 1989), and other as yet unidentified endonucleases (Cannistraro et al. 1986; Baga et al. 1988; Melefors and von Gabain 1988; Uzan et al. 1988) have been implicated in the decay of a few specific bacterial or phage mRNAs. In this paper we present evidence suggesting that E. coli RNase E has a major role in the functional and chemical decay of many bacteriophage T4 mRNAs. Results E. coli RNase E affects the functional stability of T4 mRNAsThe functional stability of mRNA can be estimated from the ability of t...

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“…Similarly, RNase E must have a very stringent enzyme specificity, since it cleaves (i) 9S RNA (but not many other RNAs) and does so only at two specific sites (43), (ii) the small RNA 1 at one site (51), (iii) specific sites in some phage RNAs (28,36), and (iv) a specific site on the ribosomal protein S20 message (30). However, most RNA substrates tested were not degraded (34), and the substrate specificity so far appears to include a 9-nt sequence and, possibly, secondary structure (2).…”

Section: Resultsmentioning

confidence: 99%

“…The rne and ams genes are probably the same (4, 13,35,49). An ams mutant shows slower mass decay of mRNA but normal functional decay rates (39,40), and the normal endonucleolytic cleavages are still observed (3,36). The primary function of RNase E, and how it affects mRNA mass decay, may be difficult to identify.…”

Section: Resultsmentioning

confidence: 99%

Broad-specificity endoribonucleases and mRNA degradation in Escherichia coli

1992

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Crude extracts from Escherichia coli were screened for any broad-specificity endoribonuclease after the cell proteins were fractionated by size. In a mutant lacking the gene for RNase I (molecular mass, 27,156 Da), the only such activities were also in the size range of 23 to 28 kDa. Fractionation by chromatography on a strong cation-exchange resin revealed only two activities. One of them eluted at a salt concentration expected for RNase M and had the specificity of RNase M. It preferred pyriimdine-adenosine bonds, could not degrade purine homopolymers, and had a molecular mass of -27 kDa (V. J. Cannistraro and D. Kennell, Eur. J. Biochem. 181:363-370, 1989). A second fraction, eluting at a higher salt concentration, was active against any phosphodiester bond but was about 100 times less active than are kNase I and RNase I* (a form of RNase I) in the wild-type cell. On the basis of sizing-gel chromatography, this enzyme had a molecular mass of -24 kDa.We call it RNase R (for residual). RNase R is not an abnormal product of the mutant rna gene; a cell carrying many copies of that gene on a plasmid did not synthesize more RNase R. Our search for broad-specificity endoribonucleases was prompted by the expectation that the primary activities for mRNA degradation are expressed by a relatively small number of broad-specificity RNases. If correct, the results suggest that the endoribonucleases for this major metabolic activity reside in the 24-to 28-kDa size range. Endoribonucleases with much greater specificity must have as primary functions the processing of specific RNA molecules at a very limited number of sites as steps in their biosynthesis. In exceptional cases, these endoribonucleases inactivate a specific message that has such a site, and they can also affect total mRNA metabolism indirectly by a global disturbance of the cell physiology. It is suggested that a distinction be made between these processing and degradative activities. mRNA was first identified 30 years ago (6,20) and provided the sought-after link between DNA and protein. Its most unusual property was its extreme instability. Furthermore, each message (i.e., the mRNA for a specific protein) has a unique rate of decay. In Escherichia coli this rate can vary from a half-life of 30 s to >8 min at 37°C (5) and to wider ranges at lower growth temperatures (25,41). This diversity of decay rates could result from the presence of many different RNase activities, each of which is specific for a specific sequence or structure on a certain class of messages. Alternatively, all messages could be degraded by a relatively small number of RNases, and differences in rates could reflect the modulating effects of other parameters of mRNA metabolism, such as the translation frequency (24, 45).In the work described in this paper, we have screened for all broad-specificity endoribonucleases (endoRNases) in E. coli and have only detected such activities in proteins in the size range of 23 to 30 kDa. Besides RNases M (8) and I and I* (9), we observed another endoRNas...

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Processing of unstable bacteriophage T4 gene 32 mRNAs into a stable species requires Escherichia coli ribonuclease E.

Cited by 127 publications

References 56 publications

Cloning, Sequencing, and Expression of a Gene Encoding the Monomeric Isocitrate Dehydrogenase of the Nitrogen-fixing Bacterium,Azotobacter vinelandii

Cloning, Sequencing, and Expression of a Gene Encoding the Monomeric Isocitrate Dehydrogenase of the Nitrogen-fixing Bacterium,Azotobacter vinelandii

Escherichia coli RNase E has a role in the decay of bacteriophage T4 mRNA.

Broad-specificity endoribonucleases and mRNA degradation in Escherichia coli

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