On the control mechanism of bacterial growth by cyclic adenosine 3′, 5′-monophosphate

Robertis, Edward M. De; Judewicz, Norberto D.; Torres, Héctor N.

doi:10.1016/0006-291x(73)91209-6

Cited by 19 publications

(8 citation statements)

References 12 publications

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“…We suggest that, under these conditions, the ATG initiation sequence results in overexpression of adenylate cyclase with concomitant overproduction of cAMP to growth-inhibitory levels (28).…”

Section: Discussionmentioning

confidence: 99%

Translational efficiency of the Escherichia coli adenylate cyclase gene: mutating the UUG initiation codon to GUG or AUG results in increased gene expression.

Reddy¹,

Peterkofsky²,

McKenney³

1985

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

135

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Roy etal. [Roy, A., Haziza, C. & Danchin, A. (1983) EMBO J. 2,[791][792][793][794][795][796][797] established that translation of Escherichia coli adenylate cyclase initiates at a UUG codon, and they suggested this might decrease the efficiency of translation. We investigated the effect of varying the initiation codon on the expression of the adenylate cyclase (cya) gene. Using oligonucleotide-directed mutagenesis, we changed the UUG initiation codon to GUG and the more common initiator AUG and assayed for cya gene expression in a number of ways. First, the GUG initiation codon, in place of UUG, doubled cya expression when cya was expressed from the dual cya P1/P2 promoters. The corresponding AUG codon construct was nonviable. Second, when the cya gene was placed under the transcriptional control of the thermoinducible phage A PL promoter, the relative amounts of cya gene product were 1:2:6 for the UUG, GUG, and AUG initiation codons, respectively. Finally, the cya P2 promoter, Shine-Dalgarno sequence, and the DNA corresponding to the first 86 codons of cya were fused to DNA encoding the E. coli galactokinase gene beginning at the second codon. The relative amounts of the fusion polypeptides, which had galactokinase activity, were 1:2:3 for the UUG, GUG, and AUG initiation codons, respectively. These results demonstrate that the cya UUG initiation codon limits cya expression at the level of translation.Translation initiation requires an initiation codon and a properly spaced sequence upstream of the initiation codon that has base pairing potential with the 3' end of the 16S ribosomal RNA (the Shine and Dalgarno or SD sequence) (1, 2). AUG, GUG, and UUG triplets have been shown to stabilize the binding of initiator fMet-tRNA to ribosomes in vitro, suggesting that these three codons may function in vivo as initiation codons (3). Comparison of protein sequence data with the corresponding nucleic acid sequence data for more than 100 genes has shown that, in vivo, all eukaryotic and nearly all prokaryotic genes use the translation initiation codon AUG. However, there are 9 examples of GUG and 3 examples of UUG functioning as initiation codons in Escherichia coli (2, 4). The gene for E. coli adenylate cyclase (cya), the enzyme that synthesizes the important cellular regulator cAMP, is one of the genes that uses the unusual UUG initiation codon (4-6).We have investigated the effect of this unusual initiation codon on cya expression by changing the DNA sequence coding for the UUG initiation codon to ATG and GTG, using oligonucleotide-directed mutagenesis. A comparison of the activities associated with the three codons was made in three different environments: (i) in the normal cya environment, with the cya gene expressed from the dual cya P1/P2 promoters, (it) in a transcription fusion with the cya gene under the transcriptional control of the phage X PL promoter, and (iii) in a gene fusion with the cya gene fused to the E. coli galactokinase (galK) gene to generate a fusion protein with galactokinase activity....

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Section: Discussionmentioning

confidence: 99%

Translational efficiency of the Escherichia coli adenylate cyclase gene: mutating the UUG initiation codon to GUG or AUG results in increased gene expression.

Reddy¹,

Peterkofsky²,

McKenney³

1985

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

135

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“…Concentrations of about I mwcyclic AMP are reported to be necessary both to overcome glucose repression of P-galactosidase synthesis and to inhibit growth of E. coli (Perlman & Pastan, 1968;Judewicz et al, 1973;De Robertis, Judewicz & Torres, 1973). In addition to the above mentioned data, we found that 2iP, at concentrations of I O -~ to IO-' M, overcame the effects of cyclic AMP at every concentration at which cyclic AMP was capable of modifying growth and catabolite repression in E. coli B/b.…”

Section: Resultsmentioning

confidence: 99%

“…Cyclic adenosine 3': 5'-monophosphate (cyclic AMP) has a marked inhibitory action on the growth of Escherichia coli (Judewicz, De Robertis & Torres, 1973), and it also affects lac-operon expression and /I-galactosidase synthesis in the organism (Ullmann & Monod, 1968;Perlman & Pastan, 1968;Perlman, De Combrugghe & Pastan, 1969). These two phenomena may be considered as typical and reproducible responses of some E. coZi strains to cyclic AMP.…”

Section: Introductionmentioning

confidence: 99%

Interactions of N6-( 2-Isopentenyl)adenine with Cyclic AMP on the Regulation of Growth and -Galactosidase Synthesis in Escherichia coli

Coppola¹,

Zoina²,

Marino³

1976

Journal of General Microbiology

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“…3A and B) 10-fold into L broth containing IPTG (0.5 mg/ml) (A), L broth containing both theophylline (1.8 mg/ml) add IPTG (0.5 mg/ml) (0), or L broth alone (O) and incubated at 42°C. Then, samples were taken at 0 (immediately), 10, and 120 min and boiled in 1 N HCl for 10 min (15). Total cAMP levels were assayed by the radioimmunological method described previously (15).…”

Section: Methodsmentioning

confidence: 99%

“…We believe that such autogenous regulation of cya is responsible for the normal growth of E. coli, because cell growth is inhibited by increased cAMP levels (10) and that the expression of cya could be closely related to regulation of cell cycle and growth.…”

mentioning

confidence: 98%

Expression of the adenylate cyclase gene during cell elongation in Escherichia coli K-12

Utsumi¹,

Kawamukai²,

Aiba³

et al. 1986

J Bacteriol

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Expression of the adenylate cyclase gene (cya) in synchronized Escherichia coli cells was investigated by using the cya-lacZ protein and operon fusion plasmids. The regulation of cya expression during the cell cycle is characterized as follows: (i) cya is expressed during cell elongation; (ii) expression is repressed during cell division; (iii) regulation is exerted at the transcriptional level. To test cya expression during cell elongation, we constructed a plasmid (pLCR1) in which the lacUVS promoter operator was fused to the structural gene of cya and investigated the effect of cya expression by isopropyl-,-D-thiogalactopyranoside (IPTG) on the cell division of cells containing pLCR1. By the addition of IPTG, cell division was inhibited and filaments were formed. Such an inhibitory effect was antagonized by adding cyclic GMP to the culture medium and was not observed in the crp mutant.

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On the control mechanism of bacterial growth by cyclic adenosine 3′, 5′-monophosphate

Cited by 19 publications

References 12 publications

Translational efficiency of the Escherichia coli adenylate cyclase gene: mutating the UUG initiation codon to GUG or AUG results in increased gene expression.

Translational efficiency of the Escherichia coli adenylate cyclase gene: mutating the UUG initiation codon to GUG or AUG results in increased gene expression.

Interactions of N6-( 2-Isopentenyl)adenine with Cyclic AMP on the Regulation of Growth and -Galactosidase Synthesis in Escherichia coli

Expression of the adenylate cyclase gene during cell elongation in Escherichia coli K-12

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