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Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli.

Department of Biochemistry, Wayne State University School of Medicine, Detroit, Michigan 48201.

ABSTRACT

Transcription of the Ntr regulon is controlled by the two-component system consisting of the response regulator NRI (NtrC) and the kinase/phosphatase NRII (NtrB), which both phosphorylates and dephosphorylates NRI. Even though in vitro transcription from nitrogen-regulated promoters requires phosphorylated NRI, NRII-independent activation of NRI also occurs in vivo. We show here that this activation likely involves acetyl phosphate; it is eliminated by mutations that reduce synthesis of acetyl phosphate and is elevated by a mutation expected to cause accumulation of acetyl phosphate. With purified components, we investigated the mechanism by which acetyl phosphate stimulates glutamine synthetase synthesis. Acetyl phosphate, carbamyl phosphate, and phosphoramidate but not ATP or phosphoenolpyruvate acted as substrates for the autophosphorylation of NRI in vitro. Phosphorylated NRI produced by this mechanism exhibited the properties associated with NRI phosphorylated by NRII, including the activated ATPase activity of the central domain of NRI and the ability to activate transcription from the nitrogen-regulated glutamine synthetase glnAp2 promoter.

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• Wang, J. T., Syed, A., Gralla, J. D. (1997). Multiple pathways to bypass the enhancer requirement of sigma 54 RNA polymerase: Roles for DNA and protein determinants. Proc. Natl. Acad. Sci. USA 94: 9538-9543 [Abstract] [Full Text]  
• Dahl, J. L., Wei, B.-Y., Kadner, R. J. (1997). Protein Phosphorylation Affects Binding of the Escherichia coli Transcription Activator UhpA to the uhpT Promoter. J. Biol. Chem. 272: 1910-1919 [Abstract] [Full Text]  
• Wang, J. T., Gralla, J. D. (1996). The Transcription Initiation Pathway of Sigma 54Mutants That Bypass the Enhancer Protein Requirement. IMPLICATIONS FOR THE MECHANISM OF ACTIVATION. J. Biol. Chem. 271: 32707-32713 [Abstract] [Full Text]  
• Cullen, P. J., Bowman, W. C., Kranz, R. G. (1996). In Vitro Reconstitution and Characterization of the Rhodobacter capsulatus NtrB and NtrC Two-component System. J. Biol. Chem. 271: 6530-6536 [Abstract] [Full Text]  
• Wang, J. T., Syed, A., Hsieh, M., Gralla, J. D. (1995). Converting Escherichia coli RNA Polymerase into an Enhancer-Responsive Enzyme: Role of an NH2-Terminal Leucine Patch in sigma54. Science 270: 992-994 [Abstract]  
• Tintut, Y., Wang, J. T., Gralla, J. D. (1995). Abortive Cycling and the Release of Polymerase for Elongation at the [IMAGE]54-dependent glnAp2 Promoter. J. Biol. Chem. 270: 24392-24398 [Abstract] [Full Text]  
• Tintut, Y, Wang, J T, Gralla, J D (1995). A novel bacterial transcription cycle involving sigma 54.. Genes Dev. 9: 2305-2313 [Abstract]  
• Kamberov, E. S., Atkinson, M. R., Ninfa, A. J. (1995). The Escherichia coli PII Signal Transduction Protein Is Activated upon Binding 2-Ketoglutarate and ATP. J. Biol. Chem. 270: 17797-17807 [Abstract] [Full Text]  
• Wingrove, J A, Gober, J W (1994). A sigma 54 transcriptional activator also functions as a pole-specific repressor in Caulobacter.. Genes Dev. 8: 1839-1852 [Abstract]  
• Dutta, R., Yoshida, T., Inouye, M. (2000). The Critical Role of the Conserved Thr247 Residue in the Functioning of the Osmosensor EnvZ, a Histidine Kinase/Phosphatase, in Escherichia coli. J. Biol. Chem. 275: 38645-38653 [Abstract] [Full Text]