Post-translational modification of PII signal transduction proteins

Frontiers in Microbiology

Volumn 6, Issue JAN, 2015, Pages

  Merrick, Mike ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

Adenylylation; PIIO protein; Phosphorylation; Post translational modification; Uridylylation

Indexed keywords

2 OXOGLUTARIC ACID; GLUTAMINE; N ACETYLGLUTAMATE KINASE; NITROGEN REGULATORY PROTEIN; PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADENYLATION; DNA INTEGRATION; ENZYME ACTIVITY; GENETIC REGULATION; MEMBRANE TRANSPORT; MICROBIAL ACTIVITY; NITROGEN METABOLISM; NONHUMAN; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN MODIFICATION; RNA TRANSLATION; SHORT SURVEY; SIGNAL TRANSDUCTION; URIDYLYLATION;

ACTINOBACTERIA; CYANOBACTERIA; PROTEOBACTERIA;

EID: 84920659939     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00763     Document Type: Short Survey

References (41)

1. Arcondéguy, T., Jack, R., and Merrick, M. (2001). PII signal transduction proteins: pivotal players in microbial nitrogen control. Microbiol. Mol. Biol. Rev. 65, 80-105. doi: 10.1128/MMBR.65.1.80-105.2001.
2. Berthold, C. L., Wang, H., Nordlund, S., and Hogbom, M. (2009). Mechanism of ADP-ribosylation removal revealed by the structure and ligand complexes of the dimanganese mono-ADP-ribosylhydrolase DraG. Proc. Natl. Acad. Sci. U.S.A. 106, 14247-14252. doi: 10.1073/pnas.0905906106.
3. Brown, M. S., Segal, A., and Stadtman, E. R. (1971). Modulation of glutamine synthetase adenylylation and deadenylylation is mediated by metabolic transformation of the PII regulatory protein. Proc. Natl. Acad. Sci. U.S.A. 68, 2949-2953. doi: 10.1073/pnas.68.12.2949.
4. Burillo, S., Luque, I., Fuentes, I., and Contreras, A. (2004). Interactions between the nitrogen signal transduction protein PII and N-acetyl glutamate kinase in organisms that perform oxygenic photosynthesis. J. Bacteriol. 186, 3346-3354. doi: 10.1128/JB.186.11.3346-3354.2004.
5. Chellamuthu, V. R., Alva, V., and Forchhammer, K. (2013). From cyanobacteria to plants: conservation of PII functions during plastid evolution. Planta 237, 451-462. doi: 10.1007/s00425-012-1801-0.
6. Conroy, M. J., Durand, A., Lupo, D., Li, X. D., Bullough, P. A., Winkler, F. K., et al. (2007). The crystal structure of the Escherichia coli AmtB-GlnK complex reveals how GlnK regulates the ammonia channel. Proc. Natl. Acad. Sci. U.S.A. 104, 1213-1218. doi: 10.1073/pnas.0610348104.
7. Espinosa, J., Forchhammer, K., Burillo, S., and Contreras, A. (2006). Interaction network in cyanobacterial nitrogen regulation: pipX, a protein that interacts in a 2-oxoglutarate dependent manner with PII and NtcA. Mol. Microbiol. 61, 457-469. doi: 10.1111/j.1365-2958.2006.05231.x.
8. Fokina, O., Herrmann, C., and Forchhammer, K. (2011). Signal-transduction protein PII from Synechococcus elongatus PCC 7942 senses low adenylate energy charge in vitro. Biochem. J. 440, 147-156. doi: 10.1042/BJ20110536.
9. Forchhammer, K. (2008). PII signal transducers: novel functional and structural insights. Trends Microbiol. 16, 65-72. doi: 10.1016/j.tim.2007.11.004.
10. Forchhammer, K., Irmler, A., Kloft, N., and Ruppert, U. (2004). P signalling in unicellular cyanobacteria: analysis of redox-signals and energy charge. Physiol. Plant. 120, 51-56. doi: 10.1111/j.0031-9317.2004.0218.x.
11. Heinrich, A., Maheswaran, M., Ruppert, U., and Forchhammer, K. (2004). The Synechococcus elongatus P signal transduction protein controls arginine synthesis by complex formation with N-acetyl-l-glutamate kinase. Mol. Microbiol. 52, 1303-1314. doi: 10.1111/j.1365-2958.2004.04058.x.
12. Hesketh, A., Fink, D., Gust, B., Rexer, H. U., Scheel, B., Chater, K., et al. (2002). The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol. Microbiol. 46, 319-330. doi: 10.1046/j.1365-2958.2002.03149.x.
13. Huergo, L. F., Chandra, G., and Merrick, M. (2013). PII signal transduction proteins: nitrogen regulation and beyond. FEMS Microbiol. Rev. 37, 251-283. doi: 10.1111/j.1574-6976.2012.00351.x.
14. Huergo, L. F., Pedrosa, F. O., Muller-Santos, M., Chubatsu, L. S., Monteiro, R. A., Merrick, M., et al. (2012). PII signal transduction proteins: pivotal players in post-translational control of nitrogenase activity. Microbiology 158, 176-190. doi: 10.1099/mic.0.049783-0.
15. Irmler, A., and Forchhammer, K. (2001). A PP2C-type phosphatase dephosphorylates the PII signaling protein in the cyanobacterium Synechocystis PCC 6803. Proc. Natl. Acad. Sci. U.S.A. 98, 12978-12983. doi: 10.1073/pnas.231254998.
16. Jiang, P., and Ninfa, A. J. (2007). Escherichia coli PII signal transduction protein controlling nitrogen assimilation acts as a sensor of adenylate energy charge in vitro. Biochemistry 46, 12979-12996. doi: 10.1021/bi701062t.
17. Jiang, P., and Ninfa, A. J. (2009). Sensation and signaling of alpha-ketoglutarate and adenylylate energy charge by the Escherichia coli PII signal transduction protein require cooperation of the three ligand-binding sites within the PII trimer. Biochemistry 48, 11522-11531. doi: 10.1021/bi9011594.
18. Jiang, P., Peliska, J. A., and Ninfa, A. J. (1998). Enzymological characterization of the signal-transducing uridylyltransferase/uridylyl-removing enzyme (EC 2.7.7.59) of Escherichia coli and its interaction with the PII protein. Biochemistry 37, 12782-12794. doi: 10.1021/bi980667m.
19. Leigh, J. A., and Dodsworth, J. A. (2007). Nitrogen regulation in bacteria and archaea. Annu. Rev. Microbiol. 61, 349-377. doi: 10.1146/annurev.micro.61.080706.093409.
20. Li, X. D., Huergo, L. F., Gasperina, A., Pedrosa, F. O., Merrick, M., and Winkler, F. K. (2009). Crystal structure of dinitrogenase reductase activating glycohydrolase (DRAG) reveals conservation in the ADP-ribosylhydrolase fold and specific features in the ADP-ribose-binding pocket. J. Mol. Biol. 390, 737-746. doi: 10.1016/j.jmb.2009.05.031.
21. Llacer, J. L., Contreras, A., Forchhammer, K., Marco-Marin, C., Gil-Ortiz, F., Maldonado, R., et al. (2007). The crystal structure of the complex of PII and acetylglutamate kinase reveals how PII controls the storage of nitrogen as arginine. Proc. Natl. Acad. Sci. U.S.A. 104, 17644-17649. doi: 10.1073/pnas.0705987104.
22. Llacer, J. L., Espinosa, J., Castells, M. A., Contreras, A., Forchhammer, K., and Rubio, V. (2010). Structural basis for the regulation of NtcA-dependent transcription by proteins PipX and PII. Proc. Natl. Acad. Sci. U.S.A. 107, 15397-15402. doi: 10.1073/pnas.1007015107.
23. Maheswaran, M., Urbanke, C., and Forchhammer, K. (2004). Complex formation and catalytic activation by the PII signaling protein of N-acetyl-L-glutamate kinase from Synechococcus elongatus strain PCC 7942. J. Biol. Chem. 279, 55202-55210. doi: 10.1074/jbc.M410971200.
24. Mizuno, Y., Moorhead, G. B., and Ng, K. K. (2007). Structural basis for the regulation of N-acetylglutamate kinase by PII in Arabidopsis thaliana. J. Biol. Chem. 282, 35733-35740. doi: 10.1074/jbc.M707127200.
25. Radchenko, M., and Merrick, M. (2011). The role of effector molecules in signal transduction by PII proteins. Biochem. Soc. Trans. 39, 189-194. doi: 10.1042/BST0390189.
26. Radchenko, M. V., Thornton, J., and Merrick, M. (2010). Control of AmtB-GlnK complex formation by intracellular levels of ATP, ADP and 2-oxoglutarate. J. Biol. Chem. 285, 31037-31045. doi: 10.1074/jbc.M110.153908.
27. Radchenko, M. V., Thornton, J., and Merrick, M. (2013). P(II) signal transduction proteins are ATPases whose activity is regulated by 2-oxoglutarate. Proc. Natl. Acad. Sci. U.S.A. 110, 12948-12953. doi: 10.1073/pnas.1304386110.
28. Radchenko, M. V., Thornton, J., and Merrick, M. (2014). Association and dissociation of the GlnK-AmtB complex in response to cellular nitrogen status can occur in the absence of GlnK post-translational modification. Front. Microbiol. 5:731. doi: 10.3389/fmicb.2014.00731.
29. Rajendran, C., Gerhardt, E. C., Bjelic, S., Gasperina, A., Scarduelli, M., Pedrosa, F. O., et al. (2011). Crystal structure of the GlnZ-DraG complex reveals a different form of PII-target interaction. Proc. Natl. Acad. Sci. U.S.A. 108, 18972-18976. doi: 10.1073/pnas.1108038108.
30. Ruppert, U., Irmler, A., Kloft, N., and Forchhammer, K. (2002). The novel protein phosphatase PphA from Synechocyctis PCC 6803 controls dephosphorylation of the signalling protein PII. Mol. Microbiol. 44, 855-864. doi: 10.1046/j.1365-2958.2002.02927.x.
31. Sant'Anna, F. H., Trentini, D. B., de Souto, W. S., Cecagno, R., da Silva, S. C., and Schrank, I. S. (2009). The PII superfamily revised: a novel group and evolutionary insights. J. Mol. Evol. 68, 322-336. doi: 10.1007/s00239-009-9209-6.
32. Shapiro, B. M. (1969). The glutamine synthetase deadenylylating enzyme system from Escherichia coli. Resolution into two components, specific nucleotide stimulation, and cofactor requirements. Biochemistry 8, 659-670. doi: 10.1021/bi00830a030.
33. Smith, C. S., Morrice, N. A., and Moorhead, G. B. (2004). Lack of evidence for phosphorylation of Arabidopsis thaliana PII: implications for plastid carbon and nitrogen signaling. Biochim. Biophys. Acta 1699, 145-154. doi: 10.1016/j.bbapap.2004.02.009.
34. Strosser, J., Ludke, A., Schaffer, S., Kramer, R., and Burkovski, A. (2004). Regulation of GlnK activity: modification, membrane sequestration and proteolysis as regulatory principles in the network of nitrogen control in Corynebacterium glutamicum. Mol. Microbiol. 54, 132-147. doi: 10.1111/j.1365-2958.2004.04247.x.
35. Thomas, G., Coutts, G., and Merrick, M. (2000). The glnKamtB operon: a conserved gene pair in prokaryotes. Trends Genet. 16, 11-14. doi: 10.1016/S0168-9525(99)01887-9.
36. Truan, D., Bjelic, S., Li, X. D., and Winkler, F. K. (2014). Structure and thermodynamics of effector molecule binding to the nitrogen signal transduction PII protein GlnZ from Azospirillum brasilense. J. Mol. Biol. 426, 2783-2799. doi: 10.1016/j.jmb.2014.05.008.
37. Truan, D., Huergo, L. F., Chubatsu, L. S., Merrick, M., Li, X. D., and Winkler, F. K. (2010). A new PII protein structure identifies the 2-oxoglutarate binding site. J. Mol. Biol. 400, 531-539. doi: 10.1016/j.jmb.2010.05.036.
38. Zeth, K., Fokina, O., and Forchhammer, K. (2014). Structural basis and target-specific modulation of ADP sensing by the Synechococcus elongatus PII signaling protein. J. Biol. Chem. 289, 8960-8972. doi: 10.1074/jbc.M113.536557.
39. Zhang, Y., Pohlmann, E. L., Serate, J., Conrad, M. C., and Roberts, G. P. (2010). Mutagenesis and functional characterization of the four domains of GlnD, a bifunctional nitrogen sensor protein. J. Bacteriol. 192, 2711-2721. doi: 10.1128/JB.01674-09.
40. Zhang, Y., Pu, H., Wang, Q., Cheng, S., Zhao, W., Zhang, Y., et al. (2007). PII is important in regulation of nitrogen metabolism but not required for heterocyst formation in the cyanobacterium Anabaena sp. PCC 7120. J. Biol. Chem. 282, 33641-33648. doi: 10.1074/jbc.M706500200.
41. Zhao, M. X., Jiang, Y. L., Xu, B. Y., Chen, Y., Zhang, C. C., and Zhou, C. Z. (2010). Crystal structure of the cyanobacterial signal transduction protein PII in complex with PipX. J. Mol. Biol. 402, 552-559. doi: 10.1016/j.jmb.2010.08.006.