Chloroplast acetyl-CoA carboxylase activity is 2-oxoglutarate-regulated by interaction of PII with the biotin carboxyl carrier subunit

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 1, 2010, Pages 502-507

  Bourrellier, Ana Belen Feria ^a   Valot, Benoit ^b   Guillot, Alain ^c   Ambard Bretteville, Françoise ^a   Vidal, Jean ^a   Hodges, Michael ^a  

^a INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c CEMAGREF   (France)

Author keywords

Arabidopsis thaliana; Biotin carboxy; Carrier protein; PII protein organic acids fatty acid metabolism

Indexed keywords

2 OXOGLUTARIC ACID; ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE MAGNESIUM; BIOTIN; CARRIER PROTEIN; FATTY ACID; OXALOACETIC ACID; PII PROTEIN; PROTEIN DERIVATIVE; PYRUVIC ACID; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARABIDOPSIS; ARTICLE; BIOLOGICAL ACTIVITY; CARBON METABOLISM; CHLOROPLAST; FATTY ACID SYNTHESIS; IN VITRO STUDY; MASS SPECTROMETRY; NITROGEN METABOLISM; NONHUMAN; PLANT LEAF; PLASTID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING;

ACETYL COENZYME A; ACETYL-COA CARBOXYLASE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOTIN; CHLOROPLASTS; KETOGLUTARIC ACIDS; MOLECULAR SEQUENCE DATA; PII NITROGEN REGULATORY PROTEINS; PLANT LEAVES; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS);

EID: 76249096491     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0910097107     Document Type: Article

References (46)

1. Arcondeguy T, Jack R, Merrick M (2001) PII signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80-105.
2. Ninfa AJ, Jing P (2005) PII signal transduction proteins: sensors of ?-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8:168-173.
3. Forchhammer K (2004) Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets. FEMS Microbiol Rev 28:319-333.
4. Osanai T, Tanika K (2007) Keeping in touch with PII: PII-interacting proteins in unicellular cyanobacteria. Plant Cell Physiol 48:908-914.
5. Forchhammer K (2008) PII signal transducers: novel functional and structural insights. Trends Microbiol 16:65-72.
6. Uhrig RG, Ng KKS, Moorhead GBG (2009) PII in higher plants: a modern role for an ancient protein. Trends Plant Sci 14:505-511.
7. Coutts G, Thomas G, Blakey D, MerrickM(2002) Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO J 21:536-545.
8. Durand A, Merrick M (2006) In vitro analysis of the Escherichia coli AmtB-GlnK complex reveals a stoichiometric interaction and sensitivity to ATP and 2-oxoglutarate. J Biol Chem 281:29558-29567.
9. Heinrich A, et al. (2006) Interaction of the membrane-bound GlnK-AmtB complex with the master regulator of nitrogen metabolism TnrA in Bacillus subtilis. J Biol Chem 281:34909-34917.
10. Heurgo LF, et al. (2006) Interactions between PII proteins and nitrogenase regulatory enzymes DraT and DraG in Azospirillum brasilense. FEBS Lett 580:5232-5236.
11. Dodsworth JA, Leigh JA (2006) Regulation of nitrogenase by 2-oxoglutaratereversible, direct binding of a PII-like nitrogen sensor protein to dinitrogenase. Proc Natl Acad Sci USA 103:9779-9784.
12. Osanai T, Sato S, Tabata S, Tanaka K (2005) Identification of PamA as a PII-binding membrane protein important in nitrogen-related and sugar-catabolic gene expression in Synechocystis sp. PCC 6803. J Biol Chem 280:34684-34690.
13. Espinosa J, Forchhammer K, Burillo S, 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.
14. Burillo S, Luque I, Feuntes I, 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.
15. Heinrich A, Maheswaran M, Ruppert U, Forchhammer K (2004) The Synechococcus elongatus PII signal transduction protein controls arginine synthesis by complex formation with N-acetyl-L-glutamate kinase. Mol Microbiol 52:1303-1314.
16. Maheswaran M, Urbanke C, 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.
17. Hsieh M-H, Lam H-M, van de Loo FJ, Coruzzi G (1998) A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proc Natl Acad Sci USA 95:13965-13970.
18. Sugiyama K, Hayakawa T, Kudo T, Ito T, Yamaya T (2004) Interaction of N-acetyl glutamate kinase with a PII-like protein in rice. Plant Cell Physiol 45:1768-1778.
19. Ferrario-Méry S, et al. (2005) Physiological characterisation of Arabidopsis mutants affected in the expression of the putative regulatory protein PII. Planta 223:28-39.
20. Chen YM, et al. (2006) The PII signal transduction protein of Arabidopsis thaliana forms an arginine-regulated complex with plastid N-acetyl glutamate kinase. J Biol Chem 281:5726-5733.
21. Ferrario-Méry S, Besin E, Pichon O, Meyer C, Hodges M (2006) The regulatory PII protein controls arginine biosynthesis in Arabidopsis. FEBS Lett 580:2015-2020.
22. Mizuno Y, Moorhead GB, Ng KK (2007) Structural basis for the regulation of Nacetylglutamate kinase by PII in Arabidopsis thaliana. J Biol Chem 282:35733-35740.
23. Llácer JL, 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 USA 104:17644-17649.
24. Ferrario-Méry S, Meyer C, Hodges M (2008) Chloroplast nitrite uptake is enhanced in Arabidopsis PII mutants. FEBS Lett 582:1061-1066.
25. Sasaki Y, Nagano Y (2004) Plant acetyl-CoA carboxylase: Structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci Biotechnol Biochem 68: 1175-1184.
26. Mekhedov S, Martinez de Ilarduya O, Ohlrogge JB (2000) Toward a functional catalog of the plant genome. A survey of genes for lipid biosynthesis. Plant Physiol 122: 389-401.
27. Konishi T, Shinohara K, Yamada K, Sasaki Y (1996) Acetyl-CoA carboxylase in higher plants; most plants other than Gramineae have both the prokaryotic and the eukaryotic forms of this enzyme. Plant Cell Physiol 37:117-122.
28. Kamberov ES, Atkinson MR, Ninfa AJ (1995) The Escherichia coli signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J Biol Chem 270: 17797-17807.
29. Beez S, Fokina O, Herrmann C, Forchhammer K (2009) N-acetyl-L-glutamate kinase (NAGK) from oxygenic phototrophs: PII signal transduction across domains of life reveals novel insights in NAGK control. J Mol Biol 389:748-758.
30. Feria Bourrellier AB, Ferrario-Méry S, Vidal J, Hodges M (2009) Metabolite regulation of the interaction between Arabidopsis thaliana PII and N-acetyl-L-glutamate kinase. Biochem Biophys Res Commun 387:700-704.
31. Thelen JJ, Ohlogge JB (2002) The multisubunit acetyl-CoA carboxylase is strongly associated with the chloroplast envelope through non-ionic interactions to carboxyltransferase subunits. Arch Biochem Biophys 400:245-257.
32. Sasaki Y, Kozaki A, Hatano M (1997) Link between light and fatty acid synthesis: thioredoxin-linked reductive activation of plastidic acetyl-CoA carboxylase. Proc Natl Acad Sci USA 94:11096-11101.
33. Konishi T, Sasaki Y (1994) Compartmentalization of two forms of acetyl-CoA carboxylase in plants and the origin of their tolerance toward herbicides. Proc Natl Acad Sci USA 91:3598-3601.
34. Smith CS, Weljie AM, Moorhead GBG (2003) Molecular properties of the putative nitrogen sensor PII from Arabidopsis thaliana. Plant J 33:353-360.
35. Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolic concentrations in spinach leaves. Planta 193:530-535.
36. Ruppert U, Irmler A, Kloft N, Forchhammer K (2002) The novel protein phosphatase PphA from Synechocystis PCC 6803 controls dephosphorylation of the signalling protein PII. Mol Microbiol 44:855-864.
37. Yildiz O, Kalthoff C, Raunser S, Kühlbrandt W (2007) Structure of GlnK1 with bound effectors indicates regulatory mechanism for ammonia uptake. EMBO J 26:589-599.
38. Savage L J, Ohlrogge JB (1999) Phosphorylation of pea chloroplast acetyl-CoA carboxylase. Plant J 18:521-527.
39. Gálvez S, Lancien M, Hodges M (1999) Are isocitrate dehhydrogenases and 2-oxoglutarate involved in the regulation of glutamate synthesis? Trends Plant Sci 4: 484-490.
40. Baud S, Boutin J-P, Miquel M, Lepiniec L, Rochat C (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 40: 151-160.
41. Smith CS, Zaplachinski ST, Muench D, Moorhead GBG (2002) Expression and purification of the chloroplast putative nitrogen sensor, PII, of Arabidopsis thaliana. Protein Expr Purif 25:342-347.
42. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277:680-685.
43. Sinha P, Poland J, Schnolzer M, Rabilloud T (2001) A new silver staining apparatus and procedure for matrix-assisted laser desorption/ionization-time of flight analysis of proteins after two-dimensional electrophoresis. Proteomics 7:835-840.
44. Thelen JJ, Mekhedov S, Ohlrogge JB (2001) Brassicaceae express multiple isoforms of biotin carboxyl carrier protein in a tissue-specific manner. Plant Physiol 125: 2016-2028.
45. Albertin W, et al. (2007) Differential regulation of gene products in newly synthesized Brassica napus allotetraploids is not related to protein function nor subcellular localization. BMC Genomics 8:56.
46. Nikolau BJ, Hawke JC, Slack CR (1981) Acetyl-Coenzyme A carboxylase in maize leaves. Arch Biochem Biophys 211:605-612.