Home LiteratureArticle Details
PMID: 9079902 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Characterization of membrane-associated Pseudomonas aeruginosa Ras-like protein Pra, a GTP-binding protein that forms complexes with truncated nucleoside diphosphate kinase and pyruvate kinase to modulate GTP synthesis.

Journal of bacteriology ·Vol. 179 ·No. 7 ·1997-04-00 ·Pages 2181-8

Chopade BA, Shankar S, Sundin GW, Mukhopadhyay S, Chakrabarty AM

Abstract

We report the purification and characterization of a protein from the membrane fraction of Pseudomonas aeruginosa showing intrinsic guanosine triphosphatase (GTPase) activity. The protein was purified as a 48-kDa polypeptide capable of binding and hydrolyzing GTP. The N-terminal sequence of the purified protein revealed its similarity to the Escherichia coli Ras-like protein (Era), and the protein cross-reacted with anti-Era antibodies. This protein was named Pseudomonas Ras-like protein (Pra). Anti-Pra antibodies also cross-reacted with E. coli Era protein. Pra is autophosphorylated in vitro, with phosphotransfer of the terminal phosphate from [gamma-32P]GTP but not [gamma-32P]ATP. Pra is capable of complex formation with the truncated 12-kDa form of nucleoside diphosphate kinase (Ndk) but not with the 16-kDa form. Purified Pra was also shown to physically interact with pyruvate kinase (Pk); Pk and Pra can form a complex, but when the 12-kDa Ndk, Pk, and Pra are all present, Pk has a higher affinity than Pra for forming a complex with the 12-kDa Ndk. The 12-kDa Ndk-Pra complex catalyzed increased synthesis of GTP and dGTP and diminished synthesis of CTP and UTP or dCTP and dTTP relative to their synthesis by uncomplexed Ndk. Moreover, the complex of Pra with Pk resulted in the specific synthesis of GTP as well when Pra was present in concentrations in excess of that of Pk. Membrane fractions from cells harvested in the mid-log phase demonstrated very little nucleoside triphosphate (NTP)-synthesizing activity and no detectable Ndk. Membranes from cells harvested at late exponential phase showed NTP-synthesizing activity and the physical presence of Ndk but not of Pk or Pra. In contrast, membrane fractions of cells harvested at early to late stationary phase showed predominant GTP synthesis and the presence of increasing amounts of Pk and Pra. It is likely that the association of Pra with Ndk and/or Pk restricts its intrinsic GTPase activity, which may modulate stationary-phase gene expression and the survival of P. aeruginosa by modulating the level of GTP.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/physiology Blotting, Western Cell Membrane/metabolism Escherichia coli Proteins GTP Phosphohydrolases/physiology GTP-Binding Proteins/physiology Guanosine Triphosphate/biosynthesis Macromolecular Substances Nucleoside-Diphosphate Kinase/metabolism Nucleotides/metabolism Oligopeptides/chemistry Protein Binding Pseudomonas aeruginosa/genetics,metabolism Pyruvate Kinase/metabolism RNA-Binding Proteins Species Specificity Substrate Specificity
Chemicals
Bacterial Proteins Escherichia coli Proteins Macromolecular Substances Nucleotides Oligopeptides RNA-Binding Proteins era protein, E coli Guanosine Triphosphate Pyruvate Kinase Nucleoside-Diphosphate Kinase GTP Phosphohydrolases GTP-Binding Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Chopade B A
Department of Microbiology and Immunology, University of Illinois College of Medicine, Chicago 60612-7344, USA.
Shankar S
Sundin G W
Mukhopadhyay S
Chakrabarty A M
References (35)
35 references, click to expand
  1. The ras oncogene--an important regulatory element in lower eucaryotic organisms.
    Microbiol Rev. 1989 Jun;53(2):171-85 PMID: 2547147
  2. Mutational analysis of nucleoside diphosphate kinase from Pseudomonas aeruginosa: characterization of critical amino acid residues involved in exopolysaccharide alginate synthesis.
    J Bacteriol. 1996 Dec;178(24):7120-8 PMID: 8955392
  3. Biochemical characterization of the essential GTP-binding protein Obg of Bacillus subtilis.
    J Bacteriol. 1994 Dec;176(23):7161-8 PMID: 7961487
  4. The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration.
    Mol Microbiol. 1993 Aug;9(3):435-42 PMID: 8412693
  5. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp.
    J Bacteriol. 1993 Dec;175(24):7982-9 PMID: 8253685
  6. Mechanism of adenylate cyclase activation by cholera toxin: inhibition of GTP hydrolysis at the regulatory site.
    Proc Natl Acad Sci U S A. 1977 Aug;74(8):3307-11 PMID: 198781
  7. Purification and characterization of the plasma membrane ATPase of Neurospora crassa.
    J Biol Chem. 1981 Dec 10;256(23):12343-9 PMID: 6457834
  8. Function and regulation of ras.
    Annu Rev Biochem. 1993;62:851-91 PMID: 8352603
  9. Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA.
    J Bacteriol. 1996 Aug;178(16):4990-6 PMID: 8759865
  10. Membrane-associated GTPases in bacteria.
    Mol Microbiol. 1992 May;6(10):1253-7 PMID: 1640828
  11. GTPase-dependent signaling in bacteria: characterization of a membrane-binding site for era in Escherichia coli.
    J Bacteriol. 1994 Jan;176(1):44-9 PMID: 8282709
  12. The Bacillus subtilis spo0B stage 0 sporulation operon encodes an essential GTP-binding protein.
    J Bacteriol. 1989 Mar;171(3):1362-71 PMID: 2537815
  13. Genetic analysis of yeast RAS1 and RAS2 genes.
    Cell. 1984 Jun;37(2):437-45 PMID: 6327067
  14. Expression and characterization of RNase III and Era proteins. Products of the rnc operon of Escherichia coli.
    J Biol Chem. 1990 Feb 15;265(5):2888-95 PMID: 2105934
  15. Cross-species complementation of the indispensable Escherichia coli era gene highlights amino acid regions essential for activity.
    J Bacteriol. 1995 Apr;177(8):2194-6 PMID: 7721709
  16. Pseudomonas aeruginosa: genes and enzymes of alginate synthesis.
    Trends Microbiol. 1994 May;2(5):151-7 PMID: 8055178
  17. ras genes.
    Annu Rev Biochem. 1987;56:779-827 PMID: 3304147
  18. Molecular mimicry in protein synthesis?
    Science. 1995 Dec 1;270(5241):1453-4 PMID: 7491488
  19. Sequence and genomic structure of ras homologues Dmras85D and Dmras64B of Drosophila melanogaster.
    Gene. 1987;51(2-3):129-37 PMID: 3110012
  20. G proteins: transducers of receptor-generated signals.
    Annu Rev Biochem. 1987;56:615-49 PMID: 3113327
  21. Analysis of the rnc locus of Coxiella burnetii.
    Mol Microbiol. 1994 Oct;14(2):291-300 PMID: 7830573
  22. Nucleoside diphosphate kinase from Escherichia coli.
    J Bacteriol. 1995 May;177(9):2524-9 PMID: 7730286
  23. Two forms of the nucleoside diphosphate kinase of Pseudomonas aeruginosa 8830: altered specificity of nucleoside triphosphate synthesis by the cell membrane-associated form of the truncated enzyme.
    J Bacteriol. 1996 Apr;178(7):1777-81 PMID: 8606147
  24. Pleiotropic changes resulting from depletion of Era, an essential GTP-binding protein in Escherichia coli.
    Mol Microbiol. 1991 Apr;5(4):951-7 PMID: 1906969
  25. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  26. Guanosine-5'-triphosphate hydrolysis and tubulin polymerization. Review article.
    Mol Cell Biochem. 1982 Sep 3;47(2):97-113 PMID: 6755216
  27. Nucleoside diphosphate kinase from Pseudomonas aeruginosa: characterization of the gene and its role in cellular growth and exopolysaccharide alginate synthesis.
    Mol Microbiol. 1996 Jun;20(5):965-79 PMID: 8809750
  28. Cloning of genes controlling alginate biosynthesis from a mucoid cystic fibrosis isolate of Pseudomonas aeruginosa.
    J Bacteriol. 1984 Jul;159(1):9-18 PMID: 6330052
  29. Role of a ras homolog in the life cycle of Schizosaccharomyces pombe.
    Cell. 1986 Jan 31;44(2):329-36 PMID: 3002633
  30. Aberrant transmembrane signal transduction in Dictyostelium cells expressing a mutated ras gene.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4905-9 PMID: 2885843
  31. Characterization and developmental expression of a Drosophila ras oncogene.
    Mol Cell Biol. 1985 Apr;5(4):885-9 PMID: 3921827
  32. The Escherichia coli Ras-like protein (Era) has GTPase activity and is essential for cell growth.
    Oncogene. 1988 Jun;2(6):539-44 PMID: 2838786
  33. Are guanine nucleotide binding proteins a distinct class of regulatory proteins?
    FEBS Lett. 1983 Nov 28;164(1):1-8 PMID: 6317436
  34. Fatty acylation is important but not essential for Saccharomyces cerevisiae RAS function.
    Mol Cell Biol. 1987 Jul;7(7):2344-51 PMID: 3302674
  35. Mating pheromone-like diffusible factor released by Schizosaccharomyces pombe.
    EMBO J. 1986 Aug;5(8):1991-3 PMID: 16453698
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1997-04-00
Pages
2181-8
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC178953
Subset
IM
Grants
NIAID NIH HHS · AI-16790-16 · United States
NIAID NIH HHS · AI-31546-03 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]