Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Feb;175(4):1176–1181. doi: 10.1128/jb.175.4.1176-1181.1993

Autophosphorylation of nucleoside diphosphate kinase from Myxococcus xanthus.

J Muñoz-Dorado 1, N Almaula 1, S Inouye 1, M Inouye 1
PMCID: PMC193035  PMID: 8381783

Abstract

The nucleoside diphosphate kinase (NDP kinase) from Myxococcus xanthus has been purified to homogeneity and crystallized (J. Munoz-Dorado, M. Inouye, and S. Inouye, J. Biol. Chem. 265:2702-2706, 1990). In the presence of ATP, the NDP kinase was autophosphorylated. Phosphoamino acid analysis was carried out after acid and base hydrolyses of phosphorylated NDP kinase. It was found that the protein was phosphorylated not only at a histidine residue but also at a serine residue. Replacement of histidine 117 with a glutamine residue completely abolished the autophosphorylation and nucleotide-binding activity of the NDP kinase. Since histidine 117 is the only histidine residue that is conserved in all known NDP kinases so far characterized, the results suggest that the phosphohistidine intermediate is formed at this residue during the transphosphorylation reaction from nucleoside triphosphates to nucleoside diphosphates. Preliminary mutational analysis of putative ATP-binding sites is also presented.

Full text

PDF
1176

Images in this article

1177Image
on p.1177
1178Image
on p.1178
1179Image
on p.1179

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BERG P., JOKLIK W. K. Transphosphorylation between nucleoside polyphosphates. Nature. 1953 Nov 28;172(4387):1008–1009. doi: 10.1038/1721008a0. [DOI] [PubMed] [Google Scholar]
  2. Biggs J., Hersperger E., Steeg P. S., Liotta L. A., Shearn A. A Drosophila gene that is homologous to a mammalian gene associated with tumor metastasis codes for a nucleoside diphosphate kinase. Cell. 1990 Nov 30;63(5):933–940. doi: 10.1016/0092-8674(90)90496-2. [DOI] [PubMed] [Google Scholar]
  3. Biggs J., Tripoulas N., Hersperger E., Dearolf C., Shearn A. Analysis of the lethal interaction between the prune and Killer of prune mutations of Drosophila. Genes Dev. 1988 Oct;2(10):1333–1343. doi: 10.1101/gad.2.10.1333. [DOI] [PubMed] [Google Scholar]
  4. Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991 Jan 10;349(6305):117–127. doi: 10.1038/349117a0. [DOI] [PubMed] [Google Scholar]
  5. Duclos B., Marcandier S., Cozzone A. J. Chemical properties and separation of phosphoamino acids by thin-layer chromatography and/or electrophoresis. Methods Enzymol. 1991;201:10–21. doi: 10.1016/0076-6879(91)01004-l. [DOI] [PubMed] [Google Scholar]
  6. Dumas C., Lebras G., Wallet V., Lacombe M. L., Véron M., Janin J. Crystallization and preliminary X-ray diffraction studies of nucleoside diphosphate kinase from Dictyostelium discoideum. J Mol Biol. 1991 Jan 20;217(2):239–240. doi: 10.1016/0022-2836(91)90537-g. [DOI] [PubMed] [Google Scholar]
  7. Edlund B., Rask L., Olsson P., Wålinder O., Zetterqvist O., Engström L. Preparation of crystalline nucleoside diphosphate kinase from baker's yeast and identification of 1-[32P]phosphohistidine as the main phosphorylated product of an alkaline hydrolysate of enzyme incubated with adenosine [32P]triphosphate. Eur J Biochem. 1969 Jul;9(4):451–455. doi: 10.1111/j.1432-1033.1969.tb00630.x. [DOI] [PubMed] [Google Scholar]
  8. Gilles A. M., Presecan E., Vonica A., Lascu I. Nucleoside diphosphate kinase from human erythrocytes. Structural characterization of the two polypeptide chains responsible for heterogeneity of the hexameric enzyme. J Biol Chem. 1991 May 15;266(14):8784–8789. [PubMed] [Google Scholar]
  9. Hama H., Almaula N., Lerner C. G., Inouye S., Inouye M. Nucleoside diphosphate kinase from Escherichia coli; its overproduction and sequence comparison with eukaryotic enzymes. Gene. 1991 Aug 30;105(1):31–36. doi: 10.1016/0378-1119(91)90510-i. [DOI] [PubMed] [Google Scholar]
  10. Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. doi: 10.1126/science.3291115. [DOI] [PubMed] [Google Scholar]
  11. Hess J. F., Bourret R. B., Simon M. I. Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature. 1988 Nov 10;336(6195):139–143. doi: 10.1038/336139a0. [DOI] [PubMed] [Google Scholar]
  12. Hunter T., Sefton B. M. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1311–1315. doi: 10.1073/pnas.77.3.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. KREBS H. A., HEMS R. Some reactions of adenosine and inosine phosphates in animal tissues. Biochim Biophys Acta. 1953 Sep-Oct;12(1-2):172–180. doi: 10.1016/0006-3002(53)90136-x. [DOI] [PubMed] [Google Scholar]
  14. Kamps M. P., Sefton B. M. Acid and base hydrolysis of phosphoproteins bound to immobilon facilitates analysis of phosphoamino acids in gel-fractionated proteins. Anal Biochem. 1989 Jan;176(1):22–27. doi: 10.1016/0003-2697(89)90266-2. [DOI] [PubMed] [Google Scholar]
  15. Kimura N., Shimada N. Membrane-associated nucleoside diphosphate kinase from rat liver. Purification, characterization, and comparison with cytosolic enzyme. J Biol Chem. 1988 Apr 5;263(10):4647–4653. [PubMed] [Google Scholar]
  16. Kimura N., Shimada N., Nomura K., Watanabe K. Isolation and characterization of a cDNA clone encoding rat nucleoside diphosphate kinase. J Biol Chem. 1990 Sep 15;265(26):15744–15749. [PubMed] [Google Scholar]
  17. Lacombe M. L., Wallet V., Troll H., Véron M. Functional cloning of a nucleoside diphosphate kinase from Dictyostelium discoideum. J Biol Chem. 1990 Jun 15;265(17):10012–10018. [PubMed] [Google Scholar]
  18. Muñoz-Dorado J., Inouye M., Inouye S. Nucleoside diphosphate kinase from Myxococcus xanthus. I. Cloning and sequencing of the gene. J Biol Chem. 1990 Feb 15;265(5):2702–2706. [PubMed] [Google Scholar]
  19. Muñoz-Dorado J., Inouye S., Inouye M. Nucleoside diphosphate kinase from Myxococcus xanthus. II. Biochemical characterization. J Biol Chem. 1990 Feb 15;265(5):2707–2712. [PubMed] [Google Scholar]
  20. Pai E. F., Kabsch W., Krengel U., Holmes K. C., John J., Wittinghofer A. Structure of the guanine-nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation. Nature. 1989 Sep 21;341(6239):209–214. doi: 10.1038/341209a0. [DOI] [PubMed] [Google Scholar]
  21. Rosengard A. M., Krutzsch H. C., Shearn A., Biggs J. R., Barker E., Margulies I. M., King C. R., Liotta L. A., Steeg P. S. Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosophila development. Nature. 1989 Nov 9;342(6246):177–180. doi: 10.1038/342177a0. [DOI] [PubMed] [Google Scholar]
  22. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sedmak J., Ramaley R. Purification and properties of Bacillus subtilis nucleoside diphosphokinase. J Biol Chem. 1971 Sep 10;246(17):5365–5372. [PubMed] [Google Scholar]
  24. Stahl J. A., Leone A., Rosengard A. M., Porter L., King C. R., Steeg P. S. Identification of a second human nm23 gene, nm23-H2. Cancer Res. 1991 Jan 1;51(1):445–449. [PubMed] [Google Scholar]
  25. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  26. Wallet V., Mutzel R., Troll H., Barzu O., Wurster B., Veron M., Lacombe M. L. Dictyostelium nucleoside diphosphate kinase highly homologous to Nm23 and Awd proteins involved in mammalian tumor metastasis and Drosophila development. J Natl Cancer Inst. 1990 Jul 18;82(14):1199–1202. doi: 10.1093/jnci/82.14.1199. [DOI] [PubMed] [Google Scholar]
  27. Williams R. L., Muñoz-Dorado J., Jacobo-Molina A., Inouye S., Inouye M., Arnold E. Crystallization and preliminary X-ray diffraction analysis of oucleoside diphosphate kinase from Myxococcus xanthus. J Mol Biol. 1991 Jul 5;220(1):5–7. doi: 10.1016/0022-2836(91)90374-f. [DOI] [PubMed] [Google Scholar]
  28. Wålinder O. Identification of a phosphate-incorporating protein from bovine liver as nucleoside diphosphate kinase and isolation of 1-32P-phosphohistidine, 3-32P-phosphohistidine, and N-epsilon-32P-phospholysine from erythrocytic nucleoside diphosphate kinase, incubated with adenosine triphosphate-32P. J Biol Chem. 1968 Jul 25;243(14):3947–3952. [PubMed] [Google Scholar]
  29. de Vos A. M., Tong L., Milburn M. V., Matias P. M., Jancarik J., Noguchi S., Nishimura S., Miura K., Ohtsuka E., Kim S. H. Three-dimensional structure of an oncogene protein: catalytic domain of human c-H-ras p21. Science. 1988 Feb 19;239(4842):888–893. doi: 10.1126/science.2448879. [DOI] [PubMed] [Google Scholar]
  30. la Cour T. F., Nyborg J., Thirup S., Clark B. F. Structural details of the binding of guanosine diphosphate to elongation factor Tu from E. coli as studied by X-ray crystallography. EMBO J. 1985 Sep;4(9):2385–2388. doi: 10.1002/j.1460-2075.1985.tb03943.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES