Amino Acids

, Volume 32, Issue 3, pp 347–357 | Cite as

Mass spectrometric analysis of protein histidine phosphorylation

  • X.-L. Zu
  • P. G. Besant
  • A. Imhof
  • P. V. Attwood
Article

Summary.

Protein histidine phosphorylation is now recognized as an important form of post-translational modification. The acid-lability of phosphohistidine has meant that this phosphorylation has not been as well studied as serine/threonine or tyrosine phosphorylation. We show that phosphohistidine and phosphohistidine-containing phosphopeptides derived from proteolytic digestion of phosphohistone H4 are detectable by ESI-MS. We also demonstrate reverse-phase HPLC separation of these phosphopeptides and their detection by MALDI-TOF-MS.

Keywords: Phosphohistidine – Mass spectrometry – Phosphoamino acid analysis – Histone H4 – Phosphopeptide – Histidine kinase 

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References

  1. Besant, PG, Attwood, PV 2000Detection of a mammalian histone H4 kinase that has yeast histidine kinase-like enzymic activityInt J Biochem Cell Biol32243253PubMedCrossRefGoogle Scholar
  2. Besant, PG, Attwood, PV 2005Mammalian histidine kinasesBiochim Biophys Acta1754281290PubMedGoogle Scholar
  3. Besant, PG, Lasker, MV, Bui, CD, Turck, CW 2000Phosphohistidine analysis using reversed-phase thin-layer chromatographyAnal Biochem282149153PubMedCrossRefGoogle Scholar
  4. Besant, PG, Tan, E, Attwood, PV 2003Mammalian protein histidine kinasesInt J Biochem Cell Biol35297309PubMedCrossRefGoogle Scholar
  5. Bonaldi, T, Regula, JT, Imhof, A 2004The use of mass spectrometry for the analysis of histone modificationsMethods Enzymol77111130Google Scholar
  6. Chen, CC, Smith, DL, Bruegger, BB, Halpern, RM, Smith, RA 1974Occurrence and distribution of acid-labile histone phosphates in regenerating rat liverBiochemistry1337853789PubMedCrossRefGoogle Scholar
  7. Chen, CC, Bruegger, BB, Kern, CW, Lin, YC, Halpern, RM, Smith, RA 1977Phosphorylation of nuclear proteins in rat regenerating liverBiochemistry1648524855PubMedCrossRefGoogle Scholar
  8. Cuello, F, Schulze, RA, Heemeyer, F, Meyer, HE, Lutz, S, Jakobs, KH, Niroomand, F, Wieland, T 2003Activation of heterotrimeric g proteins by a high energy phosphate transfer via nucleoside diphosphate kinase (NDPK) B and Gβ subunits. Complex formation of NDPK B with Gβγ dimers and phosphorylation of His-266 in GβJ Biol Chem27872207226PubMedCrossRefGoogle Scholar
  9. Fujitaki, JM, Fung, G, Oh, EY, Smith, RA 1981Characterization of chemical and enzymatic acid-labile phosphorylation of histone H4 using phosphorus-31 nuclear magnetic resonanceBiochemistry2036583664PubMedCrossRefGoogle Scholar
  10. Hippe, HJ, Lutz, S, Cuello, F, Knorr, K, Vogt, A, Jakobs, KH, Wieland, T, Niroomand, F 2003Activation of heterotrimeric g proteins by a high energy phosphate transfer via nucleoside diphosphate kinase (NDPK) B and Gβsubunits. Specific activation of Gsα by an NDPK B. Gβγ complex in H10 cellsJ Biol Chem27872277233PubMedCrossRefGoogle Scholar
  11. Huang, JM, Wei, YF, Kim, YH, Osterberg, L, Matthews, HR 1991Purification of a protein histidine kinase from the yeast Saccharomyces cerevisiae. The first member of this class of protein kinasesJ Biol Chem26690239031PubMedGoogle Scholar
  12. Kikkawa, S, Takahashi, K, Shimada, N, Ui, M, Kimura, N, Katada, T 1990Conversion of GDP into GTP by nucleoside diphosphate kinase on the gtp-binding proteinsJ Biol Chem2652153621540PubMedGoogle Scholar
  13. Kimura, N, Shimada, N 1988Direct interaction between membrane-associated nucleoside diphosphate kinase and GTP-binding protein (Gs), and its regulation by hormones and guanine nucleotidesBiochem Biophys Res Commun151248256PubMedGoogle Scholar
  14. Medzihradszky, KF, Phillipps, NJ, Senderowicz, L, Wang, P, Turck, CW 1997Synthesis and characterization of histidine-phosphorylated peptidesProtein Sci614051411PubMedCrossRefGoogle Scholar
  15. Muimo, R, Banner, SJ, Marshall, LJ, Mehta, A 1998Nucleoside diphosphate kinase and Cl-sensitive protein phosphorylation in apical membranes from ovine airway epitheliumAm J Respir Cell Mol Biol18270278PubMedGoogle Scholar
  16. Muimo, R, Hornickova, Z, Riemen, CE, Gerke, V, Matthews, H, Mehta, A 2000Histidine phosphorylation of annexin I in airway epitheliaJ Biol Chem2753663236636PubMedCrossRefGoogle Scholar
  17. Munoz-Dorado, J, Almaula, N, Inouye, S, Inouye, M 1993Autophosphorylation of nucleoside diphosphate kinase from myxococcus xanthusJ Bacteriol17511761181PubMedGoogle Scholar
  18. Napper, S, Kindrachuk, J, Olson, DJ, Ambrose, SJ, Dereniwsky, C, Ross, AR 2003Selective extraction and characterization of a histidine-phosphorylated peptide using immobilized copper(II) ion affinity chromatography and matrix-assisted laser desorption/ionization time-of-flight mass spectrometryAnal Chem7517411747PubMedCrossRefGoogle Scholar
  19. Smith, DL, Bruegger, BB, Halpern, RM, Smith, RA 1973New histone kinases in nuclei of rat tissuesNature246103104PubMedCrossRefGoogle Scholar
  20. Stock, AM, Robinson, VL, Goudreau, PN 2000Two-component signal transductionAnnu Rev Biochem69183215PubMedCrossRefGoogle Scholar
  21. Tan, E, Zu, XL, Yeoh, GC, Besant, PG, Attwood, PV 2003Detection of histidine kinases via a filter-based assay and reverse-phase thin-layer chromatographic phosphoamino acid analysisAnal Biochem323122126PubMedCrossRefGoogle Scholar
  22. Tan, E, Besant, PG, Zu, XL, Turck, CW, Bogoyevitch, MA, Lim, SG, Attwood, PV, Yeoh, GC 2004Histone H4 histidine kinase displays the expression pattern of a liver oncodevelopmental markerCarcinogenesis2520832088PubMedCrossRefGoogle Scholar
  23. Treharne, KJ, Marshall, LJ, Mehta, A 1994A novel chloride-dependent GTP-utilizing protein kinase in plasma membranes from human respiratory epitheliumAm J Physiol267L592L601PubMedGoogle Scholar
  24. Treharne, KJ, Riemen, CE, Marshall, LJ, Muimo, R, Mehta, A 2001Nucleoside diphosphate kinase – a component of the [Na+]- and [Cl]-sensitive phosphorylation cascade in human and murine airway epitheliumPflugers Arch443S97S102PubMedGoogle Scholar
  25. Uesaka, H, Yokoyama, M, Ohtsuki, K 1987Physiological correlation between nucleoside-diphosphate kinase and the enzyme-associated guanine nucleotide binding proteinsBiochem Biophys Res Commun143552559PubMedCrossRefGoogle Scholar
  26. Wei, YF, Matthews, HR 1990A filter-based protein kinase assay selective for alkali-stable protein phosphorylation and suitable for acid-labile protein phosphorylationAnal Biochem190188192PubMedCrossRefGoogle Scholar
  27. Wei, YF, Matthews, HR 1991Identification of phosphohistidine in proteins and purification of protein-histidine kinasesMethods Enzymol200388414PubMedCrossRefGoogle Scholar
  28. Wind, M, Wegener, A, Kellner, R, Lehmann, WD 2005Analysis of CheA histidine phosphorylation and its influence on protein stability by high-resolution element and electrospray mass spectrometryAnal Chem7719571962PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • X.-L. Zu
    • 1
  • P. G. Besant
    • 1
  • A. Imhof
    • 2
  • P. V. Attwood
    • 1
  1. 1.School of Biomedical, Biomolecular and Chemical Sciences (M310)The University of Western AustraliaCrawleyAustralia
  2. 2.Department of Molecular Biology, Adolf-Butenandt Institute, Histone Modifications GroupLudwig-Maximilians-University of MunichMunichGermany

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