Abstract
Protein histidine phosphorylation is well established as an important part of signalling systems in bacteria, fungi and plants and there is growing evidence of its role in mammalian cell biology. Compared to phosphoserine, phosphothreonine and phosphotyrosine, phosphohistidine is relatively labile, especially under the acidic conditions that were developed to analyse protein phosphorylation. In recent years, there has been an increasing impetus to develop specific methods for the analysis of histidine phosphorylation and assay of histidine kinase activity. Most recently attention has focussed on the application of mass spectrometry to this end. This review provides an overview of methods available for the detection and analysis of phosphohistidine in phosphoproteins, with particular emphasis on the application of mass spectrometric techniques.
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References
Pawson T, Scott JD (2005) Protein phosphorylation in signaling—50 years and counting. Trends Biochem Sci 30:286–290. doi:10.1016/j.tibs.2005.04.013
Attwood PV, Piggott MJ, Zu XL et al (2007) Focus on phosphohistidine. Amino Acids 32:145–156. doi:10.1007/s00726-006-0443-6
Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215. doi:10.1146/annurev.biochem.69.1.183
Besant PG, Attwood PV (2005) Mammalian histidine kinases. Biochim Biophys Acta 1754:281–290
Besant PG, Tan E, Attwood PV (2003) Mammalian protein histidine kinases. Int J Biochem Cell Biol 35:297–309. doi:10.1016/S1357-2725(02)00257-1
Edlund B, Heldin CH, Engstrom L (1982) Effect of chemical modification of a histidine and a lysine residue of pea seed nucleoside diphosphate kinase. Ups J Med Sci 87:243–250
Gross J, Rajavel M, Segura E et al (1996) Energy coupling in salmonella typhimurium nicotinic acid phosphoribosyltransferase—identification of his-219 as site of phosphorylation. Biochemistry 35:3917–3924. doi:10.1021/bi9517906
Huang JM, Wei YF, Kim YH et al (1991) Purification of a protein histidine kinase from the yeast Saccharomyces cerevisiae. The first member of this class of protein kinases. J Biol Chem 266:9023–9031
Huebner VD, Matthews HR (1985) Phosphorylation of histidine in proteins by a nuclear extract of Physarum polycephalum plasmodia. J Biol Chem 260:16106–16113
Kumble KD, Ahn K, Kornberg A (1996) Phosphohistidyl active sites in polyphosphate kinase of Escherichia Coli. Proc Natl Acad Sci USA 93:14391–14395. doi:10.1073/pnas.93.25.14391
Narindrasorasak S, Bridger WA (1977) Phosphoenolypyruvate synthetase of Escherichia Coli: molecular weight, subunit composition, and identification of phosphohistidine in phosphoenzyme intermediate. J Biol Chem 252:3121–3127
Spronk AM, Yoshida H, Wood HG (1976) Isolation of 3-phosphohistidine from phosphorylated pyruvate, phosphate dikinase. Proc Natl Acad Sci USA 73:4415–4419. doi:10.1073/pnas.73.12.4415
Tauler A, El-Maghrabi MR, Pilkis SJ (1987) Functional homology of 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphatase, phosphoglycerate mutase, and 2, 3-bisphosphoglycerate mutase. J Biol Chem 262:16808–16815
Walinder O (1969) Evidence of the presence of 1-phosphohistidine as the main phosphohistidine as the main phosphorylated component at the active site of bovine liver nucleoside diphosphate kinase. Acta Chem Scand 23:339–341. doi:10.3891/acta.chem.scand.23-0339
Waygood EB, Pasloske K, Delbaere LT et al (1988) Characterization of the 1-phosphohistidinyl residue in the phosphocarrier protein HPr of the phosphoenolpyruvate: sugar phosphotransferase system of Streptococcus faecalis. Biochem Cell Biol 66:76–80
Stock JB, Stock AM, Mottonen JM (1990) Signal transduction in bacteria. Nature 344:395–400. doi:10.1038/344395a0
Duclos B, Marcandier S, Cozzone AJ (1991) Chemical properties and separation of phosphoamino acids by thin-layer chromatography and/or electrophoresis. Methods Enzymol 201:10–21. doi:10.1016/0076-6879(91)01004-L
Hultquist DE (1968) The preparation and characterization of phosphorylated derivatives of histidine. Biochim Biophys Acta 153:329–340. doi:10.1016/0005-2728(68)90078-9
Lasker M, Bui CD, Besant PG et al (1999) Protein histidine phosphorylation: increased stability of thiophosphohistidine. Protein Sci 8:2177–2185
Wei YF, Matthews HR (1991) Identification of phosphohistidine in proteins and purification of protein-histidine kinases. Methods Enzymol 200:388–414. doi:10.1016/0076-6879(91)00156-Q
Pirrung MC, James KD, Rana VS (2000) Thiophosphorylation of histidine. J Org Chem 65:8448–8453. doi:10.1021/jo000771l
Kaldenberg-Stasch S, Baden M, Fesseler B et al (1994) Receptor-stimulated guanine-nucleotide-triphosphate binding to guanine-nucleotide-binding regulatory proteins. Nucleotide exchange and beta-subunit-mediated phosphotransfer reactions. Eur J Biochem 221:25–33. doi:10.1111/j.1432-1033.1994.tb18711.x
Nurnberg B, Harhammer R, Exner T et al (1996) Species- and tissue-dependent diversity of G-protein beta subunit phosphorylation: evidence for a cofactor. Biochem J 318:717–722
Wieland T, Nurnberg B, Ulibarri I et al (1993) Guanine nucleotide-specific phosphate transfer by guanine nucleotide-binding regulatory protein beta-subunits. Characterization of the phosphorylated amino acid. J Biol Chem 268:18111–18118
Wieland T, Ronzani M, Jakobs KH (1992) Stimulation and inhibition of human platelet adenylylcyclase by thiophosphorylated transducin beta gamma-subunits. J Biol Chem 267:20791–20797
Wieland T, Ulibarri I, Gierschik P et al (1991) Activation of signal-transducing guanine-nucleotide-binding regulatory proteins by guanosine 5′-[gamma-thio]triphosphate. Information transfer by intermediately thiophosphorylated beta gamma subunits. Eur J Biochem 196:707–716. doi:10.1111/j.1432-1033.1991.tb15869.x
Witt JJ, Roskoski R Jr (1975) Rapid protein kinase assay using phosphocellulose-paper absorption. Anal Biochem 66:253–258. doi:10.1016/0003-2697(75)90743-5
Smith DL, Chen CC, Bruegger BB et al (1974) Characterization of protein kinases forming acid-labile histone phosphates in Walker-256 carcinosarcoma cell nuclei. Biochemistry 13:3780–3785. doi:10.1021/bi00715a025
Wei YF, Morgan JE, Matthews HR (1989) Studies of histidine phosphorylation by a nuclear protein histidine kinase show that histidine-75 in histone H4 is masked in nucleosome core particles and in chromatin. Arch Biochem Biophys 268:546–550. doi:10.1016/0003-9861(89)90321-4
Wei YF, Matthews HR (1990) A filter-based protein kinase assay selective for alkali-stable protein phosphorylation and suitable for acid-labile protein phosphorylation. Anal Biochem 190:188–192. doi:10.1016/0003-2697(90)90179-D
Tan E, Lin Zu X, Yeoh GC et al (2003) Detection of histidine kinases via a filter-based assay and reverse-phase thin-layer chromatographic phosphoamino acid analysis. Anal Biochem 323:122–126. doi:10.1016/j.ab.2003.08.035
Besant PG, Attwood PV (2000) Detection of a mammalian histone H4 kinase that has yeast histidine kinase-like enzymic activity. Int J Biochem Cell Biol 32:243–253. doi:10.1016/S1357-2725(99)00119-3
Kameshita I, Fujisawa H (1996) Detection of protein kinase activities toward oligopeptides in sodium dodecyl sulfate-polyacrylamide gel. Anal Biochem 237:198–203. doi:10.1006/abio.1996.0229
Tan E, Besant PG, Zu XL et al (2004) Histone H4 histidine kinase displays the expression pattern of a liver oncodevelopmental marker. Carcinogenesis 25:2083–2088. doi:10.1093/carcin/bgh222
Kameshita I, Fujisawa H (1989) A sensitive method for detection of calmodulin-dependent protein kinase II activity in sodium dodecyl sulfate-polyacrylamide gel. Anal Biochem 183:139–143. doi:10.1016/0003-2697(89)90181-4
Crovello CS, Furie BC, Furie B (1995) Histidine phosphorylation of P-selectin upon stimulation of human platelets: a novel pathway for activation-dependent signal transduction. Cell 82:279–286. doi:10.1016/0092-8674(95)90315-1
Besant PG, Lasker MV, Bui CD et al (2000) Phosphohistidine analysis using reversed-phase thin-layer chromatography. Anal Biochem 282:149–153. doi:10.1006/abio.2000.4576
Walinder O (1968) 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 243:3947–3952
Besant PG, Attwood PV (1998) Problems with phosphoamino acid analysis using alkaline hydrolysis. Anal Biochem 265:187–190. doi:10.1006/abio.1998.2880
Hultquist DE, Moyer RW, Boyer PD (1966) The preparation and characterization of 1-phosphohistidine and 3-phosphohistidine. Biochemistry 5:322–331. doi:10.1021/bi00865a041
Collins MO, Yu L, Choudhary JS (2007) Analysis of protein phosphorylation on a proteome-scale. Proteomics 7:2751–2768. doi:10.1002/pmic.200700145
Ross AR (2007) Identification of histidine phosphorylations in proteins using mass spectrometry and affinity-based techniques. Methods Enzymol 423:549–572. doi:10.1016/S0076-6879(07)23027-7
Salih E (2005) Phosphoproteomics by mass spectrometry and classical protein chemistry approaches. Mass Spectrom Rev 24:828–846. doi:10.1002/mas.20042
Witze ES, Old WM, Resing KA et al (2007) Mapping protein post-translational modifications with mass spectrometry. Nat Methods 4:798–806. doi:10.1038/nmeth1100
Kinoshita E, Kinoshita-Kikuta E, Koike T (2007) Specific recognition and detection of phosphorylated proteins using characteristics of metal ion. Yakugaku Zasshi 127:1897–1913. doi:10.1248/yakushi.127.1897
Besant PG, Byrne L, Thomas G et al (1998) A chromatographic method for the preparative separation of phosphohistidines. Anal Biochem 258:372–375. doi:10.1006/abio.1998.2595
Zu XL, Besant PG, Imhof A et al (2007) Mass spectrometric analysis of protein histidine phosphorylation. Amino Acids 32:347–357. doi:10.1007/s00726-007-0493-4
Medzihradszky KF, Phillipps NJ, Senderowicz L et al (1997) Synthesis and characterization of histidine-phosphorylated peptides. Protein Sci 6:1405–1411
Kleinnijenhuis AJ, Kjeldsen F, Kallipolitis B et al (2007) Analysis of histidine phosphorylation using tandem MS and ion-electron reactions. Anal Chem 79:7450–7456. doi:10.1021/ac0707838
Napper S, Kindrachuk J, Olson DJ et al (2003) Selective 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 spectrometry. Anal Chem 75:1741–1747. doi:10.1021/ac026340f
Wind M, Wegener A, Kellner R et al (2005) Analysis of CheA histidine phosphorylation and its influence on protein stability by high-resolution element and electrospray mass spectrometry. Anal Chem 77:1957–1962. doi:10.1021/ac040140h
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We would like to thank the UWA Small Grant Scheme and the Raine Medical Research Foundation for their financial support.
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Besant, P.G., Attwood, P.V. Detection and analysis of protein histidine phosphorylation. Mol Cell Biochem 329, 93–106 (2009). https://doi.org/10.1007/s11010-009-0117-2
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DOI: https://doi.org/10.1007/s11010-009-0117-2