Preferences help
enabled [disable] Abstract
Number of results
2011 | 58 | 2 | 137-148
Article title

Phosphorylation of basic amino acid residues in proteins: important but easily missed

Title variants
Languages of publication
Reversible phosphorylation is the most widespread posttranslational protein modification, playing regulatory role in almost every aspect of cell life. The majority of protein phosphorylation research has been focused on serine, threonine and tyrosine that form acid-stable phosphomonoesters. However, protein histidine, arginine and lysine residues also may undergo phosphorylation to yield acid-labile phosphoramidates, most often remaining undetected in conventional studies of protein phosphorylation. It has become increasingly evident that acid-labile protein phosphorylations play important roles in signal transduction and other regulatory processes. Beside acting as high-energy intermediates in the transfer of the phosphoryl group from donor to acceptor molecules, phosphohistidines have been found so far in histone H4, heterotrimeric G proteins, ion channel KCa3.1, annexin 1, P-selectin and myelin basic protein, as well as in recombinant thymidylate synthase expressed in bacterial cells. Phosphoarginines occur in histone H3, myelin basic protein and capsidic protein VP12 of granulosis virus, whereas phospholysine in histone H1. This overview of the current knowledge on phosphorylation of protein basic amino-acid residues takes into consideration its proved or possible roles in cell functioning. Specific requirements of studies on acid-labile protein phosphorylation are also indicated.
Physical description
  • Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warszawa, Poland
  • Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warszawa, Poland
  • Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warszawa, Poland
  • Allen JJ, Lazerwith SE, Shokat KM (2005) Bio-orthogonal affinity purification of direct kinase substrates. J Am Chem Soc 127: 5288-5289.
  • Attwood PV, Piggott MJ, Zu XL, Besant PG (2007) Focus on phosphohistidine. Amino Acids 32: 145-156.
  • Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415: 198-205.
  • Besant PG, Attwood PV (1998) Problems with phosphoamino acid analysis using alkaline hydrolysis. Anal Biochem 265: 187-190.
  • Besant PG, Attwood PV (2000) Detection of mammalian histone H4 kinase that has yeast histidine kinase-like enzymic activity. Int J Biochem Cell Biol 32: 243-253.
  • Besant PG, Attwood PV (2005) Mammalian histidine kinases. Biochim Biophys Acta 1754: 281-290.
  • Besant PG, Attwood PV (2009) Detection and analysis of protein histidine phosphorylation. Mol Cell Biochem 329: 93-106.
  • Besant PG, Attwood PV (2010) Histidine phosphorylation in histones and in other mammalian proteins. Methods Enzymol 471: 403-426.
  • Besant PG, Lasker MV, Bui CD, Turck CW (2000) Phosphohistidine analysis using reversed-phase thin-layer chromatography. Anal Biochem 282: 149-153.
  • Besant PG, Tan E, Attwood PV (2003) Mammalian protein histidine kinases. Int J Biochem Cell Biol 35: 297-309.
  • Besant PG, Attwood PV, Piggott MJ (2009) Focus on phosphoarginine and phospholysine. Curr Protein Pept Sci 10: 536-550.
  • Blackwell GJ, Carnuccio R, Di Rosa M, Flower RJ, Parente L, Persico P (1980) Macrocortin: a polypeptide causing the anti-phospholipase effect of glucocorticoids. Nature 287: 147-149.
  • Blumer JB, Smrcka AV, Lanier SM (2007) Mechanistic pathways and biological roles for receptor-independent activators of G-proteins signaling. Pharmacol Ther 113: 488-506.
  • Boyer PD, Deluca M, Ebner KE, Hultquist DE, Peter JB (1962) Identification of phosphohistidine in digests from a probable intermediate of oxidative phosphorylation. J Biol Chem 237: PC3306-PC3308.
  • Broday L, Peng W, Kuo M, Salnikow K, Zorrodu M, Costa M (2000) Nickel compounds are novel inhibitors of histone H4 acetylation. Cancer Res 60: 238-241.
  • Cahalan MD, Wulff H, Chandy KG (2001) Molecular properties and physiological roles of ion channels in the immune system. J Clin Immunol 21: 235-252.
  • Carlson HK, Plate L, Price MS, Allen JJ, Shokat KM, Marletta MA (2010) Use of semisynthetic epitope to probe histidine kinase activity and regulation. Anal Biochem 397: 139-143.
  • Carreras CW, Santi DV (1995) The catalytic mechanism and structure of thymidylate synthase. Annu Rev Biochem 64: 721-762.
  • Chen CC, Smith DL, Bruegger BB, Halpern RM, Smith RA (1974) Occurrence and distribution of acid-labile histone phosphates in regenerating rat liver. Biochemistry 13: 3785-3789.
  • Chen CC, Bruegger BB, Kern CW, Lin YC, Halpern RM, Smith RA (1977) Phosphorylation of nuclear proteins in rat regenerating liver. Biochemistry 16: 4852-4855.
  • Cieśla J, Frączyk T, Zieliński Z, Sikora J, Rode W (2006) Altered mouse leukemia L1210 thymidylate synthase, associated with cell resistance to 5-fluoro-dUrd, is not mutated but rather reflects posttranslational modification. Acta Biochim Polon 53: 189-198.
  • Cohen P (2000) The regulation of protein function by multisite phosphorylation - A 25-year update. Trends Biochem Sci 25: 596-601.
  • Cohen BE, Lee G, Arispe N, Pollard HB (1995) Cyclic 3'-5'-adenosine monophosphate binds to annexin I and regulates calcium-dependent membrane aggregation and ion channel activity. FEBS Lett 377: 444-450.
  • Collet JF, Stoobant V, Pirard M, Delpierre G, Van Schaftingen E (1998) A new class of phosphotransferases phosphorylated on an aspartate residue in amino-terminal DXDX(T/V) motif. J Biol Chem 273: 14107-14112.
  • Costi MP, Ferrari S, Venturelli A, Calò S, Tondi D, Barlocco D (2005) Thymidylate synthase structure, function and implication in drug discovery. Curr Med Chem 12: 2241-2258
  • Coughlin SR (1994) Molecular mechanisms of thrombin signaling. Semin Hematol 31: 270-277.
  • Crovello CS, Furie BC, Furie B (1993) Rapid phosphorylation and selective dephosphorylation of P-selectin accomopanies platelet activation. J Biol Chem 268: 14590-14593.
  • 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.
  • Cuello F, Schultze RA, Heemeyer F, Meyer HE, Lutz S, Jakobs KH, Niroomand F, Wieland T (2003) Activation 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 Gβ. J Biol Chem 278: 7220-7226.
  • Czernik AJ, Girault J-A, Nairn AC, Chen J, Snyder G, Kebabian J, Greengard P (1991) Production of phosphorylation state-specific antibodies. Methods Enzymol 201: 264-283.
  • DeLuca M, Ebner KE, Hultquist DE, Kreil G, Peter JB, Moyer R, Boyer PD (1963) The isolation and identification of phosphohistidine from mitochondrial protein. Biochem Z 338: 512-525.
  • Deutscher J, Saier MH Jr (2005) Ser/Thr/Tyr protein phosphorylation in bacteria - for long time neglected, now well established. J Mol Microbiol Biotechnol 9: 125-131.
  • DiSabato G, Jencks WP (1961) Mechanism and catalysis of reactions of acyl phosphates. I. Nucleophilic reactions. J Am Chem Soc 83: 4393-4400.
  • Donnelly SR, Moss SE (1997) Annexins in the secretory pathway. Cell Mol Life Sci 53: 533-538.
  • Dorovkov MV, Ryazanov AG (2004) Phosphorylation of annexin I by TRPM7 channel-kinase. J Biol Chem 279: 50643-50646.
  • 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.
  • Ek P, Pettersson G, Ek B, Gong F, Li JP, Zetterquist O (2002) Identification and characterization of a mammalian 14-kDa phosphohistidine phosphatases. Eur J Biochem 269: 5016-5023.
  • Engel M, Veron M, Theisinger B, Lacombe M-L, Seib T, Dooley S, Welter C (1995) A novel serine/threonine-specific protein phosphotransferase activity of Nm23/nucleoside diphosphate kinase. Eur J Biochem 234: 200-207.
  • Engelhardt S, Rochais F (2007) G proteins: more than transducers of receptor-generated signals? Circ Res 100: 1109-1111.
  • Feldman F, Butler FG (1969) Detection and characterization of the phosphorylated form of microsomal glucose-6-phosphatase. Biochem Biophys Res Commun 36: 119-125.
  • Frączyk T, Ruman T, Rut D, Dąbrowska-Maś E, Cieśla J, Zieliński Z, Sieczka K, Dębski J, Gołos B, Wińska P, Wałajtys-Rode E, Shugar D, Rode W (2009) Histidine phosphorylation, or tyrosine nitration, affect thymidylate synthase properties. Pteridines 20: 137-142.
  • Fujimoto T, McEver RP (1993) The cytoplasmic domain of P-selectin is phosphorylated on serine and threonine residues. Blood 82: 1758-1766.
  • Fujitaki JM, Smith RA (1984) Techniques in the detection and characterization of phosphoramidate-containing proteins. Methods Enzymol 107: 23-36.
  • Fujitaki JM, Fung G, Oh EY, Smith RA (1981) Characterization of chemical and enzymatic acid-labile phosphorylation of histone H4 using phosphorus-31 nuclear magnetic resonance. Biochemistry 20: 3658-3664.
  • Gerke V, Moss SE (1997) Annexins and membrane dynamics. Biochim Biophys Acta 1357: 129-154.
  • Ghosh A, Shieh J-J, Pan C-J, Chou JY (2004) Histidine 167 is the phosphate acceptor in glucose-6-phosphatase-βforming a phosphohistidine enzyme intermediate during catalysis. J Biol Chem 279: 12479-12483.
  • Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56: 615-649.
  • Gottlin EB, Rudolph AE, Zhao Y, Matthews HR, Dixon JE (1998) Catalytic mechanism of the phospholipase D superfamily proceeds via a covalent phosphohistidine intermediate. Proc Natl Acad Sci USA 95: 9202-9207.
  • Grefen C, Harter K (2004) Plant two-component systems: principles, functions, complexity and cross-talk. Planta 219: 733-742.
  • Hardison R, Chalkley R (1978) Polyacrylamide gel electrophoretic fractionation of histones. Methods Cell Biol 17: 235-251.
  • Hermesmeier J, Klumpp S (1999) Histidine phosphatases activity in vertebrates. Pharm Med Chem 332: 34.
  • Hess JF, Bourret RB, Simon MI (1988) Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature 336: 139-143.
  • Hippe HJ, Lutz S, Cuello F, Knorr K, Vogt A, Jakobs KH, Wieland T (2003) Activation of heterotrimeric G proteins by a high energy phosphate transfer via nucleoside diphosphate kinase (NDPK) B and Gβ subunits. Specific activation of Gsα by NDPK B. Gβγ complex in H10 cells. J Biol Chem 278: 7227-7233.
  • Hippe HJ, Luedde M, Lutz S, Koehler H, Eschenhagen T, Frey N, Katus HA, Wieland T, Niroomand F (2007) Regulation of cardiac cAMP synthesis and contractility by nucleoside diphosphate kinase B/G protein βγ dimer complexes. Circ Res 100: 1191-1199.
  • Hohenegger M, Mitterauer T, Voss T, Nanoff C, Freissmuth M (1996) Thiophosphorylation of the G protein beta subunit in human platelet membranes: evidence against a direct phosphate transfer reaction to Gα subunits. Mol Pharmacol 49: 73-80.
  • Homeyer N, Horn AH, Lanig H, Sticht H (2006) AMBER force-field parameters for phosphorylated amino acids in different protonation states: phosphoserine, phosphothreonine, phosphotyrosine, and phosphohistidine. J Mol Model 12: 281-289.
  • Huang Y, Wei Y, Kim Y, Osterberg L, Matthews HR (1991) Purification of protein histidine kinase from yeast Saccharomyces cerevisiae. The first member of this class of protein kinases. J Biol Chem 266: 9023-9031.
  • Hultquist DE (1968) The preparation and characterization of phosphorylated derivatives of histidine. Biochim Biophys Acta 153: 329-340.
  • Jarmuła A, Frączyk T, Cieplak P, Rode W (2010) Mechanism of influence of phosphorylation on serine 124 on a decrease of catalytic activity of human thymidylate synthase. Bioorg Med Chem 18: 3361-3370.
  • Johnston GI, Cook RG, McEver RP (1989) Cloning of GMP-140, a granule membrane protein of platelets and endothelium: sequence similarity to protein involved in cell adhesion and inflammation. Cell 56: 1033-1044.
  • Kee J-M, Villani B, Carpenter LR, Muir TW (2010) Development of stable phosphohistidine analogues. J Am Chem Soc 132: 14327-14329.
  • Khorasanizadeh S (2004) The nucleosome: from genomic organization to genomic regulation. Cell 116: 259-272.
  • Kim Y, Huang J, Cohen P, Matthews HR (1993) Protein phosphatases 1, 2A and 2C are protein histidine phosphatases. J Biol Chem 268: 18513-18518.
  • Kimura N, Shimada N, Fukuda M, Ishijama Y, Miyazaki H, Ishii A, Takagi Y, Ishikawa N (2000) Regulation of cellular functions by nucleoside diphosphate kinase in mammals. J Bioenerg Biomembr 32: 309-315.
  • Kimura N, Shimada N, Ishijama Y, Fukuda M, Takagi Y, Ishikawa N (2003) Nucleoside diphosphate kinases in mammalian signal transduction systems: recent development and perspective. J Bioenerg Biomembr 35: 41-47.
  • Kleinnijenhuis AJ, Kjelsden F, Kalipolitis B, Haselmann KF, Jensen ON (2007) Analysis of histidine phosphorylation using tandem MS and ion-electron reactions. Anal Chem 79: 7450-7456.
  • Klumpp S, Krieglstein J (2002) Phosphorylation and dephosphorylation of histidine residues in proteins. Eur J Biochem 269: 1067-1071.
  • Klumpp S, Krieglstein J (2009) Reversible phosphorylation of histidine residues in proteins from vertebrates. Sci Signal 2: pe13.
  • Klumpp S, Hermesmeier J, Selke D, Bechmann G, van den Brulle J, Weidner G, Scharm B, Güssow D, Baumeister R, Kellner R, Krieglstein J (2002) Protein histidine phosphatase: a novel enzyme with potency for neuronal signaling. J Cereb Blood Flow Metab 22: 1420-1424.
  • Koshland DE Jr (1952) Effect of catalysts on the hydrolysis of acetyl phosphate. nucleophilic displacement mechanisms in enzymatic reactions. J Am Chem Soc 74: 2286-2292.
  • Kosinsky YA, Volynsky PE, Lagant P, Vergoten G, Suzuki E, Arseniev AS, Efremov RG (2004) Development of the force field parameters for phosphoimidazole and phosphohistidine. J Comput Chem 25: 1313-1321.
  • Kowalewska K, Stefanowicz P, Ruman T, Frączyk T, Rode W, Szewczuk Z (2010) Electron capture dissociation mass spectrometric analysis of lysine-phosphorylated peptides. Biosci Rep 30: 433-443
  • Kowluru A (2002) Identification and characterization of a novel protein histidine kinase in the islet β-cell: evidence for its regulation by mastoparan, an activator of G-proteins and insulin secretion. Biochem Pharmacol 63: 2091-2100.
  • Kowluru A (2003) Regulatory roles for small G-proteins in the pancreatic beta cell: lessons from models of impaired insulin secretion. Am J Physiol Endocrynol Metab 285: E669-684.
  • Kowluru A (2008) Emerging roles for protein histidine phosphorylation in cellular signal transduction: lessons from the islet β-cell. J Cell Mol Med 12: 1885-1908.
  • Kowluru A, Metz SA (1994) Characterization of nucleoside diphosphokinase activity in human and rodent pancreatic beta cells: evidence for its role in the formation of guanosine triphosphate, a permissive factor for nutrient-induced insulin secretion. Biochemistry 33: 12495-12503.
  • Kowluru A, Seavey SE, Rhodes CJ, Metz SA (1996) A novel regulatory mechanism for trimeric GTP-binding proteins in the membrane and secretory granule fractions of human and rodent beta cells. Biochem J 313: 97-108.
  • Krivanek J, Novakova L (1991) ATP-citrate lyase is another enzyme the histidine phosphorylation of which is inhibited by vanadate. FEBS Lett 282: 32-34.
  • Kruppa M, Calderone R (2006) Two-component signal transduction in human fungal pathogens. FEMS Yeast Res 6: 149-159.
  • Kumon A, Kodama H, Kondo M, Yokoi F, Hiraishi H (1996) Nω-phosphoarginine phosphatases (17 kDa) and alkaline phosphatases as protein arginine phosphatases. J Biochem 119: 719-724.
  • Lapek JD, Tombline G, Friedman AE (2011) Mass spectrometry detection of histidine phosphorylation on NM23 H1. J Proteome Res 10: 751-755.
  • Larsen E, Celi A, Gilbert GE, Furie BC, Erban JK, Bonfanti R, Wagner DD, Furie B (1989) PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes Cell 59: 305-312.
  • Lasker M, Bui CD, Besant PG, Sugawara K, Thai P, Medzihradszky G, Turck CW (1999) Protein histidine phosphorylation: increased stability of thiophosphohistidine. Protein Sci 8: 2177-2185.
  • Levy-Favatier F, Depelch M, Kruh J (1987) Characterization of the arginine-specific protein kinase tightly bound to rat liver DNA. Eur J Biochem 166: 617-621.
  • Lienhard GE (2008) Non-functional phosphorylations? Trends Biochem Sci 33: 351-352.
  • Lim LKH, Pervaiz S (2007) Annexin 1: the new face of an old molecule. FASEB J 21: 968-975.
  • Lott JS, Paget B, Johnston JM, Delbaere LTJ, Sigrell-Simon JA, Banfield MJ, Baker EN (2006) The structure of an ancient conserved domain establishes a structural basis for stable histidine phosphorylation and identifies a new family of adenosine-specific kinases. J Biol Chem 281: 22131-22141.
  • Lu Y, Hu Q, Yang C, Gao F (2006) Histidine 89 is an essential residue for Hsp70 in the phosphate transfer reaction. Cell Stress Chaperones 11: s 148-153.
  • Lutz S, Mura RA, Hippe HJ, Tiefenbacher C, Niroomand F (2003) Plasma membrane-associated nucleoside diphosphate kinase (nm23) in the heart is regulated by β-adrenergic signaling. Br J Pharmacol 140: 1019-1026.
  • Manning C, Plowman GD, Hunter T, Sudarsanam S (2002) Evolution of protein kinase signalling from yeast to man. Trends Biochem Sci 27: 514-520.
  • Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002a) The protein kinase complement of the human genome. Science 298: 1912-1934.
  • Marcus F, Morrison JF (1964) The preparation of phosphoarginine: a comparative study. Biochem J 92: 429-435.
  • Matthews HR (1995) Protein kinases and phosphatases that act on histidine, lysine, or arginine residues in eukaryotic proteins: a possible regulator of the mitogen activated protein kinase cascade. Pharmacol Ther 67: 323-350.
  • Matthews HR, Mackintosh C (1995) Protein histidine phosphatase activity in rat liver and spinach leaves. FEBS Lett 364: 51-54.
  • Matthews HR, Wei YF (1991) Identification of phosphohistidine in proteins and purification of protein-histidine kinases. Methods Enzymol 200: 388-414.
  • Mäurer A, Wieland T, Meissl F, Niroomand F, Mehringer R, Krieglstein J, Klumpp S (2005) The β-subunit of G proteins is a substrate of protein histidine phosphatase. Biochem Biophys Res Commun 334: 1115-1120.
  • McTigue JJ, Van Etten RL (1978) An essential active-site histidine residue in human prostatic acid phosphatase. Ethoxyformylation by diethyl pyrocarbonate and phosphorylation by a substrate. Biochim Biophys Acta 523: 407-421.
  • Meadow ND, Fox DK, Roseman S (1990) The bacterial phosphoenolpyruvate: glycose phosphotransferase system. Annu Rev Biochem 59: 497-542.
  • Mehta A, Orchard S (2010) Nucleoside diphosphate kinase (NDPK, NM23, AWD): recent regulatory advances in endocytosis, metastasis, psoriasis, insulin release, fetal erythroid lineage and heart failure; translational medicine exemplified. Mol Cell Biochem 329: 3-15.
  • Medzihradszky KF, Phillipps NJ, Senderowicz L, Wang P, Turck CW (1997) Synthesis and characterization of histidine-phosphorylated peptides. Protein Sci 6: 1405-1411.
  • Mizoguchi H, Cook PF, Haseman CA, Uyeda K (1999) Reaction mechanism of fructose 2,6-bisphosphatase. A mutation of nucleophilic catalyst, histidine 256, induces and alteration in the reaction pathway. J Biol Chem 274: 2166-2175.
  • Muimo R, Banner SJ, Marshal LJ, Mehta A (1998) Nucleotide diphosphate kinase and Cl- sensitive protein phosphorylation in apical membranes form ovine airway epithelium. Am J Respir Cell Mol Biol 18: 270-278.
  • Muimo R, Hornickova Z, Riemen CE, Gerke V, Matthews H, Mehta A (2000) Histidine phosphorylation of annexin I in airway epithelia. J Biol Chem 275: 36632-36636.
  • Mulla A, Christian HC, Solito E, Mendoza N, Morris JF, Buckingham JC (2004) Expression, subcellular localization and phosphorylation status of annexins 1 and 5 in human pituitary adenomas and a growth hormone-secreting carcinoma. Clin Endocrinol (Oxf) 60: 107-119.
  • Ohmori H, Kuba M, Kumon A (1993) Two phosphatases for 6-phospholysine and 3-phosphohistidine from rat brain. J Biol Chem 268: 7625-7627.
  • Ostrowski W (1978) Isolation of tau-phosphohistidine from a phosphoryl-enzyme intermediate of human prostatic acid phosphatase. Biochim Biophys Acta 526: 147-153.
  • Pigiet V, Conley RR (1978) Isolation and characterization of phosphothioredoxin from Excherichia coli. J Biol Chem 253: 1910-1920.
  • Pilkis SJ, Walderhaug M, Murray K, Beth A, Venkataramu SD, Pilkis J, El-Maghrabi MR (1983) 6-phosphofructo-2-kinase/fructose 2,6-bisphosphatase from rat liver. J Biol Chem 258: 6135-6141.
  • Pirrung MC, James KD, Rana VS (2000) Thiophosphorylation of histidine. J Org Chem 65: 8448-8453.
  • Post RL, Kume S (1973) Evidence for an aspartyl phosphate residue at the active site of sodium and potassium ion transport adenosine triphosphatase. J Biol Chem 248: 6993-7000.
  • Raynal P, Pollard HB (1994) Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim Biophys Acta 1197: 63-93.
  • Rescher U, Gerke V (2004) Annexins - unique membrane binding proteins with diverse functions. J Cell Sci 2631-2639.
  • Robertson EF, Hoyt JC, Reeves HC (1988) Evidence of histidine phosphorylation in isocitrate lyase from Escherichia coli. J Biol Chem 263: 2477-2482.
  • Rockman HA, Koch WJ, Lefkowitz RJ (2002) Seven-transmembrane-spanning receptors and heart function. Nature 415: 206-212.
  • Rose ZB (1970) Evidence for a phosphohistidine protein intermediate in the phosphoglycerate mutase reaction. Arch Biochem Biophys 140: 508-513.
  • Ross ARS (2007) Identification of histidine phosphorylations in proteins using mass spectrometry and affinity-based techniques. Methods Enzymol 423: 549-572.
  • Ross AH, Baltimore D, Eisen HN (1981) Phosphotyrosine-containing proteins isolated by affinity chromatography with antibodies to a synthetic hapten. Nature 294: 654-656.
  • Rothhut B (1997) Participation of annexins in protein phosphorylation. Cell Mol Life Sci 53: 522-526.
  • Roymans D, Willems R, Van Blockstaele DR, Slegers H (2002) Nucleoside diphosphate kinase (NDPK/NM23) and the waltz with multiple partners: possible consequences in tumor metastasis. Clin Exp Metastasis 19: 465-476.
  • Ruman T, Długopolska K, Jurkiewicz A, Kramarz D, Frączyk T, Leś A, Rode W (2009) The synthesis, reactivity and NMR investigation on 15N-thiophosphoramidates. Lett Org Chem 6: 642-647.
  • Ruman T, Długopolska K, Jurkiewicz A, Rut D, Frączyk T, Cieśla J, Leś A, Szewczuk Z, Rode W (2010) Thiophosphorylation of free amino acids and enzyme protein by thiophosphoramidate ions. Bioorg Chem 38: 74-80.
  • Samsonoff WA, Reston J, McKee M, O'Connor B, Galivan J, Maley G, Maley F (1997) Intracellular location of thymidylate synthase and its state of phosphorylation. J Biol Chem 272: 13281-13285.
  • Schenkels C, Erni B, Reymond JL (1999) Phosphofurylalanine, a stable analog of phosphohistidine. Bioorg Med Chem Lett 9: 1443-1446.
  • Seemann J, Weber K, Gerke V (1997) Annexin I targets S100C to early endosomes. FEBS Lett 413: 185-190.
  • Shibata K, Inagaki M, Ajiro K (1990) Mitosis-specific histone H3 phosphorylation in vitro in nucleosome structures. Eur J Biochem 192: 87-93.
  • Smith DL, Bruegger BB, Halpern RM, Smith RA (1973) New histone kinases in nuclei of rat tissues. Nature 246: 103-104.
  • Smith DL, Chen CC, Bruegger BB, Holtz SL, Halpern RM, Smith RA (1974) Characterization of protein kinases forming acid-labile histone phosphates in Walker-256 carcinoma cell nuclei. Biochemistry 13: 3780-3785.
  • Smith LS, Kern CW, Halpern RM, Smith RA (1976) Phosphorylation on basic amino acids in myelin basic protein. Biochem Biophys Res Commun 71: 459-465.
  • Solito E, Christian HC, Festa M, Mulla A, Tierney T, Flower RJ, Buckingham JC (2006) Post-translational modification plays an essential role in the translocation of annexin A1 from the cytoplasm to the cell surface. FASEB J 20: 1498-500.
  • Srivastava S, Li Z, Ko K, Choudhury P, Albaqumi M, Johnson AK, Yan Y, Backer JM, Unutmaz D, Coetzee WA, Skolnik EY (2006) Histidine phosphorylation of the potassium channel KCa3.1 by nucleoside diphosphate kinase B is required for activation of KCa3.1 and CD4 T cells. Mol Cell 24: 665-675.
  • Srivastava S, Choudhury P, Li Z, Liu G, Nadkarni V, Ko K, Coetzee WA, Skolnik EY (2006a) Phosphatidylinositol 3-phosphate indirectly activates KCA3.1 via 14 amino acids in the carboxy terminus of KCa3.1. Mol Biol Cell 17: 146-154.
  • Srivastava S, Zhdanova O, Di L, Li Z, Albaqumi M, Wulff H, Skolnik EY (2008) Protein histidine phosphatases 1 negatively regulates CD4 T cells by inhibiting the K+ channel KCa3.1. Proc Natl Acad Sci USA 105: 14442-14446.
  • Stadtman TC (1994) Emerging awarness of the critical roles of S-phosphocysteine and selenophosphate in biological systems. BioFactors 4: 181-185.
  • Steeg PS, Palmieri D, Ouatas T, Salerno M (2003) Histidine kinases and histidine phosphorylated proteins in mammalian cell biology, signal transduction and cancer. Cancer Lett 190: 1-12.
  • Steiner AW, Helander ER, Fujitaki JM, Smith LS, Smith RA (1980) High-performance liquid chromatography of acid-stable and acid-labile phosphoamino acids. J Chromatogr 202: 263-269.
  • Stock JB, Stock AM, Mottonen JM (1990) Signal transduction in bacteria. Nature 344: 395-400.
  • Tan E, Besant PG, Attwood PV (2002) Mammalian histidine kinases: do they really exist? Biochemistry 41: 3843-3851.
  • Tan E, Lin SG, Zu X, Yeoh GC, Besant PG, Attwood PV (2003) Detection of histidine kinases via a filter-based assay and reverse-phase thin-layer chromatographic phosphoamino acid analysis. Anal Biochem 323: 122-126.
  • Tan E, Besant PG, Zu XL, Turck CW, Bogoyevitch MA, Lin SG, Attwood PV, Yeoh GC (2004) Histone H4 histidine kinase displays the expression pattern of a liver oncodevelopmental marker. Carcinogenesis 25: 2083-2088.
  • Treharne KJ, Crawford RM, Mehta A (2006) CFTR, chloride concentration and cell volume: could mammalian protein histidine phosphorylation play a latent role? Exp Physiol 91: 131-139.
  • Wakim BT, Aswad GD (1994) Ca2+-calmodulin-dependent phosphorylation of arginine in histone 3 by a nuclear kinases from mouse leukemia cells. J Biol Chem 269: 2722-2727.
  • Wakim BT, Grutkoski PS, Vaughan AT, Engelmann GL (1995) Stimulation of a Ca2+-calmodulin-activated histone 3 arginine kinase in quiescent rat heart endothelial cells compared to actively dividing cells. J Biol Chem 270: 23155-23158.
  • Waygood EB, Erickson E, el-Kabbani OA, Delbaere LT (1985) Characterization of phosphorylated histidine-containing protein (HPr) of the bacterial phosphoenolpyruvate:sugar phosphotransferase system. Biochemistry 24: 6938-6945.
  • Wålinder 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.
  • 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.
  • Wettschureck N, Offermanns S (2005) Mammalian G proteins and their cell type specific functions. Physiol Rev 85: 1159-1204.
  • Wieland T (2007) Interaction of nucleoside diphosphate kinase B with heterotrimeric G protein βγ dimers: consequences on G protein activation and stability. Naunyn-Schmiedeberg's Arch Pharmacol 374: 373-383.
  • Wieland T, Ulibarri I, Gierschik P, Jakobs KH (1991) Activation of signal-transducing guanine-nucleotide-binding regulatory proteins by guanosine 5'-[γ-thio]triphosphate. Information transfer by intermediately thiophosphorylated βγ subunits. Eur J Biochem 196: 707-716.
  • Wieland T, Ronzani M, Jakobs KH (1992) Stimulation and inhibition of human platelet adenylcyclase by thiophosphorylated transducin βγ-subunits. J Biol Chem 267: 20791-20797.
  • Wieland T, Nürnberg B, Ulibarri I, Kaldenberg-Stasch S, Schultz G, Jakobs KH (1993) Guanine nucleotide-specific phosphate transfer by guanine nucleotide-binding regulatory protein β-subunits. Characterization of the phosphorylated amino acid. J Biol Chem 268: 18111-18118.
  • Wieland T, Hippe H-J, Ludwig K, Zhou X-B, Korth M, Klumpp S (2010) Reversible histidine phosphorylation in mammalian cells: a teeter-totter formed by nucleoside diphosphate kinase and protein histidine phosphatase 1. Methods Enzymol 471: 379-402.
  • Williams SP, Sykes BD, Bridger WA (1985) Phosphorus-31 nuclear magnetic resonance study of the active site phosphohistidine and regulatory phosphoserine residues of rat liver ATP-citrate lyase. Biochemistry 24: 5527-5531.
  • Wilson ME, Consigli RA (1985) Characterization of a protein kinase activity associated with purified capsids of the granulosis virus infecting Plodia interpunctella. Virology 143: 516-525.
  • Wong C, Faiola B, Wu W, Kennelly PJ (1993) Phosphohistidine and phospholysine phosphatases activities in the rat: potential protein-lysine and protein-histidine phosphatases? Biochem J 296: 293-296.
  • Yano M, Mori S, Kido H (1999) Intrinsic nucleoside diphosphate kinase-like activity is a novel function of 20 S proteasome. J Biol Chem 274: 34375-34382.
  • Zetterquist Ö, Engström L (1967) Isolation of N-e-[32P]phosphoryl-lysine from rat-liver cell sap after incubation with [32P]adenosine triphosphate. Biochim Biophys Acta 141: 523-532.
  • Zoroddu M, Kowalik-Jankowska T, Kozłowski H, Molinari H, Salnikow K, Broday L, Costa M (2000) Interaction of Ni(II) and Cu(II) with a metal binding sequence of histone H4: AKRHRK, a model of the H4 tail. Biochem Biophys Acta 1475: 163-168.
  • Zu XL, Besant PG, Imhof A, Attwood PV (2007) Mass spectrometric analysis of protein histidine phosphorylation. Amino Acids 32: 347-357.
  • Zu XL, Besant PG, Attwood PV (2009) Protein histidine phosphorylation. Comprehensive Analytical Chemistry 52: 315-352.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.