Chemical Approaches to Studying Labile Amino Acid Phosphorylation

Alan M. Marmelstein1, Javier Moreno1, Dorothea Fiedler1
1Leibniz-Institut für Molekulare Pharmakologie, Robert-Rössle-Straße 10, 13125, Berlin, Germany

Tóm tắt

Từ khóa


Tài liệu tham khảo

Hunter T (2012) Why nature chose phosphate to modify proteins. Philos Trans R Soc B Biol Sci 367:2513–2516

Zhang J, Yang PL, Gray NS (2009) Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 9:28–39

Freschi L, Osseni M, Landry CR (2014) Functional divergence and evolutionary turnover in mammalian phosphoproteomes. PLoS Genet 10:e1004062

Bhandari R, Saiardi A, Ahmadibeni Y, Snowman AM, Resnick AC, Kristiansen TZ, Molina H, Pandey A, Werner JK, Juluri KR, Xu Y, Prestwich GD, Parang K, Snyder SH (2007) Protein pyrophosphorylation by inositol pyrophosphates is a posttranslational event. Proc Natl Acad Sci USA 104:15305–15310

Azevedo C, Livermore T, Saiardi A (2015) Protein polyphosphorylation of lysine residues by inorganic polyphosphate. Mol Cell 58:71–82

Attwood PV, Piggott MJ, Zu XL, Besant PG (2007) Focus on phosphohistidine. Amino Acids 32:145–156

Besant PG, Attwood PV, Piggott MJ (2009) Focus on phosphorarginine and phospholysine. Curr Protein Pept Sci 10:536–550

Attwood PV, Besant PG, Piggott MJ (2011) Focus on phosphoaspartate and phosphoglutamate. Amino Acids 40:1035–1051

Boyer PD, DeLuca M, Ebner KE, Hultquist DE, Peter JB (1962) Identification of phosphohistidine digests from a probable intermediate of qxidative phosphorylation. J Biol Chem 237:PC3306–PC3308

Perry J, Koteva K, Wright G (2011) Receptor domains of two-component signal transduction systems. Mol BioSyst 7:1388–1398

Khorchid A, Ikura M (2006) Bacterial histidine kinase as signal sensor and transducer. Int J Biochem Cell Biol 38:307–312

Neiditch MB, Federle MJ, Miller ST, Bassler BL, Hughson FM (2005) Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 18:507–518

Mayville P, Ji G, Beavis R, Yang H, Goger M, Novick RP, Muir TW (1999) Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc Natl Acad Sci USA 96:1218–1223

Koteva K, Hong H-J, Wang XD, Nazi I, Hughes D, Naldrett MJ, Buttner MJ, Wright GD (2010) A vancomycin photoprobe identifies the histidine kinase VanSsc as a vancomycin receptor. Nat Chem Biol 6:327–329

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

Kee JM, Villani B, Carpenter LR, Muir TW (2010) Development of stable phosphohistidine analogues. J Am Chem Soc 132:14327–14329

Kee JM, Muir TW (2012) Chasing phosphohistidine, an elusive sibling in the phosphoamino acid family. ACS Chem Biol 7:44–51

Morera S, Chiadmi M, LeBras G, Lascu I, Janin J (1995) Mechanism of phosphate transfer by nucleoside diphosphate kinase: X-ray structures of the phosphohistidine intermediate of the enzymes from Drosophila and Dictyostelium. Biochemistry 34:11062–11070

Bond CS, White MF, Hunter WN (2001) High resolution structure of the phosphohistidine-activated form of Escherichia coli cofactor-dependent phosphoglycerate mutase. J Biol Chem 276:3247–3253

Hultquist DE (1968) The preparation and characterization of phosphorylated derivatives of histidine. Biochim Biophys Acta Bioenerg 153:329–340

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

Lloyd GJ, Cooperman BS (1971) Nucleophilic attack by zinc (II)-pyridine-2-carbaldoxine anion on phosphorylimidazole. A model for enzymatic phosphate transfer. J Am Chem Soc 93:4883–4889

Hohenester UM, Ludwig K, König S (2013) Chemical phosphorylation of histidine residues in proteins using potassium phosphoramidate—a tool for the analysis of acid-labile phos- phorylation. Curr Drug Deliv 10:58–63

Medzihradszky KF, Phillipps NJ, Senderowicz L, Wang P, Turck CW (1997) Synthesis and characterization of histidine-phosphorylated peptides. Protein Sci 6:1405–1411

Attwood PV, Ludwig K, Bergander K, Besant PG, Adina-Zada A, Krieglstein J, Klumpp S (2010) Chemical phosphorylation of histidine-containing peptides based on the sequence of histone H4 and their dephosphorylation by protein histidine phosphatase. Biochim Biophys Acta Proteins Proteomics 1804:199–205

Gustafson C, Wagner-Jauregg T (1954) Phosphorimidazole and phosphohistidine. Fed Proc 13:222

Rosenberg TH (1964) A simple preparation method for diphosphoimidazole. Arch Biochem Biophys 105:315–318

Muller T, Rathlev T, Rosenberg T (1956) Special cases of non-enzymic transphosphorylation. Biochim Biophys Acta 19:563–564

Wagner-Jauregg T, Hackley BE (1953) Model reactions of phosphorus-containing enzyme inactivators. III. Interaction of imidazole, pyridine, and some of their derivatives with dialkyl halogeno-phosphates. J Am Chem Soc 75:2125–2130

Hultquist DE, Moyer RW, Boyer PD (1966) The preparation and characterization of 1-phosphohistidine and 3-phosphohistidine. Biochemistry 5:322–331

Wei Y-F, Matthews HR (1991) Identification of phosphohistidine in proteins and purification of protein-histidine kinases. Methods Enzymol 200:388–414

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

Kee J-M, Oslund RC, Perlman DH, Muir TW (2013) A pan-specific antibody for direct detection of protein histidine phosphorylation. Nat Chem Biol 9:416–421

Oslund RC, Kee JM, Couvillon AD, Bhatia VN, Perlman DH, Muir TW (2014) A phosphohistidine proteomics strategy based on elucidation of a unique gas-phase phosphopeptide fragmentation mechanism. J Am Chem Soc 136:12899–12911

Schenkels C, Erni B, Reymond J-L (1999) Phosphofurylalanine, a stable analog of phosphohistidine. Bioorganic Med Chem Lett 9:1443–1446

McAllister TE, Webb ME (2012) Triazole phosphohistidine analogues compatible with the Fmoc-strategy. Org Biomol Chem 10:4043–4049

Kee JM, Oslund RC, Couvillon AD, Muir TW (2015) A second-generation phosphohistidine analog for production of phosphohistidine antibodies. Org Lett 17:187–189

Lilley MB, Mambwe B, Thompson MJ, Jackson RFW, Muimo R (2015) 4-Phosphopyrazol-2-yl alanine: a non-hydrolysable analogue of phosphohistidine. Chem Commun 51:7305–7308

Fuhs SR, Meisenhelder J, Aslanian A, Ma L, Zagorska A, Stankova M, Binnie A, Al-Obeidi F, Mauger J, Lemke G, Yates JR, Hunter T (2015) Monoclonal 1- and 3-phosphohistidine antibodies: new tools to study histidine phosphorylation. Cell 162:198–210

Ennor AH, Morrison JF (1958) Biochemstry of the phosphagens and related guanidines. Physiol Rev 36:631–674

Cieśla J, Fraczyk T, Rode W (2011) Phosphorylation of basic amino acid residues in proteins: important but easily missed. Acta Biochim Pol 58:137–148

Fuhrmann J, Clancy KW, Thompson PR (2015) Chemical biology of protein arginine modifications in epigenetic regulation. Chem Rev 115:5413–5461

Fuhrmann J, Schmidt A, Spiess S, Lehner A, Turgay K, Mechtler K, Charpentier E, Clausen T (2009) McsB is a protein arginine kinase that phosphorylates and inhibits the heat-shock regulator CtsR. Science 324:1323–1327

Elsholz AKW, Turgay K, Michalik S, Hessling B, Gronau K, Oertel D, Mader U, Bernhardt J, Becher D, Hecker M, Gerth U (2012) Global impact of protein arginine phosphorylation on the physiology of Bacillus subtilis. Proc Natl Acad Sci USA 109:7451–7456

Schmidt A, Trentini DB, Spiess S, Fuhrmann J, Ammerer G, Mechtler K, Clausen T (2014) Quantitative phosphoproteomics reveals the role of protein arginine phosphorylation in the bacterial stress response. Mol Cell Proteomics 13:537–550

Mijakovic I, Grangeasse C, Turgay K (2016) Exploring the diversity of protein modifications: special bacterial phosphorylation systems. FEMS Microbiol Rev 40:398–417

Wozniak DJ, Tiwari KB, Soufan R, Jayaswal RK (2012) The mcsB gene of the clpC operon is required for stress tolerance and virulence in Staphylococcus aureus. Microbiology 158:2568–2576

Trentini DB, Suskiewicz MJ, Heuck A, Kurzbauer R, Deszcz L, Mechtler K, Clausen T (2016) Arginine phosphorylation marks proteins for degradation by a Clp protease. Nature 539:48–53

Fujitaki JM, Smith RA (1984) Techniques in the detection and characterization of phosphoramidate-containing proteins. Methods Enzymol 107:23–36

Ellington WR (2001) Evolution and physiological roles of phosphagen systems. Annu Rev Physiol 63:289–325

Trentini DB, Fuhrmann J, Mechtler K, Clausen T (2014) Chasing phosphoarginine proteins: development of a selective enrichment method using a phosphatase trap. Mol Cell Proteomics mcp.O113.035790

Schmidt A, Ammerer G, Mechtler K (2013) Studying the fragmentation behavior of peptides with arginine phosphorylation and its influence on phospho-site localization. Proteomics 13:945–954

Marcus F, Morrison JF (1964) The preparation of phosphoarginine: a comparative study. Biochem J 92:429–435

Cramer F, Scheiffele E, Vollmar A (1962) Die synthese der argininphosphorsäure und die reaktion von isoureidophosphonaten mit aminen. Chem Ber 95:1670–1682

Kumon A, Yokoi F, Hiraishi H (1996) N-phosphoarginine phosphatase (17 kDa) and alkaline phosphatase as protein arginine phosphatases. J Biochem 119:719–724

Hofmann FT, Lindemann C, Salia H, Adamitzki P, Karanicolas J, Seebeck FP (2011) A phosphoarginine containing peptide as an artificial SH2 ligand. Chem Commun (Camb) 47:10335–10337

Fuhrmann J, Mierzwa B, Trentini DB, Spiess S, Lehner A, Charpentier E, Clausen T (2013) Structural basis for recognizing phosphoarginine and evolving residue-specific protein phosphatases in Gram-positive bacteria. Cell Rep 3:1832–1839

Fuhrmann J, Subramanian V, Thompson PR (2015) Synthesis and use of a phosphonate amidine to generate an anti-phosphoarginine-specific antibody. Angew Chemie Int Ed 54:14715–14718

Ouyang H, Fu C, Fu S, Ji Z, Sun Y, Deng P, Zhao Y (2016) Development of a stable phosphoarginine analog for producing phosphoarginine antibodies. Org Biomol Chem 14:1925–1929

Zetterqvist Ö, Engström L (1967) Isolation of N-ε-[32P]phosphoryl-lysine from rat-liver cell sap after incubation with [32P] adenosine triphosphate. Biochem Biophisycal Acta 141:523–532

Wålinder O (1968) Identification of a phosphate-incorporating protein from bovine liver as nucleoside identification of a phosphate-incorporating protein from bovine liver as nucleoside diphosphate kinase and isolation of and N-e-32-P-phospholysine from erythrocytic nucleo. J Biol Chem 243:3947–3952

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

Smith DL, Bruegger BB, Halpern RM, Smith RA (1973) New histone kinases in nuclei of rat tissues. Nature 246:103–104

Postel EH, Abramczyk BM, Levit MN, Kyin S (2000) Catalysis of DNA cleavage and nucleoside triphosphate synthesis by NM23-H2/NDP kinase share an active site that implies a DNA repair function. Proc Natl Acad Sci USA 97:14194–14199

Ohmori H, Kuba M, Kumon A (1994) 3-Phosphohistidine/6-phospholysine phosphatase from rat brain as. J Biochem 116:380–385

Benkovic SJ, Sampson EJ (1971) Structure-reactivity correlation for the hydrolysis of phosphoramidate monoanions. J Am Chem Soc 93:4009–4016

Modro TA (1981) Phosphoric and carboxylic amides. ACS Symp Ser 171:619–622

Denehy E, White JM, Williams SJ (2007) Electronic structure of the sulfonyl and phosphonyl groups: a computational and crystallographic study. Inorg Chem 46:8871–8886

Bertran-Vicente J, Serwa RA, Schümann M, Schmieder P, Krause E, Hackenberger CPR (2014) Site-specifically phosphorylated lysine peptides. J Am Chem Soc 136:13622–13628

Fujitaki JM, Steiner AW, Nichols SE, Helander ER, Lin YC, Smith RA (1980) A simple preparation of N-phosphorylated lysine and arginine. Prep Biochem 10:205–213

Bertran-Vicente J, Schumann M, Schmieder P, Krause E, Hackenberger CPR (2015) Direct access to site-specifically phosphorylated-lysine peptides from a solid-support. Org Biomol Chem 13:6839–6843

Pas HH, Robillard GT (1988) S-Phosphocysteine and phosphohistidine are intermediates in the phosphoenolpyruvate-dependent mannitol transport catalyzed by Escherichia coli EIImtl. Biochemistry 27:5835–5839

Cho H, Krishnaraj R, Kitas E, Bannwarth W, Walsh CT, Anderson KS (1992) Isolation and structural elucidation of a novel phosphocysteine intermediate in the LAR protein tyrosine phosphatase enzymic pathway. J Am Chem Soc 114:7296–7298

Brandão TAS, Hengge AC, Johnson SJ (2010) Insights into the reaction of protein-tyrosine phosphatase 1B: crystal structures for transition state analogs of both catalytic steps. J Biol Chem 285:15874–15883

Asthagiri D, Liu T, Noodleman L, Van Etten RL, Bashford D (2004) On the role of the conserved aspartate in the hydrolysis of the phosphocysteine intermediate of the low molecular weight tyrosine phosphatase. J Am Chem Soc 126:12677–12684. doi: 10.1021/JA048638O

Pas HH, Meyer GH, Kruizinga WH, Tamminga KS, van Weeghel RP, Robillard GT (1991) 31phospho-NMR demonstration of phosphocysteine as a catalytic intermediate on the Escherichia coli phosphotransferase system EIIMtl. J Biol Chem 266:6690–6692

Meins M, Jenö P, Müller D, Richter WJ, Rosenbusch JP, Erni B (1993) Cysteine phosphorylation of the glucose transporter of Escherichia coli. J Biol Chem 268:11604–11609

Sun F, Ding Y, Ji Q, Liang Z, Deng X, Wong CCL, Yi C, Zhang L, Xie S, Alvarez S, Hicks LM, Luo C, Jiang H, Lan L, He C (2012) Protein cysteine phosphorylation of SarA/MgrA family transcriptional regulators mediates bacterial virulence and antibiotic resistance. Proc Natl Acad Sci USA 109:15461–15466

Buchowiecka AK (2014) Puzzling over protein cysteine phosphorylation—assessment of proteomic tools for S-phosphorylation profiling. Analyst 139:4118–4123

Chalker JM, Lercher L, Rose NR, Schofield CJ, Davis BG (2012) Conversion of cysteine into dehydroalanine enables access to synthetic histones bearing diverse post-translational modifications. Angew Chemie Int Ed 51:1835–1839

Chooi KP, Galan SRG, Raj R, McCullagh JSO, Mohammed S, Jones LH, Davis BG (2014) Synthetic phosphorylation of p38# recapitulates protein kinase activity. J Am Chem Soc 136:1698–1701

Rowan FC, Richards M, Bibby RA, Thompson A, Bayliss R, Blagg J (2013) Insights into aurora-a kinase activation using unnatural amino acids incorporated by chemical modification. ACS Chem Biol 8:2184–2191

Åkerfeldt S, Willman N-E, Berggren B, Thomelius H, Westin G (1960) Cysteamine S-phosphoric acid. Acta Chem Scand 14:1980–1984

Åkerfeldt S, Hasselquist H, Prange I, Dam H, Sjöberg B, Toft J (1961) Further studies on S-substituted phosphorothioic acids. Mixed lithiumsodium salts of S-(1-carboxyethyl) phosphorothioic acid and S-(2-carboxyethyl) phosphorothioic acid. Acta Chem Scand 15:575–582

Åkerfeldt S, Weidler A-M, Mandell L, Kvande PC, Meisingseth E (1963) Further studies on S-substituted phosphorothioic acids. III. Rates of hydrolysis and dissociation constants. Acta Chem Scand 17:319–328

Swaney DL, McAlister GC, Wirtala M, Schwartz JC, Syka JEP, Coon JJ (2007) Supplemental activation method for high-efficiency electron-transfer dissociation of doubly protonated peptide precursors. Anal Chem 79:477–485

Bertran-Vicente J, Penkert M, Nieto-Garcia O, Jeckelmann J-M, Schmieder P, Krause E, Hackenberger CPR (2016) Chemoselective synthesis and analysis of naturally occurring phosphorylated cysteine peptides. Nat Commun 7:12703

Ruman T, Długopolska K, Jurkiewicz A, Rut D, Fraczyk 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

Bernardes GJL, Chalker JM, Errey JC, Davis BG (2008) Facile conversion of cysteine and alkyl cysteines to dehydroalanine on protein surfaces: versatile and switchable access to functionalized proteins. J Am Chem Soc 130:5052–5053

Chalker JM, Gunnoo SB, Boutureira O, Gerstberger SC, Fernández-González M, Bernardes GJL, Griffin L, Hailu H, Schofield CJ, Davis BG (2011) Methods for converting cysteine to dehydroalanine on peptides and proteins. Chem Sci 2:1666

Chen Z, Cole PA (2015) Synthetic approaches to protein phosphorylation. Curr Opin Chem Biol 28:115–122

Ridder IS, Dijkstra BW (1999) Identification of the Mg2+-binding site in the P-type ATPase and phosphatase members of the HAD (haloacid dehalogenase) superfamily by structural similarity to the response regulator protein CheY. Biochem J 339:223–226

Allen KN, Dunaway-Mariano D (2004) Phosphoryl group transfer: evolution of a catalytic scaffold. Trends Biochem Sci 29:495–503

Lee SY, Cho HS, Pelton JG, Yan D, Henderson RK, King DS, Huang L, Kustu S, Berry EA, Wemmer DE (2001) Crystal structure of an activated response regulator bound to its target. Nat Struct Biol 8:52–56

Lee SY, Cho HS, Pelton JG, Yan D, Berry EA, Wemmer DE (2001) Crystal structure of activated CheY. Comparison with other activated receiver domains. J Biol Chem 276:16425–16431

Zhao R, Collins EJ, Bourret RB, Silversmith RE (2002) Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat Struct Biol 9:570–575

Ibrahim IM, Puthiyaveetil S, Allen JF (2016) A two-component regulatory system in transcriptional control of photosystem stoichiometry: redox-dependent and sodium ion-dependent phosphoryl transfer from cyanobacterial histidine kinase Hik2 to response regulators Rre1 and RppA. Front Plant Sci 7:137

Trumbore MW, Wang RH, Enkemann SA, Berger SL (1997) Prothymosin alpha in vivo contains phosphorylated glutamic acid residues. J Biol Chem 272:26394–26404

Wang RH, Tao L, Trumbore MW, Berger SL (1997) Turnover of the acyl phosphates of human and murine prothymosin alpha in vivo. J Biol Chem 272:26405–26412

Tao L, Wang RH, Enkemann SA, Trumbore MW, Berger SL (1999) Metabolic regulation of protein-bound glutamyl phosphates: insights into the function of prothymosin alpha. J Cell Physiol 178:154–163

Koshland DE (1952) Effect of catalysts on the hydrolysis of acetyl phosphate. nucleophilic displacement mechanisms in enzymatic reactions. J Am Chem Soc 74:2286–2292

Purich DL (2002) Use of sodium borohydride to detect acyl-phosphate linkages in enzyme reactions. Methods Enzymol 354:168–177

Andersson J, Barth A (2006) FTIR studies on the bond properties of the aspartyl phosphate moiety of the Ca2+-ATPase. Biopolymers 82:353–357

Schlemmer H, Sontheimer GM, Kalbitzer HR (1988) 31P nuclear magnetic resonance spectroscopy of the phosphorylated tetrapeptide Gly–Gly–Asp–Ala. Magn Reson Chem 26:260–263

Platzer G, Okon M, McIntosh LP (2014) pH-dependent random coil 1H, 13C, and 15 N chemical shifts of the ionizable amino acids: a guide for protein pKa measurements. J Biomol NMR 60:109–129

Black S, Wright NG (1953) Enzymatic reduction of β-aspartylphosphate to homoserine. J Am Chem Soc 75:5766

Wright G, Black S, Wright NG (1955) b-Aspartokinase and b-aspartyl phosphate. J Biol Chem 213:27–38

Katchalsky A, Paecht M (1954) Phosphate anhydrides of amino acids. J Am Chem Soc 76:6042–6044

Saxl RL, Anand GS, Stock AM (2001) Synthesis and biochemical characterization of a phosphorylated analogue of the response regulator CheB. Biochemistry 40:12896–12903

Stewart RC (1993) Activating and inhibitory mutations in the regulatory domain of CheB, the methylesterase in bacterial chemotaxis. J Biol Chem 268:1921–1930

Berlicki Ł (2008) Inhibitors of glutamine synthetase and their potential application in medicine. Mini Rev Med Chem 8:869–878

Colquhoun A, Newsholme E (1997) Aspects of glutamine metabolism in human tumour cells. IUBMB Life 41:583–596

Saiardi A, Bhandari R, Resnick AC, Snowman AM, Snyder SH (2004) Phosphorylation of proteins by inositol pyrophosphates. Science 306:2101–2105

Chakraborty A, Koldobskiy MA, Bello NT, Maxwell M, Potter JJ, Juluri KR, Maag D, Kim S, Huang AS, Dailey MJ, Saleh M, Snowman AM, Moran TH, Mezey E, Snyder SH (2010) Inositol pyrophosphates inhibit akt signaling, thereby regulating insulin sensitivity and weight gain. Cell 143:897–910

Thota SG, Unnikannan CP, Thampatty SR, Manorama R, Bhandari R (2015) Inositol pyrophosphates regulate RNA polymerase I-mediated rRNA transcription in Saccharomyces cerevisiae. Biochem J 466:105–114

Voglmaier SM, Bembenek ME, Kaplin AI, Dormán G, Olszewski JD, Prestwich GD, Snyder SH (1996) Purified inositol hexakisphosphate kinase is an ATP synthase: diphosphoinositol pentakisphosphate as a high-energy phosphate donor. Proc Natl Acad Sci USA 93:4305–4310

Brown NW, Marmelstein AM, Fiedler D (2016) Chemical tools for interrogating inositol pyrophosphate structure and function. Chem Soc Rev 45:6311–6326

Shears SB (2015) Inositol pyrophosphates: why so many phosphates? Adv Biol Regul 57:203–216

Marmelstein AM, Yates LM, Conway JH, Fiedler D (2014) Chemical pyrophosphorylation of functionally diverse peptides. J Am Chem Soc 136:108–111

Yates LM, Fiedler D (2015) Establishing the stability and reversibility of protein pyrophosphorylation with synthetic peptides. ChemBioChem 16:415–423

Conway JH, Fiedler D (2015) An affinity reagent for the recognition of pyrophosphorylated peptides. Angew Chemie Int Ed 54:3941–3945

Williams FJ, Fiedler D (2015) A fluorescent sensor and gel stain for detection of pyrophosphorylated proteins. ACS Chem Biol 10:1958–1963

Yates LM, Fiedler D (2016) A stable pyrophosphoserine analog for incorporation into peptides and proteins. ACS Chem Biol 11:1066–1073

Kornberg A, Rao NN, Ault-riché D (1999) Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68:89–125

Gray MJ, Wholey WY, Wagner NO, Cremers CM, Mueller-Schickert A, Hock NT, Krieger AG, Smith EM, Bender RA, Bardwell JCA, Jakob U (2014) Polyphosphate is a primordial chaperone. Mol Cell 53:689–699

Holmström KM, Marina N, Baev AY, Wood NW, Gourine AV, Abramov AY (2013) Signalling properties of inorganic polyphosphate in the mammalian brain. Nat Commun 4:1362

Cremers CM, Knoefler D, Gates S, Galvan V, Southworth DR, Jakob U, Cremers CM, Knoefler D, Gates S, Martin N, Dahl J, Lempart J, Xie L, Chapman MR, Galvan V, Southworth DR, Jakob U (2016) Polyphosphate: a conserved modifier of amyloidogenic processes. Mol Cell 63:1–13

Wild R, Gerasimaite R, Jung J-Y, Truffault V, Pavlovic I, Schmidt A, Saiardi A, Jessen HJ, Poirier Y, Hothorn M, Mayer A (2016) Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science 352:986–990