Mechanism of adenylate kinase: site-directed mutagenesis versus X-ray and NMR.

Controversy is an integral part of scientific research and is often a precursor to the truth. However, this lesson has been learned in a very hard way in the case of the structure-function relationship of adenylate kinase (AK), which catalyzes the interconversion between MgATP+AMP and MgADP+ADP. While this small kinase has been considered a model kinase and the enzyme-substrate interaction of AK was among the first investigated by X-ray crystallography and NMR the substrate binding sites deduced from the early studies by these two powerful techniques (termed the X-ray model and the NMR model, respectively) were dramatically different. Ironically, both models have had substantial impact on researchers in related fields. The problems have finally been dealt with since 1987 by the interplay between site-directed mutagenesis, X-ray, and NMR. The purpose of this review is not only to summarize the current knowledge in the structure-function relationship of adenylate kinase but also to accurately document and critically analyze historical developments in the hope that history will not be repeated.

[1]  G. Schulz,et al.  Induced-fit movements in adenylate kinases. , 1990, Faraday discussions.

[2]  M. Tsai,et al.  Mechanism of adenylate kinase. 10. Reversing phosphorus stereospecificity by site-directed mutagenesis , 1991 .

[3]  M. Tsai,et al.  Mechanism of adenylate kinase. Demonstration of a functional relationship between aspartate 93 and Mg2+ by site-directed mutagenesis and proton, phosphorus-31, and magnesium-25 NMR. , 1991, Biochemistry.

[4]  M. Konrad,et al.  Complexes of yeast adenylate kinase and nucleotides investigated by proton NMR , 1991 .

[5]  A. Wittinghofer,et al.  Identification of valine/leucine/isoleucine and threonine/alanine/glycine proton-spin systems of Escherichia coli adenylate kinase by selective deuteration and selective protonation. , 1991, The Biochemical journal.

[6]  G. Phillips,et al.  Assignment of the nucleotide binding sites and the mechanism of substrate inhibition of Escherichia coli adenylate kinase , 1991, Proteins.

[7]  T. Yoneya,et al.  The role of Leu-190 in the function and stability of adenylate kinase. , 1990, The Journal of biological chemistry.

[8]  M. Tsai,et al.  Mechanism of adenylate kinase. Critical evaluation of the X-ray model and assignment of the AMP site. , 1990, Biochemistry.

[9]  P. R. Sibbald,et al.  The P-loop--a common motif in ATP- and GTP-binding proteins. , 1990, Trends in biochemical sciences.

[10]  O. Bârzu,et al.  The binding of ATP and AMP to Escherichia coli adenylate kinase investigated by 1H and 15N NMR spectroscopy. , 1990, Biochemical and biophysical research communications.

[11]  P. Schimmel.  Hazards and their exploitation in the applications of molecular biology to structure-function relationships. , 1990, Biochemistry.

[12]  K. Diederichs,et al.  Three-dimensional structure of the complex between the mitochondrial matrix adenylate kinase and its substrate AMP. , 1990, Biochemistry.

[13]  I. Schlichting,et al.  Structurally and catalytically important residues in the phosphate binding loop of adenylate kinase of Escherichia coli. , 1990, Biochemistry.

[14]  J. Reinstein,et al.  Complexes of Escherichia coli adenylate kinase and nucleotides: 1H NMR studies of the nucleotide sites in solution. , 1990, Biochemistry.

[15]  I R Vetter,et al.  Fluorescence and NMR investigations on the ligand binding properties of adenylate kinases. , 1990, Biochemistry.

[16]  M. Tsai,et al.  Mechanism of adenylate kinase. Structural and functional demonstration of arginine-138 as a key catalytic residue that cannot be replaced by lysine. , 1990, Biochemistry.

[17]  M. Tsai,et al.  Mechanism of adenylate kinase. Are the essential lysines essential? , 1990, Biochemistry.

[18]  H. J. Kim,et al.  In vitro mutagenesis studies at the arginine residues of adenylate kinase. A revised binding site for AMP in the X-ray-deduced model. , 1990, Biochemistry.

[19]  G. Schulz,et al.  Three-dimensional structure of the complex of guanylate kinase from yeast with its substrate GMP. , 1990, Journal of molecular biology.

[20]  C. Pace,et al.  Conformational stability of globular proteins. , 1990, Trends in biochemical sciences.

[21]  M. Yamada,et al.  Isolation and characterization of the gene encoding bovine adenylate kinase isozyme 2. , 1990, Gene.

[22]  M. Yamada,et al.  Cloning and characterization of cDNA for mitochondrial GTP:AMP phosphotransferase of bovine liver. , 1989, The Journal of biological chemistry.

[23]  C. Sanders,et al.  Mechanism of adenylate kinase. Is there a relationship between local substrate dynamics, local binding energy, and the catalytic mechanism? , 1989, Biochemistry.

[24]  W. Kabsch,et al.  Structure of the guanine-nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation , 1989, Nature.

[25]  P. Schimmel.  Hazards of deducing enzyme structure-activity relationships on the basis of chemical applications of molecular biology , 1989 .

[26]  M. Yamada,et al.  Human adenylate kinase deficiency associated with hemolytic anemia. A single base substitution affecting solubility and catalytic activity of the cytosolic adenylate kinase. , 1989, Journal of Biological Chemistry.

[27]  R. Goody,et al.  Nucleotide and AP5A complexes of porcine adenylate kinase: A 1H and 19F NMR study. , 1989, Biochemistry.

[28]  H. Mantsch,et al.  Structural and catalytic role of arginine 88 in Escherichia coli adenylate kinase as evidenced by chemical modification and site-directed mutagenesis. , 1989, The Journal of biological chemistry.

[29]  J. H. Wang,et al.  8-Azido-2'-O-dansyl-ATP. A fluorescent photoaffinity reagent for ATP-binding proteins and its application to adenylate kinase. , 1989, The Journal of biological chemistry.

[30]  E. Pai,et al.  Adenylate kinases from thermosensitive Escherichia coli strains. , 1989, Journal of molecular biology.

[31]  T. Noumi,et al.  Site-directed mutagenesis of Pro-17 located in the glycine-rich region of adenylate kinase. , 1989, The Journal of biological chemistry.

[32]  G. Schulz,et al.  The switch between two conformations of adenylate kinase. , 1988, Journal of molecular biology.

[33]  G. Schulz,et al.  Structure of the complex of adenylate kinase from Escherichia coli with the inhibitor P1,P5-di(adenosine-5'-)pentaphosphate. , 1988, Journal of molecular biology.

[34]  S. Zimmermann,et al.  Two-dimensional NMR studies of the porcine muscle adenylate kinase. , 1988, Biochemistry.

[35]  C. Sanders,et al.  Mechanism of adenylate kinase. Histidine-36 is not directly involved in catalysis, but protects cysteine-25 and stabilizes the tertiary structure. , 1988, Biochemistry.

[36]  T. Hunter,et al.  The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. , 1988, Science.

[37]  J. Reinstein,et al.  Mutations in the nucleotide binding loop of adenylate kinase of Escherichia coli. , 1988, Biochemistry.

[38]  J. Reinstein,et al.  Proton-nuclear magnetic resonance studies of the aromatic spin systems of Escherichia coli adenylate kinase. , 1988, Journal of molecular biology.

[39]  P. Karplus,et al.  Refined structure of porcine cytosolic adenylate kinase at 2.1 A resolution. , 1988, Journal of molecular biology.

[40]  A. Mildvan,et al.  Solution structure of the 45-residue MgATP-binding peptide of adenylate kinase as examined by 2-D NMR, FTIR, and CD spectroscopy. , 1986, Biochemistry.

[41]  Caldwell Jw,et al.  Investigation of the substrate binding and phosphate transfer in adenylate kinase by molecular mechanics. , 1988 .

[42]  M. Tsai,et al.  Mechanism of adenylate kinase. Does adenosine 5'-triphosphate bind to the adenosine 5'-monophosphate site? , 1987, Biochemistry.

[43]  J. Gerlt,et al.  Site-directed mutants of staphylococcal nuclease. Detection and localization by 1H NMR spectroscopy of conformational changes accompanying substitutions for glutamic acid-43. , 1987, Biochemistry.

[44]  G. Schulz,et al.  The cDNA sequence encoding cytosolic adenylate kinase from baker's yeast (Saccharomyces cerevisiae). , 1987, Nucleic acids research.

[45]  M. Tagaya,et al.  Affinity labeling of adenylate kinase with adenosine diphosphopyridoxal. Presence of Lys21 in the ATP-binding site. , 1987, The Journal of biological chemistry.

[46]  G. Schulz,et al.  Structure of the complex of yeast adenylate kinase with the inhibitor P1,P5-di(adenosine-5'-)pentaphosphate at 2.6 A resolution. , 1987, Journal of molecular biology.

[47]  F. Kishi,et al.  High level expression of chicken muscle adenylate kinase in Escherichia coli. , 1987, Journal of biochemistry.

[48]  A. Mildvan,et al.  NMR studies of the AMP-binding site and mechanism of adenylate kinase. , 1986, Biochemistry.

[49]  G. Schulz.  Structural and functional relationships in the adenylate kinase family. , 1987, Cold Spring Harbor symposia on quantitative biology.

[50]  G. Schulz,et al.  The glycine‐rich loop of adenylate kinase forms a giant anion hole , 1986, FEBS letters.

[51]  G. Schulz,et al.  Structural relationships in the adenylate kinase family. , 1986, European journal of biochemistry.

[52]  A. Gilles,et al.  Substitution of a serine residue for proline-87 reduces catalytic activity and increases susceptibility to proteolysis of Escherichia coli adenylate kinase. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[53]  F. Kishi,et al.  Isolation and characterization of cDNA for chicken muscle adenylate kinase. , 1986, The Journal of biological chemistry.

[54]  A. Tomasselli,et al.  The complete amino acid sequence of adenylate kinase from baker's yeast. , 1986, European journal of biochemistry.

[55]  C. Pace.  Determination and analysis of urea and guanidine hydrochloride denaturation curves. , 1986, Methods in enzymology.

[56]  F. Wittinghofer,et al.  Cloning and sequencing of the adenylate kinase gene (adk) of Escherichia coli. , 1985, Nucleic acids research.

[57]  A. Mildvan,et al.  NMR studies of the MgATP binding site of adenylate kinase and of a 45-residue peptide fragment of the enzyme. , 1985, Biochemistry.

[58]  M. Hermodson,et al.  Inactivation of muscle adenylate kinase by site-specific destruction of tyrosine 95 using potassium ferrate. , 1985, The Journal of biological chemistry.

[59]  H. Kalbitzer,et al.  Structural investigations of the Mg.ATP complex at the active site of porcine adenylate kinase using phosphorothioate analogs and electron paramagnetic resonance of Mn(II) with chiral 17O-labelled ATP analogs. , 1983, European journal of biochemistry.

[60]  A. Tomasselli,et al.  Baker's Yeast Adenlate Kinase , 1983 .

[61]  A. Mildvan,et al.  Nuclear magnetic resonance studies of the nucleotide binding sites of porcine adenylate kinase. , 1982, Biochemistry.

[62]  F. Raushel,et al.  Substrate synergism and the kinetic mechanism of yeast hexokinase. , 1982, Biochemistry.

[63]  M. Hamada,et al.  Studies of adenosine triphosphate transphosphorylases. XIV. Equilibrium binding properties of the crystalline rabbit and calf muscle ATP--AMP transphosphorylase (adenylate kinase) and derived peptide fragments. , 1979, Archives of biochemistry and biophysics.

[64]  M. Dixon-Woods,et al.  Enzymes. 3rd ed , 1979 .

[65]  A. Mildvan.  The role of metals in enzyme-catalyzed substitutions at each of the phosphorus atoms of ATP. , 1979, Advances in enzymology and related areas of molecular biology.

[66]  M. Hamada,et al.  Studies on adenosine triphosphate transphosphorylases. XIII. Kinetic properties of the crystalline rabbit muscle ATP-AMP transphorphorylase (adenylate kinase) and a comparison with the crystalline calf muscle and liver adenylate kinases. , 1978, Archives of biochemistry and biophysics.

[67]  M. Cohn,et al.  Differentiation of nucleotide binding sites and role of metal ion in the adenylate kinase reaction by 31P NMR. Equilibria, interconversion rates, and NMR parameters of bound substrates. , 1978, The Journal of biological chemistry.

[68]  G. Schulz,et al.  Two conformations of crystalline adenylate kinase. , 1977, Journal of molecular biology.

[69]  G. Schulz,et al.  Substrate positions and induced-fit in crystalline adenylate kinase. , 1977, Journal of molecular biology.

[70]  P. Frey,et al.  Enzymatic and 32P nuclear magnetic resonance study of adenylate kinase-catalyzed stereospecific phosphorylation of adenosine 5'-phosphorothioate. , 1977, The Journal of biological chemistry.

[71]  R. Goody,et al.  Synthesis and properties of diastereoisomers of adenosine 5'-(O-1-thiotriphosphate) and adenosine 5'-(O-2-thiotriphosphate). , 1976, Biochemistry.

[72]  M. Cohn,et al.  Proton magnetic resonance spectra or porcine muscle adenylate kinase and substrate complexes. , 1975, The Journal of biological chemistry.

[73]  G. Schulz,et al.  Three-dimensional structure of adenyl kinase , 1974, Nature.

[74]  I. von Zabern,et al.  The amino-acid sequence of sarcine adenylate kinase from skeletal muscle. , 1974, European journal of biochemistry.

[75]  Arnold Weissberger,et al.  Investigation of Rates and Mechanisms of Reactions , 1974 .

[76]  K Biedermann,et al.  Low resolution structure of adenylate kinase. , 1973, Journal of molecular biology.

[77]  A. Sols,et al.  Induced fit in yeast hexokinase. , 1970, European journal of biochemistry.

[78]  D G Rhoads,et al.  Initial velocity and equilibrium kinetics of myokinase. , 1968, The Journal of biological chemistry.

[79]  Joseph Needham,et al.  PERSPECTIVES IN BIOCHEMISTRY , 1940 .

[80]  C. K. Drinker,et al.  Perspectives in Biochemistry , 1938, The Yale Journal of Biology and Medicine.