Aminotransferases: demonstration of homology and division into evolutionary subgroups.

A total of 150 amino acid sequences of vitamin B6-dependent enzymes are known to date, the largest contingent being furnished by the aminotransferases with 51 sequences of 14 different enzymes. All aminotransferase sequences were aligned by using algorithms for sequence comparison, hydropathy patterns and secondary structure predictions. The aminotransferases could be divided into four subgroups on the basis of their mutual structural relatedness. Subgroup I comprises aspartate, alanine, tyrosine, histidinol-phosphate, and phenylalanine aminotransferases; subgroup II acetylornithine, ornithine, omega-amino acid, 4-aminobutyrate and diaminopelargonate aminotransferases; subgroup III D-alanine and branched-chain amino acid aminotransferases, and subgroup IV serine and phosphoserine aminotransferases. (N-1) Profile analysis, a more stringent application of profile analysis [Gribskov, M., McLachlan, A. D. and Eisenberg, D. (1987) Proc. Natl Acad. Sci. USA 84, 4355-4358], established the homology among the enzymes of each subgroup as well as among all subgroups except subgroup III. However, similarity of active-site segments and the hydropathy patterns around invariant residues suggest that subgroup III, though most distantly related, might also be homologous with the other aminotransferases. On the basis of the comprehensive alignment, a new numbering of amino acid residues applicable to aminotransferases (AT) in general is proposed. In the multiply aligned sequences, only four out of a total of about 400 amino acid residues proved invariant in all 51 sequences, i.e. Gly(314AT)197, Asp/Glu(340AT)222, Lys(385AT)258 and Arg(562AT)386, the number not in parentheses corresponding to the structure of porcine cytosolic aspartate aminotransferase. Apparently, the aminotransferases constitute a group of homologous proteins which diverged into subgroups and, with some exceptions, into substrate-specific individual enzymes already in the universal ancestor cell.

[1]  J. Kirsch,et al.  The tyrosine-225 to phenylalanine mutation of Escherichia coli aspartate aminotransferase results in an alkaline transition in the spectrophotometric and kinetic pKa values and reduced values of both kcat and Km. , 1991, Biochemistry.

[2]  R. Barouki,et al.  Properties of human liver cytosolic aspartate aminotransferase mRNAs generated by alternative polyadenylation site selection. , 1990, Biochemistry.

[3]  P. Christen,et al.  Evolutionary relationships among aminotransferases , 1989 .

[4]  M. O. Dayhoff,et al.  Atlas of protein sequence and structure , 1965 .

[5]  Y. Suzuki,et al.  Nucleotide sequence of the cDNA encoding the precursor for mitochondrial serine:pyruvate aminotransferase of rat liver. , 1987, European journal of biochemistry.

[6]  H. Kagamiyama,et al.  Complete amino acid sequence of mitochondrial aspartate aminotransferase from pig heart muscle. Peptide ordering procedures and the complete sequence. , 1980, The Journal of biological chemistry.

[7]  S. Primrose,et al.  The cloning and sequence analysis of the aspC and tyrB genes from Escherichia coli K12. Comparison of the primary structures of the aspartate aminotransferase and aromatic aminotransferase of E. coli with those of the pig aspartate aminotransferase isoenzymes. , 1986, The Biochemical journal.

[8]  F. B. Armstrong,et al.  Amino acid sequence of Salmonella typhimurium branched-chain amino acid aminotransferase. , 1989, Biochemistry.

[9]  F. Bossa,et al.  Primary structure of mitochondrial aspartate aminotransferase from turkey liver , 1979, FEBS letters.

[10]  W. Doolittle,et al.  Characterization of a gene involved in histidine biosynthesis in Halobacterium (Haloferax) volcanii: isolation and rapid mapping by transformation of an auxotroph with cosmid DNA , 1990, Journal of bacteriology.

[11]  G. Petsko,et al.  Activity and structure of the active-site mutants R386Y and R386F of Escherichia coli aspartate aminotransferase. , 1991, Biochemistry.

[12]  N. Glansdorff,et al.  Escherichia coli and Saccharomyces cerevisiae acetylornithine aminotransferases : evolutionary relationship with ornithine aminotransferases , 1990 .

[13]  H. Kagamiyama,et al.  Substitution of a lysyl residue for arginine 386 of Escherichia coli aspartate aminotransferase. , 1989, The Journal of biological chemistry.

[14]  P. Y. Chou,et al.  Prediction of protein conformation. , 1974, Biochemistry.

[15]  N. Watanabe,et al.  Crystal Structure Analysis of ω-Amino Acid: Pyruvate Aminotransferase with a Newly Developed Weissenberg Camera and an Imaging Plate Using Synchrotron Radiation , 1989 .

[16]  A. D. McLachlan,et al.  Profile analysis: detection of distantly related proteins. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Coggins,et al.  The serC-aro A operon of Escherichia coli. A mixed function operon encoding enzymes from two different amino acid biosynthetic pathways. , 1986, The Biochemical journal.

[18]  S. V. Shlyapnikov,et al.  Primary structure of cytoplasmic aspartate aminotransferase from chicken heart and its homology with pig heart isoenzymes , 1979, FEBS letters.

[19]  C. Bruni,et al.  Cloning and characterization of histidine biosynthetic gene cluster of Streptomyces coelicolor A3(2). , 1990, Gene.

[20]  P. Christen,et al.  The covalent structure of mitochondrial aspartate aminotransferase from chicken. Identification of segments of the polypeptide chain invariant specifically in the mitochondrial isoenzyme. , 1983, The Journal of biological chemistry.

[21]  P. O'Gaora,et al.  Cloning and characterisation of the serC and aroA genes of Yersinia enterocolitica, and construction of an aroA mutant. , 1989, Gene.

[22]  R. Pictet,et al.  Complete complementary DNA of rat tyrosine aminotransferase messenger RNA. Deduction of the primary structure of the enzyme. , 1985, Journal of molecular biology.

[23]  K. Titani,et al.  Complete amino acid sequence of rat liver cytosolic alanine aminotransferase. , 1991, Biochemistry.

[24]  C. Bruni,et al.  Cloning, structure, and expression of the Escherichia coli K-12 hisC gene , 1985, Journal of bacteriology.

[25]  A. D. McLachlan,et al.  Secondary structure‐based profiles: Use of structure‐conserving scoring tables in searching protein sequence databases for structural similarities , 1991, Proteins.

[26]  T. Watanabe,et al.  The complete amino acid sequence of mitochondrial glutamic oxaloacetic transaminase from rat liver. , 1981, Journal of Biochemistry (Tokyo).

[27]  C. Mcphalen,et al.  X-ray structure refinement and comparison of three forms of mitochondrial aspartate aminotransferase. , 1993, Journal of molecular biology.

[28]  K. Titani,et al.  Complete amino acid sequence of human liver cytosolic alanine aminotransferase (GPT) determined by a combination of conventional and mass spectral methods. , 1991, Biochemistry.

[29]  C. Thaller,et al.  The open/closed conformational equilibrium of aspartate aminotransferase. Studies in the crystalline state and with a fluorescent probe in solution. , 1991, European journal of biochemistry.

[30]  H. Esumi,et al.  Human peroxisomal L-alanine: glyoxylate aminotransferase. Evolutionary loss of a mitochondrial targeting signal by point mutation of the initiation codon. , 1990, The Biochemical journal.

[31]  H. Dunathan.  Conformation and reaction specificity in pyridoxal phosphate enzymes. , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Rettenmeier,et al.  Isolation and characterization of the human tyrosine aminotransferase gene , 1990, Nucleic Acids Res..

[33]  H. Kagamiyama,et al.  Branched-chain amino acid aminotransferase of Escherichia coli: nucleotide sequence of the ilvE gene and the deduced amino acid sequence. , 1985, Journal of biochemistry.

[34]  A. Okamoto,et al.  Tyr225 in aspartate aminotransferase: contribution of the hydrogen bond between Tyr225 and coenzyme to the catalytic reaction. , 1991, Journal of biochemistry.

[35]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[36]  B. Maras,et al.  The amino acid sequence of the aspartate aminotransferase from baker's yeast (Saccharomyces cerevisiae). , 1991, The Biochemical journal.

[37]  H. Kagamiyama,et al.  Role of Asp222 in the catalytic mechanism of Escherichia coli aspartate aminotransferase: the amino acid residue which enhances the function of the enzyme-bound coenzyme pyridoxal 5'-phosphate. , 1992, Biochemistry.

[38]  T. Tanaka,et al.  Rat cytosolic aspartate aminotransferase: molecular cloning of cDNA and expression in Escherichia coli. , 1988, Journal of biochemistry.

[39]  A. Das,et al.  Rapid sequencing of cloned DNA using a transposon for bidirectional priming: sequence of the Escherichia coli K-12 avtA gene. , 1987, Nucleic acids research.

[40]  M. Gribskov,et al.  [9] Profile analysis , 1990 .

[41]  H. Pitot,et al.  Sequence of the precursor to rat ornithine aminotransferase deduced from a cDNA clone. , 1985, The Journal of biological chemistry.

[42]  J. Jauniaux,et al.  Nucleotide sequence of the yeast UGA1 gene encoding GABA transaminase. , 1990, Nucleic Acids Research.

[43]  P. Christen,et al.  Homology of pyridoxal-5'-phosphate-dependent aminotransferases with the cobC (cobalamin synthesis), nifS (nitrogen fixation), pabC (p-aminobenzoate synthesis) and malY (abolishing endogenous induction of the maltose system) gene products. , 1993, European journal of biochemistry.

[44]  G. Degols.  Functional analysis of the regulatory region adjacent to the cargB gene of Saccharomyces cerevisiae. Nucleotide sequence, gene fusion experiments and cis-dominant regulatory mutation analysis. , 1987, European journal of biochemistry.

[45]  Y. Ovchinnikov,et al.  The complete amino acid sequence of cytoplasmic aspartate aminotransferase from pig heart , 1973, FEBS letters.

[46]  A. Schulz,et al.  Molecular analysis of two genes of the Escherichia coli gab cluster: nucleotide sequence of the glutamate:succinic semialdehyde transaminase gene (gabT) and characterization of the succinic semialdehyde dehydrogenase gene (gabD) , 1990, Journal of bacteriology.

[47]  J. Kirsch,et al.  Site-directed mutagenesis of aspartate aminotransferase from E. coli. , 1985, Biochemical and biophysical research communications.

[48]  P. Alifano,et al.  Structure and function of the Salmonella typhimurium and Escherichia coli K-12 histidine operons. , 1988, Journal of molecular biology.

[49]  S. Pascarella,et al.  The primary structure of mitochondrial aspartate aminotransferase from human heart. , 1985, Biochimica et biophysica acta.

[50]  S. B. Needleman,et al.  A general method applicable to the search for similarities in the amino acid sequence of two proteins. , 1970, Journal of molecular biology.

[51]  E. Milgrom,et al.  A novel progesterone-induced messenger RNA in rabbit and human endometria. Cloning and sequence analysis of the complementary DNA. , 1987, Biochemistry.

[52]  J. Nagle,et al.  Molecular cloning of human ornithine aminotransferase mRNA. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[53]  P. Christen,et al.  Mitochondrial and cytosolic aspartate aminotransferase from chicken: activity toward aromatic amino acids. , 1978, Biochemical and biophysical research communications.

[54]  P. Christen,et al.  Mutant aspartate aminotransferase (K258H) without pyridoxal-5'-phosphate-binding lysine residue. Structural and catalytic properties. , 1993, European journal of biochemistry.

[55]  R. Doolittle,et al.  A simple method for displaying the hydropathic character of a protein. , 1982, Journal of molecular biology.

[56]  J. Jansonius,et al.  The Three-Dimensional Structure of Phosphoserine Aminotransferase from Escherichia coli , 1991 .

[57]  H. Kagamiyama,et al.  Asp222, His143, and Tyr70 in Escherichia coli Aspartate Aminotransferase , 1991 .

[58]  M. Cubellis,et al.  Cloning and sequencing of the gene coding for aspartate aminotransferase from the thermoacidophilic archaebacterium Sulfolobus solfataricus. , 1989, European journal of biochemistry.

[59]  A. Okamoto,et al.  Thermostable aspartate aminotransferase from a thermophilic Bacillus species. Gene cloning, sequence determination, and preliminary x-ray characterization. , 1991, The Journal of biological chemistry.

[60]  R. Sokal,et al.  Principles of numerical taxonomy , 1965 .

[61]  P. Christen,et al.  Aspartate aminotransferase with the pyridoxal-5'-phosphate-binding lysine residue replaced by histidine retains partial catalytic competence. , 1990, European journal of biochemistry.

[62]  G. Eichele,et al.  Mechanism of action of aspartate aminotransferase proposed on the basis of its spatial structure. , 1984, Journal of molecular biology.

[63]  D. Henner,et al.  The organization and nucleotide sequence of the Bacillus subtilis hisH, tyrA and aroE genes. , 1986, Gene.

[64]  J. Ruppert,et al.  The Escherichia coli biotin biosynthetic enzyme sequences predicted from the nucleotide sequence of the bio operon. , 1988, The Journal of biological chemistry.

[65]  H. Kagamiyama,et al.  Aspartate aminotransferase of Escherichia coli: nucleotide sequence of the aspC gene. , 1985, Journal of biochemistry.

[66]  Y. Morino,et al.  Cloning and sequence analysis of mRNA for mouse aspartate aminotransferase isoenzymes. , 1986, The Journal of biological chemistry.

[67]  H. Kagamiyama,et al.  The primary structure of thermostable D-amino acid aminotransferase from a thermophilic Bacillus species and its correlation with L-amino acid aminotransferases. , 1989, The Journal of biological chemistry.

[68]  H. Griffin.  Nucleotide sequence of the Salmonella serC gene. , 1990, Nucleic acids research.

[69]  Y. Lemoine,et al.  Cloning and characterization of the Bacillus sphaericus genes controlling the bioconversion of pimelate into dethiobiotin. , 1990, Gene.