Structure, mechanism, and evolution of the mRNA capping apparatus.

Publisher Summary This chapter discusses the recent progress, concerning the mechanism of cap synthesis, by fungal and mammalian enzymes. Viral capping enzymes are discussed to the extent that their study illuminates the mechanistic features, shared by their cellular counterparts. The chapter discusses the structural features of the capping enzymes that are required for guanylyltransferase, triphosphatase, and methyltransferase activities. It also describes how these features are conserved in evolution. The essential structural elements illuminate the reaction mechanisms that are described briefly in this chapter. It emphasizes the importance of recent structure determinations in clarifying the mechanistic models of catalysis, opening new lines of biochemical investigation, and illuminating the surprising structural complexities for seemingly “simple” enzymatic steps. The chapter concludes with the following: (i) the cloning of genes and complementary DNA (cDNA) encoding the cap-forming enzymes from a wide variety of sources; (ii) the delineation of functional domains and catalytically essential amino acid side chains by mutagenesis; and (iii) the application of X-ray crystallography to determine the structure of the capping enzymes. The physical and functional organizations of the component activities diverged during evolution are also discussed in this chapter.

[1]  S. Buratowski,et al.  Conditional mutants of the yeast mRNA capping enzyme show that the cap enhances, but is not required for, mRNA splicing. , 1996, RNA.

[2]  S. Shuman,et al.  Structure-function analysis of the triphosphatase component of vaccinia virus mRNA capping enzyme , 1997, Journal of virology.

[3]  S. Shuman,et al.  RNA capping enzyme and DNA ligase: a superfamily of covalent nucleotidyl transferases , 1995, Molecular microbiology.

[4]  S. Shuman,et al.  Mutational analysis of mRNA capping enzyme identifies amino acids involved in GTP binding, enzyme-guanylate formation, and GMP transfer to RNA , 1995, Molecular and cellular biology.

[5]  C. Ho,et al.  Mutational analysis of Escherichia coli DNA ligase identifies amino acids required for nick-ligation in vitro and for in vivo complementation of the growth of yeast cells deleted for CDC9 and LIG4. , 1999, Nucleic acids research.

[6]  S. Nagata,et al.  mRNA capping enzyme. Isolation and characterization of the gene encoding mRNA guanylytransferase subunit from Saccharomyces cerevisiae. , 1992, The Journal of biological chemistry.

[7]  D. Bentley,et al.  5'-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. , 1997, Genes & development.

[8]  A. Shatkin,et al.  Mammalian capping enzyme binds RNA and uses protein tyrosine phosphatase mechanism. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Dixon,et al.  A protein phosphatase related to the vaccinia virus VH1 is encoded in the genomes of several orthopoxviruses and a baculovirus. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[10]  F. Quiocho,et al.  Specific protein recognition of an mRNA cap through its alkylated base , 1997, Nature Structural Biology.

[11]  S. Shuman,et al.  Characterization of Human, Schizosaccharomyces pombe, and Candida albicans mRNA Cap Methyltransferases and Complete Replacement of the Yeast Capping Apparatus by Mammalian Enzymes* , 1999, The Journal of Biological Chemistry.

[12]  C. Ho,et al.  Genetic, Physical, and Functional Interactions between the Triphosphatase and Guanylyltransferase Components of the Yeast mRNA Capping Apparatus , 1998, Molecular and Cellular Biology.

[13]  S. Shuman,et al.  Conditional inactivation of mRNA capping enzyme affects yeast pre-mRNA splicing in vivo. , 1996, RNA.

[14]  S. Shuman,et al.  Covalent catalysis in nucleotidyl transfer. A KTDG motif essential for enzyme-GMP complex formation by mRNA capping enzyme is conserved at the active sites of RNA and DNA ligases. , 1993, The Journal of biological chemistry.

[15]  Stewart Shuman,et al.  X-Ray Crystallography Reveals a Large Conformational Change during Guanyl Transfer by mRNA Capping Enzymes , 1997, Cell.

[16]  D. Bentley,et al.  The Guanylyltransferase Domain of Mammalian mRNA Capping Enzyme Binds to the Phosphorylated Carboxyl-terminal Domain of RNA Polymerase II* , 1998, The Journal of Biological Chemistry.

[17]  Jack E. Dixon,et al.  Crystal Structure of the Dual Specificity Protein Phosphatase VHR , 1996, Science.

[18]  C. Ho,et al.  Mutational Analyses of Yeast RNA Triphosphatases Highlight a Common Mechanism of Metal-dependent NTP Hydrolysis and a Means of Targeting Enzymes to Pre-mRNAs in Vivo by Fusion to the Guanylyltransferase Component of the Capping Apparatus* , 1999, The Journal of Biological Chemistry.

[19]  C. Ho,et al.  Phylogeny of mRNA capping enzymes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Myette,et al.  Domain Structure of the Vaccinia Virus mRNA Capping Enzyme , 1996, The Journal of Biological Chemistry.

[21]  R. Possee,et al.  The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. , 1994, Virology.

[22]  E. Cho,et al.  mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. , 1997, Genes & development.

[23]  D. Wigley,et al.  Functional domains of an NAD+-dependent DNA ligase. , 1999 .

[24]  S. Shuman.  Origins of mRNA identity: capping enzymes bind to the phosphorylated C-terminal domain of RNA polymerase II. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[25]  E. G. Niles,et al.  Identification of the vaccinia virus mRNA guanyltransferase active site lysine. , 1993, The Journal of biological chemistry.

[26]  S. Buratowski,et al.  An RNA 5′-Triphosphatase Related to the Protein Tyrosine Phosphatases , 1997, Cell.

[27]  E. Cho,et al.  Allosteric interactions between capping enzyme subunits and the RNA polymerase II carboxy-terminal domain. , 1998, Genes & development.

[28]  S. Buratowski,et al.  Human PIR1 of the Protein-tyrosine Phosphatase Superfamily Has RNA 5′-Triphosphatase and Diphosphatase Activities* , 1999, The Journal of Biological Chemistry.

[29]  A. Shatkin,et al.  Recombinant Human mRNA Cap Methyltransferase Binds Capping Enzyme/RNA Polymerase IIo Complexes* , 1998, The Journal of Biological Chemistry.

[30]  K. Mizumoto,et al.  Cloning and characterization of three human cDNAs encoding mRNA (guanine-7-)-methyltransferase, an mRNA cap methylase. , 1998, Biochemical and biophysical research communications.

[31]  P. Frey,et al.  Standard Free Energy for the Hydrolysis of Adenylylated T4 DNA Ligase and the Apparent pK a of Lysine 159* , 1999, The Journal of Biological Chemistry.

[32]  M. Arisawa,et al.  Isolation and characterization of the Candida albicans gene for mRNA 5′‐triphosphatase: association of mRNA 5′‐triphosphatase and mRNA 5′‐guanylyltransferase activities is essential for the function of mRNA 5′‐capping enzyme in vivo 1 , 1998, FEBS letters.

[33]  S. Shuman,et al.  Mutational analysis of yeast mRNA capping enzyme. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Shuman,et al.  Accelerated mRNA decay in conditional mutants of yeast mRNA capping enzyme. , 1998, Nucleic acids research.

[35]  J. Hurwitz,et al.  Mechanism of mRNA capping by vaccinia virus guanylyltransferase: characterization of an enzyme--guanylate intermediate. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Shuman,et al.  Vaccinia virus mRNA (guanine-7-)methyltransferase: mutational effects on cap methylation and AdoHcy-dependent photo-cross-linking of the cap to the methyl acceptor site. , 1996, Biochemistry.

[37]  H. Charbonneau,et al.  The baculovirus Autographa californica encodes a protein tyrosine phosphatase. , 1993, The Journal of biological chemistry.

[38]  C. Ho,et al.  Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. , 1999, Molecular cell.

[39]  S. Shuman,et al.  Mutational analysis of Chlorella virus DNA ligase: catalytic roles of domain I and motif VI. , 1998, Nucleic acids research.

[40]  S. Shuman,et al.  Structure-Function Analysis of the mRNA Cap Methyltransferase of Saccharomyces cerevisiae * , 1997, The Journal of Biological Chemistry.

[41]  F A Quiocho,et al.  mRNA cap recognition: dominant role of enhanced stacking interactions between methylated bases and protein aromatic side chains. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. Doherty.  Conversion of a DNA ligase into an RNA capping enzyme. , 1999, Nucleic acids research.

[43]  C. Ho,et al.  Yeast and Viral RNA 5′ Triphosphatases Comprise a New Nucleoside Triphosphatase Family* , 1998, The Journal of Biological Chemistry.

[44]  P. Nordlund,et al.  The crystal structure of a low-molecular-weight phosphotyrosine protein phosphatase , 1994, Nature.

[45]  F A Quiocho,et al.  Structural basis for sequence-nonspecific recognition of 5'-capped mRNA by a cap-modifying enzyme. , 1998, Molecular cell.

[46]  S. Shuman,et al.  Mutational analysis of the Saccharomyces cerevisiae ABD1 gene: cap methyltransferase activity is essential for cell growth , 1996, Molecular and cellular biology.

[47]  D. Wigley,et al.  Crystal Structure of an ATP-Dependent DNA Ligase from Bacteriophage T7 , 1996, Cell.

[48]  S. Shuman,et al.  Mutational analysis of vaccinia DNA ligase defines residues essential for covalent catalysis. , 1995, Virology.

[49]  S. Shuman,et al.  Chlorella virus DNA ligase: nick recognition and mutational analysis. , 1998, Nucleic acids research.

[50]  S. Shuman,et al.  RNA 5′-Triphosphatase, Nucleoside Triphosphatase, and Guanylyltransferase Activities of Baculovirus LEF-4 Protein , 1998, Journal of Virology.

[51]  C. Ho,et al.  A Conserved Domain of Yeast RNA Triphosphatase Flanking the Catalytic Core Regulates Self-association and Interaction with the Guanylyltransferase Component of the mRNA Capping Apparatus* , 1999, The Journal of Biological Chemistry.

[52]  E. Cho,et al.  A Saccharomyces cerevisiae RNA 5'-triphosphatase related to mRNA capping enzyme. , 1999, Nucleic acids research.

[53]  S. Shuman,et al.  Mutational analysis of the RNA triphosphatase component of vaccinia virus mRNA capping enzyme , 1996, Journal of virology.

[54]  S. Buratowski,et al.  A protein tyrosine phosphatase-like protein from baculovirus has RNA 5'-triphosphatase and diphosphatase activities. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  D. Wigley,et al.  Functional domains of an ATP-dependent DNA ligase. , 1999, Journal of molecular biology.

[56]  W. Dong,et al.  Guanylyltransferase Activity of the LEF-4 Subunit of Baculovirus RNA Polymerase , 1998, Journal of Virology.

[57]  S. Telford,et al.  REFERENCES CONTENT ALERTS , 1998 .

[58]  D. Wigley,et al.  Structure of a complex between a cap analogue and mRNA guanylyl transferase demonstrates the structural chemistry of RNA capping. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[59]  S. Shuman.  Capping enzyme in eukaryotic mRNA synthesis. , 1995, Progress in nucleic acid research and molecular biology.

[60]  S. Shuman,et al.  Yeast mRNA cap methyltransferase is a 50-kilodalton protein encoded by an essential gene , 1995, Molecular and cellular biology.

[61]  D. Barford,et al.  Structural basis for phosphotyrosine peptide recognition by protein tyrosine phosphatase 1B. , 1995, Science.

[62]  Da-ming Li,et al.  PIR1, a Novel Phosphatase That Exhibits High Affinity to RNA·Ribonucleoprotein Complexes* , 1998, The Journal of Biological Chemistry.

[63]  S. Clarke,et al.  S-Adenosylmethionine-dependent Methylation in Saccharomyces cerevisiae , 1999, The Journal of Biological Chemistry.

[64]  Y. Kaziro,et al.  Messenger RNA guanylyltransferase from Saccharomyces cerevisiae. Large scale purification, subunit functions, and subcellular localization. , 1987, The Journal of biological chemistry.

[65]  J. V. Van Etten,et al.  Expression and characterization of an RNA capping enzyme encoded by Chlorella virus PBCV-1 , 1996, Journal of virology.

[66]  S. Buratowski,et al.  Active site of the mRNA-capping enzyme guanylyltransferase from Saccharomyces cerevisiae: similarity to the nucleotidyl attachment motif of DNA and RNA ligases. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[67]  C. Ho,et al.  An essential surface motif (WAQKW) of yeast RNA triphosphatase mediates formation of the mRNA capping enzyme complex with RNA guanylyltransferase. , 1999, Nucleic acids research.

[68]  B. Moss,et al.  Modification of the 5' terminus of mRNA by an RNA (guanine-7-)-methyltransferase from HeLa cells. , 1976, The Journal of biological chemistry.

[69]  D. Barford,et al.  Crystal structure of human protein tyrosine phosphatase 1B. , 1994, Science.

[70]  A. Tomkinson,et al.  Location of the active site for enzyme-adenylate formation in DNA ligases. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[71]  A. Tomkinson,et al.  Mammalian DNA ligase II is highly homologous with vaccinia DNA ligase. Identification of the DNA ligase II active site for enzyme-adenylate formation. , 1994, The Journal of biological chemistry.

[72]  K. Mizumoto,et al.  Localization and in vitro mutagenesis of the active site in the Saccharomyces cerevisiae mRNA capping enzyme. , 1995, Journal of biochemistry.

[73]  E. Fauman,et al.  The X-ray Crystal Structures of Yersinia Tyrosine Phosphatase with Bound Tungstate and Nitrate , 1996, The Journal of Biological Chemistry.

[74]  Y. Li,et al.  Properties of a baculovirus mutant defective in the protein phosphatase gene , 1995, Journal of virology.

[75]  Stewart Shuman,et al.  Structure and Mechanism of Yeast RNA Triphosphatase An Essential Component of the mRNA Capping Apparatus , 1999, Cell.

[76]  H. Yamada-Okabe,et al.  Isolation and characterization of a human cDNA for mRNA 5'-capping enzyme. , 1998, Nucleic acids research.

[77]  J. Myette,et al.  Characterization of the vaccinia virus RNA 5'-triphosphatase and nucleotide triphosphate phosphohydrolase activities. Demonstrate that both activities are carried out at the same active site. , 1996, The Journal of biological chemistry.

[78]  J. Dixon,et al.  Visualization of intermediate and transition-state structures in protein-tyrosine phosphatase catalysis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[79]  R. Kagan,et al.  Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. , 1994, Archives of biochemistry and biophysics.

[80]  O. Shimmi,et al.  Isolation of the mRNA-capping enzyme and ferric-reductase-related genes from Candida albicans. , 1996, Microbiology.

[81]  K. Mizumoto,et al.  Cloning and characterization of two human cDNAs encoding the mRNA capping enzyme. , 1998, Biochemical and biophysical research communications.

[82]  J. V. Van Etten,et al.  Viruses and viruslike particles of eukaryotic algae , 1991, Microbiological reviews.

[83]  S. Imajoh-ohmi,et al.  Isolation and characterization of the yeast mRNA capping enzyme beta subunit gene encoding RNA 5'-triphosphatase, which is essential for cell viability. , 1997, Biochemical and biophysical research communications.

[84]  E. Fauman,et al.  Crystal structure of Yersinia protein tyrosine phosphatase at 2.5 Å and the complex with tungstate , 1994, Nature.

[85]  A. Gingras,et al.  Cocrystal Structure of the Messenger RNA 5′ Cap-Binding Protein (eIF4E) Bound to 7-methyl-GDP , 1997, Cell.

[86]  S. Shuman,et al.  Characterization of a Baculovirus-Encoded RNA 5′-Triphosphatase , 1998, Journal of Virology.