Control of prokaryotic translational initiation by mRNA secondary structure

Publisher Summary This chapter describes the evidence that differences in the secondary structures of RNA are probably the main cause of this unpredictability. Although it has been known for many years that secondary structures of mRNA can interfere with translational initiation, it is quite surprising to find a simple, linear relationship between the efficiency of a ribosome binding site and the fraction of unfolded mRNA molecules. Presumably, a non-sequence-specific interaction of ribosomes with single-stranded RNA constitutes the first step in the process of initiation. The existence of such an interaction is supported by several lines of evidence. For example, the binding of ribosomes to synthetic polynucleotides like poly(U) must rely solely on nonspecific contacts, yet results in efficient polypeptide synthesis. Several sophisticated mechanisms of translational regulation that function through reversible changes in inhibitory secondary structures have been elucidated and are discussed in this chapter.

[1]  L. Gold,et al.  Maximizing Gene Expression , 1986 .

[2]  K. Imahori,et al.  Control of translation by the conformation of messenger RNA. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C. Squires,et al.  Translational coupling of the trpB and trpA genes in the Escherichia coli tryptophan operon , 1984, Journal of bacteriology.

[4]  H. Gassen,et al.  On the function of the ribosomal protein S1 in the elongation cycle of bacterial protein synthesis. , 1979, European journal of biochemistry.

[5]  B. Berkhout,et al.  Lysis gene of bacteriophage MS2 is activated by translation termination at the overlapping coat gene. , 1987, Journal of molecular biology.

[6]  J. Steitz,et al.  Two ribosome binding sites from the gene 0-3 messenger RNA of bacteriophages T7. , 1977, Journal of molecular biology.

[7]  J. Friesen,et al.  RNA secondary structure and translation inhibition: analysis of mutants in the rplJ leader. , 1984, The EMBO journal.

[8]  V. Pirrotta Operators and promoters in the OR region of phage 434. , 1979, Nucleic acids research.

[9]  D. Peabody,et al.  Termination-reinitiation occurs in the translation of mammalian cell mRNAs , 1986, Molecular and cellular biology.

[10]  S. Ao,et al.  A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. , 1988, Science.

[11]  D. Dubnau,et al.  Posttranscriptional regulation of an erythromycin resistance protein specified by plasmic pE194. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Jacobson,et al.  The complete nucleotide sequence of the group II RNA coliphage GA. , 1986, Journal of biochemistry.

[13]  M. D. Rosa Structure analysis of three T7 late mRNA ribosome binding sites. , 1981, Journal of molecular biology.

[14]  B. Berkhout,et al.  Opening the closed ribosome-binding site of the lysis cistron of bacteriophage MS2 , 1983, Nature.

[15]  N. Zinder,et al.  Cell Lysis: Another Function of the Coat Protein of the Bacteriophage f2 , 1968, Science.

[16]  E. Duvall,et al.  Chloramphenicol induction of cat-86 requires ribosome stalling at a specific site in the leader. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[17]  D. Dubnau,et al.  Cloning and analysis of ermG, a new macrolide-lincosamide-streptogramin B resistance element from Bacillus sphaericus , 1987, Journal of bacteriology.

[18]  M. Inouye,et al.  Gene structure of the OmpA protein, a major surface protein of Escherichia coli required for cell-cell interaction. , 1980, Journal of molecular biology.

[19]  E. Duvall,et al.  Analysis of the regulatory sequences needed for induction of the chloramphenicol acetyltransferase gene cat-86 by chloramphenicol and amicetin , 1986, Journal of bacteriology.

[20]  M Ptashne,et al.  Autoregulation and function of a repressor in bacteriophage lambda. , 1976, Science.

[21]  E. Murphy Nucleotide sequence of ermA, a macrolide-lincosamide-streptogramin B determinant in Staphylococcus aureus , 1985, Journal of bacteriology.

[22]  J. Tooze,et al.  Isolation and characterization of amber mutants of bacteriophage R17. , 1967, Journal of molecular biology.

[23]  S. Mongkolsuk,et al.  Constitutive variants of the pC194 cat gene exhibit DNA alterations in the vicinity of the ribosome binding site sequence. , 1984, Gene.

[24]  D. Dubnau,et al.  Evidence for the translational attenuation model: ribosome-binding studies and structural analysis with an in vitro run-off transcript of ermC. , 1985, Nucleic acids research.

[25]  J. van Duin,et al.  Expression of the rat interferon-alpha 1 gene in Escherichia coli controlled by the secondary structure of the translation-initiation region. , 1989, Gene.

[26]  W. Fiers,et al.  Nucleotide Sequence of the Gene Coding for the Bacteriophage MS2 Coat Protein , 1972, Nature.

[27]  M. Ivey-Hoyle,et al.  Translation of phage f1 gene VII occurs from an inherently defective initiation site made functional by coupling. , 1989, Journal of molecular biology.

[28]  M. Bolotin-Fukuhara,et al.  Mutational alterations of translational coupling in the L11 ribosomal protein operon of Escherichia coli , 1987, Journal of bacteriology.

[29]  Kees Van Der Laken,et al.  Polyuridylic acid‐dependent binding of fMet‐tRNA to Escherichia coli ribosomes and incorporation of formylmethionine into polyphenylalanine , 1979, FEBS letters.

[30]  K. Blumer,et al.  Translational control of phage f1 gene expression by differential activities of the gene V, VII, IX and VIII initiation sites. , 1987, Journal of molecular biology.

[31]  B. Berkhout,et al.  Translational interference at overlapping reading frames in prokaryotic messenger RNA. , 1985, Gene.

[32]  G. Stormo,et al.  The bacteriophage T4 regA gene: primary sequence of a translational repressor. , 1984, Nucleic acids research.

[33]  S. Horinouchi,et al.  A complex attenuator regulates inducible resistance to macrolides, lincosamides, and streptogramin type B antibiotics in Streptococcus sanguis , 1983, Journal of bacteriology.

[34]  H. Lodish Thermal melting of bacteriophage f2 RNA and initiation of synthesis of the maturation protein. , 1971, Journal of molecular biology.

[35]  L. Lindahl,et al.  Protein L4 of the E. coli ribosome regulates an eleven gene r protein operon , 1980, Cell.

[36]  M. C. Ganoza,et al.  Potential secondary structure at translation-initiation sites [published erratum appears in Nucleic Acids Res 1988 May 11;16(9): 4196] , 1987, Nucleic Acids Res..

[37]  J. van Duin,et al.  Basepairing potential of the 3' terminus of 16S RNA: dependence on the functional state of the 30S subunit and the presence of protein S21. , 1981, Nucleic acids research.

[38]  S. Arnott,et al.  The ribosome binding sites recognized by E. coli ribosomes have regions with signal character in both the leader and protein coding segments. , 1980, Nucleic acids research.

[39]  D. Williams,et al.  Chloramphenicol-inducible gene expression in Bacillus subtilis. , 1983, Gene.

[40]  L. Hardy,et al.  Mutations in an upstream regulatory sequence that increase expression of the bacteriophage T4 lysozyme gene , 1987, Journal of bacteriology.

[41]  G. Stormo,et al.  Translational regulation of expression of the bacteriophage T4 lysozyme gene. , 1986, Nucleic acids research.

[42]  M. Mayford,et al.  ermC leader peptide. Amino acid sequence critical for induction by translational attenuation. , 1989, Journal of molecular biology.

[43]  B. Weisblum,et al.  Translational attenuation control of ermSF, an inducible resistance determinant encoding rRNA N-methyltransferase from Streptomyces fradiae , 1988, Journal of bacteriology.

[44]  B. Berkhout,et al.  Mechanism of translational coupling between coat protein and replicase genes of RNA bacteriophage MS2. , 1985, Nucleic acids research.

[45]  B. Weisblum,et al.  Post-transcriptional Regulation of Chloramphenicol Acetyl Transferase , 1984, Journal of bacteriology.

[46]  F. Studier,et al.  Effect of RNAase III, cleavage on translation of bacteriophage T7 messenger RNAs. , 1975, Journal of molecular biology.

[47]  C. Richardson,et al.  Processing of mRNA by ribonuclease III regulates expression of gene 1.2 of bacteriophage T7 , 1981, Cell.

[48]  J. Steitz,et al.  Binding of mammalian ribosomes to ms2 phage rna reveals an overlapping gene encoding a lysis function , 1979, Cell.

[49]  E. Duvall,et al.  Chloramphenicol induces translation of the mRNA for a chloramphenicol-resistance gene in Bacillus subtilis. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Konings,et al.  Oligonucleotide-directed mutagenesis of gene IX of bacteriophage M13. , 1982, Nucleic acids research.

[51]  D. Dubnau Induction of ermC requires translation of the leader peptide. , 1985, The EMBO journal.

[52]  S. Altuvia,et al.  RNase III stimulates the translation of the cIII gene of bacteriophage lambda. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[53]  T. Faure,et al.  The influence of mRNA primary and secondary structure on human IFN-γ gene expression in E. coli , 1984 .

[54]  G. Stormo,et al.  CUUCGG hairpins: extraordinarily stable RNA secondary structures associated with various biochemical processes. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[55]  W. Reznikoff,et al.  Molecular cloning and sequence analysis of trp-lac fusion deletions. , 1984, Journal of molecular biology.

[56]  H. Lodish,et al.  Secondary structure of bacteriophage f2 ribonucleic acid and the initiation of in vitro protein biosynthesis. , 1970, Journal of molecular biology.

[57]  L. J. Perry,et al.  Non-toxic expression in Escherichia coli of a plasmid-encoded gene for phage T4 lysozyme. , 1985, Gene.

[58]  S. Horinouchi,et al.  Posttranscriptional modification of mRNA conformation: mechanism that regulates erythromycin-induced resistance. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[59]  M. Mayford,et al.  Messenger RNA from Staphylococcus aureus that specifies macrolide-lincosamide-streptogramin resistance. Demonstration of its conformations and of the leader peptide it encodes. , 1985, Journal of molecular biology.

[60]  C. Smith,et al.  Nucleotide sequence analysis of Tn4551: use of ermFS operon fusions to detect promoter activity in Bacteroides fragilis , 1987, Journal of bacteriology.

[61]  E. Kawashima,et al.  Optimizing the expression in E. coli of a synthetic gene encoding somatomedin-C (IGF-I). , 1985, Nucleic acids research.

[62]  C. Yanofsky,et al.  A ribosome binding site sequence is necessary for efficient expression of the distal gene of a translationally-coupled gene pair. , 1984, Nucleic acids research.

[63]  L. Freedman,et al.  Autogenous control of the S10 ribosomal protein operon of Escherichia coli: genetic dissection of transcriptional and posttranscriptional regulation. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[64]  K. Cone,et al.  Functional analysis of lac repressor restart sites in translational initiation and reinitiation. , 1985, Journal of molecular biology.

[65]  F. Studier,et al.  Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. , 1983, Journal of molecular biology.

[66]  M. Nomura,et al.  E. coli ribosomal protein L4 is a feedback regulatory protein , 1980, Cell.

[67]  C. Yanofsky,et al.  Translational coupling during expression of the tryptophan operon of Escherichia coli. , 1980, Genetics.

[68]  P. Shen,et al.  Secondary structure of the leader transcript from the Escherichia coli S10 ribosomal protein operon. , 1988, Nucleic acids research.

[69]  C. Merril,et al.  Escherichia coli gal operon proteins made after prophage lambda induction , 1981, Journal of bacteriology.

[70]  R. E. Webster,et al.  Characterization of Op3, a lysis-defective mutant of bacteriophage f2 , 1979, Cell.

[71]  Michael N. Hall,et al.  A role for mRNA secondary structure in the control of translation initiation , 1982, Nature.

[72]  B. Berkhout,et al.  Effect of the sequences upstream from the ribosome-binding site on the yield of protein from the cloned gene for phage MS2 coat protein. , 1983, Gene.

[73]  D. Schümperli,et al.  Translational coupling at an intercistronic boundary of the Escherichia coli galactose operon , 1982, Cell.

[74]  R. Brückner,et al.  Regulation of the inducible chloramphenicol acetyltransferase gene of the Staphylococcus aureus plasmid pUB112. , 1985, The EMBO journal.

[75]  T. Blumenthal,et al.  Overlapping genes in rna phage: a new protein implicated in lysis , 1979, Cell.

[76]  B. Berkhout,et al.  Determination of the RNA secondary structure that regulates lysis gene expression in bacteriophage MS2. , 1987, Journal of molecular biology.

[77]  D. Dubnau,et al.  Sequence and properties of pIM13, a macrolide-lincosamide-streptogramin B resistance plasmid from Bacillus subtilis , 1986, Journal of Bacteriology.

[78]  K. Cone,et al.  Messenger RNA conformation and ribosome selection of translational reinitiation sites in the lac repressor mRNA. , 1985, Journal of molecular biology.

[79]  M. Rosenberg,et al.  Differential translation efficiency explains discoordinate expression of the galactose operon , 1981, Cell.

[80]  D. Turner,et al.  Improved free-energy parameters for predictions of RNA duplex stability. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[81]  D. Peabody,et al.  Effect of upstream reading frames on translation efficiency in simian virus 40 recombinants , 1986, Molecular and cellular biology.

[82]  D. Dubnau,et al.  Conformational alteration of mRNA structure and the posttranscriptional regulation of erythromycin-induced drug resistance. , 1980, Nucleic acids research.