The making of a phage

As a consequence of the structural work on DNA, the concerted investigations on the T even phages and the in vitro work on DNA polymerase, the replication of DNA-containing viruses was understood in outline by the end of the fifties. However, at this time virtually nothing was known about the propagation of RNA viruses, mainly because biochemical work on plant and animal viruses entailed considerable technical difficulties. The discovery of the RNA-containing coliphage f2 in Manhattan sewage by Loeb and Zinder in 1960 [l] presaged rapid advances in the field and-great interest among virologists. Excursions were undertaken to sewers of citjqs throughout the world, bringing to light numerous further isolates of RNA phages fcan in Canberra, R17 in Philadelphia, Ml2 in Munich, Q@ in Kyoto, MS2 in Berkeley, to mention but a few. These phages proved to be ideal objects for biochemical investigations. Not only do they multiply rapidly, providing impatient experimenters with fast (if not always clear) results, but they also subvert almost half of their host’s metabolism to their own needs, which greatly aids the biochemical analysis of the phage-specific processes. Last but not least, RNA phages can be grown and purified by the tens of grams, providing adequate amounts of material for structural and functional analyses. All phages isolated in the USA and in Europe are closely related, belonging to serological group I. They show only slight immunological differences, which can be related to a few amino acid substitutions in the coat protein. The Japanese phages QP and VK belong to the serological group III, which shows no cross-reactivity with group I [2-41. The structure of

[1]  H. Lodish,et al.  Mutants of the bacteriophage f2. 8. Control mechanisms for phage-specific syntheses. , 1966, Journal of molecular biology.

[2]  E. Viñuela Virus-specific proteins in Escherichia coli infected with the RNA bacteriophage MS2. , 1967, Bulletin de la Societe de chimie biologique.

[3]  R. O'Callaghan,et al.  Stages in phage R17 infection. VI. Injection of A protein and RNA into the host cell. , 1972, Virology.

[4]  M. Billeter,et al.  REPLICATION OF VIRAL RNA, III. DOUBLE-STRANDED REPLICATIVE FORM OF MSW PHAGE RNA. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[5]  H. Lodish Bacteriophage f2 RNA: Control of Translation and Gene Order , 1968, Nature.

[6]  K. Hori Replication of viral nucleic acids. I. Enzyme-RNA complexes involved in the synthesis of Q-beta RNA. , 1970, Biochimica et biophysica acta.

[7]  H. Slor,et al.  Replication of viral RNA. 13. The early product of phage RNA synthesis in vitro. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[8]  L. Gold,et al.  Translation of the UGA triplet in vitro by tryptophan transfer RNA's. , 1971, Journal of molecular biology.

[9]  P. Hofschneider,et al.  Secondary structure of RNA phage M12 replicative intermediates in vivo. , 1973, Biochimica et Biophysica Acta.

[10]  M. Billeter,et al.  Structure and function of phage RNA. , 1973, Annual review of biochemistry.

[11]  M. Billeter,et al.  Localization of Qβ Maturation Cistron Ribosome Binding Site , 1971 .

[12]  J. Roberts,et al.  The reconstitution of infective bacteriophage R17. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Valentine,et al.  Translational repression of f2 protein synthesis. , 1968, Biochemical and biophysical research communications.

[14]  S. Ochoa,et al.  Messenger discriminating species of initiation factor F3. , 1971, Nature: New biology.

[15]  R. Kamen,et al.  Reconstitution of Q replicase lacking subunit with protein-synthesis-interference factor i. , 1972, European journal of biochemistry.

[16]  M. Billeter,et al.  Nucleotide sequence analysis of an enzymatically synthesized RNA corresponding to the 5'-terminal region of Q beta RNA. , 1969, Cold Spring Harbor symposia on quantitative biology.

[17]  H. Boedtker Conformation independent molecular weight determinations of RNA by gel electrophoresis , 1971 .

[18]  A. Mclachlan Tests for comparing related amino-acid sequences. Cytochrome c and cytochrome c 551 . , 1971, Journal of molecular biology.

[19]  R. Gesteland,et al.  The adsorption of bacteriophage R-17 , 1964 .

[20]  Y. Groner,et al.  Characterization of cistron specific factors for the initiation of messenger RNA translation inE. coli , 1972, FEBS letters.

[21]  N. Fedoroff,et al.  Structure of the poly(G) polymerase component of the bacteriophage f2 replicase. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. August,et al.  The 3′-Terminus and the Replication of Phage RNA , 1969, Nature.

[23]  Y. Groner,et al.  Cistron specific translation control protein in Escherichia coli. , 1972, Nature: New biology.

[24]  M. Billeter,et al.  Location of the coat cistron on the RNA of phage Q-beta. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[25]  P. Hofschneider,et al.  Gene Order of RNA Bacteriophage M12 , 1970, Nature.

[26]  T. Shiba,et al.  Isolation and Grouping of RNA Phages , 1967 .

[27]  G. Gussin Three complementation groups in bacteriophage R17. , 1966, Journal of molecular biology.

[28]  P. Kaesberg,et al.  RIBONUCLEASE DIGESTION OF R17 VIRAL RNA. , 1965, Journal of molecular biology.

[29]  David William Scott SEROLOGICAL CROSS REACTIONS AMONG THE RNA-CONTAINING COLIPHAGES. , 1965, Virology.

[30]  H. Lodish,et al.  Messenger characteristics of nascent bacteriophage RNA. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[31]  C. Weissmann,et al.  Subunit Structure of Qβ Replicase , 1970, Nature.

[32]  W. S. Hayward,et al.  Bacterial proteins required for replication of phage Q ribonucleic acid. Pruification and properties of host factor I, a ribonucleic acid-binding protein. , 1972, The Journal of biological chemistry.

[33]  S. Spiegelman,et al.  Homology Test between the Nucleic Acid of an RNA Virus and the DNA in the Host Cell , 1962, Science.

[34]  C. Weissmann,et al.  Possible Origin of a Minor Virus Specific Protein (A1) in Qβ Particles , 1971 .

[35]  T. Shiba,et al.  Grouping of RNA phages based on the template specificity of their RNA replicases. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Silverman Replication of RNA viruses: analysis by liquid polymer phase partition of the binding of Q RNA polymerase to nucleic acid. , 1973, Archives of biochemistry and biophysics.

[37]  D. Baltimore,et al.  RNA-directed DNA synthesis and RNA tumor viruses. , 1972, Advances in virus research.

[38]  A. Weiner,et al.  Natural Read-through at the UGA Termination Signal of Qβ Coat Protein Cistron , 1971 .

[39]  R. Thach,et al.  Mechanism of viral replication. I. Structure of replication complexes of R17 bacteriophage. , 1973, Journal of molecular biology.

[40]  H. Slor,et al.  In vitro synthesis of phage RNA: the nature of the intermediates. , 1968, Cold Spring Harbor symposia on quantitative biology.

[41]  R. Kamen Characterization of the Subunits of Qβ Replicase , 1970, Nature.

[42]  J. Steitz,et al.  Gene Order in the Bacteriophage R17 RNA : 5′–;A Protein–Coat Protein–Synthetase–3′ , 1970, Nature.

[43]  M. Edgell,et al.  The fate during infection of the coat protein of the spherical bacteriophage R-17. , 1965, Virology.

[44]  D. Kolakofsky,et al.  Q replicase as repressor of Q RNA-directed protein synthesis. , 1971, Biochimica et biophysica acta.

[45]  C. Brinton The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. , 1965, Transactions of the New York Academy of Sciences.

[46]  P. Borst,et al.  Replication of viral RNA, 8. Studies on the enzymatic mechanism of replication of MS2 RNA. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[47]  J. Hudson,et al.  Effect of Bacteriophage R17 Infection on Hostdirected Synthesis of Ribosomal Ribonucleates , 1967, Journal of virology.

[48]  A. Sillero,et al.  Virus-specific proteins in Escherichia coli infected with phage Qb. , 1969, Biochimica et biophysica acta.

[49]  S. Cory,et al.  Untranslated Nucleotide Sequence at the 5′-End of R 17 Bacteriophage RNA , 1970, Nature.

[50]  D. Nathans,et al.  Fate of maturation protein during infection by coliphage MS2. , 1971, Nature: New biology.

[51]  R. Kamen,et al.  Host subunit of Q replicase is translation control factor i. , 1972, Nature: New biology.

[52]  S. Cory,et al.  Nucleotide sequences of fragments of R17 bacteriophage RNA from the region immediately preceding the coat-protein cistron. , 1972, European journal of biochemistry.

[53]  S. Spiegelman,et al.  AN RNA "REPLICASE" INDUCED BY AND SELECTIVE FOR A VIRAL RNA: ISOLATION AND PROPERTIES. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[54]  R. E. Webster,et al.  Gene products of bacteriophage Qβ , 1971 .

[55]  J. Hindley Structure and strategy in phage RNA. , 1973, Progress in biophysics and molecular biology.

[56]  L. Phelps Isolation and characterization of bacteriophages for Neisseria. , 1967, The Journal of general virology.

[57]  H. Hoffmann-Berling RELEASE OF MALE-SPECIFIC BACTERIOPHAGES FROM SURVIVING HOST BACTERIA. , 1964 .

[58]  D. Kolakofsky,et al.  Possible mechanism for transition of viral RNA from polysome to replication complex. , 1971, Nature: New biology.

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

[60]  T. Blumenthal,et al.  Bacteriophage Q replicase contains the protein biosynthesis elongation factors EF Tu and EF Ts. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[61]  K. Weber,et al.  Amino-acid Sequence of the Qβ Coat Protein , 1970, Nature.

[62]  R. Contreras,et al.  Bacteriophage Ms2 RNA: nucleotide sequence of the end of the a protein gene and the intercistronic region. , 1973, Nature: New biology.

[63]  G. Godson,et al.  The replication of bacteriophage MS2. VI. Interaction between bacteriophage RNA and cellular components in MS2-infected Escherichia coli. , 1967, Journal of molecular biology.

[64]  D. Mills,et al.  The synthesis of a self-propagating and infectious nucleic acid with a purified enzyme. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[65]  H. Lodish,et al.  Mutants of the bacteriophage f2. VI. Homology of temperature-sensitive and host-dependent mutants. , 1966, Virology.

[66]  N. Zinder,et al.  A bacteriophage containing RNA. , 1961, Proceedings of the National Academy of Sciences of the United States of America.

[67]  D. Nathans,et al.  Regulation of protein synthesis directed by coliphage MS2 RNA. II. In vitro repression by phage coat protein. , 1969, Journal of molecular biology.

[68]  Y. Groner,et al.  Effect of a purified initiation factor F3 (B) on the selection of ribosomal binding sites on phage MS2 RNA. , 1971, Nature: New biology.

[69]  J. H. Strauss A MODIFIED METHOD OF MS2-RNA ASSAY. , 1964, Journal of molecular biology.

[70]  Y. Shimura,et al.  BACTERIOPHAGE-SPECIFIC PROTEINS IN E. COLI INFECTED WITH AN RNA BACTERIOPHAGE* , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[71]  R. E. Webster,et al.  Bacteriophage Coat Protein as Repressor , 1968, Nature.

[72]  K. Horiuchi,et al.  Three cistrons in bacteriophage Qβ , 1970 .

[73]  K. Weber Amino acid sequence studies on the tryptic peptides of the coat protein of the bacteriophage R17. , 1967, Biochemistry.

[74]  J. H. Cramer,et al.  Replication of bacteriophage MS2. X. Phage-specific ribonucleoprotein particles found in MS2-infected Escherichia coli. , 1971, Journal of molecular biology.

[75]  D. E. Bradley Evidence for the retraction of Pseudomonas aeruginosa RNA phage pili. , 1972, Biochemical and biophysical research communications.

[76]  M. Billeter,et al.  The nucleotide sequence at the 5'-terminus of the Q RNA minus trand. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[77]  H. Goodman,et al.  Sequence of the First 175 Nucleotides from the 5′ Terminus of Qβ RNA synthesized in vitro , 1969, Nature.

[78]  M. Billeter,et al.  Replication of viral ribonucleic acid. X. Turnover of virus-specific double-stranded ribonucleic acid during replication of phage MS2 in Escherichia coli. , 1966, The Journal of biological chemistry.

[79]  S. Spiegelman,et al.  Specific template requirments of RNA replicases. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[80]  W. Paranchych,et al.  Heterogeneous distribution of A protein in R17 phage preparations. , 1971, Virology.

[81]  J. Steitz Polypeptide Chain Initiation: Nucleotide Sequences of the Three Ribosomal Binding Sites in Bacteriophage R17 RNA , 1969, Nature.

[82]  S. Cory,et al.  Untranslated Nucleotide Sequences in R17 Bacteriophage RNA , 1970 .

[83]  J. Hindley,et al.  Sequence of a Ribosome Binding Site in Bacteriophage Qβ-RNA , 1969, Nature.

[84]  J. Hindley,et al.  Ribosome Binding Site of Qβ RNA Polymerase Cistron , 1971 .

[85]  P. Harrison,et al.  An X-ray scattering study of the bacterial virus R17 , 1965 .

[86]  M. Billeter,et al.  Molecular basis for repressor activity of Q replicase. , 1972, Nature: New biology.

[87]  S. Ochoa,et al.  Specific inhibitors of MS2 and late T4 RNA translation in E. coli. , 1972, Biochemical and biophysical research communications.

[88]  J. Nichols Nucleotide Sequence from the Polypeptide Chain Termination Region of the Coat Protein Cistron in Bacteriophage R17 RNA , 1970, Nature.

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

[90]  S. Ochoa,et al.  Replication of phage RNA. , 1967, Progress in nucleic acid research and molecular biology.

[91]  L. Shapiro,et al.  Synthesis of bacteriophage Q-beta RNA. , 1968, Cold Spring Harbor Symposia on Quantitative Biology.

[92]  H. Lodish,et al.  Mutants of the bacteriophage f2. V. On the production of noninfectious phage particles. , 1965, Virology.

[93]  P. Silverman Replication of RNA viruses: specific binding of the Q RNA polymerase to Q RNA. , 1973, Archives of biochemistry and biophysics.

[94]  T. Shiba,et al.  Isolation and properties of RNA replicases induced by SP and FI phages. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[95]  D. Mills,et al.  An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. , 1967, Proceedings of the National Academy of Sciences of the United States of America.