Membrane-Associated Metabolic Systems Induced by Bacteriophage T4 Infection of Escherichia coli

  • James F. Koerner
  • D. Peter Snustad
  • Huber R. Warner


In this chapter, we review evidence that certain metabolic systems established during the process of infection of Escherichia coli with bacteriophage T4 are associated with the cell envelope of the host. Information pertaining to this subject is incomplete and often controversial. Nevertheless, we are encouraged to review what is known on the premise that the T4 phage system, as has been demonstrated so often in the past, is uniquely endowed with favorable properties for exploring important questions in biology including the structure and functions of cell membranes. Our format is intended to be descriptive rather than comprehensive, and the literature cited is illustrative rather than exhaustive.


Cell Envelope Amber Mutant Head Assembly Superinfection Exclusion Temporal Exclusion 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alberts, B. M., 1970, Function of gene 32-protein, a new protein essential for the genetic recombination and replication of T4 bacteriophage DNA, Fed. Proc. 29:1154.PubMedGoogle Scholar
  2. Alberts, B., 1971, On the structure of the replication apparatus, in: Nucleic Acid-Protein InteractionsNucleic Acid Synthesis in Viral Infection (D. W. Ribbons, J. F. Woessner, and J. Schultz, eds.), pp. 128–143, North-Holland Publishing Co., Amsterdam.Google Scholar
  3. Alberts, B., 1973, Studies on the replication of DNA, in: Molecular Cytogenetics (B. A. Hamkalo, and J. Papaconstantinou, eds.), pp. 233–251, Plenum Press, New York.Google Scholar
  4. Alberts, B. M., and Frey, L., 1970, T4 bacteriophage gene 32: A structural protein in the replication and recombination of DNA, Nature (London) 227:1313.Google Scholar
  5. Alberts, B. M., Amodio, F. J., Jenkins, M., Gutmann, E. D., and Ferris, F. L., 1968, Studies with DNA-cellulose chromatography. I. DNA-binding proteins from Escherichia coli, Cold Spring Harbor Symp. Quant. Biol. 33:289.PubMedGoogle Scholar
  6. Altman, S., and Lerman, L. S., 1970, Kinetics and intermediates in the intracellular synthesis of bacteriophage T4 deoxyribonucleic acid, J. Mol. Biol. 50:235.PubMedGoogle Scholar
  7. Anderson, C. W., and Eigner, J., 1971, Breakdown and exclusion of superinfecting T-even bacteriophage in Escherichia coli, J. Virol. 8:869.PubMedGoogle Scholar
  8. Anderson, C. W., Williamson, J. R., and Eigner, J., 1971, Localization of parental deoxyribonucleic acid from superinfecting T4 bacteriophage in Escherichia coli, J. Virol. 8:887.PubMedGoogle Scholar
  9. Baghrach, U., Friedman, A., Levin, R., and Nygaard, A. P., 1974, Transfer of internal proteins from phage to host and their association with bacterial membranes, J. Gen. Virol. 23:117.Google Scholar
  10. Barry, J., and Alberts, B., 1972, In vitro complementation as an assay for new proteins required for bacteriophage T4 DNA replication: Purification of the complex specified by T4 genes 44 and 62, Proc. Natl. Acad. Sci. U.S.A. 69:2717.PubMedGoogle Scholar
  11. Barry, J., Hama-Inaba, H., Moran, L., Alberts, B., and Wiberg, J., 1973, Proteins of the T4 bacteriophage replication apparatus, in: DNA Synthesis in Vitro (R. D. Wells, and R. B. Inman, eds.), pp. 195–213, University Park Press, Baltimore.Google Scholar
  12. Beckey, A. D., Wulff, J. L., and Earhart, C. F., 1974, Early synthesis of membrane protein after bacteriophage T4 infection, J. Virol. 14:886.PubMedGoogle Scholar
  13. Bennett, J., Glavinovich, J., Liskay, R., Wulff, D. L., and Cronan, J. E., Jr., 1971, Phospholipid hydrolysis in Escherichia coli infected with rapid lysis mutants of phage T4, Virology 43:516.PubMedGoogle Scholar
  14. Bernstein, C., and Bernstein, H., 1974, Coiled rings of DNA released from cells infected with bacteriophages T7 or T4 or from uninfected Escherichia coli, J. Virol. 13:1346.PubMedGoogle Scholar
  15. Bijlenga, R. K. L., Scraba, D., and Kellenberger, E., 1973, Studies on the morphopoiesis of the head of T-even phage. IX. τ-particles: Their morphology, kinetics of appearance and possible precursor function, Virology 56:250.PubMedGoogle Scholar
  16. Black, L. W., 1974, Bacteriophage T4 internal protein mutants: Isolation and properties, Virology 60:166.PubMedGoogle Scholar
  17. Black, L. W., and Abremski, K., 1974, Restriction of phage T4 internal protein I mutants by a strain of Escherichia coli, Virology 60:180.PubMedGoogle Scholar
  18. Bonifas, V., and Kellenberger, E., 1955, Étude de l’action des membranes du bactériophage T2 sur Escherichia coli, Biochim. Biophys. Acta 16:330.PubMedGoogle Scholar
  19. Bradley, W. E. G., and Astrachan, L., 1971, Occurrence of lysophosphatides in bacteriophage T4rII-infected Escherichia coli S/6, J. Virol. 8:437.PubMedGoogle Scholar
  20. Braun, V., and Hantke, K., 1974, Biochemistry of bacterial cell envelopes, Ann. Rev. Biochem. 43:89.PubMedGoogle Scholar
  21. Brown, D. T., and Anderson, T. F., 1969, Effect of host cell wall material on the adsorbability of cofactor-requiring T4, J. Virol. 4:94.PubMedGoogle Scholar
  22. Brutlag, D., and Kornberg, A., 1972, Enzymatic synthesis of deoxyribonucleic acid. XXXVI. A proofreading function for the 3′ —> 5′ exonuclease activity in deoxyribonucleic acid polymerases, J. Biol. Chem. 247:241.PubMedGoogle Scholar
  23. Buller, G. S., and Astrachan, L., 1968, Replication of T4rII bacteriophage in Escherichia coli K-12 (λ), J. Virol. 2:298.PubMedGoogle Scholar
  24. Carroll, R. B., Neet, K. E., and Goldthwait, D. A., 1972, Self-association of gene 32-protein of bacteriophage T4, Proc. Natl. Acad. Sci. U.S.A. 69:2741.PubMedGoogle Scholar
  25. Ghao, J., Chao, L., and Speyer, J. F., 1974, Bacteriophage T4 head morphogenesis: Host DNA enzymes affect frequency of petite forms, J. Mol. Biol. 85:41.Google Scholar
  26. Childs, J. D., 1973, Superinfection exclusion by incomplete genomes of bacteriophage T4, J. Virol. 11:1.PubMedGoogle Scholar
  27. Cohen, S. S., 1968, Virus-Induced Enzymes, Columbia University Press, New York.Google Scholar
  28. Collinsworth, W. L., and Mathews, G. K., 1974, Biochemistry of DNA-defective amber mutants of bacteriophage T4. IV. DNA synthesis in plasmolysed cells, J. Virol. 13:908.PubMedGoogle Scholar
  29. Coppo, A., Manzi, A., Pulitzer, J. F., and Takahashi, H., 1973, Abortive bacteriophage T4 head assembly in mutants of Escherichia coli, J. Mol. Biol. 76:61.PubMedGoogle Scholar
  30. Costerton, J. W., Ingram, J. M., and Cheng, K.J., 1974, Structure and function of the cell envelope of Gram-negative bacteria, Bacteriol. Rev. 38:87.PubMedGoogle Scholar
  31. Cronan, J. E., Jr., and Vagelos, P. R., 1971, Abortive infection by phage T4 under conditions of defective host membrane lipid biosynthesis, Virology 43:412.PubMedGoogle Scholar
  32. Cronan, J. E., Jr., and Wulff, D. L., 1969, A role for phospholipid hydrolysis in the lysis of Escherichia coli infected with bacteriophage T4, Virology 38:241.PubMedGoogle Scholar
  33. Delius, H., Mantell, N. J., and Alberts, B., 1972, Characterization by electron microscopy of the complex formed between T4 bacteriophage gene 32-protein and DNA, J. Mol. Biol. 67:341.PubMedGoogle Scholar
  34. de Waard, A., Paul, A. V., and Lehman, I. R., 1965, The structural gene for deoxyribonucleic acid polymerase in bacteriophages T4 and T5, Proc. Natl. Acad. Sci. U.S.A. 54:1241.PubMedGoogle Scholar
  35. Dirksen, M., Hutson, J. C., and Buchanan, J. M., 1963, Host-dependent synthesis of altered deoxycytidylate hydroxymethylase after infection of Escherichia coli with certain amber mutants of bacteriophage T4, Proc. Natl. Acad. Sci. U.S.A. 50:507.PubMedGoogle Scholar
  36. Doermann, A. H., 1948, Lysis and lysis inhibition with Escherichia coli bacteriophage, J. Bacteriol. 55:257.Google Scholar
  37. Doermann, A. H., Eiserling, F. A., and Boehner, L., 1973, Genetic control of capsid length in bacteriophage T4. I. Isolation and preliminary description of four new mutants, J. Virol. 12:374.PubMedGoogle Scholar
  38. Duckworth, D. H., 1970, Biological activity of bacteriophage ghosts and “take over” of host functions by bacteriophage, Bacteriol. Rev. 34:344.PubMedGoogle Scholar
  39. Duckworth, D. H., and Bessman, M. J., 1967, The enzymology of virus-infected bacteria. X. A biochemical-genetic study of the deoxynucleotide kinase induced by wild type and amber mutants of phage T4, J. Biol. Chem. 242:2877.PubMedGoogle Scholar
  40. Dulbecco, R., 1952, Mutual exclusion between related phages, J. Bacteriol. 63:209.PubMedGoogle Scholar
  41. Dürwald, H., and Hoffmann-Berling, H., 1968, Endonuclease I-deficient and ribonuclease I-deficient Escherichia coli mutants, J. Mol. Biol. 34:331.PubMedGoogle Scholar
  42. Dworsky, P., and Schaechter, M., 1973, Effect of rifampin on the structure and membrane attachment of the nucleoid of Escherichia coli, J. Bacteriol. 116:1364.PubMedGoogle Scholar
  43. Earhart, G. F., 1970, The association of host and phage DNA with the membrane of Escherichia coli, Virology 42:429.PubMedGoogle Scholar
  44. Earhart, G. F., Tremblay, G. Y., Daniels, M. J., and Schaechter, M., 1968, DNA replication studied by a new method for the isolation of cell membrane-DNA complexes, Cold Spring Harbor Symp. Quant. Biol. 33:707.PubMedGoogle Scholar
  45. Earhart, C. F., Sauri, C. J., Fletcher, G., and Wulff, J. L., 1973, Effect of inhibition of macromolecule synthesis on the association of bacteriophage T4 DNA with membrane, J. Virol. 11:527.PubMedGoogle Scholar
  46. Eiserling, F. A., Geiduschek, E. P., Epstein, R. H., and Metter, E. J., 1970, Capsid size and deoxyribonucleic acid length: The petite variant of bacteriophage T4, J. Virol. 6:865.PubMedGoogle Scholar
  47. Ennis, H. L., and Kievitt, K. D., 1973, Association of the rIIA protein with the bacterial membrane, Proc. Natl. Acad. Sci. U.S.A. 70:1468.PubMedGoogle Scholar
  48. Epstein, R. H., Bolle, A., Steinberg, C. M., Kellenberger, E., de la Tour E., Chevalley, R., Edgar, R. S., Susman, M., Denhardt, G. H., and Lielausis, A., 1963, Physiological studies of conditional lethal mutants of bacteriophage T4D, Cold Spring Harbor Symp. Quant. Biol. 28:375.Google Scholar
  49. Fielding, P. E., and Lunt, M. R., 1970, The relation between breakdown of superinfecting virus deoxyribonucleic acid and temporal exclusion induced by T4 and T5 bacteriophages, J. Gen. Virol. 6:333.PubMedGoogle Scholar
  50. Fletcher, G., Wulff, J. L., and Earhart, G. F., 1974, Localization of membrane protein synthesized after infection with bacteriophage T4, J. Virol. 13:73.PubMedGoogle Scholar
  51. Frankel, F. R., 1966a, The absence of mature phage DNA molecules from the replicating pool of T-even-infected Escherichia coli, J. Mol. Biol. 18:109.PubMedGoogle Scholar
  52. Frankel, F. R., 1966b, Studies on the nature of replicating DNA in T4-infected Escherichia coli, J. Mol. Biol. 18:127.PubMedGoogle Scholar
  53. Frankel, F. R., 1968, Evidence for long DNA strands in the replicating pool after T4 infection, Proc. Natl. Acad. Sä. U.S.A. 59:131.Google Scholar
  54. Furrow, M. H., and Pizer, L. I., 1968, Phospholipid synthesis in Escherichia coli infected with T4 bacteriophages, J. Virol. 2:594.PubMedGoogle Scholar
  55. Georgopoulos, G. P., Hendrix, R. W., Kaiser, A. D., and Wood, W. B., 1972, Role of the host cell in bacteriophage morphogenesis: Effects of a bacterial mutation on T4 head assembly, Nature (London), New Biol. 239:38.Google Scholar
  56. Graham, A. F., 1953, The fate of the infecting phage particle, Ann. Inst. Pasteur Paris 84:90.PubMedGoogle Scholar
  57. Goulian, M., Lucas, Z. J., and Kornberg, A., 1968, Enzymatic synthesis of deoxyribonucleic acid. XXV. Purification and properties of deoxyribonucleic acid polymerase induced by infection with phage T4 +, J. Biol. Chem. 243:627.PubMedGoogle Scholar
  58. Hercules, K., Munro, J. L., Mendelsohn, S., and Wiberg, J. S., 1971, Mutants in a nonessential gene of bacteriophage T4 which are defective in the degradation of Escherichia coli deoxyribonucleic acid, J. Virol. 7:95.PubMedGoogle Scholar
  59. Hershey, A. D., 1946, Mutation of bacteriophage with respect to type of plaque, Genetics 31:620.Google Scholar
  60. Hershey, A. D., Garen, A., Fraser, D. K., and Hudis, J. D., 1954, Growth and inheritance in bacteriophage, Carnegie Inst. Washington Yearb. 53:210.Google Scholar
  61. Huberman, J. A., 1968, Visualization of replicating mammalian and T4 bacteriophage DNA, Cold Spring Harbor Symp. Quant. Biol. 33:509.PubMedGoogle Scholar
  62. Huberman, J. A., Kornberg, A., and Alberts, B. M., 1971, Stimulation of T4 bacteriophage DNA polymerase by the protein product of T4 gene 32, J. Mol. Biol. 62:39.PubMedGoogle Scholar
  63. Josslin, R., 1970, The lysis mechanism of phage T4: Mutants affecting lysis, Virology 40:719.PubMedGoogle Scholar
  64. Josslin, R., 1971a, The effect of phage T4 infection on phospholipid hydrolysis in Escherichia coli, Virology 44:94.PubMedGoogle Scholar
  65. Josslin, R., 1971b, Physiological studies on the t gene defect in T4-infected Escherichia coli, Virology 44:101.PubMedGoogle Scholar
  66. Kellenberger, E., 1960, The physical state of the bacterial nucleus, in: Microbial Genetics, Tenth Symposium of the Society for General Microbiology (W. Hayes, and R. G. Clowes, eds.), pp. 39–66, Cambridge University Press, London.Google Scholar
  67. Kellenberger, E., Séchaud, J., and Ryter, A., 1959, Electron microscopical studies of phage multiplication. IV. The establishment of the DNA pool of vegetative phage and the maturation of phage particles, Virology 8:478.PubMedGoogle Scholar
  68. King, J., and Laemmli, U. K., 1971, Polypeptides of the tail fibres of bacteriophage T4, J. Mol. Biol. 62:465.PubMedGoogle Scholar
  69. Koerner, J. F., 1970, Enzymes of nucleic acid metabolism, Ann. Rev. Biochem. 39:291.PubMedGoogle Scholar
  70. Korn, D., Protass, J. J., and Leive, L., 1965, A novel effect of actinomycin D in preventing bacteriophage T4 maturation in Escherichia coli, Biochem. Biophys. Res. Commun. 19:473.PubMedGoogle Scholar
  71. Kornberg, A., 1974, DNA Synthesis, W. H. Freeman, San Francisco.Google Scholar
  72. Kornberg, T., Lockwood, A., and Worcel, A., 1974, Replication of the Escherichia coli chromosome with a soluble enzyme system, Proc. Natl. Acad. Sci. U.S.A. 71:3189.PubMedGoogle Scholar
  73. Kozinski, A. W., and Lin, T. H., 1965, Early intracellular events in the replication of T4 phage DNA. I. Complex formation of replicative DNA, Proc. Natl. Acad. Sci. U.S.A. 54:273.PubMedGoogle Scholar
  74. Laemmli, U. K., Beguin, F., and Gujer-Kellenberger, G., 1970, A factor preventing the major head protein of bacteriophage T4 from random aggregation, J. Mol. Biol. 47:69.PubMedGoogle Scholar
  75. Langworthy, T. A., and Buller, C. S., 1973, The effect of phage infection on the synthesis of lipid A by Escherichia coli, Virology 54:80.PubMedGoogle Scholar
  76. Lehman, I. R., Roussos, G. G., and Pratt, E. A., 1962, The deoxyribonucleases of Escherichia coli. II. Purification and properties of a ribonucleic acid-inhibitable endonuclease, J. Biol. Chem. 237:819.PubMedGoogle Scholar
  77. Levinthal, G., and Visconti, N., 1953, Growth and recombination in bacterial viruses, Genetics 38:500.PubMedGoogle Scholar
  78. Loeb, M. R., 1974, Bacteriophage T4-mediated release of envelope components from Escherichia coli, J. Virol. 13:631.PubMedGoogle Scholar
  79. Luria, S. E., and Human, M. L., 1950, Chromatin staining of bacteria during bacteriophage infection, J. Bacteriol. 59:551.PubMedGoogle Scholar
  80. Majumdar, C., Dewey, M., and Frankel, F. R., 1972, Bacteriophage-directed association of DNA polymerase I with host membrane: A dispensable function, Virology 49:134.PubMedGoogle Scholar
  81. Mathews, C. K., 1971, Bacteriophage Biochemistry, ACS Monograph 166, Van Nostrand Reinhold Co., New York.Google Scholar
  82. Miller, R. C., Jr., 1972, Association of replicative T4 deoxyribonucleic acid and bacterial membranes, J. Virol. 10:920.PubMedGoogle Scholar
  83. Miller, R. C., Jr., and Buckley, P., 1970, Early intracellular events in the replication of bacteriophage T4 deoxyribonucleic acid. VI. Newly synthesized proteins in the T4 protein-deoxyribo-nucleic acid complex, J. Virol. 5:502.PubMedGoogle Scholar
  84. Miller, R. C., Jr., and Kozinski, A. W., 1970, Early intracellular events in the replication of bacteriophage T4 deoxyribonucleic acid. V. Further studies on the T4 protein-deoxyribonucleic acid complex, J. Virol. 5:490.PubMedGoogle Scholar
  85. Mosig, G., 1963, Genetic recombination in bacteriophage T4 during replication of DNA fragments, Cold Spring Harbor Symp. Quant. Biol. 28:35.Google Scholar
  86. Mufti, S., 1972, A bacteriophage T4 mutant defective in protection against superinfecting phage, J. Gen. Virol. 17:119.PubMedGoogle Scholar
  87. Munch-Petersen, A., and Schwartz, M., 1972, Inhibition of catabolism of deoxyribonucleosides in Escherichia coli after infection by T4 phage, Eur. J. Biochem. 27:443.PubMedGoogle Scholar
  88. Murray, R. G. E., Gillen, D. H., and Heagy, F. C., 1950, Cytological changes in Escherichia coli produced by infection with phage T2, J. Bacteriol. 59:603.PubMedGoogle Scholar
  89. Nelson, E. T., and Buller, C. S., 1974, Phospholipase activity in bacteriophage-infected Escherichia coli. I. Demonstration of a T4 bacteriophage-associated phospholipase, J. Virol. 14:479.PubMedGoogle Scholar
  90. Nossal, N. G., and Heppel, L. A., 1966, The release of enzymes by osmotic shock from Escherichia coli in exponential phase, J. Biol. Chem. 241:3055.PubMedGoogle Scholar
  91. Parson, K. A., and Snustad, D. P., 1975, Host DNA degradation after infection of Escherichia coli with bacteriophage T4: Dependence of the alternate pathway of degradation which occurs in the absence of both T4 endonuclease II and nuclear disruption on T4 endonuclease IV, J. Virol. 15:221.PubMedGoogle Scholar
  92. Peterson, R. H. F., and Buller, G. S., 1969, Phospholipid metabolism in T4 bacteriophage-infected Escherichia coli K-12 (A), J. Virol. 3:463.PubMedGoogle Scholar
  93. Peterson, R. F., Kievitt, K. D., and Ennis, H. L., 1972, Membrane protein synthesis after infection of Escherichia coli B with phage T4. The rIIB protein, Virology 50:520.PubMedGoogle Scholar
  94. Pollock, P. N., and Duckworth, D. H., 1973, Outer membrane proteins induced by T4 bacteriophage, Biochim. Biophys. Acta. 322:321.PubMedGoogle Scholar
  95. Puck, T. T., and Lee, H. H., 1954, Mechanism of cell wall penetration by viruses. I. An increase in host cell permeability induced by bacteriophage infection, J. Exp. Med. 99:481.PubMedGoogle Scholar
  96. Puck, T. T., and Lee, H. H., 1955, Mechanism of cell wall penetration by viruses. II. Demonstration of cyclic permeability change accompanying virus infection of Escherichia coli B cells, J. Exp. Med. 101:151.PubMedGoogle Scholar
  97. Pulitzer, J. F., and Yanagida, M., 1971, Inactive T4 progeny virus formation in a temperature-sensitive mutant of Escherichia coli K12, Virology 45:539.PubMedGoogle Scholar
  98. Riva, S., Gascino, A., and Geiduschek, E. P., 1970, Coupling of late transcription to viral replication in bacteriophage T4 development, J. Mol. Biol. 54:85.PubMedGoogle Scholar
  99. Sadowski, P. D., Warner, H. R., Hercules, K., Munro, J. L., Mendelsohn, S., and Wiberg, J. S., 1971, Mutants of bacteriophage T4 defective in the induction of T4 endonuclease II, J. Biol. Chem. 246:3431.PubMedGoogle Scholar
  100. Shalitin, C., and Naot, Y., 1971, Role of gene 46 in bacteriophage T4 deoxyribonucleic acid synthesis, J. Virol. 8:142.PubMedGoogle Scholar
  101. Showe, M. K., and Black, L. W., 1973, Assembly core of bacteriophage T4: An intermediate in head formation, Nature (London), New Biol. 242:70.Google Scholar
  102. Siegel, P. J., and Schaechter, M., 1973a, The role of the host cell membrane in the replication and morphogenesis of bacteriophage, Ann. Rev. Microbiol. 27:261.Google Scholar
  103. Siegel, P. J., and Schaechter, M., 1973b, Bacteriophage T4 head maturation: release of progeny DNA from the host cell membrane, J. Virol. 11:359.PubMedGoogle Scholar
  104. Silver, S., 1967, Acridine sensitivity of bacteriophage T2: A virus gene affecting cell permeability, J. Mol. Biol. 29:191.PubMedGoogle Scholar
  105. Silver, S., Levine, E., and Spielman, P. M., 1968, Cation fluxes and permeability changes accompanying bacteriophage infection of Escherichia coli, J. Virol. 2:763.PubMedGoogle Scholar
  106. Simon, L. D., 1969, The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. III. Membrane-associated intracellular bacteriophages, Virology 38:285.PubMedGoogle Scholar
  107. Simon, L. D., 1972, Infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope: T4 head morphogenesis, Proc. Natl. Acad. Sci. U.S.A. 69:907.PubMedGoogle Scholar
  108. Sinha, N. K., and Snustad, D. P., 1971, DNA synthesis in bacteriophage T4-infected Escherichia coli: Evidence supporting a stoichiometric role for gene 32-product, J. Mol. Biol. 62:267.PubMedGoogle Scholar
  109. Snustad, D. P., 1968, Dominance interactions in Escherichia coli cells mixedly infected with bacteriophage T4D wild-type and amber mutants and their possible implications as to type of gene-product function: Catalytic vs. stoichiometric, Virology 35:550.PubMedGoogle Scholar
  110. Snustad, D. P., and Conroy, L. M., 1974, Mutants of bacteriophage T4 deficient in the ability to induce nuclear disruption. I. Isolation and genetic characterization, J. Mol. Biol. 89:663.PubMedGoogle Scholar
  111. Snustad, D. P., Warner, H. R., Parson, K. A., and Anderson, D. L., 1972, Nuclear disruption after infection of Escherichia coli with a bacteriophage T4 mutant unable to induce endonuclease II, J. Virol. 10:124.PubMedGoogle Scholar
  112. Snustad, D. P., Parson, K. A., Warner, H. R., Tutas, D. J., Wehner, J. M., and Koerner, J. F., 1974, Mutants of bacteriophage T4 deficient in the ability to induce nuclear disruption. II. Physiological state of the host nucleoid in infected cells, J. Mol. Biol. 89:675.PubMedGoogle Scholar
  113. Stonington, O. G., and Pettijohn, D. E., 1971, The folded genome of Escherichia coli isolated in a protein-DNA-RNA complex, Proc. Natl. Acad. Sci. U.S.A. 68:6.PubMedGoogle Scholar
  114. Streisinger, G., Mukai, F., Dreyer, W. J., Miller, B., and Horiuchi, S., 1961, Mutations affecting the lysozyme of phage T4, Cold Spring Harbor Symp. Quant. Biol. 26:25.PubMedGoogle Scholar
  115. Takano, T., and Kakefuda, T., 1972, Involvement of a bacterial factor in morphogenesis of bacteriophage capsid, Nature (London), New. Biol. 239:34.Google Scholar
  116. Tutas, D. J., Wehner, J. M., and Koerner, J. F., 1974, Unfolding of the host genome after infection of Escherichia coli with bacteriophage T4, J. Virol. 13:548.PubMedGoogle Scholar
  117. Vallée, M., and Cornett, J. B., 1972, A new gene of bacteriophage T4 determining immunity against superinfecting ghosts and phage in T4-infected Escherichia coli, Virology 48:777.PubMedGoogle Scholar
  118. Vallée, M., Cornett, J. B., and Bernstein, H., 1972, The action of bacteriophage T4 ghosts on Escherichia coli and the immunity to this action developed in cells preinfected with T4, Virology 48:766.PubMedGoogle Scholar
  119. Vander Maten, M., Nelson, E. T., and Buller, C. S., 1974, Does phospholipase have a role in killing and sodium dodecyl sulfate lysis of T4 ghost-infected Escherichia coli?, J. Virol. 14:1617.PubMedGoogle Scholar
  120. Warner, H. R., and Barnes, J. E., 1966, Deoxyribonucleic acid synthesis in Escherichia coli infected with some deoxyribonucleic acid polymerase-less mutants of bacteriophage T4, Virology 28:100.PubMedGoogle Scholar
  121. Warner, H. R., and Hobbs, M. D., 1967, Incorporation of uracil-14C into nucleic acids in Escherichia coli infected with bacteriophage T4 and T4 amber mutants, Virology 33:376.PubMedGoogle Scholar
  122. Warner, H. R., and Hobbs, M. D., 1969, Effect of hydroxyurea on replication of bacteriophage T4 in Escherichia coli, J. Virol. 3:331.PubMedGoogle Scholar
  123. Warner, H. R., Snustad, D. P., Jorgensen, S. E., and Koerner, J. F., 1970, Isolation of bacteriophage T4 mutants defective in the ability to degrade host deoxyribonucleic acid, J. Virol. 5:700.PubMedGoogle Scholar
  124. Weintraub, S. B., and Frankel, F. R., 1972, Identification of the T4rIIB gene product as a membrane protein, J. Mol. Biol. 70:589.PubMedGoogle Scholar
  125. Werner, R., 1968a, Distribution of growing points in DNA of bacteriophage T4, J. Mol. Biol. 33:679.PubMedGoogle Scholar
  126. Werner, R., 1968b, Initiation and propagation of growing points in the DNA of phage T4, Cold Spring Harbor Symp. Quant. Biol. 33:501.PubMedGoogle Scholar
  127. Wiberg, J. S., 1966, Mutants of bacteriophage T4 unable to cause breakdown of host DNA, Proc. Natl. Acad. Sci. U.S.A. 55:614.PubMedGoogle Scholar
  128. Wiberg, J. S., and Buchanan, J. M., 1964, Studies on labile deoxycytidylate hydroxymethylases from Escherichia coli B infected with temperature-sensitive mutants of bacteriophage T4, Proc.Natl. Acad. Sci. U.S.A. 51:421.PubMedGoogle Scholar
  129. Wiberg, J. S., Dirksen, M., Epstein, R. H., Luria, S. E., and Buchanan, J. M., 1962, Early enzyme synthesis and its control in Escherichia coli infected with some amber mutants of bacteriophage T4, Proc. Natl. Acad. Sci. U.S.A. 48:293.PubMedGoogle Scholar
  130. Worcel, A., and Burgi, E., 1972, On the structure of the folded chromosome of Escherichia coli, J. Mol. Biol. 71:127.PubMedGoogle Scholar
  131. Wovcha, M. G., Tomich, P. K., Chiu, C., and Greenberg, G. R., 1973, Direct participation of dCMP hydroxymethylase in synthesis of bacteriophage T4 DNA, Proc. Natl. Acad. Sci. U.S.A. 70:2196.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1976

Authors and Affiliations

  • James F. Koerner
    • 1
  • D. Peter Snustad
    • 2
  • Huber R. Warner
    • 3
  1. 1.Department of Biochemistry, Medical SchoolUniversity of MinnesotaMinneapolisUSA
  2. 2.Department of Genetics and Cell Biology, College of Biological SciencesUniversity of MinnesotaSt. PaulUSA
  3. 3.Department of Biochemistry, College of Biological SciencesUniversity of MinnesotaSt. PaulUSA

Personalised recommendations