Structure and Synthesis of Bacteriophage PM2, with Particular Emphasis on the Viral Lipid Bilayer

  • Richard M. Franklin
Part of the Current Topics in Microbiology and Immunology / Ergebnisse der Mikrobiologie und Immunitätsforschung book series (CT MICROBIOLOGY, volume 68)


Although a number of bacterial viruses contain lipids, probably arranged in a bilayer, the only one which has been investigated systematically and in detail from the structural and biochemical point of view is bacteriophage PM2, which grows on a marine pseudomonad, Pseudomonas BAL-31 (Espejo and Canelo, 1968a, b). Therefore, the major portion of this review will deal with the molecular biology of bacteriophage PM2. We will commence, however, with a brief review of the other bacteriophages reported to contain lipids and end with a brief comparison between PM2 and other lipid-containing viruses.


Phosphatidic Acid African Swine Fever Virus Semliki Forest Virus Particle Weight Sindbis Virus 
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  1. Acheson, N. H., Tamm, I.: Replication of Semliki Forest virus: An electron microscopic study. Virology 32, 128–143 (1967)PubMedGoogle Scholar
  2. Alderton, G., Ward, W. H., Fevold, H. L.: Isolation of lysozyme from egg white. J. biol. Chem. 157, 43–58 (1945)Google Scholar
  3. Archetti, I., Steve-Bocciarelli, D.: Structure of some simian adenoviruses. Virology 20, 399–404 (1963)PubMedGoogle Scholar
  4. Axel, F., Seelig, J.: Cis double bonds in liquid crystalline bilayers. J. Amer. chem. Soc. 95, 7972–7977 (1973)Google Scholar
  5. Barrantes, F. J.: A comparative study of several membrane proteins from the nervous system. Biochem. biophys. Res. Commun. 54, 395–402 (1973)PubMedGoogle Scholar
  6. Barrantes, F. J., La Torre, J. L., De Carlin, M. C. L., De Robertis, E.: Studies on proteolipid proteins from cerebral cortex. I. Preparation and some properties. Biochim. biophys. Acta (Amst.) 263, 368–381 (1972)Google Scholar
  7. Bell, R. M., Mavis, R. D., Osborn, M. J., Roy Vagelos, P.: Enzymes of phospholipid metabolism: Localization in the cytoplasmic and outer membrane of the cell envelope of Escherichia coli and Salmonella typhimurium. Biochim. biophys. Acta (Amst.) 249, 628–635 (1971)Google Scholar
  8. Bellett, A. J. D.: The iridescent virus group. In: Advances in virus research, vol. 13, p. 225–246, ed. by Smith, K.M., and Lauffer, M. A. New York: Academic Press 1968Google Scholar
  9. Bender, W., Garan, H., Berg, H.: Proteins of the human erythrocyte membrane as modified by pronase. J. molec. Biol. 58, 783–797 (1971)PubMedGoogle Scholar
  10. Berg, H. C.: Sulfanilic acid diazonium salt: A label for the outside of the human erythrocyte membrane. Biochim. biophys. Acta (Amst.) 183, 65–78 (1969)Google Scholar
  11. Best, R. B.: Tomato spotted wilt virus. In: Advances in virus research, vol. 13, p. 65–146, ed. by Smith, K. M., and Lauffer, M. A. New York: Academic Press 1968Google Scholar
  12. Billmeyer, F. W., Jr.: An absorption-extrapolation light scattering method. J. Amer. chem. Soc. 76, 4636–4639 (1954)Google Scholar
  13. Blaurock, A. E., Worthington, C. R.: Low-angle X-ray diffraction patterns from a variety of myelinated nerves. Biochim. biophys. Acta (Amst.) 173, 419–426 (1969)Google Scholar
  14. Bligh, E. G., Dyer, W. J.: A rapid method of total lipid extraction and purification. Canad. J. Biochem. 37, 911–917 (1959)PubMedGoogle Scholar
  15. Boni, I. Y., Budowsky, E. I.: Transformation of non-covalent interactions in nucleo-proteins into covalent bonds induced by nucleophilic reagents. I. The preparation and properties of the products of bisulfite ion-catalyzed reaction of amino acids and peptides with cytosine derivatives. J. Biochem. 73, 821–830 (1973)PubMedGoogle Scholar
  16. Bowman, B. U., Jr.: Quantitative studies on some mycobacterial phage-host systems. J. Bact. 76, 52–62 (1953)Google Scholar
  17. Bowman, B. U., Jr.: Antigenicity of mycobacteriophages R1, D29, and Leo in rabbits. Proc. Soc. exp. Biol. (N.Y.) 128, 441–445 (1968)Google Scholar
  18. Bowman, B. U., Jr.: Effect of chloroform on mycobacteriophages. Microbios 4, 347–352 (1969a)Google Scholar
  19. Bowman, B. U., Jr.: Properties of mycobacteriophage DS6A. I. Immunogenicity in rabbits. Proc. Soc. exp. Biol. (N.Y.) 131, 196–200 (1969b)Google Scholar
  20. Bowman, B. U., Jr., Newman, H. A. I., Moritz, J. M., Koehler, R. M.: Properties of mycobacteriophage DS6A. II. Lipid composition. Amer. Rev. resp. Dis. 107, 42–49 (1973)PubMedGoogle Scholar
  21. Bowman, B. U., Jr., Patnode, R. A.: Neutralization of bacteriophage φX174 by specific antiserum. J. Immunol. 92, 507–514 (1964)PubMedGoogle Scholar
  22. Bowman, B. U., Jr., Redmond, W. B.: A temperate bacteriophage from Myobacterium butyricum. Amer. Rev. resp. Dis. 80, 232–239 (1959)PubMedGoogle Scholar
  23. Bragg, L., Perutz, M. F.: The structure of haemoglobin. Proc. Roy. Soc. A 213, 425–435 (1952)Google Scholar
  24. Braunstein, S. N.: Proteins and phospholipids of the lipid-containing marine bacteriophage PM2. Ph. D. Thesis. New York University (1972)Google Scholar
  25. Braunstein, S. N., Datta, A., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. VIII. Effect of nalidixic acid on some membrane-associated activities of control and infected cells. Virology 46, 161–163 (1971)PubMedGoogle Scholar
  26. Braunstein, S. N., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. V. Phospholipids of the host BAL-31 and of the bacteriophage PM2. Virology 43, 685–695 (1971)PubMedGoogle Scholar
  27. Breese, S. S., Jr., Deboer, C. J.: Electron microscope observations of African swine fever in tissue culture cells. Virology 28, 120–128 (1966)Google Scholar
  28. Breese, S. S., Jr., Stone, S. S., Deboer, C. J., Hess, W. R.: Electron microscopy of the interaction of African swine fever virus with ferritin-conjugated antibody. Virology 31, 508–513 (1967)PubMedGoogle Scholar
  29. Bretscher, M. S.: Asymmetrical lipid bilayer structure for biological membranes. Nature (Lond.) 236, 11–12 (1972a)Google Scholar
  30. Bretscher, M. S.: Phosphatidyl-ethanolamine: Differential labelling in intact cells and cell ghosts of human erythrocytes by a membrane-impermeable reagent. J. molec. Biol. 71, 523–528 (1972b)PubMedGoogle Scholar
  31. Bretscher, M. S.: Membrane structure: Some general principles. Science 181, 622–629 (1973)PubMedGoogle Scholar
  32. Brewer, G. J.: The structure of the membrane-containing bacteriophage PM2. Ph. D. Thesis. University of California at San Diego. La Jolla. (1972)Google Scholar
  33. Burge, B. W., Huang, A. S.: Comparison of membrane protein glycopeptides of Sindbis virus and vesicular stomatitis virus. J.Virol. 6, 176–182 (1970)PubMedGoogle Scholar
  34. Burge, B.W., Strauss, J. H., Jr.: Glycopeptides of the membrane glycoprotein of Sindbis virus. J. molec. Biol. 47, 449–466 (1970)PubMedGoogle Scholar
  35. Camerini-Otero, R. D., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. XII. The fatty acids and lipid content of bacteriophage PM2. Virology 49, 385–393 (1972)PubMedGoogle Scholar
  36. Camerini-Otero, R. D., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. XVII. The molecular weight and other physical properties of bacteriophage PM2. Europ. J. Biochem., Submitted for publication (1974)Google Scholar
  37. Camerini-Otero, R. D., Franklin, R. M., Day, L. A.: Molecular weights, dispersion of refractive index increments, and dimensions from transmittance spectrophotometry: Bacteriophages R17, T7 and PM2, and tobacco mosaic virus. Biochemistry (Wash.), 13, 3763–3773 (1974a)Google Scholar
  38. Camerini-Otero, R. D., Datta, A., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. XI. Studies on the structural glycoprotein of the virus particle. Virology 49, 522–536 (1972)PubMedGoogle Scholar
  39. Camerini-Otero, R. D., Pusey, P. N., Koppel, D. E., Schaefer, D. W., Franklin, R. M.: Intensity fluctuation spectroscopy of laser light scattered by solutions of spherical viruses: R17, , BSV, PM2, and T7. II. Diffusion coefficients, molecular weights, solvation and particle dimensions. Biochemistry (Wash.) 13, 960–970 (1974b)Google Scholar
  40. Carnegie, P. R.: Properties, structure and possible neuroreceptor role of the ence-phalitogenic protein of human brain. Nature (Lond.) 229, 25–28 (1971)Google Scholar
  41. Casassa, E. F., Eisenberg, H.: Partial specific volumes and refractive index increments in multicomponent systems. J. phys. Chem. 65, 427–433 (1961)Google Scholar
  42. Casassa, E. F., Eisenberg, H.: Thermodynamic analysis of multicomponent solutions. In: Advances in protein chemistry, vol. 19, p. 287–395, ed. by Anfinson, C. B., Jr., Anson, M. L., Edsall, J. T., Richards, F. M. New York-London: Academic Press 1964Google Scholar
  43. Cashin, W. M., Debye, P.: Determination of molecular weights and sizes by absorption. Phys. Rev., 2. Ser. 75, 1307 (1949)Google Scholar
  44. Caspar, D. L. D., Kirschner, D. A.: Myelin membrane structure at 10 Å resolution. Nature (Lond.) New Biol. 231, 46–52 (1971)Google Scholar
  45. Caspar, D. L. D., Klug, A.: Physical principles in the construction of regular viruses. Cold Spr. Harb. Symp. quant. Biol. 27, 1–24 (1962)Google Scholar
  46. Chapman, D., Wallach, D. F. H.: Recent physical studies of phospholipids and natural membranes. In: Biological membranes, p. 125–202, ed. by Chapman, D. New York: Academic Press 1968Google Scholar
  47. Chargaff, E.: Isolation and composition of the deoxypentose nucleic acids and of the corresponding nucleoproteins. In: The nucleic acids, vol. I, p. 307–371, ed. by Chargaff, E., Davidson, J.N. New York: Academic Press 1955Google Scholar
  48. Clarke, D. D., Mycek, M. J., Neidle, A., Waelsch, H.: The incorporation of amines into protein. Arch. Biochem. Biophys. 79, 338–354 (1959)Google Scholar
  49. Compans, R. W., Klenk, H.-D., Caliguiri, L. A., Choppin, P. W.: Influenza virus proteins. I. Analysis of polypeptides of the virion and identification of spike glycoproteins. Virology 42, 880–889 (1970)PubMedGoogle Scholar
  50. Cota-Robles, E., Espejo, R. T., Haywood, P. W.: Ultrastructure of bacterial cells infected with bacteriophage PM2, a lipid-containing bacterial virus. J. Virol. 2, 56–68 (1968)PubMedGoogle Scholar
  51. Darnell, J. E., Levintow, L., Thonen, M. M., Hooper, J. L.: The time of synthesis of poliovirus RNA. Virology 13, 271–279 (1961)PubMedGoogle Scholar
  52. Datta, A., Braunstein, S., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. VI. The spectrum of cytoplasmic and membrane-associated proteins in Pseudomonas BAL-31 during replication of bacteriophage PM2. Virology 43, 696–707 (1971a)PubMedGoogle Scholar
  53. Datta, A., Camerini-Otero, R. D., Braunstein, S. N., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. VIL Structural proteins of bacteriophage PM2. Virology 45, 232–239 (1971b)PubMedGoogle Scholar
  54. Datta, A., Camerini-Otero, R. D., Braunstein, S. N., Franklin, R. M.: Proteins of the cell envelope of a marine pseudomonad, Pseudomonas BAL-31. Biochim. biophys. Acta (Amst.) 311, 163–172 (1973)Google Scholar
  55. Datta, A., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. II. Alterations in cytoplasmic and membrane-bound enzymes during replication of bacteriophage PM2. Virology 39, 408–418 (1969)PubMedGoogle Scholar
  56. Datta, A., Franklin, R. M.: DNA-dependent RNA polymerase associated with bacteriophage PM2. Nature (Lond.) New Biol. 236, 131–132 (1972)Google Scholar
  57. Dahlberg, J. E., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. IV. Electron microscopic studies of PM2-infected Pseudomonas BAL-31. Virology 42, 1073–1086 (1970)PubMedGoogle Scholar
  58. Dales, S., Mosbach, E. H.: Vaccinia as a model of membrane biogenesis. Virology 35, 564–583 (1968)PubMedGoogle Scholar
  59. David, A. E.: Lipid composition of Sindbis virus. Virology 46, 711–720 (1971)PubMedGoogle Scholar
  60. Day, M. F., Mercer, E. H.: Properties of an iridescent virus from the beetle Sericesthis pruinosa. Aust. J. biol. Sci. 17, 892–902 (1964)Google Scholar
  61. Doty, P., Steiner, R. F.: Light scattering and spectrophotometry of colloidal solutions. J. chem. Phys. 18, 1211–1220 (1950)Google Scholar
  62. Eldefrawi, M. E., Eldefrawi, A. T.: Characterization and partial purification of the acetylcholine receptor from Torpedo electroplax. Proc. nat. Acad. Sci. (Wash.) 69, 1776–1780 (1972)Google Scholar
  63. Espejo, R. T., Canelo, E. S.: Properties of bacteriophage PM2: A lipid-containing bacterial virus. Virology 34, 738–747 (1968a)PubMedGoogle Scholar
  64. Espejo, R. T., Canelo, E. S.: Properties and characterization of the host bacterium of bacteriophage PM2. J. Bact. 95, 1887–1891 (1968b)PubMedGoogle Scholar
  65. Espejo, R. T., Canelo, E. S.: Origin of phospholipid in bacteriophage PM2. J. Virol. 2, 1235–1240 (1968c)PubMedGoogle Scholar
  66. Espejo, R. T., Canelo, E. S.: The DNA of bacteriophage PM2. Ultracentrifugal evidence for a circular structure. Virology 37, 495–498 (1969)PubMedGoogle Scholar
  67. Espejo, R. T., Canelo, E. S., Sinsheimer, R. L.: DNA of bacteriophage PM2: a closed circular double-stranded molecule. Proc. nat. Acad. Sci. (Wash.) 63, 1164–1168 (1969)Google Scholar
  68. Espejo, R. T., Canelo, E. S., Sinsheimer, R. L.: Replication of bacteriophage PM2 deoxyribonucleic acid: A closed circular double-stranded molecule. J. molec. Biol. 56, 597–621 (1971a)PubMedGoogle Scholar
  69. Espejo, R. T., Espejo-Canelo, E., Sinsheimer, R. L.: A difference between intracellular and viral supercoiled PM2 DNA. J. molec. Biol. 56, 623–626 (1971b)PubMedGoogle Scholar
  70. Eylar, E. H., Brostoff, S., Hashim, G., Caccam, J., Burnett, P.: Basic Al protein of the myelin membrane. The complete amino acid sequence. J. biol. Chem. 246, 5770–5784 (1971)PubMedGoogle Scholar
  71. Finlay, J. R., Teakle, D. S.: The effect of pH on the particle stability of a phosphotungstate-stained tobacco necrosis virus. J. gen. Virol. 5, 93–96 (1969)Google Scholar
  72. Fish, W. W., Mann, K. G., Tanford, C.: Gel chromatography of proteins in denaturing solvents. Comparison between sodium dodecyl sulfate and guanidine hydrochloride as denaturants. J. biol. Chem. 245, 5166–5168 (1970)PubMedGoogle Scholar
  73. Folch, J., Lees, M.: Proteolipides, a new type of tissue lipoproteins. J. biol. Chem. 191, 807–817 (1951)PubMedGoogle Scholar
  74. Folch, J., Lees, M., Carr, S.: Studies of the chemical composition of the nervous system. Exp. Cell Res., Suppl. 5, 58–71 (1958)Google Scholar
  75. Franklin, R. M.: The significance of lipids in animal viruses. An essay on virus multiplication. In: Progress in medical virology, vol. 4, p. 1–53, ed. by Berger, E., Melnick, J. L. Basel-New York: S. Karger 1962Google Scholar
  76. Franklin, R. M.: PM2 bacteriophage as a model for the structure and synthesis of lipid membranes. In: Membrane-mediated information, vol. 2, p. 57–80, edit, by Kent, P. W., Lancaster: Medical and Technical Publishing Co., Ltd. 1973Google Scholar
  77. Franklin, R. M., Datta, A., Dahlberg, J. E., Braunstein, S. N.: The cell membrane of a marine pseudomonad, Pseudomonas BAL-31; Physical, chemical, and biochemical properties. Biochim. biophys. Acta (Amst.) 233, 521–537 (1971)Google Scholar
  78. Franklin, R. M., Hinnen, R., Schäfer, R., Tsukagoshi, N.: Biochemical aspects of the structure and synthesis of bacteriophage PM2. Proc. Soc. gen. Microbiol., 36–37 (1974)Google Scholar
  79. Franklin, R. M., Salditt, M., Silbert, J. A.: Structure and synthesis of a lipid-containing bacteriophage. I. Growth of bacteriophage PM2 and alterations in nucleic acid metabolism in the infected cell. Virology 38, 627–640 (1969)PubMedGoogle Scholar
  80. Frensdorff, H. K., Watson, M. T., Kauzmann, W.: The kinetics of protein denaturation. IV. The viscosity and gelation of urea solutions of ovalbumin. J. Amer. chem. Soc. 75, 5157–5166(1953)Google Scholar
  81. Fromageot, C., Schnek, G.: Le spectre ultra-violet du lysozyme; avec des considérations sur le spectre ultra-violet de divers acides aminés et de quelques-uns de leur peptides. Biochim. biophys. Acta (Amst.) 6, 113–122 (1950)Google Scholar
  82. Garon, C. F., Moss, B.: Glycoprotein synthesis in cells infected with vaccinia virus. II. A glycoprotein component of the virion. Virology 46, 233–246 (1971)PubMedGoogle Scholar
  83. Gordesky, S. E., Martinetti, G. V.: The asymmetric arrangement of phospholipids in the human erythrocyte membrane. Biochem. biophys. Res. Commun. 50, 1027–1031 (1973)PubMedGoogle Scholar
  84. Gray, H. B., Upholt, W. B., Vinograd, J.: A buoyant method for the determination of the superhelix density of closed circular DNA. J. molec. Biol. 62, 1–19 (1971)PubMedGoogle Scholar
  85. Harrison, S. C., Caspar, D. L. D., Camerini-Otero, R. D., Franklin, R. M.: Lipid and protein arrangement in bacteriophage PM2. Nature (Lond.) New Biol. 229, 197–201 (1971a)Google Scholar
  86. Harrison, S. C., David, A., Jumblatt, J., Darnell, J. E.: Lipid and protein organization in Sindbis virus. J. molec. Biol. 60, 523–528 (1971b)Google Scholar
  87. Helenius, A.: The effects of detergents on membranes and lipoproteins. Ph. D. Thesis. Department of Serology and Bacteriology, University of Helsinki (1973)Google Scholar
  88. Helenius, A., Söderlund, H.: Stepwise dissociation of the Semliki Forest virus membrane with Triton X-100. Biochim. biophys. Acta (Amst.) 307, 287–300 (1973)Google Scholar
  89. Hinnen, R., Schäfer, R., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. XIV. Large scale preparation of virus and localization of the structural proteins. Europ. J. Biochem. In press (1974)Google Scholar
  90. Huang, H. V., Molday, R. S., Dreyer, W. J.: Isoelectric focusing of rod outer segment membrane proteins. FEBS Letters 37, 285–290 (1973)PubMedGoogle Scholar
  91. Hubbell, W. L., McConnel, H. M.: Molecular motion in spin-labeled phospholipids and membranes. J. Amer. chem. Soc. 93, 314–326 (1971)Google Scholar
  92. Israelachvili, J.N.: Theoretical considerations on the asymmetric distribution of charged phospholipid molecules on the inner and outer layers of curved bilayer membranes. Biochim. biophys. Acta (Amst.) 323, 659–663Google Scholar
  93. Jolchine, G., Reiss-Husson, F.: Proteins of R. spheroides Y reaction center: Gel electrophoresis and electrofocusing studies. Biochem. biophys. Res. Commun. 48, 333–340 (1972)PubMedGoogle Scholar
  94. Jones, W. D., Jr.: Studies on the bacteriophage of a natural lysogenic Mycobacterium fortuitum. Amer. Rev. resp. Dis. 108, 1438–1441 (1973)PubMedGoogle Scholar
  95. Jones, W. D., Jr., Beam, R. E.: Lysogeny in the mycobacteria. II. Alterations of bacterial antigens mediated by mycobacteriophage. Canad. J. Microbiol. 15, 1112–1114 (1969)Google Scholar
  96. Jones, W. D., Jr., David, H. L., Beam, R. E.: The occurence of lipids in mycobacteriophage D29 propagated in Mycobacterium smegmatis ATCC 607. Amer. Rev. resp. Dis. 102, 814–817 (1970)PubMedGoogle Scholar
  97. Jones, W. D., Jr., White, A.: Lysogeny in mycobacteria. I. Conversion of colony morphology, nitrate reductase activity and Tween 80 hydrolysis of Mycobacterium sp. ATCC 607 associated with lysogeny. Canad. J. Microbiol. 14, 551–555 (1968)Google Scholar
  98. Kääriäinen, L., Simons, K., Bonsdorff, C.-H. von: Studies in subviral components of Semliki Forest virus. Ann. Med. exp. Fenn. 47, 235–248 (1969)PubMedGoogle Scholar
  99. Keller, J. M., Spear, P. G., Roizman, B.: Proteins specified by Herpes simplex virus. III. Viruses differing in their effects on the social behavior of infected cells specify different membrane glycoproteins. Proc. nat. Acad. Sci. (Wash.) 65, 865–871 (1970)Google Scholar
  100. Kelly, D. C., Robertson, J. S.: Icosahedral cytoplasmic deoxyriboviruses. J. gen. Virol. 20, 17–41 (1973)PubMedGoogle Scholar
  101. Kelly, D. C., Tinsley, T. W.: Iridescent virus replication: a microscope study of Aedes aegypti and Antherea eucalypti cells in culture infected with iridescent virus types 2 and 6. Microbios 9, 75–93 (1974)PubMedGoogle Scholar
  102. Kelly, D. C., Vance, D. E.: The lipid content of two iridescent viruses. J. gen. Virol. 21,417–423 (1973)PubMedGoogle Scholar
  103. Kibler, R. F., Shapira, R., McKneally, S., Jenkins, J., Selden, P., Chou, F.: Encephalitogenic protein: Structure. Science 164, 577–580 (1969)PubMedGoogle Scholar
  104. Klenk, H.-D.: Virus membranes. In: Biological membranes, vol. 2, p. 145–183, ed. by Chapman, D., Wallach, D. F. H. London-New York: Academic Press 1973Google Scholar
  105. Klenk, H.-D., Choppin, P. W.: Plasma membrane lipids and parainfluenza virus assembly. Virology 40, 939–947 (1970 a)PubMedGoogle Scholar
  106. Klenk, H.-D., Choppin, P. W.: Glycosphingolipids of plasma membrane of cultered cells and an enveloped virus (SV5) grown in these cells. Proc. nat. Acad. Sci. (Wash.) 66, 57–64 (1970b)Google Scholar
  107. Kornberg, R. D., McConnell, H. M.: Lateral diffusion of phospholipids in a vesicle membrane. Proc. nat. Acad. Sci. (Wash.) 68, 2564–2568 (1971)Google Scholar
  108. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.) 227, 680–687 (1970)Google Scholar
  109. Laine, R., Kettunen, M.-L., Gahmberg, C. G., Kääriäinen, L., Renkonen, O.: Fatty chains of different lipid classes of Semliki Forest virus and host cell membranes. J. Virol. 10, 433–438 (1972)PubMedGoogle Scholar
  110. Laine, R., Söderlund, H., Renkonen, O.: Chemical composition of Semliki Forest virus. Intervirology 1, 110–118 (1973)PubMedGoogle Scholar
  111. Levine, Y. K., Wilkins, M. H. F.: Structure of oriented lipid bilayers. Nature (Lond.) 230, 69–72 (1971)Google Scholar
  112. Limacher, H., Seelig, J.: Folding of fatty acid chains in liquid crystalline bilayers. Angew. Chem. Internat. Edit. 11, 920–922 (1972)Google Scholar
  113. Maddy, A. H.: A fluorescent label for the outer components of the plasma membrane. Biochim. biophys. Acta (Amst.) 88, 390–399 (1964)Google Scholar
  114. Mankiewicz, E.: The relationship of sarcoidosis to anonymous bacteria. Acta med. scand., Suppl. 425, 68–73 (1964)Google Scholar
  115. Mankiewicz, E., Béland, J.: The role of mycobacteriophages and of cortisone in experimental tuberculosis and sarcoidosis. Amer. Rev. resp. Dis. 89, 707–720 (1964)PubMedGoogle Scholar
  116. Mateu, L., Luzzati, V., London, Y., Gould, R. M., Vosseberg, F. G. A., Olive, J.: X-ray diffraction and electron microscope study of the interactions of myelin components. The structure of a lamellar phase with a 150 to 180 Å repeat distance containing basic proteins and acidic lipids. J. molec. Biol. 75, 697–709Google Scholar
  117. McSharry, J. J., Wagner, R. R.: Lipid composition of purified vesicular stomatitis virus. J. Virol. 7, 59–70 (1971)PubMedGoogle Scholar
  118. Michaelson, D. M., Horwitz, A. F., Klein, P.: Transbilayer asymmetry and surface homogeneity of mixed phospholipids in cosonicated vesicles. Biochemistry 12, 2637–2645 (1973)PubMedGoogle Scholar
  119. Morrison, M., Bayse, G., Danner, D. J.: The role of mammalian peroxides in iodination reactions. In: Biochemistry of the phagocytic process, p. 51–66, ed. by Schultz, J. Amsterdam: North Holland 1970Google Scholar
  120. Moss, B., Rosenblum, E. N., Garon, C. F.: Glycoprotein synthesis in cells infected with Vaccinia virus. Virology 46, 221–232 (1971)PubMedGoogle Scholar
  121. Murphy, J. R.: Erythrocyte metabolism. IV. Equilibration of cholesterol-4-C14 between erythrocytes and variously treated sera. J. Lab. clin. Med. 60, 571–578 (1962)PubMedGoogle Scholar
  122. Nakai, T., Howatson, A. F.: The fine structure of vesicular stomatitis virus. Virology 35, 268–281 (1968)PubMedGoogle Scholar
  123. Nakanishi, H., Iida, Y., Maeshima, K., Teramoto, T.: Isolation and properties of bacteriophages in Vibrio parahaemolyticus. Biken’s J. 9, 149–157 (1966)Google Scholar
  124. Nozaki, Y., Tanford, C.: The solubility of amino acids and related compounds in aqueous urea solutions. J. biol. Chem. 238, 4074–4081 (1963)PubMedGoogle Scholar
  125. Oró, J., Tornabene, T. G., Nooner, D.W., Gelpi, E.: Aliphatic hydrocarbons and fatty acids of some marine and freshwater microorganisms. J. Bact. 93, 1811–1818 (1967)PubMedGoogle Scholar
  126. Overman, T. L., Friend, P. L.: Chloroform sensitivity of streptococcal bacteriophages. Bact. Proc. 271, 174 (1971)Google Scholar
  127. Palmer, F. B., Dawson, R. M. C.: Complex-formation between triphosphoinositide and experimental allergic encephalitogenic protein. Biochem. J. 111, 637–646 (1969)Google Scholar
  128. Patterson, P. H., Lennarz, W. J.: Studies on the membranes of bacilli. I. Phospholipid biosynthesis. J. biol. Chem. 246, 1062–1072 (1971)PubMedGoogle Scholar
  129. Perutz, M. F.: The composition and swelling properties of haemoglobin crystals. Trans. Faraday Soc. 42B, 187–197 (1946)Google Scholar
  130. Pfefferkorn, E. R., Hunter, H. S.: The source of the ribonucleic acid and phospholipid of Sindbis virus. Virology 20, 446–456 (1963)PubMedGoogle Scholar
  131. Phillips, D. R., Morrison, M.: The arrangement of proteins in the human erythrocyte membrane. Biochem. biophys. Res. Commun. 40, 284–288 (1970)PubMedGoogle Scholar
  132. Phillips, D. R., Morrison, M.: Exposed protein on the intact human erythrocyte. Biochemistry (Wash.) 10, 1766–1771 (1971)Google Scholar
  133. Pusey, P. N., Koppel, D. E., Schaefer, D. W., Camerini-Otero, R. D., Koenig, S. H.: Intensity fluctuation spectroscopy of laser light sacttered by solutions of spherical viruses: R17, Qβ, BSV, PM2 and T7. I. The light scattering technique. Biochemistry (Wash.) 13, 952–960 (1974)Google Scholar
  134. Pusey, P. N., Schaefer, D. W., Koppel, D. E., Camerini-Otero, R. D., Franklin, R. M.: A study of the diffusion properties of R17 virus by time-dependent light scattering. J. de Physique. Colloque C 1. supplément au N° 2–3, 33, C1–163-C1–168 (1972)Google Scholar
  135. Quigley, J. P., RifkiN, D. B., Reich, E.: Phospholipid composition of Rous sarcoma virus, host cell membranes and other enveloped RNA viruses. Virology 46, 106–116 (1971)PubMedGoogle Scholar
  136. Rouser, G., Nelson, G. J., Fleischer, S., Simon, G.: Lipid composition of animal cell membranes, organelles and organs. In: Biological membranes, p. 5–69, ed. by Chapman, D. New York-London: Academic Press 1968Google Scholar
  137. Rand, R. P., Luzzati, V.: X-ray diffraction study in water of lipids extracted from human erythrocytes. Biophys. J. 8, 125–137 (1968)PubMedGoogle Scholar
  138. Reed, C. F.: Phospholipid exchange between plasma and erythrocytes in man and dog. J. clin. Invest. 47, 749–760 (1968)PubMedGoogle Scholar
  139. Renkonen, O., Kääräinen, L., Simons, K., Gahmberg, C. G.: The lipid class composition of Semliki Forest virus and of plasma membranes of the host cells. Virology 46, 318–326 (1971)PubMedGoogle Scholar
  140. Riordan, J. F., Vallee, B. L.: Diazonium salts as specific reagents and probes of protein conformation. In: Methods in enzymology, vol. XXV, Enzyme structure, part B, p. 521–531, ed. by Hirs, C. H. W., Timasheff, S.N. New York-London: Academic Press 1972Google Scholar
  141. Sangar, D. V., Rowlands, D. J., Smale, C. J., Brown, F.: Reaction of glutaraldehyde with Foot- and Mouth disease virus. J. gen. Virol. 21, 399–406 (1973)PubMedGoogle Scholar
  142. Salditt, M., Braunstein, S. N., Camerini-Otero, R. D., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. X. Improved techniques for the purification of bacteriophage PM2. Virology 48, 259–262 (1972)PubMedGoogle Scholar
  143. Scandella, C. J., Devaux, P., McConnell, H. M.: Rapid lateral diffusion on phospholipids in rabbit sarcoplasmic reticulum. Proc. nat. Acad. Sci. (Wash.) 69, 2056–2060 (1972)Google Scholar
  144. Scandella, C. J., Schindler, H., Franklin, R. M., Seelig, J.: Structure and synthesis of a lipid-containing bacteriophage. XVI. Acyl chain motion in the PM2 virus membrane. Europ. J. Biochem. In press (1974)Google Scholar
  145. Schäfer, R., Hinnen, R., Franklin, R. M.: Further observations on the structure of the lipid-containing bacteriophage PM2. Nature (Lond.) 248, 681–682 (1974a)Google Scholar
  146. Schäfer, R., Hinnen, R., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. XV. Properties of the structural proteins and distribution of the phospholipid. Europ. J. Biochem. In press (1974b)Google Scholar
  147. Schindler, H., Seelig, J.: ESR spectra of spin labels in lipid bilayers. J. chem. Phys. 59, 1841–1850 (1973)Google Scholar
  148. Seelig, J.: Spin label studies of oriented smectic liquid crystals. (A model system for bilayer membranes.) J. Amer. chem. Soc. 92, 3881–3887 (1970)Google Scholar
  149. Seelig, J.: On the flexibility of hydrocarbon chains in lipid bilayers. J. Amer. chem. Soc. 93, 5017–5022 (1971)Google Scholar
  150. Seelig, J., Hasselbach, W.: A spin label study of sarcoplasmic vesicles. Europ. J. Biochem. 21, 17–21 (1971)PubMedGoogle Scholar
  151. Seelig, J., Limacher, H.: Lipid molecules in lyotropic liquid crystals with cylindrical structure (A spin label study). Molec. Cryst. Liquid Cryst. 25, 105–112 (1974)Google Scholar
  152. Seelig, J., Limacher, H., Bader, P.: Molecular architecture of liquid crystalline bilayers. J. Amer. chem. Soc. 94, 6364–6371 (1972)Google Scholar
  153. Seelig, J., Niederberger, W.: Deuterium labeled lipids as structural probes in liquid bilayers. J. Amer. chem. Soc. 96, 2069–2072 (1974)Google Scholar
  154. Sellers, M. I., Tokunaga, T.: Inactivation of mycobacteriophages by lipid solvents. In: Host-virus relationships in mycobacterium, nocardia, and actinomycetes, p. 134–143. Springfield: Charles C. Thomas 1970Google Scholar
  155. Semancik, J. S., Vidaver, A. K., van Etten, J. L.: Characterization of a segmented double-helical RNA from bacteriophage φ6. J. molec. Biol. 78, 617–625 (1973)PubMedGoogle Scholar
  156. Silbert, J. A., Salditt, M., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. III. Purification of bacteriophage PM2 and some structural studies on the virion. Virology 39, 666–681 (1969)PubMedGoogle Scholar
  157. Simons, K., Helenius, A., Garoff, H.: Solubilization of the membrane proteins from Semliki Forest virus with Triton X-100. J. molec. Biol. 80, 119–133 (1973)PubMedGoogle Scholar
  158. Simpson, R. B., Kauzmann, W.: The kinetics of protein denaturation. I. The behavior of the optical rotation of ovalbumin in urea solutions. J. Amer. chem. Soc. 75, 5139–5152(1953)Google Scholar
  159. Singer, S. J., Nicolson, G. L.: The fluid mosaic model of the structure of cell membranes. Science 175, 720–731 (1972)PubMedGoogle Scholar
  160. Spencer, R.: Indigenous marine bacteriophages. J. Bact. 79, 614 (1960)PubMedGoogle Scholar
  161. Spencer, R.: Bacterial viruses in the sea. In: Symposium on marine microbiology, Chicago 1961, p. 350–365, ed. by Oppenheimer, C. H. Springfield, Illinois: Charles C.Thomas 1963Google Scholar
  162. Strauss, J. H., Jr., Burge, B.W., Pfefferkorn, E. R., Danrell, J. E.: Identification of the membrane protein and “core” protein of Sindbis virus. Proc. nat. Acad. Sci. (Wash.) 59, 533–537 (1968)Google Scholar
  163. Takeya, K., Yoshimura, T., Yamaura, K., Toda, T.: Studies on the biologic properties of mycobacteriophage. Amer. Rev. resp. Dis. 80, 543–553 (1959)PubMedGoogle Scholar
  164. Tanford, C.: Physical chemistry of macromolecules. New York-London: J. Wiley & Sons, Inc. 1961Google Scholar
  165. Tikhonenko, T. I., Koudelka, Ya., Borishpolets, Z. I.: Concentration and purification of phages by the method of column chromatography. Mikrobiologia 32, 614–616 (1963) [Translated from Mikrobiologiya 32, 723–726 (1963)]Google Scholar
  166. Tikhonenkho, T. I., Solov’eva, N. Ya.: The concentration and purification of the Cd phage of Escherichia coli strain CK. Biochemistry (USSR) 26, 686–690 (1961). [Translated from Biokhimiya 26, 794–799 (1961)]Google Scholar
  167. Tikhonenko, T. I., Velikodvorskaya, G. A., Belykh, R. A.: The action of various agents on “SD” phages. Mikrobiologia 33, 732–737 (1964). [Translated from Mikrobiologiya 33, 824–830 (1964)]Google Scholar
  168. Tikhonenko, T. I., Veliskodvorskaya, G. A., Zemtsova, E. V.: Chemical and biological properties of bacteriophage S d. Biochemistry (USSR) 27, 615–622 (1962). [Translated from Biokhimiya 27, 726–733 (1962)]Google Scholar
  169. Tikhonenko, T. I., Vinetskii, Yu. P., Zemtsova, E. V.: A method for obtaining phage-lysates from Escherichia coli S d with high initial titers. Mikrobiologiya 30, 831–833 (1961). [Translated from Mikrobiologiya 30, 1020–1022 (1961)]Google Scholar
  170. Truden, J. L., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. IX. Serological disparity between bacteriophage PM2 and its host cell components. Virology 46, 808–816 (1971)PubMedGoogle Scholar
  171. Tsukagoshi, N., Fox, C. F.: Transport system assembly and the mobility of membrane lipids in Escherichia coli. Biochemistry (Wash.) 12, 2822–2829 (1973)Google Scholar
  172. Tsukagoshi, N., Franklin, R. M.: Structure and synthesis of a lipid-containing bacteriophage. XIII. Studies on the origin of the viral phospholipids. Virology 59, 408–417 (1974)PubMedGoogle Scholar
  173. Van Etten, J. L., Vidaver, A. K., Koski, R. K., Semancik, J. S.: RNA polymerase activity associated with bacteriophage φ6. J.Virol. 12, 464–471 (1973)PubMedGoogle Scholar
  174. Velikodvorskaya, G. A., Chikova, T. S., Lysenko, A. M.: Identification of lipids in S d phage particles. Acta virol. 9, 558 (1965)PubMedGoogle Scholar
  175. Vidaver, A. K., Koski, R. K., Van Etten, J. L.: Bacteriophage φ6: A lipid-containing virus of Pseudomonas phaseolicola. J. Virol. 11, 799–805 (1973)PubMedGoogle Scholar
  176. White, D. A., Albright, F. R., Lennarz, W. J., Schnaitman, C. A.: Distribution of phospholipid-synthesizing enzymes in the wall and membrane subfractions of the envelope of Escherichia coli. Biochim. biophys. Acta (Amst.) 249, 636–642 (1971)Google Scholar
  177. Wirtz, K. W. A., Zilversmit, D. B.: Participation of soluble liver proteins in the exchange of membrane phospholipids. Biochim. biophys. Acta (Amst.) 193, 105–116 (1969)Google Scholar
  178. Wolfgram, F., Kotorii, K.: The composition of the myelin proteins of the central nervous system. J. Neurochem. 15, 1281–1290 (1968a)PubMedGoogle Scholar
  179. Wolfgram, F., Kotorii, K.: The composition of the myelin proteins of the peripheral nervous system. J. Neurochem. 15, 1291–1295 (1968b)PubMedGoogle Scholar
  180. Wouters, M., Miller, A. O. A., Fenwick, M. L.: Distortion of poliovirus particles by fixation with formaldehyde. J. gen. Virol. 18, 211–214 (1973)PubMedGoogle Scholar
  181. Zee, Y. C., Hackett, A. J., Tolems, L.: Vesicular stomatitis virus maturation sites in six different host cells. J. gen. Virol. 7, 95–102 (1970)PubMedGoogle Scholar
  182. Zilversmit, D. B.: Stimulation of phospholipid exchange between mitochondria and artificially prepared phospholipid aggregates by a soluble fraction from liver. J. biol. Chem. 246, 2645–2649 (1971)PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1974

Authors and Affiliations

  • Richard M. Franklin
    • 1
  1. 1.Abteilung für StrukturbiologieBiozentrum der Universität BaselBaselSwitzerland

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