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Molecular architecture of bacteriophage T4

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Abstract

In studying bacteriophage T4—one of the basic models of molecular biology for several decades—there has come a Renaissance, and this virus is now actively used as object of structural biology. The structures of six proteins of the phage particle have recently been determined at atomic resolution by X-ray crystallography. Three-dimensional reconstruction of the infection device—one of the most complex multiprotein components—has been developed on the basis of cryo-electron microscopy images. The further study of bacteriophage T4 structure will allow a better understanding of the regulation of protein folding, assembly of biological structures, and also mechanisms of functioning of the complex biological molecular machines.

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REFERENCES

  1. E. Kellenberger (1990) Eur. J. Biochem. 190 233–248

    Google Scholar 

  2. P. G. Leiman S. Kanamaru V. V. Mesyanzhinov F. Arisaka M. G. Rossmann (2003) Cell Mol Life Sci. 60 2356–2370

    Google Scholar 

  3. E. Kutter B. Guttman D. Batts S. Peterson T. Djavakhishvili T. Stidham F. Arisaka V. Mesyanzhinov W. Ruger G. Mosig (1993) NoChapterTitle S. J. O’Brien (Eds) Genomic Maps Cold Spring Harbor Laboratory Press N. Y. 1–27

    Google Scholar 

  4. E. S. Miller E. Kutter G. Mosig F. Arisaka T. Kunisawa W. Ruger (2003) Microbiol. Mol. Biol. Rev. 67 86–156

    Google Scholar 

  5. W. B. Wood R. S. Edgar J. King I. Lielausis M. Henninger (1968) Fed. Proc. 27 1160–1166

    Google Scholar 

  6. E. Kellenberger (1976) Phylos. Trans. R. Soc. Lond. B. Biol. Sci. 276 3–13

    Google Scholar 

  7. W. B. Wood (1980) Q. Rev. Biol. 55 353–367

    Google Scholar 

  8. T. S. Baker N. H. Olson S. D. Fuller (1999) Microbiol. Mol. Biol. Rev. 63 862–922

    Google Scholar 

  9. S. D. Fuller J. A. Berriman S. J. Butcher B. E. Gowen (1995) Cell 81 715–725

    Google Scholar 

  10. J. B. Heymann N. Cheng W. W. Newcomb B. L. Trus J. C. Brown A. C. Steven (2003) Nat. Struct. Biol. 10 334–341

    Google Scholar 

  11. S. Kanamaru P. G. Leiman V. A. Kostyuchenko P. R. Chipman V. V. Mesyanzhinov F. Arisaka M. G. Rossmann (2002) Nature 415 553–557

    Google Scholar 

  12. V. A. Kostyuchenko P. G. Leiman P. R. Chipman S. Kanamaru M. J. Raaij Particlevan F. Arisaka V. V. Mesyanzhinov M. G. Rossmann (2003) Nat. Struct. Biol. 10 688–693

    Google Scholar 

  13. A. Fokine P. R. Chipman P. G. Leiman V. V. Mesyanzhinov V. B. Rao M. G. Rossmann (2004) Proc. Natl. Acad. Sci. USA 101 6003–6008

    Google Scholar 

  14. Leiman, P. G., Chipman, P. R., Kostyuchenko, V. A., Mesyanzhinov, V. V., and Rossmann, M. G. (2004) Cell, in press.

  15. U. Aebi R. K. L. Bijlenga J. Broek Particlevan den R. Broek Particlevan den F. Eiserling C. Kellenberger E. Kellenberger V. Mesyanzhinov L. Müller M. Showe R. Smith A. Steven (1974) J. Supramol. Struct. 2 253–275

    Google Scholar 

  16. D. L. D. Caspar A. Klug (1962) Cold Spring Harbor Symp. Quant. Biol. 27 1–24

    Google Scholar 

  17. N. H. Olson M. Gingery F. A. Eiserling T. S. Baker (2001) Virology 279 385–391

    Google Scholar 

  18. T. Ishii Y. Yamaguchi M. Yanagida (1978) J. Mol. Biol. 120 533–544

    Google Scholar 

  19. A. Richardson S. J. Landry C. Georgopoulos (1998) Trends Biochem. Sci. 23 138–143

    Google Scholar 

  20. D. Ang F. Keppel G. Klein A. Richardson C. Georgopoulos (2000) Ann. Rev. Gen. 34 439–456

    Google Scholar 

  21. J. F. Hunt S. M. Vies Particlevan der L. Henry J. Deisenhofer (1997) Cell 90 361–371

    Google Scholar 

  22. U. K. Laemmli E. Molbert M. Showe E. Kellenberger (1970) J. Mol. Biol. 49 99–113

    Google Scholar 

  23. C. L. Hsiao L. W. Black (1978) Virology 91 15–25

    Google Scholar 

  24. L. Onorato B. Stirmer M. K. Showe (1978) J. Virol. 27 409–426

    Google Scholar 

  25. M. K. Showe L. W. Black (1973) J. Mol. Biol. 107 35–54

    Google Scholar 

  26. T. Lane F. Eiserling (1990) J. Struct. Biol. 104 9–23

    Google Scholar 

  27. L. W. Black M. K. Showe A. C. Steven (1994) NoChapterTitle J. D. Karam (Eds) Molecular Biology of Bacteriophage T4 American Society for Microbiology Washington, D. C. 218–258

    Google Scholar 

  28. L. Onorato B. Stirmer M. K. Showe (1978) J. Virol. 27 409–426

    Google Scholar 

  29. A. H. Doermann F. A. Eiserling L. Boeher (1973) J. Virol. 12 374–385

    Google Scholar 

  30. L. E. Donate H. Murialdo J. L. Carrascosa (1990) Virology 179 936–940

    Google Scholar 

  31. A. A. McNicol L. D. Simon L. W. Black (1997) J. Mol. Biol. 116 261–283

    Google Scholar 

  32. J. R. Paulson S. Lazaroff U. K. Laemmli (1976) J. Mol. Biol. 103 99–109

    Google Scholar 

  33. T. A. Volker J. Gafner T. A. Bickle M. K. Showe (1982) J. Mol. Biol. 161 479–489

    Google Scholar 

  34. T. A. Volker A. Kuhn M. K. Showe T. A. Bickle (1982) J. Mol. Biol. 161 491–504

    Google Scholar 

  35. B. Keller J. Dubochet M. Andrian M. Maeder M. Wurtz E. Kellenberger (1988) J. Virol. 62 2960–2969

    Google Scholar 

  36. A. Engel R. Driel Particlevan R. Driedonks (1982) J. Ultrastruct. Res. 80 12–22

    Google Scholar 

  37. V. V. Mesyanzhinov B. N. Sobolev E. I. Marusich A. G. Prilipov V. P. Efimov (1990) J. Struct. Biol. 104 24–31

    Google Scholar 

  38. B. Keller T. A. Bickle (1986) Gene 49 245–251

    Google Scholar 

  39. A. V. Kaliman M. A. Khasanova V. M. Kryukov V. I. Tanyashin A. A. Bayev (1990) Nucleic Acids Res. 18 4277

    Google Scholar 

  40. M. L. Parker A. C. Christensen A. Boosman J. Stockard E. T. Young A. H. Doermann (1984) J. Mol. Biol. 180 399–416

    Google Scholar 

  41. U. Aebi R. Driel Particlevan R. K. L. Bijlenga B. Heggeler ParticleTen R. Broek Particlevan der A. Steven P. R. Smith (1977) J. Mol. Biol. 110 687–698

    Google Scholar 

  42. V. B. Rao L. W. Black (1988) J. Mol. Biol. 200 475–488

    Google Scholar 

  43. H. Lin M. N. Simon L. W. Black (1997) J. Biol. Chem. 272 3495–3501

    Google Scholar 

  44. H. Lin L. W. Black (1998) Virology 242 118–127

    Google Scholar 

  45. D. Kuebler V. B. Rao (1998) J. Mol. Biol. 281 803–814

    Google Scholar 

  46. G. Leffers V. B. Rao (2000) J. Biol. Chem. 275 37127–37136

    Google Scholar 

  47. N. Malys D. Y. Chang R. G. Baumann D. Xie L. W. Black (2002) J. Mol. Biol. 319 289–304

    Google Scholar 

  48. R. W. Hendrix (1978) Proc. Natl. Acad. Sci. USA 75 4779–4783

    Google Scholar 

  49. A. A. Simpson Y. Tao P. G. Leiman M. O. Badasso Y. He P. J. Jardine N. H. Olson M. C. Morais S. Grimes D. L. Anderson T. S. Baker M. G. Rossmann (2000) Nature 408 745–750

    Google Scholar 

  50. K. Iwasaki B. L. Trus P. T. Wingfield N. Cheng G. Campusano V. B. Rao A. C. Steven (2000) Virology 271 321–333

    Google Scholar 

  51. N. H. Olson M. Gingery F. A. Eiserling T. S. Baker (2001) Virology 279 385–391

    Google Scholar 

  52. S. P. Leibo E. Kellenberger C. Kelenberger Particlevan der Kamp T. G. Frey C. M. Sternberg (1979) J. Virol. 30 327–338

    Google Scholar 

  53. W. R. Wikoff L. Liljas R. L. Duda H. Tsuruta R. W. Hendrix J. E. Johnson (2000) Science 289 2129–2133

    Google Scholar 

  54. E. V. Orlova P. Dube E. Beckmann F. Zemlin R. Lurz T. A. Trautner P. Tavares M. Heel Particlevan (1999) Nat. Struct. Biol. 6 842–846

    Google Scholar 

  55. Y. Kikuchi J. King (1975) J. Mol. Biol. 99 645–672

    Google Scholar 

  56. Y. Kikuchi J. King (1975) J. Mol. Biol. 99 673–694

    Google Scholar 

  57. Y. Kikuchi J. King (1975) J. Mol. Biol. 99 695–716

    Google Scholar 

  58. M. F. Plishker M. Chidambaram P. B. Berget (1983) J. Mol. Biol. 170 119–135

    Google Scholar 

  59. N. R. Watts D. H. Coombs (1990) J. Virol. 64 143–154

    Google Scholar 

  60. P. L. Ferguson D. H. Coombs (2000) J. Mol. Biol. 297 99–117

    Google Scholar 

  61. L. Zhao S. Takeda P. G. Leiman F. Arisaka (2000) Biochim. Biophys. Acta 1479 286–292

    Google Scholar 

  62. D. H. Coombs F. Arisaka (1994) NoChapterTitle J. D. Karam (Eds) Molecular Biology of Bacteriophage American Society for Microbiology Washington, D. C. 259–281

    Google Scholar 

  63. N. K. Abuladze M. Gingery J. Tsai F. A. Eiserling (1994) Virology 199 301–310

    Google Scholar 

  64. E. Kellenberger E. Boy Particlede la Tour (1964) J. Ultrastruct. Res. 11 545–563

    Google Scholar 

  65. M. F. Moody (1973) J. Mol. Biol. 80 613–635

    Google Scholar 

  66. M. F. Moody L. Makowski (1981) J. Mol. Biol. 150 217 244

    Google Scholar 

  67. L. Zhao S. Kanamaru C. Chaidirek F. Arisaka (2003) J. Bacteriol. 185 1693–1700

    Google Scholar 

  68. E. Kellenberger A. Bolle E. Boy Particlede la Tour R. H. Epstein N. C. Franklin N. K. Jerne A. Reale-Scafati J. Sechaud I. Benet D. Goldstein M. A. Lauffer (1965) Virology 26 419–440

    Google Scholar 

  69. E. Goldberg L. Grinius L. Letellier (1994) NoChapterTitle J. D. Karam (Eds) Molecular Biology of Bacteriophage T4 American Society for Microbiology Washington, D. C. 347–356

    Google Scholar 

  70. W. B. Wood F. A. Eiserling R. A. Crowther (1994) NoChapterTitle J. D. Karam (Eds) Molecular Biology of Bacteriophage T4 American Society for Microbiology Washington, D. C. 282–290

    Google Scholar 

  71. M. E. Cerritelli J. S. Wall M. N. Simon J. F. Conway A. C. Steven (1996) J. Mol. Biol. 260 767–780

    Google Scholar 

  72. U. Henning S. Hashemolhosseini (1994) NoChapterTitle J. D. Karam (Eds) Molecular Biology of Bacteriophage T4 American Society for Microbiology Washington, D. C. 291–298

    Google Scholar 

  73. W. S. Mason R. Haselkorn (1972) J. Mol. Biol. 66 445–469

    Google Scholar 

  74. A. M. Makhov B. L. Trus J. F. Conway M. N. Simon T. G. Zurabishvili V. V. Mesyanzhinov A. C. Steven (1993) Virology 194 117–127

    Google Scholar 

  75. M. J. Raaij ParticleVan G. Schoehn M. R. Burda S. Miller (2001) J. Mol. Biol. 314 1137–1146

    Google Scholar 

  76. E. Thomassen G. Gielen M. Schutz G. Schoehn J. P. Abrahams S. Miller M. J. Raaij Particlevan (2003) J. Mol. Biol. 331 361–373

    Google Scholar 

  77. M. J. Raaij ParticleVan A. Mitraki G. Lavigne S. Cusack (1999) Nature 401 935–938

    Google Scholar 

  78. F. K. Athappilly R. Murali J. J. Rux Z. Cai R. M. Burnett (1994) J. Mol. Biol. 242 430–455

    Google Scholar 

  79. Y. Liu D. Eisenberg (2002) Prot. Sci. 11 1285–1299

    Google Scholar 

  80. Y. Liu G. Gotte M. Libonati D. Eisenberg (2002) Prot. Sci. 11 371–380

    Google Scholar 

  81. S. Steinbacher R. Seckler S. Miller B. Steipe R. Huber P. Reinemer (1994) Science 265 383–386

    Google Scholar 

  82. V. P. Efimov I. V. Nepluev B. N. Sobolev T. G. Zurabishvili T. Schulthess A. Lustig J. Engel M. Haener U. Aebi S. Yu. Venyaminov S. A. Potekhin V. V. Mesyanzhinov (1994) J. Mol. Biol. 242 470–486

    Google Scholar 

  83. S. P. Boudko Y. Y. Londer A. V. Letarov N. V. Sernova J. Engel V. V. Mesyanzhinov (2002) Eur. J. Biochem. 269 833–841

    Google Scholar 

  84. M.-H. Yu J. King (1984) Proc. Natl. Acad. Sci. USA 81 6584–6588

    Google Scholar 

  85. A. R. Panchenko Z. Luthey-Schulten P. G. Wolynes (1996) Proc. Natl. Acad. Sci. USA 93 2008–2013

    Google Scholar 

  86. K. Inaba N. Kobayashi A. R. Fersht (2000) J. Mol. Biol. 302 219–233

    Google Scholar 

  87. H. Yanagawa K. Yoshida C. Torigoe J. S. Prak K. Sato T. Shirai M. Go (1993) J. Biol. Chem. 268 5861–5865

    Google Scholar 

  88. K. Wakasugi K. Isimori K. Imai Y. Wada I. Morishima (1994) J. Biol. Chem. 269 18750–18756

    Google Scholar 

  89. B. E. Terzaghi E. Terzaghi D. Coombs (1979) J. Mol. Biol. 127 1–14

    Google Scholar 

  90. M. P. Coombs F. A. Eiserling (1977) J. Mol. Biol. 116 375–405

    Google Scholar 

  91. M. P. Conley W. B. Wood (1975) Proc. Natl. Acad. Sci. USA 72 3701–3705

    Google Scholar 

  92. B. N. Sobolev V. V. Mesyanzhinov (1991) J. Biomol. Struct. Dyn. 8 953–965

    Google Scholar 

  93. C. Cohen D. A. Parry (1994) Science 263 488–489

    Google Scholar 

  94. S. V. Strelkov Y. Tao M. G. Rossmann L. P. Kurochkina M. M. Shneider V. V. Mesyanzhinov (1997) Virology 219 190–194

    Google Scholar 

  95. Y. Tao S. V. Strelkov V. V. Mesyanzhinov M. G. Rossmann (1997) Structure 5 789–798

    Google Scholar 

  96. Strelkov, S. V., Tao, Y., Shneider, M. M., Mesyanzhinov, V. V., and Rossmann, M. G. (1998) Acta Crystallogr., D54, 805–816.

  97. S. P. Boudko S. V. Strelkov J. Engel J. Stetefeld (2004) J. Mol. Biol. 339 927–935

    Google Scholar 

  98. A. V. Letarov Y. Y. Londer S. P. Boudko V. V. Mesyanzhinov (1999) Biochemistry (Moscow) 64 817–823

    Google Scholar 

  99. S. Boudko S. Frank R. A. Kammerer J. Stetefeld T. Schulthess R. Landwehr A. Lustig H. P. Bachinger J. Engel (2002) J. Mol. Biol. 317 459–470

    Google Scholar 

  100. K. A. Miroshnikov E. I. Marusich M. E. Cerritelli N. Cheng C. C. Hyde A. C. Steven V. V. Mesyanzhinov (1998) Prot. Eng. 11 329–332

    Google Scholar 

  101. K. A. Miroshnikov N. V. Sernova M. M. Shneider V. V. Mesyanzhinov (2000) Biochemistry (Moscow) 65 1346–1351

    Google Scholar 

  102. S. Frank R. A. Kammerer D. Mechling T. Schulthess R. Landwehr J. Bann Y. Guo A. Lustig H. P. Bachinger J. Engel (2001) J. Mol. Biol. 308 1081–1089

    Google Scholar 

  103. J. Stetefeld S. Frank M. Jenny T. Schulthess R. A. Kammerer S. Boudko R. Landwehr K. Okuyama J. Engel (2003) Structure 11 339–346

    Google Scholar 

  104. V. Krasnykh N. Belousova N. Korokhov G. Mikheeva D. T. Curiel (2001) J. Virol. 75 4176–4183

    Google Scholar 

  105. E. A. Kashentseva T. Seki D. T. Curiel I. P. Dmitriev (2002) Cancer Res. 62 609–616

    Google Scholar 

  106. X. Yang J. Lee E. M. Mahony P. D. Kwong R. Wyatt J. Sodroski (2002) J. Virol. 76 4634–4642

    Google Scholar 

  107. R. A. Crowther E. V. Lenk Y. Kikuchi J. King (1977) J. Mol. Biol. 116 489–523

    Google Scholar 

  108. N. R. Watts D. H. Coombs (1990) J. Virol. 64 143–154

    Google Scholar 

  109. N. R. Watts J. Hainfeld D. H. Coombs (1990) J. Mol. Biol. 216 315–325

    Google Scholar 

  110. R. A. Crowther (1980) J. Mol. Biol. 137 159–174

    Google Scholar 

  111. W. B. Wood M. P. Conley H. L. Lyle R. C. Dickson (1978) J. Biol. Chem. 253 2437–2445

    Google Scholar 

  112. G. A. Navruzbekov L. P. Kurochkina V. A. Kostyuchenko T. G. Zurabishvili S. Y. Venyaminov V. V. Mesyanzhinov (1999) Biochemistry (Moscow) 64 1266–1272

    Google Scholar 

  113. V. A. Kostyuchenko G. A. Navruzbekov L. P. Kurochkina S. V. Strelkov V. V. Mesyanzhinov M. G. Rossmann (1999) Struct. Fold. Des. 7 1213–1222

    Google Scholar 

  114. S. Betts J. King (1999) Struct. Fold. Des. 7 R131–R139

    Google Scholar 

  115. M. G. Rossmann J. E. Johnson (1989) Annu Rev. Biochem. 58 533–573

    Google Scholar 

  116. N. Nandhagopal A. A. Simpson J. R. Gurnon X. Yan T. S. Baker M. V. Graves J. L. Etten Particlevan M. G. Rossmann (2002) Proc. Natl. Acad. Sci. USA 99 14758–14763

    Google Scholar 

  117. L. Liljas (1999) Curr. Opin. Struct. Biol. 9 129–134

    Google Scholar 

  118. P. G. Leiman V. A. Kostyuchenko M. M. Shneider L. P. Kurochkina V. V. Mesyanzhinov M. G. Rossmann (2000) J. Mol. Biol. 301 975–985

    Google Scholar 

  119. L. Holm C. Sander (1993) J. Mol. Biol. 233 123–138

    Google Scholar 

  120. M. M. Shneider S. P. Boudko A. Lustig V. V. Mesyanzhinov (2001) Biochemistry (Moscow) 66 693–697

    Google Scholar 

  121. C. P. Georgopoulos M. Georgiou G. Selzer H. Eisen (1977) Experientia 33 1157–1158

    Google Scholar 

  122. P. G. Leiman M. M. Shneider V. A. Kostyuchenko P. R. Chipman V. V. Mesyanzhinov M. G. Rossmann (2003) J. Mol. Biol. 328 821–833

    Google Scholar 

  123. H. Nakagawa F. Arisaka S. Ishii (1985) J. Virol. 54 460–466

    Google Scholar 

  124. B. W. Matthews S. J. Remington (1974) Proc. Natl. Acad. Sci. USA 71 4178–4182

    Google Scholar 

  125. S. Kanamaru N. C. Gassner N. Ye S. Takeda F. Arisaka (1999) J. Bacteriol. 181 2739–2744

    Google Scholar 

  126. A. G. Murzin C. Chothia (1992) Curr. Opin. Struct. Biol. 2 895–903

    Google Scholar 

  127. R. Kuroki L. H. Weaver B. W. Matthews (1993) Science 262 2030–2033

    Google Scholar 

  128. R. Seckler (1998) J. Struct. Biol. 122 216–222

    Google Scholar 

  129. E. Meezan W. B. Wood (1971) J. Mol. Biol. 58 685–692

    Google Scholar 

  130. J. King (1971) J. Mol. Biol. 58 693–709

    Google Scholar 

  131. R. L. Duda M. Gingery F. A. Eiserling (1986) Virology 151 296–314

    Google Scholar 

  132. C. M. To E. Kellenberger A. Eisenstark (1969) J. Mol. Biol. 46 493–511

    Google Scholar 

  133. E. Kellenberger E. Stauffer M. Haner A. Lustig D. Karamata (1996) Biophys. Chem. 59 41–59

    Google Scholar 

  134. L. Letellier P. Boulanger M. de Frutos P. Jacquot (2003) Res. Microbiol. 154 283–287

    Google Scholar 

  135. S. Brenner G. Streisenger R. W. Horne S. P. Champe L. Barnett S. Benzer M. W. Rees (1959) J. Mol. Biol. 1 281–292

    Google Scholar 

  136. D. DeRosier A. Klug (1968) Nature 217 130–134

    Google Scholar 

  137. L. Amos A. Klug (1975) J. Mol. Biol. 99 51–73

    Google Scholar 

  138. B. F. Poglazov (1973) Monogr. Dev. Biol. 7 1–105

    Google Scholar 

  139. I. I. Serysheva A. I. Tourkin S. Y. Venyaminov B. F. Poglazov (1984) J. Mol. Biol. 179 565–569

    Google Scholar 

  140. M. G. Rossmann V. V. Mesyanzhinov F. Arisaka P. G. Leiman (2004) Curr. Opin. Struct. Biol. 14 171–180

    Google Scholar 

  141. B. F. Poglazov A. V. Efimov S. Marco J. Carrascosa T. A. Kuznetsova L. G. Aijrich L. P. Kurochkina V. V. Mesyanzhinov (1999) J. Struct. Biol. 127 224–230

    Google Scholar 

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Translated from Biokhimiya, Vol. 69, No. 11, 2004, pp. 1463–1476.

Original Russian Text Copyright © 2004 by Mesyanzhinov, Leiman, Kostyuchenko, Kurochkina, Miroshnikov, Sykilinda, Shneider.

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Mesyanzhinov, V.V., Leiman, P.G., Kostyuchenko, V.A. et al. Molecular architecture of bacteriophage T4. Biochemistry (Moscow) 69, 1190–1202 (2004). https://doi.org/10.1007/s10541-005-0064-9

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