Viral Molecular Machines pp 423-439

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 726)

Procapsid Assembly, Maturation, Nuclear Exit: Dynamic Steps in the Production of Infectious Herpesvirions

  • Giovanni Cardone
  • J. Bernard Heymann
  • Naiqian Cheng
  • Benes L. Trus
  • Alasdair C. Steven


Herpesviruses, a family of animal viruses with large (125–250 kbp) linear DNA genomes, are highly diversified in terms of host range; nevertheless, their virions conform to a common architecture. The genome is confined at high density within a thick-walled icosahedral capsid with the uncommon (among viruses, generally) but unvarying triangulation number T = 16. The envelope is a membrane in which some 11 different viral glycoproteins are implanted. Between the capsid and the envelope is a capacious compartment called the tegument that accommodates ∼20–40 different viral proteins (depending on which virus) destined for delivery into a host cell. A strong body of evidence supports the hypothesis that herpesvirus capsids and those of tailed bacteriophages stem from a distant common ancestor, whereas their radically different infection apparatuses – envelope on one hand and tail on the other – reflect subsequent coevolution with divergent hosts. Here we review the molecular components of herpesvirus capsids and the mechanisms that regulate their assembly, with particular reference to the archetypal alphaherpesvirus, herpes simplex virus type 1; assess their duality with the capsids of tailed bacteriophages; and discuss the mechanism whereby, once DNA packaging has been completed, herpesvirus nucleocapsids exit from the nucleus to embark on later stages of the replication cycle.


  1. Agirrezabala X, Martin-Benito J, Valle M, Gonzalez JM, Valencia A, Valpuesta JM, Carrascosa JL (2005) Structure of the connector of bacteriophage T7 at 8 Å resolution: structural homologies of a basic component of a DNA translocating machinery. J Mol Biol 347(5):895–902PubMedCrossRefGoogle Scholar
  2. Agirrezabala X, Velazquez-Muriel JA, Gomez-Puertas P, Scheres SH, Carazo JM, Carrascosa JL (2007) Quasi-atomic model of bacteriophage T7 procapsid shell: insights into the structure and evolution of a basic fold. Structure 15(4):461–472PubMedCrossRefGoogle Scholar
  3. Baines JD (2007) Chapter 11. Envelopment of herpes simplex virus nucleocapsids at the inner membrane. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, CambridgeGoogle Scholar
  4. Baker ML, Jiang W, Rixon FJ, Chiu W (2005) Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 79(23):14967–14970PubMedCrossRefGoogle Scholar
  5. Baker ML, Jiang W, Wedemeyer WJ, Rixon FJ, Baker D, Chiu W (2006) Ab initio modeling of the herpesvirus VP26 core domain assessed by CryoEM density. PLoS Comput Biol 2(10):e146PubMedCrossRefGoogle Scholar
  6. Bamford DH, Grimes JM, Stuart DI (2005) What does structure tell us about virus evolution? Curr Opin Struct Biol 15(6):655–663PubMedCrossRefGoogle Scholar
  7. Benson SD, Bamford JKH, Bamford DH, Burnett RM (1999) Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98(6):825–833PubMedCrossRefGoogle Scholar
  8. Booy FP, Newcomb WW, Trus BL, Brown JC, Baker TS, Steven AC (1991) Liquid-crystalline, phage-like, packing of encapsidated DNA in herpes simplex virus. Cell 64:1007–1015PubMedCrossRefGoogle Scholar
  9. Booy FP, Trus BL, Davison AJ, Steven AC (1996) The capsid architecture of channel catfish virus, an evolutionarily distant herpesvirus, is largely conserved in the absence of discernible sequence homology with herpes simplex virus. Virology 215:134–141PubMedCrossRefGoogle Scholar
  10. Bowman BR, Baker ML, Rixon FJ, Chiu W, Quiocho FA (2003) Structure of the herpesvirus major capsid protein. EMBO J 22(4):757–765PubMedCrossRefGoogle Scholar
  11. Bowman BR, Welschhans RL, Jayaram H, Stow ND, Preston VG, Quiocho FA (2006) Structural characterization of the UL25 DNA-packaging protein from herpes simplex virus type 1. J Virol 80(5):2309–2317PubMedCrossRefGoogle Scholar
  12. Briggs JA, Riches JD, Glass B, Bartonova V, Zanetti G, Krausslich HG (2009) Structure and assembly of immature HIV. Proc Natl Acad Sci USA 106(27):11090–11095PubMedCrossRefGoogle Scholar
  13. Britt B (2007) Chapter 20. Maturation and egress. In: Arvin A, Campadelli-Fiume G, Mocarski E et al (eds) Human herpesviruses: biology, therapy and immunoprophylaxis. Cambridge University Press, CambridgeGoogle Scholar
  14. Cardone G, Winkler DC, Trus BL, Cheng N, Heuser JE, Newcomb WW, Brown JC, Steven AC (2007) Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361(2):426–434PubMedCrossRefGoogle Scholar
  15. Cerritelli ME, Cheng N, Rosenberg AH, McPherson CE, Booy FP, Steven AC (1997) Encapsidated conformation of bacteriophage T7 DNA. Cell 91:271–280PubMedCrossRefGoogle Scholar
  16. Chang JT, Schmid MF, Rixon FJ, Chiu W (2007) Electron cryotomography reveals the portal in the herpesvirus capsid. J Virol 81(4):2065–2068PubMedCrossRefGoogle Scholar
  17. Chen DH, Jakana J, McNab D, Mitchell J, Zhou ZH, Dougherty M, Chiu W, Rixon FJ (2001) The pattern of tegument-capsid interaction in the herpes simplex virus type 1 virion is not influenced by the small hexon-associated protein VP26. J Virol 75(23):11863–11867PubMedCrossRefGoogle Scholar
  18. Chen DH, Baker ML, Hryc CF, DiMaio F, Jakana J, Wu W, Dougherty M, Haase-Pettingell C, Schmid MF, Jiang W, Baker D, King JA, Chiu W (2011) Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc Natl Acad Sci USA 108(4):1355–1360PubMedCrossRefGoogle Scholar
  19. Cheng H, Shen N, Pei J, Grishin NV (2004) Double-stranded DNA bacteriophage prohead protease is homologous to herpesvirus protease. Protein Sci 13(8):2260–2269PubMedCrossRefGoogle Scholar
  20. Cockrell SK, Sanchez ME, Erazo A, Homa FL (2009) Role of the UL25 protein in herpes simplex virus DNA encapsidation. J Virol 83(1):47–57PubMedCrossRefGoogle Scholar
  21. Cockrell SK, Huffman JB, Toropova K, Conway JF, Homa FL (2011) Residues of the UL25 protein of herpes simplex virus that are required for its stable interaction with capsids. J Virol 85(10):4875–4887PubMedCrossRefGoogle Scholar
  22. Coller KE, Lee JI, Ueda A, Smith GA (2007) The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J Virol 81(21):11790–11797PubMedCrossRefGoogle Scholar
  23. Conway JF, Wikoff WR, Cheng N, Duda RL, Hendrix RW, Johnson JE, Steven AC (2001) Virus maturation involving large subunit rotations and local refolding. Science 292(5517):744–748PubMedCrossRefGoogle Scholar
  24. Conway JF, Cockrell SK, Copeland AM, Newcomb WW, Brown JC, Homa FL (2010) Labeling and localization of the herpes simplex virus capsid protein UL25 and its interaction with the two triplexes closest to the penton. J Mol Biol 397(2):575–586PubMedCrossRefGoogle Scholar
  25. Davison AJ, Trus BL, Cheng N, Steven AC, Watson MS, Cunningham C, Le Deuff RM, Renault T (2005) A novel class of herpesvirus with bivalve hosts. J Gen Virol 86(Pt 1):41–53PubMedCrossRefGoogle Scholar
  26. Deng B, O’Connor CM, Kedes DH, Zhou ZH (2007) Direct visualization of the putative portal in the Kaposi’s ­sarcoma-associated herpesvirus capsid by cryoelectron tomography. J Virol 81(7):3640–3644PubMedCrossRefGoogle Scholar
  27. Dokland T (1999) Scaffolding proteins and their role in viral assembly. Cell Mol Life Sci 56(7–8):580–603PubMedCrossRefGoogle Scholar
  28. Duda RL (1998) Protein chainmail: catenated protein in viral capsids. Cell 94(1):55–60PubMedCrossRefGoogle Scholar
  29. Duda RL, Hendrix RW, Huang WM, Conway JF (2006) Shared architecture of bacteriophage SPO1 and herpesvirus capsids. Curr Biol 16(1):R11–R13PubMedCrossRefGoogle Scholar
  30. Duda RL, Ross PD, Cheng N, Firek BA, Hendrix RW, Conway JF, Steven AC (2009) Structure and energetics of encapsidated DNA in bacteriophage HK97 studied by scanning calorimetry and cryo-electron microscopy. J Mol Biol 391(2):471–483PubMedCrossRefGoogle Scholar
  31. Fokine A, Chipman PR, Leiman PG, Mesyanzhinov VV, Rao VB, Rossmann MG (2004) Molecular architecture of the prolate head of bacteriophage T4. Proc Natl Acad Sci USA. 101(16):6003–6008PubMedCrossRefGoogle Scholar
  32. Friedmann A, Coward JE, Rosenkranz HS, Morgan C (1975) Electron microscopic studies on assembly of herpes simplex virus upon removal of hydroxyurea block. J Gen Virol 26:171–181PubMedCrossRefGoogle Scholar
  33. Gertsman I, Gan L, Guttman M, Lee K, Speir JA, Duda RL, Hendrix RW, Komives EA, Johnson JE (2009) An unexpected twist in viral capsid maturation. Nature 458(7238):646–650PubMedCrossRefGoogle Scholar
  34. Grünewald K, Desai P, Winkler DC, Heymann JB, Belnap DM, Baumeister W, Steven AC (2003) Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302(5649):1396–1398PubMedCrossRefGoogle Scholar
  35. Guo H, Shen S, Wang L, Deng H (2010) Role of tegument proteins in herpesvirus assembly and egress. Protein Cell 1(11):987–998PubMedCrossRefGoogle Scholar
  36. Hendrix RW (2003) Bacteriophage genomics. Curr Opin Microbiol 6(5):506–511PubMedCrossRefGoogle Scholar
  37. Henson BW, Johnson N, Bera A, Okoye ME, Desai KV, Desai PJ (2011) Expression of the HSV-1 capsid protein VP19C in Escherichia coli: a single amino acid change overcomes an expression block of the full-length polypeptide. Protein Expr Purif 77(1):80–85PubMedCrossRefGoogle Scholar
  38. Heymann JB, Cheng N, Newcomb WW, Trus BL, Brown JC, Steven AC (2003) Dynamics of herpes simplex virus capsid maturation visualized by time-lapse cryo-electron microscopy. Nat Struct Biol 10(5):334–341PubMedCrossRefGoogle Scholar
  39. Hoog SS, Smith WW, Qiu X, Janson CA, Hellmig B, McQueney MS, O’Donnell K, O’Shannessy D, DiLella AG, Debouck C, Abdel-Meguid SS (1997) Active site cavity of herpesvirus proteases revealed by the crystal structure of herpes simplex virus protease/inhibitor complex. Biochemistry 36(46):14023–14029PubMedCrossRefGoogle Scholar
  40. Huffman JB, Newcomb WW, Brown JC, Homa FL (2008) Amino acids 143 to 150 of the herpes simplex virus type 1 scaffold protein are required for the formation of portal-containing capsids. J Virol 82(13):6778–6781PubMedCrossRefGoogle Scholar
  41. Ionel A, Velazquez-Muriel JA, Luque D, Cuervo A, Caston JR, Valpuesta JM, Martin-Benito J, Carrascosa JL (2011) Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7. J Biol Chem 286(1):234–242PubMedCrossRefGoogle Scholar
  42. Iwasaki K, Trus BL, Wingfield PT, Cheng N, Campusano G, Rao VB, Steven AC (2000) Molecular architecture of bacteriophage T4 capsid: vertex structure and bimodal binding of the stabilizing accessory protein, Soc. Virology. 271(2):321–333PubMedCrossRefGoogle Scholar
  43. Kirkitadze MD, Barlow PN, Price NC, Kelly SM, Boutell CJ, Rixon FJ, McClelland DA (1998) The herpes simplex virus triplex protein, VP23, exists as a molten globule. J Virol 72(12):10066–10072PubMedGoogle Scholar
  44. Klupp BG, Granzow H, Keil GM, Mettenleiter TC (2006) The capsid-associated UL25 protein of the alphaherpesvirus pseudorabies virus is nonessential for cleavage and encapsidation of genomic DNA but is required for nuclear egress of capsids. J Virol 80(13):6235–6246PubMedCrossRefGoogle Scholar
  45. Krupovic M, Bamford DH (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol 6(12):941–948PubMedCrossRefGoogle Scholar
  46. Kuznetsov YG, Martiny JB, McPherson A (2010) Structural analysis of a Synechococcus myovirus S-CAM4 and infected cells by atomic force microscopy. J Gen Virol 91(Pt 12):3095–3104PubMedCrossRefGoogle Scholar
  47. Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26(7):1984–1994PubMedCrossRefGoogle Scholar
  48. Lurz R, Orlova EV, Gunther D, Dube P, Droge A, Weise F, van Heel M, Tavares P (2001) Structural organisation of the head-to-tail interface of a bacterial virus. J Mol Biol 310(5):1027–1037PubMedCrossRefGoogle Scholar
  49. Marintcheva B, Weller SK (2001) A tale of two HSV-1 helicases: roles of phage and animal virus helicases in DNA replication and recombination. Prog Nucleic Acid Res Mol Biol 70:77–118PubMedCrossRefGoogle Scholar
  50. Maurer UE, Sodeik B, Grünewald K (2008) Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc Natl Acad Sci USA 105(30):10559–10564PubMedCrossRefGoogle Scholar
  51. McNab AR, Desai P, Person S, Roof LL, Thomsen DR, Newcomb WW, Brown JC, Homa FL (1998) The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J Virol 72(2):1060–1070PubMedGoogle Scholar
  52. Mettenleiter TC, Klupp BG, Granzow H (2009) Herpesvirus assembly: an update. Virus Res 143(2):222–234PubMedCrossRefGoogle Scholar
  53. Morais MC, Kanamaru S, Badasso MO, Koti JS, Owen BA, McMurray CT, Anderson DL, Rossmann MG (2003) Bacteriophage phi29 scaffolding protein gp7 before and after prohead assembly. Nat Struct Biol 10(7):572–576PubMedCrossRefGoogle Scholar
  54. Newcomb WW, Brown JC (2009) Time-dependent transformation of the herpesvirus tegument. J Virol 83(16):8082–8089PubMedCrossRefGoogle Scholar
  55. Newcomb WW, Brown JC (2010) Structure and capsid association of the herpesvirus large tegument protein UL36. J Virol 84(18):9408–9414PubMedCrossRefGoogle Scholar
  56. Newcomb WW, Homa FL, Thomsen DR, Booy FP, Trus BL, Steven AC, Spencer JV, Brown JC (1996) Assembly of the herpes simplex virus capsid: characterization of intermediates observed during cell-free capsid formation. J Mol Biol. 263(3):432–446PubMedCrossRefGoogle Scholar
  57. Newcomb WW, Trus BL, Cheng N, Steven AC, Sheaffer AK, Tenney DJ, Weller SK, Brown JC (2000) Isolation of herpes simplex virus procapsids from cells infected with a protease-deficient mutant virus. J Virol 74(4):1663–1673PubMedCrossRefGoogle Scholar
  58. Newcomb WW, Homa FL, Brown JC (2006) Herpes simplex virus capsid structure: DNA packaging protein UL25 is located on the external surface of the capsid near the vertices. J Virol 80(13):6286–6294PubMedCrossRefGoogle Scholar
  59. Ogasawara M, Suzutani T, Yoshida I, Azuma M (2001) Role of the UL25 gene product in packaging DNA into the herpes simplex virus capsid: location of UL25 product in the capsid and demonstration that it binds DNA. J Virol 75(3):1427–1436PubMedCrossRefGoogle Scholar
  60. Olia AS, Prevelige PE Jr, Johnson JE, Cingolani G (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18(5):597–603PubMedCrossRefGoogle Scholar
  61. Parker ML, Ralston EJ, Eiserling FA (1983) Bacteriophage SPO1 structure and morphogenesis. II. Head structure and DNA size. J Virol 46(1):250–259PubMedGoogle Scholar
  62. Pasdeloup D, Blondel D, Isidro AL, Rixon FJ (2009) Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J Virol 83(13):6610–6623PubMedCrossRefGoogle Scholar
  63. Pelletier A, Do F, Brisebois JJ, Lagace L, Cordingley MG (1997) Self-association of herpes simplex virus type 1 ICP35 is via coiled-coil interactions and promotes stable interaction with the major capsid protein. J Virol 71:5197–5208PubMedGoogle Scholar
  64. Preston VG, Murray J, Preston CM, McDougall IM, Stow ND (2008) The UL25 gene product of herpes simplex virus type 1 is involved in uncoating of the viral genome. J Virol 82(13):6654–6666PubMedCrossRefGoogle Scholar
  65. Qiu X, Culp JS, DiLella AG, Hellmig B, Hoog SS, Janson CA, Smith WW, Abdel-Meguid SS (1996) Unique fold and active site in cytomegalovirus protease. Nature 383:275–279PubMedCrossRefGoogle Scholar
  66. Qiu X, Janson CA, Culp JS, Richardson SB, Debouck C, Smith WW, Abdel-Meguid SS (1997) Crystal structure of varicella-zoster virus protease. Proc Natl Acad Sci USA 94(7):2874–2879PubMedCrossRefGoogle Scholar
  67. Radtke K, Kieneke D, Wolfstein A, Michael K, Steffen W, Scholz T, Karger A, Sodeik B (2010) Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog 6(7):e1000991PubMedCrossRefGoogle Scholar
  68. Rochat RH, Liu X, Murata K, Nagayama K, Rixon FJ, Chiu W (2011) Seeing the portal in herpes simplex virus type 1 B capsids. J Virol 85(4):1871–1874PubMedCrossRefGoogle Scholar
  69. Scrivano L, Esterlechner J, Mühlbach H, Ettischer N, Hagen C, Grünewald K, Mohr CA, Ruzsics Z, Koszinowski U, Adler B (2010) The m74 gene product of murine cytomegalovirus (MCMV) is a functional homolog of human CMV gO and determines the entry pathway of MCMV. J Virol. 84(9):4469–4480PubMedCrossRefGoogle Scholar
  70. Salmon B, Baines JD (1998) Herpes simplex virus DNA cleavage and packaging: association of multiple forms of U(L)15-encoded proteins with B capsids requires at least the U(L)6, U(L)17, and U(L)28 genes. J Virol 72(4):3045–3050PubMedGoogle Scholar
  71. Shanda SK, Wilson DW (2008) UL36p is required for efficient transport of membrane-associated herpes simplex virus type 1 along microtubules. J Virol 82(15):7388–7394PubMedCrossRefGoogle Scholar
  72. Sheaffer AK, Newcomb WW, Brown JC, Gao M, Weller SK, Tenney DJ (2000) Evidence for controlled incorporation of herpes simplex virus type 1 UL26 protease into capsids. J Virol 74(15):6838–6848PubMedCrossRefGoogle Scholar
  73. Simpson AA, Leiman PG, Tao Y, He Y, Badasso MO, Jardine PJ, Anderson DL, Rossmann MG (2001) Structure determination of the head-tail connector of bacteriophage phi29. Acta Crystallogr D Biol Crystallogr 57(Pt 9):1260–1269PubMedCrossRefGoogle Scholar
  74. Steven AC, Heymann JB, Cheng N, Trus BL, Conway JF (2005) Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr Opin Struct Biol 15(2):227–236PubMedCrossRefGoogle Scholar
  75. Stow ND (2001) Packaging of genomic and amplicon DNA by the herpes simplex virus type 1 UL25-null mutant KUL25NS. J Virol 75(22):10755–10765PubMedCrossRefGoogle Scholar
  76. Szilagyi JF, Berriman J (1994) Herpes simplex virus L particles contain spherical membrane-enclosed inclusion vesicles. J Gen Virol 75(Pt 7):1749–1753PubMedCrossRefGoogle Scholar
  77. Thurlow JK, Murphy M, Stow ND, Preston VG (2006) Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids. J Virol 80(5):2118–2126PubMedCrossRefGoogle Scholar
  78. Tong L (2002) Viral proteases. Chem Rev 102(12):4609–4626PubMedCrossRefGoogle Scholar
  79. Trus BL, Newcomb WW, Booy FP, Brown JC, Steven AC (1992) Distinct monoclonal antibodies separately label the hexons or the pentons of herpes simplex virus capsid. Proc Natl Acad Sci USA 89:11508–11512PubMedCrossRefGoogle Scholar
  80. Trus BL, Homa FL, Booy FP, Newcomb WW, Thomsen DR, Cheng N, Brown JC, Steven AC (1995) Herpes simplex virus capsids assembled in insect cells infected with recombinant baculoviruses: structural authenticity and localization of VP26. J Virol 69:7362–7366PubMedGoogle Scholar
  81. Trus BL, Booy FP, Newcomb WW, Brown JC, Homa FL, Thomsen DR, Steven AC (1996) The herpes simplex virus procapsid: structure, conformational changes upon maturation, and roles of the triplex proteins VP19c and VP23 in assembly. J Mol Biol. 263(3):447–462PubMedCrossRefGoogle Scholar
  82. Trus BL, Gibson W, Cheng N, Steven AC (1999) Capsid structure of simian cytomegalovirus from cryoelectron microscopy: evidence for tegument attachment sites [published erratum appears in J Virol 1999 May;73(5):4530]. J Virol 73(3):2181–2192PubMedGoogle Scholar
  83. Trus BL, Heymann JB, Nealon K, Cheng N, Newcomb WW, Brown JC, Kedes DH, Steven AC (2001) Capsid structure of Kaposi’s sarcoma-associated herpesvirus, a gammaherpesvirus, compared to an alphaherpesvirus, HSV1, and a betaherpesvirus, CMV. J Virol 75(6):2879–2890PubMedCrossRefGoogle Scholar
  84. Trus BL, Cheng N, Newcomb WW, Homa FL, Brown JC, Steven AC (2004) Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J Virol 78(22):12668–12671PubMedCrossRefGoogle Scholar
  85. Trus BL, Newcomb WW, Cheng N, Cardone G, Marekov L, Homa FL, Brown JC, Steven AC (2007) Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol Cell 26(4):479–489PubMedCrossRefGoogle Scholar
  86. Weigele PR, Pope WH, Pedulla ML, Houtz JM, Smith AL, Conway JF, King J, Hatfull GF, Lawrence JG, Hendrix RW (2007) Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol 9(7):1675–1695PubMedCrossRefGoogle Scholar
  87. Welch AR, McNally LM, Hall MRT, Gibson W (1993) Herpesvirus proteinase: site-directed mutagenesis used to study maturational, release, and inactivation cleavage sites of precursor and to identify a possible catalytic site serine and histidine. J Virol 67:7360–7372PubMedGoogle Scholar
  88. Wikoff WR, Liljas L, Duda RL, Tsuruta H, Hendrix RW, Johnson JE (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289(5487):2129–2133PubMedCrossRefGoogle Scholar
  89. Wingfield PT, Stahl SJ, Thomsen DR, Homa FL, Booy FP, Trus BL, Steven AC (1997) Hexon-only binding of VP26 reflects differences between the hexon and penton conformations of VP5, the major capsid protein of herpes simplex virus. J Virol 71:8955–8961PubMedGoogle Scholar
  90. Wolfstein A, Nagel CH, Radtke K, Dohner K, Allan VJ, Sodeik B (2006) The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7(2):227–237PubMedCrossRefGoogle Scholar
  91. Yang F, Forrer P, Dauter Z, Conway JF, Cheng N, Cerritelli ME, Steven AC, Plückthun A, Wlodawer A (2000) Novel Fold and Capsid-binding Properties of the l Phage Display Platform Protein gpD. Nat. Struct. Biol. 7:230–237PubMedCrossRefGoogle Scholar
  92. Yang K, Baines JD (2008) Domain within herpes simplex virus 1 scaffold proteins required for interaction with portal protein in infected cells and incorporation of the portal vertex into capsids. J Virol 82(10):5021–5030PubMedCrossRefGoogle Scholar
  93. Zhou ZH, He J, Jakana J, Tatman JD, Rixon FJ, Chiu W (1995) Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat Struct Biol 2:1026–1030PubMedCrossRefGoogle Scholar
  94. Zhou ZH, Dougherty M, Jakana J, He J, Rixon FJ, Chiu W (2000) Seeing the herpesvirus capsid at 8.5 Å. Science 288(5467):877–880PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Giovanni Cardone
    • 1
  • J. Bernard Heymann
    • 1
  • Naiqian Cheng
    • 1
  • Benes L. Trus
    • 1
    • 2
  • Alasdair C. Steven
    • 1
  1. 1.Laboratory of Structural BiologyNational Institute for Arthritis, Musculoskeletal and Skin Diseases, National Institutes of HealthBethesdaUSA
  2. 2.Imaging Sciences Laboratory, Center for Information TechnologyNational Institutes of HealthBethesdaUSA

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