Assemblins as maturational proteases in herpesviruses Free

Abstract

During assembly of herpesvirus capsids, a protein scaffold self-assembles to ring-like structures forming the scaffold of the spherical procapsids. Proteolytic activity of the herpesvirus maturational protease causes structural changes that result in angularization of the capsids. In those mature icosahedral capsids, the packaging of viral DNA into the capsids can take place. The strictly regulated protease is called assemblin. It is inactive in its monomeric state and activated by dimerization. The structures of the dimeric forms of several assemblins from all herpesvirus subfamilies have been elucidated in the last two decades. They revealed a unique serine-protease fold with a catalytic triad consisting of a serine and two histidines. Inhibitors that disturb dimerization by binding to the dimerization area were found recently. Additionally, the structure of the monomeric form of assemblin from pseudorabies virus and some monomer-like structures of Kaposi's sarcoma-associated herpesvirus assemblin were solved. These findings are the proof-of-principle for the development of new anti-herpesvirus drugs. Therefore, the most important information on this fascinating and unique class of proteases is summarized here.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000872
2017-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/8/1969.html?itemId=/content/journal/jgv/10.1099/jgv.0.000872&mimeType=html&fmt=ahah

References

  1. Fields BN, Knipe DM, Howley PM. (editors) Fields Virology, 6th ed. Philadelphia, PA: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2013 pp. 2456
    [Google Scholar]
  2. Mahy BWJ, van Regenmortel MHV. (editors). Encyclopedia of Virology, 3rd ed. Oxford, UK: Elsevier; 2008
    [Google Scholar]
  3. Tischer BK, Osterrieder N. Herpesviruses – a zoonotic threat?. Vet Microbiol 2010; 140:266–270 [View Article][PubMed]
    [Google Scholar]
  4. Woźniakowski G, Samorek-Salamonowicz E. Animal herpesviruses and their zoonotic potential for cross-species infection. Ann Agric Environ Med 2015; 22:191–194 [View Article][PubMed]
    [Google Scholar]
  5. Preston CM, Efstathiou S. Molecular basis of HSV latency and reactivation, chapter 33. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K et al. (editors) Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis Cambridge: Cambridge University Press; 2007
    [Google Scholar]
  6. van Lint AL, Knipe DM. Herpesviruses. In Schaechter M. (editor) Encyclopedia of Microbiology, 3rd ed. Oxford: Academic Press; 2009
    [Google Scholar]
  7. Furlong D. Direct evidence for 6-fold symmetry of the herpesvirus hexon capsomere. Proc Natl Acad Sci USA 1978; 75:2764–2766 [View Article][PubMed]
    [Google Scholar]
  8. Vernon SK, Ponce de Leon M, Cohen GH, Eisenberg RJ, Rubin BA. Morphological components of herpesvirus. III. Localization of herpes simplex virus type 1 nucleocapsid polypeptides by immune electron microscopy. J Gen Virol 1981; 54:39–46 [View Article][PubMed]
    [Google Scholar]
  9. Schrag JD, Prasad BV, Rixon FJ, Chiu W. Three-dimensional structure of the HSV1 nucleocapsid. Cell 1989; 56:651–660 [View Article][PubMed]
    [Google Scholar]
  10. Newcomb WW, Trus BL, Booy FP, Steven AC, Wall JS et al. Structure of the herpes simplex virus capsid. Molecular composition of the pentons and the triplexes. J Mol Biol 1993; 232:499–511 [View Article][PubMed]
    [Google Scholar]
  11. Newcomb WW, Juhas RM, Thomsen DR, Homa FL, Burch AD et al. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J Virol 2001; 75:10923–10932 [View Article][PubMed]
    [Google Scholar]
  12. Newcomb WW, Homa FL, Brown JC. Involvement of the portal at an early step in herpes simplex virus capsid assembly. J Virol 2005; 79:10540–10546 [View Article][PubMed]
    [Google Scholar]
  13. Newcomb WW, Thomsen DR, Homa FL, Brown JC. Assembly of the herpes simplex virus capsid: identification of soluble scaffold-portal complexes and their role in formation of portal-containing capsids. J Virol 2003; 77:9862–9871 [View Article][PubMed]
    [Google Scholar]
  14. Wildy P, Russell WC, Horne RW. The morphology of herpes virus. Virology 1960; 12:204–222 [View Article][PubMed]
    [Google Scholar]
  15. Baker TS, Newcomb WW, Booy FP, Brown JC, Steven AC. Three-dimensional structures of maturable and abortive capsids of equine herpesvirus 1 from cryoelectron microscopy. J Virol 1990; 64:563–573[PubMed]
    [Google Scholar]
  16. Singer GP, Newcomb WW, Thomsen DR, Homa FL, Brown JC. Identification of a region in the herpes simplex virus scaffolding protein required for interaction with the portal. J Virol 2005; 79:132–139 [View Article][PubMed]
    [Google Scholar]
  17. Yang K, Baines JD. 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 2008; 82:5021–5030 [View Article][PubMed]
    [Google Scholar]
  18. Plafker SM, Gibson W. Cytomegalovirus assembly protein precursor and proteinase precursor contain two nuclear localization signals that mediate their own nuclear translocation and that of the major capsid protein. J Virol 1998; 72:7722–7732[PubMed]
    [Google Scholar]
  19. Nicholson P, Addison C, Cross AM, Kennard J, Preston VG et al. Localization of the herpes simplex virus type 1 major capsid protein VP5 to the cell nucleus requires the abundant scaffolding protein VP22a. J Gen Virol 1994; 75:1091–1099 [View Article][PubMed]
    [Google Scholar]
  20. Welch AR, McNally LM, Gibson W. Cytomegalovirus assembly protein nested gene family: four 3'-coterminal transcripts encode four in-frame, overlapping proteins. J Virol 1991; 65:4091–4100[PubMed]
    [Google Scholar]
  21. Barrett A, Rawlings N, Woessner J. (editors) Handbook of Proteolytic Enzymes, 3rd ed. London, UK: Academic Press; 2013 pp. 3241
    [Google Scholar]
  22. Klupp BG, Hengartner CJ, Mettenleiter TC, Enquist LW. Complete, annotated sequence of the pseudorabies virus genome. J Virol 2004; 78:424–440 [View Article][PubMed]
    [Google Scholar]
  23. Liu FY, Roizman B. The herpes simplex virus 1 gene encoding a protease also contains within its coding domain the gene encoding the more abundant substrate. J Virol 1991; 65:5149–5156[PubMed]
    [Google Scholar]
  24. Ward PL, Ogle WO, Roizman B. Assemblons: nuclear structures defined by aggregation of immature capsids and some tegument proteins of herpes simplex virus 1. J Virol 1996; 70:4623–4631[PubMed]
    [Google Scholar]
  25. Sheaffer AK, Newcomb WW, Brown JC, Gao M, Weller SK et al. Evidence for controlled incorporation of herpes simplex virus type 1 UL26 protease into capsids. J Virol 2000; 74:6838–6848 [View Article][PubMed]
    [Google Scholar]
  26. Newcomb WW, Homa FL, Thomsen DR, Trus BL, Cheng N et al. Assembly of the herpes simplex virus procapsid from purified components and identification of small complexes containing the major capsid and scaffolding proteins. J Virol 1999; 73:4239–4250[PubMed]
    [Google Scholar]
  27. Newcomb WW, Brown JC. Structure of the herpes simplex virus capsid: effects of extraction with guanidine hydrochloride and partial reconstitution of extracted capsids. J Virol 1991; 65:613–620[PubMed]
    [Google Scholar]
  28. Pelletier A, Do F, Brisebois JJ, Lagacé L, Cordingley MG. 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 1997; 71:5197–5208[PubMed]
    [Google Scholar]
  29. Newcomb WW, Trus BL, Cheng N, Steven AC, Sheaffer AK et al. Isolation of herpes simplex virus procapsids from cells infected with a protease-deficient mutant virus. J Virol 2000; 74:1663–1673 [View Article][PubMed]
    [Google Scholar]
  30. Spencer JV, Newcomb WW, Thomsen DR, Homa FL, Brown JC. Assembly of the herpes simplex virus capsid: preformed triplexes bind to the nascent capsid. J Virol 1998; 72:3944–3951[PubMed]
    [Google Scholar]
  31. Trus BL, Booy FP, Newcomb WW, Brown JC, Homa FL et al. The herpes simplex virus procapsid: structure, conformational changes upon maturation, and roles of the triplex proteins VP19c and VP23 in assembly. J Mol Biol 1996; 263:447–462 [View Article][PubMed]
    [Google Scholar]
  32. Wingfield PT, Stahl SJ, Thomsen DR, Homa FL, Booy FP et al. 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 1997; 71:8955–8961[PubMed]
    [Google Scholar]
  33. Heymann JB, Cheng N, Newcomb WW, Trus BL, Brown JC et al. Dynamics of herpes simplex virus capsid maturation visualized by time-lapse cryo-electron microscopy. Nat Struct Biol 2003; 10:334–341 [View Article][PubMed]
    [Google Scholar]
  34. Rixon FJ, Addison C, McGregor A, Macnab SJ, Nicholson P et al. Multiple interactions control the intracellular localization of the herpes simplex virus type 1 capsid proteins. J Gen Virol 1996; 77:2251–2260 [View Article][PubMed]
    [Google Scholar]
  35. Chi JH, Wilson DW. ATP-dependent localization of the herpes simplex virus capsid protein VP26 to sites of procapsid maturation. J Virol 2000; 74:1468–1476 [View Article][PubMed]
    [Google Scholar]
  36. Thomsen DR, Roof LL, Homa FL. Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with recombinant baculoviruses expressing HSV capsid proteins. J Virol 1994; 68:2442–2457[PubMed]
    [Google Scholar]
  37. Darke PL, Cole JL, Waxman L, Hall DL, Sardana MK et al. Active human cytomegalovirus protease is a dimer. J Biol Chem 1996; 271:7445–7449 [View Article][PubMed]
    [Google Scholar]
  38. Nomura AM, Marnett AB, Shimba N, Dötsch V, Craik CS. Induced structure of a helical switch as a mechanism to regulate enzymatic activity. Nat Struct Mol Biol 2005; 12:1019–1020 [View Article][PubMed]
    [Google Scholar]
  39. Robertson BJ, McCann PJ, Matusick-Kumar L, Newcomb WW, Brown JC et al. Separate functional domains of the herpes simplex virus type 1 protease: evidence for cleavage inside capsids. J Virol 1996; 70:4317–4328[PubMed]
    [Google Scholar]
  40. Newcomb WW, Homa FL, Thomsen DR, Booy FP, Trus BL et al. Assembly of the herpes simplex virus capsid: characterization of intermediates observed during cell-free capsid formation. J Mol Biol 1996; 263:432–446 [View Article][PubMed]
    [Google Scholar]
  41. Welch AR, Woods AS, McNally LM, Cotter RJ, Gibson W. A herpesvirus maturational proteinase, assemblin: identification of its gene, putative active site domain, and cleavage site. Proc Natl Acad Sci USA 1991; 88:10792–10796 [View Article][PubMed]
    [Google Scholar]
  42. Yang K, Wills EG, Baines JD. Release of the herpes simplex virus 1 protease by self cleavage is required for proper conformation of the portal vertex. Virology 2012; 429:63–73 [View Article][PubMed]
    [Google Scholar]
  43. Thomsen DR, Newcomb WW, Brown JC, Homa FL. Assembly of the herpes simplex virus capsid: requirement for the carboxyl-terminal twenty-five amino acids of the proteins encoded by the UL26 and UL26.5 genes. J Virol 1995; 69:3690–3703[PubMed]
    [Google Scholar]
  44. Deiss LP, Chou J, Frenkel N. Functional domains within the a sequence involved in the cleavage-packaging of herpes simplex virus DNA. J Virol 1986; 59:605–618[PubMed]
    [Google Scholar]
  45. Fujisawa H, Morita M. Phage DNA packaging. Genes Cells 1997; 2:537–545 [View Article][PubMed]
    [Google Scholar]
  46. Harper L, Demarchi J, Ben-Porat T. Sequence of the genome ends and of the junction between the ends in concatemeric DNA of pseudorabies virus. J Virol 1986; 60:1183–1185[PubMed]
    [Google Scholar]
  47. Wu CA, Harper L, Ben-Porat T. Cis functions involved in replication and cleavage-encapsidation of pseudorabies virus. J Virol 1986; 59:318–327[PubMed]
    [Google Scholar]
  48. Beard PM, Taus NS, Baines JD. DNA cleavage and packaging proteins encoded by genes UL28, UL15, and UL33 of herpes simplex virus type 1 form a complex in infected cells. J Virol 2002; 76:4785–4791 [View Article][PubMed]
    [Google Scholar]
  49. White CA, Stow ND, Patel AH, Hughes M, Preston VG. Herpes simplex virus type 1 portal protein UL6 interacts with the putative terminase subunits UL15 and UL28. J Virol 2003; 77:6351–6358 [View Article][PubMed]
    [Google Scholar]
  50. Spear PG, Roizman B. Proteins specified by herpes simplex virus V. Purification and structural proteins of the herpesvirion. J Virol 1972; 9:143–159[PubMed]
    [Google Scholar]
  51. Gibson W, Roizman B. Proteins specified by herpes simplex virus VIII. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J Virol 1972; 10:1044–1052[PubMed]
    [Google Scholar]
  52. Maier O, Sollars PJ, Pickard GE, Smith GA. Visualizing herpesvirus procapsids in living cells. J Virol 2016; 90:10182–10192 [View Article][PubMed]
    [Google Scholar]
  53. Chan CK, Brignole EJ, Gibson W. Cytomegalovirus assemblin (pUL80a): cleavage at internal site not essential for virus growth; proteinase absent from virions. J Virol 2002; 76:8667–8674 [View Article][PubMed]
    [Google Scholar]
  54. Conway JF, Homa FL. Nucleocapsid structure, assembly and DNA packaging of herpes simplex virus. In Weller S. (editor) Alphaheresviruses: Molecular Virology Norwich, UK: Caister Academic Press; 2011
    [Google Scholar]
  55. Fokine A, Rossmann MG. Common evolutionary origin of procapsid proteases, phage tail tubes, and tubes of bacterial type VI secretion systems. Structure 2016; 24:1928–1935 [View Article][PubMed]
    [Google Scholar]
  56. UniProt Consortium UniProt: a hub for protein information. Nucleic Acids Res 2015; 43:D204–D212 [View Article][PubMed]
    [Google Scholar]
  57. Rawlings ND, Waller M, Barrett AJ, Bateman A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 2014; 42:D503–D509 [View Article][PubMed]
    [Google Scholar]
  58. Tong L, Qian C, Massariol MJ, Bonneau PR, Cordingley MG et al. A new serine-protease fold revealed by the crystal structure of human cytomegalovirus protease. Nature 1996; 383:272–275 [View Article][PubMed]
    [Google Scholar]
  59. Shieh HS, Kurumbail RG, Stevens AM, Stegeman RA, Sturman EJ et al. Three-dimensional structure of human cytomegalovirus protease. Nature 1996; 383:279–282 [View Article][PubMed]
    [Google Scholar]
  60. Baum EZ, Bebernitz GA, Hulmes JD, Muzithras VP, Jones TR et al. Expression and analysis of the human cytomegalovirus UL80-encoded protease: identification of autoproteolytic sites. J Virol 1993; 67:497–506[PubMed]
    [Google Scholar]
  61. Welch AR, McNally LM, Hall MR, Gibson W. 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 1993; 67:7360–7372[PubMed]
    [Google Scholar]
  62. Holwerda BC, Wittwer AJ, Duffin KL, Smith C, Toth MV et al. Activity of two-chain recombinant human cytomegalovirus protease. J Biol Chem 1994; 269:25911–25915[PubMed]
    [Google Scholar]
  63. Jones TR, Sun L, Bebernitz GA, Muzithras VP, Kim HJ et al. Proteolytic activity of human cytomegalovirus UL80 protease cleavage site mutants. J Virol 1994; 68:3742–3752[PubMed]
    [Google Scholar]
  64. Loveland AN, Chan CK, Brignole EJ, Gibson W. Cleavage of human cytomegalovirus protease pUL80a at internal and cryptic sites is not essential but enhances infectivity. J Virol 2005; 79:12961–12968 [View Article][PubMed]
    [Google Scholar]
  65. Brignole EJ, Gibson W. Enzymatic activities of human cytomegalovirus maturational protease assemblin and its precursor (pPR, pUL80a) are comparable: [corrected] maximal activity of pPR requires self-interaction through its scaffolding domain. J Virol 2007; 81:4091–4103 [View Article][PubMed]
    [Google Scholar]
  66. Pray TR, Nomura AM, Pennington MW, Craik CS. Auto-inactivation by cleavage within the dimer interface of Kaposi's sarcoma-associated herpesvirus protease. J Mol Biol 1999; 289:197–203 [View Article][PubMed]
    [Google Scholar]
  67. Gibson W, Welch AR, Hall MRT, Assemblin H. Assemblin, a herpes virus serine maturational proteinase and new molecular target for antivirals. Perspect Drug Discov Des 1995; 2:413–426 [View Article]
    [Google Scholar]
  68. Welch AR, Villarreal EC, Gibson W. Cytomegalovirus protein substrates are not cleaved by the herpes simplex virus type 1 proteinase. J Virol 1995; 69:341–347[PubMed]
    [Google Scholar]
  69. Zühlsdorf M. Strukturanalysen ausgewählter Proteine des pseudorabies virus. PhD Thesis, Universität Greifswald, Greifswald, Germany 2015
  70. Kattenhorn LM, Korbel GA, Kessler BM, Spooner E, Ploegh HL. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol Cell 2005; 19:547–557 [View Article][PubMed]
    [Google Scholar]
  71. Fernandes SM, Brignole EJ, Taori K, Gibson W. Cytomegalovirus capsid protease: biological substrates are cleaved more efficiently by full-length enzyme (pUL80a) than by the catalytic domain (assemblin). J Virol 2011; 85:3526–3534 [View Article][PubMed]
    [Google Scholar]
  72. Wei Y, Schottel JL, Derewenda U, Swenson L, Patkar S et al. A novel variant of the catalytic triad in the Streptomyces scabies esterase. Nat Struct Biol 1995; 2:218–223 [View Article][PubMed]
    [Google Scholar]
  73. Khayat R, Batra R, Massariol MJ, Lagacé L, Tong L. Investigating the role of histidine 157 in the catalytic activity of human cytomegalovirus protease. Biochemistry 2001; 40:6344–6351 [View Article][PubMed]
    [Google Scholar]
  74. Thomsen M, Tuukkanen A, Dickerhoff J, Palm GJ, Kratzat H et al. Structure and catalytic mechanism of the evolutionarily unique bacterial chalcone isomerase. Acta Crystallogr D Biol Crystallogr 2015; 71:907–917 [View Article][PubMed]
    [Google Scholar]
  75. Zühlsdorf M, Werten S, Klupp BG, Palm GJ, Mettenleiter TC et al. Dimerization-Induced allosteric changes of the oxyanion-hole loop activate the pseudorabies virus assemblin pUL26N, a herpesvirus serine protease. PLoS Pathog 2015; 11:e1005045 [View Article][PubMed]
    [Google Scholar]
  76. Buisson M, Hernandez JF, Lascoux D, Schoehn G, Forest E et al. The crystal structure of the Epstein-Barr virus protease shows rearrangement of the processed C terminus. J Mol Biol 2002; 324:89–103 [View Article][PubMed]
    [Google Scholar]
  77. Smith MC, Giordano J, Cook JA, Wakulchik M, Villarreal EC et al. Purification and kinetic characterization of human cytomegalovirus assemblin. Methods Enzymol 1994; 244:412–423[PubMed] [CrossRef]
    [Google Scholar]
  78. Matusick-Kumar L, Hurlburt W, Weinheimer SP, Newcomb WW, Brown JC et al. Phenotype of the herpes simplex virus type 1 protease substrate ICP35 mutant virus. J Virol 1994; 68:5384–5394[PubMed]
    [Google Scholar]
  79. Waxman L, Darke PL. The herpesvirus proteases as targets for antiviral chemotherapy. Antivir Chem Chemother 2000; 11:1–22 [View Article][PubMed]
    [Google Scholar]
  80. Batra R, Khayat R, Tong L. Molecular mechanism for dimerization to regulate the catalytic activity of human cytomegalovirus protease. Nat Struct Biol 2001; 8:810–817 [View Article][PubMed]
    [Google Scholar]
  81. Gable JE, Lee GM, Jaishankar P, Hearn BR, Waddling CA et al. Broad-spectrum allosteric inhibition of herpesvirus proteases. Biochemistry 2014; 53:4648–4660 [View Article][PubMed]
    [Google Scholar]
  82. Liang PH, Brun KA, Feild JA, O'Donnell K, Doyle ML et al. Site-directed mutagenesis probing the catalytic role of arginines 165 and 166 of human cytomegalovirus protease. Biochemistry 1998; 37:5923–5929 [View Article][PubMed]
    [Google Scholar]
  83. Qiu X, Culp JS, Dilella AG, Hellmig B, Hoog SS et al. Unique fold and active site in cytomegalovirus protease. Nature 1996; 383:275–279 [View Article][PubMed]
    [Google Scholar]
  84. Lee GM, Shahian T, Baharuddin A, Gable JE, Craik CS. Enzyme inhibition by allosteric capture of an inactive conformation. JMol Biol 2011; 411:999–1016 [View Article][PubMed]
    [Google Scholar]
  85. Qiu X, Janson CA, Culp JS, Richardson SB, Debouck C et al. Crystal structure of varicella-zoster virus protease. Proc Natl Acad Sci USA 1997; 94:2874–2879 [View Article][PubMed]
    [Google Scholar]
  86. Register RB, Shafer JA. A facile system for construction of HSV-1 variants: site directed mutation of the UL26 protease gene in HSV-1. J Virol Methods 1996; 57:181–193 [View Article][PubMed]
    [Google Scholar]
  87. Church GA, Wilson DW. Study of herpes simplex virus maturation during a synchronous wave of assembly. J Virol 1997; 71:3603–3612[PubMed]
    [Google Scholar]
  88. Burck PJ, Berg DH, Luk TP, Sassmannshausen LM, Wakulchik M et al. Human cytomegalovirus maturational proteinase: expression in Escherichia coli, purification, and enzymatic characterization by using peptide substrate mimics of natural cleavage sites. J Virol 1994; 68:2937–2946[PubMed]
    [Google Scholar]
  89. Park SH, Raines RT. Genetic selection for dissociative inhibitors of designated protein-protein interactions. Nat Biotechnol 2000; 18:847–851 [View Article][PubMed]
    [Google Scholar]
  90. Nikolay R, Schmidt S, Schlömer R, Deuerling E, Nierhaus KH. Ribosome assembly as antimicrobial target. Antibiotics 2016; 5:18 [View Article][PubMed]
    [Google Scholar]
  91. Thenin-Houssier S, Valente ST. HIV-1 capsid inhibitors as antiretroviral agents. Curr HIV Res 2016; 14:270–282 [View Article][PubMed]
    [Google Scholar]
  92. Ma B, Nussinov R. Trp/Met/Phe hot spots in protein-protein interactions: potential targets in drug design. Curr Top Med Chem 2007; 7:999–1005 [View Article][PubMed]
    [Google Scholar]
  93. Shahian T, Lee GM, Lazic A, Arnold LA, Velusamy P et al. Inhibition of a viral enzyme by a small-molecule dimer disruptor. Nat Chem Biol 2009; 5:640–646 [View Article][PubMed]
    [Google Scholar]
  94. Gable JE, Lee GM, Acker TM, Hulce KR, Gonzalez ER et al. Fragment-based protein-protein interaction antagonists of a viral dimeric protease. ChemMedChem 2016; 11:862–869 [View Article][PubMed]
    [Google Scholar]
  95. Hendrix RW. Bacteriophage genomics. Curr Opin Microbiol 2003; 6:506–511 [View Article][PubMed]
    [Google Scholar]
  96. Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 2010; 20:202–213 [View Article][PubMed]
    [Google Scholar]
  97. Kangro HO, Osman HK, Lau YL, Heath RB, Yeung CY et al. Seroprevalence of antibodies to human herpesviruses in England and Hong Kong. J Med Virol 1994; 43:91–96 [View Article][PubMed]
    [Google Scholar]
  98. Pebody RG, Andrews N, Brown D, Gopal R, de Melker H et al. The seroepidemiology of herpes simplex virus type 1 and 2 in Europe. Sex Transm Infect 2004; 80:185–191 [View Article][PubMed]
    [Google Scholar]
  99. Nahmias AJ, Lee FK, Beckman-Nahmias S. Sero-epidemiological and -sociological patterns of herpes simplex virus infection in the world. Scand J Infect Dis Suppl 1990; 69:19–36[PubMed]
    [Google Scholar]
  100. Schulz TF. Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8): epidemiology and pathogenesis. J Antimicrob Chemother 2000; 45:15–27 [View Article][PubMed]
    [Google Scholar]
  101. Kudesia G, Partridge S, Farrington CP, Soltanpoor N. Changes in age related seroprevalence of antibody to varicella zoster virus: impact on vaccine strategy. J Clin Pathol 2002; 55:154–155 [View Article][PubMed]
    [Google Scholar]
  102. Dowd JB, Palermo T, Brite J, Mcdade TW, Aiello A. Seroprevalence of Epstein-Barr virus infection in U.S. children ages 6-19, 2003–2010. PLoS One 2013; 8:e64921 [View Article][PubMed]
    [Google Scholar]
  103. Schechter I, Berger A. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 1967; 27:157–162 [View Article][PubMed]
    [Google Scholar]
  104. Linding R, Jensen LJ, Diella F, Bork P, Gibson TJ et al. Protein disorder prediction: implications for structural proteomics. Structure 2003; 11:1453–1459[PubMed] [CrossRef]
    [Google Scholar]
  105. Schmidt U, Darke PL. Dimerization and activation of the herpes simplex virus type 1 protease. J Biol Chem 1997; 272:7732–7735 [View Article][PubMed]
    [Google Scholar]
  106. Carter P, Wells JA. Dissecting the catalytic triad of a serine protease. Nature 1988; 332:564–568 [View Article][PubMed]
    [Google Scholar]
  107. Corey DR, Craik CS. An investigation into the minimum requirements for peptide hydrolysis by mutation of the catalytic triad of trypsin. J Am Chem Soc 1992; 114:1784–1790 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000872
Loading
/content/journal/jgv/10.1099/jgv.0.000872
Loading

Data & Media loading...

Most cited Most Cited RSS feed