A wide extent of inter-strain diversity in virulent and vaccine strains of Alphaherpesviruses

PLoS Pathogens

Volumn 7, Issue 10, 2011, Pages

  Szpara, Moriah L ^a   Tafuri, Yolanda R ^a   Parsons, Lance ^a   Shamim, S Rafi ^a   Verstrepen, Kevin J ^b   Legendre, Matthieu ^c   Enquist, L W ^a  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; NUCLEIC ACID; PROTEOME; PSEUDORABIES VACCINE; VIRUS PROTEIN; HERPES VACCINE; MICROSATELLITE DNA;

ALPHAHERPESVIRUS; AMINO ACID SEQUENCE; ARTICLE; DNA BINDING; GENE SEQUENCE; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; HERPES VIRUS; HIGH THROUGHPUT SEQUENCING; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN INTERACTION; PSEUDORABIES HERPETOVIRUS; SHORT TANDEM REPEAT; TRANSCRIPTION REGULATION; VIRUS GENOME; VIRUS ISOLATION; VIRUS VIRULENCE; ALPHAHERPESVIRINAE; ANIMAL; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; HERPES SIMPLEX VIRUS 1; HUMAN; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PATHOGENICITY; SEQUENCE ALIGNMENT; VARICELLA ZOSTER VIRUS;

DNA VIRUSES; HERPESVIRIDAE; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 3; MAMMALIA; SUID HERPESVIRUS 1;

ALPHAHERPESVIRINAE; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; GENETIC VARIATION; GENOME, VIRAL; HERPESVIRUS 1, HUMAN; HERPESVIRUS 1, SUID; HERPESVIRUS 3, HUMAN; HERPESVIRUS VACCINES; HUMANS; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; PSEUDORABIES VACCINES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS;

EID: 80055089065     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002282     Document Type: Article

References (193)

1. Roizman B, Pellett PE, (2001) The family Herpesviridae: A brief introduction. In: Knipe DM, Howley PM, editors. Fields Virology 4 ed Philadelphia Lippincott Williams & Wilkins pp. 2381-2397.
2. Steiner I, Kennedy PG, Pachner AR, (2007) The neurotropic herpes viruses: herpes simplex and varicella-zoster. Lancet Neurol 6: 1015-1028.
3. Arvin AM, (1996) Varicella-zoster virus. Clin Microbiol Rev 9: 361-381.
4. Pomeranz LE, Reynolds AE, Hengartner CJ, (2005) Molecular biology of pseudorabies virus: impact on neurovirology and veterinary medicine. Microbiol Mol Biol Rev 69: 462-500.
5. Mettenleiter TC, Keil GM, Fuchs W, (2008) Molecular Biology of Animal Herpesviruses. In: Mettenleiter TC, Sobrino F, editors. Animal viruses: molecular biology xii Norfolk, UK Caister Academic Press: 531.
6. Muller WJ, Jones CA, Koelle DM, (2010) Immunobiology of herpes simplex virus and cytomegalovirus infections of the fetus and newborn. Curr Immunol Rev 6: 38-55.
7. Arvin AM, Gershon AA, (1996) Live attenuated varicella vaccine. Annu Rev Microbiol 50: 59-100.
8. Mettenleiter TC, (1996) Immunobiology of pseudorabies (Aujeszky's disease). Vet Immunol Immunopathol 54: 221-229.
9. Koelle DM, Corey L, (2003) Recent progress in herpes simplex virus immunobiology and vaccine research. Clin Microbiol Rev 16: 96-113.
10. Koelle DM, Corey L, (2008) Herpes simplex: insights on pathogenesis and possible vaccines. Annu Rev Med 59: 381-395.
11. Nikolic DS, Piguet V, (2009) Vaccines and microbicides preventing HIV-1, HSV-2, and HPV mucosal transmission. J Invest Dermatol 130: 352-361.
12. Strick LB, Wald A, Celum C, (2006) Management of herpes simplex virus type 2 infection in HIV type 1-infected persons. Clin Infect Dis 43: 347-356.
13. Ramaswamy M, Geretti AM, (2007) Interactions and management issues in HSV and HIV coinfection. Expert Rev Anti Infect Ther 5: 231-243.
14. Watson RJ, Enquist LW, (1985) Genetically engineered herpes simplex virus vaccines. Prog Med Virol 31: 84-108.
15. Weis JH, Enquist LW, Salstrom JS, Watson RJ, (1983) An immunologically active chimaeric protein containing herpes simplex virus type 1 glycoprotein D. Nature 302: 72-74.
16. Brittle EE, Reynolds AE, Enquist LW, (2004) Two modes of pseudorabies virus neuroinvasion and lethality in mice. J Virol 78: 12951-12963.
17. Simmons A, Nash AA, (1984) Zosteriform spread of herpes simplex virus as a model of recrudescence and its use to investigate the role of immune cells in prevention of recurrent disease. J Virol 52: 816-821.
18. Arvin AM, (2006) Investigations of the pathogenesis of Varicella zoster virus infection in the SCIDhu mouse model. Herpes 13: 75-80.
19. White TM, Gilden DH, Mahalingam R, (2001) An animal model of varicella virus infection. Brain Pathol 11: 475-479.
20. Myers MG, Connelly BL, (1992) Animal models of varicella. J Infect Dis 166 (Suppl 1): S48-50.
21. Lomniczi B, Watanabe S, Ben-Porat T, Kaplan AS, (1987) Genome location and identification of functions defective in the Bartha vaccine strain of pseudorabies virus. J Virol 61: 796-801.
22. Todd D, McFerran JB, (1985) Restriction endonuclease analysis of Aujeszky's disease (pseudorabies) virus DNA: comparison of Northern Ireland isolates and isolates from other countries. Arch Virol 86: 167-176.
23. Mettenleiter TC, Lukacs N, Rziha HJ, (1985) Pseudorabies virus avirulent strains fail to express a major glycoprotein. J Virol 56: 307-311.
24. Aston-Jones G, Card JP, (2000) Use of pseudorabies virus to delineate multisynaptic circuits in brain: opportunities and limitations. J Neurosci Methods 103: 51-61.
25. Enquist LW, (2002) Exploiting circuit-specific spread of pseudorabies virus in the central nervous system: insights to pathogenesis and circuit tracers. J Infect Dis 186 (Suppl 2): S209-214.
26. Ekstrand MI, Enquist LW, Pomeranz LE, (2008) The alpha-herpesviruses: molecular pathfinders in nervous system circuits. Trends Mol Med 14: 134-140.
27. Granstedt AE, Szpara ML, Kuhn B, Wang SS, Enquist LW, (2009) Fluorescence-based monitoring of in vivo neural activity using a circuit-tracing pseudorabies virus. PLoS One 4: e6923.
28. Lomniczi B, Blankenship ML, Ben-Porat T, (1984) Deletions in the genomes of pseudorabies virus vaccine strains and existence of four isomers of the genomes. J Virol 49: 970-979.
29. Bartha A, (1961) Experimental reduction of virulence of Aujeszky's disease virus. Magy Allatorv Lapja 16: 42-45.
30. Klupp BG, Hengartner CJ, Mettenleiter TC, Enquist LW, (2004) Complete, annotated sequence of the pseudorabies virus genome. J Virol 78: 424-440.
31. Lyman MG, Demmin GL, Banfield BW, (2003) The attenuated pseudorabies virus strain Bartha fails to package the tegument proteins Us3 and VP22. J Virol 77: 1403-1414.
32. Christensen LS, Medveczky I, Strandbygaard BS, Pejsak Z, (1992) Characterization of field isolates of suid herpesvirus 1 (Aujeszky's disease virus) as derivatives of attenuated vaccine strains. Arch Virol 124: 225-234.
33. Muller T, Klupp BG, Freuling C, Hoffmann B, Mojcicz M, et al. (2010) Characterization of pseudorabies virus of wild boar origin from Europe. Epidemiol Infect 138: 1590-1600.
34. Hahn EC, Fadl-Alla B, Lichtensteiger CA, (2010) Variation of Aujeszky's disease viruses in wild swine in USA. Vet Microbiol 143: 45-51.
35. Gielkens AL, Van Oirschot JT, Berns AJ, (1985) Genome differences among field isolates and vaccine strains of pseudorabies virus. J Gen Virol66 (Pt 1): 69-82.
36. Watson RJ, Umene K, Enquist LW, (1981) Reiterated sequences within the intron of an immediate-early gene of herpes simplex virus type 1. Nucleic Acids Res 9: 4189-4199.
37. Umene K, Watson RJ, Enquist LW, (1984) Tandem repeated DNA in an intergenic region of herpes simplex virus type 1 (Patton). Gene 30: 33-39.
38. Mocarski ES, Roizman B, (1981) Site-specific inversion sequence of the herpes simplex virus genome: domain and structural features. Proc Natl Acad Sci U S A 78: 7047-7051.
39. Wagner MJ, Summers WC, (1978) Structure of the joint region and the termini of the DNA of herpes simplex virus type 1. J Virol 27: 374-387.
40. Given D, Yee D, Griem K, Kieff E, (1979) DNA of Epstein-Barr virus. V. Direct repeats of the ends of Epstein-Barr virus DNA. J Virol 30: 852-862.
41. Ben-Porat T, Kaplan AS, (1985) Molecular Biology of Pseudorabies Virus. In: Roizman B, editors. The Herpesviruses New York Plenum Press pp. 105-173.
42. Wathen MW, Pirtle EC, (1984) Stability of the pseudorabies virus genome after in vivo serial passage. J Gen Virol65 (Pt 8): 1401-1404.
43. Davison AJ, Wilkie NM, (1981) Nucleotide sequences of the joint between the L and S segments of herpes simplex virus types 1 and 2. J Gen Virol55: 315-331.
44. Richard GF, Kerrest A, Dujon B, (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol Mol Biol Rev 72: 686-727.
45. Gemayel R, Vinces MD, Legendre M, Verstrepen KJ, (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu Rev Genet 44: 445-477.
46. Buschiazzo E, Gemmell NJ, (2006) The rise, fall and renaissance of microsatellites in eukaryotic genomes. Bioessays 28: 1040-1050.
47. Schmidt AL, Anderson LM, (2006) Repetitive DNA elements as mediators of genomic change in response to environmental cues. Biol Rev Camb Philos Soc 81: 531-543.
48. Verstrepen KJ, Jansen A, Lewitter F, Fink GR, (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-990.
49. Vinces MD, Legendre M, Caldara M, Hagihara M, Verstrepen KJ, (2009) Unstable tandem repeats in promoters confer transcriptional evolvability. Science 324: 1213-1216.
50. Brouwer JR, Willemsen R, Oostra BA, (2009) Microsatellite repeat instability and neurological disease. Bioessays 31: 71-83.
51. Krobitsch S, Kazantsev AG, (2010) Huntington's disease: From molecular basis to therapeutic advances. Int J Biochem Cell Biol 43: 20-24.
52. Orr HT, Zoghbi HY, (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30: 575-621.
53. Willemsen R, Levenga J, Oostra B, (2011) CGG repeat in the FMR1 gene: size matters. Clin Genet 80: 214-225.
54. Pfister LA, Letvin NL, Koralnik IJ, (2001) JC virus regulatory region tandem repeats in plasma and central nervous system isolates correlate with poor clinical outcome in patients with progressive multifocal leukoencephalopathy. J Virol 75: 5672-5676.
55. Kaufer BB, Jarosinski KW, Osterrieder N, (2011) Herpesvirus telomeric repeats facilitate genomic integration into host telomeres and mobilization of viral DNA during reactivation. J Exp Med 208: 605-615.
56. Bates PA, DeLuca NA, (1998) The polyserine tract of herpes simplex virus ICP4 is required for normal viral gene expression and growth in murine trigeminal ganglia. J Virol 72: 7115-7124.
57. Bedadala GR, Pinnoji RC, Hsia SC, (2007) Early growth response gene 1 (Egr-1) regulates HSV-1 ICP4 and ICP22 gene expression. Cell Res 17: 546-555.
58. Legendre M, Pochet N, Pak T, Verstrepen KJ, (2007) Sequence-based estimation of minisatellite and microsatellite repeat variability. Genome Res 17: 1787-1796.
59. Harismendy O, Ng PC, Strausberg RL, Wang X, Stockwell TB, et al. (2009) Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome Biol 10: R32.
60. Dohm JC, Lottaz C, Borodina T, Himmelbauer H, (2008) Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res 36: e105.
61. Mettenleiter TC, Zsak L, Kaplan AS, Ben-Porat T, Lomniczi B, (1987) Role of a structural glycoprotein of pseudorabies in virus virulence. J Virol 61: 4030-4032.
62. Robbins AK, Ryan JP, Whealy ME, Enquist LW, (1989) The gene encoding the gIII envelope protein of pseudorabies virus vaccine strain Bartha contains a mutation affecting protein localization. J Virol 63: 250-258.
63. Klupp BG, Lomniczi B, Visser N, Fuchs W, Mettenleiter TC, (1995) Mutations affecting the UL21 gene contribute to avirulence of pseudorabies virus vaccine strain Bartha. Virology 212: 466-473.
64. Dijkstra JM, Mettenleiter TC, Klupp BG, (1997) Intracellular processing of pseudorabies virus glycoprotein M (gM): gM of strain Bartha lacks N-glycosylation. Virology 237: 113-122.
65. Curanovic D, Lyman MG, Bou-Abboud C, Card JP, Enquist LW, (2009) Repair of the UL21 locus in pseudorabies virus Bartha enhances the kinetics of retrograde, transneuronal infection in vitro and in vivo. J Virol 83: 1173-1183.
66. Petrovskis EA, Timmins JG, Gierman TM, Post LE, (1986) Deletions in vaccine strains of pseudorabies virus and their effect on synthesis of glycoprotein gp63. J Virol 60: 1166-1169.
67. Viejo-Borbolla A, Munoz A, Tabares E, Alcami A, (2010) Glycoprotein G from pseudorabies virus binds to chemokines with high affinity and inhibits their function. J Gen Virol91: 23-31.
68. Matsuura H, Kirschner AN, Longnecker R, Jardetzky TS, (2010) Crystal structure of the Epstein-Barr virus (EBV) glycoprotein H/glycoprotein L (gH/gL) complex. Proc Natl Acad Sci U S A 107: 22641-22646.
69. Chowdary TK, Cairns TM, Atanasiu D, Cohen GH, Eisenberg RJ, et al. (2010) Crystal structure of the conserved herpesvirus fusion regulator complex gH-gL. Nat Struct Mol Biol 17: 882-888.
70. Backovic M, DuBois RM, Cockburn JJ, Sharff AJ, Vaney MC, et al. (2010) Structure of a core fragment of glycoprotein H from pseudorabies virus in complex with antibody. Proc Natl Acad Sci U S A 107: 22635-22640.
71. Oliver SL, Sommer M, Zerboni L, Rajamani J, Grose C, et al. (2009) Mutagenesis of varicella-zoster virus glycoprotein B: putative fusion loop residues are essential for viral replication, and the furin cleavage motif contributes to pathogenesis in skin tissue in vivo. J Virol 83: 7495-7506.
72. Okazaki K, (2007) Proteolytic cleavage of glycoprotein B is dispensable for in vitro replication, but required for syncytium formation of pseudorabies virus. J Gen Virol88: 1859-1865.
73. Whealy ME, Robbins AK, Enquist LW, (1990) The export pathway of the pseudorabies virus gB homolog gII involves oligomer formation in the endoplasmic reticulum and protease processing in the Golgi apparatus. J Virol 64: 1946-1955.
74. Jons A, Granzow H, Kuchling R, Mettenleiter TC, (1996) The UL49.5 gene of pseudorabies virus codes for an O-glycosylated structural protein of the viral envelope. J Virol 70: 1237-1241.
75. Jons A, Dijkstra JM, Mettenleiter TC, (1998) Glycoproteins M and N of pseudorabies virus form a disulfide-linked complex. J Virol 72: 550-557.
76. McGeoch DJ, Rixon FJ, Davison AJ, (2006) Topics in herpesvirus genomics and evolution. Virus Res 117: 90-104.
77. Minson AC, Davison AJ, Desrosiers RC, Fleckenstein B, Mc-Geoch DJ, et al. (2000) Herpesviridae. In: van Regenmortel MHV, Claude MF, Bishop DHL, Carstens EB, Estes MK, editors. Virus taxonomy New York Academic Press pp. 203-255.
78. Tyler SD, Peters GA, Grose C, Severini A, Gray MJ, et al. (2007) Genomic cartography of varicella-zoster virus: a complete genome-based analysis of strain variability with implications for attenuation and phenotypic differences. Virology 359: 447-458.
79. Peters GA, Tyler SD, Grose C, Severini A, Gray MJ, et al. (2006) A full-genome phylogenetic analysis of varicella-zoster virus reveals a novel origin of replication-based genotyping scheme and evidence of recombination between major circulating clades. J Virol 80: 9850-9860.
80. Ushijima Y, Luo C, Goshima F, Yamauchi Y, Kimura H, et al. (2007) Determination and analysis of the DNA sequence of highly attenuated herpes simplex virus type 1 mutant HF10, a potential oncolytic virus. Microbes Infect 9: 142-149.
81. Szpara ML, Parsons L, Enquist LW, (2010) Sequence variability in clinical and laboratory isolates of herpes simplex virus 1 reveals new mutations. J Virol 84: 5303-5313.
82. McGeoch DJ, Dalrymple MA, Davison AJ, Dolan A, Frame MC, et al. (1988) The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol69 (Pt 7): 1531-1574.
83. McGeoch DJ, Dolan A, Donald S, Brauer DH, (1986) Complete DNA sequence of the short repeat region in the genome of herpes simplex virus type 1. Nucleic Acids Res 14: 1727-1745.
84. Ogle WO, Roizman B, (1999) Functional anatomy of herpes simplex virus 1 overlapping genes encoding infected-cell protein 22 and US1.5 protein. J Virol 73: 4305-4315.
85. Derbigny WA, Kim SK, Jang HK, O'Callaghan DJ, (2002) EHV-1 EICP22 protein sequences that mediate its physical interaction with the immediate-early protein are not sufficient to enhance the trans-activation activity of the IE protein. Virus Res 84: 1-15.
86. Zhang G, Leader DP, (1990) The structure of the pseudorabies virus genome at the end of the inverted repeat sequences proximal to the junction with the short unique region. J Gen Virol71 (Pt 10): 2433-2441.
87. Fuchs W, Ehrlich C, Klupp BG, Mettenleiter TC, (2000) Characterization of the replication origin (Ori(S)) and adjoining parts of the inverted repeat sequences of the pseudorabies virus genome. J Gen Virol81: 1539-1543.
88. Wu CL, Wilcox KW, (1991) The conserved DNA-binding domains encoded by the herpes simplex virus type 1 ICP4, pseudorabies virus IE180, and varicella-zoster virus ORF62 genes recognize similar sites in the corresponding promoters. J Virol 65: 1149-1159.
89. Vlcek C, Kozmik Z, Paces V, Schirm S, Schwyzer M, (1990) Pseudorabies virus immediate-early gene overlaps with an oppositely oriented open reading frame: characterization of their promoter and enhancer regions. Virology 179: 365-377.
90. Taharaguchi S, Inoue H, Ono E, Kida H, Yamada S, et al. (1994) Mapping of transcriptional regulatory domains of pseudorabies virus immediate-early protein. Arch Virol 137: 289-302.
91. Lee JI, Sollars PJ, Baver SB, Pickard GE, Leelawong M, et al. (2009) A Herpesvirus Encoded Deubiquitinase Is a Novel Neuroinvasive Determinant. PLoS Pathog 5: e1000387.
92. Luxton GW, Haverlock S, Coller KE, Antinone SE, Pincetic A, et al. (2005) Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc Natl Acad Sci U S A 102: 5832-5837.
93. Mohl BS, Bottcher S, Granzow H, Fuchs W, Klupp BG, et al. (2010) Random transposon-mediated mutagenesis of the essential large tegument protein pUL36 of pseudorabies virus. J Virol 84: 8153-8162.
94. Bottcher S, Maresch C, Granzow H, Klupp BG, Teifke JP, et al. (2008) Mutagenesis of the active-site cysteine in the ubiquitin-specific protease contained in large tegument protein pUL36 of pseudorabies virus impairs viral replication in vitro and neuroinvasion in vivo. J Virol 82: 6009-6016.
95. Bottcher S, Granzow H, Maresch C, Mohl B, Klupp BG, et al. (2007) Identification of functional domains within the essential large tegument protein pUL36 of pseudorabies virus. J Virol 81: 13403-13411.
96. Bottcher S, Klupp BG, Granzow H, Fuchs W, Michael K, et al. (2006) Identification of a 709-amino-acid internal nonessential region within the essential conserved tegument protein (p)UL36 of pseudorabies virus. J Virol 80: 9910-9915.
97. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, et al. (2003) A giant virus in amoebae. Science 299: 2033.
98. Chen M, Tan Z, Jiang J, Li M, Chen H, et al. (2009) Similar distribution of simple sequence repeats in diverse completed Human Immunodeficiency Virus Type 1 genomes. FEBS Lett 583: 2959-2963.
99. Walker A, Petheram SJ, Ballard L, Murph JR, Demmler GJ, et al. (2001) Characterization of human cytomegalovirus strains by analysis of short tandem repeat polymorphisms. J Clin Microbiol 39: 2219-2226.
100. Deback C, Boutolleau D, Depienne C, Luyt CE, Bonnafous P, et al. (2009) Utilization of microsatellite polymorphism for differentiating herpes simplex virus type 1 strains. J Clin Microbiol 47: 533-540.
101. Tempera I, Wiedmer A, Dheekollu J, Lieberman PM, (2010) CTCF prevents the epigenetic drift of EBV latency promoter Qp. PLoS Pathog 6: e1001048.
102. Chau CM, Zhang XY, McMahon SB, Lieberman PM, (2006) Regulation of Epstein-Barr virus latency type by the chromatin boundary factor CTCF. J Virol 80: 5723-5732.
103. Bloom DC, Giordani NV, Kwiatkowski DL, (2010) Epigenetic regulation of latent HSV-1 gene expression. Biochim Biophys Acta 1799: 246-256.
104. Amelio AL, McAnany PK, Bloom DC, (2006) A chromatin insulator-like element in the herpes simplex virus type 1 latency-associated transcript region binds CCCTC-binding factor and displays enhancer-blocking and silencing activities. J Virol 80: 2358-2368.
105. Chen Q, Lin L, Smith S, Huang J, Berger SL, et al. (2007) CTCF-dependent chromatin boundary element between the latency-associated transcript and ICP0 promoters in the herpes simplex virus type 1 genome. J Virol 81: 5192-5201.
106. Kang H, Lieberman PM, (2009) Cell cycle control of Kaposi's sarcoma-associated herpesvirus latency transcription by CTCF-cohesin interactions. J Virol 83: 6199-6210.
107. Stedman W, Kang H, Lin S, Kissil JL, Bartolomei MS, et al. (2008) Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J 27: 654-666.
108. Tempera I, Lieberman PM, (2009) Chromatin organization of gammaherpesvirus latent genomes. Biochim Biophys Acta 1799: 236-245.
109. Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, et al. (2009) Diversity and complexity in DNA recognition by transcription factors. Science 324: 1720-1723.
110. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, et al. (2009) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105-110.
111. Elemento O, Slonim N, Tavazoie S, (2007) A universal framework for regulatory element discovery across all genomes and data types. Mol Cell 28: 337-350.
112. Schatz MC, Delcher AL, Salzberg SL, (2010) Assembly of large genomes using second-generation sequencing. Genome Res 20: 1165-1173.
113. Yoon S, Xuan Z, Makarov V, Ye K, Sebat J, (2009) Sensitive and accurate detection of copy number variants using read depth of coverage. Genome Res 19: 1586-1592.
114. Medvedev P, Stanciu M, Brudno M, (2009) Computational methods for discovering structural variation with next-generation sequencing. Nat Methods 6: S13-20.
115. Simon A, Mettenleiter TC, Rziha HJ, (1989) Pseudorabies virus displays variable numbers of a repeat unit adjacent to the 3′ end of the glycoprotein gII gene. J Gen Virol70 (Pt 5): 1239-1246.
116. Nugent J, Birch-Machin I, Smith KC, Mumford JA, Swann Z, et al. (2006) Analysis of equid herpesvirus 1 strain variation reveals a point mutation of the DNA polymerase strongly associated with neuropathogenic versus nonneuropathogenic disease outbreaks. J Virol 80: 4047-4060.
117. Chibo D, Druce J, Sasadeusz J, Birch C, (2004) Molecular analysis of clinical isolates of acyclovir resistant herpes simplex virus. Antiviral Res 61: 83-91.
118. Sasadeusz JJ, Tufaro F, Safrin S, Schubert K, Hubinette MM, et al. (1997) Homopolymer mutational hot spots mediate herpes simplex virus resistance to acyclovir. J Virol 71: 3872-3878.
119. Wang K, Mahalingam G, Hoover SE, Mont EK, Holland SM, et al. (2007) Diverse herpes simplex virus type 1 thymidine kinase mutants in individual human neurons and Ganglia. J Virol 81: 6817-6826.
120. Spatz SJ, Rue CA, (2008) Sequence determination of a mildly virulent strain (CU-2) of Gallid herpesvirus type 2 using 454 pyrosequencing. Virus Genes 36: 479-489.
121. Bradley AJ, Lurain NS, Ghazal P, Trivedi U, Cunningham C, et al. (2009) High-throughput sequence analysis of variants of human cytomegalovirus strains Towne and AD169. J Gen Virol90: 2375-2380.
122. Dargan DJ, Douglas E, Cunningham C, Jamieson F, Stanton RJ, et al. (2010) Sequential mutations associated with adaptation of human cytomegalovirus to growth in cell culture. J Gen Virol91: 1535-1546.
123. Gorzer I, Guelly C, Trajanoski S, Puchhammer-Stockl E, (2010) Deep sequencing reveals highly complex dynamics of human cytomegalovirus genotypes in transplant patients over time. J Virol 84: 7195-7203.
124. Renzette N, Bhattacharjee B, Jensen JD, Gibson L, Kowalik TF, (2011) Extensive genome-wide variability of human cytomegalovirus in congenitally infected infants. PLoS Pathog 7: e1001344.
125. Legendre M, Santini S, Rico A, Abergel C, Claverie JM, (2011) Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing. Virol J 8: 99.
126. Kaplan AS, Vatter AE, (1959) A comparison of herpes simplex and pseudorabies viruses. Virology 7: 394-407.
127. Falkenberg M, Elias P, Lehman IR, (1998) The herpes simplex virus type 1 helicase-primase. Analysis of helicase activity. J Biol Chem 273: 32154-32157.
128. Gao M, Knipe DM, (1991) Potential role for herpes simplex virus ICP8 DNA replication protein in stimulation of late gene expression. J Virol 65: 2666-2675.
129. Mapelli M, Panjikar S, Tucker PA, (2005) The crystal structure of the herpes simplex virus 1 ssDNA-binding protein suggests the structural basis for flexible, cooperative single-stranded DNA binding. J Biol Chem 280: 2990-2997.
130. Bekal S, Domier LL, Niblack TL, Lambert KN, (2011) Discovery and initial analysis of novel viral genomes in the soybean cyst nematode. J Gen Virol92: 1870-1879.
131. Cheval J, Sauvage V, Frangeul L, Dacheux L, Guigon G, et al. (2011) Evaluation of High Throughput Sequencing for identifying known and unknown viruses in biological samples. J Clin Microbiol 49: 3268-3275.
132. Greninger AL, Runckel C, Chiu CY, Haggerty T, Parsonnet J, et al. (2009) The complete genome of klassevirus- a novel picornavirus in pediatric stool. Virol J 6: 82.
133. Kreuze JF, Perez A, Untiveros M, Quispe D, Fuentes S, et al. (2009) Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology 388: 1-7.
134. Presti RM, Zhao G, Beatty WL, Mihindukulasuriya KA, da Rosa AP, et al. (2009) Quaranfil, Johnston Atoll, and Lake Chad viruses are novel members of the family Orthomyxoviridae. J Virol 83: 11599-11606.
135. Loh J, Zhao G, Presti RM, Holtz LR, Finkbeiner SR, et al. (2009) Detection of novel sequences related to african Swine Fever virus in human serum and sewage. J Virol 83: 13019-13025.
136. Al Rwahnih M, Daubert S, Golino D, Rowhani A, (2009) Deep sequencing analysis of RNAs from a grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus. Virology 387: 395-401.
137. Cunningham C, Gatherer D, Hilfrich B, Baluchova K, Dargan DJ, et al. (2010) Sequences of complete human cytomegalovirus genomes from infected cell cultures and clinical specimens. J Gen Virol91: 605-615.
138. Lee SW, Markham PF, Markham JF, Petermann I, Noormohammadi AH, et al. (2011) First complete genome sequence of infectious laryngotracheitis virus. BMC Genomics 12: 197.
139. Awasthi S, Lubinski JM, Eisenberg RJ, Cohen GH, Friedman HM, (2008) An HSV-1 gD mutant virus as an entry-impaired live virus vaccine. Vaccine 26: 1195-1203.
140. Awasthi S, Lubinski JM, Friedman HM, (2009) Immunization with HSV-1 glycoprotein C prevents immune evasion from complement and enhances the efficacy of an HSV-1 glycoprotein D subunit vaccine. Vaccine 27: 6845-6853.
141. Koelle DM, Magaret A, McClurkan CL, Remington ML, Warren T, et al. (2008) Phase I dose-escalation study of a monovalent heat shock protein 70-herpes simplex virus type 2 (HSV-2) peptide-based vaccine designed to prime or boost CD8 T-cell responses in HSV-naive and HSV-2-infected subjects. Clin Vaccine Immunol 15: 773-782.
142. Klupp BG, Kern H, Mettenleiter TC, (1992) The virulence-determining genomic BamHI fragment 4 of pseudorabies virus contains genes corresponding to the UL15 (partial), UL18, UL19, UL20, and UL21 genes of herpes simplex virus and a putative origin of replication. Virology 191: 900-908.
143. Cheung A, Maes R, (1993) Nucleotide sequence variations surrounding the standard recombination junction of pseudorabies viruses. Nucleic Acids Res 21: 5522-5523.
144. Fuchs W, Bauer B, Mettenleiter TC, Rziha HJ, (1994) A novel intergenic site for integration and expression of foreign genes in the genome of pseudorabies virus. J Virol Methods 46: 95-105.
145. DeMarchi JM, Lu ZQ, Rall G, Kupershmidt S, Ben-Porat T, (1990) Structural organization of the termini of the L and S components of the genome of pseudorabies virus. J Virol 64: 4968-4977.
146. Mittal SK, Field HJ, (1989) Analysis of the bovine herpesvirus type 1 thymidine kinase (TK) gene from wild-type virus and TK-deficient mutants. J Gen Virol70 (Pt 4): 901-918.
147. Grey F, Sowa M, Collins P, Fenton RJ, Harris W, et al. (2003) Characterization of a neurovirulent aciclovir-resistant variant of herpes simplex virus. J Gen Virol84: 1403-1410.
148. Sauerbrei A, Deinhardt S, Zell R, Wutzler P, (2010) Phenotypic and genotypic characterization of acyclovir-resistant clinical isolates of herpes simplex virus. Antiviral Res 86: 246-252.
149. Liljeqvist JA, Svennerholm B, Bergstrom T, (1999) Herpes simplex virus type 2 glycoprotein G-negative clinical isolates are generated by single frameshift mutations. J Virol 73: 9796-9802.
150. Rekabdar E, Tunback P, Liljeqvist JA, Lindh M, Bergstrom T, (2002) Dichotomy of glycoprotein g gene in herpes simplex virus type 1 isolates. J Clin Microbiol 40: 3245-3251.
151. Dolan A, McKie E, MacLean AR, McGeoch DJ, (1992) Status of the ICP34.5 gene in herpes simplex virus type 1 strain 17. J Gen Virol73 (Pt 4): 971-973.
152. Everett RD, Fenwick ML, (1990) Comparative DNA sequence analysis of the host shutoff genes of different strains of herpes simplex virus: type 2 strain HG52 encodes a truncated UL41 product. J Gen Virol71 (Pt 6): 1387-1390.
153. Spatz SJ, (2010) Accumulation of attenuating mutations in varying proportions within a high passage very virulent plus strain of Gallid herpesvirus type 2. Virus Res 149: 135-142.
154. Tirabassi RS, Enquist LW, (1999) Mutation of the YXXL endocytosis motif in the cytoplasmic tail of pseudorabies virus gE. J Virol 73: 2717-2728.
155. Tyler S, Severini A, Black D, Walker M, Eberle R, (2011) Structure and sequence of the saimiriine herpesvirus 1 genome. Virology 410: 181-191.
156. Hwang CB, Chen HJ, (1995) An altered spectrum of herpes simplex virus mutations mediated by an antimutator DNA polymerase. Gene 152: 191-193.
157. LaBoissiere S, Trudel M, Simard C, (1992) Characterization and transcript mapping of a bovine herpesvirus type 1 gene encoding a polypeptide homologous to the herpes simplex virus type 1 major tegument proteins VP13/14. J Gen Virol73 (Pt 11): 2941-2947.
158. Norberg P, Bergstrom T, Rekabdar E, Lindh M, Liljeqvist JA, (2004) Phylogenetic analysis of clinical herpes simplex virus type 1 isolates identified three genetic groups and recombinant viruses. J Virol 78: 10755-10764.
159. Lynch M, Sung W, Morris K, Coffey N, Landry CR, et al. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci U S A 105: 9272-9277.
160. Denver DR, Morris K, Kewalramani A, Harris KE, Chow A, et al. (2004) Abundance, distribution, and mutation rates of homopolymeric nucleotide runs in the genome of Caenorhabditis elegans. J Mol Evol 58: 584-595.
161. Levy S, Sutton G, Ng PC, Feuk L, Halpern AL, et al. (2007) The diploid genome sequence of an individual human. PLoS Biol 5: e254.
162. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59.
163. Lee HC, Yin PH, Lin JC, Wu CC, Chen CY, et al. (2005) Mitochondrial genome instability and mtDNA depletion in human cancers. Ann N Y Acad Sci 1042: 109-122.
164. Bianchi NO, Bianchi MS, Richard SM, (2001) Mitochondrial genome instability in human cancers. Mutat Res 488: 9-23.
165. Ball EV, Stenson PD, Abeysinghe SS, Krawczak M, Cooper DN, et al. (2005) Microdeletions and microinsertions causing human genetic disease: common mechanisms of mutagenesis and the role of local DNA sequence complexity. Hum Mutat 26: 205-213.
166. Platt KB, Mare CJ, Hinz PN, (1979) Differentiation of vaccine strains and field isolates of pseudorabies (Aujeszky's disease) virus: thermal sensitivity and rabbit virulence markers. Arch Virol 60: 13-23.
167. Haff RF, (1964) Inhibition of the Multiplication of Pseudorabies Virus by Cyclohexamide. Virology 22: 430-431.
168. Smith GA, Enquist LW, (1999) Construction and transposon mutagenesis in Escherichia coli of a full-length infectious clone of pseudorabies virus, an alphaherpesvirus. J Virol 73: 6405-6414.
169. Enquist LW, Madden MJ, Schiop-Stanley P, Vande Woude GF, (1979) Cloning of herpes simplex type 1 DNA fragments in a bacteriophage lambda vector. Science 203: 541-544.
170. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
171. Warren RL, Sutton GG, Jones SJ, Holt RA, (2007) Assembling millions of short DNA sequences using SSAKE. Bioinformatics 23: 500-501.
172. Staden R, Judge DP, Bonfield JK, (2001) Sequence assembly and finishing methods. Methods Biochem Anal 43: 303-322.
173. Staden R, (1996) The Staden sequence analysis package. Mol Biotechnol 5: 233-241.
174. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
175. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I, (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32: W273-279.
176. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, et al. (2003) LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13: 721-731.
177. Fonseca AA Jr, Camargos MF, de Oliveira AM, Ciacci-Zanella JR, Patricio MA, et al. (2009) Molecular epidemiology of Brazilian pseudorabies viral isolates. Vet Microbiol 141: 238-245.
178. Babic N, Klupp BG, Makoschey B, Karger A, Flamand A, et al. (1996) Glycoprotein gH of pseudorabies virus is essential for penetration and propagation in cell culture and in the nervous system of mice. J Gen Virol77 (Pt 9): 2277-2285.
179. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
180. Nicol JW, Helt GA, Blanchard SG Jr, Raja A, Loraine AE, (2009) The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25: 2730-2731.
181. Nakamura K, Oshima T, Morimoto T, Ikeda S, Yoshikawa H, et al. (2011) Sequence-specific error profile of Illumina sequencers. Nucleic Acids Res 39: e90.
182. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26.
183. Thurston MI, Field D, (2005) MsatFinder: detection and characterization of microsatellites. Oxford, United Kingdom CEH Oxford.
184. Benson G, (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573-580.
185. Bao Y, Federhen S, Leipe D, Pham V, Resenchuk S, et al. (2004) National center for biotechnology information viral genomes project. J Virol 78: 7291-7298.
186. Davison AJ, Scott JE, (1986) The complete DNA sequence of varicella-zoster virus. J Gen Virol67 (Pt 9): 1759-1816.
187. Dolan A, Cunningham C, Hector RD, Hassan-Walker AF, Lee L, et al. (2004) Genetic content of wild-type human cytomegalovirus. J Gen Virol85: 1301-1312.
188. Baer R, Bankier AT, Biggin MD, Deininger PL, Farrell PJ, et al. (1984) DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 310: 207-211.
189. Hatfull G, Bankier AT, Barrell BG, Farrell PJ, (1988) Sequence analysis of Raji Epstein-Barr virus DNA. Virology 164: 334-340.
190. Parker BD, Bankier A, Satchwell S, Barrell B, Farrell PJ, (1990) Sequence and transcription of Raji Epstein-Barr virus DNA spanning the B95-8 deletion region. Virology 179: 339-346.
191. Jeang KT, Hayward SD, (1983) Organization of the Epstein-Barr virus DNA molecule. III. Location of the P3HR-1 deletion junction and characterization of the NotI repeat units that form part of the template for an abundant 12-O-tetradecanoylphorbol-13-acetate-induced mRNA transcript. J Virol 48: 135-148.
192. de Jesus O, Smith PR, Spender LC, Elgueta Karstegl C, Niller HH, et al. (2003) Updated Epstein-Barr virus (EBV) DNA sequence and analysis of a promoter for the BART (CST, BARF0) RNAs of EBV. J Gen Virol84: 1443-1450.
193. Rezaee SA, Cunningham C, Davison AJ, Blackbourn DJ, (2006) Kaposi's sarcoma-associated herpesvirus immune modulation: an overview. J Gen Virol87: 1781-1804.